Subtropical Broad-Leaved Urban Forests as the Foremost Dynamic and Complex Habitats for a Wide Range of Bird Species

Abstract

Broad-leaved subtropical forests are the most productive, diversified, and complex ecosystems on the planet. Unfortunately, they are currently under severe threat from anthropogenic activities, such as. deforestation, housing settlements, and agricultural expansion. In response to these severe effects, the present study was conducted to explore the current conservation status and population structure of a wide range of bird species inhabiting different subtropical broad-leaved urban forests of Pakistan. In total, 2879 individuals comprising 53 species and 28 families were detected between December 2017 and November 2018 as revealed through the distance sampling line transect method. The habitat selection among bird species varied according to vegetation structure and composition, food resources, adjoining habitats, and human settlements. According to IUCN Red List data, one species was deemed vulnerable out of 53 bird species, while the remaining 52 species were ranked as ofleast concern. The findings of the density analysis revealed that bird density varied between six subtropical broad-leaved forests. Palamar (3.954 ± 0.221 birds/ha) and Kityari (3.138 ± 0.162 birds/ha) were densely populated, whereas Kamal Khan (1.102 ± 0.178 birds/ha) was of the least concern. Likewise, the diversity analysis showed that Kamal Khan was a more diverse habitat (Shannon–Wiener Index; H’ = 3.581 ± 0.021). Shahabad was richer (Margalef Richness Index; R1 = 8.007 ± 0.053) and Dob Ghar was evenly distributed (Pielou J Evenness Index; E = 0.940 ± 0.005) compared to other urban habitats studied. Eight foraging guilds were identified among the bird species. Insectivores were the most abundant bird species utilizing the urban dwelling habitats. carnivores/piscivores/insectivores utilized Dob Ghar forest, while more frugivores utilized Kamal Khan and Dob Ghar. Based on the data, it was concluded that subtropical broad-leaved urban forests are dynamic, complex, and of vital significance for a diverse range of bird species.

1. Introduction

Broad-leaved subtropical forests are among Pakistan’s most productive, diversified and complex ecosystems [1], covering approximately 30–40% of the country’s ’s forest area [2]. In broad-leaved subtropical forests, the composition of vegetation is dominated by persistent and semi-persistent deciduous species. The main tree and shrub species that grow in the habitats include Indian horse chestnut (Aesculus indica), Indian maple (Acer caesium), tapering leaf maple (Acer acuminatum), Himalayan elm (Ulmus wallichiana), West Himalayan alder or sharol (Alnus nitida), kamala or kumkum tree (Mallotus philippensis), Indian willow (Salix tetrasperma), common fig (Ficus carica), chamror (Ehretia aspera), and sweet plum (Sageretia theezans). The shrubs comprised kau (Olea ferruginea), phulai (Acacia modesta), fragrant bay tree (Persea odoratissima), Christmas flower (Phoebe pulcherrima), Indian laburnum (Cassia fistula), phulai (Acacia modesta) and snatha (Dodonaea viscosa, Berberis lyceum, Indigo fera, Carica spinarium), common buckthorn (Rhamnus pentapomica) and mallah ber (Zizyphus nummularia). Grass species include aucher’s grass (Chrysopogon aucheri), elephant grass (Pennisetum purpureum), tanglehead grass (Heteropogon contortus), sabai grass (Eulaliopsis binate), buffelgrass (Cenchrus ciliaris), khabbal (Cynodon dactylus), and other turfgrasses. The vegetation diversity and cover percentage are crucial variables used to predict the relative abundance of avian species and richness [3,4]. Complex floristic compositions harbor a wide array of avian species [5].

Urban forests are ecotones that are rich in diverse of vegetation and food supplies that harbor a range of of bird species [6,7,8] and are considered as hotspots of biodiversity [9,10]. Birds are a vital indicator of the ecosystem of an urban forest [11]. Avian community parameters are impacted by the extent of spatiotemporal dissemination of floristic structure, microclimate conditions and food resources [12,13]. These resources are key factors that determine when and which bird species reside in a particular urban forest habitat. Birds prefer sites that fulfill their needs, such as water, cover, and breeding shelter [14,15]. Birds are food and habitat specialists motivated by richness and diversity; they often select urban forest habitats to satisfy their needs [16,17]. Furthermore, the urban forest habitats are critical for halting biodiversity loss [18], providing ample potential habitats for birds [19,20], and increasing availability of distinct niches to exploit [21]. They also provide a diverse range of benefits for human well-being [22,23].

The urban forests possess characteristics that help to conserve bird species, creating a one-of-a-kind set of challenges [24]. Birds in urban woods are diverse and numerous, and they frequently form complex groups [25]. They may differ from region to region [26,27]. Birds are an integral component of broad-leaved subtropical urban forests and play important roles in protecting them, such as managing the pest populations that can destroy seeds, leaves, and roots of trees, shrubs, and grasses [28]. In addition, the flowers of trees and shrubs are pollinated by avian species to increase the development of seeds. They spread seeds from one region to another through droppings, which may assist in regeneration. Birds are also the best bioindicators of the health of a subtropical broad-leaved forest ecosystem (two–thirds of bird species occupy forested habitats). Their presence in a broad-leaved forest ecosystem indicates productivity and habitat suitability [29,30,31]. Birds are experts in habitat and food that have occupied every conceivable habitat and niche diversity in the food chain and food web of the forest. Unfortunately, urban forests are facing overwhelming threats due to the invasion of non-native plant species and human interventions such as continuous sprawl, development of housing settlements and expansion of agriculture, which may decrease habitat suitability and productivity [32,33]. Furthermore, these urban forests are deforested, degraded, isolated, and converted into agricultural fields and human settlements, which has caused bird populations to decline. Hence, we strongly recommend that these urban forests be protected on a priority basis. Habitat loss and degradation reduces the suitability and productivity of ecosystems, resulting in declines in the populations of many species of forest birds [34,35,36]. Some species become vulnerable, endangered, threatened, critically endangered, and even vanish due to illegal hunting for bushmeat, habitat destruction from deforestation, and the introduction of invasive species into primary ecosystems [37,38,39].

