Botanical Studies (2006) 47: 435-441.

*

Corresponding author: E-mail: yehuagu@scbg.ac.cn; Tel:

86-20-37252779; Fax: 86-20-37252692; Dr. Hui YU:

Email: yuhui@scbg.ac.cn.

INTRODUCTION

Globally, there are over 750 species of Ficus (Mora-

ceae) (Berg, 2003). Figs are distinguished as a genus by

the syconium, a unique enclosed inflorescence which

also functions as a pseudocarp. Syconia are considered

to be key plant resources in tropical rainforests owing to

their heavy and continuous production, providing food

for a range of frugivores (especially birds) during periods

of fruit scarcity (Janzen, 1979; McKey, 1989). The pol-

lination of figs by highly specific wasps (Hymenoptera:

Agaonidae) is arguably the most widely known example

of obligate mutualism between plants and their pollinators

(Ramirez, 1970; Janzen, 1979; Herre, 1996; Machado et

al., 2001). Approximately half of all fig species are mon-

oecious. In these species each inflorescence bears male

flowers and female flowers with varying style lengths.

When pollen-loaded female wasps enter a syconium, they

pollinate the female flowers and oviposit in some of the

ovaries. Hence, monoecious figs produce a mixture of pol-

linators, seeds and pollen in every fruit. In dioecious fig

species, the syconium of functionally male trees bear male

flowers and modified female flowers with short styles for

wasp production, though some species also produce a few

viable seeds (Galil, 1973; Valdeyron and Lloyd, 1979;

Jousselin and Kjellberg, 2001). Dioecious figs also have

true female trees with syconia that do not have male flow-

ers and only very long-styled female flowers. The pollina-

tors cannot lay eggs in these flowers because the styles are

too long and thin for their ovipositors (Verkerke, 1987;

Weiblen, 2000), so only seeds are produced.

The major developmental phases of the syconia of

monoecious figs (Galil and Eisikowitch, 1968) can be ap-

plied, with appropriate modifications, to dioecious figs

(Patel, 1996; Yu et al., 2003). An immature syconium (A-

phase) develops to the receptive phase (B-phase) when it

is entered by the first female wasp. During the developing

phase (C-phase), each wasp larva feeds on the contents

of a single ovary in male trees, and seeds develop in fe-

male trees. During the brief wasp-releasing phase (D-

phase) in male trees, mature wasp offspring mate within

the syconium and then the female pollen-bearing wasps

leave the natal syconium to search for another receptive

syconium. After the departure of the wasps, the syconia

fall to the ground and rot. Female syconia, which do not

have wasps, bypass the D-phase and develop further to the

mature phase (E-phase). These mature syconia become

soft and fleshy, and are attractive to seed dispersers such

as birds.

ECOLOGY

Phenology and reproductive strategy of a common fig in

Guangzhou

Hui YU, Nan-Xian ZHAO, Yi-Zhu CHEN, Yuan DENG, Jin-Yan YAO, and Hua-Gu YE*

South China Botanical Garden, the Chinese Academy of Sciences, Guangzhou 510650, P.R. China

(Received December 6, 2005; Accepted April 14, 2006)

ABSTRACTS.

Ficus spp. (Moraceae) and their pollinator wasps (Chalcidoidae: Agaonidae) have co-evolved

a highly mutualistic relationship, and depend completely on each other for

reproductive success. Here, we

present data on syconia, seed and pollinator production of the dioecious fig Ficus hirta Vahly, which were

gathered to investigate the phenology and sexual specialization

of individual trees. Syconia were produced

asynchronously within trees, and there were sufficient degrees of both synchrony and asynchrony among

trees to maintain pollinator production

throughout the year. Production of receptive syconia and mature male

syconia peaked at the same time to facilitate both pollination and pollinator production. The duration of crop

development in female trees was longer than that in male trees, and the mean interval between syconia pro-

duction was also longer in female trees. The mean diameter and total number of female syconia in receptive

and ripe phase were lower, but the proportion of female flowers utilized in them was higher than that in male

syconia. Syconium production was not correlated with the height of either female or male trees. The num-

ber of syconia produced was significantly correlated with the amount of branches on female trees but not on

males.

Keywords: Dioecy; Ficus hirta; Fig wasps; Mutualism; Sexual specialization.

