Anthropogenic nesting materials and reproductive performance of Chinese Bulbuls (Pycnonotus sinensis) along the urbanization gradient in Hangzhou, China

1.   Introduction

Urbanization caused by humans is one of the most profound and rapidly evolving environmental shifts worldwide (Marzluff et al., 2001; Seto et al., 2012; Minias, 2015). Urbanization often results in significant disruption to natural habitats, especially with the burgeoning human population driving the conversion of agricultural and other natural terrains into urban landscapes (Montoya-Tangarife et al., 2017). Rapid human population growth along with the urbanization process has led to the accumulation of waste in the urban environment (Kaza et al., 2018; Jagiello et al., 2022), and plastic pollution in waste has become a global threat to biodiversity (UNEP, 2014; Jagiello et al., 2019; Mansfield et al., 2024), affecting the behavior, physiology, and survival of invertebrates and vertebrates (Lavers et al., 2014; Setälä et al., 2014; Jagiello et al., 2023).

Birds can be used as bioindicators of plastic pollution in terrestrial and freshwater environments (Mansfield et al., 2024). Although urbanization is usually considered to lead to a homogenization of bird species communities (Devictor et al., 2007; Leveau et al., 2015), some bird species worldwide are actively colonizing and successfully adapting to urban environments (Evans et al., 2009; Morelli et al., 2018). The effects of urbanization have caused some natural elements to be replaced by artificial structures and artificial materials (Kaza et al., 2018), and many studies have found that artificial materials appear in the nests of urban birds (Wang et al., 2009; Jagiello et al., 2019; Briggs et al., 2023; Sheard et al., 2024). Birds may nest directly on manufactured structures such as house buildings (Reynolds et al., 2019), bridges and metal pipes (Mainwaring, 2015), wall ledges or air condition mounts (Wang et al., 2015).

Nests are crucial in determining the reproductive success of birds (Hansell, 2005; Collias and Collias, 2016). The nest protects the eggs and offspring from predators and environmental stressors (Deeming and Reynolds, 2016). Urban birds have been found to integrate anthropogenic nesting materials (ANMs) into their nests to adapt to the city environment (Wang et al., 2009; Reynolds et al., 2019; Jagiello et al., 2022). However, such new ANMs can yield mixed consequences for birds. For instance, the incorporation of ANMs affects the cooling dynamics of Clay-colored Thrush (Turdus grayi) nests (Corrales-Moya et al., 2021), but can simultaneously decrease nest survival rates (Corrales-Moya et al., 2023). Some ANMs like cigarette butts might deter parasites, affect the physical well-being of adult birds, but elevate the reproductive costs in urban settings (Suárez-Rodríguez et al., 2013, 2017). Jagiello et al. (2022) also showed that the higher the ANMs' proportion in the Blue Tits' (Cyanistes caeruleus) nests in urban habitats, the lower the number of hatchlings.

Several hypotheses have been proposed to explain why birds use ANMs to build nests (Reynolds et al., 2019; Jagiello et al., 2022, Jagiello et al., 2023). First, the availability hypothesis holds that urban birds are left with little choice due to the scarcity of natural nesting materials, leading them to resort to readily available anthropogenic substitutes (Wang et al., 2009). Second, the adaptive hypothesis suggests that the selection of ANMs by birds may be related to their increased reproductive performance (Suárez-Rodríguez et al., 2013; Reynolds et al., 2019). Third, the new location hypothesis posits that birds choose different nest materials due to changes in nest sites (Reynolds et al., 2019). Finally, the search image hypothesis indicates that birds using ANMs on the outer layer of the nest will change the original image of the nest and then can avoid predator search (Corrales-Moya et al., 2023).

In this study, we investigated the relationship between the incorporation of ANMs into nests and the reproductive performance of Chinese Bulbuls (Pycnonotus sinensis) by monitoring and collecting data on 136 breeding nests along the urbanization gradient in Hangzhou, China. We aimed to address the following questions: (1) Does urbanization intensity influence the amount of ANMs in the nests of Chinese Bulbuls? (2) Whether ANMs may influence reproductive traits of Chinese Bulbuls?

2.   Materials and methods

2.1   Study area

The study was conducted in Hangzhou (29°11′–30°33′ N, 118°21′–120°30′ E) (Fig. 1), the capital city of Zhejiang Province, China. Serving as the administrative, financial and cultural hub of Zhejiang Province, Hangzhou is one the most urbanized cities in the Yangtze River Delta (Wang et al., 2008; Chen et al., 2022). Hangzhou has a population of 12.376 million people as of the year 2022, with a high proportion of urban population of 84.0% (http://www.hangzhou.gov.cn/). The city is covered by hills, flatlands and water systems such as rivers and lakes, which make up 65.6%, 26.4%, and 8.0% of the total land area (Chen et al., 2000), respectively.

