Urban Forestry & Urban Greening 64 (2021) 127245

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Urban Forestry & Urban Greening

journal homepage: www.elsevier.com/locate/ufug

Functional traits change but species diversity is not influenced by edge

effects in an urban forest of Eastern China
Chao Jin a, b, Bo Jiang a, Yi Ding c, Shaozong Yang a, Yue Xu c, Jiejie Jiao a, Jihong Huang c,
Weigao Yuan a, Chuping Wu a, *
a
Zhejiang Academy of Forestry, Hangzhou, 310023, China
b
School of Forestry and Biotechnology, Zhejiang Agriculture and Forestry University, Hangzhou 311300, China
c
Research Institute of Forest Ecology, Environment and Protection, Chinese Academy of Forest, Key Laboratory of Forest Ecology and Environment of National Forestry
and Grassland Administration, Beijing 100091, China

A R T I C L E I N F O A B S T R A C T

Handling Editor: Richard Hauer Forest edges have significant effects on plant species and trait compositions. However, most current studies on
edge effects are based on natural forests, and studies on edge effects in urban forests are still limited. Here, we set
Keywords: up 50 survey plots in Wuchao Mountain National Forest Park, an urban forest of Hangzhou, China. We tested
Edge effect how species composition changed with distance from the forest edge. Specifically, we investigated dispersal-
Urban forest
related traits for 86 species, and analyzed trait composition changes with distance from the forest edge. The
Mammals
NMDS analysis revealed a significant difference in species composition between forest edge and interior, but
Birds
Plant abundance species richness and functional diversity remain unchanged. However, single traits showed higher divergence
Seed dispersal than expected. The percentage of fleshy-fruited species declined with distance from the edge, but plant abun­
Seed mass dance of mammal-dispersed and animal-dispersal seed mass was increased. The different trend in seed size of
Functional traits different dispersal mode and seed mass from edge to the interior within the community may be related to the loss
Functional diversity of mammal-dispersed plant species at the forest edge. This suggests that edge effects have a high influence on
functional traits in urban forests, but not on species diversity. Edges had significant effects on animal-dispersed
species and trait composition of plant communities. Our study highlights the importance of maintaining forest
integrity by protecting interior habitats in urban regions. We also recommend reducing the creation of new edges
and increasing the buffer area for biodiversity conservation.

1. Introduction
More than half of the global forested areas in the world are influ­
enced by edge effect (Haddad et al., 2015). Changes in microclimate,
energy flows and biological interaction at the forest edges can result in
the loss of species that are vulnerable to edge environment (Razafin­
dratsima et al., 2017; Liu et al., 2019a; Hawes et al., 2020), which can
influence species composition, reduce biodiversity, and alter ecosystem
function (Anderson et al., 2003; Deal et al., 2014; Razafindratsima et al.,
2017; Smith et al., 2018). In urban areas, forests are mainly small
fragments divided by roads, or recreational use (Lehvavirta et al., 2014).
With the decreasing of forest areas and increasing disturbance at the
forest edges, edge effects can occur more critically in urban forests
(Guerra et al., 2017; Razafindratsima et al., 2017).
On account of accelerating urbanization and increasing interference
with human activities, urban forests may experience different causes of
edge effects compared to natural forests (Latimer and Zuckerberg, 2016;
Vakhlamova et al., 2016; Haddock et al., 2019; Meili et al., 2020). At
habitat edge, increased artificial light at night may result in the reduc­
tion of available habitat areas and wildlife corridors, which can affect
functional connectivity of local species (Haddock et al., 2019). There are
a variety of human activities in urban forests, such as recreation, exer­
cise, and climbing (Basu and Nagendra, 2020), thus a study found that
edge effects in urban forest have a positive influence on the regeneration
of some deciduous trees, but especially have direct effects of trampling
on all species (Lehvavirta et al., 2014). The effect arising from edge
habitat represents the interaction of urban environment and organism.
