ORIGINAL ARTICLE

Ning Li

Shu-qing An

Zhao Liu

Chang-hu Lu
Fruit consumption and seed dispersal by birds in native vs. ex situ
individuals of the endangered Chinese yew, Taxus chinensis
Received: 11 February 2014 / Accepted: 1 July 2014
The Ecological Society of Japan 2014
Abstract The conservation success of endangered trees
may depend on re-establishing or replacing the mutu-
alisms that were important in their native habitats. In
this study, we quantied avian frugivore diversity on
individuals of the endangered Chinese yew (Taxus
chinensis) in a botanical garden and at a natural site. We
found that frugivore species diversity was lower in the
botanical garden than in the natural site. In spite of the
relatively low frugivore diversity, however, the ex-situ
population of Chinese yew attracted similar disperser
species to those in the natural population, and trees in
the ex-situ population were visited more frequently than
those in the natural population. Furthermore, the dif-
ferent perching behavior of dispersers resulted in dif-
ferent dispersal eciencies. Although the Chinese bulbul
(Pycnonotus sinensis) was the most common forager in
the botanical garden, its dispersal eciency was the
lowest, and thus it could not like the role played by the
mountain bulbul (Hypsipetes maclellandii) in the natural
site. Only the red-billed blue magpie (Urocissa ery-
throrhyncha) provided a high-quality dispersal service in
both sites. Our results highlight the ability of the Chinese
yew to recruit seed dispersal agents in new habitats.
However, if the newly recruited species is a low-quality
disperser, the plants will depend more heavily on other
avian vectors for regeneration.
Keywords Seed dispersal Dispersal eectiveness
Taxus chinensis Ex-situ population Nature
population
Introduction
When endangered plant species are transplanted to
botanical gardens in order to restore populations (Gu-
errant et al. 2004), their interactions with resident
organisms may determine whether they establish suc-
cessful (Carroll and Fox 2008). Non-native establish-
ment is limited by competition with, or herbivory by,
resident species (Cogni 2010). In contrast, mutualisms
with pollinators or dispersers may permit population
establishment in new environments (Bascompte and
Jordano 2007; Morales et al. 2013).
Generally, many endangered eshy-fruited plant
species can easily attarcted native birds to dispersal its
seeds (Howe and Smallwood 1982; Bacles et al. 2010;
Carnicer et al. 2009). These seed dispersal are generally
diuse: many bird species interact with the plant species
(Bascompte and Jordano 2007; Breitbach et al. 2010),
although dispersal eciency clearly diers among the
dierent bird species (Jordano et al. 2007; Spiegel and
Nathan 2007; Calvin o-Cancela and Mart n-Herrero
2009). It is vitally important for ex-situ plants to form
mutualistic interactions with eective dispersers in
botanical gardens; however, botanical gardens, which
are subjected to a relatively high degree of human
interference (Maunder 1992; Guerrant et al. 2004; Car-
roll and Fox 2008), dier signicantly from natural sites.
This dierence may result in distinct variations in the
seed dispersal.
Previous studies have shown that several alien eshy-
fruited plants could easily attarcted native birds to dis-
persal their seed in the new habitats (Gleditsch and Carlo
Electronic supplementary material The online version of this article
(doi:10.1007/s11284-014-1180-z) contains supplementary material,
which is available to authorized users.
N. Li C. Lu (&)
Laboratory of Plant-Animal Interactions, College of Forest
Resources and Environment, Nanjing Forestry University,
Nanjing 210037 Jiangsu, China
E-mail: [email protected]
E-mail: [email protected]
Tel.: +86-25-85427085
S. An N. Li
School of Life Science, Nanjing University, Nanjing 210093
Jiangsu, China
Z. Liu
Key Laboratory of Animal Ecology and Conservation Biology,
Institute of Zoology, Chinese Academy of Sciences,
Beijing 100101, China
Ecol Res
DOI 10.1007/s11284-014-1180-z
2011; Caughlin et al. 2012; Cruz et al. 2013). These plants
can successfully establish in these habitats and may even
become invasive (Gosper et al. 2005; Aslan 2011; Heleno
et al. 2013). However, there are few reports regarding the
seed dispersal of ex situ plants in new habitats.
