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a Center for Ecological Research, Kyoto University, Sakyo, Kyoto, 606-8502; b Biological Laboratory, Yoshida College, Kyoto University, Sakyo, Kyoto, 606-8501, Japan
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Key Words: beetle • Dipterocarpaceae • general flowering • pollination • Sarawak • Shorea • thrips
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The pollination system of Shorea section Mutica (Dipterocarpaceae) has been reported during a GFP at Pasoh Forest Reserve, Peninsular Malaysia (Chan and Appanah, 1980; Appanah and Chan, 1981). All six species of Shorea sect. Mutica in Pasoh including S. parvifolia Dyer were exclusively visited and pollinated by thrips (Appanah and Chan, 1981). Appanah and his colleague noted that the short generation time and high reproductive rate of thrips permit a quick response of thrips to an abrupt increase of flowers at the beginning of the general flowering and that thrips provide sufficient pollination service for multiple species of Shorea.
We began monitoring plant phenology using a canopy observation system in August 1992 in Lambir Hills National Park, Sarawak (Inoue et al., 1995). A general flowering was observed in 1996 for the first time (S. Sakai et al., in press). Sixty-five species of Shorea including 14 species of sect. Mutica have been recorded from the Park (P. S. Ashton, personal communication). Among the nine species of sect. Mutica that we monitored, four species flowered during the period. Unexpectedly, beetles were found to be the predominant flower visitors of all nine species of Shorea sect. Mutica, and also other sections under observation in emergent and canopy layers of the forest (Momose et al., 1998).
This paper presents field observations and experiments on the breeding system and pollination of an emergent tree, Shorea parvifolia, a member of sect. Mutica. The canopy observation system (Inoue et al., 1995) allowed continuous observation of flowering phenology and pollination processes, and manipulation of experiments on tree crowns over 60 m above the forest floor. In addition to flower visitation frequency and the amount of body pollen loads, the ability of flower visitors to effect fruit set was examined by experiments in which potential pollinators were introduced to bagged flowering inflorescences. This study suggests that different pollination systems work in dipterocarp forests in Peninsular Malaysia and in Sarawak.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The genus Shorea (Dipterocarpaceae) is the dominant emergent tree genus of the lowland forest of West Malesia, with 163 species throughout Malesia (Ashton, 1982; Ashton, Givnish, and Appanah, 1988) and 65 species in Lambir (P. S. Ashton, personal communication). Shorea parvifolia is a member of sect. Mutica with 27 species in Malesia and 14 species in Lambir and is one of the constituents of the emergent layer. In CBP, eight trees of S. parvifolia with >40 cm dbh (diameter at breast height) were found.
Pollination of three individuals of S. parvifolia was studied during 14–28 May 1996. Two trees in CBP, trees 225 (132 cm dbh, height 60 m) and 229 (44 cm dbh, height 35 m) (Table 1), were accessed by the canopy observation system (Fig. 1). In addition, a crown of one other emergent tree near the headquarters of the National Park (tree 1001) was accessed by aluminum ladders.
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We recorded the magnitude of flowering and fruiting events using the following grades: –, flowers/fruits absent; +, few, scattered, or covering only a small part of the crown; 1, covering less than half of the crown; 2, abundant but not over the whole crown; 3, covering the whole crown.
Collection of flower visitors and pollen on stigma
Flower visitors were collected by net-sweeping or by flower collection. In net-sweeping, we put a branch with ~200 open flowers into an insect net and quickly shook insects into a sealable plastic bag. We repeated the procedure five times on different branches at each collection time. The numbers of beetles and thrips per flower were calculated from eight samples taken on 13–15 May 1996 (1800 and 2200 on 13 May; 0300, 1000, 1730 and 2230 on 14 May; 0230 and 0630 on 15 May) on tree 225. Variation in flower visitors among the trees was examined using additional samples collected at 1700 on 19 May on trees 225 and 229, and at 1000 on 16 May and 1700 on 20 May on tree 1001. The insects were brought to the laboratory within an hour and killed in a refrigerator. They were then pinned or fixed in alcohol and labeled.
