1. Introduction
Urbanization significantly impacts avian communities in and around urban areas by causing the disappearance and deterioration of native habitats [
1], amplifying edge effects [
2], diminishing habitat interconnectivity [
3,
4,
5], and exacerbating the effects of human activities and noise disruption [
6]. The theory of island biogeography [
7] is of great importance for understanding the dynamics of avian communities within urban landscapes. This theory suggests that larger habitat patches support more diverse species, known as the species–area relationship, while more isolated patches tend to harbor fewer species, known as the habitat–isolation relationship. Moreover, the increasingly fragmented habitats, largely caused by human activities, complicate these relationships and highlight the impact of landscape structure, which includes both composition and configuration, on urban bird diversity [
8,
9]. Studies indicate that the shape and area of open water habitats, along with the connectivity of urban wetlands, have been recognized as critical drivers of bird community diversity [
10,
11,
12]. Furthermore, studies have underscored the importance of connectivity and the area of forest habitats in influencing bird diversity [
13,
14,
15]. These findings point towards the complex, multi-scale impacts of habitat loss and fragmentation on biotic responses, highlighting the need for a multi-scale perspective in urban avian ecology [
16,
17].
The majority of studies investigating the relationship between urban bird diversity and landscape structure focus on a single scale [
18,
19] or incorporate a limited number of nested levels of hierarchy (such as patch-, local-, and landscape-scale) with different absolute sizes [
20,
21,
22,
23,
24,
25]. For instance, studies have evaluated the percentage of each land cover type at different spatial scales (e.g., 200 m, 1000 m, and 2500 m buffer zones from the green space) and have included these multi-scale variables in prediction models [
20,
23,
25].
However, the influence of environmental variables on ecological communities is closely tied to the spatial scales used for measurements, which impact the strength, significance, and even direction of observed effects [
26,
27]. If we do not measure landscape structure at its most impactful scale, otherwise known as the “scale of effect” [
17], we might fail to detect crucial community–landscape relationships. To identify these relationships between communities and landscape structure, recent studies adopt a hypothetical focal site multi-scale approach [
17,
26]. In this method, landscape structure is measured within nested scales (for example, 1, 2, and 3 km) of absolute size [
17]. This approach allows for the determination of the “scale of effect”, ensuring comparability of metrics across scales. It has been applied to studies on primates [
28], insects [
29], and birds [
30,
31].
Though the hypothetical focal site multi-scale method has been employed in a handful of studies to investigate the multi-scale responses of avian species to landscape structure, the majority of research has predominantly focused on minimally human-disturbed forest ecosystems [
30,
31]. For instance, the effects of landscape variables on avian diversity in Brazilian Eucalyptus plantations were examined, revealing the negative impacts of forest fragmentation [
31]. Another study explored the most appropriate spatial scale for the incidence of certain bird species in fragmented Brazilian Atlantic forests [
30]. However, there is a dearth of studies regarding the “scale of effect” of bird community–landscape relationships on functional and taxonomic aspects in urban areas. Furthermore, there is a need for more discussion on landscape structure at the configuration aspect (such as dispersion, subdivision, and isolation) rather than merely at the composition aspect. Understanding these elements of dynamic, complex urban landscapes could enhance our comprehension of urban ecology and inform effective biodiversity conservation strategies.
In this study, by analyzing data from 28 sampling sites in the city of Kunming at 16 different spatial scales, we aimed to gain insights into the relationships between landscape structure, elevation attributes, and bird diversity (both taxonomic and functional) as they vary across different spatial scales. The study utilized variable importance in projection (VIP) scores, which are based on partial least squares regression (PLSR), to quantify the significance of each predictor variable in our model, incorporating both its effect and reliability. This approach effectively overcomes the limitations posed by multicollinearity among predictors. Our objective was to identify the “scale of effect”, which refers to the most influential scale at which the environmental variables being investigated impact the taxonomic and functional diversity of bird species. This multi-scale approach provides a comprehensive understanding of biodiversity and aids in identifying the conservation actions that have the greatest impact at various scales.