The Chinese yew (Taxus chinensis) is a typical gym-
nosperm plant that is endemic to China. It has been
listed as an endangered (EN) species by the IUCN
(Thomas et al. 2013) and a rst-class national protected
plant in China. The regeneration of wild populations is
limited (Deng et al. 2008) due to low pollination rates,
seed-predator pressure, weak competitive ability of
seedlings, and scarcity of microhabitats for recruitment
(Li et al. 2000,2014a). To protect this endangered tree
species, 11 seedlings were transplanted from their native
area, the Lu Mountains in Jiangxi Province, to the
Nanjing Botanical Garden Memorial Sun Yat-Sen in
Jiangsu Province in the 1950s. These trees formed cones
and produce seeds in the 1980s, and a regenerated
population established that relies on avian dispersers
(Lu et al. 2008). In this study, we quantied avian fru-
givore diversity on individuals of the endangered Chi-
nese yew (Taxus chinensis) in a botanical garden and at a
natural site. We addressed the following scientic ques-
tions: (1) How do bird dispersers dier in fruit con-
sumption in native vs. ex situ individuals of Chinese yew,
thus aecting seed removal in two sites? (2) How do bird
dispersers perch after foraging in two sites, thus aecting
seed dispersal eectiveness of Chinese yew?
Materials and methods
Species and study site
The Chinese yew has been listed as an endangered (EN)
species by the IUCN (Thomas et al. 2013); it is a dioe-
cious and wind-pollinated species that is distributed in
evergreen broadleaf forests. Every year, female plants
bear axillary cones which, in autumn, develop into eshy
arils (commonly, although incorrectly, referred to as
fruits) that contain a single seed. An average tree
bears more than 4000 of these fruits (Lu et al. 2008;
Thomas et al. 2013).
We selected two sites with dense populations of
Chinese yewone was a natural population in Anhui
Province and the other was a ex situ population intro-
duced into Jiangsu Province.
Anhui Province is an important native area for Chi-
nese yew. The study site, Shuangkeng village (3000N,
11718E; AL: 540 m), is located on Xianyu Mountain
in the southern part of Anhui Province. The annual
average temperature is 16 C, with a mean annual pre-
cipitation of 1626.4 mm. Human-modied patches of r
(Cunninghamia lanceolata) and bamboo (Phyllostachys
heterocycla) and natural patches (broadleaf forest,
mixed coniferous-broadleaf forest) are interlaced with
plantations of tea (Camellia sinensis) to form a hetero-
geneous mosaic. The only mature population of yew in
the area occupies approximately 2.33 ha in a human-
modied bamboo patch located at the far end of the
village. Seedlings and saplings were found in the patch in
which mature trees were distributed (Deng et al. 2008).
An ex situ population of Chinese yew at the Sun-Yat
Sen Memorial Botanical Garden, Nanjing, Jiangsu
Province, China (325N, 11848E; AL: 3050 m), was
also investigated. The garden covers a fenced area of
approximately 186 ha at the south foot of the Purple
Mountain, Jiangsu Province. No wild Chinese yew
populations exist in Jiangsu Province. This ex situ
population consisted of ve females and four males.
Seedlings and saplings were found on a hillside in an
approximately 0.5-ha area that was separated from the
mother trees by a small stream. The vegetation was
dominated by Pterocarya stenoptera and Quercus acu-
tissi, mixed with other species such as Q. variabilis,
Liquidambar formosana, Cryptomeria fortunei, Pinus
thunbergii, Lindera glauca, Ilex purpurea, Photinia
serrulata, Ilex cornuta, Cyrtomium fortunei, Asplenium
incisum, and Milletia reticulata (Li and Yin. 2004; Lu
et al. 2008).