436

Botanical Studies, Vol. 47, 2006

Adult female wasps have extremely short life spans and

most live less than a day (Kjellberg et al., 1988; Harrison

et al., 2000). If they are to reproduce, the availability of

receptive syconia within their dispersal range is therefore

vital. In order to maintain a sufficiently large wasp popula-

tion to ensure pollination, both monoecious and dioecious

figs must provide a continuous source of receptive syconia

for emerging wasps

(Frank, 1989; Harrison et al., 2000).

It is therefore necessary for syconia in B-and D-phases

to overlap, either on the same or on different trees within

wasp dispersal range. However, in dioecious figs the two

sexes specialize in either seed or wasp production, so the

situation may be more complex. For example, the D-phase

syconia have to coincide temporally with B-phase syco-

nia not only in the female trees but also in the male. The

separation of female and male functions between different

trees could have led to adaptive changes in some char-

acters of the figs that facilitate pollination and pollinator

dispersal, which may have resulted in a greater array of

phenological patterns.

Studies of phenology in fig plants, such as the time of

flowering and fruiting in relation to abiotic factors (e.g.

habitat or climatic variables) and biotic factors (e.g. the

availability of pollinators, and the impact of herbivores

and seed predators) are useful in furthering our under-

standing of the reproductive basis of the mutualism (van

Schaik et al., 1993; Harrison et al., 2000).

Because pol-

linating wasps have such short lifespans the influence of

climatic fluctuations and biotic interactions on figs can

only be examined over a relatively brief period. Although

much attention has been paid to the phenology of monoe-

cious figs

(Hill, 1967; Galil, 1973; Milton et al., 1982;

Corlett, 1987; Bronstein and McKey, 1989; Herre, 1989;

1993; Weiblen et al., 1995; Patel, 1996; Spencer et al.,

1996; Patel and McKey, 1998; 2000; Harrison et al., 2000;

Yang et al., 2002; Wang et al., 2005), studies of dioecious

figs are few with most being concentrated in the tropics

(Galil, 1973; Corlett, 1987; 1993; Weiblen et al., 1995;

Patel, 1996; Spencer et al., 1996; Patel and McKey, 1998;

2000; Harrison et al., 2000; Yang et al., 2002).

There are two main phenological types at the level of

the individual fig tree: 1) synchronous and 2) asynchro-

nous. The former can be characterized by synchronous

receptivity within both male and female trees, and low

temporal overlap between the sexes. The latter can be

characterized by asynchronous receptivity of both male

and female trees, and moderate to high temporal over-

lap between sexes. In the subtropics, climates are more

seasonal and this provides a good opportunity to study

the phenological traits of fig trees (Berg, 2003). This is

especially so for dioecious species, whose more complex

reproductive systems are considered to have evolved as an

adaptation to seasonality by some scholars (Kjellberg et

al., 1987; Beck and Lord, 1988; Patel and McKey, 1998;

Weiblen, 2000; Machado et al., 2001).

The purpose of this paper is to report on a field inves-

tigation into sexual specialization and the influence of

temperature on the flowering, seed and pollinator produc-

tion of a common fig species, Ficus hirta, in Guangzhou,

southern China. Our study consisted of four questions:

1) what are the individual-level phenological traits of F.

hirta. 2) how does the production of syconia, seeds and

pollinators vary during the study phase. 3) what sexual

specialization is evident in F. hirta; 4) does temperature

affect the production of syconia, seeds and pollinators.

MATERIALS AND METHODS

Study site and species

Our study was conducted at the South China Botanical

Garden (SCBG, 23¢X11¡¦ N, 113¢X11¡¦ E, elevation 20-327

m) in Guangzhou, southern China. The mean annual tem-

perature is 21.8¢XC. Temperature data for SCBG from July

2002 to July 2003 (Figure 1) were obtained from a climate

station which is 2 km from the study site.

Ficus hirta is a

shrub that grows to the height of approximately 3 m and

is pollinated by Blastophaga (B.) javana Mayr. Three spe-

cies of non-pollinating wasp have been reported in F. hirta

(Mayr, 1885; Nair et al., 1981), but in SCBG there are

mainly two non-pollinating wasps, Philotrypesis josephi

and Sycoscapter hirticola (identified by Prof. Jean-Yves

Rasplus and Dr. Zhen Wen-Quan).