3. Results
3.1. Bird Species Diversity
During both the breeding and non-breeding seasons, we carried out a total of twelve replicated surveys at 28 sampling sites. This approach allowed us to gather comprehensive data across various locations and seasons. In total, we recorded 132 bird species from 44 families and 15 orders, for a total of 5386 counts (see
Table S1). During the breeding season, bird species richness per sampling site ranged from 6 to 29, with a mean of 15.1 (s.e. = ±1.2), and FDis ranged from 0.77 to 1.88, with a mean of 1.14 (s.e. = ±0.05). In contrast, during the non-breeding season, species richness ranged from 6 to 34, with a mean of 17.3 (s.e. = ±1.5), and FDis ranged from 0.74 to 1.57, with a mean of 1.11 (s.e. = ±0.05). We conducted a spatial autocorrelation analysis using Moran’s I and found that neither species richness nor FDis exhibited significant spatial autocorrelation (richness during the breeding season
p = 0.057; richness during the non-breeding season
p = 0.144; FDis during the breeding season
p = 0.538; FDis during the non-breeding season
p = 0.955).
During the breeding season, the first principal component explained 56.83% of the total variance in diet and 44.48% in foraging strata (
Figure S1). During the non-breeding season, it explained 48.25% and 43.96%, respectively (
Figure S2). Each bird species was also assigned to one of five dominant diet categories based on the summed scores of the constituent individual diets. Our results revealed that the majority of diet categories of bird species were assigned to invertebrates (76 species, 57.58%), followed by omnivores (21 species, 15.91%), plants and seeds (15 species, 11.36%), vertebrates, fish, and carrion (15 species, 11.36%), and finally, fruits and nectar (5 species, 3.79%). The dominant diets and foraging strata of the most common 30 bird species from our survey can be found in
Table 2.
3.2. Analyzing Species Diversity and Multiscale Landscape Metrics Relationships Using PLSR
We utilized PLSR to investigate the relationship between multiscale landscape metrics (explanatory variables) and richness as well as FDis (response variables). The first components derived from the analysis explained 62.54% of the variation in richness during the breeding season, 44.91% of the variation in richness during the non-breeding season, 36.92% of the variation in FDis during the breeding season, and 43.46% of the variation in FDis during the non-breeding season. To provide a clearer understanding of the scale-dependent effect of these metrics on bird richness and FDis, we analyzed the changes in the VIP scores of multiple types of landscape metrics (including area, edge, shape, dispersion, subdivision, interspersion, isolation, and diversity) of different land-use types with varying buffer sizes (
Figure 2 and
Figure 3).
The area and edge of constructed land play a crucial role in species richness and FDis, and their VIP scores remain relatively stable across different buffer areas. As spatial scale increases, the subdivision and dispersion of constructed land gradually become more important. The area, edge, and subdivision of roads exert a substantial influence on both richness and FDis, and this influence grows stronger with increasing scale. Notably, the dispersion of roads has a more pronounced effect on FDis (VIP > 1) compared to richness.
The dispersion and area of open water mainly influence species richness and FDis. The influence of open water’s area on FDis diminishes as the spatial scale expands, while its effect on richness remains stable. Therefore, the “scale of effect” of open water area for FDis likely occurs at small and medium scales, while the “scale of effect” of open water dispersion is most likely at scales greater than or equal to a 3000 m buffer.
Both richness and FDis are significantly impacted by several attributes of the forest, including edge, dispersion, subdivision, area, and interspersion. Similarly, the dispersion, subdivision, and interspersion of open green space also significantly impact both richness and FDis, with the significance of dispersion increasing as the spatial scale enlarges. Elevation has a pronounced effect on species richness and FDis during the breeding season, but this influence is not significant in the non-breeding season. In both breeding and non-breeding seasons, dispersion and subdivision at the landscape level are crucial factors influencing species richness and FDis. Among these, subdivision exerts a notably stronger effect on FDis. Therefore, reducing landscape-level subdivision is indispensable for safeguarding species richness and functional diversity across an urban matrix.