Figure  1.  Distribution map of the nest sites of the Chinese Bulbul (Pycnonotus sinensis) in Hangzhou, China.

DownLoad: Full-Size Img PowerPoint

2.2   Study species

The Chinese Bulbul is a small passerine bird with widespread distribution across southern China and East Asia (Zhuge, 1990). This bird species is highly adaptable to urban environments and can thrive even in intensely urbanized areas (Wang et al., 2009; Chen et al., 2023). Previous studies have demonstrated that Chinese Bulbuls can adapt to urban ecosystems by altering their nesting materials (Wang et al., 2009), using food provided by humans (Wang, 2003), adjusting their flight initiation distance in urban areas (Wang et al., 2004), and changing reproductive traits such as laying date (Chen et al., 2023). Chinese Bulbuls in urban areas often nest in some tree species such as Osmanthus fragrans, Photinia serrulata, Bambusoideae sp., Elaeocarpus sylvestris (Lan et al., 2013). Chinese Bulbuls build a tall cup nest, which is typically 2–4 m above the ground and usually constructed from natural materials such as hay stems, fine roots, and plant fibers (Zhuge, 1990).

2.3   Nest surveys

During two breeding seasons in 2012 and 2013, we conducted nest surveys across an urbanization gradient in Hangzhou, spanning from intensely constructed urban centers to pristine natural environments of the western mountainous areas (Fig. 1) (Chen et al., 2022, 2023). We searched for active breeding nests of Chinese Bulbuls by listening for their chirping and observing their nesting material transportation behaviors through telescopes (Wang et al., 2009). The detection of bulbuls' nests was further informed by their nest site preferences (Wang, 2003; Chen et al., 2006), favored nesting trees, particularly osmanthus trees (Lan et al., 2013), and observed behaviors of carrying nesting materials (Wang et al., 2009). Once a breeding nest was discovered, we recorded its coordinates using a GPS for subsequent monitoring (Lan et al., 2013). More details about nest surveys have been described in our previous work (Chen et al., 2022).

2.4   Reproductive parameters

We observed the reproductive behaviors of Chinese Bulbuls from mid-March (Lan, 2013). The breeding periods of Chinese Bulbuls were April 9–May 30 in 2012 and April 1–June 4 in 2013 (Lan et al., 2013). We documented seven reproductive parameters, including laying date, incubation period, nestling period, clutch size, egg volume, hatching success rate, and fledging success rate (Chen et al., 2023). The laying date was defined as the day when the first egg was laid. We calculated the incubation duration as the days from the final egg's laying to the first chick's hatching (Chen et al., 2023). The nestling period spanned from the time when the first chick hatched to the fledging date (Ibáñez-Álamo and Soler, 2010). We defined clutch size as the number of eggs in each nest (Bailly et al., 2015). Chinese Bulbuls usually lay one egg per day, and the number of eggs in a clutch is usually 3 or 4 (Zhuge, 1990). Within two days after the end of egg laying, we measured the long and short radii of eggs with Vernier calipers to the millimeter (Lan et al., 2013). Egg volume was then calculated using the formula: Volume (V) = K_v × mean egg length × mean egg width², in which K_v is the volume coefficient (Hoyt, 1979). All the above measurements were conducted during the periods when parent birds were absent from the nests to reduce potential human disturbance (Zhang, 2014).

We calculated the reproductive success rates for each nest after the end of breeding periods. The hatching success rate was calculated as the number of hatchlings divided by the clutch size (Chen et al., 2023). The fledging success rate was defined as the number of fledglings divided by the number of hatchlings (Corsini et al., 2017).

2.5   Nest composition

Although we initially found 234 natural breeding nests (Chen et al., 2023), after the breeding seasons we eventually obtained 136 nests that can be used for nest material analysis. The other 98 nests were damaged before we removed them from trees due to bad weather conditions and long-time exposures (Zhang, 2014). To maintain the nests' structural integrity and composition, we removed these 136 nests carefully in situ and placed them in well-padded boxes for transportation to our laboratory (Biddle et al., 2019).

Since the collection time was different, we treated each nest in a dryer (HASUC Blower Dryer DHG-9070A) at 60 ℃ for 12 h before performing nest material analysis. We first weighed each nest and then carefully separated all nest materials with clippers (Zhang, 2014). The nesting materials were divided into categories according to the degree of identification (Wang et al., 2009). Finally, we weighed and analyzed each category of nesting materials separately. After dismantling nests of Chinese Bulbuls, we classified all the nest materials into two general groups, i.e. natural or anthropogenic nesting materials (Table 1).

