Rather than single habitat types,  habitat assemblages may significantly shape avian communities in urban fringe

doi:10.21203/rs.3.rs-4933243/v1

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Rather than single habitat types, habitat assemblages may significantly shape avian communities in urban fringe

https://doi.org/10.21203/rs.3.rs-4933243/v1

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Context:

In the context of accelerated urbanization, comprehending the influence of habitat diversity and its dynamics on species is imperative for biodiversity conservation. Specifically, in urban fringe areas, the interactions among various habitat types substantially affect the composition and ecological resilience of avian communities. Nevertheless, the nuanced relationship between habitat assemblages and avian diversity remains unclear relative to studies focusing on single habitat types. Consequently, targeted research is essential to inform and enhance effective conservation practices.

Objectives

The aim of this study was to investigate the utilisation characteristics of habitat assemblages and seasonal changes in habitat assemblages by different avian communities in the urban fringe, in order to reveal the potential ecological mechanisms of habitat assemblage effects.

Methods

In Yinglong Lake Wetland Park, Chongqing, we conducted a year-long avian survey employing the line transect method, supplemented by high-resolution remote sensing imagery and field habitat survey data to classify habitat types and perform habitat mapping. Utilizing these data, we applied integrated statistical methods, including two-way clustering, to investigate the selection and utilization patterns of habitat assemblages by avian communities, with a particular focus on seasonal dynamics.

Results

The findings indicated that 60 species (60%) were present across multiple habitat types, with the greatest number of shared avian species (38) identified within the habitat assemblage of evergreen broadleaf forest (EF) and shrubbery(SH). A two-way clustering analysis categorized the avian species into 10 distinct groups, revealing significant differences in the utilization patterns of habitat assemblages among these communities. Furthermore, seasonal variation notably influenced the habitat utilization strategies of avian communities, especially during the breeding and migratory periods.

Conclusions

This study underscores the importance of diverse habitat assemblages and seasonal dynamics in supporting avian diversity in urban fringe areas. Based on our findings, we have developed targeted recommendations to enhance habitat construction and biodiversity conservation in these regions.

Urban fringe

Habitat assemblages

Avian communities

Biodiversity

Yinglong Lake Wetland Park

As urban populations expand, many cities increasingly encroach upon ecologically significant areas, commonly referred to as the geographical 'urban fringe'. This zone is also known by various terms such as 'suburbia', 'peri-urban', 'edge', or 'interface' (Graham and Ernstson 2012). Conflicts between human activities and biodiversity conservation are most pronounced in the urban fringe, particularly in regions with favorable natural environments such as mountains, forests, and bodies of water (McKinney 2002). Urban fringe areas characterized by favorable environmental substrates exhibit high biodiversity, with a significant presence of threatened species in these areas (Bekessy et al. 2012). The conservation of biodiversity in urban fringes is crucial not only for preserving the ecological functions and ecosystem service capacity of these areas, thereby ensuring the ecological security of the region (Radford and James 2013), but also for its long-term impact on the quality of life and public health of urban residents (Bolund and Hunhammar 1999; Pett et al. 2016)

Habitat loss (Brooks et al. 2002; Foley et al. 2005), fragmentation (Crossman et al. 2007), and the proliferation of invasive species (Blair and Johnson 2008; Cubino et al. 2015) associated with the development of urban fringe areas continue to present significant challenges for biodiversity conservation. Consequently, scholars have increasingly concentrated their research efforts on biodiversity conservation within these urban fringe areas, examining various taxa including mammals (Reichert et al. 2017; Boakes et al. 2024), birds (Catterall et al. 2010; Ikin et al. 2014), reptiles (Marsh et al. 2023), amphibians (Rubbo and Kiesecker 2005), and insects (Goertzen and Suhling 2015). Owing to their extensive distribution (Sekercioglu 2006), sensitivity to environmental fluctuations (Carignan and Villard 2002; Furness and Greenwood 2013), and pivotal role in trophic dynamics (Sergio et al. 2005), avian species have become central subjects in biodiversity conservation research within urban fringe areas. Empirical evidence suggests that these urban fringe areas have emerged as critical hotspots for avian diversity, where factors such as habitat structure (McKinney 2008a), resource availability (Wilson et al. 1999), and habitat heterogeneity (Hughes et al. 2022) play substantial roles in shaping avian diversity and community distribution. The physical characteristics of habitats in urban fringe areas, including size, perimeter, and degree of fragmentation, significantly influence the distribution of avian communities (Fernández-Juricic 2004; Radford et al. 2005). Furthermore, distinct habitat types within these areas, such as deciduous forests (Batáry et al. 2014), grasslands (Pithon et al. 2021a), and farmlands (Robinson et al. 2001), are crucial for avian communities, primarily due to birds' strong reliance on specific resources (Wiens 1989).