Frugivorous bird diversity in the botanical garden
and natural site
To quantify the avian frugivore diversity in the vicinity
of the population of Chinese yew, we estimated the
species richness, diversity, and total abundance of fru-
givorous birds during the fruiting season using line
transects. In both study sites, a 50-m-wide, 3-km-long
transect was set across the plant population and two
further transects (50 m wide, 3 km long) were set 100 m
either side of, and parallel to, the rst transect. Two
investigators walked along the lines between 0700 and
1000 and 1600 and 1800 hours on two separate days and
counted frugivorous birds (Gil-Tena et al. 2007). Each
line transect was surveyed four times by the same
observers. In total, each site was surveyed for 240 h over
2 years.
For each frugivore species, we retained for each
species the highest of the three values recorded during
three censuses. We then used the Shannon-Wiener index,
Pielou species evenness index, Sorensen similarity index,
and Simpsons dominance index to compare frugivore
species diversity between the two habitats under inves-
tigation (Magurran 1988; Sutherland et al. 2004).
Fruit consumption of frugivorous birds in the botanical
garden and natural site
We observed mother trees during two fruiting seasons
(from late October to early December). Five mother
trees were observed between 20 October and 10
December in 2011 and 2012 at the botanical garden and
the natural site. Each mother tree was observed for an
8-h period starting at sunrise. Observations were made
with binoculars from a hide placed at least 20 m from
the trees. Observations ended when no more fruits re-
mained on the mother trees. All observations were made
in good weather.
For each bird that visited a mother tree, we recorded
the species, time spent foraging in the tree, number of
fruits foraged during the visit, and the fruit-handling
behavior from the time of the birds arrival until it left
the tree. If a group of conspecic birds visited the tree
and the behavior of all birds could not be observed
simultaneously, we focused on the individual that was
most visible (Altmann 1974; Breitbach et al. 2010). Seed
dispersers were dened as bird species that were ob-
served swallowing fruits or carrying fruits away in their
beaks (Traveset 1994). We used t tests to compare the
visiting frequency of both frugivorous bird species and
disperser species at the botanical garden with those at
the natural site (Quinn and Keough 2002).
Seed dispersal eectiveness of bird dispersers
in the ex situ and natural populations
Previous studies have shown that the seeds of Chinese
yew are mainly dispersed by Corvidae and Pycnonot-
idae (Lu et al. 2008; Li et al. 2014a). In our study, we
focused on bird species in these two families and their
post-foraging behaviors were tracked. The eectiveness
of seed dispersal was evaluated by the spatial corre-
lation between bird perching frequency and the
quantity of 1-year-old seedlings, because the seedling
numbers and its distribution are signicantly aected
by disperser behavior in patchy environments (Breit-
bach et al. 2010). A strong, positive spatial correlation
between perching frequency and 1-year-old seedlings
indicates that the bird is able to transport a relatively
large number of seeds to seedling habitats, thereby
contributing to the quality component of dispersal
eectiveness (Breitbach et al. 2010, 2012; Puerta-Pin -
ero et al. 2012).
Initially, 10 10 m
2
habitat cells were used to digitize
two study sites. The 1-year-old seedlings (H 10 cm)
in each cell were then located. In all, we surveyed 48
sampling cells in the botanical garden and 72 cells in the
natural site. We modeled seedling distribution at both
sites using the biharmonic-spline surfaces interpolation
method (Quinn and Keough 2002).
We observed the post-foraging behaviors of avian
dispersers and recorded the habitat cells in which birds
perched after they left the study trees. The perching
locations of each bird were recorded every 30 s until the
bird was lost from sight (Breitbach et al. 2010). These
perching locations were used to identify characteristic
landmarks near the study trees for later verication of
estimates through measuring on maps. Spearmans rank
correlation coecient indices and a simple regression
model were used to test the correlation between bird
perching and seedling numbers at each study site (Quinn
and Keough 2002).
