Annals of Botany 103: 1159– 1163, 2009
doi:10.1093/aob/mcp051, available online at www.aob.oxfordjournals.org
SHORT COMMUNICATION
Flower thermoregulation facilitates fertilization in Asian sacred lotus
Jiao-Kun Li and Shuang-Quan Huang*
College of Life Sciences, Wuhan University, Wuhan 430072, China
Received: 2 January 2009 Returned for revision: 23 January 2009 Accepted: 27 January 2009 Published electronically: 12 March 2009
† Background and Aims The thermoregulatory flower of the Asian sacred lotus (Nelumbo nucifera) can maintain a
relatively stable temperature despite great variations in ambient temperature during anthesis. The thermoregulation has been hypothesized to offer a direct energy reward for pollinators in lotus flowers. This study aims to
examine whether the stable temperature maintained in the floral chamber influences the fertilization process
and seed development.
† Methods An artificial refrigeration instrument was employed to cool flowers during the fertilization process and
post-fertilization period in an experimental population. The effect of temperature on post-pollination events was
also examined by removing petals in two field populations.
† Key Results Treatments with low floral temperature did not reduce stigma receptivity or pollen viability in undehisced anthers. Low temperature during the fertilization period significantly decreased seed set per flower but low
temperature during the phase of seed development had no effect, suggesting that temperature regulation by lotus
flowers facilitated fertilization success. Hand-pollination treatments in two field populations indicated that seed
set of flowers with petals removed was lower than that of intact flowers in north China, where ambient temperatures are low, but not in south China, confirming that reducing the temperature of carpels did influence postpollination events.
† Conclusions The experiments suggest that floral thermoregulation in lotus could enhance female reproductive
success by facilitating fertilization.
Key words: Nelumbo nucifera, Asian sacred lotus, beetle-pollination syndrome, fertilization process, postpollination events, pollen viability, stigma receptivity, thermoregulation.
IN T RO DU C T IO N
Favourable temperature is crucial for various phases of sexual
reproduction in flowering plants, including pollen development,
pollen transfer, stigmatic receptivity, pollen germination,
pollen-tube growth, double-fertilization and seed development
(Pigott and Huntley, 1981; Kjellberg et al., 1982; Young,
1984; Corbet, 1990; Stephenson et al., 1992; Kudo, 1995;
Delph et al., 1997; Hedhly et al., 2003). To maximize reproductive success, flowering plants have evolved various strategies to
maintain an optimal microclimate within flowers. In some
plants, flowers possess dense pubescence and overlapping
bracts to minimize heat loss and protect their flowers from
cold (Meinzer and Goldstein, 1985; Miller, 1986; Tsukaya
et al., 2002), whereas others elevate floral temperature by positioning flowers in a convenient position on the plant (Lu et al.,
1992) or sun-tracking to absorb solar energy (Hocking and
Sharplin, 1965; Kevan, 1975; Corbet, 1990). In contrast to
those plants passively receiving energy from the sun during
anthesis, thermoregulatory plants can actively produce a significant amount of heat to warm themselves and can precisely adjust
the rate of heat production in relation to ambient temperature
(Seymour and Schultze-Motel, 1997).
The role of thermoregulation in Asian sacred lotus, Nelumbo
nucifera, as well as other homoeothermic species, such as
Philodendron selloum (Nagy et al., 1972), Symplocarpus
foetidus (Knutson, 1974) and Dracunculus vulgaris (Seymour
and Schultze-Motel, 1999), has been interpreted as rewarding
* For correspondence. Email [email protected]
endothermic beetles (Schneider and Buchanan, 1980;
Seymour and Schultze-Motel, 1996) or warming beetles to
flight temperature and thus allowing them to depart carrying
pollen (Burquez et al., 1987), and accelerating scent emission.
