The impact of urbanization on avian communities during the breeding
season in the Huanghuai Plain of China
Meiting Liu1, Jiayi Shi1, Ziruo
Zhang1, Xinyi Zhang2, Xiaohan
Li2, Ruohui Tang1, Chunna
Zhang2, Siyu Wu2, Chenfang
Wu2, Junpo Zhu2, Zhirong
He2, Yujia Sun2, Yuehuan
Wang3, Supen Wang2*, Na
Zhao2*
1 Collaborative Innovation Center of Recovery and
Reconstruction of Degraded Ecosystem in Wanjiang Basin Co-founded by
Anhui Province and Ministry of Education, College of Ecology and
Environment, Anhui Normal University, Wuhu, China |2 The Anhui Provincial Key Laboratory of Biodiversity
Conservation and Ecological Security in the Yangtze River Basin, College
of Life Science, Anhui Normal University, Wuhu, China |3 College of Life Sciences, Nanjing Agricultural
University, Nanjing, China
Correspondence: Na Zhao
(nazhao2007@163.com)
| Supen Wang
(frog2019@ahnu.edu.cn)
Funding: This study was supported by the Beijing Municipal Natural
Science Foundation (5252015), China Postdoctoral Science Foundation
funded project (2022M723135) and National Key Research and Development
Program of China (2024YFC2607500).
Abstract: The noise pollution, habitat loss and human
disturbance caused by urbanization have led to damage in bird
communities. Research on the relationship between urbanization and birds
predominantly focuses on highly urbanized areas, with few studies in
underdeveloped urbanized areas. Given the greater stability of the bird
community during breeding season, it was chosen for this study. Here, we
conducted bird surveys along the urban-rural continuum by utilizing 150
line transects within a 51385 km2 area from June to
August in 2022 and 2023, aiming to explore the impact of urbanization on
bird species diversity and functional traits during the breeding season
in the Huanghuai Plain of China. We found that species diversity and
functional traits had significant differences among three habitats
(i.e., urban, suburban, and rural). Additionally, the urbanization
synthetic index had significant negative correlations with species
richness and Shannon-Wiener index, while had no significant correlation
with functional traits. We then assessed that the environmental noise,
the distance to the county center, and the proportion of building area
within a 250-meter radius were critical factors affecting species
diversity, as well as environmental noise and the distance to the county
center were best predictors for functional traits. Urban birds preferred
to construct nests at crown, and the diets of them tended to be
omnivorous. Our study highlights the importance of the environmental
noise, the distance to county center and building index for protection
of urban birds in Huanghuai Plain. The research findings filled the gap
in the study area regarding the relationship between urbanization and
avian communities based on urban-rural continuum.
Keywords: Huanghuai Plain; Urbanization; Breeding season;Bird
species diversity; Functional characteristics;
Dear Editors,
We are pleased to submit our manuscript entitled “The impact of
urbanization on avian communities during the breeding season in the
Huanghuai Plain of China” (authors: Meiting Liu, Jiayi Shi, Ziruo
Zhang, Xinyi Zhang, Xiaohan Li, Ruohui Tang, Chunna Zhang, Siyu Wu,
Chenfang Wu, Junpo Zhu, Zhirong He, Yujia Sun, Yuehuan Wang, Supen Wang,
Na Zhao) for consideration as an article in Ecology and
Evolution .
Our paper represents a novel contribution to provide recommendations for
the conservation of avian populations under the pressure of urbanization
and will be highly cited because, firstly, we investigated the variation
of species diversity and functional traits along the urban-rural
continuum, including three habitats (i.e., urban, suburban, and rural).
Then, we explored the relationship between urbanization synthetic index
and species diversity and functional traits. Finally, we identified
which urbanization-related factors most associated with the species
diversity and functional traits of birds in the Huanghuai Plain of
China. And the identification of urbanization-related factors
influencing the loss of species diversity and the changes of functional
traits is crucial for the effective management of protected birds of the
study area.