There is still insufficient comprehensive information on bird conservation status and population structure in various subtropical broad-leaved urban forests. For conservation activities, the determination of the conservation status of bird species and population structure (relative abundance, indices of diversity, and density) are of critical importance [40,41]. Determining conservation status enables the assessment of the vulnerability of endangered or threatened bird species and their habitats based on their distribution across heterogeneous urban forest habitats. This aids in prioritizing the protection of endangered birds [42,43,44]. The objective of the present study is to determine the conservation status and population structure of a wide range of bird species inhabiting different subtropical urban forests to ensure that bird conservation increases the population and minimizes the potential threats. The second objective is to determine the urban forest that harbors the highest bird diversity and density. The third objective is to determine the species that are endangered or threatened and should be protected on a priority basis.

2. Materials and Methods

2.1. Study Area

The present research work was conducted in subtropical broad-leaved urban forests, namely Dob Ghar, Kamal Khan, Kityari, Palamar, Seya Sar, and Shahabad, occurring 1600–3300 feet elevation above mean sea level in the inner foothills of the Himalayas in Pakistan (Figure 1). These forests contain evergreen trees and shrubs varying in floristic composition, ranging from dense to scattered canopy and groups in well-protected sites.

These forests are the transitional ecosystem between coniferous and thorn forests. The vegetation encompasses the trees such as Indian horse–chestnut (Aesculus indica), Indian maple (Acer caesium), tapering leaf maple (Acer acuminatum), Himalayan elm (Ulmus wallichiana), West Himalayan alder or sharol (Alnus nitida), kamala or kumkum tree (Mallotus philippensis), Indian willow (Salix tetrasperma), common fig (Ficus carica), chamror (Ehretia aspera), and sweet plum (Sageretia theezans). The shrubs comprised kau (Olea ferruginea), phulai (Acacia modesta), fragrant bay tree (Persea odoratissima), Christmas flower (Phoebe pulcherrima), Indian laburnum (Cassia fistula), phulai (Acacia modesta) and snatha (Dodonaea viscosa, Berberis lyceum, Indigo fera, Carica spinarium), common buckthorn (Rhamnus pentapomica) and mallah ber (Zizyphus nummularia). Grass species include aucher’s grass (Chrysopogon aucheri), elephant grass (Pennisetum purpureum), tanglehead grass (Heteropogon contortus), sabai grass (Eulaliopsis binate), buffelgrass (Cenchrus ciliaris), khabbal (Cynodon dactylus), and other turfgrasses. The vegetation diversity forms a multi-layered canopy comprising trees, shrubs, and grasses. Depending on rainfall pattern, aspect, topography, elevation and anthropogenic variables such as unregulated grazing, selection of heavy fuelwood, and land use pattern, the composition of vegetation species varies from site to site. Each urban forest represents a distinct habitat type supporting different avian species. The characteristics of each habitat are given in

Table 1. Descriptions of each subtropical broad-leaved urban forest habitat.

Description	Name of Subtropical Broad-Leaved Urban Forest
	Dob Ghar	Kamal Khan	Kityari	Palamar	Seya Sar	Shahabad
Latitude	34°43′36″ N	34°42′32″ N	34°44′46″ N	34°46′46″ N	34°47′44″ N	34°45′31″ N
Longitude	72°05′56″ E	72°05′53″ E	72°04′29″ E	72°0′04″ E	72°01′26″ E	71°59′47″ E
Elevation feet (asl)	3942 to 4487 feet	3017 to 3966 feet	2968 to 3125 feet	4044 to 4959 feet	5015 to 5822 feet	3319 to 3775 feet
Landscape	Comprises hilly terrain dominated by small trees and shrubs	Encompasses hilly terrain and riparian areas	Contains hilly terrain ridges that are covered by coniferous vegetation on a higher elevation	It is a transition zone between coniferous and scrub vegetation, surrounded by agricultural fields	Comprises inner ridges of the mountains	It is a hilly terrain dominated by evergreen vegetation
Vegetation Cover %	30.0%	38.0%	70.0%	50.0%	45.0%	40.0%
Total area	150 ha	135 ha	140 ha	145 ha	130 ha	125 ha
Surveyed area	50 ha	45 ha	46 ha	46 ha	65 ha	55 ha
Most Dominant flora	Phulai (Acacia modesta), kau (Olea ferruginea), snatha (Dodonaea viscosa), mallah ber (Zizyphus nummularia), yellow Himalayan raspberry (Rubus ellipticus), shrubby blackberry(Rubus fruticosus), Scarlet spiderling (Boerhavia coccinea)	White mulberry (Morus alba), black mulberry (Morus nigra), common fig (Ficus carica), paper mulberry (Broussonetia papyrifera), bhimal (Grewia optiva), bakain or dharek (Melia azedarach), snatha (Dodonaea viscosa), mallah ber (Zizyphus nummularia), yellow Himalayan raspberry (Rubus ellipticus)and shrubby blackberry (Rubus fruticosus)	Chir pine (Pinus roxburghii), snatha (Dodonaea viscosa), blackberry (Rubus fruticosus), mallah ber (Zizyphus nummularia), yellow Himalayan raspberry (Rubus ellipticus), shrubby blackberry (Rubus fruticosus), Bermuda grass (Cynodon dactylon), bluegrass (Poa annua) and tall fescue (Festuca arundinacae)	Chir pine (Pinus roxburghii), kamala or kumkum tree (Mallotus philippensis), kau (Olea ferruginea), Snatha (Dodonaea viscosa), wild anar (Punica granatum), bhaikar (Adatoda vasica), Indian Lycium (Berberis lycium), Indigo (Indigfera trictoria), bhaikar or beheda (Justicia adhatoda), royale’s spike thorn (Gymnosporia royleana), and barbery (Berberis lyceum)	Chir pine (Pinus roxburghii), kau (Olea ferruginea), snatha (Dodonaea viscosa), bhaikar or beheda (Justicia adhatoda), scarlet spiderling (Boerhavia coccinea), and bhaikar or beheda (Justicia adhatoda)	Phulai (Acacia modesta), white mulberry (Morus alba), black mulberry (Morus nigra), kau (Olea ferruginea), snatha (Dodonaea viscosa), Indian lycium (Berberis lycium), bhaikar or beheda (Justicia adhatoda), and barbery (Berberis lyceum)
Surrounding habitat	Agricultural fields and human settlements	Agriculture fields and human settlement	Agriculture fields and human settlement	Agriculture fields	Agriculture fields and human settlement	Agriculture fields and orchards

.

