1 Acta Botanica Sinica 2004, 46 (3): Pollination Ecology of Caesalpinia crista (Leguminosae: Caesalpinioideae) LI Shi-Jin 1, ZHANG Dian-Xiang 1*, LI Lin 2, CHEN Zhong-Yi 1 (1. South China Institute of Botany, The Chinese Academy of Sciences, Guangzhou , China; 2. No.1 Middle School of Guangzhou Railway Company, Guangzhou , China) Abstract: The flowering phenology, pollination ecology and breeding system of Caesalpinia crista L. were studied in Dinghushan Nature Reserve, Guangdong, China. The species started blooming in February or March, then last till late April. It took about one week from first flower appearance to its full blooming, which lasted for 2-4 d. The pollen-ovule ratio was ±500. The breeding system was self-incompatible, and protogynous xenogamy. Hymenoptera constituted the major group of pollinators. The pollination type is ambophily, the species could be pollinated by wind if the pollinators were unavailable: this is the first record of ambophily in the genus Caesalpinia. The floral structure adaptation to the pollinating behavior of carpenter bees was described. The influences of artificial treatments in pollination biological studies on the flowering and fruiting of the plants were also discussed. Key words: pollination; ambophily; breeding system; flowering phenology; Caesalpinioideae; Caesalpinia crista Plant reproductive ecology is a vital and highly productive field within modern biology (Lovett Doust and Lovett Doust, 1988; Richards, 1997; Geber et al., 1999). Caesalpinia is a pantropical genus with species of trees, shrubs, and lianas, but the study of pollination ecology of the genus is so far limited to the New World species (Lewis, 1998). Only a few species of Caesalpinia have been studied with regard to their pollination biology: C. pulcherrima (L.) Sw. (Ali, 1932; Cruden and Heaman-Parker, 1979; Bullock, 1985); C. (Erythrostemon) gilliesii (Wall. ex Hook.) Dietr. (Coccuci et al., 1992); C. calycina Benth. and C. pluviosa DC. var. sanfranciscana G. P. Lewis (Lewis and Gibbs, 1999). Vogel (1990) reported that four flower types were found in Caesalpinia, and each of which adapted to a different pollinator (bee, butterfly, moth and hummingbird), suggesting that the floral character suits in the segregated genera of Caesalpinia may be closely related to the type of pollinators. Jones and Buchmann (1974) stated that Caesalpinia relied heavily on Centris species for pollination. Twenty species of Caesalpinia have been recorded from China (Chen, 1988; Li et al., 2001). C. crista is a species widely distributed from India to Polynesia. In China, it is found in Sichuan and Hubei provinces in the north and covers all the provinces south of the Yangtzi River (Larsen et al., 1984; Chen, 1988). 1 Materials and Methods Caesalpinia crista L. is a liana climbing to 10 m, with glossy branchlets more or less armed with recurved prickles. Flower buds are glabrous. The lowest calyx lobe brown, cucullate, covers the flower bud before blossom. The other four calyx lobes are yellow. Petals are yellow, standard blade limb suborbicular and with a red spot (Fig.1). The other four petals have oblong-elliptic blades. Stamens 10, filaments unequal, ca. 12 mm long, are woolly from the base to the middle. The filaments form a pseudotube at the base and remain only two splits (Fig.2). The splits are covered by the standard s claw. Style ca. 10 mm long; stigma truncated, wider than the style, with a mucilage cavity at the top and ciliate around the rim (Figs.7, 8). Data were obtained throughout three flowering seasons ( ), from March to April, in three separate natural populations. The site is located in Dinghushan Nature Reserve (Guangdong, China) at approximately 23 o 10' N, 112 o 34' E. The first population is located at an altitude of 20 m.a.s.l, with about 10 individuals along a small stream in front of the Reserve s headquarters building. The other two populations are both situated near the Baodingyuan Sight at an elevation of 70 m.a.s.l, with 12 and three individuals respectively. The last two populations are distant of 500 m and are separated by a forest of Pinus massoniana. 1.1 Floral phenology To determine the flowering period, flower lifespan and anther dehiscence, two individuals were randomly chosen from each population and two large panicles were taken from each plant. Stigmatic receptivity was determined by hand-pollination in 2000 and Stigma viability was determined by the changes in color and moisture of the stigma Received 6 Jun Accepted 30 Aug Supported by the Knowledge Innovation Program of The Chinese Academy of Sciences (KSCX B), Scib Directors Fund of South China Institute of Botany, The Chinese Academy of Sciences, Special Fund for Biological Systematics and Floristics, Fund for Scholars and Students Returned from Overseas and a grant from the Bureau of Environmental Protection of Guangdong Province (970165). * Author for correspondence.