Field observations

Phenology censuses of nine male trees and five female

trees were conducted every 5-14 days from July 2002

to July 2003 (2-4 times per month). The crops were

determined to begin just as a single syconium appeared

and to end as all the syconia in an individual disappeared.

At each census the number and diameter of syconia in

each individual were recorded, and their development was

also followed. The diameters were measured at the equator

to the nearest 0.1 mm with vernier calipers. The height of

each tree and number of its branches were also recorded.

To investigate the development of syconia, especially

Figure 1. Annual variation of temperature (¢XC) obtained from

the climate station where is 2 km from South China Botanical

Garden (SCBG), South of China. (

¡µ

) Represents monthly mean

temperature.

YU et al. ¡X Phenology and reproductive strategy of a common fig in Guangzhou

437

B- and D-phases, syconia on individuals near the sample

trees were dissected and their positions on the tree were

noted in September in 2003.

The number of seeds and pollinators per syconium

provide indicators of female and male function, and may

be affected by the temperature. Between July 2002 and

June 2003, 10-20 C-phase female and D-phase syconia

were collected randomly from SCBG in each month. The

key syconia parameters, such as the number of flowers,

seeds and pollinators were counted under a dissecting

microscope (SE-CTV, Olympus, Japan).

Data analysis

Total syconia production was calculated for individuals

over the entire study period. Number of syconia produced

in each individual was classified by plotting log-trans-

formed frequency distributions in classes of 1-10, 11-20,

21-30 and >30. Mean durations of crops at individual and

population-level were calculated. Mean durations of inter-

crop interval at individual and population-level were also

calculated. Monthly mean number syconia initiated, B-

phase syconia, D-phase syconia, seeds and pollinators

in syconia were calculated from all the censuses of this

month. Mean diameters of syconia at each developmental

stage were calculated from all the censuses. Frequency

distributions of diameters were plotted in 5.5 mm intervals

(0-5.4 mm, 5.5-10.4 mm, 10.5-15.4 mm, 15.5-20.4 mm

and 20.5-25.4 mm).

All tests were carried out at P . 0.05 significance level

using SPSS (version 11.0). The differences in syconia ini-

tiation, production of B- and D-phase syconia, production

of pollinators and seeds were tested by One-way ANOVA

among different months in our study period. Means of the

significant ANOVA effects were compared using Tukey

post hoc comparisons. Differences in mean duration of

crops, mean duration of inter-crop interval (bearing no

syconia), and the mean height of male and female trees

were tested by Student¡¦s t-test. Correlation analysis was

performed for temperature versus syconia initiation, B-

and D- phase syconia production, seeds and pollinators

production; female versus male syconia initiation and

B-phase syconia production; D-phase versus B-phase sy-

conia production; pollinator production versus short-styled

female flowers; and height and branches versus syconia

production.

RESULTS

Reproductive phenology

Syconia at different developmental stages appeared

both synchronously and asynchronously on a single plant

and between sample trees. They were produced in all

seasons of the year. At each census, most syconia were in

A- or C-phase. The duration of these phases was longer

than the others phases, but there were wide variations in

the development of syconia. Occurrence of both B- and

D-phase syconia on the same tree was common (Table 1).

The numbers of syconia found on a single plant generally

ranged from several to 30, and never exceeded 100 (Figure

2). Female trees were devoid of syconia for 26.2% of the

time, on average, whereas for male trees for only 5.6% of

the time and two male trees bore more than five syconia

every time they were observed.

Figure 2. Reproductive phenology of 5 female and 9 male

individuals of Ficus hirta in SCBG, South of China. Each bar

represents a period in which syconia were present on the plant.

(¡X1-10; .11-12;

.

21-30;

.

>30) Four bar thic kne ss es

represent number of syconia in individual in our study period.

Table 1. Syconia developments of Ficus hirta in South China Botanical Garden (SCBG), Guangzhou, South of China observed in

Sept. 2003. A, B, C, D and E represent syconia in the A-, B-, C-, D- and E-phases, respectively; n represent number of individuals

sampled in SCBG.