2.2. Bird Survey

The distance sampling line transect method is the most robust, accurate and efficient method of ascertaining the avian community parameters in different territories [45,46]. This technique measured the perpendicular distance between the bird and the observer through visual approximation. DISTANCE Software (version 7.0 St Andrews, Fife, Scotland) computes x values that can be used to determine the degree of the avian populace [45]. Bird location exactness and reliability depend on natural conditions, species range, and spectator aptitudes [47,48]. The problem of variable discovery is solved by distance sampling and accurate density estimates [49]. In total, 120 transect lines were established randomly over a hilly topography (20 transect lines in each habitat with a length of 2 km) to assess bird populations in each habitat. Birds were detected early in the morning from 7:30 a.m. to 11:00 a.m. from December 2017 to November 2018.

All the birds seen and heard were listed in each survey. By visual assessment, the perpendicular distance between the birds and the transect line was recorded. Opportunistic observations of airborne birds of unknown origin were also reported but were not included in the analysis. Buckland et al. [45], Gregory et al. [50], Aborn [51], and Nadeau et al. [52] were the basis for the sampling method.

2.3. Data Analysis

2.3.1. Relative Species Abundance

Relative abundance is the number of bird individuals of a particular species that occupy the subtropical broad-leaved urban forest habitat. A bird’s relative abundance often changes with time, altitude, aspect, weather conditions, geographic range and rebuilding endeavors [53,54]. The relative abundance of bird species in each urban forest was assessed using the following equation:

$$\mathrm{Relative}\mathrm{species}\mathrm{abundance}(\%)=\mathrm{Isi}/{{\displaystyle \sum }}^{}\mathrm{Nsi}\times 100$$

where Isi = Total number of bird individual species and ∑Nsi = Total number of bird species [55].

2.3.2. Bird Relative Abundance among Six Coniferous Forests

Bird relative abundance was compared using one-way analysis of variance (ANOVA) and Tukey’s honestly significant difference (HSD) test (Analytical Software, version 8.1) by McGraw–Hill (located in New York City, NY, USA) [56].

2.3.3. Bird Density

Ascertaining the exact population size is imperative in obtaining the current population status of different bird species in a dwelling habitat. The bird population was determined through the DISTANCE Software (Version 7.1) by Buckland (located in AK Northwest Arctic Borough, USA) et al. [45]. The key to distance sampling is to utilize the distribution of the observed distances to determine the detection function g (y). This is the probability of ascertaining the bird at distance y. This function can then be used to determine the mean probability of detecting a bird given that it is within w of the point, denoted Pa. Given an estimate of Pa, bird density can be determined using the following equation:

$$\widehat{\mathrm{D}}=\frac{1}{\mathrm{a}}{\displaystyle \sum }_{\mathrm{i}=1}^{\mathrm{n}}\frac{1}{\widehat{{\mathrm{P}}_{\mathrm{a}}}\left({\mathrm{z}}_{\mathrm{i}}\right)}$$

where a is the size of the covered region, n is the number of birds detected, and $\widehat{{\mathrm{P}}_{\mathrm{a}}}$ (Z_i) is the probability of detecting the i^th bird given that it is within w of the point and has the covariate values Z_i [47,57,58].

2.4. Diversity Indices

Examining the distinguishing features in avian assemblages and diversity is a critical step in depicting of subtropical broad-leaved urban forest habitats. Diversity indices such as species diversity, species richness, and regularity were identified using the Community Analysis Package by Henderson and Seaby [59] (CAP, version 4.0, Pisces Conservation Ltd, Lymington, UK). In this study, the avian Shannon Diversity Index, Margalef Richness Index, and Pielou J Evenness Index were investigated in six broad-leaved forest habitats to determine which urban forest habitat was more attractive to birds.

2.4.1. Species Diversity Index

The Species Diversity Index takes into account the number of birds in a particular urban forest ecosystem. It indicates relative abundance, population scarcity and dominance. The bird variability, richness and distribution often varied between urban forests. This index accounts for plenitude by giving data on the irregularity and commonality of bird species. Shannon’s Diversity Index is calculated as follows:

$$\acute{\mathrm{H}}=-{{\displaystyle \sum }}_{\mathrm{i}}^{\mathrm{s}}\left[\left(\mathrm{pi}\right)\times \ln \mathrm{pi}\right]$$

(1)

where H’ designates diversity, s indicates the number of species, i specifies the abundance of species, p_i is the relative abundance of each species, and ln is the natural logarithm.

2.4.2. Species Richness Index

The Species richness index indicates the number of diverse bird species that occur in an urban habitat. It provides more data on the homogeneity and irregularity of bird distribution and occurrence. Margalef Richness Index (R) is calculated as follows:

$$\mathrm{R}=\left(\mathrm{S}-1\right)/\ln \mathrm{N}$$

(2)

where S is the total number of species and N is the total number of individuals in the sample.

2.4.3. Species Evenness Index

The species evenness index is the degree of the relative plenitude of distinctive bird species in a specific range. Pielou J Evenness Index (J) is calculated as follows:

$$\mathrm{J}=\mathrm{H}/\log \left(\mathrm{S}\right)$$

(3)

where H is the observed Shannon-Wiener Index and S is the total number of bird species in the coniferous forest.

2.5. Comparison of Bird Diversity Indices in Six Subtropical Broad-Leaved Urban Forest Habitats

A Kruskal-Wallis ANOVA and a Tukey’s HSD test (Analytical Software, version 8.1) were used to investigate the significance of differences in diversity indices between six subtropical broad-leaved forest habitats [56].

2.6. Comparison of Foraging Guild Structure in Six Subtropical Broad-Leaved Urban Forest Habitats

The structure of the feeding guild is an assemblage of bird species that consume the same food resources using different techniques. Bird species were grouped into eight guilds based on dietary behavior, food selection, and territory preferences. The method used as described by Nebel et al. [60], Leso and Kropil, [61], and Pinotti et al. [35].