Table  1.  The composition of 136 nests of Chinese Bulbuls in Hangzhou, China. Number of nests represents the total number of nests that contain each type of nesting material, and the proportion represents the ratio of the number of nests divided by the total number of nests (136).

Types of anthropogenic nesting materials	Number of nests	Proportion (%)	Types of natural nesting materials	Number of nests	Proportion (%)
Plastic	130	95.6	Stem	134	98.5
Cotton	55	40.4	Grassroot	61	44.9
Chemical fiber	121	89.0	Leaf	134	98.5
Paper	35	25.7	Palm leaves	56	41.2
Polyurethane foam	12	8.2	Inflorescence	44	32.4
Tinfoil	3	2.2	Natural debris	117	86.0
Human hair	10	7.4	Bark	99	72.8
Metal	1	0.7	Root	19	14.0
Woundplast	2	1.5	Branch	16	11.8
			Pericarp	2	1.5
			Feather	1	0.7

 | Show Table

DownLoad: CSV

2.6   Urbanization characteristic parameters

In earlier urbanization research, several simple measures such as the percentage of the urban landscape or the distance to human settlements were used to quantify urbanization intensity (Marzluff et al., 2001). However, these simple measures often overlooked other important urbanization factors like human disturbance and environmental noise (Wang et al., 2008, 2009). Due to the complexities of urban environment, one single factor is not enough to capture the full urbanization context (McDonnell and Pickett, 1990; Wang et al., 2008).

In our study, we measured the following four urbanization characteristic parameters to quantify urbanization intensity (Chen et al., 2022, 2023).

1. Distance to City Center (DCC): Measured as the straight-line distance from the nest site of Chinese Bulbuls to the Hangzhou City Government Hall (the city center of Hangzhou) using the ArcGIS (ArcView 3.3) (Wang et al., 2008).

2. Building Index (BI): Calculated using the ArcGIS (ArcView 3.3) by measuring the proportion of the area covered by buildings around each nest at varying radii (250 m, 500 m, 1000 m, 2000 m) (Bolger et al., 1997; Wang et al., 2008). Building Index was then calculated using the following formula: BI = 250 m × 1 + 500 m × 0.5 + 1000 m × 0.25 + 2000 m × 0.125.

3. Environmental Noise (EN): Measured using a HS5633A sound meter near the nest in 3-min intervals from 09:00 to 10:00 h on both weekdays and weekends. The average environmental noise (dB) was calculated as: EN = weekday noise × 5/7 + weekend noise × 2/7 (Chen et al., 2022, 2023).

4. Disturbance Index (DI): Represents the number of people and vehicles passing by the nest between 8:00 to 10:00 a.m. It was the sum of average foot traffic and vehicle traffic, both of which were calculated similarly to the environmental noise (Chen et al., 2022, 2023).

These four urbanization characteristic parameters were standardized to values between 0 and 100 and then were combined to create the Urbanization Synthetic Index (USI) to quantitively measure urbanization intensity as follows (Wang et al., 2008; Chen et al., 2022): USI = BI × 100/2 + EN + DI/3 + 1/DCC × 100.

2.7   Data analyses

For each nest, we measured the weight of ANMs and the proportion of ANMs (the weight of ANMs/total weight of the nest). We used the arcsine square root transformation to convert the proportion of ANMs (Zar, 1999) and log-transformed the USI. Prior to analysis, we used the R package "fitdistrplus" (Delignette-Muller and Dutang, 2015) to examine the distribution of the dependent variable. We then constructed a linear mixed effect model (LMM) (Bates et al., 2015) to examine the relationship between the USI and the amount of ANMs, with USI as the fixed effect and tree species as a random effect (Chen et al., 2023).

We applied binary logistic regressions to analyze the relationship between the amount of ANMs and clutch size. We only observed three or four eggs in the nests of Chinese Bulbuls after removing invalid data such as abandoned nests or predated nests (Chen et al., 2023). Therefore, we converted clutch size into a two-valued response variable (three eggs = 0, four eggs = 1) and then applied binary logistic regressions to analyze its relationship with the proportion and weight of ANMs.

We built LMMs to analyze the influence of the amount of ANMs on the other six reproductive parameters (laying date, incubation period, nestling period, egg volume, hatching success rate, and fledging success rate). In these LMMs, we used the proportion or weight of ANMs as the fixed effect and tree species as random factor. Before data analyses, we converted the hatching success rate and fledging success rate using the arcsine square root transformation.