Several studies have demonstrated that the integration of diverse habitat types exerts significant effects on species, particularly amphibians, which generally necessitate both terrestrial and aquatic environments (Fahrig 2003). Terrestrial habitats offer dry conditions conducive to resting and foraging, while aquatic habitats are essential for reproduction and larval development (Semlitsch 2008). For non-amphibian species, the assemblage of varied habitats can similarly supply a range of resources and conditions, facilitating the acquisition of necessary resources throughout different stages of their life cycles (Haddad et al. 2015). For instance, avian species may necessitate forested habitats during the breeding season while depending more on open grasslands or wetlands for foraging (Chace and Walsh 2006). However, extant research on habitat assemblages predominantly concentrates on relatively homogeneous urban habitat types (Seress and Liker 2015), with peripheral areas receiving less attention due to their complexity and transient characteristics. Nevertheless, avian species inhabiting marginal landscapes frequently encounter elevated levels of environmental heterogeneity and dynamic changes. Therefore, investigating the utilization of diverse habitat assemblages by these avian species can yield critical insights into their responses to environmental changes and resource variability. This knowledge is particularly crucial for biodiversity conservation in the face of anthropogenic impacts.

A review of the existing literature reveals that the characteristics of habitat assemblages employed by avian communities in urban fringe areas have not been comprehensively examined. This study aims to address this gap by focusing on these specific habitats. Yinglong Lake Wetland Park, located on the edge of the central urban area of Chongqing, was selected as the focal point of our research. Using the line transect method, we conducted a year-long investigation to document the avian species, their population numbers, and the specific habitat types they occupy within the park. We will employ statistical techniques, including two-way clustering, to conduct a comprehensive analysis of the characteristics of various avian communities' utilization of habitat assemblages. This approach will enable us to identify critical habitat assemblages and examine the seasonal variations associated with these assemblages. The primary objectives of this study are to address the following key questions: How do different avian communities select and utilize distinct habitat assemblages? How do these habitat assemblages vary across seasons, and what implications do these variations have for the distribution and diversity of avian species? Based on our findings, we will formulate recommendations and strategies for habitat construction and biodiversity conservation in urban fringe areas.

2.1 Study area

Chongqing is located in the transitional zone at the southeastern edge of the Sichuan Basin, China. This region exemplifies a typical mountainous city characterized by a humid subtropical monsoon climate. The climatic conditions include warm winters and early springs, hot summers, and cool autumns, delineating four distinct seasons. The average annual precipitation ranges from 1000 to 1350 mm, with approximately 70% occurring between May and September. The region's relative humidity averages between 70% and 80%, and annual sunshine hours range from 1000 to 1400, with a sunshine percentage of 25–35%. The average annual temperature in Chongqing ranges between 16°C and 18°C, with summer temperatures averaging from 26°C to 29°C and winter temperatures varying from 4°C to 8°C. The city's distinctive topography, characterized by parallel ridges and valleys (Fig. 1a), establishes it as a significant node on the East Asian-Australasian Flyway. By the end of 2022, Chongqing had documented 530 530 avian species, encompassing 21 orders and 78 families.

Yinglong Lake Wetland Park, situated at the base of Mingyue Mountain in Nanan District, Chongqing, and on the periphery of Chongqing's central urban area (Fig. 1b), serves as a critical site for the conservation efforts of Chongqing's "Four Mountains." The park encompasses an area of approximately 364 hectares. As of 2017, the park has documented 438 species of higher plants, 155 species of vertebrates spanning 28 orders and 64 families, and 79 530 avian species. Among them, there are three species of national-level protected plants, seven species of national-level protected plants, and six species of national-level protected animals. The Yinglong Lake Wetland Park hosts a variety of species, including three species of nationally protected plants, seven additional species of nationally protected plants, and six species of nationally protected animals. Yinglong Lake Wetland Park features diverse wetland landscapes, including reservoirs, hill areas, valleys, and mudflats. The park's abundant forest vegetation and water sources provide natural habitats for a range of avian species.