Although forest specialists, such as animal-dispersed large-seed species,
are generally replaced by ubiquitous species or pioneer tree species
(small-seed tree species) as a result of lack of specialist seed dispersers

* Corresponding author.
E-mail address: wcp1117@hotmail.com (C. Wu).

https://doi.org/10.1016/j.ufug.2021.127245
Received 27 March 2021; Received in revised form 24 May 2021; Accepted 1 July 2021
Available online 7 July 2021
1618-8667/© 2021 Elsevier GmbH. All rights reserved.
C. Jin et al.
and increasing non-animal-dispersed plants at the natural forest edge
(Liu et al., 2019a), few studies investigated this in urban forests.
Functional traits, such as traits related to dispersal and productivity,
can be used to evaluate plant ability to survive and colonize in a specific
environmental condition (Asanok et al., 2013). For example, seed and
fruit traits related to plant dispersal ability are important determinants
of animal-plant interactions, evaluating resource availability (McKin­
ney, 2006; Galetti et al., 2013). And, there is growing evidence that seed
size and fruit type of species can respond to edge effects (Ewers and
Didham, 2006; Magnago et al., 2014; Razafindratsima et al., 2017).
Moreover, the decreasing number of large frugivorous dispersers at
forest edges limit the regeneration and reproduction of counterpart
plants (Laurance et al., 2006; Magnago et al., 2014). As for productive
traits, characterizing the traits such as potential maximum height, leaf
traits and wood density can reflect plant competition ability and phys­
iological responses to environmental changes (Bolmgren and Eriksson,
2005; Girão et al., 2007; Moran and Catterall, 2010; Ding et al., 2012;
Lasky et al., 2013). For instance, specific leaf area has been found to
decrease in highly disturbance sites, such as forest edge (Ding et al.,
2012; Wright et al., 2013). Besides, some studies have suggested that
due to habitat destruction, forest specialists or late-successional species
would be replaced by pioneer species, with low wood density (Girão
et al., 2007; Tabarelli et al., 2010). Assessing differences of dispersal and
productive traits along edge-to-interior gradients can provide more in­
formation about understanding patterns of species composition of urban
forests in the face of edge effect (Oliveira et al., 2004; Hawes et al.,
2020).
Functional diversity, functional trait-based analysis, have been
widely used to evaluate the effects of habitat fragmentation on plant
community (Magnago et al., 2014; Haddock et al., 2019), changes in
that metric resulting from edge disturbance may have implications
about species composition in response to ecosystem functioning and
environment change (Moran and Catterall, 2010; Razafindratsima et al.,
2017; Liu et al., 2020). A study comparing taxonomic diversity and
functional diversity suggested that significant edge effects on species
community were showed by using functional diversity (Magura, 2017).
For example, edge effects can intensify environmental filtering or
weaken biological interactions (Guerra et al., 2017), and the community
would become functionally more convergent (Razafindratsima et al.,
2017; Liu et al., 2019a). Thus, these changes may mirror in urban forests
edges where functionally similar species tend to increase over time (Ben
et al., 2017).
The plant community structure of urban forests is directly affected by
their surrounding habitats, and this effect may be amplified by the plant-
animal feedback mechanism (Razafindratsima et al., 2017; d’Albertas
et al., 2018). In this regard, the assessment of dispersal and productive
traits is an effective approach to explore edge effects of urban forests,
and urban forests can be managed and restored with experimental re­
sults and policy interventions. In this study, we investigated edge effects
on plant community composition and functional diversity in an urban
forest. Specifically, we aim to answer two questions: 1) do species
composition and taxonomic diversity change from the edge to the
interior of urban forest? 2) do dispersal- and productive-related plant
traits respond to edge-to-interior gradient? We hypothesized that urban
forest should show an increasing tendency of functional diversity and
shifts in functions related to dispersal towards species with traits, such as
animal dispersion, fleshy-fruited and large seed, in edge-to-interior
gradient.
