Abstract
Urbanization has resulted in changes in bird life histories, and some species have successfully adapted to urban environments, resulting in synurbization. Nest site selection in urban areas challenges cavity nesters because natural nest sites are often replaced by artificial holes. This study was conducted to identify the nest site selection and nest characteristics of the Eurasian tree sparrow (Passer montanus) living in an urban environment. This species inhabits artificial structures and tree holes around human settlements. We surveyed nests of tree sparrows on the Chonnam National University campus, located in Gwangju, Republic of Korea, during the first clutch from March to May 2020. We categorized nest types into natural and artificial nest sites. The tree sparrows selected natural nest sites such as woodpecker's holes and cracks in trees, and selected artificial nest sites which included holes in concrete buildings, under roofs, and in steel frames and nesting boxes. No significant differences were found in breeding schedules and reproductive success between birds nesting in artificial and natural holes. The results suggest that tree sparrows can successfully adapt to an urban environment by selecting nest sites regardless of nest hole type, and can reproduce successfully when nesting in both natural and artificial holes.
Introduction
Rapid urbanization linked to human activities has caused changes in the behavior and life histories of wild animals (Luniak 2004, Mikula et al. 2014). An increase in the extent of urban areas results in vegetation changes and the destruction and fragmentation of habitat and food resources for wild animals (Lowry et al. 2012, Sol et al. 2013, Han et al. 2019). In particular, habitat changes due to urbanization are causing the decline and extinction of bird populations because of the associated decrease in suitable breeding sites and the increase in new habitat types (McKinney 2006, Mikula et al. 2014, Marzluff et al. 2016). In contrast, some species have successfully adapted to the changes in habitat types and food resources brought on by urbanization; consequently, there is an increase in the distribution of certain adapted species within cities (Luniak 2004, Partecke et al. 2006, Francis & Chadwick 2012, Han et al. 2019). As a result, the adaptation of wildlife to urban environments has been consistently observed, and has recently been described by the term ‘synurbization’. (Luniak 2004, Francis & Chadwick 2012).
Nest site selection in birds is a major factor that influences reproductive success and survival of avian species (Buckley & Buckley 1980, Burger & Gochfeld 1986, Misenhelter & Rotenberry 2000, Baek et al. 2016), because a number of factors affect nest success, including nest concealment and defense from potential predators, protection of eggs and chicks from extreme weather conditions, and intra- and interspecific competition for resources (Li & Martin 1991, Holt & Martin 1997, Lõhmus & Remm 2005, Cockle et al. 2008, de la Parra-Martínez et al. 2015). Therefore, optimal nest site selection in birds is the basis for an increase in the reproductive success rate and a reduction in the possibility of reproductive failure due to factors such as predation, flooding, and heat loss. Nest site selection is particularly important for cavity nesters. including primary cavity nesters (species such as woodpeckers that can excavate their own cavities in nature), and secondary cavity nesters (species that cannot make their own nest holes but use natural holes and old woodpeckers' nests; Holt & Martin 1997, Losin et al. 2006, de la Parra-Martínez et al. 2015, Tomasevic & Marzluff 2017). In natural environments, nest site selection in cavity nesters is affected by the location, size, height, microclimate inside the cavity, hole orientation, and internal depth of the hole (Rendell & Robertson 1989, Li & Martin 1991, Losin et al. 2006, de la Parra-Martínez et al. 2015), as well as selection of nest sites that are safe from predators and competitors (Newton 1994). In the case of secondary cavity nesters, competition for nest sites occurs among individuals because there is an insufficient availability of holes in the breeding areas, making selection of suitable nesting places difficult (Li & Martin 1991, Lõhmus & Remm 2005, Cockle et al. 2008, 2010). In natural environments, secondary cavity nesters occasionally use holes in artificial structures (Tomasevic & Marzluff 2017).