Types of syconium developments in individuals in SCBG

Female (n=15)

Male (n=17)

Type of syconia developments in individual A AB ABC ABCE AC ACE A ABC ABCD AC ACE C

% Of individuals of the type in total

individual observed

6.7 6.7 6.7 6.7 40 33.3

11.8 17.6 47.1 5.9 11.8 5.9

438

Botanical Studies, Vol. 47, 2006

Production of syconia, seeds and pollinators

There were significant differences in syconia initiation

among different months in both sexes (Figure 3; P<0.01).

The female trees initiated more syconia in May, and

male trees in February and May. Annual variations in the

number of B- and D-phase syconia are shown in Figure 4

and have significant differences (P<0.01) among different

months except D-phase syconia (P>0.05). They were

generally low reflecting the normally short duration of

these two phases. However, they present a large degree

of overlap that could maintain continuous productions

of seeds and pollinators. Productions of three types of

syconia in May-June were all significantly different from

that in most of the other months (P<0.05), indicating that

all three types of syconia were peaking in this period.

Moreover, they were significantly correlated with each

other in this period (P<0.01).

Significant differences are in annual production of

pollinators and seeds (P<0.01). Pollinator production

was significantly higher in May (P<0.05) and has no

correlation with number of short-styled female flowers

(P>0.05). Seed production was significantly higher in

January and June (P<0.05), and correlated with pollinator

production in June (P<0.01).

Sexual specialization

Male trees were significantly taller than females. The

height of the individuals had no correlation to syconia

production, but the number of branches was significantly

correlated with female syconia production (P<0.05). The

mean duration of crops on male trees was shorter than that

of on the females (P<0.05). The mean duration of the time

between crops was shorter for male trees compared to the

females (P<0.05). The mean diameter and total number

of syconia in B- and D-phase were both higher on male

trees than those in B- and E-phase syconia on female trees

(Table 2).

In male syconia, the mean number of female flowers

utilized by pollinators was 21¡Ó9%, and the mean number

Figure 4. Annual variations of syconia in B- and D-phase in

didividual in SCBG, South of China. („T) Represents monthly

mean production of female syconia in B-phase (5.5-10.4 mm);

(

.

) Repres ents monthly mean production of male syconia

in B-phase (10.5-15.4 mm); („I ) Repres ents monthly mean

production of male syconia in D-phase (15.5-20.4 mm).

Figure 3. Annual variations of initiated syconia in individual

in S CBG, South of China. („T ) Represents monthly me an

production of female syconia initiation; (

.

) Represents monthly

mean production of male syconia initiation.

utilized by symbiotic wasps (including pollinators and

non-pollinating wasps) was 37¡Ó7%, indicating that less

than half of the short-styled female flowers were used by

symbiotic wasps. In female syconia, the mean number of

pollinated female flowers was 50¡Ó13%, nearly half of the

total. So the number of female flowers utilized in female

syconia was 30% higher than that in males. In D-phase

syconia a few seeds could be found, whereas in E-phase

syconia offspring of pollinators were never found.

The effects of temperature on the production of

syconia, seeds and pollinators

Correlations between temperature and production of

syconia, seeds and pollinators were only significant in

some months. Temperature was not correlated with female

syconium initiation (P>0.05), but was correlated with

male syconium initiation in

August and January (P<0.05),

which were the hottest and coldest months, respectively.

Temperature was correlated with production of female

B-phase syconia in March and December (P<0.01), with

male B-phase syconia in July and August (P<0.05), and

with male D-phase syconia in August (P<0.05). Pollinator

production has no correlation with temperature, but seed

production was correlated with increase in temperature

in January (P<0.05). Of course these results are only

preliminary, more accurate conclusions on temperature

effect warrant further examination, and more data should

be included.

DISCUSSION

Reproductive strategy

Female pollinators of F. hirta can survive in the

laboratory for 24-48 hours at most (personal observation),

so it is essential for them to find receptive syconia as soon

YU et al. ¡X Phenology and reproductive strategy of a common fig in Guangzhou

439

as possible. Within the sampled trees, the combination of

inter-tree asynchrony and varying degrees of intra-tree

synchrony and asynchrony resulted in a broad overlap

between D- and B-phase syconia, allowing pollinators

to potentially find receptive syconia relatively easily.

In addition, B-phase syconia in both sexes and D-phase

syconia all peaked at same time and were significantly

correlated with each other which may facilitate both

pollination and pollinator production. Thus, asynchrony

between and within trees seems to optimize the chance for

pollinators to find a receptive tree.