2. Material and methods
2.1. Study area
Wuchao Mountain National Forest Park (WMNFP) of Eastern China
(33◦ 41′ N, 120◦ 00′ E) is located in the western suburb of Hangzhou,
Zhejiang Province, China, with a total area of 5.22 km2, of which 93 % is
2
Urban Forestry & Urban Greening 64 (2021) 127245
covered by forest. This area experienced a subtropical climate with an
average annual temperature of 16.1℃, and a monthly average temper­
ature of 3.6℃ in the coldest month. The annual rainfall is 1400.7 mm,
with the maximum rainfall in summer. Our study region in WMNFP
covers an area of 222.7 ha with an elevation of 264–514 m. The original
vegetation in the forest of Wuchao Mountain is an evergreen broad-leaf
forest, which has been clear-cut before 1945. In 1960, the evergreen
secondary broad-leaf forest with Schima superba as the dominant species
has been formed by the way of natural regeneration since closing off
hillsides for forest reservation. Since WMNFP opened to urban residents
in 1992, human activities such as climbing, logging and hunting began
to affect the restoration of forests (Liu et al., 1983). The large area and
history of Wuchao Mountain forest contribute to a suitable edge-interior
gradient for us to study the edge effect on urban forests.
2.2. Tree sampling
According to previous studies on edge effects, most abiotic and biotic
edge parameters have an influence depth of less than 300 m (Laurance
et al., 2002). Therefore, we took 300 m from the forest edge as the
median and set a list of sampling plots at a random distance with average
8 m intervals between neighbouring plots. Fifty plots of 20 × 20 m (116
m–514 m with the center of the plot from forest edge) were established
on the north of the forest area. This survey area was chosen because it
was covered with secondary broad-leaf forest, and plots were located at
similar altitudes (243.1 m–375.2 m; Table S1) and with soil conditions
(red earth). We used ArcGIS 9.3 to calculate the shortest distance from
the sample plot to the forest edge. Forest boundaries of Wuchao
Mountain were characterized by hard edges, with no successional
gradient and hard paths in our study area. The non-forest matrix
adjoining Wuchao Mountain mainly consisted of the construction of
small-scale cities, including roads, schools and residential houses. Such a
landscape has gradually begun to take shape for 24 years since WMNFP
was established in 1992. Boundaries of WMNFP have been initially
designed as tourist areas without strict banning of wood theft and
hunting, forming edge-to-interior gradients of human activity intensity.
Our survey plots were established in accordance with the principles of
the Center for Tropical Forest Science (CTFS) (Richard, 1998). Within
plots, all living woody plants with a diameter at breast height (DBH; 1.3
m above ground) ≥ 1 cm were investigated and included in our analysis.
2.3. Traits collection
In this study, plant functional traits related to seed dispersal and
productivity were collected, including fruit type, seed mass, seed size,
seed dispersal mode, tree potential maximum height, specific leaf area
(SLA), leaf area (LA), leaf dry matter content (LDMC), leaf chlorophyll
content (ChL), wood density (WD), and plant life form (Table 1).
Fruit type was characterized as fleshy fruits (Coombe, 1976) and
non-fleshy fruits. Previous studies have shown that seeds of
Table 1
Traits used to measure tree functional diversity.
Trait Ranges, categories
Dispersal traits
Fruit type Fleshy, non-fleshy
Seed mass 0.00002− 2.20000 g
Dispersal mode Mammal, bird, non-animal,
Seed size Small: <5 mm, medium: 5− 10 mm, large: >10 mm
Productive traits
Potential maximum height 1.5− 35.0 m
Wood density 0.28− 0.90 g/cm3
Specific leaf area 74.23− 462.54 cm2/g
Leaf area 5.35− 281.69 cm2
Leaf dry matter content 0.17− 0.60 g/g
Chlorophyll content 33.50− 73.57 mg/g
Life form Tree, shrub, tree or shrub
C. Jin et al.
fleshy-fruited plants are mainly dispersed by frugivorous animals
including birds and mammals (Fleming and Kress, 2011; Masaki et al.,
2012). Data of fruit type was obtained from the online database of Flora
of China (http://frps.iplant.cn), and data of species that are not available
online were acquired by referring to literature or field observation (Du
et al., 2009; Liu et al., 2019b).