Inter- and intraspecific competition for suitable nesting sites is common among birds that live in urban environments because they are seeking breeding sites in nest-limited rather than in natural places (Wang et al. 2009). In urban environments, suitable nesting sites for cavity nesters such as tree holes and old nests of woodpeckers have a limited distribution; consequently, secondary cavity nesters have adapted to nesting in artificial environments such as in cracks in buildings, in steel structures, under roofs, in gaps in concrete, behind signboards, on electric poles, and in artificial nesting boxes (Luniak 2004, Tomasevic & Marzluff 2017, Jeong & Lee 2020).
Generally, the food-limitation hypothesis and the nest-predation hypothesis are used to explain bird adaptation to a specific environment (Newton 1994). The food-limitation hypothesis suggests that the total amount of available food resources acts as the key factor determining the reproductive success of a mating pair (Martin 1987), and the nest-predation hypothesis suggests that predation pressure acts as the main factor that limits the reproductive success of an individual (Martin 1995). Our understanding of bird life history is based on these two hypotheses, because food resources and predation pressure are important factors in reproductive success (Martin 2004, Ferretti et al. 2005, Vincze et al. 2017). To explain adaptation of urbanized bird species, several hypotheses have been proposed. Of these, the predator-safe zone hypothesis (Gering & Blair 1999, Ryder et al. 2010), proposes that the urban environment is selected by birds because it supports a high nest survival rate due to low predation pressure under urban conditions. The predator-prey decouple hypothesis (Rodewald & Kearns 2011, Stracey 2011), proposes that the urban environment changes the composition of predators, resulting in fewer predators directly harming nests. The urban food limitation hypothesis proposes that a reduction in food sources (e.g., biomass of caterpillars) in urban environments is related to a reduction in the amount of vegetated area because of urban development (Seress et al. 2018).
In this study, we researched the Eurasian tree sparrow (Passer montanus), a typical urban bird (synurbic avian species; Mardiastuti et al. 2020), and a secondary cavity nester, which is distributed across the Eurasian continent. Tree sparrows are known to build nests in several types of holes, including holes in trees around human settlements, disused woodpecker's nests, holes in power poles, cracks in buildings, and nesting boxes (Summers-Smith 1995, Field & Anderson 2004, Lee et al. 2020). The tree sparrow populations in Europe and the United States reside outside of cities because they have been out competed and displaced from urban areas by the house sparrow (Passer domesticus; Lang & Barlow 1997, Šálek et al. 2015, Skórka et al. 2016). However, tree sparrows reside in city centers in the Republic of Korea, China, and Japan where house sparrows do not occur (Yamashina 1974, Summers-Smith 1995). Previous tree sparrow studies have focused on nest site competition and habitat preference between house sparrows and sparrows living in urban areas (Šálek et al. 2015, Skórka et al. 2016), hole size preference of tree sparrow populations using nesting boxes (Löhrl 1978), changes in the distribution and abundance of sparrow populations following urbanization (Zhang & Zheng 2010), and the breeding ecology of tree sparrow populations living in urban areas (Lee et al. 2020). However, most of the research on tree sparrows to date has focused on breeding in nesting boxes, rather than on the breeding ecology of this species in urban environments. Therefore, we focused our research on the nesting sites and nest characteristics of tree sparrows in an urban environment, including natural sites and artificial sites, and we investigated differences in the breeding schedule and breeding success of tree sparrows between natural and artificial areas within this urban environment.
Materials and methods
Study site
This study was conducted during the first clutches of tree sparrows from March to May 2020 on the campus of Chonnam National University, College of Agriculture and Life Sciences (Fig. 1; N 35°10′31.02″, E 126°53′56.33″) which is located in Gwangju, Republic of Korea. Multiple campus buildings with different shapes and sizes, and constructed from different materials, including brick, cement, and steel are located in the research area. The buildings are surrounded by trees and urban forests, and there are greenhouses, farmland, and poultry farms on the site of the College of Agriculture. In the study area, we installed 20 nest boxes from November 2019 to February 2020 (hole diameter equal: 30 mm). During the breeding season, we used binoculars (10 × 32, Zeiss, Oberkochen, Germany) to search for breeding nests in the study area by tracking and observing tree sparrows entering and exiting holes. Thereafter, we physically approached and observed the nest holes using ladders and ladder trucks to confirm breeding and to record nest characteristics.
