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(American Journal of Botany. 2004;91:289-293.)
© 2004 Botanical Society of America, Inc.

Brief Communications

The floral biology of Curcumorpha longiflora (Zingiberaceae): a ginger with two-day flowers1

Jiang-Yun Gao, Ling Zhang, Xiao-Bao Deng, Pan-Yu Ren, Ji-Jun Kong and Qing-Jun Li2

Xishuangbanna Tropical Botanical Garden, The Chinese Academy of Sciences, Mengla, Yunnan 666303 China

Received for publication May 15, 2003. Accepted for publication August 19, 2003.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 LITERATURE CITED
 
Curcumorpha longiflora is a perennial chasmophyte (rock fissure plant) ginger that usually grows in crevices of calcareous rocks and forms patches on the understory of limestone monsoon rainforests. The pollination ecology of C. longiflora was studied by monitoring phenology and flowering behavior, observing pollinator activity (frequency and behavior of visitors), and the quantity and quality of pollination services. We also investigated the germination of pollen grains and growth of pollen tubes after different pollination treatments to detect its breeding system. Based on the results: (1) for the first time in Zingiberaceae a new protandrous mechanism was found with a two-day flowering to avoid autogamy in this species; (2) under field conditions, all individuals of C. longiflora usually produced only one flower every other day to keep geitonogamy to a minimum; (3) germination of pollen grains and growth rates of pollen tubes under different pollination treatments were the same 4 h later after pollination, suggesting that C. longiflora is completely self-compatible; (4) among the limited visitors, Bombus sp. and Apis florae were effective pollinators, but they were active at different times and at different stages of the flower, probably receiving different rewards.

Key Words: Curcumorpha longiflora • floral biology • pollination systems • protandry • Zingiberaceae


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 LITERATURE CITED
 
Flowering plants have a diverse array of floral mechanisms that reduce the incidence of self-pollination and the interference between female and male sexual function (Darwin, 1877 ; Lloyd and Webb, 1986 ; Webb and Lloyd, 1986 ; Bertin and Newman, 1993 ; Barrett, 2002a ). Several features of the floral biology of animal-pollinated plants are particularly important in reducing or minimizing self-pollination, these include the spatial and temporal deployment of anthers and stigmas (herkogamy and dichogamy, respectively) and the size of floral displays. Flowers that present anthers and stigmas simultaneously are more likely to experience intrafloral self-pollination (Lloyd, 1979 ), and large floral displays increase the opportunities for geitonogamous self-pollination (de Jong et al., 1993 ; Harder and Barrett, 1995 ). Because self-pollination can result in inbreeding depression (Charlesworth and Charlesworth, 1987 ) and pollen discounting (Harder and Wilson, 1994 ), it is not unexpected that many floral adaptations have evolved to reduce these mating costs.

The Zingiberaceae is a large family of animal-pollinated tropical monocotyledons (Endress, 1994 ). Members of this family display a broad range of pollination and breeding systems (Kress and Beach, 1994 ; Sakai et al., 1999 ). Major pollinators include bees (Porsch, 1924 ; van der Pijl, 1954 ), hawkmoths (Knuth et al., 1904 ), and birds (Maas, 1977 ; Ippolito and Armstrong, 1993 ). As in other families of the Zingiberales, flowers of all species of observed gingers last for less than 1 d (Endress, 1994 ; Larsen et al., 1998 ). Nevertheless, our preliminary observations indicated that, unlike all other gingers studied, some species have flowers that last for more than 1 d.

Motivated by these observations, we decided to investigate the floral biology of Curcumorpha longiflora, a ginger from Southeast Asia include the Yunnan Province in China. Here we present the results of our investigations, which addressed three principal questions concerning the floral biology of C. longiflora: (1) What is the phenology of sexual function within individual flowers and does this species possess mechanisms to reduce self-pollination? (2) What is the compatibility system in relation to self-pollination? (3) What are the main pollinators of C. longiflora, and do they discriminate between flowers of different ages and sexual stages?


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 LITERATURE CITED
 
Research site and plant material
The study site was a slope of limestone mountain monsoon rainforest in Xishuangbannan National Nature Reserve, south Yunnan Province, China (21°41' N, 101°25' E; altitude 580 m), 5 km (southeast) from Xishuangbanna Tropical Botanical Garden (XTBG). In addition, observations of flowering phenology and hand-pollination experiments were also carried out in a ginger collection at XTBG.

Curcumorpha, with only one species (C. longiflora), is found in northeastern India, Myanmar, and Thailand (Kress et al., 2002 ). It is a small herb with a robust, fleshy rhizome, and inflorescences on separate shoots that arise from rhizomes. It usually grows in infertile cracks and crevices of calcareous rocks (Fig. 3). At our study site, plants of C. longiflora occur in a 30x25 m2 patch with ~2000 adult individuals.