Seed mass and seed size have been widely used to reflect animal-
plant interaction (Chen and Moles, 2015; Liu et al., 2019b). And
community-weighted mean (CWM) of seed mass is an important indi­
cator parameter reflecting ecosystem functions (Osuri and Sankaran,
2016). Specifically, the mean seed mass value in each sampled plot is
calculated by averaging the weight of seed mass of all sampled in­
dividuals. Seed size is divided into three categorical types: small, me­
dium, and large (Table 1). Seed mass and seed size of all sampled plant
species were obtained from the Kew Seed Information Database (http:
//data.kew.org/sid/), the Institute of Botany (IB), and literature
(Table S2). For species that seed mass and seed size data was not
available, the genus average value from the Kew Seed Information
Database was used.
Seed dispersal mode was first divided into animal-dispersed (i.e.,
fleshy fruits) and non-animal-dispersed (i.e., seeds or fruits have struc­
tures such as wings or hairs, and seeds that are dispersed by gravity or
cracking) (Du et al., 2009). As for animal-dispersed species, we further
classified them into two groups: bird-dispersed and mammal-dispersed
according to literature recording, field observation, and expert consul­
tation (Table S3) (Chen and Moles, 2015).
In addition to dispersal traits, tree potential maximum height and
plant life form (tree, shrub, and tree or shrub species) were corrected
based on the data from the Flora of China. As for leaf traits, we sampled
3–5 leaves per species from 10 individuals (≥ 10 cm in DBH) of each
species. Then, leaf fresh weight and LA were measured using an elec­
tronic balance, LI-6400 portable photosynthesis measurement system
(LI-6400, Li-Cor, Lincoln, NE, USA), and ChL was measured with a
chlorophyll meter (SPAD 502 Plus Meter, Konica Minolta, Japan). Then,
leaves were collected back to laboratory, oven-dried at 65 ◦ C for 48 h to
a constant weight to obtain leaf dry weight. And SLA was calculated as
LA per leaf dry weight. Wood density was determined for branches,
which was calculated as dry weight per fresh volume. Wood samples
were oven dried at 103 ◦ C for 72 h. Every continuous productive trait
was analyzed using averaged parameters of each sample. For uncol­
lected data, the wood density of morphospecies was either collected
through literature or only identified to family or genus level (Table S2).
Only 10 species (11.6 %) and 127 stems (1.3 %) were unmeasured in
terms of leaf traits (Table S5), and only 3 species (3.4 %) and 47 stems
(0.5 %) uncollected for wood density. These species were excluded in
the calculation of functional diversity.
2.4. Data analysis
For each community, we calculated species richness and plant
abundance to represent the composition of species. We also examined
species distribution of community composition in edge-to-interior
gradient using non-metric multidimensional scaling (NMDS). Then, we
used results from NMDS analysis as the evaluation of community
structure (Barlow et al., 2010; Magnago et al., 2014). The NMDS anal­
ysis was performed using the Vegan package (ver.2.4–6) in R 3.6.0
(Oksanen et al., 2018).