Given that these species share an obvious cantharophily syndrome including a large chamber enclosed by petals, a large
number of stamens and odour release, homoeothermic flowers
have been considered as a warm shelter for pollinator activity
(Seymour and Schultze-Motel, 1997). Heat production attracts
pollinators, or facilitates their departure (Burquez et al.,
1987), helping to remove pollen and so facilitating male reproductive success. Meanwhile, the stable temperature maintained
in flowers can warm the sexual organs, which may affect the
development of pollen and ovules, and facilitate fertilization
and seed development. For example, solar tracking enhances
sexual reproduction by increasing pollination, fertilization and
seed development in Adonis ramosa (Ranunculaceae, Kudo,
1995) and by promoting pollen germination in the snow buttercup Ranunculus adoneus (Galen and Stanton, 2003). Although
it is known that favourable temperature is crucial for postpollination events, it remains unclear whether stable temperature is necessary for fertilization and seed development in
thermoregulating plants.
Lotus flowers can physiologically regulate the floral temperature during anthesis by heat production via a large obconical
receptacle, maintaining a relatively favourable temperature
between 30 and 36 8C when the ambient temperature fluctuates
between 10 and 45 8C (Seymour and Schultze-Motel, 1996,
1998; Seymour et al., 1998). The homoeothermy coincides
# The Author 2009. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved.
For Permissions, please email: [email protected]
1160
Li & Huang — Thermoregulation in lotus flowers
with the period of stigma receptivity in lotus flowers (Seymour
and Blaylock, 2000), suggesting that events at, or soon after, pollination can be influenced by floral temperature. Here, we investigate the effect of temperature on post-pollination events in
hand-pollinated flowers by reducing flower temperature using
an artificial refrigerator in an experimental population. It was
found that stigma receptivity and pollen viability in undehisced
anthers were not influenced by low temperature, whereas low
floral temperature during the fertilization period significantly
decreased seed production. To test whether similar effects
occurred in the field, flower temperature was reduced by removing petals and a comparison was made of seed production after
hand-pollination in two populations experiencing different
ambient temperatures. The field hand-pollination treatments
confirmed that the stable temperature was important in postpollination events in lotus flowers.
M AT E R IA L S A ND M E T HO DS
Study species and populations
Nelumbo nucifera Gaertn (Nelumbonaceae) is an emergent
aquatic plant with a wide distributional range in the Old World
throughout temperate and tropical Asia (Borsch and Barthlott,
1994). The bowl-shaped flowers are solitary and large, up to
25 cm in diameter, emitting intense odours during anthesis.
Each flower has about 20 –30 carpels in an obconical receptacle
and 200– 400 stamens (Ni, 1987; Hayes et al., 2000). Each
carpel has a single ovule. Placentation is laminar, and the
ovule is anatropous, bitegmic, crassinucellate and pendulous
(Gupta and Ahluwalia, 1977). Lotus flowers are protogynous,
and anthesis of one flower lasts 3 – 4 d. The protruding stigmas
of flowers on the first day of anthesis (hereafter termed D-1)
are receptive and covered with a mucilaginous secretion,
whereas undehisced stamens are tightly pressed by erect petals
around the receptacle and are not accessible (Schneider and
Buchanan, 1980). The male stage starts from the second day
(D-2) of anthesis, as numerous stamens are revealed, bearing
abundant pollen. Notable thermoregulation occurs in D-1
flowers and is maintained throughout the night when the
flower petals close (Seymour and Schultze-Motel, 1996, 1998).
Flower refrigeration and thermography
To test the effect of low floral temperature on postpollination processes, a refrigerating instrument was constructed. In an experimental population at Wuhan Institute of
Vegetable Science, Hubei Province (298580 N, 1138410 E)
during 2007 and 2008, a heat-insulated foam box (10 10 10 cm) with a circular hole (5 cm in diameter) at the
bottom in the centre, allowing a flower with petals removed
to be inserted, was used to simulate a real floral chamber.