When male and female trees are receptive

simultaneously, there should theoretically be strong

selection for pollinators to avoid female syconia, in which

they have zero fitness, and to enter only male syconia,

in which they can reproduce (Patel, 1996). However, in

contrast to this expectation, both seeds and pollinators

were produced simultaneously. It is essential for

pollinators to find receptive syconia quickly due to their

short life-spans and high mortality rates, so the most likely

reason is that pollinators may simply try to enter the first

receptive syconium they meet (Patel et al., 1995; Moore et

al., 2003), though other causes, such as pollinators cannot

discriminate between male and female trees (Grafen and

Godfray, 1991) or syconia could emit volatile chemicals

that attract their specific wasps (Hossaert-McKey et al.,

1994; Ware and Compton, 1994), maybe existed too.

Sexual specialization

In this study, considerable sexual specialization was

found. The crop development period for female trees

was significantly longer than the corresponding period

for male trees, as found for other dioecious figs (Hill,

1967; Corlett, 1987; 1993; Patel and McKey, 1998; 2000;

Harrison et al., 2000). Mean duration of inter-crop interval

was significantly longer in female trees than that in male

trees. This shows that the degree of synchrony was highest

among female trees.

I n F. hirta, more syconia were

produced in male trees than in female trees, but mean

production of pollinators was lower than that of seeds in a

single syconium.

Male syconia were larger than female syconia. In

female syconia, flowers have longer styles, but the lengths

of flowers are much shorter than the radius of syconium

cavity (personal observation), so the smaller diameter of

female syconia could not affect the action of pollinator in

them. The proportions of female flowers utilized for seed

production and pollinator production in individual syconia

could be 97.7% and 85.9% at most, respectively, but the

average proportion of female flowers utilized in both sexes

were much lower than them (50¡Ó13% in female syconia

and 21¡Ó9% in male syconia) which maybe limited by

resource limitation or dispersal selection.

Phenological characters of F. hirta at other sites

Although few details have been published about the

syconia and flowering phenology of F. hirta, in Hong

Kong (Hill, 1967) they appear to be similar to those trees

in our study. This may reflect the climatic similarities

between the two regions. Li et al. (2003), however,

found in a study of F. hirta in the more seasonal Chinese

province of Fujan, that syconia were more synchronous

among trees. Li and colleagues also found that crops of

female and male trees were initiated alternately, with one

population-level crop per year in female trees and two in

males. Other studies of dioecious fig phenology have also

found that crops tend to be smaller, with a greater degree

of population synchrony in more seasonal environments

Table 2. Sexual specialization of Ficus hirta in South China Botanical Garden (SCBG), Guangzhou, South of China*.

Sex

Mean duration of

bearing no syconia

(days)

Mean duration of

crops (days)

Mean diameter of syconia in

different phases (mm) Total syconia initiated in

individual (13 months)

B-phase D-phase E-phase

Female (n=5)

95.5¡Ó85.9

61¡Ó21.4

8.5¡Ó2.2

13.2¡Ó2.6

60.6¡Ó42.8

Male (n=9)

20.3¡Ó23.2

49.3¡Ó15.9

12.1¡Ó1.9 17.1¡Ó2.8

81.6¡Ó17.5

Total syconia of selection

Mean % of seeds, pollinator wasps and all symbiltic wasps in female flowers in syconia

(female: n=112; male=105)

Seed

Pollinator wasp

All symbiotic wasp

50¡Ó13

21¡Ó9

37¡Ó7

Height of the sampled individuals (cm)

Number of branches in individual

The first measurement The last measurement Range of increasing Range

Mean

Female (n=5)

133.8¡Ó75

166.6¡Ó76

32.8¡Ó9.5

1-6

2.6¡Ó2.3

Male (n=9)

173.8¡Ó48.1

222.3¡Ó52.6

48.6¡Ó23.1

0-6

2.6¡Ó1.8

*Data presented as mean ¡Ó SD.

440

Botanical Studies, Vol. 47, 2006

(Valdeyron and Lloyd, 1979; Corlett, 1987; Patel, 1996).

Whether or not these findings apply to all dioecious figs

warrant further examination.

Acknowlegements. The authors are most grateful to Prof.