We conducted bird surveys along the urban-rural continuum by utilizing
150 line transects within 51385 km2 area from June to
August in 2022 and 2023 in Huanghuai Plain of China. Here, 106 species
were recorded in field surveys. And we found that the urbanization
synthetic index had significant negative correlations with
Shannon-Wiener diversity index and species richness, and had no
significant correlation functional traits. Urban birds tended to
construct nests at crown, and the diets of them tended to be omnivorous.
The results of models showed that the environmental noise, the distance
to county center and the proportion of building area within 250-meter
radius were critical factors affecting species diversity, as well as
environmental noise and the distance to county center were best
predictors for functional traits. Our study reported the effect of
urbanization on the bird communities during the breeding season and
underscored the significance of these urbanization-related factors in
the protection of birds within the study area. This finding addressed
the gap in research that had been previously identified in the Huanghuai
Plain. And our paper will provide important insights into ecology and
conservation biology.
None of the material in this paper has been published or is under
consideration for publication elsewhere, including the internet. All
relevant authors and institutions have approved the submission for
publication, and all authors have seen and agreed to the submitted
version of the manuscript. Our research methods also conform to the
legal requirements of China, the country in which the study was carried
out, including those relating to conservation and animal welfare, and to
the journal’s policy on these matters.
Thank you very much for your consideration of our manuscript. We believe
that you will find our work to be an important contribution toEcology and Evolution . We hope you enjoy our work and
find it relevant for publication in your journal upon review.
Sincerely,
Na Zhao, corresponding author
1 Introduction
Urbanization drastically transforms natural landscape and leads to a
decline in biodiversity (Marzluff et al., 2012; McDonald et al., 2020).
By 2030, projections suggest that the urban land may be 1.2 million km²
(Seto et al., 2012) and approximately 5.2 billion urban populations
around the world (United Nations, 2018). Urbanization is concurrent with
the reduction in biodiversity (Aronson et al., 2014; Evans et al., 2018;
Barbosa et al., 2020). Numerous studies have found that there is a
decline in animal diversity with the increase of impermeable surface
from rural to urban region (McKinney, 2002; Piano et al., 2020; Hastedt
& Tietze, 2023; Vaz et al., 2023). For example, the species-area
relationship indicates that the increase of urban land (e. g.,
artificial grass, paved surfaces, and buildings) result in the loss of
plant species richness (Blair & Launer, 1997; Mckinney et al., 2008).
And the plant structure in cities often tends to be simplified (Marzluff
& Ewing, 2008). These have a negative influence on the diversity of
animals, as their diversity concerns the complexity and species richness
of vegetation (Savard et al., 2000). Moreover, urbanization is a major
driver of biotic homogenization (Mckinney, 2006). Despite being a
minority view, certain research findings argue that moderate levels of
urbanization can support the highest levels of species diversity, thus
supporting the Intermediate Disturbance Hypothesis (IDH) (Lepczyk et
al., 2008; Callaghan et al., 2019). As urban areas may have highly
spatial habitat heterogeneity (Savard et al., 2000) and the invasion and
establishment of exotic species that exceeds the rate of loss (McKinney,
2002, 2006).
Birds are widely distributed in urban ecosystems. Their ecological
characteristics (e.g., active behavior and variable vocalizations) make
them more easily observable when compared to other biological taxa.
Given their sensitivity to environmental changes, the population density
and diversity of birds serve as critical indicators of environmental
quality and biodiversity in urban ecosystems (Gregory et al., 2003).
Consequently, birds are often chosen as focal species in urbanization
studies (Neate-Clegg et al., 2023; Duan et al., 2024; Zhong et al.,
2024). However, most of studies were focused on developed regions in
China, while there is little attention given to other regions (Chen et
al., 2000; Chen et al., 2022; Duan et al., 2024).
