全 文 ：Pollination Biology of Ficus hispida in the Tropical
Rainforests of Xishuangbanna , China
YANG Da_Rong＊ , PENG Yan_Qiong , SONG Qi_Shi , ZHANG Guang_Ming ,
WANG Rui_Wu , ZHAO Ting_Zhou , WANG Qiu_Yan
(Kunming Section , Xishuangbanna Tropical Botanical Garden , The Chinese Academy of Sciences , Kunming 650223 , China)
Abstract:　Ficus hispida L.(Moraceae)is a remarkable species in the ecosystem of tropical rainforests in
Xishuangbanna , China.The figs and fig_pollination wasps(Chalcidoidae:Agaonidae)are highly co_evolved
mutualists that depend completely on each other for propagating descendants.Pollination of all fig species is
done by fig wasps;their unique symbiotic associates , the fig wasps , cannot develop in anywhere except in the
fig syconia.The present paper reports on the biology and flowering phenology of F .hispida , as well as the
propagation character and pollination behavior of the fig wasps(Ceratosolen solmsi marchali Mayr)based on
our observations in the rainforests of Xishuangbanna , southern Yunnan of China.F.hispida is a dioecious
tree that annually blossoms and bears fruits 6-8 times , with four to five fruit_bearing peaks.The male trees
produce pollen and provide fig wasps with reproductive havens , while the female trees produce fig seeds after
pollination by the female wasps.Pollen of F.hispida cannot escape from the dehiscent anthers until they are
disturbed by fig wasps.The female wasps open the anthers and collect pollen with their antennal scrapes ,
mandibles and legs , and then carry pollen to the female receptive syconia where fertilization takes place.
Meanwhile , some of the female wasps lay eggs in the male receptive syconia.It takes about 3-67 min to
search for the receptive syconia for pollination , and 15-23 h to enter the female receptive syconia.The num-
ber of female wasps entering a syconium has close relation with the impregnation and seed_bearing rate of fe-
male flowers , as well as the oviposition and reproduction rate of the fig wasps themselves.F .hispida is en-
dowed with a relatively high level of seed bearing(54.1%-82.5%, average 73.8 %).The wasp oviposition
rate on the male flowers is between 72.3% and 93.8%with a mean of 84.4%.
Key words:　Ficus hispida;Ceratosolen solmsi marchali;pollination biology;tropical rainforest;Xishuang-
banna
　　Xishuangbanna Nature Reserve is the largest among
the tropical rainforest reserves in China.Ficus is one of
the most colossal woody genera , either trees or shrubs , in
tropical rainforests , occupying the main space layer.Fig
individual has the highest fruit_bearing capability in the
plant kingdom , and the rich figs are present all year
round.Thus they can afford food and habitats for mam-
mals , birds , bats , insects , soil animals and microorgan-
isms.These kinds of habitats are also good for sapro-
phytes , epiphytes , parasitic plants and shade_enduring
plants.For this reason , many species of Ficus are inter-
nationally acknowledged to be a kind of keystone species
in the tropical rainforests[ 1-5] .They must be each polli-
nated by a special pollinatorwasp , the only way for Ficus
to propagate its offspring sexually.On the contrary , the
pollinator wasps depend on the ovaries of the short_styled
female flowers(which can grow into galls after the wasps
oviposit)to oviposit and foster their descendants.Both
are highly specialized and sophisticated[ 6-17] , being one
of the most remarkable examples of co_evolution.
Ficus hispida L.(1781)is a dioecious species ,
distributed in India , Nepal , Thailand , Laos , Malaysia
and in South China , including Yunnan , Guangdong ,
Guangxi , Hainan , Hongkong and Guizhou[ 18 ,19] .As a
pioneer species , it plays an important role in the proceed-
ings of restoration and renewal of tropical rainforests.The
tropical rainforests , after being devastated naturally or ar-
tificially , may turn into secondary forests or bare land.
