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Male and Female Booths with Separate Entrances in the Tiny Flowers Of ARTICLE IN PRESS Flora 201 (2006) 389–395 www.elsevier.de/flora Male and female booths with separate entrances in the tiny flowers of Guazuma ulmifolia (Malvaceae–Byttnerioideae). I. Structural integration Christian WesterkampÃ, Arlete Aparecida Soares, Lae´ rcio P. do Amaral Neto Departamento de Biologia, Universidade Federal do Ceara´ (UFC), Campus do Pici, 906, Cx. P. 6009, 60.451-970 Fortaleza, CE, Brazil Received 7 April 2005; accepted 27 July 2005 Dedicated to Prof. Dr. Stefan Vogel, the most esteemed academic teacher of the first author, on the occasion of his 80th birthday Abstract In spite of their tiny dimensions (3 Â 5mm2), the strongly honey-scented flowers of Guazuma ulmifolia (Malvaceae–Byttnerioideae) provide six sexual chambers. A central female unit is surrounded by five interconnected male compartments. At the onset of anthesis the strap-shaped odoriferous petal appendages form an open star with the female chamber in the centre. Hereafter, they wilt, intermingle and finally lock access to the stigma. Meanwhile, wilting sepals liberate new entrances from the back between the petal claws. They give way to nectar-offering male chambers. In each of them a well-lit (but closed) window lures the visitor into a standard position for passive pollen uptake. Finally, the insects have to back out of one of the rear entrances. It remains unknown how the minute visitors (maximum height ca. 0.5 mm) – if ever – overcome the distance to another Guazuma tree. r 2006 Elsevier GmbH. All rights reserved. Keywords: Herkogamy; Dichogamy; Myiophily; Deceptive phase; Nectar flower; Revolver flower Introduction reforestation tree all over Latin America (Powell, 1997; Neto and Aguiar, 1999) as well as a commercial timber In spite of the huge amount of literature relating to (Richter and Dallwitz, 2000). The tiny flowers appear in the reproduction of cocoa (Theobroma cacao) (see masses all over the year, and thus are easily accessible Young et al. (1987), and references therein), very little and ideal for study. The still unresolved problem is why is known on the floral biology of other members of the (and which) animals visit the small and extremely Theobromeae (Malvaceae–Byttnerioideae). Guazuma complex flowers of the cocoa alliance. The present ulmifolia Lam. belongs to this alliance and shows some results may contribute to a solution of the pollination similarity to the flowers of cocoa. It is a widespread and problems cocoa growers are confronted with. variable species, distributed from Mexico to northern Argentina and growing as a pioneer plant (Salazar and Jøker, 2000). It is a much-utilized multipurpose and Materials and methods ÃCorresponding author. The plants used for analysis were from the Campus do E-mail address: [email protected] (C. Westerkamp). Pici of the Ceara´ Federal University, Fortaleza, Ceara´ 0367-2530/$ - see front matter r 2006 Elsevier GmbH. All rights reserved. doi:10.1016/j.flora.2005.07.015 ARTICLE IN PRESS 390 C. Westerkamp et al. / Flora 201 (2006) 389–395 (Northeastern Brazil), 3.81S; 38.5 1W. The specimens partly occupy the gaps between the corollar cuculli differed in many aspects, they were obviously planted (Fig. 2a). Hairs from both sides intermingle and close and apparently came from various origins. the spaces remaining between the petals and staminodia. Flowers were studied on the trees and in the At the beginning of anthesis, these attractive inner laboratory. In the lab, we used a dissecting microscope staminodes give the flower centre the aspect of a reddish WILD M5 with drawing device. Details were documen- eye, recalling those described by Endress (1984) for ted by drawings. Photos were taken using a Nikon F some primitive angiosperm families (Austrobaileyaceae, 90X camera with a Sigma 105 mm macro lens and a ring Degeneriaceae, Eupomatiaceae, Himantandraceae). flash (Nikon SB 29). The receptive area of the stigma The whitish fertile stamens are set off from the was demarcated by applying the peroxide (H2O2) test androecial complex between and below the tips of the after Zeisler (1938). staminodes. They bend slightly outward, and then divide into 2–3 arms (two upper, one lower). Hereafter, they suddenly bend outwards in a right angle, the two upper Results arms forming distinct ‘‘knees’’ at the bend (Fig. 2g). In many flowers, one of the three stamens is fused to one of the others. Thus, instead of three pollen-displaying areas Flower morphology of two thecae each, in these cases one area of two and one area of four result. The small thecae are red (or even Gynoecium blackish) while closed and yellowish to off-coloured The whitish gynoecium consists of five fused carpels when open. They open sequentially and expose their few that form a star-shaped structure with rounded rays pollen grains in an outward-downward (extrorse) when seen from above. The ovary is barrel-shaped and position into the