Previous findings that urbanization has negative effect on birds, such
as birds are particularly vulnerable to traffic noise, with a notable
decline in population density in areas with high traffic volumes (Cai,
2012); Light and noise pollution generated by energy infrastructure
construction directly affect foraging, breeding, and migration behaviors
of bird (Kunz et al., 2007; Tryjanowski et al., 2013), and indirectly
influence their choice of habitats and nest sites (National Research
Council et al., 2007). However, urban areas also provide green spaces
that birds treat it as “refuge habitats”, such as urban parks,
artificial lakes (Sandström et al., 2005; Callaghan et al., 2019).
Moreover, the urban habitats filter out ecologically specialized
species, retaining those with specific traits or combinations of traits
that are adapted to the urban environment (Zhong et al., 2024).
Generally, urban-adapted birds are identified as ecological generalists,
characterized by smaller body mass (Cooper et al., 2022), larger clutch
size (Callaghan et al., 2019), enhanced migration abilities (Møller,
2009; Zhong et al., 2024), broad ecological niche and diverse diets
(Bonier et al., 2007; Callaghan et al., 2019; Palacio, 2020). In
addition, urban birds tended to be arboreal, avoiding the ground nest
(Conole & Kirkpatrick, 2011; Dale et al., 2015). Despite extensive
evidences on the ecological and life history characteristics of birds
related to urbanization, the results are often contradictory. For
example, urban tolerant birds are medium-sized in a large city in
south-eastern Australia (Conole & Kirkpatrick, 2011). It is essential
to investigate which functional traits most closely related to the urban
adapted birds in urban, which helps us understand the relationship
between urban birds and urbanization.
The Huanghuai Plain, the most populous plain in China, features flat
terrain, numerous rivers, temperate climate. It has grown into a
significant political, economic, cultural, and transportation hub as
urbanization. However, prior research on the effects of urbanization on
birds has primarily focused on developed areas (e.g., Shanghai, Beijing,
and Hangzhou), with a notable lack of studies in underdeveloped areas in
China. Therefore, this experiment will fill a gap in the effect of
urbanization on birds in the Huanghuai Plain. This study will provide
insights into the differences in adaptive traits of birds across various
levels of urbanization, offering recommendations for biodiversity
conservation.
Here, this study explored the relationship between birds and
urbanization by examining species diversity and functional traits in
breeding season within Huanghuai Plain of China. We hypothesized that
the urbanization has profound impact on birds. Specifically, we
considered three alternative hypotheses: (1) species diversity will
exhibit a significant difference among three habitats (i.e., urban,
suburban, and rural), with the lowest in urban habitat. (2) urban birds
will be smaller body mass, larger clutch size, wider distribution
breadth than other habitats. And they tend to be arboreal and diverse
diets. (3) species diversity and functional traits will have significant
negative correlations with the urbanization synthetic index, including
the building index, the environmental noise, and the disturbance index,
while have significant positive correlations with the distance to the
county center.
2 Methods
2.1 Study area
We conducted this study in the southern of Huanghuai Plain in China
(33°16′~34°14N, 116°23′~117°02′E), situating
in the northern of the Anhui province and certain regions within Henan
province. The terrain of the study area is predominantly characterized
by plains, and scattered low-lying hills and mountains, with altitudes
generally below 200 m. The climate belongs to the warm temperate
semi-moist monsoon climate, which the climate is mild and rainy, with an
average annual temperature ranging from 14°C to 16°C and an annual
precipitation of between 800 and 1000 mm. The vegetation type is warm
temperate deciduous broadleaf forests, complemented by coniferous
forests and shrublands, offering a relatively diverse habitat
composition (Figure 1).
