Aeshita Mukherjee

Bing Liang

Lian-Xi Sheng

Min Cao

Richard T Corlett

Shu-Yi Zhang

Zhan-Hui Tang

CiteSeerX

Journal of Tropical Ecology (2007) 23:125–127. Copyright © 2007 Cambridge University Press
doi:10.1017/S0266467406003737 Printed in the United Kingdom
SHORT COMMUNICATION
Effect of ingestion by two frugivorous bat species on the seed germination
of Ficus racemosa and F. hispida (Moraceae)
Zhan-Hui Tang∗†‡, Aeshita Mukherjee∗, Lian-Xi Sheng†1, Min Cao∗, Bing Liang§, Richard T. Corlett#
and Shu-Yi Zhang‡1
∗ Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, Yunnan 666303, China
† Department of Environmental Science and Engineering, North East Normal University, Changchun 130024, China
‡ School of Life Science, East China Normal University, Shanghai 200062, China
§ Institute of Zoology, Chinese Academy of Sciences, Beijing 100080, China
# Department of Ecology and Biodiversity, University of Hong Kong, Pokfulam Road, Hong Kong, China
(Accepted 14 September 2006)
Key Words: China, Cynopterus sphinx, figs, frugivorous bats, Rousettus leschenaulti, seed dispersal, seed germination,
Xishuangbanna
Frugivorous bats are important seed dispersers for many
plant species (Cox et al. 1991, Fleming & Heithaus
1981, Hodgkison et al. 2003a, McConkey & Drake 2006,
Nyhagen et al. 2005, Utzurrum 1995). They regularly
consume figs in the wild (Fujita & Tuttle 1991, Kalko et al.
1996, Shilton et al. 1999). Various species of pteropodid
bats have been reported foraging on the fruits of more
than 30 fig species in tropical and subtropical Asia, Africa
and Australia (Bhat 1994, Fujita & Tuttle 1991, Marshall
& McWilliam 1982, Thomas 1984). Food transit times in
frugivorous bats are relatively rapid; generally less than
30 min (Laska 1990, Tedman & Hall 1985). Several
studies have demonstrated that seed germination was
either enhanced or unaffected after passage through the
digestive tract of bats (Figueiredo & Perin 1995, Fleming
& Heithaus 1981, Lieberman & Lieberman 1986).
In Xishuangbanna, two fig species (Ficus hispida L. and
Ficus racemosa L.) are distributed widely and are thought
to be key species in the rebuilding of degraded habitats
(Peng et al. 2005). Two frugivorous bat species (Rousettus
leschenaulti Desmarest and Cynopterus sphinx Vahl) are
common and widely distributed in Xishuangbanna and
fruits of Ficus hispida and F. racemosa are consumed
heavily by these two bats (Tang et al. 2005). When they
feed on the fruits of these two fig species, a proportion of
seeds was swallowed and excreted through the digestive
tract as scats and others were spat out in compact fibrous
pellets (ejecta). In this study, we investigate the effect
1 Corresponding authors. Email: shenglx@ncnu.edu.cn or zhangsy@
ioz.ac.cn
of bat feeding behaviour on the seed germination of
two common fig species and compare characteristics of
germination for different treatments. We want to know if
foraging behaviour significantly affects seed germination.
We captured bats using mist nests between 1 and 7 July
2005 in a protected area of forest (21 ◦55′N, 101 ◦16′E,
550 m asl) in the Xishuangbanna Tropical Botanical
Garden (XTBG), in Yunnan Province of south-west China.
Seven individuals of R. leschenaulti (3 females and 4 males)
and four of C. sphinx (2 females and 2 males) were selected
and kept in two separate cages (80 × 50 × 50 cm). All
the bats were adult and non-reproductive. Before the
experiments were carried out, the bats were housed in
the cages for 2 d with food (pieces of apple or banana) and
water provided.
We gathered ripe F. racemosa and F. hispida fruits during
their peak fruiting period (between 5 and 30 July 2005
for both species). Bats were fed after sunset each night
and scats and ejecta were collected next morning over a
period of 1 wk for both fig species. We offered fruits of F.
racemosa to R. leschenaulti and C. sphinx, and F. hispida only
to R. leschenaulti. The seeds then were collected and the
germination patterns of three treatments were compared:
(1) seeds from scats; (2) seeds from ejecta; (3) control seeds,
