Botanical Studies (2006) 47: 307-318.
*
Corresponding author: e-mail: erecta9283@yahoo.com.tw.
INTRODUCTION
A total ca. 750 Ficus species worldwide are distributed
in tropical to subtropical areas (Corner, 1965; Berg, 1989),
and each species is typically pollinated by females of its
own specific species of fig wasp (Galil, 1973; Wiebes,
1979; Van Noort and Compton, 1996). The relationship
between Ficus species and their pollinating wasps
(Agonidae, Chalcidoidea, Hymenoptera) is considered
to be an extreme instance of plant-animal co-evolution
(Janzen, 1979). Fig trees are defined by the syconium
(syncarp or fig), a unique enclosed inflorescence, which
is lined with several dozen to thousands of tiny, unisexual
flowers (Berg, 1989; Verkerke, 1989; Tzeng et al., 2001).
This is also the arena for interactions with fig wasps.
The morphologically specific fig wasp enters the syconia
through the bract-lined entrance of the ostiole, often losing
their wings and antennae in the process. The pollen-loaded
wasps then pollinate the female flowers. In turn, wasp
reproduction is dependent on the fig, as its larvae feed on
galling flowers (Ramirez, 1970; Galil, 1973; 1977; Janzen,
1979; Van Noort and Compton, 1996).
Fig trees can be classified as either monoecious or
dioecious, with each group comprising roughly 50% of
the species (Corner, 1965; Berg, 1989). In monoecious
fig trees, male and female flowers line the inner wall of
the same syconium. Female flowers, differing in style
and length, comprise the imperfect heterostyle (Verkerke,
1989). Additionally, the ovules of female flowers can
be pollinated for seed-production and oviposited for fig
wasp developing the gall, in which larvae feed (Bronstein,
1988). Several weeks later, adult fig wasps emerge and
mate while still in the syconium. The wingless males can
then cut a tunnel out of the syconia, often dying inside
the natal syconium. The female pollen-carrier emerges
from the now-mature male flowers, either through passive
ducting or packing special pollen pockets and depart to
search for receptive syconia (Galil and Eisikowitch, 1968;
eCOlOgy
Pollinational-mutualism strategy of Ficus erecta var.
beecheyana and Blastophaga nipponica in seasonal
guandaushi Forest ecosystem, Taiwan
Hsy-Yu TZENG
1,
*, Fu-Yuan LU
2
, Chern-Hsiung OU
3
, King-Cherng LU
3
, and Li-Jung TSENG
3
1
Hengchun Center, Taiwan Forestry Research Institute, 203 Kungyuan Rd., Hengchun 94644, Pingtung, TAIWAN
2
Department of Forestry and Natural Resources, National Chiayi University, 300 University Rd., Chiayi 60004, TAIWAN
3
Department of Forestry, National Chunghsing University, 250 Kuokwang Rd., Taichung 40227, TAIWAN
(Received November 23, 2004; Accepted January 26, 2006)
ABSTRACT.
This study investigates pollination mutualism between F. erecta var. beecheyana and its
obligate pollinator Blastophaga nipponica using detailed phenology data from the seasonal Guandaushi Forest
Station. The symbiotic cycle resembled that of the F. carica and B. psenes in southern France. Blastophaga
nipponica emerged from the D-phase syconia of over-winter male crops and entered the receptive male
syconia to lay its eggs during the spring male main crop reproductive period. Several weeks later, dozens of
offspring emerged and pollinated the receptive syconia of the summer female major crop. A few pollinators
entered the receptive male syconia to oviposite, and their offspring wintered inside the male fig as larvae or
pupae. The fig trees could control the developmental period of wasp-producing syconia during pollination.
The peak of B-phase syconia (pollinators pollinate or set eggs) of both genders appeared earlier than the
abundant D-phase syconia (pollinators released) by about two to three weeks. On the other hand, the flowering
syconia of both genders occurred abundantly, staggered about two to four weeks after heavy rainfall, and the
fly-out pollinators would pollinate or lay eggs during this period. This fig flowering phenology accommodates
the shorter life span of the obligate species-special pollen carrier to enter the receptive syconia for effective
oviposition or seed-setting. Ficus erecta var. beecheyana and B. nipponica thus have a successful mutualism
strategy of pollination at the Guandaushi Forest Station.