Values are given as mean ± SE, all tests are two-tailed, and statistical significance was set at α ≤ 0.05 (Zar, 1999). All analyses were performed in R 4.1.2 (R Core Team, 2021).

3.   Results

Among the 136 examined nests of Chinese Bulbuls, 131 (96.32%) contained anthropogenic materials. Among the types of ANMs, the most highest frequency was plastic (95.6%) and chemical fiber (89.0%), while the lowest frequency was metal (0.7%). Among natural nesting materials, stems and leaves were the most frequent (98.5%), whereas feathers (0.7%) were the lowest (Table 1).

Both the proportion and weight of ANMs in the nests of Chinese Bulbuls increased significantly with the urbanization synthetic index (Fig. 2; t₁ = 3.463, p < 0.01; t₂ = 4.220, p < 0.01).

Figure  2.  The relationship between the content of anthropogenic nesting materials in nests of Chinese Bulbuls and the degree of urbanization. (A: proportion of anthropogenic nesting materials, arcsine square root; B: weight of anthropogenic nesting materials).

DownLoad: Full-Size Img PowerPoint

We observed a significantly higher hatching success rate for Chinese Bulbuls with an increasing proportion of ANMs (Fig. 3, Table 2). However, the other six reproductive traits, i.e., laying date, incubation period, nestling period, clutch size, egg volume, and fledging success rate, did not vary significantly with the proportion of ANMs (Table 2). In addition, the weight of ANMs was not significantly correlated with all the seven reproductive traits (Table 3).

Figure  3.  The relationship between the content of anthropogenic nesting materials and reproductive traits of Chinese Bulbuls. Solid lines represent significant influences, based on whether the 95% CI overlaps zeroes.

DownLoad: Full-Size Img PowerPoint

Table  2.  Results of linear mixed effects models (LMMs) and binary logistic regressions relating the proportion of anthropogenic nesting materials to reproductive traits of Chinese Bulbuls. n is the sample size for each variable. Significant results are shown in bold type.

Variables	Intercept	Estimate ± SE	t/Z	p
Laying date (n = 58)	−1.541	−0.067 ± 0.216	−0.309	0.759
Incubation period (n = 57)	11.426	0.025 ± 0.576	0.043	0.965
Nestling period (n = 69)	11.307	0.568 ± 0.789	0.720	0.474
Clutch size (n = 131)	−0.204	−0.819 ± 0.977	−0.838	0.402
Egg volume (n = 66)	2.952	0.085 ± 0.182	0.466	0.643
Hatching success rate (n = 113)	0.987	0.557 ± 0.279	1.995	0.049*
Fledging success rate (n = 113)	0.849	−0.298 ± 0.316	−0.944	0.347

 | Show Table

DownLoad: CSV

Table  3.  Results of linear mixed effects models (LMMs) and binary logistic regressions relating the weight of anthropogenic nesting materials to reproductive traits of Chinese Bulbuls. n is the sample size for each variable.

Variables	Intercept	Estimate ± SE	t/Z	p
Laying date (n = 58)	1.532	−0.006 ± 0.012	−0.470	0.640
Incubation period (n = 57)	11.294	0.027 ± 0.031	0.870	0.388
Nestling period (n = 69)	11.397	0.035 ± 0.034	1.063	0.292
Clutch size (n = 131)	−0.197	−0.085 ± 0.060	−1.414	0.157
Egg volume (n = 66)	2.935	0.014 ± 0.010	1.379	0.173
Hatching success rate (n = 113)	1.135	0.024 ± 0.015	1.632	0.106
Fledging success rate (n = 113)	0.712	0.0004 ± 0.002	0.026	0.979

 | Show Table

DownLoad: CSV

4.   Discussion

In this study, we systematically examined the relationship between the incorporation of ANMs into nests and the reproductive performance of Chinese Bulbuls by monitoring and collecting data on 136 breeding nests in Hangzhou, China. We found significant increases in both the proportion and weight of ANMs in the nests of Chinese Bulbuls with increasing urbanization intensity. This result may be related to the reduction of natural nesting material in urbanized environment (Wang et al., 2009). With the advancement of urbanization, the natural environment and ecosystems have undergone significant changes. Natural habitats such as forests and grasslands are gradually replaced by artificial facilities such as buildings and roads (Marzluff et al., 2001). Many natural resources are exploited and utilized by birds, resulting in a scarcity of sources of natural nest timber (e.g., twigs, dead grass stems and leaves, etc.). These results indicate that as one of the urban adaptable species, Chinese Bulbuls choose to use ANMs for nesting in highly urbanized habitats.