The light_preferred and dry_enduring plants , such as F.
hispida and others , will emerge first during rehabilitating
succession.With the growth of F .hispida , a shady mi-
cro_environment forms , which enables the shade_enduring
and warm_preferred plants to grow vigorously.When other
plants grow and exceed F.hispida , the pioneer commu-
nity will start to fade away and be replaced gradually by
other plant communities , and the succession continues to
go forward to recover the tropical rainforests.Recently ,
Hill
[ 20 ,21]
reported on the primary biology and ecological
characteristics of F .hispida and its pollinator wasps in
Hongkong;Patel and Hossaert_McKey[ 22] worked on the
insect community around F .hispida and its reproductive
strategy in a deciduous forest;Song et al[ 23] studied the
volatile compounds from this fig tree and their attractive-
ness to fig wasps.In this paper , our attention will be
Received:2001-04-11　Accepted:2002-03-18
Supported by the National NaturalScience Foundation of China(30170171);the Chinese Academy of Sciences(KZ951_A1_104_01);the NaturalS cience Founda-
tion of Yunnan Province(98C093M;2000C0083M;2001C0065M).
＊ Author for correspondence.E_mail:.
植　物　学　报　　　　　　　　　　　　　　　　　　　　　　　　　　　　　　　　　　　　　　　　　　　　　　　　　　　
Acta Botanica Sinica　2002 , 44(5):519-526
concentrated on the pollination biology of F.hispida
found in the tropical seasonal rainforests of southern Yun-
nan , China.
1　Materials and Methods
1.1　Study sites
The study sites are in the Menglun town of Mengla
County in Xishuangbanna , SW China , where the mean
annual temperature is 21.4 ℃per year , the mean annual
precipitation 1 557.0 mm , and the average relative hu-
midity 86%.There is neither hot summer nor severe win-
ter , but the alternation of dry to humid season is distinct.
The dry season is from November to next May , while the
humid season from June to October with 75%yearly rain-
fall then.The study sites include:(1)tropical valley
rainforest at a nature reserve along Xiaola road 52-56 km
from Mengla County;(2)Green Stone Forest Reserve ,
roughly 1 km away from the eastern gate of Xishuangbanna
Tropical Botanical Garden , the Chinese Academy of Sci-
ences(CAS);(3)the meadow beside the power plant of
Xishuangbanna Tropical Botanical Garden , CAS and (4)
the fallow land of Menglun town.The general conditions
of the sampling sites are described in Table 1.
1.2　Plant and animal species studied
Plant species:Ficus hispida L.(1781), a common
tropical shrub or small tree of Moraceae.
Animal species:Ceratosolen solmsi marchali Mayr ,
belonging to Blastophaginae , Agaonidae , Chalcidoidea ,
Hymenoptera.
1.3　Methods
1.3.1　Sampling and marking method　Two female
and two male trees of F .hispida that are easily
observable were selected and marked in each sampling
site.At the fig_bearing stage , 60 syconia with similar
shape and size were randomly selected and the following
aspects were observed at 5 day_intervals for 2 years con-
secutively:the growth of the syconium;biological charac-
teristics of F .hispida and the behavior ecology of its pol-
linator wasps.In addition , the fig fecundity was counted
once every 15 days for mastering the numerical dynamics
of the annual syconium production.
1.3.2　Observation of the entrance and emergence of
the fig wasps　When the female florets of the young
syconium are in blossom , the ostile becomes loose.Ob-
servation was made hourly starting from 6:00 a.m.Once
a fig wasp was seen hovering around the receptive fig , the
observation did not stop until the foundress entered the
syconium and vanished.Fig wasp emerging process was
observed when male figs developed into the male flower
phase and fig wasps in the gall flowers began to hatch.
When the first male fig wasp was seen around the ostile ,
transparent organdy bags(100 sieves)were used to en-
close figs.Hatching behavior of fig wasps was investigat-
ed.Fig wasps emerged from fig syconia were collected ,
counted and identified hourly.
1.3.3　Anatomical observation　Altogether 60 syconia
with six developing phases were picked and studied at in-
tervals of five days.At early_floral phase , the syconium
was seen as the size of a soybean , when the florets in the
fig cavity were not visible.At pre_female floral phase
when the syconium had just developed for 3-5 days , the
miniature florets could be seen.At female floral phase ,
the female flowers inside the syconium were in
blossom and the fig wasps penetrated into the female
Table 1　General conditions of the sampling sites
Location Area(ha) Natural conditions Disturbance Main figs
Tropical Valley Rainforest
Nature Reserve (№1 sam-
pling site)
860 The nature reserve , 52 - 56 km from
Mengla , is divided by the road down from a
hill top into two parts.The sample site is on
the southwest slope , where the rainforest is
well_conserved with forest coverage ratio 90
-95%.Major woody plants are Pomet ia
tomentosa and Terminalia myriocarpa.