Keywords: Blastophaga nipponica; Ficus erecta var. beecheyana; Guandaushi Forest Ecosystem; Mutualism;
Pollination.
pg_0002
308
Botanical Studies, Vol. 47, 2006
Bronstein et al., 1990). Because monoecy have syconia,
with ripeness is synchronized within an individual tree
and are typically asynchronous between trees, the female
pollinators flying out of the syconia must search for
another receptive syconium on another tree to oviposite
and pollinate in (Galil et al., 1970; Janzen, 1979; Wiebes,
1979; Bronstein et al., 1990; Bronstein and Patel, 1992;
Thomson et al., 1997).
Dioecious fig species, however, have divided the
production of seeds and the rearing of pollinators into
two inflorescent types on separate plants: syconia male
and female figs. Male and short-style female flowers
(gall flowers, for fig wasp ovipositing), line the male
syconium while long-style female flowers (seed flowers
for seed production) and/or neutral flowers line the female
syconium (Weiblen et al., 1995; Tseng, 1999; Tzeng
et al., 2001). Short- and long-style female flowers are
differentiated by length of style, morphology, structure of
stigma and ovary (Verkerke, 1990; Beck and Lord, 1988a;
Tseng et al., 2000; Tzeng et al., 2001), and by pollination
physiology (Verkerke, 1990; Beck and Lord, 1988b),
which displays the perfect heterostyle (Verkerke, 1989;
1990).
Adult female pollinators emerge from D-phase syconia
and search for male receptive syconia to oviposit or female
receptive syconia to pollinate during their extremely short
lifespan ranging from several hours to two days (Kjellberg
et al., 1988; Tzeng, 1997; Wu, 1996; Tseng, 1999). After
pollination or oviposition, the wasp usually dies inside the
syconium it last visited. Otherwise, unvisited syconia are
then aborted.
Dioecious figs must produce D- and B-phase male
syconia during the same period to maintain a continuous
pollinator life cycle (Anstett et al., 1995; Tzeng, 1997;
Kameyama et al., 1999), and pollination success is
dependent on the continuous cyclical production of
pollinators with pollen-entering receptive syconia (Chen,
1998; Tseng, 1999; Harrison et al., 2000). Syconia
phenology has been shown to be useful in investigating
the influence of climatic fluctuation and biotic interactions
in some studies on dioecious figs in seasonal environments
which show sexual specialization (Valdeyron and
Lloyd, 1979; Spencer et al., 1996; Tzeng et al., 2003;
Chang, 2003). Dioecious figs do not necessarily ensure
outcrossing (Corlett, 1987), but the fig trees must imitate
the morphology, color, and odor of their syconia to keep
the fig wasps from distinguishing male from female
syconia and, thereby, only setting eggs (Grafen and
Godfray, 1991; Ware et al., 1993; Ware and Compton,
1994); they must also be prevented from recognizing the
fig phenology between male and female trees (Kjellberg
et al., 1987; Kjellberg and McKey, 1989; Spencer et al.,
1996; Patel and McKey, 1998; Harrison et al., 2000;
Tzeng et al., 2004).
The short lifespan of a pollinator (Kjellberg et al.,
1988; Wu, 1996; Tseng, 1999) and the receptive syconia
can prevent aborting when pollinators do not pollinate
or oviposite on the female flowers during a 2- to 3-week
period (Khadari et al., 1995; Tzeng, 1997). Kjellberg et al.
(1987) elucidated the stability of the symbiotic relationship
between the dioecious figs F. carica L. and Blastophaga
psenes L. and their pollinators during seasonal
environments. However, no studies have identified the
relationship between the life cycle of the pollinator¡Xwith
their short-lived escape from D-phase syconia¡X and the
receptive syconia for both genders year round. The goal
of the present study is to elucidate the syconia phenology
o f F. erecta Thunb. var. beecheyana (Hook. et Arn.)
King and determine the relationship between flowering-
phase syconia reproduction and the dynamic processes
of the obligate pollinator Blastophaga nipponica Grandi.
under sporadic rainfall. Additionally, this study identifies
the pollination-mutualism ecology between a fig and its
pollinator in the seasonal environment at the Guandaushi
Forest Station.