2 in 2000 and 2001 and tested by using the MTT solution (Rodriguez-Riano and Dafni, 2000) in Pollen viability was also tested by the method of MTT. The volume and sucrose concentration of the floral and extrafloral nectar were measured by microcaps (Sigma Co.) and a hand refractometer (Atago) respectively. Floral nectar was collected from full blooming flowers that were bagged with nylon nets prior to their anthesis, and the extrafloral nectar from one rachis at nine o clock in fine weather. 1.2 Breeding system and pollination success Emasculation was performed one day before the flowers open. Hand-pollination treatments were carried out twice a day (morning and afternoon). Fruit set was calculated as number of young fruits (two weeks after flowering) to number of pollinated flowers. Counting out immature rather than mature pods was a precaution against herbivora, as insects were eating young pods at different stages. Several treatments were given to test the breeding system (Table 4). The nets and bags were made of fine nylon fabric and thick waterproof paper respectively. Bags were used to prevent pollination by insects and air-disseminated pollens, whereas nets served to stop only insects. The pollen-ovule ratio (P/O rate) was estimated following the method of Cruden (1976) and Dafni (1992). Ten flowers in each population were chosen at random, and the number of pollen grains and ovules in each flower were calculated and finally an average and standard deviation was estimated. 1.3 Visitors Flower visitors were observed in the field over the peak of flowering period between 07:00 am and 19:00 pm. The voucher specimens were collected and taken to the laboratory for identification. To determine if the main visitors are pollinators, the pollen on the stigmas was recorded after being first visited. 1.4 The flower-pollinator interaction test Virgin flowers were bagged prior to anthesis and the pollen grain numbers on the stigma were counted after the first visit. In order to test the nectar volume consumed by visitors in each visit, the nectar volume in unvisited and once visited flowers were recorded and compared. To determine the function and importance of each floral organ (standard, anthers and other petals) in attracting the pollinators, 600 flowers on three large panicles were chosen. The three manipulations are: standard removed only, anthers removed only and all the petals removed. The visiting frequency of the two principal pollinators on these manipulated flowers were recorded. 1.5 The influences of the treatments to flowering Since bagging and netting may influence the function of flowering and fruiting, their impact on the flowering of C. crista was tested by control experiment. The influence of flowers bagging and netting to the lasting time of the stigma receptivity, the petals longevity, the extra-floral nectar volume on the rachis, and the nectar volume in the flowers were all recorded and compared with untreated flowers. 2 Results 2.1 Floral phenology C. crista started blooming from March to July across its distribution range. The flowering period started from February to March at Dinghushan. It usually takes about 10 d for an inflorescence with fully developed buds to open all its flowers, although it may take two to three weeks for one inflorescence to develop its flower buds. The lifespan of a single flower (from petals opening to stamens and petals lost) was 4 5 d. More than five months were needed for fruit to mature (Table 1). 2.2 Sexual and breeding system The flowers of C. crista are bisexual and protogynous. The protogyny in the species was revealed by the fact that the stigma becomes viable and receptive, and stretched out before corolla opened and anther dehisced (Fig.3). Hand-pollinated one day before opening, the flowers could be fertilized and produce fruits, which indicated the occurrence of protogyny in the species (Table 2). The flowers were slightly but sweetly fragrant. There were about 200 flowers for one panicle and more than flowers for one plant. The petals were yellow. The style was 15 mm long and the stigma light creamy green, ciliated around the rim and chambered (Figs.7, 8), turning brownish in color soon after being pollinated. One flower displayed 10 stamens. Table 1 Floral phenology of Caesalpinia crista at Dinghushan Mountain, Guangdong, China Year Elevation Inflorescence First flower Full Flowering termination Fruit (m.a.s.l.) appearing appearing blooming and first fruit appearing maturing Mar. 22 Mar Mar Apr Oct Mar. 28 Mar. 1 3 Apr Apr Oct Feb. 6 Mar Mar. 1 4 Apr Sept Feb. 9 Mar Mar. 2 5 Apr Sept Feb Feb. 3 7 Mar Feb Feb Mar.