3.3. Analyzing Species Diversity and Multiscale Landscape Metrics Relationships Using GLMs
We used PLSR and VIP approaches to identify potential explanatory variables for bird richness and FDis during both breeding and non-breeding seasons. For the breeding and non-breeding seasons, these analyses resulted in a total of 712, 607, 606, and 659 variables, respectively, each with a VIP value greater than 1. To mitigate multicollinearity, we selected the highest VIP score from environmental variables in each land-use category or landscape level across the 16 scales. This approach ensured that each type of metric for every land cover type or landscape level was represented solely by one scale. We set the VIP score threshold at 1.6 for richness in the breeding season and 1.7 for richness in the non-breeding season, as well as for FDis in both breeding and non-breeding seasons. Further, we removed the explanatory variables with a VIF ≥ 10 to avoid multicollinearity. Ultimately, this process generated four and nine explanatory variables of interest for richness in breeding and non-breeding seasons, respectively, and eight and five explanatory variables of interest for FDis in breeding and non-breeding seasons. Then, we fitted separate GLMs with a Gaussian family for richness and FDis. By applying the criteria that the count of independent variables ≤ 3 and ΔAICc < 2, we identified three and six top-ranked models for richness in breeding and non-breeding seasons (
Tables S2 and S3) and five and four top-ranked models for FDis in breeding and non-breeding seasons (
Tables S4 and S5), respectively.
To further refine our analysis, we performed model averaging on the top-ranked model set for bird species richness and FDis in both breeding and non-breeding seasons. The outcomes indicated that bird species richness was significantly influenced by PLAND of constructed land at a 100 m scale and Altitude_RANGE at a 2200 m scale in the breeding season (
Table 3 and
Figure 4), as well as by PLADJ of constructed land at a 100 m scale and AREA_MN of Open Water at a 3000 m scale in the non-breeding season (
Table 4 and
Figure 4). The outcomes of model averaging also indicated that bird species FDis was significantly influenced by AREA_MN of open water at a 1200 m scale and ENN_MN in landscape level at a 200 m scale during the breeding season (
Table 5 and
Figure 5), and by COHESION of constructed land at a 100 m scale and COHESION of open water at a 3000 m scale during the non-breeding season (
Table 6 and
Figure 5).
4. Discussion
Our study underlines the significant relationship between bird species richness, FDis, and multi-scale landscape metrics. The link between bird species diversity and landscape structure is scale-dependent. We recognize that the patterns and dynamics linking bird diversity to landscape structure can vary across different spatial scales. Notably, no single buffer size applies universally to all indicators, as illustrated in
Figure 2 and
Figure 3. Various ecological processes operate at different spatial scales, resulting in the observed variation in species responses [
26,
28,
29]. Urban landscapes are characterized by high levels of heterogeneity, disturbance, complexity, and dynamism. These factors operate across multiple scales, with community responses intricately linked to both the composition and configuration of landscapes across a variety of scales [
17,
26].
In our study, bird species richness appears to be significantly influenced by the dispersion of open water, with its influence increasing as the scale expands. This implies that the “scale of effect” of open water dispersion on species richness is likely above 3 km. Interestingly, as the scale increases, the influence of area on the FDis diminishes, while its effect on species richness remains comparatively stable. Thus, for FDis, the area of open water assumes greater significance at small to medium scales. Accordingly, the “scale of effect” of open water area metrics on bird FDis in this study is likely to be at medium and small scales (<1 km buffer zones). Several studies underscore the importance of water coverage and connectivity in affecting avian diversity [
4,
43,
59,
60]. Additional research indicates the influence of the area of open water on bird community structure [
61,
62,
63]. Our findings reinforce these relationships, illustrating how the interplay between open water parameters and spatial scales shapes bird species richness and functional diversity in our study area.