Studied site
The studied area was located at the Guandaushi Forest
Station of the Hue-Sun Experimental Forest Station (24o4¡¦
N, 12 o80¡¦E), one of the Long Term Ecological Research
(LTER) sites in Central Taiwan (Figure 1). During the
study period of 1996, the average annual rainfall, relative
humidity, and yearly temperature were 2,596.9 mm,
79.1%, and 21.0¢XC, respectively (data from the station).
Most of the rainfall (96.2% of total) occurred during
the rainy and typhoon seasons. The average rainfall
over ten years was 2,683.3 mm (Figure 2, from 1987 to
1996), and 93.2% occurred during the warm-wet season.
According to the classification of Thomthwite, this study
area belongs to AB¡¦wa¡¦, a wet but warmed wintertrochene
klima (Yu, 2001). The vegetation of the site is typical of
a warm forest and is characterized by a Ficus ¡V Machilus
vegetation zone at about 500-800 m (Liu, 1968; Su, 1992;
Lu and Ou, 1994).
F igu re 1. T he s tudied area was located at the Guandaus hi
Forest Station of the Hue-Sun Experimental Forest Station in
Central Taiwan.
pg_0003
TZENG et al. ¡X Pollinational-mutualism strategy of
F. erecta
var.
beecheyana
and
B. nipponic
a in Taiwan
309
Biology of Ficus erecta var. beecheyana
Ficus erecta Thunb. var. beecheyana (Hook. et Arn.)
King (Figure 7a) is a small semi-deciduous to deciduous
tree or big shrub from 2 to 5 m, distributed mainly in
southern China, from Ryukyu, Taiwan, Orchid Is., Hong
Kong, to the Malay Peninsula (Corner, 1965; Liu et al.,
1994; Liao, 1995; Tzeng, 2004). It is a pioneer species,
usually occurring in the lowland to medium altitude of
disturbed forests, second forests, or along roadsides (Liu
et al., 1994; Liao, 1995; Tzeng, 2004). The fig¡¦s obligate
pollinator is Blastophaga nipponica Grandi. (Figure 3a,
b) (Chen and Chou, 1997). The non-pollinating fig wasp,
Sycoscapter inubiae Ishii (Figure 3c, d), which oviposites
through the syconium exterior during the C-phase, and
its offspring may feed on the pollinator ¡¦s larvae inside
the ovary (Wu, 1996; Tzeng, 1997). The special-species
pollinator is also shared with F. erecta Thunb. var. erecta
(Okamoto and Tashiro, 1981; Chen and Chou, 1997).
This fig is morphologically gynodioecious and
functionally dioecious, with populations comprised of
female and hermaphrodite individuals, and this study
refers to the two tree sexes as female and male (Tzeng et
al., 2001). The syconia are axillary but male syconia are
generally born on the older branches while the female
syconia are mostly initiated on new branches (Tzeng et
al., 2003). The classification of the post-budding period
development processes of F. erecta var. beecheyana
is based on Galil and Eisikowitch (1968) and on
modifications by Tzeng et al. (2001).
A fig tree can produce one to four crops each year for
both genders within the tree, and the syconia productions
were seasonally at population level, which responded to
the fluctuation of climate and showed sexual difference
(Tzeng et al., 2003; Tzeng et al., 2004). The specific
pollinator must fly out the D-phase syconium from its
natal tree to find another B-phase syconium to set eggs or
pollinate in during its short-life span of several hours to
two days (Okamoto and Tashiro, 1981; Wu, 1996; Tzeng,
1997). The phenology of this fig indicated that the syconia
production of each gender was adapted to the environment,
and it would be helpful for seed production, germination,
and maintaining the population of the obligate pollinator,
Bl. nipponica, respectively (Tzeng et al., 2004).
MATeRIAlS AND MeTHODS
Samples selection
A total of 71 trees of F. erecta var. beecheyana were
marked (40 male and 31 female mature trees), from
which 30 mature trees (17 male and 13 female) were
selected for pollination examination. The figs trees were
somewhat closely distributed along the roadside or under
a 36-year-old China fir (Cunninghamia lanceolata) in an
artificial forest at the study site. Two to three branches
roughly 50 cm long from one tree or a whole, small
tree approximately 2 to 3 m high were selected for each
census. The figs, in the form of a shrub to small tree, were
2-5 m high with a diameter at breast height (DBH) of 2-10
cm.