Slightly disturbed by people
and livestock
Ficus racemosa , F.auric-
ulata , F.altissima and F.
semicordata. F. hispida
found in gaps or open_spaces
in forests and on the defor-
ested land.
Lime stone forest at the
Green Stone Forest Reserve
(№2.sampling site)
60 In the east of Menglun town , 1 km or so
from the Botanical Garden.The forest cover-
age ratio is 85-95%.Major woody plants
are Celti wightii , Cleistanthus sumatranus
and Lasiococca comberi var.pseudoverti-
cella_ta.
Increasingly disturbed by
human beings in recent
years.
F.virens var.sublanceola-
ta , F.superba var.japon-
ica and F.orthoneura.F.
hispida only found along the
road sides.
Meadow beside the power
plant of the Botanical Gar-
den(№3.sampling site)
4.5 In the Botanic Garden , the narrowest part of
Hulu Island , around the power plant station ,
there are grasslands with some ornamental
and a few natural trees.
Rather seriously disturbed
by human.
F. hispida is dominant.
The strangler F.tinctoria
subsp.gibbosa can be seen
on the treesbeside the road.
Fallow land at Menglun
(№4.sampling site)
2.5 In the middle of the hi ll , northwestern of
Menglun town , which was once a part of the
Menglun Reserve in 1970 s , but then defor-
ested and deserted for 4-6 years.The for-
est coverage ratio is 25%.
Seriously disturbed by hu-
man.
F.hispida , F.tinctoria
subsp.gibbosa and F.re-
ligiosa.
520　 植物学报　Acta Botanica Sinica　Vol.44　No.5　2002
syconium for pollination and the male ones for oviposi-
tion.At the interfloral phase , after fertilization took place
in the female syconium , the fig embryos began to devel-
op;and in the male syconium the gall flowers were formed
after oviposition by the foundress wasps and the larvae ful-
ly developed.At the male floral phase , the flowers in the
male syconium were open and became mature , and then
eclosion occurred with wasp emergence.And at post_floral
phase , seeds inside the female syconium ripened , and
soon female and male syconia both fell.The figs were
brought to laboratory for dissection and observation under
the dissecting microscope of the development of female
flowers , gall flowers and fig wasps in different phases.
Ovipositing and pollinating behavior of the foundress
wasps was observed by dissecting the female floral phase
syconia with vigorous foundress wasps.The number of the
foundress wasps entering a syconium , including the
foundresses in the fig cavity and in the bracts , was count-
ed by dissecting the pre_interfloral phase syconia.Seeds ,
gall flowers and sterile flowers were investigated using
syconia at the end of interfloral phase.
2　Results and Analysis
2.1　Biological characteristics of the syconium of Fi-
cus hispida
The fruit_bearing phenology of F.hispida is charac-
terized by that the syconia can be produced all the four
seasons of a year on either female or male fig trees , and
the syconia at different developmental stages may appear
synchronously or alternately on a single plant.Most figs(80%-98%)grow on leafless branches , while a few
grow in the leaf axils.The young figs first appear on the
base of the leafless branches and then extend to the tops.
When the figs on the top of the branch become mature ,
another batch of small figs emerges from the branch base.
By our observations , each leafless branch bears figs for 7
or 8 times yearly.There are 4 or 5 fig_bearing peaks re-
spectively in December , March and May of dry season and
July and September of humid season.All the plants of F .
hispida may bear figs vigorously in favorable seasons ,
though there are trifling differences in fig_bearing peak
among the individuals.When the conditions become rig-
orous , they seem to be mutually complementary , bearing
figs alternately.In a small population of F .hispida ,
some trees reach the fig_bearing peak at the beginning of a
month , while the others bear at the same time few syconia
or even none.At the end of the month , however , the sit-
uation usually reverse(Figs.1 ,2).