3. Results

3.1. Bird Species Composition and Relative Abundance

In total, 2879 bird individuals representing 53 species from 28 families were detected in 6 subtropical urban broad-leaved forest habitats. These habitats were Shahabad, (49 species; 594 birds), Seya Sar (45 species; 391 individuals), Palamar (50 species; 497 detections), Kamal Khan (47 species; 437 individuals), Dob Ghar (51 species; 515 individuals) and Kityari (46 species; 445 individuals) (

Table 2. List of bird species detected in six broad-leaved urban forest habitats.

Family Name	Scientific Name	Common Name	Name of Urban Forest Habitat
			Shahabad	Seya Sar	Palamar	Kamal khan	Dob Ghar	Kityari	IUCN Status
			Relative Species Abundance (%)
Sturnidae	Acridotheres tristis	Common myna	1.216	1.042	0.938	1.111	0.729	1.389	LC
Corvidae	Corvus splendens	House crow	1.042	0.347	0.278	0.556	0.175	2.779	LC
Fringillidae	Carpodacus erythrinus	Common rosefinch	1.042	1.216	0.521	0.695	0.347	1.042	LC
Passeridae	Passer montanus	Eurasian tree sparrow	1.042	0.799	0.590	0.452	0.347	1.111	LC
Phasianidae	Alectoris chakur	Chakur	0.868	0.695	1.216	0.243	0.417	0	LC
Passeridae	Passer domesticus	House sparrow	0.729	0.347	0.347	1.042	0.521	1.737	LC
Sturnidae	Sturnus vulgaris	Common starling	0.729	0.417	0.347	0.278	0.625	0.417	LC
Hirundinidae	Hirundo rustica	Common swallow	0.695	0.347	0.278	1.042	0.695	0.799	LC
Leiothrichidae	Turdoides caudate	Common babbler	0.695	0.347	0.695	0.868	0.521	0.868	LC
Dicruridae	Dicrurus macrocercus	Black drongo	0.625	0.417	0.521	0.695	0.347	0.695	LC
Leiothrichidae	Trochalopteron lineatum	Streaked laughing thrush	0.625	0.208	0.521	0.417	0.347	0.521	LC
Phasianidae	Coturnix coturnix	Common quail	0.521	0.347	0.521	0.695	0.695	0.417	LC
Monarchidae	Terpsiphone paradise	Indian paradise flycatcher	0.521	0.695	0.521	0.695	0.347	0.868	LC
Paridae	Parus cinereus	Cinereous tit	0.521	0.695	0.625	0.417	0.452	0.695	LC
Pycnonotidae	Pycnonotus cafer	Red–vented bulbul	0.521	0.695	0.625	0.521	0.347	0.521	LC
Sturnidae	Sturnus pagodarum	Brahminy starling	0.521	0.069	0.278	0.208	0.139	0.347	LC
Turdidae	Turdus atrogularis	Black–throated thrush	0.521	0.695	0.868	1.042	0.695	0.139	LC
Emberizidae	Emberiza cia	Rock bunting	0.452	0.695	0.278	0.139	0.347	0.278	LC
Corvidae	Corvus macrorhynchos	Large–billed crow	0.347	0.521	0.417	0.175	0.347	0.139	LC
Laniidae	Lanius tephronotus	Grey–backed shrike	0.347	0.313	0.243	0.278	0.347	0.695	LC
Phylloscopidae	Phylloscopus collybita	Common chiffchaff	0.347	0.243	0.486	0.625	0.521	0.417	LC
Pycnonotidae	Pycnonotus leucogenys	Himalayan bulbul	0.347	0.278	0.347	0.451	0.313	0.208	LC
Columbidae	Streptopelia orientalis	Oriental turtle dove	0.313	0.175	0.278	0.243	0.175	0.278	LC
Oriolidae	Oriolus oriolus	Golden oriole	0.313	0.347	0.417	0.486	0.452	0.660	LC
Alaudidae	Galerida cristata	Crested lark	0.278	0.139	0.069	0.104	0.069	0.139	LC
Columbidae	Streptopelia turtur	European turtle dove	0.243	0.139	0.104	0.175	0.243	0.139	VU
Columbidae	Streptopelia chinensis	Spotted dove	0.208	0.417	0.347	0.175	0.069	0.139	LC
Columbidae	Columba livia	Rock pigeon	0.175	0.347	0.243	0.139	0.069	0.069	LC
Laniidae	Lanius vittatus	Bay–backed shrike	0.175	0.139	0.069	0.139	0.175	0.347	LC
Motacillidae	Motacilla alba	White wagtail	0.175	0.139	0.556	0.347	0.139	0.347	LC
Falconidae	Falco tinnunculus	Common kestrel	0.139	0.139	0.175	0.104	0.069	0.069	LC
Phasianidae	Francolinus francolinus	Black francolin	0.139	0.104	0.278	0.175	0.208	0.069	LC
Muscicapidae	Saxicola caprata	Pied bushchat	0.139	0.175	0.139	0.208	0.278	0.208	LC
Phylloscopidae	Phylloscopus chloronotus	Lemon–rumped warbler	0.139	0.278	0.104	0.175	0.452	0.347	LC
Corvidae	Dendrocitta vagabunda	Rufous treepie	0.104	0.069	0.069	0.139	0.069	0.139	LC
Motacillidae	Motacilla cinerea	Grey wagtail	0.104	0.139	0.208	0.139	0.069	0.208	LC
Accipitridae	Accipiter virgatus	Besra	0.069	0.035	0.104	0.069	0	0.035	LC
Upupidae	Upupa epops	Common hoopoe	0.069	0	0.104	0	0.069	0.069	LC
Columbidae	Streptopelia senegalensis	Laughing dove	0.069	0.243	0.104	0.069	0.139	0.139	LC
Columbidae	Treron phoenicoptera	Yellow-footed green pigeon	0.069	0.035	0	0	0	0.069	LC
Alcedinidae	Halcyon smyrnensis	White–throated kingfisher	0.069	0.069	0.035	0.069	0	0.069	LC
Coraciidae	Coracias benghalensis	Indian roller	0.069	0.035	0	0.035	0	0.069	LC
Cuculidae	Eudynamys scolopacea	Asian koel	0.069	0	0	0.035	0	0.104	LC
Muscicapidae	Myophonus caeruleus	Blue whistling thrush	0.069	0.139	0.069	0.139	0.139	0.104	LC
Muscicapidae	Copsychus saularisi	Oriental magpie robin	0.069	0.069	0	0.069	0	0.069	LC
Phylloscopidae	Phylloscopus trochiloides	Greenish warbler	0.069	0.175	0.243	0.347	0.243	0.278	LC
Pycnonotidae	Pycnonotus leucotis	White–eared bulbul	0.069	0.104	0.139	0.347	0.521	0.139	LC
Sturnidae	Acridotheres ginginianus	Bank myna	0.069	0	0	0.208	0	0	LC
Strigidae	Glaucidium brodiei	Collard owl	0.069	0.069	0	0.313	0.139	0.139	LC
Accipitridae	Accipiter badius	Shikra	0.035	0.035	0.069	0.035	0.035	0	LC
Columbidae	Columba hodgsonii	Speckled wood pigeon	0.035	0	0.035	0	0	0.069	LC
Accipitridae	Elanus caeruleus	Black–shouldered kite	0	0	0	0.104	0.069	0.035	LC
Meropidae	Merops orientalis	Green bee–eater	0	0	0.035	0.069	0.069	0	LC
Overall Percentage			17.885	15.18	15.45	17.301	13.580	20.627
Sub-Total			515	437	445	497	391	594
Grand Total			2879