Location of the study area (left) and the nest types (right). The study was conducted at the Agricultural Practical Training Center, Chonnam National University, 77, Yongbong-ro, Buk-gu, Gwangju, Republic of Korea (N 35°10′31.02″, E 126°53′56.33″). Tree sparrow nest types located in the study area were classified into two categories: natural and artificial nest sites. A1: natural nest site (crack in a tree), A2: natural nest site (woodpecker's nest), B1: artificial nest site in a building, B2: artificial nest site in a steel frame
Citation: Animal Taxonomy and Ecology 70, 1; 10.1556/1777.2024.12046
Nest survey
We classified the tree sparrow nests into two types: natural holes and artificial holes. The natural holes were identified as breeding nests in holes in trees, cracks in trees, and in nest holes of woodpeckers (Fig. 1A1, A2). The artificial holes were identified as breeding nests in cracks in buildings, in steel frames, in electric poles, and in nesting boxes (Fig. 1B1, B2). We recorded nest height, nest entrance orientation, entrance vertical and horizontal diameter, entrance area, entrance hole to nest distance. The nest height above the ground level (m) was measured using a laser range finder (Forestry Pro Ⅱ; Nikon Corporation, Minato City, Tokyo, Japan) to measure the vertical diameter from the ground to the nest hole. The nest entrance orientation (˚) was measured using a digital compass based on 360° in the direction of the nest entrance hole. Entrance vertical and horizontal diameter (cm) were measured using a 30 cm ruler, and the nest entrance area was measured using the Image J. (v.1.52) program after photographing the hole. Distance between entrance hole and nest (cm) was measured using an endoscope camera (Bluetec BS-99E).
To confirm the breeding schedule and breeding status of the nests, we visited each nest at 3-day intervals, and recorded the reproductive schedule (egg laying date, duration of incubation period, duration of brooding period, and fledging date using the Julian calendar) and clutch size. We recorded the breeding schedules for all nests only for the first clutch except where re-breeding occurred. For nests that were found after hatching, we inferred the hatching date by tracing back the status of the chicks (see Lee et al. 2020). The reproductive success rate was defined as the proportion of all clutches with eggs that fledged at least one fledgling.
Statistical analysis
Prior to conducting the statistical analysis, we used the Kolmogorov-Smirnov test to determine the normality of the nest variable data. We used a t-test to analyze the differences between the natural holes and artificial holes for nest height, entrance vertical and horizontal diameter, and entrance hole to nest distance. We also tested mean angle for uniform orientation using the Rayleigh test (Zar 1999). We used a Mann-Whitney U test to analyze the variables that did not show normality: duration of incubation period, duration of brooding period, clutch size, the number of fledglings, and reproductive success. In addition, we used Spearman's correlation to analyze the correlation between the nest entrance area and the distance between entrance hole and nest. All data were expressed as means ± standard deviations. For statistical analysis, we used the ‘circular’ package in R software ver. 4.2.2. to conduct the Rayleigh test of uniformity, and IBM SPSS Statistics v.20 (IBM Cooperation, Armonk, NY, USA) for performing the other statistical tests.