F .hisppida commonly grows together , forming in
groups.The ratio of female trees to male ones within a
group is about 1∶1.There are usually 4 to 6 flowering
plants in an area of 90 000 square meters.Because the
temperature and humidity vary from spring to winter , the
life history of the syconia , from the early_floral phase to
the post_floral phase , may be of long or short duration.
For example , the growth period of a syconium lasts 25-
29 days inmiddle April to late July , while it lasts 45-71
days , in January and February.The annual average
growth period of a syconium is 36.5 days(Fig.3).
The amount of syconia in different months are shown
in Fig.3 , based on the observations of two male and two
female trees found in the center of a group.They all bear
figs throughout the year , each with 4 fig_bearing peaks.
In July when the temperature and humidity are appropri-
ate , and September in which humid days alternate with
dry days , both female and male trees have highly repro-
ductive capacity.But in winter and spring , when the cli-
mates are foggy_cool and dry_hot respectively , the fig_
bearing peaks of different individuals appear to be alter_
nate with each other , especially within the male trees.
Fig.1.　 Syconia at different stages of development on leafless
branches of female tree.
Fig.2.　Syconia in the leaf axils of female tree.
Fig.3.　Quantitative changes of syconia of Ficus hispida in a year.
YANG Da_Rong et al:Pollination Biology of Ficus hispida in the Tropical Rainforest of Xishuangbanna , China 521　
This seems to be beneficial to the continuity of the polli-
nator wasps , propagation and the maintenance of enough
pollinator wasps for female trees.On favorable condition ,
however , the female trees can bear figs abundantly and
are seldom seen having alternation of fig_bearing with each
other.
2.2　Emergence and courtship characteristics of fig
wasps
Fig wasps lay eggs in the ovaries of florets in male
syconia of F .hispida and these florets subsequently turn
into galls.When the larvae develop into imagoes just be-
fore hatch , the male flowers around the ostile begin to
ripen and then their anthers are open.Afterwards , the
adult wasps in the galls start to emerge.The emergence of
females and males is asynchronous and the males emerge
at first.The male wasps dig a round exit hole on the gall
wall for about 412min.As soon as the male wasps get out
of the gall , crawling on the surrounding gall flowers , they
probe acutely with antenna to search for the galls of fe-
males to copulate with.When a female gall is located ,
the male wasp cuts a hole on the gall wall and put its pe-
nis into it for measuring and then through the hole to cop-
ulate with the female inside , this lasting 15-46 seconds.
One male can mate with several females and each female
can mate with 2 or 3males usually.When most males dig
holes for mating , a few of them crawl onto the ostile to dig
exit hole on the fig wall.Occasionally , they dig exit hole
at other sites of the fig_wall.This process lasts 26-47
min generally.After digging the exit hole on the fig wall ,
the digger males then crawl out of the cavity.Some of the
other males can also get out along the same way.Because
the males are wingless and cannot fly , once out , they
drop down on the ground and become the prey of ants ,
spiders , carnivorous insects or other predators.But most
males die in the cavity.Approximately 1.5-2 h after the
emergence of males , females begin to emerge.They use
the mating holes dug by the males to get out , and then
comb their antennae , wings and abdomens occasionally
with their fore feet and hind feet.After stretching them-
selves , they crawl on the male flowers area and collect
pollen.
2.3　Pollen collecting behavior of the female wasps
When the male flowers of F.hispida matured , the
kidney_shaped anthers split open from the middle.The
male flowers are distributed inside the syconium , and the
pollen grains are sticky and most of them cannot drop off
automatically.The female wasps were required to collect
and push the pollen off.When the female wasps found out
the male flowers , they bit along the crack of the anthers
with their mouthparts , and collected pollen using the tarsi
of fore legs , middle legs and hind legs , as well as the
mouthparts.Firstly the tarsi scraped and brushed pollen
down and then put to alveoli in the pollen baskets of
breasts and legs.After pollen collection , the female
wasps returned to the torus of the galls and cleaned the
pollen adhering to the wings , heads , backs , abdomens ,
etc.Parts of the pollen grains were put into the wasps
mouths to make them humid , and then pushed into the
pollen baskets on the breasts.The remaining ones were
cleared off and fell on the wall of gall.The entire pollen_
collecting process lasted 32-76 min.Consequently , the
female wasps crawled out through the exit hole dug by the
male wasps.Most of these female wasps looked for the
male receptive syconia nearby to oviposit and propagate
their offspring.A few of them flied hundreds of meters to
search for the male receptive syconia for oviposition.And
some female wasps flied to the female trees and entered
the syconia , inside which they looked for the female f lo-
rets and then pollinated them (Fig.4).