2.2 Avian surveys

From October 2021 to September 2022, a year-long avian survey was conducted at Yinglong Lake National Wetland Park in Chongqing using the line transect method. Surveys were carried out three times per quarter under favorable weather conditions with no precipitation and low wind. The surveys were conducted primarily during peak avian activity periods, four hours after sunrise and four hours before sunset. Six representative transects were selected within the park, ranging from 0.8 to 1.6 kilometers in length, covering most of the park’s habitat types. Along these transects, surveys were conducted at a speed of 1 to 1.5 km/h with a 25-meter observation width on either side. An 8×42 binocular was used for bird observation, and a camera and recording device were employed to capture images and recordings of avian individuals and their calls. During the surveys, avian behaviors, locations, and habitat characteristics were recorded concurrently for subsequent analysis.

To ensure consistency and scientific accuracy, avian species in this study are referred to by their scientific names and abbreviations only. For instance, Turdus merula is abbreviated as TURMER. Detailed abbreviations and corresponding common names can be found in Appendix S.

2.3 Habitat survey, classification and mapping

This study utilized high-resolution remote sensing data from the Jilin-1 satellite, acquired on April 9, 2021 (resolution: 0.75 meters, cloud cover: 0%, roll: 0.8 degrees), as the basis for habitat type identification at Yinglong Lake National Wetland Park. By reviewing relevant literature (e.g., "Overall Plan for Yinglong Lake National Wetland Park, Chongqing") and combining it with field surveys, we identified the habitat types within the park. The data preprocessing involved two stages: (1) Reviewing relevant materials and literature on Yinglong Lake National Wetland Park and interpreting the Jilin-1 0.75-meter resolution remote sensing data visually to preliminarily determine habitat types based on vegetation type descriptions from the "Overall Plan for Yinglong Lake National Wetland Park (2012–2016)"; (2) Correcting and validating the preliminary habitat type results using the latest high-resolution remote sensing imagery from 2023 and field survey data on the ArcGIS platform, resulting in the final habitat unit mapping. Habitat classification followed guidelines from relevant literature (Davies 2000; Jones 2001; Jung et al. 2020), and surveys were conducted during the autumn and winter seasons, which exhibit significant seasonal vegetation changes. The classification results are presented in Table 1.

Table 1

Classification of habitat types in the study area and description
Level 1 habitat	Level 2 habitat	Habitat description
Arboreal Forest (F)	Evergreen broadleaf forest (EF)	Dominated by evergreen broadleaf species; height typically > 2.5 m. Includes Adenostoma fasciculatum (chemise), Pueraria montana (yellow kudzu), Eucalyptus spp., Cinnamomum camphora (camphor), Drosera spp. (sundew), etc.
	Deciduous broadleaf forest (DF)	Dominated by deciduous broadleaf species; seasonally shedding leaves; height typically > 2.5 m. Includes Ginkgo biloba (ginkgo), etc.
	Mingled forest (MF)	Mixed forest with at least two or more of the following: coniferous species, evergreen broadleaf species, and deciduous broadleaf species; height typically > 2.5 m; no single type is predominant
	Coniferous forest (CF)	Dominated by coniferous species with needle- or scale-like leaves; height typically > 2.5 m. Includes Pinus massoniana (masson pine), Metasequoia glyptostroboides (dawn redwood), etc.
	Forest plantation (AF)	Human-planted forest, usually with one or a few tree species
Shrubbery (SH)	Shrubbery (SH)	Vegetation predominantly 0.5 ~ 2.5 m tall, composed of low shrubs
Grassland (GR)	Grassland (GR)	Vegetation predominantly under 0.5 m in height, composed of tall grasses and herbaceous plants, with some farmland and vegetable plots included
Water (W)	Main body of water (MW)	Water body over 200 m² in area, with year-round standing water
	Unvegetated mudflat (BW)	Unvegetated, primarily composed of bare soil or mudflats
	Aquatic vegetation zone (PW)	Area densely populated with aquatic plants, including submerged, floating, and emergent species
	Rivers and ponds (RW)	Includes rivers, streams, and small water bodies such as ponds
Buildings, roads and facilities (BR)	Buildings, roads and facilities (BR)	Human-made structures such as buildings, roads, and bridges, primarily used for human activities with minimal vegetation cover

2.4 Statistical analysis

We conducted a comprehensive analysis of avian diversity at Yinglong Lake and its association with various habitat types. This analysis involved calculating multiple diversity indices, including species richness (S), evenness (E), Simpson’s diversity index (D'), and the Shannon-Wiener diversity index (H'). These metrics provide a thorough understanding of avian diversity and distribution within the wetland park. Additionally, we performed statistical analyses to investigate the avian habitat selection patterns across different habitat type combinations. We also evaluated the number of avian species shared among habitat combinations to identify which combinations support a greater diversity of species and to determine the most favored habitat configurations at Yinglong Lake Wetland Park.