For functional diversity, we focused on the parameter of functional
dispersion (FDis) of dispersal- and productive-related traits, which has
been used to indicate the degree of variation of multiple plant functional
traits in the community. FDis is defined as the mean distance of each
coexisting species in the multidimensional trait space to the community
center (Villeger et al., 2008), and it can be used to estimate the dispersal
of a community of species in trait space. High FDis values represent high
trait divergence in the community. It is structurally independent of
species richness, and the problem of redundant comparisons can be
3
Urban Forestry & Urban Greening 64 (2021) 127245
avoided by comparing a single functional diversity index (Laliberté and
Legendre, 2010). Also, we calculated community-level weighted mean
(CWM) for each continuous trait, which estimated the most probable
attribute that a species drawn at random from a community would
display (Swenson, 2014). It was calculated as:
∑
n
CWM = Pi traiti
i=1
where pi and traiti means, respectively, the relative abundance and the
trait value of species i and n presents the total number of species. For
estimating the divergence of four categorical traits (i.e., fruit type, seed
size, dispersal mode, and plant life form), we calculated species richness,
plant abundance and percentage of individuals. The percentage of in­
dividuals can reduce the difference in abundance across the edge-to-
interior gradient, we calculated the percentage of stems per plot in
each categorical trait. The functional diversity index was calculated by
using the ‘FD’ package (ver.1.0–12) (Laliberté et al., 2014).
To assess variation in species diversity and functional diversity along
the edge-to-interior gradient, we used linear mixed model with the
‘nlme’ package (ver.3.1–118) (Pinheiro et al., 2014). In the model, the
only explanatory variable was the distance from plot center to the
nearest edge (defined as the straight-line distance). Similarly, to assess
variation in each dispersal- and productive-related trait, we used a linear
mixed model for CWM each continuous trait and species richness, plant
abundance, and percentage of individuals of categorical traits. To ac­
count for potential spatial autocorrelation, longitude and latitude were
taken as a random effect in the model. Specifically, we used
community-weighted mean seed mass based on the plant abundance for
different dispersal modes as our comprehensive proxy for testing the
influence of edge effect on seed dispersal. The statistically significant
model interpretation (R2) was calculated in the ‘MuMIn’ package
(Bartoń and Anderson, 2016). These data were analyzed in R 3.6.0
(Team, 2019).
3. Results
3.1. Species composition and community
We have sampled in total of 9366 trees (≥ 1 cm DBH) in 50 forest
plots, including 86 species from 54 genera in 32 family (Table S2). The
dominant species was Schima superba (n = 703; 7.5 % of total abun­
dance) and Cyclobalanopsis glauca (n = 476; 5.1 % of total abundance).
Plant abundance increased from the forest edge to the interior (n = 50,
R2 = 0.11, P = 0.02, Fig. 1a), but species richness basically kept un­
changed (n = 50, P > 0.50, Fig. S3). NMDS analysis results of species
composition of community structure indicated that best dimensionality
used to represent the data was axis 1, 2, and 3 (Stress = 0.17; Fig. S7).
Linear mixed models reveal that axis 1 (n = 50, R2 = 0.27, P < 0.001), 2
(n = 50, R2 = 0.14, P = 0.016), and 3 (n = 50, R2 = 0.16, P = 0.011) of
community structure were significantly influenced by forest edge.
3.2. Functional composition and diversity
The value of FDis of dispersal (P = 0.08) or productive (P = 0.30)
traits was not significantly changed along edge-to-interior gradient
(Fig. S1). For the CMW of traits exhibiting particular trait attribute, we
find that forest edge had a larger effect on seed mass, LDMC and WD
(Fig. S2). Proximity to forest edge had a significant negative influence on
community-weighted seed mass, with a similar effect on the species
richness, abundance and percentage of large seed individuals (Figs.S3,
S4 and S5). In terms of dispersal mode, seed dispersal by birds is the
main dispersal mode (4600; 49.1 %), followed by mammal dispersal
(2565; 27.4 %) and non-animal dispersal (2201; 23.5 %), and the per­
centage of animal dispersal including birds and mammal exceeded 70 %
in most sample plots (Fig. 1b). The percentage of fleshy fruit individuals
C. Jin et al. Urban Forestry & Urban Greening 64 (2021) 127245

Fig. 1. Community status of Wuchao Mountain forest. Here we show (a) the effect of distance from forest edge on total plant abundance; (b) proportion of in­
dividuals with dispersal modes.