2.4 　Numeral and emigration times of the female
wasps
The emergence and emigration of the fig wasps are
visible all year round except the cloudy_rainy and low_
temperature days in Xishuangbanna.They look for the fe-
male receptive syconia for pollination and search the male
receptive syconia for oviposition and propagation.Every
day there were two emergence peaks of large number of
female wasps getting out of the ripe figs of male trees after
pollen collecting.Most female wasps got out of the ripe
figs at the first emergence peak.However , with the alter-
ation of the seasons and the climates , the emigration time
varied(Fig.5).
In southern Yunnan , the low_temperature and foggy
days of the year are in the middle of dry season , from
December to next February.During this season the fog is
Fig.4.　Pollen_collecting foundresses emigrated from the gall of the
male syconia.
Fig.5.　The seasonal variations of the number and emergence time
of the female wasps(100 syconia counted).
522　 植物学报　Acta Botanica Sinica　Vol.44　No.5　2002
heavy and the temperature is low in the morning , when
the wasps of F.hispida not active.It was not until
11:00 when the dense fog gradually dispersed , the num-
ber of active wasps increased greatly , reaching the highest
peak at 12:30 , then began to decrease with the increase
of the temperature , and at last , a small peak appeared at
18:20 at dusk.From March to May , towards the end of
the dry season , when the temperature became higher fog
thinner , the wasps began to emerge at 6:00 , reaching the
first emergence peak at 9:00 and the second peak at
17:30.From June to August in the middle of the rainy
season , the emergence time is the earliest in the morning ,
when the number of the female wasps reached the first
peak at 6:50 , and then decreased;seven hours later the
amount began to increase , reaching a small peak at
19:20.This is the period in which the emergence of the
wasps was the greatest in number.From September to
November towards the end of the rainly season , the first
emergence peak appeared at 8:10 with rather great num-
ber of the wasps , and the second small peak appeared at
18:25.The investigation indicates that the emergence and
emigration of the female wasps of F.hispida may be
mainly influenced by the temperature.The emergence of
the wasps in the low_temperature season was rather late ,
while in the high temperature season was earlier.The ex-
periment shows that when the temperature is below 19 ℃,
the female wasps did not get out of the cavity of the fig ,
although the male wasp had already dug the exit hole.
The female wasps began flying when the temperature ex-
ceeds 21 ℃, but they stopped flying when the tempera-
ture goes above 39 ℃.
Because the fig wasps , living in the fig cavity almost
in their whole lifetime , are sensitive to light.Generally ,
the wasps are not active under strong sunlight.They are
prone to weak sunlight , so they get out of the fig cavity
mainly at dawn or at dusk except in winter and spring
when low_temperature and foggy days are dominant in
Xishuangbanna.Low_temperature and foggy days were not
convenient for the flight of fig wasps , so the emergence
time of the wasps was delayed obviously.The male wasps
could not dig the exit hole on the fig wall if their emer-
gence happened to be in windy and rainy days.In this
case the female wasps could get out of the fig.If the exit
hole on the fig wall had been dug , and the weather was
rainy or strongly windy , the female wasps would stay in
the fig cavity until the wind and rain stopped.In the dry
season , the fig wasps were active when the fog dispersed
and the dew disappeared.