To investigate the habitat use characteristics of various avian communities across different habitat assemblages, we employed two-way cluster analysis (TWCA) for delineating avian communities (Legendre and Legendre 2012). We converted the data on habitat type and the number of avian individuals into a matrix representing percentage resource use, which was subsequently analyzed using the software PC-ORD 5.0 (McCune et al. 2002). The clustering method utilized the Bray-Curtis distance coefficient and group averaging to categorize avian species into similar ecological niches, thereby elucidating the characteristics of habitat use. The TWCA methodology offers the capability to concurrently analyze species and habitat types, identify ecological niche overlap and divergence, and visually represent species' resource utilization and relative abundance across various habitat types using heat maps. We refrained from categorizing avian communities based on morphological features and feeding characteristics because, despite significant differences in biological traits among certain avian species (e.g., Chroicocephalus ridibundus (CHRRID), Riparia diluta (RIPDIL), Mareca strepera (MARSTR)), their reliance on waterside habitats indicates overlapping ecological niches and similarities in habitat selection and ecological functioning. To further quantify avian community utilization of habitat type combinations, we used stacked bar charts to display the percentage of individuals for each avian community across different habitat types. This approach facilitates the comparison of relative utilization among habitat types within combinations and evaluates their contributions to avian communities. We identified the two most frequently used habitat types for each avian community as primary and secondary habitats (Cody 1985), using this classification to describe and differentiate the utilization patterns of avian communities with respect to various habitat assemblages

Based on the clustering results of the entire year's avian data, we analyzed the changes in habitat combination utilization by avian communities across different seasons. We opted not to perform separate clustering for each season because the annual clustering offers a comprehensive perspective on representative avian habitat utilization patterns. This approach reflects the overall trends in habitat use across the entire year, which enhances the generalizability of the seasonal analysis. By mitigating the potential biases associated with individual seasonal variations or data imbalances, this method ensures greater objectivity and reliability in the findings.

3.1 Avian species and habitat type relationships in Yinglong Lake Wetland Park

This survey recorded a total of 100 avian species across 41 families and 13 orders (Appendix S). Passeriformes, with 68 species, represented the largest proportion. The results of the habitat mapping are presented in Fig. 2. Among all habitat types, the evergreen broadleaved forest (EF) exhibited the highest species richness, with 67 species, and the greatest number of individuals, totaling 1,499. Additionally, this habitat type demonstrated the highest Shannon diversity index (3.099), indicating the greatest overall avian diversity. In contrast, the shrubbery (SH) demonstrated the highest mean and standard deviation in avian population abundance, with values of 23.94 ± 61.85, indicating substantial variability in avian distribution. The deciduous broad-leaved forest (DF) recorded the highest Simpson diversity index (0.9269), signifying elevated species richness and evenness. Furthermore, the aquatic vegetation zone (PW) exhibited the highest evenness (0.881) (Table 2).

Table 2

Birds in different types of habitats and analysis of diversity
Habitat types	Mean value and standard deviation	Total individuals	S	E	H'	D'
Evergreen broadleaf forest (EF)	22.37 ± 51.02	1499	67	0.737	3.099	0.9075
Deciduous broadleaf forest (DF)	17.64 ± 29.03	582	33	0.771	2.697	0.8876
Mingled forest (MF)	9.23 ± 10.09	277	30	0.846	2.879	0.9269
Coniferous forest (CF)	6.73 ± 8.20	74	11	0.802	1.924	0.7739
Forest plantation (AF)	4.11 ± 3.41	37	9	0.857	1.882	0.8123
Shrubbery (SH)	23.94 ± 61.85	1221	51	0.662	2.602	0.8495
Grassland (GR)	18.04 ± 23.00	487	27	0.824	2.715	0.9027
Main body of water (MW)	13.77 ± 22.95	179	13	0.635	1.628	0.7094
Unvegetated mudflat (BW)	5.00 ± 3.87	30	6	0.819	1.467	0.7333
Aquatic vegetation zone (PW)	6.44 ± 4.74	58	9	0.881	1.936	0.8288
Rivers and ponds (RW)	2.20 ± 1.94	11	5	0.805	1.295	0.6446
Buildings, roads and facilities (BR)	11.67 ± 14.38	35	3	0.316	0.347	0.16
S: Richness; E: Evenness; H': Shannon-wiener biodiversity index; D': Simpson's Diversity Index. The following species of raptors were excluded from the analysis due to their absence in specific habitats: Pernis ptilorhynchus (PERPTI), Accipiter trivirgatus (ACCTRI), Accipiter nisus (ACCNIS), Milvus migrans (MILMIG), and Buteo japonicus (BUTJAP).