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  		Figs. 1–5. Habitat, flowers in different sexual phases and visitors of Curcumorpha longiflora. 1. Bagged flower of C. longiflora in its male stage during the first day of flowering. 2. Bagged flower of C. longiflora in its female stage during the second day of flowering. 3. C. longiflora growing in the crevice of rocks. 4. A butterfly visiting a flower of C. longiflora. 5. Apis florae visiting a first-day flower of Curcumorpha longiflora

 
Flowering phenology
Flowering phenology was monitored once per week from May 2000 to August 2002. More detailed observations were made between 3 and 6 July 2001 on a total of eight flowers on six marked individuals. Every 3 h, we observed and recorded floral traits, including the timing and duration of flowering, anther dehiscence, resupination of anther parts, stigma exposure, stigma receptivity, and flower withering. Total flowers on each individual each day was also recorded.

Pollination experiments
Pollination experiments on 76 individuals included four treatments: (1) bagging, in which 16 plants were bagged without pollination; (2) selfing, in which 16 plants were hand-pollinated with the pollen of the same plant; (3) crossing, in which 16 plants were hand-pollinated with the pollen of another individual; and (4) control, in which 28 plants were left for unmanipulated natural pollination. For the first three treatments, inflorescences were bagged with nylon mesh before anthesis, and the number of open flowers was recorded.

Self-compatibility
To examine self-compatibility, we observed the germination and growth of pollen tubes. Three treatments were conducted on 45 flowers. (1) In the allogamous treatment, 15 second-day flowers on 15 individuals were bagged before their stigmas entered the receptive position and were hand-pollinated with pollen from first-day flowers on other individuals as soon as their stigmas reached the receptive position, then bagged again. (2) In the geitonogamous treatment, 15 second-day flowers on 15 individuals were hand-pollinated with pollen from first-day flowers of the same individuals. (3) In the autogamous treatment, 15 flowers on 15 individuals were bagged before opening, and after their stigmas entered the receptive position, they were hand-pollinated with the same flower's pollen, which had been collected after anther dehiscence. For all three treatments, three flowers were removed and immediately fixed in FAA solution (formaldehyde, acetic acid, 70% ethanol at 5 : 5 : 90, v/v/v) at 1, 2, 4, 8 and 12 h after hand-pollination. The allogamous and autogamous treatments were carried out in the study site between 19 and 20 July 2001, and the geitonogamous treatments were carried out in the ginger collection of XTBG from 21 to 23 July 2001, because finding two floral stages simultaneously on an individual is rare in the wild. Pollen tubes were measured following the aniline blue method as described by Dafni (1992) .

Pollinator visitation
We assessed pollinator visitation to male (first-day flowering) and female (second-day flowering) plants under natural conditions by observing six flowers on six plants of each stage everyday from 0700 to 1800 from 18 to 20 July and from 30 July to 4 August 2001. The duration and frequency of all pollinator visits were recorded. To determine whether insects preferred a particular floral stage, we compared the frequency of visits to each floral stage at different times of day. We did not observe nocturnal visitors, because anthers of all flowers were resupinate in the evening, and the surface with pollen could no longer be accessed by visitors.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
LITERATURE CITED
 
Floral traits and flowering phenology
Curcumorpha longiflora is dormant from the beginning of January to the middle of May. After 1.5 mo of vegetative growth, a 3-mo blooming season starts in July. Each flower contains one stigma and one anther consisting of two adjacent anther sacs, and lasts about 36 h. On the first day, soon after flowers fully open (0430–0500), the anther dehisces and begins to release the pollen grains (Fig. 1). At the same time, the stigma is concealed between the two anther sacs, making it inaccessible to any visitors. This state lasts around 15 h. At evening (1800–1900), the two pollen sacs begin to separate from the ventral face of the anther and curl up, exposing the stigma. The stigma then begins to curve downward and reaches the receptive position at midnight (Fig. 2). Afterwards, the flowers are in the female stage and wither in the evening of the second day. Thus, pollen transfer is only possible between different flowers (Fig. 6), and autogamy is prevented. To our knowledge, this is the first report of two-day flowering with a protandrous mechanism in Zingiberaceae. Although Roxburgh (1820) and Porsch (1924) also observed protandry in Alpinia galange and A. hookeriana, these observations were incomplete, and they correctly reported protandry but missed protogyny. Recent researches have revealed that several Amomum and Alpinia species have a remarkable sexual polymorphism, involving the coexistence of protandrous and protogynous morphs (Cui et al., 1995 , 1996 ; Li et al., 2001a , b , 2002 ). We refer to this gender strategy as flexistyly, and the polymorphism is an example of heterodichogamy (Renner, 2001 ; Barrett, 2002b ).



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  		Fig. 6. Three flowers of Curcumorpha longiflora at different sexual function stages. Flower A blooming on the first day, flower B blooming on the second day, and flower C blooming on the third day. Two sexual functions are not overlapping in a single flower. Moreover, in the natural environment, each individual plant bloomed every other day, thus pollination possibly only happened between interplant flowers. Arrows indicate direction of pollen transfer

 
Each potted individual of C. longiflora in the ginger collection of XTBG had 1–2 inflorescences at any one time, and each inflorescence had 1–2 flowers at anthesis each day. At the natural site, 61 of 70 blooming individuals of C. longiflora studied on 23–26 July 2001 produced one inflorescence, bearing one flower every other day; eight individuals produced two inflorescences that each had one flower every other day synchronously; only one individual produced one blooming inflorescence with two flowers at different sexual stages (one first-day flower and one second-day flower). Thus, under natural conditions, most individuals of C. longiflora bear only one flower or several flowers but in the same stage. It is rare that an individual simultaneously has several flowers at different sexual stages (first-day flower and second-day flower). These results imply that although geitonogamy seems possible, it seldom happens under natural conditions.