decreased from forest edge to the interior (n = 50, R2 = 0.1, P = 0.027;
Fig. 2a). The abundance of mammal-dispersed plants increased with
distance from the edge (n = 50, R2 = 0.19, P = 0.001; Fig. 2b), but the
abundance of bird-dispersed and non-animal-dispersed plants basically
kept unchanged. Community-weighted mean seed mass of different
dispersal mode as an overall indicator of edge effect was significantly
influenced by forest edge. Seed mass of bird-dispersed species was
significantly smaller than that of mammal-dispersed species (t test: t =
− 98.486, P < 0.001, Table S6).
Overall, the community-weighted value of seed mass was signifi­
cantly lower at the forest edges than that in the interior (R2 = 0.20, P =
0.001), while bird-dispersed seed mass increased with distance from the
edge (R2 = 0.10, P = 0.02; Fig. 3b), and the mammal-dispersed seed
mass increased with distance from the edge (R2 = 0.3, P < 0.001;
Fig. 3c).
4. Discussion
Our results show that edge effect has little influence on species di­
versity, but there are significant changes in functional trait compositions
along forest edges to the interiors in an urban forest of Eastern China. In
particular, our study indicates that edge effects in urban forests can lead
to a lower proportion of mammal-dispersed plants in the community,
and the forest edge features a significant shift to small-sized species with
small seed.
4.1. Responses of urban forest biodiversity to edge effects
In Wuchao Mountain, we found that distance from forest edge had a
significant positive effect on plant abundance in tree communities, and
forest edge was dominated by small-seeded and fleshy-fruited species

Fig. 2. Graphs of effect of plant traits and forest edge. Here we show (a) the effect of habitat on proportion of fleshy fruit species; (b) the effect of habitat on
abundance of mammal-dispersal species; (c) the effect of habitat on percentage of individuals of mammal-dispersal species.

4
C. Jin et al.
Fig. 3. Relationships between distance from edge and community-weighted mean seed mass with different dispersal types. Here we show (a) community-weighted
mean seed mass of all species in response to distance from forest edge; (b) community-weighted mean seed mass of bird-dispersed in response to distance from forest
edge; (c) community-weighted mean seed mass of mammal-dispersed in response to distance from forest edge; (d) community-weighted mean seed mass of non-
animal-dispersed in response to distance from forest edge.
that lack mammal-dispersed species compared to forest interiors (Fig. S5
I). It is remarkable that forest edge had a higher percentage of fleshy-
fruited species, but lower mammal-dispersed species, which may
result from the screening of human-driven conditions at forest edge
(Swenson and Enquist, 2009; Der Plas et al., 2012). These changes may
be caused by a variety of factors, for example, intensive human activities
at forest edges (such as climbing and outdoor activities) may reduce the
seed dispersal activity by large birds and mammals (McAlpine et al.,
2006; Lander and Brunson, 2018). Meanwhile, following changes in
wind speed, temperature, low humidity (Laurance et al., 2002, 2011)
and other abiotic factors can gradually change specific seed dispersal
modes (Hawes et al., 2020). This pattern may also be affected by land­
scape configuration and connectivity (Brudvig et al., 2009), as internal
species and substrate species (edge-preferring species) coexist in the
edge habitat, and the resulting ecotone has higher species richness
(Magura, 2002).