Of the 95 avian species effectively recorded (excluding five raptors not found in specific habitats), 60 utilized multiple habitat types. Specifically, 22 species (36.7%) were found exclusively in two habitat types, while 12% and 10% were observed in exactly six and four habitat types, respectively. In addition, we found that the habitat combination of evergreen broadleaf forest (EF) and shrubland (SH) shared the greatest number of shared avian species totaling 38.

3.2 Utilization patterns of habitat assemblages by different avian communities

Figure 3 presents a two-way clustering heatmap that categorizes habitat types into four broad groups, retaining 35% of the information in the habitat rows. Habitat types are categorized according to shared characteristics, resulting in the classification of forest habitats (EF, DF, MF, CF, AF), shrubbery (SH), and grassland (GR). These categories are characterized by diverse and multi-layered vegetation, which provides numerous roosting, foraging, and breeding sites for avian species. Additionally, lake-associated habitats (MW, BW, PW) constitute a significant group of habitat types that are spatially contiguous and offer abundant water resources, wetland vegetation, and open spaces conducive to roosting and foraging activities for avian species.

The avian species were categorized into ten groups(Table 3) based on a threshold of 70% of the remaining information in the avian species list. Among these groups, Group G contained the highest number of species, with a total of 42. The study's findings indicated significant differences in habitat utilization patterns among the avian groups. Specifically, Mareca strepera (MARSTR), Anas platyrhynchos (ANAPLA), Tachybaptus ruficollis (TACRUF), Chroicocephalus ridibundus (CHRRID), and Riparia diluta (RIPDIL) in Group B were exclusively observed in the main body of water (MW), whereas the other nine groups exploited multiple habitat types. Furthermore, substantial variations were observed in the extent of dependence exhibited by different avian communities on each habitat type within the assemblage (Fig. 4). Individuals from Groups A, D, F, and G were predominantly concentrated within their primary habitats, constituting over 70% of the total population. This indicates that primary habitats play a crucial role in supporting these avian groups. Conversely, Groups C, E, H, I, and J exhibited a relatively balanced distribution of individuals across various habitat types within the assemblage. The species within these groups demonstrated lower dependence on specific habitats and exhibited a broader ecological niche width.

Table 3

Bird groups from two-way clustering analysis
Avian groups (species count)	Habitat assemblages (number of habitat types)	Representative avian species
Group A(3)	PW—RW (2)	AIXGAL, FULATR, GALCHL
Group B(5)	MW(1)	MARSTR, ANAPLA, TACRUF, CHRRID, RIPDIL
Group C(5)	BW—MW(5)	ARDCIN, EGRGAR, ALCATT, TRIOCH, ACTHYP
Group D(2)	RW—MW(2)	PHOFUL, PHOLEU
Group E(9)	GR—SH(9)	BAMTHO, LONSTR, MYOCAE, HORFOR, EMBPUS, LONPUN, ANTHOD, FRIMON, MOTCIN
Group F(16)	SH—EF(5)	PHACOL, PHYFUS, POMRUF, CYARUF, PTESAN, SINWEB, TUREUN, etc.
Group G(42)	EF—GR(11)	PARMON, DICHOT, ABRALB, CUCMIC, PHYINO, IXOMCC, PICINN, PYCXAN etc.
Group H(7)	DF—EF(7)	EOPMIG, SPOCIN, CHLSIN, FICZAN, PERCAN, PARMIN, ALCDAV
Group I(5)	MF—EF(4)	YUHNIG, STRORI, CUCCAN, PICCAN, EMBELE
Group J(1)	BR—GR(8)	MOTALB
For example, in the GR—SH combination (9), GR is the primary habitat, SH is the secondary habitat, and the combination includes 9 habitat types. Avian species abbreviations are detailed in Appendix S.