3 LI Shi-Jin et al.: Pollination Ecology of Caesalpinia crista (Leguminosae: Caesalpinioideae) Figs.1 8. Flower and pollinators of Caesalpinia crista. 1. Flowers in blooming. 2. Base of the androecium, showing the two splits. 3. Flowers before the corolla open, showing the stretched stigmas. 4. Xylocopa sinensis sucking nectar in the flower. 5. Apis cerana sucking extraflora nectar along the rachis. 6. Episyrphus balteata eating pollen on the anthers. 7. A stigma, showing the cilia. 8. Stigma, showing the cavity and the pollen in the cavity.
4 Table 2 Stigma receptivity of Caesalpinia crista as evaluated by fruit set under artificial hand-pollination Date Flowers Fruit Fruit set (%) One day before bloom 3/14/ The blooming day 3/28/ /15/ Two days after blooming 3/29/ /15/ Five days after blooming 3/19/ Nine days after blooming 3/22/ Table 3 Pollen viability during different stages of anthesis Days after anther Total number of Viable Percentage of dehiscence pollens tested pollen viable pollen (%) The immature anthers exhibited approximately the same color as the corolla, and became ochre after dehiscence. The pollen remained viable for 2 3 d (Table 3). Nectar was produced within the flowers at near the base of style and filaments, and on the flower rachis by the extra-floral nectariferous glands upon anthesis. Honeybees (Apis cerana) have been observed sucking the nectar along the rachis even after the flowers had withered (Fig.5). The floral disc was stained red in neutral red solution, indicating that odor glands, which attracted pollinators were located in the disc. Up to (1.2 ± 0.7) µ (range from 0.55 µl to 2.8 µl; N = 20) nectar with 29%± 5% (range from 17% to 35%; N = 20) of sucrose were recorded per full blooming flower from the natural populations at 09:00 am in fine weather. Bagged by fine nylon net, the emasculated flowers set fruit and the fruit set were 0.5% 3.0%, which were slightly lower than the fruit production ratio under natural conditions (Table 4; Fig.1). The result indicated that this species could also be pollinated by wind if the pollinators are unavailable. And this is the first report of ambophily (a combination of both wind and insect pollination) in the genus Caesalpinia. Autogamy or apomixis played no role in fruit production in the species: none of the flowers bagged or with stigma cut produced fruit. All inflorescence bagged and flowers pollinated with pollen from the same plants recorded similar results (Table 4). 2.3 Pollinators Seventeen species (included to four Orders) of insects were captured while they were visiting the flowers during our study period (Table 5). Five frequently encountered visitors were proved to be pollinators by identifying the pollen on the stigmas of the previously bagged virgin flowers after they had been visited. Hymenoptera were the most common visitors and covered more than 90% of the total number of visitation. Carpenter bees (Xylocopa sinensis Smith, Xylocopa sp.), with the largest body, highest visiting frequency and bringing most pollen per visit, were the most important pollinators (Table 6). 2.4 Visitation patterns of the main pollinators and the flower-insect interaction In the flower of C. crista, the ten filaments tightly closed against each other by its widened pubescent base, while only two narrow splits were formed (Fig.2). The splits faced the upper red spotted petal (standard). The standard reflexed at the middle and closed the filaments, so the splits were covered by the standard. Of all the pollinators only the carpenter bees can easily force away the standard with its strong head and thus suck the nectar from the splits. The carpenter bees approached the flowers from above Table 4 The fruit set of Caesalpinia crista under different treatments Treatments Date Flowers Fruit Fruit set (%) Emasculation and netting 3/28/ /28/ /14/ Emasculation and no sheathing 3/30/ /16/ Hand cross pollination between different plants in same population 3/29/ /15/ Hand pollination between different inflorescences in same plant 3/28/ /14/ Emasculation and bagging 3/28/ /14/ Stigma cutting 3/28/ /14/ Flower bagging 3/28/ /14/ Inflorescence bagging 3/28/ /14/ Untreated 3/28/ /14/