Results
Frugivorous bird diversity in the botanical garden
and natural site
During the fruiting seasons, we observed 32 and 27
frugivore species in the natural site and botanical gar-
den, respectively. The composition of frugivore species
overlapped between the sites (Similarity index 57.63 %),
but species diversity diered between sites. There were
fewer dominant species in the natural site than in the
botanical garden, whereas frugivore species richness and
total abundance was lower in the botanical garden than
at the natural site (Table 1, Table S1).
Fruit consumption of frugivorous birds in the botanical
garden and natural site
During 324 h of tree observations at each site, we re-
corded 324 visits of nine bird species that foraged seeds in
the natural site and 576 visits of ve such species in the
botanical garden. The visiting frequency of frugivorous
birds was signicantly higher in the botanical garden
(576 visits) than in the natural site (324 visits)
(t = 4.250, df = 2, P = 0.005). Moreover, the species
composition of the frugivorous birds diered between
the two sites. In the natural site, the main foraging spe-
cies were mountain bulbul (Hypsipetes maclellandii; 151
visits), red-billed blue magpie (Urocissa erythrorhyncha;
76 visits), and chestnut bulbul (Hemixos castanonotus; 43
visits) (Table 2). In the botanical garden, the main for-
aging species were Chinese bulbul (Pycnonotus sinensis;
406 visits), red-billed blue magpie (118 visits) and azure-
winged magpie (Cyanopica cyana; 32 visits).
During the fruiting season, ve bird species dispersed
seeds following 244 visits in the natural site and four bird
species were observed to disperse seeds following 563 visits
in the botanical garden. The composition of disperser spe-
cies diered between the two sites and the visiting frequency
was signicantly higher in the botanical garden than in the
natural site (t = 3.850, df = 2, P = 0.001; Table 2).
Seed dispersal eectiveness of bird dispersers in ex situ
and natural populations
In the seedling census, 221 and 208 seedlings were found
in the natural site and botanical garden, respectively. All
Table 1 Diversity comparison of frugivore birds in a natural site
and a botanical garden
Measure of diversity Natural site Botanical garden
Shannon-Wiener diversity 1.580 1.524
Species evenness index 0.682 0.654
Simpsons dominance index 0.045 0.800
Sorensen similarity index (%) 57.630
seedlings were aggregated within 100 m of mother trees
(Fig. 1) showing a bird-dispersed pattern (Li et al.
2014a). The dierent perching behaviors of the main
dispersers was associated with dierences in dispersal
eectiveness (Fig. 2).
At the natural site, both mountain bulbul and red-
billed blue magpie provided a high-quality dispersal ser-
vice. The perching frequencies of these birds were signif-
icantly correlated with seedling numbers (mountain
bulbul: r = 0.428, P = 0; y = 0.382 + 0.049x, R
2
=
0.544, df = 52, F = 60.799, P = 0.001; red-billed blue
magpie: r = 0.407, P = 0; y = 0.374 + 0.054x, R
2
=
0.486, df = 52, F = 48.277, P = 0.001; Fig. 2a, b).
In the botanical garden, the forager with the highest
visit frequency, the Chinese bulbul, had low dispersal
quality and its perching frequency was not signicantly
related to seedling numbers (r = 0.299, P = 0.064;
y = 0.9120.310x, R
2
= 0.096, df = 24, F = 2.440,
P = 0.072; Fig. 2d). In contrast, the red-billed blue
magpie was a high-quality disperser, as its perching
frequency was signicantly correlated with seedling
numbers (r = 0.702, P = 0.001; y = 0.755 + 0.164x,
R
2
= 0.480, df = 24, F = 21.236, P = 0; Fig. 2c).
Discussion
Seed dispersal system in the botanical garden and natu-
ral site
Establishment of seed dispersal system between ex situ
plants and local birds implies successful ex situ con-
servation. Previous studies suggest that it is easy for
bird-dispersed tree species to establish seed dispersal
system in new habitats (Aslan 2011; Magdalena et al.
2011). With regard to the Chinese yew, the ex situ
population surveyed in this study was able to attract
local birds to forage seeds and form a seed dispersal
system that included several avian dispersers (Table 2).