To lower the internal temperature, some bags of ice were put
inside the box without touching the receptacle and stamens
of the petal-removed flower. Because heat production by
lotus flowers does not depend on the light cycle (Seymour
et al., 1998), a cover was added on the box in order to
improve the reduction of internal temperature during each
refrigeration treatment. A Delta TRAK FlashLink data
logger (http://www.deltatrak.com) was used to monitor
temperature fluctuations in the interior of the refrigerated and
control flowers.
Effect of low temperature on reproductive processes
In order to examine the effect of low temperature on stigma
receptivity, two treatments were applied to D-1 flowers commencing in the morning: (1) refrigeration for about 11 h from
0600 h to 1700 h, and then pollinated with normal pollen (see
below for different pollen types); (2) no refrigeration during
the daytime, and then pollinated at about 1700 h with normal
pollen. The period from pollination to fertilization (hereafter
termed the fertilization process) is reported to last 6 – 8 h in
lotus flowers (see Yan, 1986). To explore the effects of temperature fluctuation on the fertilization process, and/or postfertilization development, D-1 flowers were hand-pollinated
in the morning and then subjected to four additional treatments:
(3) refrigeration immediately from 0600 h to 1700 h (daytime
refrigeration); (4) no refrigeratation until 1700 h, but then
refrigerated throughout the night (nocturnal refrigeration); (5)
petals were removed around 0600 h without refrigeration; and
(6) no refrigeratation or removal of petals (control). In order
to test the effect of low temperature on pollen viability in
undehisced anthers, we pollinated normal D-1 flowers with
pollen shed from flowers previously given treatments (3) and
(4). Melting ice bags were replaced around noon with newly
frozen ones to ensure that the temperature in the box was
maintained below 30 8C.
The effect of floral temperature on reproductive success was
further examined by removing petals in two field populations
of lotus, at Lantian and Mishan, in summer 2006 and 2008.
Without petals enclosing the obconical receptacle, floral temperature approximated to the ambient air temperature. A comparision was made of seed production of hand-pollinated
D-1 flowers from which all petals were removed with that of
flowers in which petals were intact. When petals were
removed at dawn, the ambient temperature in Lantian, Hubei
Province, south China (298390 N, 1138070 E) was on average
7 8C higher than that in Mishan, Heilongjiang Province, northeast China (458320 N, 1318530 E). The average July temperatures in Lantian and Mishan were 29.3 8C and 20– 22 8C,
respectively (Wang and Zhang, 2005).
Lotus ovules expand after fertilization, so seed set was evaluated as the ratio of expanded seeds to the number of ovules.
Seed set among different treatments on lotus flowers was
compared by one-way ANOVA using SPSS, version 13.0.
R E S U LT S
Temperature variations in refrigerated and control flowers
During the daytime refrigeration period, the temperature in the
box interior fell immediately from about 30.1 to 19.2 8C when
the ice bags were put in, and then rose again gradually.
Another temperature decline occurred around noon from
about 26.2 to 23.1 8C when melting ice bags were replaced
with newly frozen ones, and then the temperature remained
at around 23.0 8C (Fig. 1). Correspondingly, the temperature
in unmanipulated control flowers during the daytime was relatively constant, increasing from 33.4 to 36.2 8C and then
Li & Huang — Thermoregulation in lotus flowers
Temperature (ºC)
35
30
25
20
Flower
Box interior
0600
0800
1000
1200
1400
1600
1800
Time (h)
F I G . 1. Temperature variation in the box interior and in a normal, intact lotus
flowers during daytime refrigeration.
dropping back to 33.4 8C (Fig. 1). During nocturnal refrigeration, the temperature first dropped immediately from 30.0 to
15.8 8C when the ice bags were put in, and then increased
gradually to 20.0 8C at the end of the night (Fig. 2). During
the same period, unmanipulated control flowers maintained a
stable temperature at around 32.0 8C (Fig. 2). Thus, our
refrigeration treatment greatly reduced flower temperature.