Field observations
Syconia censuses of F. erecta var. beecheyana were
conducted at 5-9 day intervals from November 1995 to
April 1997 at the Guandaushi Forest Station. The numbers
of all syconia in the developmental stage were counted
for each gender during each census. The classification
of syconia development was based on the following
characteristics: (Table 1, Tzeng et al., 2001) male figs
do not have an E-phase, and female figs do not have a
D-phase. Although the syconium acts as both flower and
Figure 2. The ecological climate diagram of Hue-Sun
Experimental Forest Station; (P ) re prese nts perhumid; (H)
represents relative humid; (D) represents relative drought.
Figu re 3. The pollinator of Blastophaga nipponica Grandi.
and non-pollinating fig wasp of Sycoscapter inubiae Ishii. a, c,
indicate male wasps; b, d, indicate female wasp; bars indicate 1
mm.
pg_0004
310
Botanical Studies, Vol. 47, 2006
fruit, the true flowering phases of syconia are actively
B- and D-phases, together forming the critical phase of
syconia development in the mutualistic system. Data were
analyzed using SPSS 8.0. Kendall¡¦s rank correlation was
used to assess between each phenological census and
climate at the study site.
ReSUlTS
Relationship between pollinator life-span and
the flowering-phases of syconia
The B-phase male syconia germinated abundantly
from the male spring crop during March 1996, matching
primarily the mostly D-phase syconia of the 1995 over-
winter syconium crop (Figures 4, 5). The peak of the
D-phase syconium was delayed by roughly three weeks,
after the B-phase syconia of the male trees. The obligate
pollinator, Blastophaga nipponica, emerged from the
D-phase syconia of the 1995 over-winter syconia crop to
search for the B-phase of the male syconia to set eggs.
The pollinator was observed searching for the B-phase of
the male syconia on the same tree or flying away from the
host tree to find the B-phase male syconia on other trees.
The pollinator ¡¦s larvae developed in the 1996 main
male crop in spring between March and June. Several
weeks later the male syconia had successfully developed
from C- to D-phase. D-phase syconia were located in the
bloom, and the pollinator offspring (second generation)
emerged in large numbers primarily from D-phase male
syconia while the B-phase syconia were abundant in the
main female crop in summer. The female pollinators flew
out of their host syconia to search for another B-phase
syconia to set eggs. However, most pollinators joined the
Table 1. Syconia developmental stage, size, and maturity of F. erecta var. beecheyana for both genders.
Phase
Syconium dimater
Syconium maturity
A Pre-female phase ¡ð: 2 ¡V 6 mm
¡ñ: 2 ¡V 21 mm
The young syconia prior to the opening of the ostiole and with tightly closed
ostiolar bracts. Both male and female syconium are orange, red or light
green with dark red spots.
B Female or receptive
phase
¡ð: 6 ¡V 8 mm
¡ñ: 9 ¡V 21 mm
Ostiolar bracts loose. Both seed (female syconia) (Figure 7c) and gall (male
syconia) female flowers (Figure 7d) are ripe. Pollinators, B. nipponica
penetrate into the young syconium (Figures 7b, 8a) and lay eggs into the
ovaries of gall flowers (Figures 8b-d) or pollinate with the seed flowers.
Both male and female syconia are in red or green color with dark red spot.
C Inter-floral phase ¡ð: 6 ¡V 8 mm
¡ñ: 9 ¡V 22 mm
Wasp larvae develop within the occupied ovaries, which are transformed into
galls in male syconium.
D Male phase
¡ñ: 15 ¡V 30 mm Male flowers mature, wasps reach the eclosion stage, and the wingless male
wasp mates with the female wasp which is inside the gall in the syconium
(Figure 7g, h). The female wasps leave the male syconium via the opening
ostiole (Figure 7f) with pollen. The male syconia become soft with dark red
or purple.
E Mature phase
¡ð: 9 ¡V 21 mm Female syconia ripen, becoming dark-purple and soft, sometimes with sweet
liquid outside syconium (Figure 7e).