Rasplus Jean-Yves and Dr. Zhen Wen-quan for identifying

the symbiotic wasps of Ficus hirta and Miss Liu Yun-xiao

for helping to prepare the figures. We thank Dr. Shen Hao

and Dr. Zhang Yun for helping with data analyses. We

also wish to thank Dr. Derek Dunn and two referees for

good suggestions and help in improving the English. The

study was supported by the Chinese Academy of Sciences

(KSCX2-SW-105), National Natural Science Foundation

of China (30600078), and International Foundation for

Science (D/3830-1).

LITERATURE CITED

Beck, N.G. and E.M. Lord. 1988. Breeding system in Ficus

carica, the common fig. I. Floral diversity. Ame. J. Bot. 75

(12): 1904-1912.

Berg, C.C. 2003. Flora Malesiana precursor for the treatment of

Moraceae 1: the main subdivision of Ficus: the subgenera.

Blumea 48: 167-178.

Bro ns tei n, J .L. a nd D. Mc Key. 1 989. Th e fig /pol lin ato r

mut ualis m: a model sys tem for c ompara tive biol ogy.

Experientia 45: 601-611.

Corlett, T.R. 1987. The phenology of Ficus fistulosa i n

Singapore. Biotropica 19: 122-124.

Corlett, T.R. 1993. S exual dimorphis m in the reproductive

phenology of Ficus grossularioides Burm. f. in Singapore.

Malayan Nature J. 46: 149-155.

Frank, S.A. 1989. Ecological and evolutionary dynamics of fig

communities. Experientia 45: 674-680.

Galil, J. and D. Eisikowitch. 1968. On the pollination ecology of

Ficus sycomorus in East Africa. Ecology 49: 259-269.

Galil, J. 1973. Pollination in dioecious figs: pollination of Ficus

fistulosa by Ceratosolen bewitti. Gardens Bull. Singapore

26: 303-311.

Grafen, A. and H.C.J. Godfray. 1991. Vicarious selection ex-

plains some paradoxes in dioecious fig-pollinator systems.

Proc. R. Soc. Lond. Ser. B 245: 73-76.

Harrison, R.D., N.Yamamura, and T. Inoue. 2000. Phenology of

a common roadside fig in Sarawak. Ecol. Res. 15: 47-61.

Herre, E.A. 1989. Coevolution of reproductive characteristics

in 12 species of New World figs and their pollinator wasps.

Experientia 45: 637-647.

Herre, E.A. 1996. An overview of studies on a community of

Panamanian figs. J. Biogeogr. 23: 593-607.

Hill, H.D. 1967. F igs of Hong Kong. Hong Kong University

Press, Hong Kong.

Hos sa ert-Mc Key, M., M. Giberna u, and J .E. F rey. 19 94.

Che mos ens ory a ttra ct ion of fig wa sp s t o sub st ance s

produced by receptive figs. Entomologia Experimentalis et

Appl. 70: 185-191.

Janzen, D.H. 1979. How to be a fig. Ann. Rev. Eco. Syst. 10:

13-51.

Jousselin, E. and F. Kjellberg. 2001. The functional implications

of active and passive pollination in dioecious figs. Ecol.

Lett. 4: 151-158.

Kjellberg, F., P.H. Gouyon, M. Ibrahim, M. Raymond, and G.

Valdeyron. 1987. The stability of the symbiosis between

dioecious figs and their pollinators: a study of Ficus carica

L. and Blastophaga psenes L. Evolution 41: 693-704.

Kj el lbe rg, F., B. Dou me sc he , and J.L . Bro ns tei n. 198 8.

Longe vity of a fig was p (B las tophaga psene s). P roc.

Koninklijke Nederlandse Akademie Van Wetenschappen

Ser. C Biol. Med. Sci. 91: 117-122.

Li, H.Q., Y. Chen, X.A. Lu, and W.L. Ma. 2003. The mutualism

and reproductive countermeasure between Ficus hirta and

its pollinator. In the Botanical Society of China (eds.), Re-

ports and Abstracts Presented at the 70

th

Anniversary of the

Botanical Society of China, Beijing, pp. 172-173.

Machado, C.A., E. Jousselin, F. Kjellberg, S.G. Compton, and

E.A. Herre. 2001. Phylogenetic relationships, historical bio-

geography and character evolution in fig-pollinating wasps.