5 LI Shi-Jin et al.: Pollination Ecology of Caesalpinia crista (Leguminosae: Caesalpinioideae) Table 5 Floral visitors and their rewards Order Family Species Frequency* Aim Hymenoptera Xylocopidae Xylocopa sinensis Smith 55+10** nectar Xylocopa sp. nectar Syrphidae Episyrphus balteata De Geer 10+4 pollen Syrphus sp. pollen and nectar Verpidae Vespa affinis pollen Verpidae sp. pollen Apidae Apis cerana Fabr pollen and nectar Apis sp. pollen and nectar Formicidae Formicidae sp. nectar Coleoptera Cetonnidae Potosia brevitarsis Lewis 3+2? Lepidoptera Lycaenidae Japonica lutea Hewitson 7+3 nectar Antigius attilis Bremer 6+3 nectar Pieridae Delias pasithoe Linnaeus 6+3 nectar Nymphalidae Mimathyma chevana Moore 8+4 nectar Uraniidae Uraniidae sp. 3+2 nectar Diptera Muscidae Episyrphus sp pollen Musca domestica nectar *, frequency (presented on one inflorescence per hour) of a daily average; **, very similar in outline, it is too difficult to record the frequency of the two species of Xylocopa respectively, and the frequency is the summation of the two species;, less than 5 or have not been recorded. Table 6 Pollination efficiency of the flower visitors Xylocopa sinensis Xylocopa sp. Apis cerana Episyrphus balteata Syrphus sp. Virgin stigmas visited Stigmas on which pollen grains were detected after one visit 95% 100% 75% 80% 65% Percentage Average pollen on the stigma and in front. Grasped by the carpenter bee, the flower turned down, and so the carpenter bee dangled from the flower, facing upward while sucking the nectar (and thus easier to suck the nectar). The carpenter bee grasped the upper pair of lateral petals (keel petals) and lower lateral petals (wing petals) with its middle and hind legs respectively. The front legs can help its head to push the standard away when sucking the nectar and brush the pollen which stuck on the head when it has a rest. Usually, carpenter bees are efficient pollinators. Almost all the stigmas had pollen and more than 30 pollen grains were recorded on each stigma once visited by the carpenter bees (Table 6). These pollinators could suck about 1 µl nectar in the flower at one visit and almost no nectar was left when they quitted. The nectar volume in the flower decreased about 83.3% after one visit by the carpenter bees (Table 7). Although the stamens were not equal in length, the anthers and the truncated stigma were located at the same bevel. While a carpenter bee is sucking the nectar, its hairy abdomen touches the anthers and the stigma. The second most important visitor was A. cerana species. They approached the flower from above or in front. They grasped the filaments, collected the pollen and touched the stigmas by their abdomens. Seventy-five per cent stigmas had pollen and an average of ca. 14 pollen grains was brought on one stigma at each visit on flowers visited by A. cerana. The nectar volume in the flower decreased by 16.7% after once visited by the honey bees (Table 7). Bringing pollen and taking away less nectar, A. cerana was a very economic pollinator. Episyrphus balteata was another economic pollinator. Having small and light body, they could grasp and stay on anthers when eating pollen. Eighty per cent of virgin stigmas had pollen and about eight pollen grains were brought to one stigma after once visited by E. balteata. A species of hover-fly (Episyrphus sp.) was also among the floral visitors. The insect approached the flower from above and landed on the flower to collect pollen grains from the dehisced anthers by licking. Hover-flies were even able to lick off