3.3 Seasonal variation in habitat assemblage utilization by avian groups

Since Group B exclusively utilized a single habitat type, main body of water (MW), it was excluded from this segment of the analysis. The study's findings (Fig. 5) indicated that seasonal variation significantly influenced the utilization strategies of avian communities regarding habitat assemblages. This influence was evident both in the structure and proportion of habitat assemblages, with the degree of impact differing across various avian communities.

Our findings indicate that Groups A, C, D, E, H, I, and J exhibited heightened sensitivity to seasonal variations, whereas Groups F and G demonstrated a more stable response with minimal influence from seasonal changes. Notably, within these groups, Groups A and D showed a marked preference for lake body-type habitats, such as the aquatic vegetation zone (PW) and the main body of water (MW), during the autumn and winter months. Conversely, their utilization of river and pond (RW) habitats increased significantly during the spring and summer seasons. Group C, which encompasses avian species such as Ardea cinerea (ARDCIN) and Egretta garzetta (EGRGAR), utilized a combination of three distinct habitat types—aquatic vegetation zone (PW), main body of water (MW), and unvegetated mudflat (BW)—during the autumn and winter seasons. Conversely, a higher number of individuals were observed in the evergreen broadleaf forest (EF) during the spring and summer. Similarly, Groups H and I exhibited a marked increase in the utilization of the evergreen broadleaf forest (EF) throughout the spring and summer periods. In contrast, the primary habitat for Group E transitioned from buildings, roads, and facilities (BR) during autumn and winter to shrubland (SH) in spring and summer. Similarly, habitat assemblage utilization for Group J exhibited seasonal variation. Group J predominantly occupied buildings, roads, and facilities (BR) in autumn and winter, shifted to grassland (GR) in spring, and showed a preference for deciduous broadleaf forest (DF) in summer.

4.1 Habitat assemblages better explain differences in the distribution of avian communities

In urban fringe areas, the distribution of avian communities is shaped by a multifaceted interplay of habitat factors. Although investigations focused on individual habitat types have yielded preliminary insights into avian habitat selection (Hansen et al. 1995; Brotons et al. 2004), these studies frequently encounter difficulties in comprehensively elucidating the intricate distribution patterns of avian communities. Similarly, traditional studies utilizing indicator species frequently rely on the presence or absence of avian species to infer the quality of a specific habitat (Canterbury et al. 2000; Larsen et al. 2011; Renwick et al. 2012). However, these studies often fail to adequately consider the potential impacts of habitat assemblages on avian distributions. Moreover, they tend to overlook the significance of regional habitat selection by avian species in shaping the diversity of ecological communities, as well as the critical role of resource complementarity in species distribution and ecological processes. In this study, our analyses revealed the unique advantages of habitat assemblages in explaining differences in avian community distributions.

Among the 95 avian species effectively documented, 60 were observed across multiple habitat types. These avian groups exhibited distinct patterns in their utilization of habitat assemblages, with varying degrees of emphasis on specific habitat types within these assemblages. This phenomenon can be attributed to the spatial segregation of resources, which enables avian species to perform essential ecological functions such as foraging, roosting, breeding, and sheltering by navigating between different habitat patches to access a variety of resources (Chalfoun and Schmidt 2012; Zheng et al. 2015). For instance, Group E, which encompasses avian species such as Bambusicola thoracicus (BAMTHO), Lonchura striata (LONSTR), and Myophonus caeruleus (MYOCAE), is associated with a habitat combination type classified as (GR-SH). Grassland (GR) habitats offer an abundance of food resources, including seeds, insects, and other nutritional elements (Pithon et al. 2021b). Additionally, the open environments of grasslands facilitate efficient foraging behaviors, such as rapid walking (Watson 2015). However, it is also noteworthy that shrubland (SH) serves as a secondary habitat of choice, providing shelter and supplementary food resources, particularly during breeding periods or times of resource scarcity (Schlossberg 2009). A comparable situation was examined in the study, which identified significant differences between nesting and foraging habitats for ravens(Mueller et al. 2009). Specifically, deciduous forests and open areas were found to be favorable for foraging, whereas nesting and breeding sites were predominantly located in coniferous forests. The significance of this habitat assemblage is equally critical for certain wetland birds (Pyrovetsi and Crivelli 1988; Musilová et al. 2022). Specifically, in Group C, species such as Ardea cinerea (ARDCIN), Egretta garzetta (EGRGAR), and Tringa ochropus (TRIOCH) rely on the abundance of fish, insects, and small invertebrates provided by unvegetated mudflat (BW), which are essential for their survival (Danufsky and Colwell 2003). Concurrently, these avian species benefit from the favorable visual conditions offered by the main body of water (MW) (Roth and Lima, 2003). However, the aquatic vegetation zone (PW) and evergreen broadleaf forest (EF) serve as essential refuges for these avian species, offering crucial protection particularly in the context of evading natural predators and human disturbances (Kang et al. 2015).