Figure 4. The relationships between rainfall, temperature and
flowering syconia production of both genders of F. erecta var.
beecheyana at Guandaushi Forest Station from October 1995 to
February 1997.
pg_0005
TZENG et al. ¡X Pollinational-mutualism strategy of
F. erecta
var.
beecheyana
and
B. nipponic
a in Taiwan
311
Figure 5. The relationships of flowering syconia production between D- and B-phase syconia of both genders for each sample tree of
F. erecta var. beecheyana at Guandaushi Forest Station from October 1995 to February 1997. (Ĉ) indicates female pollinators flying
out from D-phase male syconia. (ċ) indicate female pollinators entering B-phase syconia.
mass of B-phase female syconia from the main female
crop in summer for pollination (Figures 4, 5). A few
female pollinators found the B-phase male syconia of the
sub-male syconia crop for ovipositing. Some offspring
of the third or four generations of pollinators developed
in the sub-male syconia crop from September 1996 to
February 1997 (Figures 4, 5). The pollinational-symbiotic
ecological model is shown in Figure 6.
The incidence of D-phase syconia was well matched
with the abundant B-phase male and female syconia.
The largest number of B-phase syconia of both genders
developed 2 to 3 weeks before the peak of the D-phase
syconia (Figure 4). During the first peak of B-phase
male syconia, approximately 80% of male trees bore
B-phase syconia, and roughly 50% of male trees bore
syconia during the second crop (Figure 4). Roughly
80% of female trees bore B-phase syconia during the
summer main crop, and more than half trees bore B-phase
syconia during the fall sub-main crop (Figures 4, 5). The
frequency distribution of flowering syconia production
of D- and B-phase syconia for both genders were similar
to the proportional distributions of female and male trees
with flowering-phases syconia in each census, a very
significant correlation (Table 2). Each male tree produced
1 to 3 (4) generations of pollinator each year (Tzeng et al.,
2003) with the B-phase and D-phase male syconia present
continuously year round and matching each other (Figures
4, 5, 6).
The relationship between syconia development
and weather
The abundant D- and B-phase syconium reproduction
of both genders was staggered with heavy rainfall by
roughly 2 to 3 weeks although data analysis did not
identify a significant correlation between rainfall and
reproduction (Table 3). The abundance of D-phase syconia
of the 1995 over-winter crop and the B-phase syconium
reproduction in the main male crop in spring occurred
prior to the heavy rainfall in the rainy season (Figure
4). The main male crop in spring developed to the full-
bloom D-phase from June to July between the heavy
rainfall of the rainy and typhoon season. Female fig trees
bore two peaks of abundant B-phase syconia from June
to September (Figure 4). The first peak of the B-phase
female syconia occurred between the heavy rainfall of the
rainy and typhoon season. The second peak of the B-phase
female syconia occurred after the heavy rainfall in the
typhoon season.
The receptive syconia were pollinated or oviposited for
both male and female trees and developed into C-phase.
The abundance of the C-phase syconia of female trees was
significantly correlated with temperature and negatively
correlated with temperature for the males (Table 3).
However, C-phase syconia production was not correlated
with rainfall for either gender (Table 3); C-phase syconia
were plentiful during periods of heavy rainfall in the rainy
and typhoon seasons.
pg_0006
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Botanical Studies, Vol. 47, 2006
DISCUSSION
Symbiotic relationship between fig and fig
wasp
In the Guandaushi Forest Station, the B- and D-phase
syconia in the flowering stage were numerous during the
specified period. The relationship between F. erecta var.
beecheyana and its obligate pollinator, B. nipponica, is a
symbiotic-pollination relationship, somewhat similar to
the model of F. carica and B. psenes in southern France
(Kjellberg et al., 1987). Ficus erecta var. beecheyana,
which shares affinity with F. carica, belongs to the
subgenus Ficus, section Ficus (Corner, 1965; Tzeng,
2004), and might have processes similar to F. carica.
In a seasonal environment, F. erecta var. beecheyana
produced seasonal and asynchronous crops between its
male and female populations, with the males producing
syconia earlier than the females by roughly 2 to 3 months
(Wu, 1996; Tzeng et al., 2003). At the Guandaushi Forest
Station, fig wasps emerged from the D-phase syconia of
the 1995 over-winter crop between March and April when
the receptive syconia of the main male crop in spring were
Table 2. Kendall rank correlations (£n) between rainfall, temperature, and developmental syconia production for each observation
date of Ficus erecta var. beecheyana (males/females = 17/13, observation times = 74) at Guandaushi Forest Station from October
1995 to February 1997. Each significance test involves a separate risk of a type I error. NS indicates that means in a given column
do not signigicantly differ at the 5% level.