2.2 Line transects and habitats classification
We defined three habitats (i.e., urban, suburban and rural), based on
the classification system which researchers have previously established
about global rural-urban continuum in 2020 (1-kilometer resolution) (Li
et al., 2023). Specifically, the vector layer representing the boundary
of the study area was used to clip it in ARCGIS 10.8, getting the vector
layer of the rural-urban continuum classification system for the study
area at first. The vector layer includes nine classifications (i.e.,
urban, town, village, cropland, grassland, woodland, wild, water, and
ice/snow) (Li et al., 2023). Then, we excluded the vector layer of water
and classified the remaining eight vector layers, Finally, the urban
layer was categorized as urban habitat, the layers of town and village
belonging to suburban habitat, and the remaining layers belong to rural
habitat. Urbanization varies across different regions, resulting in a
gradient of urbanization rang from urban to suburban and rural, with the
urbanization decreasing as the distance from the urban increases in the
study area. According to the mapping of rural-urban continuum of study
area, we have pre-established 150 fixed 1-km line transects. For the
transects distributed in water layer, they are reclassified into the
above three habitats based on the neighborhood grid attributes of the
grid where the transects are located, with 50 line transects allocated
to each habitat.
2.3 Field surveys
Bird surveys were conducted by two experienced researchers during 4 h
from dawn and 3 h before sunset in good weather (e.g., no wind and rain)
in summer during June to August 2022. The observers walked along each
line transect at a constant speed of approximately 1.0km/h – 2.0km/h
and used binoculars for direct observation to identify birds, and
additionally, observers also utilized camera to document bird that were
unidentifiable within a 50-m radius, while not included those flying
over the head. During June to August 2023, we carried out repeat bird
surveys by using same methods. The composition of land use types of each
line transects did not change during our surveys.
2.4 Data collection
2.4.1 Avian species identification and classification
The identification and classification of birds based on A
checklist on the Classification and Distribution of Birds of China (Zheng, 2023) and A Field Guide to the Birds of China (Mackinnon
et al., 2000). The levels of endangerment and conservation status are
based on The List of National Key Protected Wildlife , The
IUCN Red List of Threatened Species (IUCN;
https://www.iucnredlist.org/) and The Red List of
Biodiversity in China: Vertebrates.
2.4.2 Functional characteristics collection
We selected 5 ecological and life history characteristics (i.e., body
mass, diet, clutch size, nest site, and distributed provinces) for our
study (Wang et al., 2021). Body mass is one of the most critical
functional traits, serving not only as a representative of morphological
traits of birds but also reflecting the nutritional metabolism and
demand of resources. It forms the foundation of physiological,
ecological, and evolutionary processes. Diet reflects the requirement of
different food, as well as methods of obtaining food, which determines
the trophic level within ecosystems and communities (Wenny et al.,
2011). Clutch size and nest site can reflect the reproductive strategies
and capacity (Larsen et al., 2005). The distributed provinces serve as a
proxy indicator for the breadth of bird distribution. Distribution
breadth is one of the indices that measures the extent to which a
species exploits food and habitats, as well as adaptive capacity to
environmental changes (Flynn et al., 2009; Luck et al., 2013).
2.4.3 Urbanization characteristics variables
Compared to earlier studies on urbanization, researchers used a single
variable or indicator to substitute the level of urbanization (Marzluff
et al., 2001). It appears to be insufficient in fully representing the
true level of urbanization within the study area. Some studies have
employed an urbanization synthetic index to conduct related research to
mitigate negative effects (Chen et al., 2022; Wang & Zhou, 2022).
Therefore, we also selected an urbanization synthetic index that
includes four main factors (i.e., the building index, the environment
noise, the disturbance index and the distance to the city center) (Chen
et al., 2000; Wang et al., 2008).
We imported all line transects into ArcGIS 10.8, and established four
buffer zones around each line transect, with a radius of 250m, 500m,
1000m, and 2000m, respectively, to estimate the proportion of buildings
surrounding the lines (Bolger et al., 1997). Wang et al. (2009) used the
method of summing the weighted building proportions to calculate the
building index: The Building Index (BI) = 250 m of building area%1 +
500 m of building area%0.5 + 1000 m of building area% 0.25 + 2000 m of
building area% 0.125.