Results
In the study area, during the primary breeding period, we located 39 tree sparrow nests. Of these, 18 were identified as natural hole and 21 as artificial hole nests. The tree sparrows that nested in natural holes used woodpecker's holes (n = 6) or cracks in trees (n = 12), whereas tree sparrows that nested in artificial holes used holes in concrete buildings (n = 4), holes under roofs (n = 3) or in steel frames (n = 7), air conditioner gaps (n = 4), and nesting boxes (n = 2). The average vertical height above ground level of the tree sparrow nests was 6.85 ± 3.49 m (range: 2.4–13.4 m), and a larger number of nests were distributed at a height of 2–4 m compared to the other height ranges (Fig. 2A). Nest entrance orientations were distributed in all four quartiles; however, 48.7% of the nests were oriented in the north-west arc, whereas only 20.5% of nests faced towards the south or southeast (Fig. 2B), and nest entrances were randomly distributed (Rayleigh's test: z = 0.23, P = 0.13). The shapes of the nest holes were mostly round, oval, or rectangular, and the average entrance horizontal and vertical diameter, and entrance area was 8.27 ± 2.54 cm, 9.52 ± 5.06 cm, and 64.77 ± 33.78 cm2, respectively (Table 1). Of these hole dimensions, the natural and artificial holes were significantly different in entrance horizontal diameter (t = 2.43, P = 0.02). The average distance between entrance hole and nest was 46.61 ± 18.73 cm, and increased as the entrance area increased. Where the entrance area to a natural and artificial hole was similar, the nest in the artificial hole was found to be located further from the entrance compared to the nest in the natural hole (Table 1; distance between entrance hole and nest: t32 = 4.66, P < 0.05), and the rate of increase in distance between entrance hole and nest relative to the increase in nest entrance area was larger for the artificial than for the natural nest sites (Fig. 3; natural sites: rs = 0.374, n = 17, P = 0.140; artificial sites: rs = 0.736, n = 17, P < 0.05). Regardless of the entrance area, the tree sparrows filled the inner nest space with nesting materials, such as dry grass and string, to create a hole just large enough for one individual to enter and exit the nest.
Distribution of tree sparrow nest height above ground level by natural and artificial site (A). Nest entrance orientation (B). The arrows indicate the number of nests in 30° subdivisions of the compass
Citation: Animal Taxonomy and Ecology 70, 1; 10.1556/1777.2024.12046
Characteristics of tree sparrow nests located in natural and artificial sites in the study area
| Total nests (n) | Natural site (n) | Artificial site (n) | t | P | |
| Nest height (m) | 6.85 ± 3.49 (39) | 6.95 ± 3.28 (18) | 6.77 ± 3.74 (21) | 0.73 | 0.94 |
| Entrance vertical diameter (cm) | 8.27 ± 2.54 (38) | 7.22 ± 2.31 (17) | 9.12 ± 2.45 (21) | 2.43 | 0.02* |
| Entrance horizontal diameter (cm) | 9.52 ± 5.06 (38) | 10.23 ± 6.58 (17) | 8.95 ± 3.45 (21) | 0.77 | 0.44 |
| Entrance area (cm2) | 64.77 ± 33.78 (38) | 58.98 ± 38.78 (17) | 69.46 ± 29.26 (21) | 0.95 | 0.35 |
| Distance between entrance hole and nest (cm) | 46.61 ± 18.73 (34) | 34.88 ± 11.32 (17) | 58.35 ± 17.41 (17) | 4.66 | <0.001* |
Correlations between tree sparrow nest entrance area and distance between entrance hole and nest. Nest entrance area correlated positively with the entrance hole to nest distance, and nests were constructed more deeply in artificial site holes than in natural site holes
Citation: Animal Taxonomy and Ecology 70, 1; 10.1556/1777.2024.12046
Nesting in natural or artificial holes did not appear to affect the breeding schedule, breeding period, or reproductive success rate of the tree sparrows (Table 2). The breeding schedule and breeding status of the tree sparrows did not show significant differences between the natural and artificial nesting sites. Although the tree sparrows nesting in the artificial holes began breeding earlier compared to those nesting in the natural holes, there was no significant difference in the breeding schedule between the nest types (Fig. 4; first egg laying date: Z = 0.17, P = 0.864; incubation initiation date: Z = 0.02, P = 0.986; hatching date: Z = 0.42, P = 0.677; and fledging date: Z = 0.39, P = 0.696). In the study area, on average, the tree sparrows laid one egg per day, the incubation period lasted 9.36 ± 0.65 days, and the brooding period 16.19 ± 1.26 days. The average clutch size per breeding pair was 4.41 ± 0.73, and the average number of fledglings per nest was 3.48 ± 1.18. The reproductive success rate for all nests in the study area was 78.56 ± 26.07%, and there was no significant difference in success rate between the natural and artificial nest types (Table 2). There was no correlation between nest height and reproductive success rate for all nests (rs = 0.316, n = 29, P = 0.095), and there was no significant difference between nest height and reproductive success rate for the natural compared to the artificial sites (natural sites: rs = 0.347, n = 16, P = 0.188; artificial sites: rs = 0.239, n = 13, P = 0.431). Factors that appeared to contribute to the reproductive failure of the tree sparrows were starvation and nest abandonment in nests in the natural holes, and non-hatching and nest abandonment in the nests in the artificial holes. We did not observe occasions of predation on tree sparrow eggs, fledglings, or adults either in the artificial or the natural nesting holes.