¡ñ D-phase syconia ¡ñ D-phase tree (%) ¡ñ B-phase tree (%) ¡ð B-phase tree (%)
¡ñ D-phase syconia
£n
1.000
0.079
-0.066
£l
0.000
NS
NS
¡ñ B-phase syconia
£n
0.121
0.121
0.834
£l
NS
NS
0.000
¡ð B-phase syconia
£n
-0.066
-0.066
1.000
£l
NS
NS
0.000
Table 3. Kendall rank correlations (£n) between rainfall, temperature, and developmental syconia production for each observation
date of Ficus erecta var. beecheyana (males/females = 17/13, observation times = 74) at Guandaushi Forest Station from October
1995 to February 1997. Each significance test involves a separate risk of a type I error. NS indicates that means in a given column
do not signigicantly differ at the 5% level.
¡ñ B-phase syconia ¡ñ C-phase syconia ¡ñ D-phase syconia ¡ð B-phase syconia ¡ð C-phase syconia
Rainfall
£n
-0.037
-0.076
0.088
0.120
-0.010
£l
NS
NS
NS
NS
NS
Temperature £n
-0.053
-0.185
-0.047
0.521
0.480
£l
NS
0.020
NS
0.000
0.000
Figure 6. Pollinational-symbiotic ecological modal of F. erecta
var. beecheyana and its obviously pollinator, B. nipponica at
Guandaushi Forest Station from October 1995 to February 1997.
Narrows indicate that female pollinators are flying-out from the
D-phase syconium to female syconium.
pg_0007
TZENG et al. ¡X Pollinational-mutualism strategy of
F. erecta
var.
beecheyana
and
B. nipponic
a in Taiwan
313
Figure 7. a, Syconia on the branch of Ficus erecta var. beecheyana; b, Blastophaga nipponica inside the B-phase syconium; c,
B-phase seed flowers of section syconium; d, stigma of B-phase gall flowers; e, E-phase female syconium; f, Opening ostiole of
D-phase syconium; g, Male B. nipponica mates with female, which is inside the gall; h, Female B. nipponica leaves the gall. Bars
indicate 10 cm for Figure 7a, 5 mm for Figure 7b, 1 mm for Figure 7c, d, g, h, and 1 cm for Figure 7e, f.
pg_0008
314
Botanical Studies, Vol. 47, 2006
plentiful. Most male fig trees initiated new syconia during
the main male crop but bore asynchronous syconia during
other periods within the population (Tzeng et al., 2003).
Male syconia developed with a similar growth ratio from
A-phase to the B-phase when the 1996 over-winter male
syconia matured and released countless of fig wasps.
If a female founder enters a B-phase male syconium
successfully during the bagged experiment, 100 to 200
offspring could be born during the D-phase syconium
several weeks later (Tzeng, 1997). This would extend
the pollinator population by an average of 152 times for
one founder. In contrast, the average number of progeny
(average = 327) inside one D-phase syconium during the
1996 main male crop in a natural state was significantly
higher than the one founder ¡¦s (T=4.209, £l=0.000), despite
the larvae of the non-pollinator S. inubiae¡Xa parasite¡X
which fed on the larvae of the pollinator inside the ovule
(mean number of pollinators=255; T=3.156, £l=0.003) and
had a negative relationship with the pollinator (Tzeng,
1997). Conversely, the fig wasp population released from
the 1995 over-winter crops was substantially larger than
the number of receptive syconia of the 1996 main male
crop in spring. Due to creating a good match between D-
and B-phase of the male syconia, the pollinator of the
1996 main male crop in spring was extended.
In dioecious figs, wasps can only breed in the gall
flowers of male syconium; consequently, pollination of
female syconia is always lethal (Kjellberg et al., 1987).