Effect of low temperature on seed production
1161
s.e. ¼ 0.85 + 0.03, n ¼ 13) or hand-pollinated without
pre-refrigeration (treatment 2; 0.89 + 0.01, n ¼ 15; F1,27 ¼
2.12, P ¼ 0.16), suggesting that stigma receptivity was not
influenced by low floral temperature. Seed set of flowers
pollinated with pollen treated with daytime refrigeration
(0.93 + 0.02, n ¼ 13) and nocturnal refrigeration (0.97 +
0.01, n ¼15) were not significantly different from those of
flowers pollinated with normal pollen (0.94 + 0.02, n ¼ 13;
F2,40 ¼ 1.81, P ¼ 0.18), indicating that low temperature in
either period before pollen shedding did not affect pollen
viability.
In two field populations, seed set of flowers from which
petals were removed was significantly lower than that of intact
flowers in the north-China population (t ¼ 2.60, P ¼ 0.01), but
this difference was not observed in the south-China population
(t ¼ 0.52, P ¼ 0.61; Fig. 3), suggesting that low ambient
temperature reduced female reproductive success in lotus.
The temperature manipulations in the experimental plants
indicated that daytime refrigeration immediately after pollination (treatment 3) significantly reduced seed set in lotus
flowers (F3,75 ¼ 497.94, P , 0.001), whereas there were no significant differences among flowers refrigerated during the night
(treatment 4), flowers with petals removed (treatment 5) and
control flowers (treatment 6; Fig. 4), indicating that low temperature significantly affected the fertilization process but not
the post-fertilization events.
DISCUSSION
The results demonstrate that the stable temperature maintained
in lotus flowers was an assurance for reproductive success
when ambient temperatures are unfavourably low. The
average air temperature on summer days is approx. 29.3 8C
Seed set was not significantly different between flowers that
were hand-pollinated after refrigeration (treatment 1; mean +
100
Petals removed
Intact
n = 15
a n = 19
a
35
80
Seed set (%)
A
Temperature (ºC)
30
25
n = 13
60
40
B
n = 28
20
20
Flower
Box interior
15
0
Mishan
Lantian
Population
1700 1900 2100 2300 0100 0300 0500 0700 0900
Time (h)
F I G . 2. Temperature variation in the box interior and in a normal, intact lotus
flower during nocturnal refrigeration.
F I G . 3. Comparison of seed set (means + s.e.) between lotus flowers with
petals removed and intact flowers, both of which were pollinated using fresh
pollen, at Mishan (north-east China) and Lantian (south China). The same
letter indicates no significant difference among treatments. The numbers of
flowers sampled in each treatment is indicated.
1162
Li & Huang — Thermoregulation in lotus flowers
n = 19 a
100
n = 23 a
n = 13 a
Seed set (%)
80
60
40
20
n = 21
b
0
Daytime
Nocturnal
refrigeration refrigeration
Petals Unmanipulated
removed
Treatment
F I G . 4. Seed set (means + s.e.) in lotus flowers subject to different treatments. The same letter indicates no significant difference among treatments.
The numbers of flowers sampled in each treatment is indicated.
in south China with a maximum reaching 39.3 8C, but the
average is lower in Mishan, north China, being only approx.
20 –22 8C (Wang and Zhang, 2005). Seed set was not significantly different between flowers with petals removed and
intact flowers in Wuhan and Lantian, Hubei Province, south
China, where the ambient temperature in summer is high,
but flowers with petals removed set fewer seeds than intact
flowers in the cooler region of north China, confirming that
low ambient temperature reduced reproductive success in
lotus flowers (Figs 3, 4). Kudo (1995) observed that the seed
set of flowers of Adonis ramosa with petals removed was significantly lower than that of intact individuals in north Japan,
indicating that elevation of temperature by heat absorption
increased reproductive success by increasing fertilization
success and seed development.