Breeding schedule and reproductive performance of tree sparrows in nests in natural and artificial sites
| Total nests (n) | Natural site (n) | Artificial site (n) | Z | P | |
| Incubating period (days) | 9.36 ± 0.65 (33) | 9.47 ± 0.62 (17) | 9.25 ± 0.68 (16) | 0.90 | 0.36 |
| Brooding period (days) | 16.19 ± 1.26 (32) | 16.38 ± 1.36 (16) | 16.00 ± 1.16 (16) | 1.28 | 0.19 |
| Clutch size (n) | 4.41 ± 0.73 (29) | 4.38 ± 0.72 (16) | 4.46 ± 0.78 (13) | 0.82 | 0.41 |
| No. of fledglings (n) | 3.48 ± 1.18 (29) | 3.56 ± 1.21 (16) | 3.38 ± 1.19 (13) | 0.36 | 0.71 |
| Reproductive success (%) | 78.6 ± 26.1 (29) | 81.5 ± 25.4 (16) | 75.0 ± 27.5 (13) | 0.42 | 0.67 |
Comparison of the breeding schedules of tree sparrows nesting in natural site holes and artificial site holes during the first breeding season
Citation: Animal Taxonomy and Ecology 70, 1; 10.1556/1777.2024.12046
Discussion
The urban environment commonly has a negative effect on bird reproduction in relation to nest site selection, nest construction, and food searching (Luniak 2004, Mikula et al. 2014). The findings of this study indicated that tree sparrows living in the urban environment of the university campus selected nest sites regardless of whether they were natural or artificial holes, and there were no differences in physical characteristics such as nest height above ground level and entrance area between the natural and artificial holes. In addition, the reproductive success rate was not significantly different between birds nesting in the natural and artificial holes, and there was no significant difference in the breeding schedule and brooding period. Therefore, the tree sparrow can be regarded as a representative species that has successfully adapted to the urban environment.
The study site, Chonnam National University, is an area where green space and buildings are harmonized in an urban environment. In this area, tree sparrows selected nests in different types of holes regardless of whether the holes were of natural or artificial origin. The natural nesting sites were holes in sycamore trees, old nests of woodpeckers, and cracks in rotten tree trunks in the study area on the university campus. The artificial nesting sites were under roofs and in cracks in buildings, nesting boxes, air conditioner holes, and steel structures. According to previous research, tree sparrows use artificial structures such as traffic lights and road signs as nesting sites in fully urbanized areas (Jeong & Lee 2020), and where nesting boxes have been installed in cities in sufficient numbers, these birds use the nesting boxes as their main breeding sites (García-Navas et al. 2008). Whereas some species of birds select specialized nesting sites, there are other species that are highly tolerant of nesting sites in alternative areas (Stauffer & Best 1980). In the campus area, the tree sparrows selected a range of hole types, not determined by natural or artificial nest sites. Other bird species that reproduce in urban artificial structures include the common swift (Apus apus) and wire-tailed swallow (Hirundo smithii), both of which nest in holes in houses; the house sparrow that uses non-specific types of holes; the rose-ringed parakeet (Psittacula krameria) that uses holes in native vegetation; and the blue tit (Cyanistes caeruleus) and great tit (Parus major) that use nest boxes (Sohi & Kler 2017, Reynolds et al. 2019). Among these species, the most tolerant nesters are the tree sparrow and house sparrow, which try to breed in urban environments, regardless of the types and locations of the holes they use, such as in buildings, power poles, or in natural holes (Indykiewicz 1991). In contrast, blue tits and great tits do not nest in a range of artificial structures but use only nesting boxes, even when adapted to the urban environment, and rose-ringed parakeets use only natural holes in urban environments (Sohi & Kler 2017). The European starling (Sturnus vulgaris), a species successfully adapted to the urban environment, attempts breeding regardless of the type of hole, and nests in places such as natural holes, old woodpecker's nests, nesting boxes, and cracks in buildings (Feare 1984). Utilization of a range of nesting sites by European starlings is associated with a population explosion of this species in North America (Cabe 1998). Along with the house sparrow and the European starling, the tree sparrow is regarded as a typical synurbic species because it tries to breed widely, using breeding sites not limited by a particular type of hole.