Proc. Roy. Soc. Lond. Ser. B 268: 685-694.

Mayr, G. 1885. Figinsecten. Verhandlungen der Zoologisch-

Botanischen Gesellschaft in Wien 35: 147-250.

McKey, D. 1989. Population biology of figs: application for

conservation. Experientia 45: 661-673.

Milton, K., D.M. Windsor, D.W. Morrison, and M. Estribi. 1982.

Fruiting phenologies of two neotropical Ficus species.

Ecology 63: 752-762.

Moore, J.C., M.J. Hatcher, A.M. Dunn, and S .G. Compton.

2003. F ig choice by the pollinator of a gynodioec ious

fig: selection to rush, or intersexual mimicry. Oikos 101:

180-186.

Nair, P.B., U.C. Abdurahiman, and M. Joseph. 1981. Two new

Torymidae (Hymenoptera: Chalcidoidea) from Ficus hirta.

Oriental Insects 15(4): 433-442.

P atel, A. 1996. Variation in a mutualism: phenology and the

maintenance of gynodioecy in two Indian fig species. J.

Ecol. 84: 667-680.

Patel, A., M-C. Anstett, M. Hossaert-McKey, and F. Kjellberg.

1995. Pollinators entering female dioecious figs: why com-

mit suicide. J. Evol. Biol. 8: 301-313.

P atel, A. 1996. Variation in a mutualism: phenology and the

maintenance of gynodioecy in two Indian fig species. J.

Ecol. 84: 667-680.

P atel, A. and D. McKey. 1998. Sexual specialization in two

tropical dioecious figs. Oecologia 115: 391-400.

P atel, A. and D. McKey. 2000. Components of reproductive

success in two dioecious fig species, Ficus exasperate and

Ficus hispida. Ecology 81: 2850-2866.

Ramirez, B.W. 1970. Host specificity of fig wasps (Agaonidae).

Evolution 24: 680-691.

YU et al. ¡X Phenology and reproductive strategy of a common fig in Guangzhou

441

Spencer, H., G. Weiblen, and B. Flick. 1996. Phenology of Ficus

variegiata in a seasonal wet tropical forest at Cape Tribula-

tion, Australia. J. Biogeogr. 23: 467-475.

Valdeyronm, G. and D.G. Lloyd. 1979. Sex differences and

flowering phenology in the common fig, Ficus carica L.

Evolution 33(2): 673-685.

Van Schaik, C.P., J.W. Terborgh, and S .J. Wright. 1993. The

phenology of tropical forests: adaptive significance and

consequences for primary consumers. Ann. Rev. Ecol. Syst.

24: 353-377.

Verkerke, W. 1987. Syconial anatomy of Ficus asper ifolia

(Moraceae) a gynodioecious tropical fig. Proc. Koninklijke

Nederlandse Akademie Van Wetenschappen C 90: 461-492.

Wang, R.W., J.X. Yang, and D.R. Yang. 2005. Seasonal changes

in the trade-off among fig-supported wasps and viable seeds

in figs and their evolutionary implications. J. Integ. Plant

Biol. (Formerly Acta Bot. Sin.) 47(2): 144-152.

Ware, A.B. and S.G. Compton. 1994. Dispersal of adult female

fig wasps: 2. movements between trees. Entomologia Ex-

perimentalis et Appl. 73: 207-216.

Weiblen, G.D., B. Flick, and H. S pencer. 1995. Seed set and

wasp production in dioecious Ficus variegata from an Aus-

tralian wet tropical forest. Biotropica 27: 391-394.

Weiblen, G.D. 2000. Phylogenetic relationships of functionally

dioecious Ficus (Moraceae) based on ribosomal DNA se-

quences and morphology. Ame. J. Bot. 87: 1342-135.

Yang, D.R., Y.Q. Peng, Q.S. Song, and G.M. Zhang. 2002. Pol-

lination biology of Ficus hispida in the tropical rainforests

of Xishuangbanna, China. Acta Bot. Sin. 44: 519-526.

Yu, H., N.X. Zhao, Y.Z. Chen, and X.Y. Hu. 2003. A study of

symbioses between Ficus hirta and Blastophaga javana.

Guihaia 23: 573-576.