Both the richness of species and the FDis are notably influenced by forest edge and dispersion at almost all scales. Interestingly, we find that the impact of forest area metrics on bird species richness intensifies as the scale increases during the breeding season, suggesting that the “scale of effect” of forest area on richness could be at or beyond 3 km. In a highly fragmented urban matrix, forest connectivity may surpass patch size in importance at medium scales. This understanding echoes the findings from a study in Southeast Brazil, which found that small forest patches serving as connectivity and corridors may have greater importance than fragment size in landscapes with moderate amounts of remaining forest [
13]. Research from urban parks in Beijing revealed the substantial influence of park green space area and its connectivity on bird occurrence and breeding bird communities [
14]. Research in Bangkok reveals that urban parks closer to the city’s largest parks have a higher species richness compared to those more distant from the largest city parks [
15]. A study on small forest patches embedded in urban landscapes found that total bird abundance was positively affected by habitat connectivity [
64]. Research in Santiago, Chile, examining a 1-square-kilometer buffer, indicates that while increased woody cover in urban landscapes enhances local bird richness, aggregation of woody cover has no such effect [
65], which might be related to the single survey scale employed. Our findings highlight the crucial role of scale in evaluating the effects of forest connectivity and area on bird diversity. However, as the dynamics may change on scales exceeding 3 km, further research is warranted to explore these potential shifts.
Our research indicates that the impact of the area of forest at larger scales significantly outweighs that at smaller scales, with its “scale of effect” being over 3 km. Therefore, priority should be placed on preserving large green spaces at larger scales to prevent fragmentation. This is supported by a study across 1581 cities in the U.S. that suggested that city-scale forest cover positively influenced bird species richness [
4]. Similarly, a study conducted in Northeast Brazil’s metropolitan region, which included nine protected areas, emphasized the necessity of giving priority to larger reserves for bird conservation [
66]. Other studies indicated that large trees contribute to increased bird species taxonomic and functional diversity [
67] and that preserving forest remnants in agricultural landscapes supports bird functional richness [
68].
For constructed land and roads, the area, edge, and dispersion of constructed land and roads have a profound impact on both richness and FDis. In the case of roads, this influence becomes more prominent as the scale increases. Other studies show that bird diversity significantly declines when built-up cover exceeds 70% [
69]. Research indicates a negative correlation between the number of buildings and bird species richness, as well as functional richness and the maximum height of buildings, leading to a precipitous decline in functional evenness [
70]. Moreover, a study in Latin American cities found a negative correlation between impervious surfaces [
71]. The intricate interaction between roads and biodiversity has long intrigued researchers. Studies have demonstrated that road noise and traffic avoidance behaviors significantly impact species richness and community structure [
6,
72,
73]. Connectivity and road density are crucial predictors of bird community composition in agricultural ecoregions [
74]. This impact intensifies as the scale increases, as larger scales incorporate a wider extent of road networks, which could lead to landscape fragmentation on a large scale.
We observed that during the breeding season, the impact of elevation changes on both bird species richness and FDis intensifies as the spatial scale enlarges. However, this relationship is not discernible during the non-breeding season. This discrepancy may be linked to the migratory behavior of waterfowl. In the migration season, a diverse array of waterfowl species congregate near water bodies, where the terrain tends to be more level. This could explain why there is no clear link between terrain changes and diversity in the non-breeding season. It is worth noting that the relationship between elevation and biological diversity has always been of paramount importance. Specific species are supported in mountain habitats at differing altitudes [
75,
76]. In mountain ecosystems, particularly those in tropical and subtropical regions, high geological heterogeneity fosters conditions that promote species spatial turnover and the emergence of endemic forms [
77,
78,
79]. This underlines the importance of incorporating elevation variation into conservation planning and management in urban areas. Besides, based on our observations, bird feeding, which is known to influence bird presence, was not common in our study area, ensuring a more authentic and naturalistic observation [
80].
In our analysis of landscape-level characteristics, we found that both dispersion and subdivision significantly influence bird species richness and the FDis, with these effects being significant across nearly all scales. Furthermore, subdivision had a particularly strong impact on FDis compared to other types of indices. Habitat fragmentation has been found to decrease animal residency within fragmented areas by reducing the available habitat area, while increased isolation restricts movement among fragments, thereby hindering fragment recolonization following local extinction events [
16]. A study in Brisbane, Australia, showed that fragmentation heightened the negative effects of built infrastructure on insectivore traits in birds [
81]. Research conducted in the agricultural landscapes of southern Finland has shown that bird functional dispersion decreases in homogeneous regions at both local and regional scales [
82].