all the pollen grains on all the opened anthers in a flower. As they also licked the stigmas for its exudate, hover-flies were presumably helping pollination. However, a direct observation of their pollination efficiency needs further observation. Two large panicles with a total of 200 flowers were selected and all the standard petals with red spots cut off. It seemed that the removal of the standard petal with nectar guides did not influence the visitors activities. In the other treatment, when all the anthers of the 200 flowers on an inflorescence were removed, the insects with pollen as their only reward never came again. In the third treatment, all the petals of the 200 flowers on an inflorescence were removed,
6 only bees with small bodies that could grasp the filaments and collect the pollen would visit the flowers again. Carpenter bees, the primary pollinator, with a larger body size, never came again, as there were no petals on which to grasp and to land on (Table 8). 2.5 Influences of the treatments on flowering Under natural conditions the petals can keep themselves on the flower for 4 5 d before withering. When caged by fine nylon fabric nets, withering will defers 2 3 d. If caged by thick waterproof paper, they will defer 5 7 d (Table 9). Under natural conditions the volume of extra-floral nectar on each rachis is (4.0 ± 2.0) µ (range from 2.2 µl to 8.0 µ ; N = 20) with 30% ± 12% (range 17% 70%; N = 20) sucrose each collecting (at nine o clock in fine weather). When the inflorescence caged by waterproof paper (12.1 ± 4.1) µ (range from 9.0 µl to 14.1µ ; N = 10) of nectar with 34% ± 8% (range 25% 55%; N = 20) mean sucrose were produced on one rachis each collecting (Table 9). (1.2 ± 0.7) µ (range from 0.55 µl to 2.8 µ ; N = 20) nectar with a concentration of 29% ± 5% (range from 17% to 35%; N =20) sucrose was recorded per untreated full blooming flower at nine o clock in fine weather. It increased to (2.0 ± 0.8) µ (range 1.6 µ 3.0 µ ; N=20) if bagged for more than 24 h and to (1.8 ± 0.8) µ (range 1.5 µ 2.8 µl; N = 20) if emasculated (Table 9). Under natural conditions the stigmas could remain viable for about 5 d. They could only be viable for 2 3 d if they had been assisted with hand-pollination. But they can remain viable for 7 and 9 d respectively when caged by fine nylon fabric nets and waterproof paper (Fig.9). 3 Discussion 3.1 Sexual and breeding system There are ± 500 pollen grains and two ovules in Fig.9. Stigma viability of Caesalpinia crista as revealed by staining with MTT solution. Table 7 The nectar volume left in the flower of Caesalpinia crista after once visited by different insects Treatments No. of flowers Range (µl) Average (µl) Percentage of the decrease (%) Natural for control Visited by carpenter bees (2)* Visited by Apis cerana Visited by Syrphus sp *, Xylocopa sinensis and Xylocopa sp. Table 8 The role of different floral organs in attracting pollinators Treatment No. of flowers Visitors Visit Percentage of the frequency frequency* changing (%) Remarks Standard removed 200 Carpenter bees (2)** No influence Apis cerana No influence Episyrphus balteata Anthers removed 200 Carpenter bees (2)** No influence A. cerana No pollen E. balteata All petals removed 200 Carpenter bees (2)** No holder A. cerana Some influence E. balteata No influence Natural for control 200 Carpenter bees (2)** A. cerana E. balteata *, frequency (presented on one inflorescence per hour) of daily average; **, Xylocopa sinensis and Xylocopa sp. Table 9 The influence of artificial treatments to the floral lifespan and behavior Inflorescence The petals keep themselves The extrafloral nectar on The nectar in the flower (N=10) on the flower (d) the rachis (µ )* (µ )** Bagged Netted 6 8 Emasculated Naturally *, one time collecting at 9 o clock in fine weather; **, from one full blooming flower at 9 o clock in fine weather.