While conducting field surveys along each line transect, we measured the
environmental noise using a decibel meter. Measurements were conducted
once during each of the three time periods: morning, midday, and
evening, with each measurement lasting for 10 minutes. The average of
the noise values obtained from each line transect was then taken as the
environmental noise (Wang & Zhou, 2022). Meanwhile, we also carried out
the collection of the disturbance index. The observation at each line
transect, human traffic was recorded, with each observation lasting for
10 minutes. The average value was then adopted. The study divided human
disturbance into five levels, with level 1 indicating the absence of
human; Level 2 indicating human traffic of 1-2 people per minute; Level
3 indicating human traffic of 3-7 people per minute; Level 4 indicating
human traffic of 8-17 people per minute; and Level 5 indicating human
traffic of 18 people per minute or more (Chen et al., 2000).
Our study divided the study area into county-level units, with the
government hall at each county serving as the central point. The
distance to the county center (DCC) was measured as the straight-line
from line transects to the government hall of each county (km) with
Google map.
Following other studies, an urbanization synthetic index (USI) for our
study as follows: USI= BI100 / 2 + EN + DI20 + 100 / DCC (Chen et al.,
2000; Wang et al., 2008; Wang & Zhou, 2022). We adjusted parameters
value to the range of 0-100, with higher numbers representing a higher
level of urbanization (Chen et al., 2000; Wang et al., 2008). In detail,
the BI value ranged from 0 to 2, we standardized it by multiplying by
100 and then dividing by 2; The EN value ranged from 0 to 100, so it
remained unchanged; The DI value ranged from 1-5, so it was multiplied
by 20; the DCC value from 0 to 60, so it was taken the reciprocal and
multiplied 100.
2.5 Data analyses
We conducted a preliminary analysis by drawing species accumulation
curves to evaluate the sampling effort. The result indicated that our
field survey was sufficiently comprehensive, allowing for subsequent
analyses (Figure 2).
For each line transect, we calculated the species richness, abundance of
every species, the Shannon-Wiener diversity index (Shannon-Wiener &
Weaver, 1998), the Pielou evenness index (Pielou, 1966) and the Simpson
diversity index (Simpson, 1949). Prior to analyses, the Pielou evenness
index and species richness were transformed by taking the square-root to
achieve normality, while the USI was log-transformed for the same
purpose. And then a one-way analysis of variance (ANOVA) was employed to
test for differences among three habitats, followed by Tukey’s Honest
Significant Difference (HSD) test for pairwise comparisons. The Pielou
evenness index did not exhibit a significant difference among the three
habitats, the rest of diversity indices showed significant differences
(Appendix Table S1). Therefore, we then conducted linear mixed models
(LMMs) to explore the relationship between urbanization synthetic index
and bird species diversity, with the USI as the fixed effect and the
research sites as random factor. In addition, we carried out the Pearson
correlation analysis to avoid interference in the results due to
multicollinearity among the various urbanization factors and species
diversity. Although the correlation between the building index and
environmental noise was greater than 0.7 (r=0.745), giving the
significant relationships between both above indices and diversity index
and retaining them for subsequent analyses (Appendix Table S3). This
experiment also employed linear mixed models to determine which factors
in the USI (i.e., BI, EN, DI, DCC) influenced species diversity and
their relative importance, with the study sites served as the random
factor. We employed the Akaike Information Criterion (AIC) to determine
which of the building index proportions within four different radiuses
had the greatest impact, and we integrated the lowest AIC value into
linear mixed models for further analyses (Appendix Table S2). The
analysis yielded a series of models. We then selected and ranked models
basing on the cumulative difference values of the Akaike Information
Criterion (ΔAICc ≤ 2), the candidate models selected were equivalent
(Burnham & Anderson, 2002). Subsequently, model averaging was conducted
to obtain the relative importance of each parameter within a 95%
confidence interval, along with the model estimates and standard errors,
in order to mitigate uncertainty in model selection. We employed the
same procedures and methods to investigate the relationship urbanization
and functional traits (i.e., body mass, clutch size and distribution
breadth) of birds. Diet and nest site are categorical data, we analyzed
the differences in species richness by calculating the number of species
present in each habitat. All analyses were performed in R 4.3.3 (R Core
Team, 2024), the significance level was set at α=0.05.