Compared to the post-fertilization process, the fertilization
process was susceptible to low temperature in lotus. Low
floral temperature during the fertilization period significantly
reduced the seed set but low temperature during the phase of
seed development did not, indicating that thermoregulation
in lotus flowers was essential for the fertilization process
rather than for the post-fertilization period (Fig. 4). Our experiments showed that low floral temperature did not affect stigma
receptivity in D-1 flowers or pollen viability in undehisced
anthers in the female phase. Therefore, the low seed set in
flowers refrigerated during the fertilization process might be
caused by the failure of some aspect of pollen performance,
such as pollen germination, pollen-tube growth or fertilization
in the pistils. The environment during stamen development has
been shown to influence subsequent pollen quality and pollen
performance in the recipient pistil in numerous plants
(Schlichting, 1986; Young and Stanton, 1990; Delph et al.,
1997; Aizen and Raffaele, 1998; Travers, 1999). The temperature in the environment of the stamens affected pollen quality
and performance in the snow buttercup Ranunculus adoneus,
where pollen from solar-tracking donor flowers exhibited a
32 % advantage in germination compared to that from stationary donor flowers (Galen and Stanton, 2003). The lack of any
obvious effect of flower temperature on pollen quality in our
study might be due to the short period of refrigeration or the
fact that it was applied only during the late stages of pollen
development. Given that the thermogenesis in lotus flowers
begins 1 – 2 d before anthesis (Seymour and Schultze-Motel,
1998), the effect on pollen quality and performance of the
resulting temperature elevation in the early stages of development needs further study. In adddition, we observed that anther
dehiscence was delayed for about 5 h at low floral temperatures
(see also Yates, 1993); thus, warming of the flowers may accelerate anther dehiscence in this aquatic plant.
Various functions have been proposed for floral thermogenesis: to protect flowers from freezing (Knutson, 1974); to
enhance the emission of floral scents to attract pollinators
(Fægri and van der Pijl, 1979; Meeuse and Raskin, 1988); to
provide a direct energy reward for insect pollinators
(Seymour and Schultze-Motel, 1997; Seymour et al., 2003);
or to enable beetles to reach flight temperature and depart
from the flower, carrying pollen away (Burquez et al., 1987).
The lotus flower has a typical beetle-pollination syndrome,
although diverse flower visitors including Coleoptera,
Hymenoptera and Diptera (Sohmer and Sefton, 1978;
Schneider and Buchanan, 1980) have been observed.
Thermoregulation has been interpreted as rewarding endothermic beetles in addition to accelerating scent emission in lotus
flowers (Schneider and Buchanan, 1980; Seymour and
Schultze-Motel, 1996). Stigma receptivity in lotus flowers
coincides with the peak of thermoregulation (Seymour and
Blaylock, 2000), and thus the temperature in the floral
chamber can greatly influence the post-pollination process,
when viable pollen has been transported onto the receptive
stigmas. We speculate that thermoregulation not only facilitates the arrival and departure of pollinators, increasing male
reproductive success, but also that elevated temperature in
female organs facilitates fertilization and seed development.
Although the optimal range of temperature for fertilization
success differs among species and cultivars of the same
species, for example 20– 25 8C in cherimoya (Rosell et al.,
1999), 15– 25 8C in mango (Sukhvibul et al., 2000) and
22– 26 8C in papaya (Cohen et al., 1989), unfavourable temperatures, far from the optimum, usually lead to the failure of
fertilization and to low seed set. Our experiments on handpollinated flowers showed that seed production was reduced
in both refrigeration-treated flowers and wild flowers experiencing low temperature. Thus, this study has shown that production of a favourable temperature could also be crucial for
post-pollination events in thermoregulatory plants.
ACK N OW L E DG E M E N T S
The authors thank Wei-Dong Ke from Wuhan Institute of
Vegetable Science, Hubei Province for his support during
the work, Qi-Chao Wang from the Lotus Society of China
for his encouragement and for suggesting this study,
Zuo-Dong Li, En-Xing Zhou, Dong-Xu Li and Xiao-Xin
Tang for their valuable help in the field, and Sarah Corbet
for helpful comments on the manuscript. Grants from the
National Science Foundation of China (no. 30825005) and
the Ministry of Education of China (no. NCET-04– 0668) to
SQH supported this work.