7 LI Shi-Jin et al.: Pollination Ecology of Caesalpinia crista (Leguminosae: Caesalpinioideae) one flower of C. crista. The P/O ratio is ± 500, and it belongs to obligate xenogamy according to Cruden (1976). It has been postulated that few plant-pollinator relationships are absolutely obligatory, and generalization appears to be the rule rather than the exception (Waser, 1996). Windpollinated species usually have much higher P/O ratio than their insect-pollinated relatives (Tomlinson et al., 1979; Melampyand Hayworth, 1980; Adams et al., 1981). The high value of the P/O ratio may also indicate that anemophily played a role in C. crista (Pohl, 1937; Cruden, 1977; Preston, 1986). Revealed by the fruit set by wind and insect pollinated flowers, the pollination pattern of C. crista is ambophily, and this is the first report in family Leguminosae. Ambophilous species are generally considered as characterized by numerous and simple flowers with small and open corollas (Linder, 1998), the more showy and intricate flower of C. crista indicated that this may not be always the rule. C. crista, as a species distributed widely in pantropical regions, could have been dispersed comparatively recently to some of its extend ranges, and ambophily, an efficacious pollination mode, may have helped it survive in its newly claimed habitat while the pollinators were not available. Under this hypothesis (adaptation hypothesis), ambophily would be an adaption to the new environment. The other possibility is that ambophily in the species was inherited from its ancestors (phylogenetic hypothesis). Further studies on more species in the genus with a close phylogenetic relationship and species with similar distribution pattern are needed to test these hypotheses. There probably existed a gradual evolution of adaptations to wind-pollination from biotic pollination, where ambophily may have been an intermediate stage (Linder, 1998; Wallander, 2001). Theresa et al. (2002) recently concluded that ambophily might be more common than was previously presumed and could represent either a stable or a transitional state. Hairs on the stigma seemed to play an important role in pollen reception in the species. When honeybees and carpenter bees came to collect pollen or nectar, pollens adhered on the abdomen of the insects were scraped off by the stigmatic fringe hairs like combs and were forced into the stigmatic chamber. The hairs could also present the pollen dissipating by wind or insects. The comb-like stigmatic fringe hairs were reported in several species of Caesalpinia previously (Lewis and Gibbs, 1999). 3.2 Combined attraction Very often, bee-pollinated plants have colored spots on the corolla attracting pollinators which is called nectar guide. Nectar guide occurs on the standard petals of many species of the genus Caesalpinia (Lewis, 1998) and it occurs in C. crista also. But the standard with red colored spots of C. crista seemed to have no function in attracting the pollinators. The petals, sepals and anthers were yellow, and could be perceived by bees (Percival, 1965). Hundreds of yellow flowers were found on the plant during the flowering period. A great deal of extrafloral nectar appeared along the rachis of C. crista even after the flowers withered. Consequently, C. crista very likely attracts pollinators by combined factors, but not by a single one. 3.3 Visitation patterns of the main pollinators and the flower-insect interaction The size and behavior of the carpenter bees fit the flower size and its structure. The nectar was protected by the androecium, and only carpenter bees with powerful heads could easily suck the nectar. Several Caesalpinia species was reported to be pollinated by Xylocopa species (Lewis, 1998; Lewis and Gibbs, 1999). 3.4 Influences of treatments on flowering The method of being bagged or netted can prolong the lifetime of the stigmas and petals. It may be the result of increased temperature and humidity in the cage that caused the prolongation of the floral lifespan, or it is more likely because bagging of the flowers prevent pollens from falling on the stigmas and thus the ovules kept un-fertilized. The lifespan of the flowers are prolonged waiting for pollination. However it is still unknown why emasculation stimulates the secretion of floral nectar. In most studies, pollination biologists routinely used nets and bags to prevent insects and the pollen in the air. Our study manifested that the artificial treatments could bring a certain degree of influence to the flowering and fruiting function of the plants, and this influence should be taken into consideration. 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