Habitat assemblages facilitate a more nuanced understanding of avian habitat selection and ecological requirements by incorporating multiple habitat types and leveraging resource complementarity. This methodology surpasses the conventional single-habitat approach, offering a more profound insight into avian distributions, particularly in urban fringe areas characterized by high habitat heterogeneity. Our findings offer novel explanatory perspectives on the contributions of habitat diversity (Leveau 2019) and habitat heterogeneity (Machar et al. 2022) to avian diversity and community stability. Simultaneously, the landscape complementarity and replenishment hypothesis (Dunning et al. 1992) furnished theoretical support for our investigation, elucidating how the complementarity of habitat patches can augment avian community diversity by offering a variety of resources and roosting spaces.

4.2 Seasonal variation significantly influences avian group utilization strategies of habitat assemblages

Seasonal variations exert a significant influence on ecosystems, shaping ecological processes and biological behaviors (Post and Stenseth 1999). For instance, fluctuations in temperature, alterations in precipitation patterns, and plant growth cycles can directly impact the availability and distribution of resources within habitats. These changes subsequently affect the foraging, breeding, and roosting behaviors of avian species (Beerens et al. 2011). Investigations into the responses of habitat assemblages to seasonal changes are crucial for elucidating ecosystem functions and mechanisms of species adaptation.

Our research demonstrated that seasonal variation significantly influenced the strategies employed by avian communities in utilizing habitat assemblages. Specifically, avian species exhibit distinct life activity patterns across different seasons (Winger et al. 2019). During spring and summer, which are typically the breeding seasons, there is an increased demand for breeding habitats, for instance, seven avian groups exhibited varying degrees of increased utilization of evergreen broadleaf forest (EF) during the spring and summer seasons. The appeal of EF to avian communities during these periods can be attributed to its provision of abundant breeding resources, including insects, fruits, and seeds (Betts et al. 2010), as well as a relatively sheltered breeding environment. The autumn and winter seasons are critical periods for migratory birds, during which lacustrine habitats such as the main body of water (MW) and the aquatic vegetation zone (PW) offer abundant high-protein and high-fat food resources, including fish, shrimp, and aquatic insects (Baschuk et al. 2012). These resources facilitate the rapid replenishment of migratory birds, resulting in significantly higher utilization of these habitats by Groups A and C compared to the spring and autumn seasons. Conversely, alterations in the physical environment resulting from seasonal variations influence not only the spatial extent and structure of avian habitats but also the spatial and temporal distribution and abundance of resources (Leira and Cantonati 2008). These factors collectively determine habitat suitability and functionality. Avian species adapt to these habitat changes, leading to adjustments in their utilization strategies of the combined habitats. Yinglong Lake Wetland Park exemplifies a reservoir-type wetland ecosystem. Seasonal fluctuations in water levels during autumn and winter result in the exposure of mudflats and shallow water areas, which in turn support diverse vegetation. These heterogeneous habitats offer abundant foraging resources, including invertebrates, fish, aquatic insects, and plant seeds (Traut and Hostetler 2004). Consequently, this environment attracts various avian groups, such as Groups A, C, and D, leading to an increased proportion of habitat utilization within the lake body.

We investigated the impact of seasonal variation on avian communities with respect to habitat assemblages. Our findings indicate that habitat assemblages not only offer a diverse array of resources that support avian diversity, but also facilitate the adaptation of avian communities to environmental changes through flexible habitat utilization strategies. This finding enhances our comprehension of the impact of habitat diversity on the interplay between ecosystem stability and species diversity (Alsterberg et al. 2017). Furthermore, when considered alongside the mechanisms of resource partitioning and adaptation as elucidated in ecological niche theory (Chesson 2000), it underscores the critical role of habitat assemblages in sustaining ecosystem function and promoting avian diversity.