which were obtained from ripe fruits taken directly from
parent trees. The pulp was removed using a soft cloth and
any pulp remains on the seeds were washed off. Sample
sizes are shown in Table 1.
Seeds were placed in Petri dishes (10 cm in diameter)
on moistened filter paper. Petri dishes were placed
in an Intelligent Man-made Climatic Incubator (MGC-
35HP-2, Yiheng Science and Technology Limited
126 ZHAN-HUI TANG ET AL.
Table 1. Germination percentage (GP) of seeds from scats, ejecta and
fleshy fruits. Percentages were compared with Kruskal–Wallis test.
No. GP
Seeds trials Scats Ejecta Control χ2 P
Rousettus leschenaulti
Ficus racemosa 6 98.4 99.7 99.8 1.55 0.461
F. hispida 6 99.2 95.6 99.5 3.10 0.212
Cynopterus sphinx
F. racemosa 6 99.3 98.5 99.8 1.67 0.433
Company, Shanghai, China), which maintained a
constant temperature of 30 ◦C, and 12 h under light in
a 24-h cycle. Petri dishes had been previously sterilized
at 160 ◦C for 10 h, and treatments were moistened with
distilled water periodically. We repeated each treatment
six times, and each repetition consisted of placing at least
60 seeds in a Petri dish. The seeds in each of the Petri dishes
were from different scats, ejecta and figs, but from the same
nights. The numbers of seeds germinating was counted
daily until there was no further germination for over 1 mo.
Germinated seeds were removed as they were counted to
reduce their effect on the remaining ungerminated seeds.
Germination was defined as the emergence of any seedling
part from the seed (Izhaki et al. 1995). Seed germination
percentage was compared among treatments by means of
the Kruskal–Wallis tests, as data could not be normalized
with any transformation.
Quantitative evaluation of seed germination was based
on the following four parameters: (1) final germination
percentage (GP), which refers to the percentage of seeds
capable of germinating under experimental conditions;
(2) germination start (GS), which was defined as the
time interval (d) between sowing and emergence of
one-sixth of the final germination percentage of the
seedlings (Izhaki et al. 1995); (3) minimum imbibition
time (Tmin), which is the minimum time required for
the seeds to start germinating once they have absorbed
the necessary amount of water; (4) time necessary
for reaching 50% germination percentage (T50), which
indicates the time necessary for germination of half the
seeds that germinated by the end of the experiment
(Naranjo et al. 2003).
We found most seeds of F. racemosa germinated during
the first 6 d for all the treatments and both bat species. For
F. racemosa, manipulation by Rousettus leschenaulti did not
significantly affect GP (Kruskal–Wallis test: χ2 = 1.55,
P = 0.461). Tmin and GS of the F. racemosa seeds ingested
by R. leschenaulti (including seeds from scats and ejecta)
were the same as those of control seeds. T50 was 4 d
for control seeds but 5 d for seeds from scats and ejecta
(Tables 1 and 2). The GP for F. racemosa seeds from C.
sphinx scats and ejecta did not differ significantly from
the controls (Kruskal–Wallis test: χ2 = 1.67, P = 0.433).
The treatment received by F. racemosa seeds ingested
by C. sphinx (including seeds from scats and ejecta) did
Table 2. Germination analysis of Ficus racemosa and F. hispida seeds
using germination start (GS), minimum imbibition time (Tmin) and time
in which 50% of the seeds that compose GP (T50) germinate.
Rousettus
leschenaulti
Cynopterus
sphinx
Scats Ejecta Scats Ejecta Control
Ficus racemosa GS(d) 4 4 4 4 4
Tmin(d) 3 3 3 3 3
T50(d) 5 5 4 4 4
Ficus hispida GS(d) 6 6 5
Tmin(d) 5 5 4
T50(d) 6 7 6
not change Tmin and GS. T50 was 4 d for all treatments
(Tables 1 and 2).
Germination in F. hispida occurred within 1 wk and
GP reached about 99% in all treatments after 7 d.
The GP of F. hispida was not significantly affected by
the manipulation by R. leschenaulti (Kruskal–Wallis test:
χ2 = 3.10, P = 0.212) (Table 1). Compared with control
seeds, the treatment received by the F. hispida seeds in the