). Out of 53 bird species, 1 species was vulnerable (VU) whereas the other 52 species were ranked of least concern (LC) according to the IUCN Red List. The relative abundance of avian species may vary from habitat to habitat. For example; common myna in Dob Ghar (35 detections), Kamal Khan (30 detections) and Kityari (27 detections); chakor in Kityari (35 detections); and house crow in Shahabad (80 detections) were the most common bird species in six urban forests. In contrast, shikra and speckled wood pigeon (Shahabad), shikra, yellow-footed green pigeon, and Indian roller (Seya Sar); blue whistling thrush, white-throated kingfisher and green bee-eater (Palamar); shikra, Indian roller and Asian koel (Kamal Khan); shikra (Dob Ghar); and shikra and black-shouldered kite (Kityari) were the rarest bird species, each recorded once (Table 2). The abundance-ranking curve showed the distribution patterns of relative abundance of bird species in six subtropical urban broad-leaved forest habitats.

The abundance analysis curve provided information on abundance, proportionate abundance, logarithmic abundance, and accumulated proportionate plenitude. The abundance curve is a 2D graph with relative abundance on the Y-axis and abundance rank on the X-axis. The graph indicates that the relative abundance of birds in six habitats can vary between territories. The curve shows the dispersion of bird species. The steep slope was low regularity. The high–ranking species were more common than the low-ranking species. In addition, the shallow gradient had the most elevated consistency (Figure 2).

3.2. Comparison of Bird Density in Six Subtropical Broa-Dleaved Urban Forest Habitats

The findings showed that Palamar (3.954 ± 0.221 birds/ha) and Kityari (3.138 ± 0.162 birds/ha) were the dynamic subtropical urban broad-leaved habitats that supported higher avian populations. In comparison, Kamal Khan’s subtropical urban broad-leaved forest (1.102 ± 0.178 birds/ha) was less preferred by avian species (

Table 3. Habitat wise bird density in six subtropical broad-leaved urban forest habitats.

Habitat	Density (birds/ha)
Palamar	3.954 ± 0.221
Kityari	3.138 ± 0.162
Dob Ghar	2.874 ± 0.230
Shahabad	2.170 ± 0.147
Seya Sar	1.808 ± 0.209
Kamal Khan	1.102 ± 0.178

).

3.2.1. Bird Density in Dob Ghar Subtropical Broad-Leaved Urban Forest

The results revealed that black-throated thrush (0.966 ± 0.329/ha), Indian paradise flycatcher (0.896 ± 0.326/ha) and common rosefinch (0.833 ± 0.259/ha) were the three most populous bird species that utilized the Dob Ghar subtropical broad-leaved urban forest territories. However, the density of 23 bird species was not analyzed due to the low detections (less than 10 individuals) (

Table 4. Bird density in six subtropical broad-leaved urban forests; Abundance in descending order.