3 Results
3.1 Bird community composition
This survey recorded a total of 106 bird species during two breed
seasons, which belong to 14 orders and 45 families and including 60
passerine species and 46 non-passerine species. There were 53 species in
urban habitats, 77 species in suburban habitats, and 91 species in rural
habitats. Among the recorded species, there were 5 listed as Near
Threatened (NT) on the The Red List of Biodiversity in China:
Vertebrates (i.e., Charadrius placidus , Circus cyaneus ,Accipiter trivirgatus , Falco peregrinus , Terpsiphone
incei ) and 6 were classified as Class II Key Protected Wildlife in
China (i.e., Platalea leucorodia , Accipiter virgatus,
Circus cyaneus, Accipiter nisus, Accipiter trivirgatus, Falco
peregrinus ) (Appendix Table S7).
3.2 Variation in species diversity with urbanization
The results of linear mixed models showed that the urbanization
synthetic index exhibited significant negative correlations with the
Shannon-Wiener diversity index (P =0.0342) and the species
richness(P =0.0316), while it showed no significant relationship
with the Simpson diversity index (P =0.6270) and the Pielou
evenness index (P =0.7060) (Figure 3; Table 1).
3.3 The models assessing the impacts of urbanization on avian species
diversity
The model average results from the linear mixed model analyses indicated
key factors influencing the Shannon-Wiener diversity index of birds
include the proportion of building area within a 250-meter radius
(wi = 1.0000, Estimate = -0.4827 ± 0.1568SE, Z =
3.7550, P = 0.0002), the environmental noise
(wi = 0.8000, Estimate = -0.0061 ± 0.0030SE,
Z=2.0190, P = 0.0435), and the distance to the county center
(wi = 1.0000, Estimate = 0.0074 ± 0.0027SE, Z =
2.7100, P = 0.0067). Key factor influencing the species richness
is environmental noise (wi = 1.0000, Estimate =
-0.0145 ± 0.0060SE, P = 0.0150). The Simpson index and the Pielou
evenness index showed no significant relationships with the urbanization
factors (Table 2).
3.4 The models assessing the impacts of urbanization on functional
traits
The body mass, clutch size and distribution breadth have showed no
significant correlations with urbanization synthetic index (Figure 4;
Appendix Table S8). However, according to the results of the model
average, there was a significant negative correlation between clutch
size and the proportion of building area within 2000-meter radius
(wi = 0.8700, Estimate = -0.3118 ± 0.1538SE,P = 0.0444). And the distribution breadth showed a significant
negative correlation with the distance to the county center
(wi = 0.8500, Estimate = -0.0249 ± 0.0108SE,P = 0.0223). In terms of body mass, there was not significant
correlation with urbanization factors (Appendix Table S9). From the
perspective of the dietary groups to which bird species belong, the
composition of diet was similar across the urban, suburban, and rural:
the order of bird species by diet, from most to least abundant, is:
omnivorous, insectivorous, carnivorous and insectivorous, and
carnivorous. The number of bird species with each nest site was as
follows: crown, ground, shrubbery, water, and rock-wall (Figure 5).
4 Discussion
Our findings revealed that a total of 106 bird species were recorded
during the breeding season. The species richness, abundance and
Shannon-Wiener diversity index were the highest in rural habitat,
followed by suburban habitat, and the lowest in urban habitat, showing
the decrease along the urbanization gradient. This pattern is not only
same as our first hypothesis, but also consistent with other outcomes of
previous studies (McKinney, 2002; Piano et al., 2020; Hastedt & Tietze,
2023; Vaz et al., 2023). And this aligns with the results of the linear
mixed model analyses, which the species richness and the Shannon-Wiener
had a significant negative relationship between urban synthetic index.
In contrast to other two habitats, suburban habitats were classified as
moderate disturbance. Nevertheless, species richness in suburban
habitats was lower than in rural areas, which counters the intermediate
disturbance hypothesis. This discrepancy contrasts with the findings of
previous research (Wang et al., 2022; Duan et al., 2024). The level of
disturbance in urban habitat is the highest, resulting in the lowest
number of bird species. This difference may be attributed to the
combined effects of various factors such as the regional biodiversity,
the extent of urbanization, and management policies, which may lead to
diverse outcomes (Wang et al., 2012).