Therefore, selection must favor wasps that avoid female
trees. The entry of fig wasps into female syconia to extend
their population in the short-term offers no apparent
benefit (Kjellberg et al., 1987). Hence, to maintain
symbiosis dioecious figs must prevent fig wasps from
developing the ability to distinguish between male and
female syconia. Conversely, syconia display sexual
differences at specific times (Valdeyron and Lloyd, 1979;
Kjellberg et al., 1987; Kjellberg and Maurice, 1989;
Spencer et al., 1996, Tzeng et al., 2003), and fig wasps
have acquired the ability to lay eggs in male syconia
only. However, male and female syconia have modified
their structure, phenology and physiology to prevent the
fig wasp from distinguishing between them (Grafen and
Godfray, 1991; Wu, 1996). Although there is no evidence
that the degree of attraction to female- and male-receptive
syconia of F. erecta var. beecheyana is the same for fig
wasps, it has been demonstrated that fig wasps do not
distinguish between male and female syconia through odor
(Ware and Compton, 1994; Hossaert-McKey et al., 1994).
Pollen carriers are likely to be attracted by receptive
syconia of female trees to pollinate, and surplus pollinators
enter B-phase male syconia to lay eggs to further the
survival of the pollinator population. In brief, fig trees
integrate syconia production phenology and modified
characteristics like odor between male and female syconia
to maintain their mutualism.
Few pollinators entered by chance the male receptive
syconia of the 1996 winter crop, and it was maintained
Figure 8. a, Female B. nipponica often lose their wings in the
ostiole when they penetrate into the B phase syconium; b, c, d,
Female B. nipponica oviposites on the gall flower. Bars indicate
500 £gm for Figure 8a, b, c and 100 £gm for Figure 8d.
pg_0009
TZENG et al. ¡X Pollinational-mutualism strategy of
F. erecta
var.
beecheyana
and
B. nipponic
a in Taiwan
315
Tseng, 1999), F. irisana (Subg. Sycidium, Chen, 1998),
and F. ampelas (Subg. Sycidium, Chang, 2003).
Kjellberg et al. demonstrated that a temporal gap was
a selective pressure favoring the fig wasp¡¦s pollinational-
symbiotic system, concluding that it is characteristic of
F. carica (Kjellberg et al., 1987). However, the receptive
syconia were not visited and were aborted while dozens
of wasps emerged before the development of receptive
syconia in F. carica in Southern France. This might be
a result of long artificial culture and small size samples
(four males and three females) of F. carica employed in
southern France (Kjellberg et al., 1987).
Was the phenomenon of D-phase syconia, which
were in abundance after the B-phase syconia, stable in
the symbiotic system. Because the D-phase syconia
only lasted for a few days (Tzeng et al., 2001), emerging
pollinators had to search for another receptive syconia in
which to lay their eggs or pollinate during their short life-
spans of several hours to 2 days (Ramirez, 1970; Janzen,
1979; Baijnath and Ramcharun, 1983; Kjellberg et al.,
1988; Chen, 1994; Wu, 1996; Chen, 1998; Tseng, 1999).
Observational results indicated that B. nipponica survived
1 to 2 days, and generally less than 1 day during the cold
winter (Wu, 1996; Tzeng, 1997). There were no receptive
syconia to enter for ovipositing or pollinating if the
D-phase syconia developed earlier than B-phase syconia.
Therefore, it is not beneficial for pollinators to emerge
before receptive syconia develop.
B-phase syconia of both tree genders remain on the tree
for roughly 2 to 3 weeks longer than D-phase syconia. In
the monoecious species F. aurea (Bouchaib et al., 1995),
female syconia can survive on the branch for 2 to 5 weeks,
as long as for dioecious species (Bouchaib et al., 1995;
Ware and Compton, 1994; Chen, 1998; Tseng, 1999). The
extended receptive period of the syconia may be a result
of the developmental asynchrony of female flowers inside
the syconia (Tzeng et al., 2001); however, temperature is
the principal factor (Bouchaib et al., 1995).
Although, extending the receptive period wastes the
resources of the trees, a prolonged B-phase provides
increased likelihood for the uncertain flowering period,
low-density population, and seasonal-efficiency of Ficus
for pollination or oviposition (Bouchaib et al., 1995). It is
a critical factor allowing fig and fig wasp to maintain their
pollinational-symbiotic ecological system in a required
minimum number of trees (Bronstein et al., 1990; Anstett
et al., 1995; Bouchaib et al., 1995; Kameyama et al.,
1999). To ensure the future of this relationship, the short-
lived pollinator must enter the B-phase syconia before
they fade. The fig wasps will die before they enter a
receptive syconia to oviposite or pollinate if the receptive
syconia have developed prior to the fig wasp emergence.