Our analysis shows that the Chinese Bulbul's hatching success rate is significantly improved after adding ANMs to the nests. The success of bird hatching is closely related to the right temperature (Deeming and Pike, 2015). A stable temperature is essential for embryonic development (Lundy, 1969). As some kinds of ANMs, such as cotton, can better keep the temperature in the nest stable, which in turn may improve the hatching success rate of Chinese Bulbuls. In our study, we found that the proportion of all nests containing cotton reached 40.4% (Table 1). It should be noted that a thermoregulation experiment is needed to prove the exact role of ANMs (e.g., cotton) in providing insulation properties in nests.

Our result appears to be consistent with the adaptive hypothesis (Reynolds et al., 2019), which argues that the inclusion of ANMs in the nest is consistent with the reproductive advantage of bird species. However, our findings do not fully support the adaptive hypothesis, as adding ANMs to the nest did not influence other reproductive traits of the Chinese Bulbul. Several studies also have found the potential hazards of ANMs for other bird species. For instance, plastics in nests might ensnare or harm chicks, even proving fatal (Montevecchi, 1991; Baker et al., 2002; Votier et al., 2011). There is also the danger of birds inadvertently feeding on debris, which can decrease their reproductive success (Mee et al., 2007; Kim et al., 2023). Therefore, the benefits and pitfalls of ANMs are quite complex and need more comprehensive exploration. Our result also accords with the availability hypothesis, because our previous study (Wang et al., 2009) found that in land types with different levels of urbanization, the degree of ANMs used in the nests of Chinese Bulbuls increased significantly with the availability of ANMs in the environments. However, the new location hypothesis is not supported, since Chinese bulbuls in our study always nest in trees or shrubs and do not change their nesting locations (Wang et al., 2009; Lan et al., 2013). Finally, we cannot test the search image hypothesis due to the lack of data on the proportion of nest area covered with ANMs.

The results showed that the proportion or weight of ANMs was not correlated with the other reproductive traits of Chinese Bulbuls. Several reasons may explain why some changes of reproductive traits with ANMs are not noticeable. First, it may be difficult for ANMs to influence certain relatively fixed reproductive traits of Chinese Bulbuls, such as the clutch size (either three or four) or egg volume (Zhang, 2014). Second, the sample sizes for all the reproductive traits among the 136 breeding nests was not consistent due to several uncontrollable or logistical reasons, such as bad weathers, abandoned nests, and labor shortage (Chen et al., 2023). The inconsistence in sample sizes may also lead to the weak relationship between ANMs and reproductive traits of Chinese Bulbuls. Finally, in previous studies, the use of ANMs has adversely affected the physical condition of chicks and adults (Suárez-Rodríguez et al., 2014; 2017), indicating that the effects of ANMs on birds may be manifested in subsequent stages following the breeding period.

5.   Conclusion

In conclusion, we found that Chinese Bulbuls choose ANMs to build their nests, with 96.32% of examined nests containing such anthropogenic components. Our analysis showed that the incorporation of ANMs into nests significantly increased the hatching success rate of Chinese Bulbuls, but was not correlated with other reproductive traits. Overall, the use of ANMs by Chinese Bulbuls seems to be consistent with the adaptive hypothesis and the availability hypothesis. However, it should be noted that our results and conclusions on the relationship between the incorporation of ANMs into nests and the reproductive performance of Chinese Bulbuls are primarily based on field observations. Further studies should use controlled experiments to accurately investigate the impact of ANMs on reproductive success.

Ethics statement

Our study was carried out in agreement with the current law of China on the protection of wildlife.

CRediT authorship contribution statement

Xingmin Chen: Writing – original draft, Validation, Software, Methodology, Formal analysis, Data curation. Qin Zhang: Validation, Methodology, Investigation, Data curation. Sisi Lan: Validation, Methodology, Investigation, Data curation. Qin Huang: Validation, Methodology, Investigation, Data curation. Shuihua Chen: Supervision, Resources, Project administration, Methodology, Investigation, Funding acquisition, Data curation, Conceptualization. Yanping Wang: Writing – review & editing, Supervision, Resources, Project administration, Methodology, Funding acquisition, Conceptualization.

Declaration of competing interest

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.

Acknowledgements

We thank Tengda Zhu, Yafei Ma, Jianwei Zhou, Chao Chen, Xiang Yu, Wen Xu, Mingming Hu and Chenchen Zhu for their field assistance in finding and monitoring bird nests.