Idea Transcript
Botanical Journal of the Linnean Society (1990), 103: 251-261. With 6 figurf's
Studies in Garcinia, dioecious tropical forest trees: the phenology, pollination biology and fertilization of G. hornbroniana Pierre A.
J.
RICHARDS
Department of Biology, Ridley Building, University
rif Newcastle
upon Tyne NEJ 7RU
Received September 1988, accepted for publication January !989
RICHARDS, A. J., 1990. Studies in Garcinia, dioecious tropical forest trees: the phenology, pollination biology and fertilization of G. hombroniana Pierre. Garcinia hombroniana is a facultative agamosperm which is pollinated by Trigona bees. Nectar is restricted to the large discoid stigma (or pistillode in male flowers), which also captures and hydrates pollen. The 'wet' stigma and binucleate pollen suggest that Garcinia arose from hermaphrodite plants with a gametophytic selfincompatibility system. On stigmas, nectar is secreted early on three or four succf'ssive days. On male pistillodes, nectar is secreted when anthers dehisce, on the second morning after anthesis. Pollen is most viable when freshly collected, but some viability remains four days after collection. Pollen germinates within 24 h of hydration. Similar results to pollinations arc obtained by germinating pollen in I% sucrose. Garcinia hombroniana flowers principally from January to June. Cultivated females are considered as 'big bang' strategists. Male flowers are considered as 'steady statf'' strategists. ADDITIONAL KEY WORDS:-Agamospermy - Clusiaceae - stigmatic nectar - Trigona. CONTENTS Introduction . Flowering phenology Pollination biology. Pollen characteristics I. Pollen formation and variability. 2. In vitro germination 3. Germination on stigmas. Natural pollination Discussion . Acknowledgements References.
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INTRODUCTION
Most Garcinia are facultative agamosperms, and in the presence of males a substantial proportion of sexual seed formation occurs (Richards, 1990). In the present paper, I report investigations into the flower phenology, pollination biology, pollen development, and pollen germination of the facultative agamosperm G. hombroniana Pierre. Work was undertaken at the Jabatan Botani, Universiti Malaya, Kuala Lumpur on two groups of cultivated trees of lowland and of upland origin. Fuller details are given in Richards ( 1990). 0024-4074j90j070251 +II $03.00/0
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Figure I . Estimated flowering dates for herbarium material of wild Garcinia hombroniana, in halt month periods. 0 , Maritime, N = 2 2 ; 0 , upland, N = 14.
FLOWERING PHENOLOGY
Exact collecting dates were given for 36 flowering or fruiting specimens of G.hombroniana at the herbaria F R I M and KLU. For fruiting material, the flowering date was estimated by a presumptive increase in the length of the ovary of 0.38 mm day-’, derived from studies of fruit development (Richards, 1990). Estimated flowering dates were bulked for each half month (Fig. 1). Material was classed as either maritime or montane, according to the disjunct habitats of this species (Whitmore, 1973). Garcinia hombroniana is restricted to non-seasonal tropical regions (Richards, in press) and flowers throughout the year. However, 72% of the flowering records are for the months January to June, and for the comparison between the number of flowering records for the first six months of the year and the last six months, x2 = 7.1, P \756
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Figure 2. Numbers of Rowers of one male and one female Garcinia hombroniana labelled as buds on 6 January 1988 at Rimba Ilmu Botanic Garden undergoing anthesis on subsequcnt dates. Arrows refer to events for all the flowers on each tree.
The male tree a t Rimbo Ilmu was in early bud on 6 January. I n contrast to females, inflorescence buds develop between three and seven flowers which open sequentially over a period of about four days. Anthers shed pollen on two successive mornings after petal reflection. The development of male buds is much slower than in females. The first male flower opened on 20 January, but between that date and 26February only about another 40 flowers opened. Heavy flowering occurred between 3 March and 18 March, when flowering ceased abruptly. Between these latter dates about 600 flowers underwent anthesis. Of 22 buds marked on 6 January, five subsequently aborted, and the remainder flowered between 25 February and 18 March. The time from bud initiation to male flowering varies between 45 and 66 days and the period of male flowering lasted 61 days. There was a remarkable lack of correspondence between male and female flowering (Fig. 2). The Titiwangsa Lake population was first visited on 20February 1988 on which date it was clear that heavy flowering had occurred in early January. Flowering recommenced on one of the females and all three males on about 10 March. By 17 March, all seven trees were in flower, with few buds still to develop. O n that date all trees bore between 50 and 100 flowers; flowering was lighter than had apparently occurred in January. POLLINATION BIOLOGY
Petals are cream and surround a green ovary/pistillode with a sessile, weakly lobed plate-like stigma about 10 mm in diameter. Male flowers are sessile and are borne vertically in clusters. They are 20-25 mm in diameter and bear four lobed clusters of many stamens. Female flowers are pedicellate, cernuous to pendant, and are usually borne singly. They are 30-35 mm in diameter and lack staminodes. The pollen of G. hombroniana is sticky, and it is unlikely that any abiotic pollen transport occurs. Male and female flowers are commonly visited by small colonial bees of the genus Trigona. Two captured at Rimba Ilmu at female
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Figure 3. Worker o f Trigona Iamiceps Smith foraging thc nectariferous stigmatic disk of female Garcinta hombroniana. Scale bar= 10 mm.