Protandry and protogyny are the two types of dichogamy that exist widely in flowering plants, both have been thought to be outcrossing mechanisms. However, if more than two flowers of an individual bloom asynchronously, neighboring flowers are still likely to be pollinated with the plant's own pollen (geitonogamy). Therefore, if dichogamy is to be an efficient outcrossing factor, it must be reinforced by further temporal mechanisms at the inflorescence, the individual, or the population level (Lloyd and Webb, 1986 ; Endress, 1994 ). In C. longiflora, geitonogamy will not be prevented through protandry due to the probability of pollination between first-day and second-day flowers blooming on the same individual. However, the behavior of almost all individuals of C. longiflora producing only one flower every other day might further a lower geitonogamy in natural populations.

Breeding system
Because of an unpredicted characteristic of seed dispersal of C. longiflora, we failed to harvest all fruits and accurately record the seed set per fruit in all four treatments of the pollination experiments. Seeds were ejected from seed capsules at a very early stage of fruit maturation and soon removed by ants. Instead, we estimated the fecundity of different pollinations from the occurrence of enlarged fruits after treatments. Enlarged fruits were found in selfing, crossing treatments, and controlled inflorescences with 15.83 ± 5.87 (mean ± 1 SE; n = 41) seeds per fruit. But in the bagging treatment, we found no enlarged fruit. The pollen tube growth experiments in the three treatments showed that: (1) pollen tubes from autogamous pollinations started to germinate and grow 2 h after pollen had been placed on the stigma; (2) pollen tubes grew more rapidly after the allogamous treatment than following geitonogamous pollination as assessed during the first 2 h (29% vs. 16%), then reached to the same at 4 h; (3) in all three treatments, pollen tubes reached the ovary within 8–12 h (Fig. 7). These results indicate that there is no stigmatic or stylar self-incompatibility in C. longiflora.



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  		Fig. 7. The pattern of pollen tube growth in the styles under three pollination treatments

 
Pollinator visitation
Four taxa of diurnal insects, Bombus spp., Apis florae, Trigona pagdeni, and an unidentified butterfly species, were observed visiting flowers of C. longiflora. Of those that visited flowers of C. longiflora regularly, Bombus spp. and Apis florae are thought to be the primary pollinators. Both of their bodies could touch stigmas and anthers, and moreover, pollen grains were obviously observed on their backs. The other two visitors, Trigona pagdeni and the butterfly, are poor pollinators: Trigona pagdeni appeared to visit C. longiflora by accident (12 flower-times during 33 h of observation on 14 flowers), and butterflies seem to visit C. longiflora as nectar robbers, i.e., they sucked nectar with their proboscises from the side and did not touch anthers or stigmas (Fig. 4).

The most common visitors to C. longiflora at the research site were bumble bees. These bees visited both flower stages without any obvious discrimination, with the most frequent visits between 0900 and 1700 hours (Fig. 8). Apis florae probed flowers of C. longiflora mainly for pollen, and they preferentially collected pollen in the early morning from first day's flowers (Figs. 5, 8).



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  		Fig. 8. The visitation patterns on the different stage flowers of C. longiflora by Bombus spp. and Apis florae (30 July–4 August 2001)

 
Nectar production is difficult to measure because of the long and fragile corolla tube with a very thin inner space. The availability of pollen grains at different sexual stages thus results in a difference in the reward composition (pollen and nectar in first-day flowers and only nectar in second-day flowers). Bumble bees (Bombus spp.) used C. longiflora primarily as a nectar source and, therefore, did not seem to prefer any particular sexual stage. In contrast, honey bees (Apis florae) visited flowers mainly for pollen and preferred to forage on first-day flowers. The visiting frequencies showed that honey bees are probably not as important as pollinators to C. longiflora at our research site because they are not as abundant as bumble bees throughout the flowering period of C. longiflora.


   FOOTNOTES
 
1 The authors thank Dr. W. John Kress, Smithsonian Institution, Prof. Spencer Barrett, University of Toronto, and Prof. Amots Dafni, University of Haifa, for their constructive discussions or valuable comments on the draft. We also want to acknowledge Dr. Lee Klinger for correcting the manuscript in format and language. This research was supported by the key project of the Ministry of Science and Technology (2001CCA00300), the key project of the Chinese Academy of Science (KSCX2-SW-105), the National Natural Science Foundation of China Grant 30225007, 30170069, and the Natural Science Foundation of Yunnan Province of China (2001C0024Q). Back

2 qjlixtbg{at}bn.yn.cninfo.net . Back


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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 LITERATURE CITED
 
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