Scientific Name	Common Name	Density (birds/ha)
		Name of the Habitat (Urban Forest)
		Dob Ghar	Shahabad	Kityari	Seya Sar	Kamal Khan	Palamar
Streptopelia chinensis	Spotted dove	–	–	–	0.406 ± 0.114	–	0.578 ± 0.210
Alectoris chakur	Chakur	0.735 ± 0.237	0.162 ± 0.553	–	0.109 ± 0.363	–	0.347 ± 0.965
Coturnix coturnix	Common quail	0.696 ± 0.307	0.158 ± 0.817	0.129 ± 0.855	0.158 ± 0.778	0.263 ± 0.153	0.173 ± 0.824
Corvus splendens	House crow	–	0.303 ± 0.119	0.386 ± 0.302	0.241 ± 0.121	0.241±0.168	–
Corvus macrorhynchos	Large–billed crow	0.252 ± 0.101	0.833 ± 0.270	–	0.168 ± 0.459	–	0.252 ± 0.975
Dicrurus macrocercus	Black drongo	0.103 ± 0.391	0.166 ± 0.732	0.996 ± 0.266	0.151 ± 0.432	0.131 ± 0.326	0.136 ± 0.504
Emberiza cia	Rock bunting	0.108 ± 0.419	0.694 ± 0.210	–	0.127 ± 0.487	–	–
Carpodacus erythrinus	Common rosefinch	0.833 ± 0.259	0.617 ± 0.177	0.558 ± 0.203	0.574 ± 0.183	0.694 ± 0.212	0.254 ± 0.111
Hirundo rustica	Common swallow	0.108 ± 0.353	0.648 ± 0.175	0.228 ± 0.170	0.129 ± 0.425	0.196 ± 0.119	–
Lanius tephronotus	Grey–backed shrike	0.103 ± 0.376	0.694 ± 0.289	0.133 ± 0.480	0.123 ± 0.476	–	–
Lanius vittatus	Bay–backed shrike	–	–	0.771 ± 0.259	–	–	–
Turdoides caudata	Common babbler	0.641 ± 0.231	0.525 ± 0.173	0.717 ± 0.186	0.222 ± 0.737	0.887 ± 0.249	0.790 ± 0.253
Trochalopteron lineatum	Streaked laughing thrush	0.205 ± 0.525	0.729 ± 0.295	0.101 ± 0.340	–	0.109 ± 0.417	0.694 ± 0.249
Terpsiphone paradisi	Indian paradise flycatcher	0.896 ± 0.326	0.120 ± 0.365	0.176 ± 0.697	0.164 ± 0.558	0.144 ± 0.420	0.121 ± 0.445
Motacilla alba	White wagtail	–	–	0.241 ± 0.152	–	0.378 ± 0.253	0.317 ± 0.197
Oriolus oriolus	Golden oriole	0.548 ± 0.259	–	0.616 ± 0.220	0.450 ± 0.162	0.635 ± 0.214	0.612 ± 0.205
Parus cinereus	Cinereous tit	0.119 ± 0.387	0.694 ± 0.238	0.109 ± 0.289	0.926 ± 0.324	0.160 ± 0.471	0.757 ± 0.235
Passer montanus	Eurasian tree sparrow	0.264 ± 0.113	0.168 ± 0.367	0.520 ± 0.151	0.716 ± 0.268	0.264 ± 0.180	0.100 ± 0.310
Passer domesticus	House sparrow	0.138 ± 0.404	0.617 ± 0.196	0.119 ± 0.308	0.222 ± 0.109	0.961 ± 0.307	0.241 ± 0.126
Phylloscopus collybita	Common chiffchaff	0.126 ± 0.430	0.757 ± 0.244	0.144 ± 0.582	–	0.120 ± 0.406	0.108 ± 0.379
Phylloscopus chloronotus	Lemon–rumped warbler	0.104 ± 0.319	–	0.114 ± 0.480	–	–	–
Phylloscopus trochiloides	Greenish warbler	–	–	–	–	0.126 ± 0.467	–
Pycnonotus cafer	Red–vented bulbul	0.747 ± 0.253	0.177 ± 0.348	0.756 ± 0.242	0.124 ± 0.391	0.129 ± 0.459	0.669 ± 0.200
Pycnonotus leucotis	White–eared bulbul	0.173 ± 0.636	–	–	–	0.195 ± 0.405	–
Pycnonotus leucogenys	Himalayan bulbul	–	0.617 ± 0.202	–	–	0.120 ± 0.391	0.252 ± 0.840
Acridotheres tristis	Common myna	0.106 ± 0.246	0.733 ± 0.203	0.105 ± 0.308	0.101 ± 0.382	0.142 ± 0.514	0.868 ± 0.284
Acridotheres ginginianus	Bank myna	–	–	–	–	–	–
Sturnus pagodarum	Brahminy starling	–	0.119 ± 0.412	0.264 ± 0.135	–	–	–
Sturnus vulgaris	Common starling	0.666 ± 0.219	0.823 ± 0.283	0.666 ± 0.236	0.100 ± 0.295	–	0.666 ± 0.231
Turdus atrogularis	Black–throated thrush	0.966 ± 0.329	0.104 ± 0.319	–	0.555 ± 0.189	0.115 ± 0.400	0.732 ± 0.281

).

3.2.2. Bird Density in Shahabad Subtropical Broad-Leaved Urban Forest

Distance test results demonstrated that five bird species, large-billed crow (0.833 ± 0.270/ha), common starling (0.823 ± 0.283/ha), common chiffchaff (0.757 ± 0.244/ha), common myna (0.733 ± 0.203/ha) and streaked laughing thrush (0.729 ± 0.295/ha), comprised the vast majority of species that occupied the Shahabad subtropical evergreen broad-leaved urban forest. However, the density of 29 bird species was not determined due to the low detection of bird individuals (Table 4).

3.2.3. Bird Density in Kityari Subtropical Broad-Leaved Urban Forest

In Kityari subtropical broad-leaved urban forest, the highest bird density was detected for the black drongo (0.996 ± 0.266/ha), bay–backed shrike (0.771 ± 0.259/ha), red–vented bulbul (0.756 ± 0.242/ha), and common babbler (0.717 ± 0.186/ha). However, the density of 28 bird species was not determined due to the low number of individual bird detections (Table 4).

3.2.4. Bird Density in Seya Sar Subtropical Broad-Leaved Urban Forest

The findings demonstrated that the cinereous tit (0.926 ± 0.324/ha) and Eurasian tree sparrow (0.716 ± 0.268/ha) were the prevailing bird species that densely occupied the Seya Sar subtropical broad-leaved urban forest. The density of 28 bird species was not ascertained due to the small sample size (Table 4).

3.2.5. Bird Density in Kamal Khan Subtropical Broad-Leaved Urban Forest

The density analysis showed that the house sparrow and common babbler were the bird species that had the highest bird density (0.961 ± 0.307/ha and 0.887 ± 0.249/ha) in Kamal Khan subtropical broad-leaved urban forest habitat. In contrast, the density of 30 bird species was not analyzed due to low detections of bird individuals (Table 4).

3.2.6. Bird Density in Palamar Subtropical Broad-Leaved Urban Forest

Notably, the results of density analysis revealed that the common myna (0.868 ± 0.284/ha), common babbler (0.790 ± 0.253/ha), cinereous tit (0.757 ± 0.235/ha) and black-throated thrush (0.732 ± 0.281/ha) were the four most common species that utilized Palamar subtropical broad-leaved urban forest habitat. The density of 26 bird species was not analyzed due to the low detection of bird individuals (Table 4).