However, there were some dierences in the seed dis-
persal systems of the ex situ population and the natural
population.
Table 2 Frugivorous birds visiting Taxus chinensis in the botanical garden and natural site
Bird visitor Feeding pattern Visiting
frequency
Feeding amount
per visit
Feeding amount
per unit time
Natural site Botanical garden Natural site Botanical garden Natural site Botanical garden
Seed disperser
Pycnonotus sinensis S 406 5.1 1.3 20.7 13.3
Urocissa erythrorhyncha S 76 118 6.2 1.0 7.8 1.3 4.7 3.3 9.2 7.8
Cyanopica cyanus S 32 3.6 1.7 1.2 2.0
Zoothera dauma S 5 7 5.6 1.5 5.8 5.0 0.3 1.2 0.4 1.6
Hypsipetes maclellandii S 151 6.1 2.0 9.2 4.8
Hemixos castanonotus S 43 5.5 2.0 2.4 1.6
Dendrocitta formosae S 4 6.8 2.6 0.3 1.2
Pulp consumers
Tarsiger cyanurus P 13 1.5 1.0 0.2 1.2
Alcippe morrisonia P 31 3.5 1.0 1.1 1.2
Abroscopus albogularis P 30 5.1 1.0 1.5 1.4
Yuhina castaniceps P 3 1.5 1.6 0
Stachyris ruceps P 20 3.5 1.5 0.7 1.3
Total 324 576
S swallow, P peck. Seed dispersers are those birds that swallow entire fruits, defecating or regurgitating the seeds. Pulp consumers are
those species that peck the fruit pulp and discard the seed (Traveset, 1994). Unit time is an 8-h period starting at sunrise. Results are
presented as the mean SE. x, species not recorded at a site
Fig. 1 Distribution of 1-year-old seedlings and mother trees of Chinese yew (Taxus chinensis) in a natural site a and a botanical garden.
b Peaking values increase with the number of seedlings in the habitat cell. Green trees repesent mother trees (color gure online)
In both seed dispersal systems, Chinese yew popula-
tions established seed dispersal systems with birds of the
Pycnonotidae and Corvidae families (Table 2), similar to
those in the Chinese yew populations in Zhejing and Fu-
jiang (Li et al. 2014a, b). Stability of disperser species
facilitates the formation of seed dispersal mutualisms
(Bascompte and Jordano 2007). Moreover, Pycnonotidae
and Corvidae have a relatively wide distribution and a
relatively high degree of adaptability. These may be the
main reasons why the ex situ study population was suc-
cessfully established and may permit wider distribution of
Chinese yew populations (Gao 2006). Our results suggest
that disperser features should be considered before trans-
porting endangered plants to new habitats (Burns 2003).
Disperser composition and visiting frequency are pri-
marily aected by habitat structure and were dierent in
the two seed dispersal systems studied. In the botanical
garden, the forests consisted of articial plants with a
simple community structure, and there were relatively few
shrub species (Li and Yin. 2004; Lu et al. 2008). This
resulted in the absence of some frugivorous birds that
require a shrub layer (Table 1, Table S1). These birds
were therefore also missing from the seed dispersal system
of the ex situ population (Table 2). In contrast, there are
numerous broad-leaved, coniferous, and mixed forests in
the vicinity of the natural site. In addition, the natural site
has rich species diversity and the community structure is
complex (Deng et al. 2008). This attracted a greater
variety of frugivorous birds to the seed dispersal system in
the natural site than in the botanical garden (Table 2,
Table S1). However, the simple habitat structure of the
botanical garden did not disrupt the seed dispersal mu-
tualisms of the ex situ population. The visiting frequency
of disperser species was higher in the botanical garden
than in the natural habitat (t = 3.850, df = 2,
P = 0.001). Two factors may contribute to the high
frequency of visits in the botanical garden. First, the seed
removal rate might be higher in the structurally simple
habitat due to amplied fruit advertisement. This view is
supported by a study of wild cherry (Prunus avium L.)