In our study, edge effects in urban forests on biodiversity show
similar to previous studies in natural parks (Oliveira et al., 2004). For
example, a study on the edge effect in the Ranomafana National Park in
southeastern Madagascar shows that species richness is not significantly
different between forest edge and interior, which is similar to our results
about species richness from the forest edge to interior. In contrast, plant
abundance on the forest edge of Wuchao Mountain was smaller than the
interior. It may be due to the large forest area of Wuchao Mountain
(distance from the forest edge to the interior is more than 300 m), and
the influence of small-scale human activities at the forest edge (low-­
density wood theft and logging) has a selective effect on the urban forest
edge (Poulsen et al., 2011). In addition, trees species favor edge envi­
ronment may make up for the loss of species that cannot persist near the
5
Urban Forestry & Urban Greening 64 (2021) 127245
edge (Hella Schlinkert et al., 2016). However, contrary to our hypoth­
esis, the functional diversity measures of dispersal (P = 0.08) and pro­
ductive (P = 0.31) traits showed that edge effects have no significant
impact on the composition of functional traits of forest species, showing
different results compared to previous studies (Magnago et al., 2014;
Razafindratsima et al., 2017; Haddock et al., 2019). Functional disper­
sion describes the degree of difference between the positions of species
combinations in the functional and trait space of species (Laliberté and
Legendre, 2010). Our results suggest that plant functional diversity is
not significantly influenced by environmental changes from the forest
edge to the interior. A recent study showed that a single functional trait
can explain fitness (Kraft et al., 2015), and significant changes of
dispersal-related traits may be a result of differences in seed dispersers
from the forest edge to interior. For example, due to the loss of frugiv­
orous mammals in edge habitats, the regeneration of plant species rely
on these disperses, which usually have large seeds, may become difficult
and result in rapid population declines (Moran and Catterall, 2010;
Kurten et al., 2015).
4.2. Response of plant functional traits to edges in urban forests
Our results show that edge effects have led to a shift in dispersal
modes, seed traits and leaf traits in woody plant communities of urban
forests. In our study, mammal-dispersed species but not bird-dispersed
species showed prominent response to edge effects, which can be
explained by three reasons. First, forest edges are usually the activity
boundary of large mammals (Tuff et al., 2016; Boesing et al., 2017), and
effective dispersal of large mammals may be limited by edge effects. The
lack of large mammals restricts the dispersal of large-seed frugivorous
C. Jin et al.
species, increases the spatial aggregation of seedlings, and the
density-dependent mortality (Harrison et al., 2013; Caughlin et al.,
2014), which hinders the effective regeneration of species depending on
mammal for seed dispersal. In this way, a negative cycle may be
generated between the animal and plant communities, resulting in a low
balance of ecosystem functions. Second, small rodents consumed plant
seeds, and the activities of small mammals keep unchanged with dis­
tance from the forest edge, resulting in a higher proportion of
fleshy-fruited species at the forest edge (Hella Schlinkert et al., 2016).
Small rodents such as Iviventer sp. eat and store Fagaceae seeds such as
Castanopsis sclerophylla and Lithocarpus glaber (Tuff et al., 2016). Third,
part of the gap caused by the lack of large mammals is balanced by bird
dispersal. Our analysis of seed mass suggests that forest edges are suit­
able habits for birds because the forest edge is dominated by
small-seeded species (Fig. S2 G) and seed mass of bird-dispersal species
was significantly lighter than mammals (Table S6). Seed dispersal effi­
ciency of birds that prefer ecotone between adjacent forest, and
non-animal dispersal efficiency are higher than large mammals in edge
habitats. And thus, it can offer potential opportunities for balancing the
lack of key seed dispersing agency (Laurance, 2004; Cramer et al., 2007;
Neuschulz et al., 2013; Tuff et al., 2016; Boesing et al., 2017). This re­
lates to the ecological habits of birds that can move in different forest
communities and disperse plant seeds (Garcia et al., 2010; Heleno and
Vargas, 2015), and bird-dispersed small-seed plants can rapidly survive
in the edge habitats (Marinés et al., 2014). Furthermore, there are more
environmentally sensitive bird species in less urbanized areas, while
environmental tolerant bird species have increased with urbanization
gradient (Pinho et al., 2016). Compared to mammals, birds have certain
anti-interference capacities to varied habitat conditions. For example,
studies have found that bird communities in the Eastern Cape of South
Africa do not differ in diversity in deforested areas and non-disturbed
areas (Leaver et al., 2019), but some birds have a low environmental
tolerance and the demand for microenvironment and predation so that
they will keep away from forest edges (Lindell et al., 2004).