3.3. Comparison of Bird Diversity Indices in Six Subtropical Broad-Leaved Urban Forest Habitats

The results of Shannon–Wiener Index illustrated that bird diversity in six subtropical broad-leaved urban forests varied. The Kamal Khan (H’ = 3.581 ± 0.021) habitat was more diverse and Kityari (H’ = 3.375 ± 0.021) was slightly varied in avian species composition. In addition, a diversity-ordering Renyi test was done to compare species diversity and richness (Table 4). The most noteworthy avian richness (Margalef Richness Index) was detected in Shahabad (R1 = 8.007 ± 0.053) and the least richness was detected in Dob Ghar (R1 = 7.372 ± 0.053). Moreover, the Pielou J Evenness Index revealed that the avian species were evenly distributed in Dob Ghar (E = 0.940 ± 0.005) and sparsely in Kityari (E = 0.867 ± 0.005;

Table 5. Habitat-wise bird diversity indices in six subtropical broad-leaved urban forests.

Habitat	Shannon–Wiener Index (H’)	Margalef Index (R1)	Pielou J Index (E)
Dob Ghar	3.580	7.372	0.940
Palamar	3.545	7.379	0.926
Kamal Khan	3.581	7.892	0.915
Shahabad	3.558	8.007	0.905
Seya Sar	3.524	7.566	0.915
Kityari	3.375	7.515	0.867
Overall	3.626	6.528	0.913
Standard Error	0.021	0.053	0.005

and Figure 3).

Furthermore, the branch lengths and topological changes of the dendrogram highlighted that avian diversity may vary from habitat to habitat (Figure 3). Kruskal-Wallis one–way ANOVA and Tukey’s HSD indicated that the bird diversity indices in six subtropical broad-leaved urban forest habitats were significantly different (F5, 17 = 61.7, p < 0.05).

3.4. Comparison of Foraging Guilds of Avian Species in Six Subtropical Broad-Leaved Urban Forest Habitats

The results of foraging guilds revealed that feeding guilds of avian species vary from habitat to habitat. Insectivores, comprising the greenish warbler, lemon–rumped warbler, common chiffchaff, cinereous tit, oriental magpie robin, pied bush chat, grey wagtail, white wagtail, Indian paradise flycatcher, common babbler, bay–backed shrike, grey-backed shrike, common swallow, rock bunting, black drongo, crested lark, green bee-eater and Indian roller, were the most abundant guild in all habitats. Omnivores (5.592%) heavily occupied the Kityari urban forest habitat. In contrast, carnivores/piscivores/insectivores (white-throated kingfisher) avoided Dob Ghar and frugivores (speckled wood pigeon and yellow-footed green pigeon) avoided Kamal Khan and Dob Ghar urban forests (

Table 6. Comparison of foraging guilds in six subtropical broad-leaved urban forests.

Guild	Shahabad	Seya Sar	Palamar	Kamal Khan	Dob Ghar	Kityari
Carnivore	0.313%	0.278%	0.347%	0.625%	0.313%	0.278%
Insectivore	5.488%	5.036%	5.175%	6.391%	5.141%	7.398%
Carnivore/Piscivore/Insectivore	0.069%	0.069%	0.035%	0.069%	0	0.069%
Granivore	1.007%	1.320%	1.077%	0.799%	0.695%	0.764%
Frugivore	0.104%	0.035%	0.035%	0	0	0.139%
Omnivore	3.890%	3.196%	2.223%	2.918%	1.667%	5.592%
Frugivore/Insectivore	3.717%	2.952%	3.612%	3.856%	3.578%	3.057%
Granivore/Insectivore	3.300%	2.292%	2.952%	2.605%	2.188%	3.334%
Sub-Total	515	437	445	497	391	594
Grand Total			2879

).

3.5. Correlation between Different Foraging Guilds and Bird Population in Six Subtropical Broad-Leaved Urban Forests

We further analyzed the data to establish a correlation between different foraging guilds and bird population in six subtropical broad-leaved urban forests (Figure 4). A strong positive correlation (R² = 0.7–0.9) between bird population and different foraging guilds was recorded. Common food sources for the foraging guilds included number of grass species (R² = 0.9), tree species (R² = 0.9), shrubs (R² = 0.8), fruiting trees (R² = 0.7) and the number of insects (R² = 0.7), reptiles (R² = 0.7) and rodents (R² = 0.7)(Figure 4).

4. Discussion

A comparative evaluation of the avian state of conservation and community parameters of bird species inhabiting various subtropical urban forests demonstrates habitat–level ecosystem health. The findings of state conservation and population structure are paramount in conservation activities because they explain the driving forces that influence population variability specifically or by implication. Birds are bioindicators of urban forest health and productivity [30,62,63]. Detailed information on avian community parameters helps to clarify the key driving variables that play important roles in the determining the home range and habitats, and the impact of human activity on avian diversity and habitat alteration [64]. Determining the state of conservation and population structure of bird species inhabiting subtropical urban forests provides a solid foundation for better understanding ecological trends and processes.

This comparative investigation provides useful data on various aspects of bird assemblages and their dwelling habitats, and how they could be managed on a sustainable basis and improve biodiversity conservation. This study, through an intra-specific comparison of bird species among six broad-leaved urban forests, demonstrated that 51 species preferred the Dob Ghar, 45 preferred Kityari, 46 preferred Kamal Khan, 50 preferred Palamar, 44 preferred Siya Sar and 49 preferred Shahabad. Previously, it has been found that species abundance tends to increase with landscape diversity and decrease with low vegetation coverage that might provide scarce food resources [65]. This premise is in line with our results presented in Figure 4. In addition, land-use patterns adjoining the urban forests influence food resources, predation, and competition between avian species present in urban forest domains [66]. Structural modifications in vegetation structure alter habitat suitability, foliage, food, and ground vegetation. These factors alter the home range and mobility of avian species [67].