(Breitbach et al. 2010). Second, in structurally complex
habits, the relatively high dominance of disperser species
may facilitate a high seed removal rate (Schupp et al.
2010). In the case of Chinese yew, more individuals of
frugivore species may have joined the seed dispersal sys-
tem of the ex situ population of plants (Table 1, Table 2,
Table S1), thereby increasing seed removal rate.
Eects of post-foraging behaviors of bird dispersers
on Chinese yew regeneration
After foraging, dispersers must decide how to move
between habitats and how to select habitats. These
Fig. 2 Post-foraging perching behaviors of two main avian
dispersers in a natural site (a, b) and a botanical garden (c,
d) and their spatial correlation with the number of Chinese yew
(Taxus chinensis) seedlings. The mountain bulbul Hypsipetes
maclellandii (a), red-billed blue magpie Urocissa erythrorhyncha
(b), red-billed blue magpie U. erythrorhyncha (c) and Chinese
bulbul Pycnonotus sinensis (d). Open circles repesent observed data;
black lines indicate the correlation between perching frequency and
seedling number; gray lines indicate the 95 % condence interval
decisions determine where seeds are deposited and,
consequently, aect the spatial patterns of 1-year-old
seedlings (Schupp et al. 2010). However, if the utilization
of habitat by avian dispersers is highly consistent with
the habitat that is suitable for plants, the dispersal e-
ciency of the birds is high (Breitbach et al. 2010; Schupp
et al. 2010).
In the case of Chinese yew, the seedling distribution
of ex situ populations and that of natural populations
reected a bird-dispersed pattern, but the aggregation
peaks of seedlings in the two types of habitat were dif-
ferent (Fig. 1). The seedling distribution in the two sites
was mainly inuenced by the post-foraging behaviors of
the seed dispersers (Fig. 2). In the natural site, most
foraging Pycnonotidae and Corvidae birds eciently
dispersed seeds to regeneration habitat (Fig. 2a, b);
disperser species from both families provided a good
seed distribution service for yew regeneration. Once
plants form a seed dispersal system with the primary
foragers at a natural site, they can easily regenerate be-
cause most of their seeds are dispersed (Loiselle et al.
2007; McConkey and Brockelman 2011; Bueno et al.
2013). However, trees in botanical gardens must depend
upon a dierent assemblage of avian vectors than those
in natural habitats. In the present study, the Chinese
bulbul was the primary forager in the botanical garden
(Table 2). However, after foraging, this species trans-
ported the majority of seeds to an unsuitable habitat for
regeneration (Fig. 2d), and is therefore an inecient
disperser. This suggests that in the botanical garden, the
Chinese bulbul is not a key disperser. On the other hand,
the red-billed blue magpie foraged less than the Chinese
bulbul in the botanical garden, but often used habitat
suitable for regeneration of the plants (Fig. 2c), thereby
facilitating plant regeneration in the botanical garden.
Seed dispersal systems in which the main disperser is a
low-quality disperser not only exist in botanical gardens
but also in natural sites, causing low regeneration rates
of plants and aecting the dynamics of plant commu-
nities (Sethi and Howe. 2009; Wotton and Kelly 2011).
Our results highlight the ability of the Chinese yew to
recruit seed dispersal agents in new habitats. However, if
the newly recruited species is a low-quality disperser, the
plants will depend more heavily on other avian vectors
for regeneration.
Acknowledgments We thank Bing Bai, Qiangjun Wang, and Yun-
feng Yin for their contributions in the eld, and three anonymous
reviewers for valuable comments. The study was supported by the
National Natural Science Foundation of China (No. 30970470),
the Priority Academic Program Development of Jiangsu Higher
Education Institutions, and Postgraduate Innovation Engineering
Fund of Jiangsu (CXZZ12_0548).