Li & Huang — Thermoregulation in lotus flowers
L I T E R AT U R E C I T E D
Aizen MA, Raffaele E. 1998. Flowering-shoot defoliation affects pollen grain
size and post-pollination pollen performance in Alstroemeria aurea.
Ecology 79: 2133–2142.
Borsch T, Barthlott W. 1994. Classification and distribution of the genus
Nelumbo Adans. (Nelumbonaceae). Beiträge zur Biologie der Pflanzen
68: 421 –450.
Burquez A, Sarukhan J K, Pedroza A. 1987. Floral biology of a primary rain
forest palm, Astrocaryum mexicanum Liebm. Botanical Journal of the
Linnean Society 94: 407–419.
Cohen E, Lavi U, Spiegel-Roy P. 1989. Papaya pollen viability and storage.
Scientia Horticulturae 40: 317 –324.
Corbet SA. 1990. Pollination and the weather. Israel Journal of Botany 39:
13–20.
Delph LF, Johannsson MH, Stephenson AG. 1997. How environmental
factors affect pollen performance: ecological and evolutionary perspectives. Ecology 78: 1632–1639.
Fægri K, van der Pijl L. 1979. The principles of pollination ecology, 3rd edn.
Oxford: Pergamon Press.
Galen C, Stanton ML. 2003. Sunny-side up: flower heliotropism as a source
of parental environmental effects on pollen quality and performance in
the snow buttercup, Ranunculus adoneus (Ranunculaceae). American
Journal of Botany 90: 724–729.
Gupta SC, Ahluwalia R. 1977. The carpel of Nelumbo nucifera.
Phytomorphology 27: 274– 281.
Hayes V, Schneider EL, Carlquist S. 2000. Floral development of Nelumbo
nucifera (Nelumbonaceae). International Journal of Plant Science
161(6 Suppl.): S183– S191.
Hedhly A, Hormaza JI, Herrero M. 2003. The effect of temperature on stigmatic receptivity in sweet cherry (Prunus avium L.). Plant, Cell &
Environment 26: 1673– 1680.
Hocking B, Sharplin CD. 1965. Flower basking by arctic insects. Nature 206:
215.
Kevan PG. 1975. Sun-tracking solar furnaces in high arctic flowers: significance for pollination and insects. Science 189: 723– 726.
Kjellberg B, Karlsson S, Kerstensson I. 1982. Effects of heliotropic movements of flowers of Dryas octopetala L. on gynoecium temperature and
seed development. Oecologia 54: 10– 13.
Knutson RM. 1974. Heat production and temperature regulation in eastern
skunk cabbage. Science 186: 746–747.
Kudo G. 1995. Ecological significance of flower heliotropism in the spring
ephemeral Adonis ramosa (Ranunculaceae). Oikos 72: 14– 20.
Lu S, Rieger M, Duemmel MJ. 1992. Flower orientation influences ovary
temperature during frost in peach. Agricultural and Forest Meteorology
60: 181 –191.
Meeuse BJD, Raskin I. 1988. Sexual reproduction in the arum lily family,
with emphasis on thermogenicity. Sexual Plant Reproduction 1: 3– 15.
Meinzer F, Goldstein G. 1985. Some consequences of leaf pubescence in the
Andean giant rosette plant Espeletia timotensis. Ecology 66: 512–520.
Miller GA. 1986. Pubescence, floral temperature and fecundity in species of
Puya (Bromeliaceae) in the Ecuadorian Andes. Oecologia 70: 155– 160.
Nagy KA, Odell DK, Seymour RS. 1972. Temperature regulation by the
inflorescence of Philodendron. Science 178: 1195–1197.
Ni XM. 1987. Chinese lotus. Beijing: Scientific Press.