In the present study, the nest heights of the tree sparrows ranged from 2 to 14 m, and the nest entrance orientation was mainly towards the northwest. Generally, nest height is considered a primary defense factor against predators, where lower nests have a higher predation pressure from ground predators than higher nests (Nilsson 1984, Albano 1992). However, the higher the nest, the greater the energy demand for movement to and from the nest, especially during nest construction, and higher nests may be disadvantageous because they may be more easily detected by aerial predators compared to lower nests (Preston & Norris 1947). In the campus area under study, the tree sparrow nests in natural holes ranged in height from 4 to 6 m, whereas the nests in artificial holes were mostly located at a height of 2–4 m. These findings are similar to those of a study on nest height in suburban habitats (Preston & Norris 1947), which indicated that adaptation works to find ecological balances, suggesting that tree sparrows find suitable sites to gain benefits from avoiding predation threats (Nilsson 1984, Indykiewicz 1991), while minimizing the energy investment required for feeding and brooding (Barnard 1980, Dobkin et al. 1995, Summers-Smith 1995). Regarding nest entrance orientation, approximately 50% of the tree sparrow nest entrances were facing northwest, but there were also a relatively large number of nests in other directions, which were randomly distributed. According to Losin et al. (2006), nest entrance orientation is related to microclimate where sunlight and temperature conditions influence the nest selection of birds (Preston & Norris 1947, Butcher et al. 2002). In addition, ease of access to feeding grounds (Dobkin et al. 1995) and wind direction (Facemire et al. 1990) also affect the selection of nest entrance orientation. In the case of the red-naped spasucker (Sphyrapicus nuchalis), a primary cavity nester, nests are built by drilling south-facing holes to maximize nest exposure to direct sunlight to create a warm nest microclimate (Losin et al. 2006). In contrast, secondary cavity nesters have to compete for occupancy of a limited number of pre-existing nest sites with a range of entrance hole orientations. Secondary cavity nesters may show a nest orientation preference, for example, Rendell and Robertson (1994) reported that the tree swallow (Tachycineta bicolor) favors a south-facing hole, whereas the European starling has no particular preference for hole orientation. Nest selection in tree swallows is known to favor sites oriented such that nest temperature is maintained by exposure to sunlight and wind prevention (Lumsden 1986). In contrast, European starlings do not show a particular preference for nest entrance orientation because avoidance of predation pressure in relation to nest exposure is more important than nest temperature control. The house wren (Troglodytes aedon) also chooses a range of nest entrance orientations, most likely because nest construction includes covering the nest hole and filling empty spaces with nesting material (Kendeigh 1963). Because tree sparrows fill all of the empty space in their nest cavities with nesting material (Lee et al. 2020), it is relatively easy to maintain the temperature condition in the nest. Thus, nest site selection in tree sparrows was more likely driven by avoidance of predation pressure, which reduces nest exposure and controls height, than by choice of nest entrance orientation.