References
Altmann J (1974) Observational study of behavior: sampling
methods. behavior 69:227263
Aslan CE (2011) Implications of newly-formed seed-dispersal mu-
tualisms between birds and introduced plants in northern Cal-
ifornia, USA. Biol Invasions 13:28292845
Bacles CFE, Lowe AJ, Ennos RA (2010) Eective seed dispersal
across a fragmented landscape. Science 311(3):628
Bascompte J, JordanoP(2007) Plant-animal mutualistic networks: the
architecture of biodiversity. Ann Rev Ecol Evol Syst 38:567593
Breitbach N, Laube I, Stean-Dewenter I, Bohning-Gaese K
(2010) Bird diversity and seed dispersal along a human land-use
gradient: high seed removal in structurally simple farmland.
Oecologia 162:965976
Breitbach N, Bo hning-Gaese K, Laube I, Schleuning M (2012)
Short seed-dispersal distances and low seedling recruitment in
farmland populations of bird-dispersed cherry trees. J Ecol
100:13491358
Bueno RS, Guevara R, Ribeiro MC, Culot L, Bufalo FS et al
(2013) Functional redundancy and complementarities of seed
dispersal by the last Neotropical Megafrugivores. PLoS ONE
8(2):e56252. doi:10.1371/journal.pone.0056252
Burns KC (2003) Broad-scale reciprocity in an avian seed dispersal
mutualism. Global Ecol Biogeog 12:421426
Calvin o-Cancela M, Mart n-Herrero J (2009) Eectiveness of a
varied assemblage of seed dispersers of a eshy-fruited plant.
Ecology 90:35033515
Carnicer J, Jordano P, Melia n C (2009) The temporal dynamics of
resource use by frugivorous birds: a network approach. Ecology
90:19581970
Carroll SP, Fox CW (2008) Conservation biology evolution in
action. Oxford University Press, New York
Caughlin T, Wheeler JH, Jankowski J, Lichstein JW (2012)
Urbanized landscapes favored by g-eating birds increase
invasive but not native juvenile strangler g abundance. Ecol-
ogy 93:15711580
Cogni R (2010) Resistance to plant invasion? A native specialist
herbivore shows preference for and higher tness on an intro-
duced host. Biotropica 42:188193
Cruz JC, Ramos JA, da Silva LP, Tenreiro PQ, Heleno RH (2013)
Seed dispersal networks in an urban novel ecosystem. Eur J For
Res. doi:10.1007/s10342-013-0722-1
Deng QS, Zhu QQ, Lu CH (2008) Natural regeneration of Taxus
chinensis var. mairei and its seed dispersal by frugivorous birds.
Chin J Ecol 27:712717
Gao ZW (2006) Research on Taxus chinensis var. mairei. China
Forestry Publishing House, Beijing
Gil-Tena A, Saura AS, Brotons L (2007) Eects of forest compo-
sition and structure on bird species richness in a Mediterranean
context: implications for forest ecosystem management. Forest
Ecol Manage 242:470476
Gleditsch JM, Carlo T (2011) Fruit quantity of invasive shrubs
predicts the abundance of common native avian frugivores in
central Pennsylvania. Divers Distrib 17(2):244253
Gosper CR, Stansbury CD, Vivian-Smith G (2005) Seed dispersal
of eshy-fruited invasive plants by birds: contributing factors
and management options. Divers Distrib 11:549558
Guerrant EO, Havens K, Maunder M (2004) Ex situ plant con-
servation: supporting species survival in the wild. Island Press,
Washington, DC, p 536
Heleno RH, Olesen JM, Nogales M, Vargas P, Traveset A (2013)
Seed dispersal networks in the Gala pagos and the consequences
of alien plant invasions. Proc R Soc Lond B Biol. doi:
10.1098/rspb.2012.2112
Howe HF, Smallwood J (1982) Ecology of seed dispersal. Annu
Rev Ecol Syst 13(1):201228
Jordano P, Garc a C, Godoy JA, Garc a-Castan o JL (2007) Dif-
ferential contribution of frugivores to complex seed dispersal
patterns. Proc Natl Acad Sci USA 104:32783282
Li XH, Yin XM (2004) Seed dispersal by birds in Nanjing
Botanical Garden Mem. Sun Yat.-Sen in spring and summer.