2.5　Behavior characteristics of the female wasps in
entering the receptive figs
After getting out of the figs , the female wasps(foundresses)had a brief stopover at the mouth of the
hole , and then flied around to look for the receptive syco-
nia (figs).Our studies indicate that when the syconia
were at receptive stage , they emitted special volatile com-
pounds as chemical information for the wasps , which are
mainly linalool and α_terpeneol[ 21] . The chemical
information may guide the female wasps to find out the re-
ceptive syconia accurately.The fig wasps firstly hovered
around the receptive figs for 2-5 circles and then landed
on the surface of the figs;they crawled rapidly , mean-
while beating the fig wall with their antennae and fore legs
constantly , and then crawled slowly for 3 or 4 circles
around the ostile.After detecting the mouth of the outer
bracts for 2 or 3 min , the foundresses crawled into the
crevice at the mouth of the outer bracts.The head of the
foundress got into the ostile firstly by its fore legs and then
by middle legs and hind legs.The foundress entered the
cavity of the receptive fig finally by doing so.It took 8-
12 min to pass one bract.After that the foundress reached
the overlapping place of two bracts , and then turned its
fore legs and head and bent its body for entering the sec-
ond bract.Because all outer acrogenous bracts are over-
lapped , the movement passage of the foundress there
looked like a Z_shaped line.After passing 5-8 outer
bracts , the insect reached the joint of the inner and outer
bracts.In the space of the joint , the foundress trimmed
its wounded parts and wings with its legs and mouthparts ,
and then continued to crawl into the interior bracts.It
took 21-108 min (average =76.5 min)to get through
the overlapped bracts from outside to the cavity of the fig.
Although the foundresses were intact and robust before en-
tering the figs , most of them lost their wings , legs or an-
tennae when reached the cavity of the fig.Nearly 40%of
the foundresses that attempted to enter the receptive figs
were seen to be dead in the bracts , and a few died before
oviposition and pollination due to the entrapment of fig
juice.Only 58% of the foundresses that penetrated the
ostile could accomplish pollinating or ovipositing to repro-
duce descendants in the cavity.
2.6　Reproductive characteristics of the female wasps
After crawling out from the ripe natal fig , the
foundress(the female wasp)looked at first for the recep-
tive figs in the canopy of the host tree of F .hispida for
oviposition and propagation.If there were few receptive
figs or none on the host tree , the female fig wasps would
look for 3-5 min around the tree and then flied away to
another male tree to seek a new source of the receptive
fig.The oviposition time of the foundress in a syconium of
the male tree was about 6-9 h and one egg could only be
laid in one floret ovary.After the oviposition , the female
wasp died in the cavity.
The number of the foundresses entering the fig cavity
for oviposition varied from 1 to 9 , and 95% receptive figs
had 2 or 3 foundresses entered.When the receptive figs
were rare , 5-9 foundresses might enter one fig.When
the number of the foundress was large or the floret ovaries
were not sufficient , the foundresses often struggled to
share the reproductive resource.They might be hurt or
even died in the fighting , making their reproductive abili-
ties drop down(Table 2).
2.7　Pollinating behavior of the fig wasps
After getting inside the female receptive syconium
from the ostile , the female wasps were very excited and
active in the syconium cavity , though most of them had
been disabled.They crawled quickly on the stigmas of the
female flowers and put the ripe pollen they carried in the
YANG Da_Rong et al:Pollination Biology of Ficus hispida in the Tropical Rainforest of Xishuangbanna , China 523　
Table 2　The relation between the average number of galls and the number of the female wasps entering the male receptive syconia of Ficus
hispida in Xishuangbanna(Data from 1998-2000)
Month
Number of
syconia
counted
Number of
foundresses
per syconium
Number of
female
f lowers per
syconium
Empty f lowers
Number per
syconium
%
Galls
Number per
syconium
%
3-5
6-8
9-11
12-2
610
480
850
700
2.8
2.0
2.2
3.6
1 246.0
1 605.5
1 584.5
1 098.5
198.0
201.5
98.2
304.5
15.9
12.6
6.2
27.7
1 048.0
1 404.0
1 486.3
794.0
84.1
87.4
93.8
72.3
Mean 660 2.7 1 383.6 200.6 15.6 1 183.1 84.4
Table 3　The relations between the average number of seeds and the number of pollinating wasps in a female syconium of Ficus hispida in
Xishuangbanna(Data from 1998-2000)
Month
Number of
syconia
counted
Number of
foundresses
per syconium
Number of
female
f lowers per
syconium
Empty f lowers
Number per
syconium
%
Seeds
Number per
syconium
%
3-5
6-8
9-11
12-2
200
250
368
510
2.2
1.8
1.5
2.6
2 195.0
2 233.5
2 400.0
1 796.4
507.5
411.2
420.0
824.3
23.1
18.4
17.5
45.9
1 687.5
1 822.3
1 980.0
972.1
76.9
81.6
82.5
54.1
Mean 332.0 2.0 2 156.2 540.8 26.2 1 615.5 73.8
alveoli of the legs , breasts and heads onto the stigmas.