Flower visitors that hid inside the corollas and could not be collected by net-sweeping were collected by flower collection. For flower collection, we cut off inflorescences with 46–124 flowers on tree 225 inside a sealable plastic bag. We brought the plastic bags to the laboratory and counted flower visitors in each of the corollas under a binocular microscope, including flower visitors fallen from the corollas in the bag. The insects were preserved for identification in vials filled with 50% alcohol, except for thrips, which were kept in vials with glycerin-alcohol. We sampled two bags at each collection time at 6-h intervals on 16 May on tree 225.
The eight net-sweeping samples on 13–15 May and the four flower-collection samples on 16 May were used to examine changes in the densities of beetles and thrips in the crown in a day. The numbers of insects per flower during four 6-h periods were calculated by summing the averaged number of insects per flower collected by net-sweeping during the period and that by flower sampling. Standard errors for thrips numbers were calculated using flower collection samples, and those for beetle numbers were calculated using net-sweeping samples. Then we adjusted the standard errors to the total means of both samples. The standard error for beetles at 1200 were not computed because only one net-sweeping sample was available.
Some of the beetles and thrips from the net-sweeping samples were used to examine pollen loads on their bodies or stomach contents. All collections for trees 229 and 1001, and seven collections among 11 for tree 225 were classified to order and family for Coleoptera. All insects collected by flower collection were classified to order and species for Thysanoptera. In addition to the above sampling in the crown, abscised corollas fallen on a terrace of the tower (25 m above the ground) were collected to examine insects at 1100 on 14 May.
Finally, we collected 20–25 open-pollinated flowers and fixed them in FAA (formalin; acetic acid; alcohol) at 1800 and 2200 on 13 May, 0300, 0600, 1000, and 1500 on 14 May, and 1200 on 16 May. Pollen grains on stigmas were counted under a microscope. Rank correlation between sampling time and the number of pollen grains on a stigma was examined by Spearman's rank correlation test, because intensity of pollinator activities might change in the course of the day. Flowers collected on 16 May were also examined for damage due to gnawing by beetles.
Pollination experiments
To examine the breeding system of S. parvifolia and the contributions of insect visitors to pollination, we performed seven experiments on tree 225: (1) open: flowers on four inflorescences were left exposed permitting unhindered insect visitation; (2) untreated, bagged: flowers on two inflorescences were bagged before the tree started blooming; (3) open, flower-reduced: flowers on three inflorescences were removed except for flowers that opened on 19–20 May as controls of experiments 4–7; (4) self-pollinated (geitonogamous); (5) cross-pollinated: flowers on 11 inflorescences were hand-pollinated with geitonogamous pollen from different inflorescences on the same tree for experiment 4 (self-pollinated), or with cross pollen from trees 229 and 1001 for experiment 5 (cross-pollinated), sampled just before anthesis on 19–20 May (pollen was transferred using Chinese writing brushes, and all untreated flowers were removed); (6) thrips-introduced; and (7) beetle-introduced. Experiments 6 and 7 were made in the following manner twice, on 22 and 27 May: we collected flower visitors on tree 229 at 2000 by sweeping four branches (~200 open flowers on each) and separated thrips, beetles, and other insects. The thrips and beetles were each released separately into two tetron bags (TORAY, tetron®, number 9000) enclosing the inflorescences before anthesis on tree 225, and left for 2 d. All untreated flowers on the inflorescences were removed. This procedure resulted in introduction of 53–54 beetles or 18–37 thrips into each bag.
We monitored changes in the number of fruits on branches every 2 wk until fruit dispersal in experiments 1 and 2, and until 32 d after flowering in experiments 3–7. In addition, we followed unbagged flowers and fruits on five inflorescences of tree 229 until seed dispersal.