4.3 Recommendations for habitat construction and biodiversity conservation in urban fringes

Habitat creation and biodiversity conservation in urban fringe areas continue to pose significant challenges and complexities in the context of urban development, necessitating targeted research to inform effective conservation practices(McKinney 2008b). Our findings indicate that habitat assemblages are crucial in supporting avian diversity in urban fringe areas, offering novel insights into habitat construction and biodiversity conservation in these areas.

Based on an integration of habitat characteristics and the requirements for avian community diversity in fringe areas, we advocate for the enhancement of avian diversity through the creation and optimization of heterogeneous habitat assemblages. This strategy encompasses the delineation of functional habitat zones, including breeding refuges and high-resource-density foraging areas, with dynamic adjustments in response to seasonal variations and avian life cycles. Such measures are essential to ensure the availability of critical resources and habitats during migratory and breeding seasons. Furthermore, given that the spatial configuration and quality of habitats significantly influence species survival and migration (Donnelly and Marzluff 2006), it is advisable to consider spatially optimizing the quality of adjacent habitats. This optimization would enable avian species to fulfill their ecological requirements within a more confined spatial area, thereby reducing the movement costs and energy expenditures associated with resource acquisition. Consequently, this approach could mitigate the adverse effects of habitat fragmentation and enhance the efficiency of habitat utilization (Johnson 2007). For instance, the quality of adjacent habitats surrounding major lake bodies can be enhanced through several measures. These include adjusting the planting density and type of aquatic vegetation to augment the availability of food resources, establishing forested swamps around the lake bodies, and optimizing broadleaved evergreen forests to improve the quality of refuges for migratory birds. Additionally, the natural form and ecological functions of mudflats can be preserved by regulating water levels and implementing appropriate artificial restoration techniques. Collectively, these measures function to harmonize and optimize the primary water body with the surrounding habitats, thereby supporting the roosting, foraging, and breeding requirements of migratory birds.

From a conservation management perspective, seasonal variations offer crucial insights into habitat management due to their substantial influence on the habitat utilization strategies of avian communities. To address the seasonal requirements of avian species, we recommend augmenting conservation efforts for lacustrine habitats during autumn and winter. This could involve replanting peri-lake areas with high-protein flora, such as legumes or specific aquatic plants, to enhance the food resources available for migratory birds (Fox et al. 2017). During the spring and summer seasons, efforts are concentrated on safeguarding breeding habitats, particularly broadleaf evergreen forests, through various measures. These include minimizing human disturbance in critical resource areas, preserving existing natural nesting sites, and planting fruit trees or berry shrubs to offer supplementary food sources and shade for breeding birds. Such initiatives are designed to enhance breeding success (Snow and Snow 2010). These actions not only address the seasonal requirements of avian species but also contribute to the overall improvement of habitat quality, thereby supporting avian diversity and promoting the long-term health and stability of the peripheral ecosystem.

Our findings indicate that habitat assemblages are crucial in elucidating the distributional disparities and diversity of avian communities in urban fringe areas. Concurrently, seasonal variation markedly affects the utilization of habitat assemblages by these avian communities. We propose that the development and optimization of diverse habitat assemblages, the seasonal adjustment of habitat resources, and the regulation of anthropogenic disturbances can significantly enhance biodiversity conservation in marginal landscapes. This study deepens the understanding of how habitat diversity in urban fringelands supports avian diversity. Habitat assemblages demonstrated distinct advantages in offering a variety of resources and habitat spaces, surpassing the scope of research focused on a single habitat type. This finding establishes a novel foundation for informing habitat construction and biodiversity conservation efforts in urban fringe areas. Future research should investigate the long-term responses of avian communities and assess the stability and efficacy of habitat assemblages. Additionally, comparative studies across different regions are essential to validate the generalizability and applicability of habitat assemblages in diverse ecosystems.

Competing Interests:

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Funding:

This work was supported by the National Natural Science Foundation of China under Grant Nos. 52078074 and 52238003, the Fundamental Research Funds for the Central Universities (No. 2024CDJXY014), and the Performance Incentive and Guidance Special Project of the Chongqing Municipal Science and Technology Bureau (No. cstc2022jxjl20018).

Author Contribution

All authors contributed to the study review and editing. Data collection was performed by Q.Z. and J.W. Analysis was performed by J.W. and D.L. Conceptualization and methodology were carried out by B.L. and C.D. The first draft of the manuscript was written by B.L. and J.W. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Acknowledgement

Data Availability:

The datasets generated during the current study are available from the corresponding author on reasonable request.

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Rather than single habitat types, habitat assemblages may significantly shape avian communities in urban fringe

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