digestive tracts of R. leschenaulti resulted in an increase in
Tmin and GS of 1 d, which was also true for the seeds from
ejecta. T50 was 6 d for control seeds and seed from scats,
but 7 d seeds from ejecta (Table 2).
Our conclusion that GP of F. racemosa and F. hispida was
not enhanced by passage through the digestive tracts of
either bat species contradicts the observed improvement
of seed germination of Ficus spp. after ingestion by
pteropodid bats in the Philippines (Utzurrum 1995), and
many other studies (Figueiredo & Perin 1995, Lieberman
& Lieberman 1986, Shilton et al. 1999). However,
Sosa (1997) found that ingestion of Stenocereus thurberi
(Cactaceae) by bats did not affect germination, which was
consistent with our results.
Seeds of F. racemosa from scats and ejecta of R.
leschenaulti had a T50 1 d longer than that of control seeds,
but those from C. sphinx did not (Table 2). Differences in
seed responses of the same species to ingestion by different
frugivores, even when frugivores belong to the same
family, as with our results, have been found in a variety
of plants (Traveset 1998). Likewise, the effect produced
by ingestion of seeds by the same bat species may vary
according to the plant species. In our experiment, the GS
and Tmin of F. racemosa seeds from scats and ejecta of R.
leschenaulti were not changed, but GS and Tmin of F. hispida
seeds from scats and ejecta of R. leschenaulti were 1 d later
than control seeds (Table 2). Since the same dispersers
are involved, the difference must be in the seeds or in the
molecular structure of the inhibitor (Naranjo et al. 2003).
Cynopterus sphinx and Rousettus leschenaulti are wide-
ranging frugivorous species (Tang et al. 2005), and are
more likely to cover long distances and hence transport
fruits/seeds further than smaller-sized frugivores with
relatively restricted ranges, such as Balionycteris maculata
Effect of ingestion by two frugivorous bat species 127
(Hodgkison et al. 2003b). Frugivorous bats have been
reported to swallow as much as 80% of the tiny seeds
of figs (Morrison 1980). Due to the short transit time
through the digestive systems of bats, we suggest that
ingestion has only a minor scarifying effect on the testa
of the seeds. So lots of viable seeds were dispersed by
bats through excretion. Because these two bat species
often change their feeding roost and they frequently
excrete during flight, the seeds from scats can be dispersed
extensively. Observations of captured bats in cages
producing defecations after the cages were cleaned in
the morning indicated that they could potentially retain
fig seeds in their digestive tracts for longer time periods
and thus have the potential to disperse them over longer
distances, as suggested by Shilton et al. (1999), who found
seeds of Ficus septica and F. variegata can be retained in the
digestive tract of C. sphinx for > 12 h and were still viable.
In summary, the seeds of two fig species that have
passed through the digestive tract of both bat species
germinate as well as the control seeds except that some
parameters were changed. In order to identify the actual
significance of change of seed germination behaviour in
seedling establishment and figs regeneration, future work
should be focus on seed fate once deposited and seedling
establishment.
ACKNOWLEDGEMENTS
This study was funded by the Laboratory for Tropical Rain
Forest Ecosystem Research and Management (TRERM),
Xishuangbanna Tropical Botanical Garden, Chinese
Academy of Sciences, and National Geographic Society
(7806-05). We especially thank Wang Hong and Tao
Guo-da for their helpful knowledge about plant species
studied.
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Effect of ingestion by two frugivorous bat species on the seed germination of Ficus racemosa and F. hispida (Moraceae

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Effect of ingestion by two frugivorous bat species on the seed germination of Ficus racemosa and F. hispida (Moraceae

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