To examine whether exclusion of flower visitors caused a decrease of fruit set, we compared fruit set in open and untreated, bagged flowers (experiments 1 and 2) on day 48 after flowering peak by Fisher's exact test. Then, fruit set in experiments 3–7 was compared with that in untreated, bagged flowers (experiment 2) on day 32 after flowering to investigate which treatments increased fruit set. At that time, the fruits weighed 0.116 ± 0.039 g (dry mass, N = 16), 40% of the dry mass of mature fruits (0.271 ± 0.075 g, N = 21), and their sepals had turned from green to red (Fig. 3).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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In the first flowering event in 1996, tree 225 flowered from 30 April to 10 June and reached a plateau from 14 to 28 May (Fig. 2). The inflorescences are terminal or axially panicles with 150 ± 65 (N = 8) branchlets. A single branchlet of an inflorescence produces 4.6 ± 1.7 flowers (N = 205). Flowers are yellow, ~1.3 cm in diameter with a dry mass of 0.037 ± 0.0034 g (N = 21). The five revolute petals form a bowl-shaped structure at the center of the corolla, in which an ovoid ovary with a distinct stylopodium is located, surrounded by 15 stamens. The stamens are arranged in three verticils. Each stamen bears two-celled anthers, each with two thecae, and a terminal awn-like appendage, which becomes reflexed at anthesis. The pollen is smooth but slightly sticky, not dry, and not easily dislodged. The pendant flowers open around 1800 (Fig. 2), releasing a strong, sweet scent. The anther thecae dehisce just before anthesis. The flowers do not secrete nectar. The corollas start to fall off in the following morning, while 68% of the expanded corollas remain in the crown until the next evening. They drop or are pushed off when new flowers open. By 2300 on the next day, almost all the old flowers are shed.
Flower visitors and pollen on stigma
In net-sweeping, 66–85% of all insects identified were small beetles (<5 mm) and 10–32% were thrips (Thysanoptera). The composition of the net-sweeping samples collected on different trees was almost the same at the level of orders, though the percentage of thrips was much higher in tree 229 (32%) than in the other trees (10–11%) (Table 2). Within Coleoptera, Chrysomelidae (42%) and Curculionidae (36%) were the most abundant (Table 3). Corylophidae was abundant (24%) on tree 1001, but were not recorded from the other two trees. In flower-collection samples, all of the collected insects were thrips (74%) or beetles (26%) (Table 4; Figs. 4, 5). The number of thrips in fallen corollas was much lower than that in the flowers on the tree crown (0.014 thrips per corolla). Ten species from three families of thrips were found from the flower-collection samples (Table 4). Thrips hawaiiensis accounted for 75% of all the thrips identified.
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The estimated number of thrips per flower (0.31) was 1.7 times larger than beetles (0.18). However, the beetles were three times more numerous at night than in the daytime, and their number was almost equal to the number of thrips at 0000 (Fig. 6). Changes in the numbers of thrips samples were smaller than for beetles. Higher density of beetles at night than in the daytime and smaller fluctuation in thrips density than that of beetles were demonstrated by both sampling methods, net-sweeping and flower collection.
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Comparison of fruit set
The number of fruits decreased considerably up to days 21–24 after flowering in experiments 3–7, but the numbers more or less stabilized thereafter (Fig. 9). Observed fruit set was highest in open, flower-reduced inflorescences (2.17%, N = 323), followed by that in cross-pollinated ones (1.74%, N = 345), and fruit set in both experiments was significantly higher than in untreated, bagged inflorescences (0.27%) (P < 0.001 for open, flower-reduced; P = 0.003 for cross-pollinated; Table 5). However, fruit set in self-pollinated (geitonogamous) inflorescences did not differ from that in bagged inflorescences.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The pollinators of S. parvifolia
Small beetles, particularly Chrysomelidae and Curculionidae, were the major flower visitors of Shorea parvifolia collected by the net-sweeping method on the three study trees, and the spectra of beetle families were not different among trees except for the occurrence of Corylophidae on one tree. On the other hand, thrips were the most abundant insects collected by flower collection. The density of thrips in the crown was greater than that of beetles if averaged throughout a day, but beetles and thrips were equally abundant at night. Two other lines of evidence, higher mean pollen loads on beetles than on thrips and more frequent movements of beetles among flowers than thrips, suggest higher potential contribution of beetles to cross-pollination than thrips. However, the contribution of flower visitors to pollination cannot be measured only by their visitation frequency (Schemske and Horvitz, 1984, and references therein), and the amount of body pollen is not always a good index of their ability to effect fruit set (Inouye et al., 1994). To evaluate this parameter, we performed introduction experiments of the two major flower visitors.