That the abundance of receptive syconia occurred
before the numerous of pollinator eclosion (D-phase
syconia) is a flowering characteristic of F. erecta var.
beecheyana. Comparing the cost of a prolonged B-phase
with the successful pollination/oviposition and delayed
by larvae or pupa during the C-phase male syconia in the
winter. For tiny pollinators with a short life span, cold and
rainy weather is fatal (Hill, 1967). However, asynchronous
syconia production can maintain and extend the pollinator
population under such conditions (Ramirez, 1970). In
some male trees, pollinators which escaped from the over-
winter syconia emerge from male syconia and quickly
begin searching for another B-phase male syconia on the
same tree. This can reduce the death ratio and increase the
likelihood of the wasp entering a B-phase male syconia
during the searching period to oviposite.
Ficus erecta var. beecheyana phenologically controls
its gender, preventing the species special pollinator, B.
nipponica, from entering only male syconia. The features
of syconia production within a tree or between trees are
a form of sexual specialization to maintain the fig wasp
populations and attract frugivores for seed dispersal
(Tzeng et al., 2003). Researchers have suggested that it is
the fig tree, not the wasp, which controls the development
time of wasp-producing syconia after pollination occurs
(Kjkllberg et al., 1987).
Observation results showed that B- and D-phase male
syconia were continually present on almost all of the
17 male trees during the study period from Oct. 1995
to Feb. 1997. There were 1 to 3 (4) crops in the male
population (Tzeng et al., 2003) and 1 to 3 (4) generations
of pollinator success in the study population year round.
Although, there was no information on the dynamics of
the pollinator population, less than 20 male trees might
be the smallest survival population of B. nipponica, the
obvious pollinator, in the pollination-symbiotic ecological
system at the Guandaushi Forest Station.
A "temporal gap" between D- and B-phase
syconia production
This study has identified a temporal gap between the
mass production of B- and D-phase syconia in F. erecta
var. beecheyana at the Guandaushi Forest Station. This
phenomenon was somewhat similar to that of F. carica
(Kjellberg et al., 1987) in southern France. However, the
temporal gap of F. erecta var. beecheyana differed from
F. carica in the number of receptive syconia since both
genders were developed earlier than the highest number
of D-phase syconia while female pollinators emerged,
i.e., the emergence of fig wasps from the delayed syconia
(D-phase) occurred earlier than the maturation of the
undelayed syconia (B-phase) in which the fig wasp
oviposited in F. carica (Kjellberg et al., 1987).
The highest D-phase syconia occurred roughly 2 to 3
weeks after the peak of B-phase male and female syconia
in F. erecta var. beecheyana; i.e., the B. nipponica were
released from the D-phase male syconia later than female
syconia of both genders. During the delay period of
D-phase syconia, a few female syconia were entered by
pollinators, released from male syconia. This phenomenon
has been observed in other dioecious figs, such as F. erecta
var. beecheyana (Wu, 1996), F. formosana (Subg. Ficus,
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316
Botanical Studies, Vol. 47, 2006
peak production of D-phase, it showed that dozens
of wasps which emerged after the peak of receptive
syconia would benefit evolution between the short life-
span of B. nipponica and F. erecta var. beecheyana
in seasonal Guandaushi Forest Ecosystem. In one big
enough population, it might present another strategy
on the pollination-symbiosis ecological system in the
seasonal environment for other fig species and its obvious
pollinator. And it has to more research in pollination-
symbiosis to understand the co-evolution of fig and fig
wasp.
Acknowledgement. The authors would like to thank
the National Science Council of the Republic of China,
Taiwan (Long Term Ecological Research: Guandaushi
Forest Ecosystem-Pollination Ecology) for financially
supporting this research under Contract No. NSC
87-2613-B-005-085 A07. Hue-Sun Forest Station and
its officials are appreciated for kindly providing research
permits. Prof. Chen Ming-Yih and Prof. Chou Lien-Siang
are appreciated for their valuable discussions. Thanks to
Dr. Chou Liang-Yi for identifying the fig wasp species.
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