Li et al. (2020) simulated the distribution habitats of 1111 bird
species across China, revealing that 220 species tended to select rural
as their habitats. It is consistent with our findings that the average
value of species richness, as well as the Shannon-Wiener and the Simpson
diversity index were highest in three habitats. This is closely related
to the higher openness and abundant food resources in rural habitat,
especially during the period of crop maturity and harvest (Crampton et
al., 2011; Rosin et al., 2016). The insects, weed seeds, and leftover
grains in the grasslands within the agricultural fields provided rich
food for birds. Consequently, rural habitat is characterized by a
prevalence of omnivorous and insectivorous bird species (Figure 5).
Additionally, the rural landscapes had many paddy field, rivers, and
artificial irrigation channels within the study area, which have
attracted many birds primarily feeding on carnivorous diets, within a
lot of aquatic birds. This finding is consistent with previous research
on the effects of artificial landscapes on breeding bird communities
(Wang et al., 2021). However, the Pielou evenness index of the three
habitats was low, due to the dominance of human-associated species
(e.g., Hirundo rustica , Cecropis daurica , Passer
montanus , Spilopelia chinensis ) within the avian communities,
which account for majority of the total bird individuals (i.e., urban
(67.35%), suburban (42.48%), and rural (54.36%)).
Life history refers to the sequence of stages that an organism goes
through from birth to death, including all the events and processes that
occur during its lifetime, which can effectively reflect the adaptive
plasticity of species (Martin, 2004). To date, although there are
numerous studies about the impact of urbanization on functional traits
in China (Chen et al., 2006; Chen et al., 2022, 2023), few studies have
compared them of urban to other build-up (towns) or non-build-up (e.g.,
open fields, forest-field ecotones, and forests) environments of the
urban-rural landscape gradient. Therefore, this study constructed an
urban-rural continuum of Huanghuai Plain and classified three habitats
(i.e., urban, suburban, and rural). There was a significant difference
in the average body mass of birds among the three habitats, with urban
birds having the smallest (Appendix Table S1). The most common raptors
(Accipitridae) in urban centers are smaller (Cooper et al., 2022). The
clutch size in urban was at an intermediate level, and a higher number
of clutches can enhance the population growth potential. Species with
high reproductive capabilities could rebuild their populations more
rapidly following disturbance (Larsen, 2005). Among the 53 bird species
recorded in urban habitats, the omnivorous birds are the most numerous
(Figure 5). It could be evergreen plants, fruiting trees in urban parks,
and residential waste generated by the community serving as food sources
for omnivorous birds (Marzluff & Ewing, 2001). The artificial lakes
within the park, along with the planting of aquatic vegetation, provide
habitats for large waterfowl and various waders, offering them spaces
for survival and reproduction (Zhang et al., 2020). Moreover, the
selection of nesting sites is crucial for the reproduction and survival
of birds. Urban birds predominantly consist of arboreal species, whereas
ground-nesting birds, particularly those that construct nests on the
ground or in shrubbery, tend to favor locations distant from urban
environments (Dale et al., 2015). In this study, nearly half of the
urban birds utilized crown sites, consistent with previous research
findings. Complex plant communities enhance the safety of nesting sites
for urban birds and ensure an abundant food supply, which are key
factors determining whether birds can inhabit urban areas. Therefore,
exploring the relationship between the life story of birds and
urbanization helps us have useful implications for the protections for
birds in urban ecosystems (Martin & Roper, 1988). In summary, the
results were consistent with our second hypothesis.