Bagged flowers onto which beetles had been introduced showed significantly higher fruit set than untreated, bagged flowers, while bagged flowers onto which thrips had been introduced did not. This demonstrates that the introduced beetles were more successful than thrips at depositing pollen on stigmas and fertilizing the flowers. The number of flowers fertilized per beetle was 1.5 times higher than that per thrips.
What was not incorporated into the experiments was proportions of self- and cross-pollen that insects carry under natural conditions, namely, the proportion of beetles or thrips individuals that move between conspecific trees each day because the beetles and thrips used in the experiments were artificially transferred between trees. Though movements of the beetles and thrips among trees were not observed, beetles seem more likely to move between conspecific trees than thrips. The number of beetles increased threefold at night compared to daytime, in spite of persistence of many corollas for >24 h in the crowns. Some thrips remained in fallen corollas.
The other problem is that net-sweeping may introduce pollen load artifacts for flower visitors. It may affect both the numbers of individuals with pollen load, and the result of experiment 7, in which flower visitors collected by net-sweeping were introduced into bagged inflorescences. However, even if the sampling caused pollen load artifacts, we believe that the difference between beetles and thrips in a pollen load is still meaningful because beetles and thrips were collected in the same method.
Nearly half of the flowers had pollen on their stigma before anthesis, and a significant increase of pollen grains was observed following anthesis. The slight decrease at 1200 may be caused by earlier drops of fertilized flowers than unfertilized ones. The activity of thrips, which had a density of only 0.31 per flower, could not be responsible for all the pollen on the stigmas. Dehiscence of the anthers before anthesis probably permits pollen to be shed on the stigma as well as inner surface of the corolla, though this is paradoxical in an obligate outcrosser. Scattered pollen on the inner surface of the corolla may be more easily attached to flower visitors than pollen remaining in the anthers. The increase of pollen grains on the stigma following anthesis may be brought about mainly by the beetles. Thrips were most active at the onset of anthesis, and between-flower movement of thrips was not observed thereafter, while the beetles were observed flying around the flowers throughout the night.
The contribution of beetles as pollinators at our study site, Lambir, Sarawak, was confirmed by the beetle-introduction experiment. The situation in Lambir seems to be different from that at Pasoh, Peninsular Malaysia, from where Appanah and Chan (1981) reported thrips pollination in six species of Shorea sect. Mutica. Beetles accounted for one-third of flower visitors at Lambir, and the density of thrips (0.31 thrips per flower) was much lower than that at Pasoh (2.4) where most flower visitors were thrips. However, we cannot eliminate the possibility that thrips contributed to pollination.