flowers were identified by Khoo So0 Ghee as T. laeviceps Smith. No other flower visitors were discovered. Bees at male flowers gathered pollen and often could be seen to have full corbiculae. These bees were dusted with pollen which for two individuals was shown microscopically to consist entirely of the pollen of G. hombroniana. Bees at male flowers also fed from the surface of the ‘stigma’ of the pistillode, from which they are presumed to have gathered nectar (see below). Bees foraged rather haphazardly, with frequent ‘escape flights’, and were often observed to fly directly from flowers on a male tree to flowers on a neighbouring female, about 10 m distant. O n female flowers, bees foraged only on the stigma (Fig. 3). Female flowers open early in the morning, and during the first day the stigma is cream in colour. During the second day the stigma develops brown spots and darkens in colour; in some cases two petals drop. During the third day the stigma is pale honey-brown in colour, and two of the four petals remain. By the fourth day, three days after anthesis, the stigma is brown and in some cases all petals have dropped. The maturation process appears to be unaffected by rainfall. O n the second morning, 24th after anthesis, the surface of the stigma glistens with liquid. Tests with ‘Diastix’ and ‘Clinistix’ reveal this to be a sugar solution with a hexose component of at least 1%. Five female stigmas at Rimbo Ilmu were labelled at first anthesis and tested for a sugar reaction on the stigma surface with ‘Diastix’ at 10.00 h and a t 15.30 h then and on three subsequent days (except day two when only one test was made) (Fig. 4).There is a greater
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STUDIES IN GARClNlA r
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Figure 4. Nectar production in five female flowers of G. hombroniana sampled on seven occasions over four successive days. 0, Flowers with detectable nectar; 0 ,flowers without detertable nectar. For a description of flowering stage classification, see text.
likelihood of obtaining a positive test for sugar in the morning than the afternoon. It is probable that nectar is only secreted at dawn. Nectar is secreted on either three or four successive mornings, and is often secreted on the morning after petal fall. It is difficult to lodge pollen on stigmas immediately after anthesis, and pollen germination at this stage is poor; in vitro, pollen germinates fairly well in a 1% sucrose solution (Fig. 5). The stigmatic exudate has three functions: (1) the lodging of pollen; (2) the germination of pollen; (3) nectar reward to visiting Trigona. The stigma of the pistillode of male flowers also gives a positive response to ‘Diastix’. At male anthesis, anthers are indehiscent, and no sugar can be detected on the cream coloured stigma. In the absence of heavy rain during the afternoon, anthers dehisce the following morning. At this stage sugar is present on the stigma. By the next morning, 48 h after anthesis, the flower has withered. If the afternoon rainfall is heavy on the day of anthesis, anthers rot without dehiscing, and no nectar is produced. POLLEN CHARACI‘ERIS‘I’ICS
1. Pollen formation and uariability Male meiosis occurs when inflorescence bracts are about 7 mm long and the buds of individual male flowers are 3.5-4mm in diameter. Male meiosis is described in Richards (1990). Meiosis is non-synchronous within an anther. Leptotene, diakenesis and telophase I stages are commonly encountered, but cells at metaphase I are uncommon, while anaphase, metaphase I1 and tetrad stages appear to be very briec pollen is formed within 24 h after meiosis; pollen grains indistinguishable from those at dehiscence can be found a t least 2 weeks prior to anthesis.
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After collection Figure 5. Pollen germination of G. hombroniunu at various times after poltination on stigmas one day after anthesis, or after culture in 1 yo sucrose using freshly collected pollen. Each spot represents the O n stigmas; 0 , plated. average of two replicates. 0,
Pollen is subspherical and tricolporate at the weakly angled corners; the exine is minutely papillose and the contents are binucleate. For the Rimba Ilmu material, stainability for samples of 100 grains stained in acetocarmine varied from 94% to 100% ( N = 5). For one of the Titiwangsa Park males, pollen was only 84% stainable. For the Rimba Ilmu male, individual pollen grains varied between 25 and 42,um diameter. For four estimates made on different dates, mean pollen diameters ranged from 3 1.02 f0.63 to 36.46 0.82 ,urn (2 x standard error). Pollen size within the one plant is statistically homogenous within a flower, but is heterogenous for flowers taken on different dates. It is presumed that this variation is developmental, and may be related to the rainfall during bud formation. For a Titiwangsa Park male, from the montane population, the mean pollen diameter was recorded as 2 9 . 6 2 k 0 . 5 8 ~ m . This is smaller than any of the estimates of the mean diameter of the pollen of the male at Rimba Ilmu of maritime origin (P