The pollination lasted 15-23 h.After the pollination ,
the female wasps(the foundresses)crawled slowly on the
stigmas of the florets till death.The corpses of the female
wasps might be digested 14-22 days later , with the de-
velopment of the syconium.When the syconium became
ripe , the entire corpses of the pollinator wasps were sel-
dom seen.
The number of the fig wasps entering one female
syconium was 1 or 2 generally , or up to 4 at most.When
one pollinator wasp entered one female syconium , the ra-
tio of seeds to total female florets was 51.3%.When two
or three wasps entered one female fig , the ratio might be
up to 86.5%, or nearly so.However , when the number
of the fig wasps entering the syconium was up to 4 or
more , the amount of seeds developed would decrease , on
the contrary , with the ratio of 40.2% to 63.8%.There-
fore , the optimum number of pollinator wasps for a female
syconium is two in the species F.hispida of Xishuang-
banna(Table 3).
As shown in Table 3 , the maximum quantities of the
female flowers and seeded ones after pollination were
found in the transition stage from humid to dry season(September-November)in Xishuangbanna , followed by
the rainy season , when the cloudy and rainy days hap-
pened rather frequent , it is not so convenient for the fig
wasps to fly and enter the syconium for pollination.In dry
and warm season (March -May , especially April and
May), the climate is rather hot and dry with temperature
alternating greatly.It is not good for the development of
the figs and fig wasps , and thus the amount of female
flowers and seeds was not so many as in the above two
seasons.In dry and cold season(December-February)
when the temperature is low and cold snap occurs occa-
sionally there , the amount of flowers and seeds in figs
dropped to the smallest.For example , in January and
February of 2000 , the cold current three times hit
Xishuangbanna area.When the mean temperature in rain-
forests was below 15 ℃, most of the fig wasps became
unable to fly and died on the ground in 2 or 3 min after
they get out of the ripe figs.As a result , the syconia
dropped off in great quantity from the late February to the
middle of March.
3　Discussion
Hill[ 20 ,21] and Kerdulhue[ 24] reported that more than
one species of wasps could enter the syconia of fig trees to
pollinate or propagate.However , according to our 5_year
observations in the rainforests of Xishuangbanna , only one
species , Ceratosolen solmsi marchali , of fig has been
seen entering the receptive syconium of Ficus hispida to
pollinate and reproduce.After the oviposition of the
foundress in the syconia of F.hispida , 3 or 4 other
species of wasps of Chalcidoidea were found laying their
eggs into the ovaries of fig flowers from the outside of the
syconia by penetrating the fig wall , and those species are
in fact the parasitoids of either pollinator wasps or ovaries
of fig florets.In the process of collecting the receptive
syconia at the female floral phase (being pollinated or
oviposited by the fig wasps)for volatile compounds ex-
traction , we dissected thousands of syconia and discovered
that there was only one species of the pollinator wasps
found in the syconia of F .hispida in Xishuangbanna.
The other species of wasps or insects are not pollinators
but parasitoids of the figs or the fig wasps(Fig.6).
There are mutually beneficial relations between F.
hipida and its pollinator wasps.The male trees of F.
hispida must afford their short_styled female flowers for
their fig wasps to oviposit;those flowers subsequently turn
524　 植物学报　Acta Botanica Sinica　Vol.44　No.5　2002
Fig.6.　Non_pollinating Chalcidoidea laying their eggs into the
ovaries from the outside of the figs by penetrating the fig wall.