free space, never in close contact to a well set off from the narrow non-branched style. On the petal. surface it is covered by fine hairs that close the space When manually opening the connection (see below) between the ovary and the surrounding androecium between petal hood and androecium, the pollen is consisting of stamens and staminodes (Fig. 2g). ejected as a cloud towards the petal when overcoming Over most of its length, the style is covered by rows of the resistance between the hood and the androecial equidistant papillae, only the base is devoid of them. In clamp. Thus, when inspecting a petal, one regularly finds the upper third, there are free stigma arms, but they are pollen on its inner side, which possibly led some authors secondarily fused to each other in a zipper-like manner (see Yeo, 1993) to suspect secondary pollen presenta- by interconnected papillae, the ends of which are slightly tion. This, however, is clearly an artefact. swollen. As indicated by the peroxide test, receptive areas cover the whole length of the style and are found Corolla as well in the lines between the papillae. Thus, the entire The five petals are independent of each other, but structure usually referred to as the style is in reality a secondarily connected via interlacing hairs. The petals complex of stigmas. are divided into four different segments (terms in parentheses according to Bayer and Hoppe (1990), Androecium Young et al. (1987)): a basal claw, a central hood The androecium consists of some 20 stamens and (pouch, cucullus, concha), a connecting strap (ligule staminodes (Fig. 2f). For their major part, they are fused strap, Taenialsegment) and two distal band-shaped into a tubular androphore with slightly diverging walls, ligules. with its tips reaching about the height of the style The claw is a rounded (in transverse section) stiff (Fig. 2g). The free ends of all members are bent structure that elevates the plate from the flower base, at outwards in two levels. Five large (antesepalous) inner right angles to floral axis and pedicel. It soon and staminodia (Fig. 2a, f) form the upper level and abruptly widens into a hood-shaped blade that forms a alternate with five (antepetalous) lower complexes of semicircular (lengthwise and crosswise) cave, the so- some three stamens each (Fig. 2f). When interpreting called cucullus (Fig. 2d, c). Inside the hood, the strong the fertile stamen complexes as single stamens with major veins diverge from the claw in a fan-shaped secondary partition, one might interprete the androe- manner (Fig. 2d). These veins are greenish in the cium as obdiplostemonous in relation to the surround- beginning and change to reddish during anthesis. As ing perianth. they are elevated and the intercostal areas bulge to the The five conspicuous staminodia dominate the com- outside (not depicted), they jointly form a structure like plex. They represent flat reddish or greenish structures corrugated iron, thus stabilizing the hood. While the covered by simple hairs on their inner surfaces. These veins are opaque to dark red, the intercostal areas are hairs only are responsible for the coloration. The translucent. This results in luminosity increasing from triangular free tips are slightly bent outwards, and thus the base to the distal end of the hood, being by far most ARTICLE IN PRESS C. Westerkamp et al. / Flora 201 (2006) 389–395 391 brilliant next to the anther complexes. At the base, the rims of the blade are bent outwards and backwards (Fig. 2e), thus forming (jointly with the neighbouring petal) wide rear openings (entrance/exit holes). The blade is hairy on the outside. At the flanges, these stiff hairs intermingle with those of the neighbouring petal, thus linking these two organs laterally and leaving no passage (neither for entering nor for leaving) between them. At the distal end, the hood is bent inwards and abruptly narrows into a strap-shaped final part that – after a U-turn – runs parallel to the final part of the hood (Fig. 2d, g). At the transition, strap and blade are folded in a V-shaped manner, forming ‘‘knees’’ with the upper end of the hood (Fig. 2d). These ‘‘knees’’ are stuck below the (antesepalous) staminodes on either side (Fig. 2a), while the stamen complex grips the petal from Fig. 1. Flower of Guazuma ulmifolia in male stage, with rear below, entering via the ‘‘V’’ formed at the transition. entrances open. Note nectar (?) droplet glistening in one The different parts of the androecium thus represent a doorway and smooth interior of a (2)-sepal-complex in front of clamp that fixes the hood mechanically from above some rear entrances (lower left). (staminodes) and below (stamen complex) and provide additional stability to its complex form. Petal hairs here complex of two combined sepals curves backwards. also intermingle with those of the neighbouring stami- With the compound of three this is more or less nodes; thus closing whatever passage between them.
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