The results of seed dispersal become complicated due to the potential
trophic level and the relative effectiveness of seed dispersers among
different plants (Schupp et al., 2010). For example, small mammals tend
to eat plant seeds (Wright et al., 2000; Fricke et al., 2016). Specifically,
Castanopsis fargesii seeds are often eaten by rodents, so that small seeds
can rarely escape the bite of rodents (Galetti et al., 2015). The key to
explaining edge effects for seed dispersal is to figure out the multiple
interactions between plants and animals. Although a simple definition of
the seed dispersal mode can help understand the impact of edge effects
on species, due to the complex fruit-frugivorous animal relationship
(Hughes et al., 1994; Bascompte and Jordano, 2007), and the lack of
information on effective seed dispersal (Howe, 2016), studying
ecosystem functions by seed dispersal modes remains challenging.
Leaf traits have been used to analyze the response of plants to ur­
banization. For example, previous studies have shown that species had
higher SLA in urban forests with less fertile soils, while rural trees in
fertile soils had higher LDMC (Song et al., 2019). Similarly, we found
that LDMC significantly increased from the forest edge to interior, but
SLA did not change. As such, leaf functional traits may explain and
predict changes in community changes in urban environments.
5. Conclusion
Our results demonstrate that edge effects can lead to the loss of urban
forest diversity and change their functional trait composition. Plant
communities at edge habitats develop towards small-seed species. Spe­
cifically, the dispersal of seeds of large-seed species by animals is largely
changed. In light of these characteristics, we suggest more attention
should be paid to the protection of mammal species and birds living in
urban forests. Our results can provide suggestions for ecological resto­
ration and maintenance of urban ecosystems. For example, the abun­
dance of mammal-dispersed tree species is significantly smaller at the
6
Urban Forestry & Urban Greening 64 (2021) 127245
forest edge than in the interior. Moreover, artificial replanting near
forest edges can reduce the impact of human disturbances such as wood
theft and logging. In addition, plants with animal-dispersed seeds are
currently being disturbed due to declining animal populations. The
control of hunting behavior or the establishment of wildlife conservation
sites (Bicknell et al., 2015) can help maintain forest ecosystems in a
more integrated way. At last, we suggest that the biodiversity of the city
can be conserved by increasing the area of ecological corridors and
habitat patches (Beninde et al., 2015). Urban forest continuity should be
a priority in the development of forest recreation because ecological
corridors are the form of protection for animal movement and plant
dispersion. Urban park planners need to design roads for both animals
and humans. Thus, the benefit of both has remained.
Authorship contribution statement
Chao Jin: Writing - original draft, Writing - review & editing,
Visualization. Chuping Wu: Conceptualization, Methodology, Writing -
review & editing, investigation, Validation, Supervision. Bo Jiang:
Investigation. Yi Ding: Investigation. Shaozong Yang: Investigation.
Yue Xu: Investigation. Jiejie Jiao: Investigation. Jihong Huang: Data
curation. Weigao Yuan: Investigation.
Funding
This work was supported by the Project of Zhejiang Province
[2020F1065-5], the Major Collaborative Project between Zhejiang
Province and the Chinese Academy of Forestry [2019SY08], and Zhe­
jiang Hangzhou Urban Forest Ecosystem Research Station.
Declaration of Competing Interest
The authors report no declarations of interest.
Acknowledgements
We thank professor Jiajia Liu and Dr. Shilu Zheng from Fudan Uni­
versity for their writing guidance and constructive comments. We thank
Lijia You, Hong Chen and Qing Ren for helpful suggestions and grammar
guidence on initial drafts of this paper. We would also like to thank
Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sci­
ences for organizing the “Scientific Paper Writing: XTBG Advanced
Workshop”, taught by Professor Richard Corlett from 8 to 12 July 2020,
during the workshop this paper was improved significantly.
Appendix A. Supplementary data
Supplementary material related to this article can be found, in the
online version, at doi:https://doi.org/10.1016/j.ufug.2021.127245.
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