Acta Ecol Sin 24(7):14521458
Li XK, Huang YQ, Su ZM (2000) Distribution pattern and its
dynamics of Taxus chinensis var. mairei population on Yun-
baoshan Mountain. Chin J Appl Ecol 11:169172
Li N, Bai B, Wang Z, Luo F, Lu XZ, Lu CH (2014a) Avian seed
dispersal and seedling distribution of the endangered tree spe-
cies, Taxus chinensis, in patchy habitats. Plant Ecol Divers. doi:
10.1080/17550874.2014.898165
Li N, Wang Z, Lu CH, Xiong TS, Fu WY, Wu JP (2014b) Seed
foraging and dispersal of Chinese yew (Taxus chinensis var.
mairei) by frugivorous birds within patchy habitats. Acta Ecol
Sin 34(7):16811689
Loiselle BA, Blendinger PG, Blake JG, Ryder TB (2007) Ecological
redundancy in seed dispersal systems: a comparison between
manakins (Aves: Pipridae) in two tropical forests. In: Dennis
AJ, Schupp EW, Green RJ, Westcott DA (eds) Seed dispersal:
theory and its application in a changing world. CABI, Wal-
lingford, pp 178195
Lu CH, Zhu QQ, Deng QS (2008) Eect of frugivorous birds on
the establishment of a naturally regenerating population of
Chinese yew in ex situ conservation. Integr Zool 3:186193
Magdalena L, Piotr S, Knops JMH, Moron D, Stanislaw T,
Woyciechowski M (2011) Plant establishment and invasions an
increase in a seed disperser combined with land abandonment
causes an invasion of the non-native walnut in Europe. Proc R
Soc Lond B Biol 279:14911497
Magurran AE (1988) Ecological Diversity and its Measurement.
Princeton University Press, Princeton
Maunder M (1992) Plant reintroduction: an overview. Biodivers
Conserv 1:5161
McConkey KR, Brockelman WY (2011) Nonredundancy in the
dispersal network of a generalist tropical forest tree. Ecology
92:14921502
Morales JM, Garc a D, Mart nez D, Rodr guez-Pe rez J, Herrera
JM (2013) Frugivore behavioural details matter for seed dis-
persal: a multi-species model for Cantabrian thrushes and trees.
PLoS ONE 6:e65216. doi:10.1371/journal.pone.0065216
Puerta-Pin ero C, Pino J, Go mez JM (2012) Direct and indirect
landscape eects on Quercus ilex regeneration in heterogeneous
environments. Oecologia 170:10091020
Quinn GP, Keough MJ (2002) Experimental design and data
analysis for biologists. Cambridge University Press, Cambridge
Schupp EW, Jordano P, Go mez JM (2010) Seed dispersal eec-
tiveness revisited: a conceptual review. New Phytol 188:333353
Sethi P, Howe HF (2009) Recruitment of hornbill-dispersed trees in
hunted and logged forests of the Indian Eastern Himalaya.
Conserv Biol 23(3):710718
Spiegel O, Nathan R (2007) Incorporating dispersal distance into
the disperser eectiveness framework: frugivorous birds provide
complementary dispersal to plants in a patchy environment.
Ecol Lett 10:718728
Sutherland WJ, Newton I, Green RE (2004) Bird ecology and
conservation: a handbook of techniques. Oxford University
Press, Oxford
Thomas P, Li N, Christian T (2013) Taxus chinensis. In: IUCN
2013. IUCN red list of threatened species. Version 2013.1.
http://www.iucnredlist.org. Downloaded 27 Aug 2013
Traveset A (1994) Inuence of type of avian frugivory on the tness
of Pistacia terebinthus L. Evol Ecol 8:618627
Wotton DM, Kelly D (2011) Frugivore loss limits recruitment of
large-seeded trees. Proc R Soc Lond B Biol 278:33453354