Thrips often occur as general pollen feeders on various plant species (Kevan and Baker, 1983; Kirk, 1984). Thrips hawaiiensis, the most abundant thrips species on S. parvifolia at Lambir, has been collected on oil palm flowers (Elaeis guineensis, Palmae) in a plantation in Peninsular Malaysia (Syed, 1979) and on Lantana camara (Verbenaceae) in India (Mathur and Mohan Ram, 1978). They usually play a minor roll as pollinators, although predominant thrips pollination has been reported for Calluna (Ericaceae) in the Faeroes, where weather condition and lack of larger insects prohibit pollination by other insects (Hagerup, 1950), and for Annonaceae (Webber and Gottsberger, 1995; Momose, Nagamitsu and Inoue, in press), Araceae (Rust, 1980), Lauraceae (Norton, 1984), and Winteraceae (Thien, 1980; Pellmyr et al., 1990) in other regions with rich insect fauna. For a thrips-pollinated tree species in the understory of Lambir forest, Popowia pisocarpa (Annonaceae), Momose, Nagamitsu, and Inoue (in press) suggested limited pollen dispersal by thrips based on low fruit set of isolated trees. Thrips, with their oar-like wings, may be dispersed by local air drafts, including convectional movements, which are frequent in tropical forest canopies, especially during the day, but seldom penetrate the understory (Richards, 1997).
S. parvifolia and beetle pollinators
Flowers of S. parvifolia have a character adapted to beetle pollination. The apical edge of their five petals is thin and soft, and damage by beetles is concentrated in that part of the petals. The apical region of the petals may be more attractive than stigmas or ovaries for the beetles. Moving from one petal to another of a flower or feeding on pollen on the inner surface of the corolla, beetles acquire pollen loads, and then deposit pollen on the stigma. These edible rewards for the beetles may promote pollination by both rewarding beetle visits and by reducing potential damage to stigmas and ovaries.
Beetles pollinate a wide range of plant species with various reproductive characters, and the specificity of the plant-pollinator interaction also varies (Endress, 1994). Throughout the Lambir forest, many plant species are reported to be pollinated by beetles, especially in the Annonaceae (Momose, Nagamitsu, and Inoue, in press). These beetle-pollinated Annonaceae have more or less specialized relationships with their beetle pollinators and offer stigmatic secretions and/or mating sites to their pollinators (e.g., Gottsberger, 1989, 1990; Momose, Nagamitsu, and Inoue, in press). In contrast, many beetle species were collected on the flowers of S. parvifolia, though a few species accounted for most visits. The flowers are exposed in the emergent layer and never act as a refuge for the beetles. Mating behavior of the beetles was not observed.
The life histories of Monolepta species, the beetle genus that was most abundant on the flowers of S. parvifolia, remain unknown. One possibility is that they feed on young leaves of Shorea and other dipterocarps, which are available all year-round even in seasons out of general flowering periods. These beetles were collected outside the general flowering period by beating on Shorea leaves (M. Kato, unpublished data).
Plant–pollinator interactions in Shorea at Lambir appear to be different from that observed in lowland dipterocarp forests in Peninsular Malaysia: there, Shorea species in the same section are pollinated by common pollinators, and the species in each section flower sequentially. In the case of Shorea sect. Mutica, sequential flowering brings about drastic increase of their pollinators, thrips, with a extraordinary short generation time (~8 d). Thrips populations large enough for their pollination are established in a few weeks (Ashton, Givinish, and Appanah, 1988; Appanah, 1990, 1993). At Lambir, in contrast, beetles were collected on the flowers of, and may pollinate nine Shorea species including species of sect. Mutica and other sections (Momose et al., 1998). Thrips densities on their flowers were much lower than that observed in Shorea at Pasoh (Appanah and Chan, 1981; Sakai, unpublished data). How can beetles with a longer generation time than thrips offer enough pollination service to these Shorea species, which flower only in general flowering periods? Monolepta species collected on S. parvifolia flowers were found rather constantly in monthly light trap samples (T. Itioka, Nagoya University, unpublished data). Instead of such a drastic multiplication as thrips show, the beetles probably respond to an abrupt increase of floral resource in a general flowering by changing foods from dipterocarp leaves to flowers. For irregular, infrequent reproductions, Shorea species may rear the pollinators during nongeneral flowering periods by providing their leaves to the pollinators.
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FOOTNOTES |
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5 Current address: Graduate School for Asian and African Area Studies, Kyoto University, Kyoto 606-8501, Japan.
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