Urban birds face various survival pressures, and the relationship
between urbanization and birds is currently of great concern to
researchers (Isaksson, 2018; Møller et al., 2015; Leveau et al., 2021;
Chen et al., 2023). Our study employed an urbanization synthetic index
and constructed linear mixed models aiming to investigate which specific
urbanization factors affect bird diversity. the results were consistent
with our third hypothesis. They exhibited a significant negative
correlation between environmental noise and the Shannon-Wiener index and
species richness. Some research have demonstrated that environmental
noise has adverse effects on bird fitness, survival and reproduction
(Habib et al., 2007; Gross et al., 2010; Schroeder et al., 2012).
Anthropogenic noise reduces bird species richness and diversity decrease
in urban parks (Perillo et al., 2017). In addition, a negative
relationship between maximum point-count noise and avian species
richness was found in research that untangled the role of anthropogenic
noise on bird species richness in a Neotropical city (Carral-Murrieta et
al., 2020). These are consistent with our findings. The distance to
county center is often used as one of the indicators to measure the
level of urbanization, with longer distance suggesting lower
urbanization (Chen et al., 2000; Wang et al., 2004). As the distance to
county center increases, there is a decline in urbanization and human
disturbance, concurrently leading to a higher proportion of natural
habitats, which contributes to an enhancement of bird diversity within
the distant area (Chen et al., 2000; Wang et al., 2004). Our findings
also yielded similar outcomes that distance to the county center
exhibited a significant positive correlation with species richness and
diversity. In addition, As the distance to the county center decreased
and the distribution breadth became broader. It indicated that birds in
urban habitats exhibited a wider distribution range and were better
adapted to habitat heterogeneity. Because urban habitat may also provide
the resources and space they require. Previous finding shown that the
increase in the proportion of buildings within the small-scale wetlands
has resulted in the loss of natural habitats, thereby posing a challenge
to the survival of certain bird species (Wang & Zhou, 2022). In this
study, the Shannon-Wiener index and clutch size had a significant
negative correlation with the proportion of building area within a
250-meter radius, yet it also indicated that an increase in building
proportion may have harmful effects on bird.
5 Conclusions
Through field surveys of birds, this study has preliminarily compiled a
checklist of breeding bird species in the Huanghuai Plain. Species
diversity (i.e., Shannon-wiener index, and species richness) have
negative relationship with USI by using LMMs. And the results also
showed that the environmental noise, the distance to the county center
and the proportion of building area within a 250-meter radius were key
factors affecting bird species diversity. The environmental noise and
the distance to the county center were critical factors affecting
functional traits. Urban birds tended to have smaller body mass, larger
clutch size, diverse diets, and arboreal nesting sites in our study.
Therefore, we understood that these functional traits associated with
the urban-adapt birds, as well as highlights the importance of the
environmental noise, the distance to the county center and the building
index for protection of urban birds in Huanghuai Plain. The research
findings filled the gap in the study area regarding the relationship
between urbanization and avian community. However, there is a slight
deficiency in fully understanding the distribution pattern of bird
diversity in the Huanghuai Plain, and efforts should be strengthened in
the future to investigate the bird resources.
Author contributions
Supen Wang and Na Zhao conceived the study. Meiting Liu collected data,
performed data analyses and wrote the first draft. Jiayi Shi gave advice
during writing and revising.
Ziruo Zhang, Xinyi Zhang, Xiaohan Li, Ruohui Tang, Chunna Zhang, Siyu
Wu, Chenfang Wu, Junpo Zhu, Zhirong He, Yujia Sun and Yuehuan Wang
collected data. Supen Wang and Na Zhao reviewed and revised the first
draft. All authors read and approved the final manuscript.
Acknowledgments
We would like to express our gratitude to everyone for their hard work
in data collection and analyses, manuscript revising. This study was
supported by the Beijing Municipal Natural Science Foundation (5252015),
China Postdoctoral Science Foundation funded project (2022M723135) and
National Key Research and Development Program of China (2024YFC2607500).
Conflict of Interest Statement
The authors declare that they have no conflicts of interest.
Data Availability Statement
All data and R code used in the study are available in Dryad.
https://doi.org/10.5061/dryad.0p2ngf2b6.
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