into gall f lowers as the food and habitats of fig wasps.In
each life circle of the fig wasps , about 40% female wasps
that carry pollen will search for the female receptive syco-
nia of F.hispida for pollination.Those wasps cannot
leave the fig and die in the cavity after pollination.Nearly
60% female wasps will look for the male receptive syconia
to oviposit and reproduce.This appears to be a division of
labor among the female wasps , the characteristics of social
insects like the bees or ants , or a result of the selection of
the fig wasps copulating behavior.The inbreeding fe-
males and those with small abdomen and bearing few eggs
prefer pollinating , while the outbreeding females bearing
large number of eggs preside at propagating.It is obvious
that further studies are needed to explain this phenomenon
clearly and logically.As to the male fig wasps , their spe-
cial morphological characteristics indicate that they are
destined to death when the male syconia become mature
and fall off.The female and males wasps are clearly dif-
ferentiated in morphology as the results of long period co_
evolution between fig trees and their pollinators.The male
wasps maxilla and genitalia are well developed , but they
are unable to fly due to lacking wings and that their ocel-
li , compound eyes and legs have degenerated obviously.
Once leaving the fig , they will die or become the food of
predators.
Patel and Hossaert_Mckey[ 22] reported that in the de-
ciduous arboreal areas of eastern India the quantity of the
pollinating wasps in the female trees was larger than that
of the ovipositing and propagating wasps in the male
trees , from which our conclusion is quite different.Our
observations , by means of marking and trace inspecting on
the female wasps , indicate that the fig wasps may invest
firstly in their offspring propagation by instinct , and then
take care of the expansion of the host resource.Altogether
58%-67% female wasps reach the male trees to oviposit
and propagate , while only 33%-42% individuals fly to
the female trees to pollinate.Little known , however , was
the cause of these difference between eastern India and
southern China until recently.
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西双版纳热带雨林对叶榕传粉生物学
杨大荣＊　彭艳琼　宋启示　张光明　王瑞武　赵庭周　王秋艳
(中国科学院西双版纳热带植物园昆明分部 , 昆明 650223)
摘要:　研究了西双版纳热带雨林地区雌雄异株植物对叶榕(Ficus hispida L.)的生物学 、传粉物候学以及榕小蜂
(Ceratosolen solmsi marchali Mayr)的传粉和繁殖行为。研究结果表明:雌雄异株的对叶榕与其他雌雄同株的榕属植物
不同 ,它的种子形成与传粉者有着更为复杂的相互关系。对叶榕一年结隐花果 6～ 8 次 , 结果高峰期 4 ～ 5 次 ,其中
雄性植株仅产生花粉和孕育榕小蜂 , 而雌性植株(无雄蕊)则需榕小蜂带花粉进入隐花果内 ,进行传粉授精 , 使之发
育成种子。对叶榕的成熟花粉不能从花药开裂处自行散发出来 , 必须由榕小蜂采集才能散落。榕小蜂雌蜂羽化 、
交配后 ,找到雄花区 , 用足 、触角 、口器在推动中采集花粉。雌蜂飞出熟榕果找寻雌株或雄株榕树上的幼嫩隐花果 ,
一般需3 ～ 67 min;一部分雌蜂在雄株中寻找幼嫩的隐花果 ,进去产卵繁殖 , 另一部分雌蜂则寻找雌株雌花期嫩隐
花果进去传粉。雌蜂在雌株榕树的隐花果内传粉时间为 15～ 23 h , 在雄株榕树的隐花果内产卵时间为 6 ～ 9 h。对
叶榕小蜂在雌株上进入单个隐花果的数量多少关系到雌花结实率;观察表明 , 每个隐花果最佳进蜂数为 2 头;榕小
蜂传粉后榕树成熟种子形成率在 54.1%～ 82.5%之间 ,平均为 73.8%;而在雄株上雌蜂进蜂数量则关系到榕小蜂
在隐花果内的产卵率 ,每个隐花果最佳进蜂数为 3 ～ 4头 , 产卵率在 72.3%～ 93.8%之间 , 平均为 84.4%。
关键词:　叶榕;对叶榕小蜂;传粉生物学;热带雨林;西双版纳
中图分类号:Q944.43　　　文献标识码:A　　　文章编号:0577-7496(2002)05-0519-08
收稿日期:2001-04-11　接收日期:2002-03-18
基金项目:国家自然科学基金(30170171);中国科学院重大项目(KZ951_A1_104_01);云南省基金项目(98C093M , 2000C0083M ,
2001C0065M)。
＊通讯作者。E_mai l:.
(责任编辑:梁　燕)
526　 植物学报　Acta Botanica Sinica　Vol.44　No.5　2002