Pigott CD, Huntley JP. 1981. Factors controlling the distribution of Tilia
cordata at the northern limits of its geographical range. III. Nature and
causes of seed sterility. New Phytologist 87: 817–839.
1163
Rosell P, Herrero M, Sauco VG. 1999. Pollen germination of cherimoya
(Annona cherimola Mill.). In vivo characterization and optimization of
in vitro germination. Scientia Horticulturae 81: 251–265.
Schlichting CD. 1986. Environmental stress reduces pollen quality in Phlox:
compounding the fitness deficit. In: Mulcahy DL, Mulcahy GB, Ottaviano
EM. eds. Biotechnology and ecology of pollen. New York:
Springer-Verlag, 483– 488.
Schneider EL, Buchanan JD. 1980. Morphological studies of the
Nymphaeaceae. XI. The floral biology of Nelumbo pentapetala.
American Journal of Botany 67: 182– 193.
Seymour RS, Blaylock AJ. 2000. Stigma peroxidase activity in association
with thermogenesis in Nelumbo nucifera. Aquatic Botany 67: 155– 159.
Seymour RS, Schultze-Motel P. 1996. Thermoregulating lotus flowers.
Nature 383: 305.
Seymour RS, Schultze-Motel P. 1997. Heat-producing flowers. Endeavour
21: 125– 129.
Seymour RS, Schultze-Motel P. 1998. Physiological temperature regulation
by flowers of the sacred lotus. Philosophical Transactions of the Royal
Society of London Series B 353: 935–943.
Seymour RS, Schultze-Motel P. 1999. Respiration, temperature regulation
and energetics of thermogenic inflorescences of the dragon lily
Dracunculus vulgaris (Araceae). Proceedings of the Royal Society of
London Series B 266: 1975– 1983.
Seymour RS, Schultze-Motel P, Lamprecht I. 1998. Heat production by
sacred lotus flowers depends on ambient temperature, not light cycle.
Journal of Experimental Botany 49: 1213– 1217.
Seymour RS, White CR, Gibernau M. 2003. Heat reward for insect pollinators. Nature 426: 243– 244.
Sohmer SH, Sefton DF. 1978. The reproductive biology of Nelumbo
pentapetala (Nelumbonaceae) on the Upper Mississippi River. II. The
insects associated with the transfer of pollen. Brittonia 30: 355 –364.
Stephenson AG, Lau TC, Quesada M, Winsor JA. 1992. Factors that affect
pollen performance. In: Wyatt R. ed. Ecology and evolution of plant
reproduction: new approaches. New York: Chapman and Hall, 119– 136.
Sukhvibul N, Whiley AW, Vithanage V, Smith MK, Doogan VJ,
Hetherington SE. 2000. Effect of temperature on pollen germination
and pollen tube growth of four cultivars of mango (Mangifera indica L.).
The Journal of Horticultural Science and Biotechnology 75: 64–68.
Travers SE. 1999. Pollen performance of plants in recently burned and
unburned environments. Ecology 80: 2427–2434.
Tsukaya H, Fujikawa K, Wu S. 2002. Thermal insulation and accumulation
of heat in the downy inflorescence of Saussurea medusa (Asteraceae) at
high elevation in Yunnan, China. Journal of Plant Research 115:
263–268.
Wang QC, Zhang XY. 2005. Lotus flower, cultivars in China. Beijing: China
Forestry Publishing House.
Yan SZ. 1986. The development of embryo and endosperm of Nelumbo
nucifera Gaertn. Acta Botanica Sinica 28: 355– 360.
Yates IE. 1993. Environmental regulation of anther dehiscence and pollen germination in Pecan. Journal of the American Society for Horticultural
Science 118: 699–706.
Young TP. 1984. Solar irradiation increases floral development rates in
afro-alpine Lobelia telekii. Biotropica 16: 243– 245.
Young HJ, Stanton ML. 1990. Influence of environmental quality on pollen
competitive ability in wild radish. Science 248: 1631–1633.