In addition, the findings of this study illustrate that urban forests bolster a distinctive range of bird communities, which may vary according to floristic composition, food resources, and extent of the impacts of human activity. For example, Palamar and Kityari dynamic subtropical urban broad-leaved habitats harbored a higher avian density than other urban territories. In addition, vegetation structure, especially foliage diversity, vegetation cover percentage, canopy cover, and food assortment, were the preeminent variables that determine higher bird diversity and density in urban forests (Figure 4). Poulin et al. [68] found that an urban forest’s plant species composition, food resources, and adjacent habitats are crucial for a wide range of bird species. In a previous study, Sweeney et al. [69] reported that food availability and diversity often vary within forests, which may, in turn, influence the density and diversity of bird species. Birds are habitat specialists, generalists, and resource users that take advantage of opportunities. Likewise, Jayson and Mathew [70] stated that the higher the avian density in dwelling habitats, the wider the assortment of food resources and niches availabile. In comparison, the less vegetated urban forest habitats favored only a few bird species as clear from the low value of correlation coefficient in Figure 4.

Furthermore, the findings of the Community Analysis Package revealed that in six subtropical urban forests, the diversity indices and population of bird species varied. This might be due to the fact that the range and selection of habitats among bird species varied depending on the floristic composition, the availability of food resources (e.g., insects, fruits, grains, amphibians, reptiles and small mammals), adjacent habitats (e.g., agricultural and orchard fields offering suitable foraging and breeding sites) and human activity [69,70]. This premise is evident from the results presented in Figure 4. It has been revealed that complex vegetation creates a pool of competence that attracts a diverse range of bird species, reducing competition and helping other species through the creation of niches [71]. It may also be due to the fact that these bird species belong to various foraging guilds in heterogeneous environments where they forage and eat a wide range of food items. Thrushes, for instance, frequently incline towards the thick scrub stands, forest edges, moist places, and grassy beds to bolster on invertebrates, such as caterpillars, ants, wasps, grasshoppers, beetles, and wing flies. Previous studies have illustrated that vegetation structure and composition affect avian community parameters such as species composition [72], habitat utilization [73], species diversity, richness [74,75], assemblages [76] and ecological behavior.

Further, frugivore/insectivore birds, such as starlings, orioles, thrushes, and bulbuls, were also measured in sufficient numbers. The reason behind the large numbers of fruit- and insect-eating birds detected could be the availability of fruit and insects that may be attributed to birds utilizing the urban forest. This might be because these urban forests are complex habitats rich in floristic composition, diverse topography and humid weather conditions that harbor a wide array of invertebrates [77,78]. Heterogeneity within the landscape, especially variation in topography (slope, aspect, and position), connectivity and vegetation complexity, are the major attributes that make an urban forest more attractive to avian species [78]. It has been reported that complex vegetation provides a variety of thermal conditions to harbor avian diversity [79]. Moreover, the urban forests are surrounded by agricultural fields and orchards that bear flowers and fleshy fruits that attract a wide variety of insect species, which are the staple diet of frugivore/insectivore birds. The insect-eating birds source insects from agriculture fields and fruit-eating birds consume the fleshy fruits of adjacent habitats [80]. This shows that birds are habitat specialists; they often prefer habitats rich in food resources that offer suitable foraging grounds, breeding sites and shelter from harsh weather and predators [81,82,83].

The recording of five species of raptors, namely, shikra, besra, kites, kestrels, and owls, showed that these subtropical broad-leaved urban forests are an attractive habitat for passerine birds, reptiles (lizards and snakes), small mammals (shrews, rats, squirrels and mice). According to Bosakoski and Smith [84], raptors are area-sensitive bird species that prefer habitats with high prey density and habitat heterogeneity. These characteristics are strongly associated with wildness. For example, Buteo jamaicensis and Buteo viriginianus preferred suburban habitat and Strix varia, B. lineatus, and Accipiter cooperii lowland areas. Likewise, Widen [85] stated that prey density and accessibility were the major driven factor that influenced habitat use of raptors. The bird species prey on ground-dwelling animals through the pause-travel search tactic. It is possible that in these urban forests, raptors capture prey from the surrounding landscapes and consume them in urban-dwelling forest areas.

Additionally, a high number of insectivore birds such as minivets, woodpeckers, bee-eaters, flycatchers, wagtails, robins, bush chats, warblers, shrikes and treecreepers were recorded in the urban forest habitats studied. The diversity of insect-eating birds might be due to the occurrence of a wide array and large number of insects, such as flies, moths, beetles, grasshoppers, caterpillars, wasps, ants, and termites, which are their staple diet. It may also be due to the presence of trees, shrubs, and grasses that bear flowers and fruits that that attract these birds. Shrub layers add habitat complexity to the urban forest ecosystem; they provide a variety of food, asylum from predators, and potential nesting sites [69,86]. The understory vegetation increases the species diversity and richness of avian communities [87].

Similarly, of game birds, specifically francolin, chakor, quails and doves, also dominated the urban forest territories in the present study. This might be due to their preference for grassy areas and open landscapes for game birds to forage on seeds, grass grains, crops for agriculture, cereals and invertebrates (centipedes and millipedes in leaf litter). Previously, it was illustrated that game birds predominate urban forests with structured complexvegetation, particularly bushes and grasses, accessible foraging and nesting sites, interspecific competition and low predation [88,89]. These factors have a significant impact on the demographic parameters of game bird populations and community structure. Babblers select moderately open woodlands, scrub plants, forest remains, and forest edges to forage on larvae, caterpillars, worms, and ants [90]. They also consume grains, insects, termites, flies, and larvae [91]. Finches utilize the thickets, woodlands, forest edges near riparian regions and orchards in search of seeds, buds, shoots, fruits, and orchards. Pigeons are often live near fruiting trees to consume a variety of fruits, especially fig trees, as well as shrubs. As grassy areas are rich in grains and insects, francolins and chakor prefer barren hills with ample grasses and few bushes, which conjointly provide hiding cover from predators and offer ideal breeding locations [78]. Francolins and chakor prey on invertebrates inhabiting leaf litter, such as centipedes and millipedes [88].

5. Conclusions

Overall, detailed information collected about Pakistan’s subtropical broad-leaved urban forests is imperative for the assurance of survival for a broad variety of avian species. The findings of this study may assist in the future planning of biodiversity conservation. Hence, we conclude that these urban forests are dynamic and complex ecosystems and are of vital significance for the protection of both wildlife and human beings. It is therefore strongly suggested that these urban forests be designated as reserved forests to increase the population of highly endangered and threatened avian species.