In the present study, the nest entrance area did not differ significantly between nests in natural and artificial structures. According to Summers-Smith (1995), tree sparrows prefer nests with small holes with a diameter of 32–34 mm, but they also choose nests with larger holes, such as owl nesting boxes (Löhrl 1978). Findings of the present study indicated that the nest entrance area of natural and artificial holes selected by tree sparrows was as small as 12.5 cm2 and as large as 138.5 cm2. This big range in nest entrance area may be because tree sparrows fill the empty spaces in their nests with nesting materials during nest construction; consequently, the internal hole into the nest chamber is mostly of a similar size in all nests, even if the entrance hole is large (Löhrl 1978, Summers-Smith 1995, Lee et al. 2020). This nesting behavior is similar to that of the Eurasian nuthatches (Sitta europaea) where narrowing the entrance hole is accomplished using mud (Cantarero et al. 2015). Hole narrowing behavior occurs for several reasons, such as protection of nests from access by other species, including potential predators (Fernandez-Juricic & Jokimäki 2001); prevention of nest uses for reproduction by other species (Reynolds et al. 2019); and optimizing thermal effects (Kendeigh 1963). In addition, findings of the present study showed that the distance from the entrance hole to the chamber increased with increasing nest entrance area for both the natural and artificial nests, and the distance from the entrance hole to the chamber created in the artificial nests was longer compared to that in the natural nests. Based on these findings, we suggested that tree sparrows have successfully adapted to the urban environment because their hole narrowing behavior enables them to utilize a range of pre-existing hole types.
Generally, the reproductive success rate of birds is higher where nests occur in natural rather than artificial sites (Wilson et al. 1998, Berry & Lill 2003, Burke et al. 2004); however, in the present study, the reproductive status (breeding period, clutch size, and reproductive success) of the tree sparrows did not show significant differences between the natural and artificial nesting sites, a finding that could be attributed to three explanations. First, the location of breeding nests in the exterior walls of buildings and in steel structures facilitates the avoidance of opportunistic nest predators such as cats and mice (see Stracey 2011), which are the main predators in urban environments. Second, the nest predation rate was low because of the low number of potential predators in the urban compared to the natural environment, including snakes, which are specialized nest predators (see Stracey 2011). Third, the study site is adjacent to large areas of paddy fields and forests; consequently, there is a sufficient supply of caterpillars, the main food source of tree sparrows. According to Zhang and Zheng (2010), the number of tree sparrows adapted to the urban environment is inversely proportional to the urbanization score, which is affected by the decrease in the size of the green environment. In addition (Šálek et al. 2015), found that the number of sparrows in an urban environment is inversely correlated to the building area, but positively correlated to the green area in the city. This is most likely because the distribution of the green environment is directly related to the abundance of caterpillars, the main food source of breeding birds, which affects the reproductive success (Pinowska et al. 1999). Similarly, house wren breeding populations in urban environments show a higher reproductive success rate due to lower predation pressure than experienced by populations breeding in the countryside; however, the size and weight of the nestlings were lower in the urban population due to a lack of nutrient supply at the early developmental stage (Newhouse et al. 2008). In contrast, in the case of the house sparrow, populations breeding in urban environments experienced a lower food source supply for the nestlings compared to populations in the countryside, and the reproductive success rate in urban populations was lower than in rural populations (Crick et al. 2002, Peach et al. 2008, Seress et al. 2012). The findings of the present study suggest that tree sparrows can successfully adapt to an urban environment where buildings and other human-related structures are sufficiently harmonized with green space because they obtain the benefits of predation pressure avoidance and a sufficient supply of food resources.
Bird species living in urban environments face several challenges, including a limited availability of suitable nest sites, lack of food sources, emergence of new predators, rapid temperature changes, and noise and light pollution (reviewed in Marzluff 2017). Tree sparrows successfully adapt to urban environments by occupying relatively empty ecological niches, including by breeding in non-specialized holes and using anthropogenic nesting materials (Reynolds et al. 2019, Lee et al. 2020). Consequently, tree sparrows have more reproductive opportunities than other bird species that do not adapt to the urban environment and show a high reproductive success rate. Therefore, we judge the tree sparrow to be a typical urban species because it demonstrates wide versatility in nest selection by selecting nest holes randomly distributed in both natural and artificial sites, despite several limiting factors associated with living in an urban environment.
Acknowledgement
We specially thanks to Prof. Ji-Woong Lee and Hyun Jeong from college of agriculture and life sciences of CNU for the providing research site. We also thank to reviewers and editor for their helpful comments of the manuscript. This study was supported by the National Research foundation of Korea (NRF) grant funded by the Korea government (MSIT) [NRF-2019R1F1A1061024].
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