Processing math: 100%
Qian Hu, Ye Wen, Gaoyang Yu, Jiangnan Yin, Haohui Guan, Lei Lv, Pengcheng Wang, Jiliang Xu, Yong Wang, Zhengwang Zhang, Jianqiang Li. 2020: Research activity does not affect nest predation rates of the Silver-throated Tit, a passerine bird building domed nests. Avian Research, 11(1): 28. DOI: 10.1186/s40657-020-00214-9
Citation: Qian Hu, Ye Wen, Gaoyang Yu, Jiangnan Yin, Haohui Guan, Lei Lv, Pengcheng Wang, Jiliang Xu, Yong Wang, Zhengwang Zhang, Jianqiang Li. 2020: Research activity does not affect nest predation rates of the Silver-throated Tit, a passerine bird building domed nests. Avian Research, 11(1): 28. DOI: 10.1186/s40657-020-00214-9

Research activity does not affect nest predation rates of the Silver-throated Tit, a passerine bird building domed nests

Funds: 

the National Natural Science Foundation of China 31970421

the National Natural Science Foundation of China 31472011

the National Natural Science Foundation of China 31101644

More Information
  • Corresponding author:

    Jianqiang Li, lijianqiang@bjfu.edu.cn

  • Received Date: 12 Jul 2020
  • Accepted Date: 29 Jul 2020
  • Available Online: 24 Apr 2022
  • Publish Date: 02 Aug 2020
  • Background 

    Research activities have often been thought to potentially influence avian nesting success by increasing nest predation rates. Although recent studies of species building open nests and cavity nests suggest that research disturbance does not generally induce nest predation, whether it is also the case in species building domednests remains unknown. In birds, domed-nest species exist in about half of the passerine families, and research disturbance to the domed nests may differ from that to the nests of other types for their different nest structures.

    Methods 

    We investigated if research activities affected nest predation rate by analyzing the relationships of the daily nest survival rate with the research activities at the egg and nestling stages of a domed-nest species, the Silverthroated Tit (Aegithalos glaucogularis).

    Results 

    Our results showed that nest daily survival rate was significantly affected by the laying date and nest age during the egg stage, and by the hatching date only during the nestling stage. By contrast, there were no significant effects of research activities, in terms of visiting nests and filming nests, on the nest survival of the Silver-throated Tit at both the egg and nestling stages.

    Conclusions 

    Our results coincide with the findings in species building other types of nests that research activities do not always have negative effects on avian nesting success.

  • Foraging habitat selection by birds is defined as a non-random choice by avian individuals of certain feeding sites, which is a connotation of understanding complex behavioral and environmental processes, and it is a decision-making process that researchers need to make an attempt to describe how the observed patterns reflect individual choice (Jones 2001; Beest et al. 2010). Thus, an understanding of how birds choose foraging sites is very important for the conservation management of winter migratory birds and their overwintering habitats (Goss-Custard et al. 2002; Davis et al. 2014; Kaminski and Elmberg 2014). The Black-necked Crane (Grus nigricollis) is the only crane species that lives on the Qinghai-Tibet Plateau throughout its lifetime, and it is also the crane species that was most recently identified and recorded by humans among the 15 species of cranes throughout the world (Qian et al. 2009; Che et al. 2018; Sun et al. 2018). The Black-necked Crane is mainly distributed in the Qinghai-Tibet Plateau and Yunnan-Guizhou Plateau of China. Its breeding area is in the northern and western Qinghai-Tibet Plateau, while its wintering area is mainly in the middle of the Yarlung Zangbo River Valley, the south slope of the Himalayas and some parts of the Yunnan-Guizhou Plateau (Qian 2009). The Black-necked Crane is considered Vulnerable (VU) according to the IUCN Red List and is a nationally protected species in China (Category I).

    In the early 20th century, the research on waterfowl mainly focused on breeding areas; however, since the end of the 20th century, more and more research on waterfowl began to shift to the non-breeding season, including habitat selection and utilization, especially in migratory waterfowl (Davis et al. 2014; Kaminski and Elmberg 2014). In addition to the lakeshore, some previous studies have revealed that Black-necked Cranes strongly depend on crop remains in the farming areas around wetlands as food for survival while overwintering (Tsamchue et al. 2008). Black-necked Cranes prefer the tuberous of Cyberaeae plants on lakeshores and potatoes (Solanum tuberosum) and maize (Zea mays) in cultivated lands (Bishop and Li 2002). However, in most of the studies of Black-necked Crane in relation to Caohai and other overwintering wetlands, it is still not so clear what and how they forage in the farming areas. According to Wiens' classification method (Wiens 1973), some researchers divided the habitat selection of Black-necked Crane into three levels (Li 1999; Sun et al. 2018). It was concluded that Black-necked Crane would prefer to choose the sedge meadow around Caohai Lake, and the selection of agricultural land was relatively low (Li 1999). Its foraging was mainly based on the roots of sedge plants, and the selection of crops was less (Li and Nie 1997; Li 1999; Li and Li 2005). According to the latest research and investigations, each day during winter, most Black-necked Cranes fly to the outer area to forage in the farmlands in the mornings and fly back to fixed points of the inner area to roost in the evening (Bishop and Li 2002; Sun et al. 2018). Bird foraging will be affected by food, water and concealment (Yang et al. 2011). But, for the Black-necked Crane of Caohai Waterland, the factors affecting the selection of foraging habitat by Black-necked Cranes in the farming area are still poorly understood.

    Based on the field investigation and analysis, this paper aims to answer the following two questions: (1) what are the factors influencing the selection of foraging land in the farming area? (2) what are the main influencing factors in different overwintering periods? By answering these questions, we hope to provide reference for local conservation of this crane species.

    The Caohai Wetland (with the main body of the Caohai National Nature Reserve, 26°47′‒26°52′N, 104°10′‒104°20′E), is located in the Guizhou Plateau, southwestern China, next to Weining County, Guizhou Province. This wetland is the largest natural freshwater lake in Guizhou, is regarded as a typical wetland ecosystem of the subtropical plateau in China due to its relatively integrated structure and function, and is an important site for the overwintering and stopover of migratory birds in southwestern China (Ran et al. 2017). The total area of Caohai is 120 km2 with 25 km2 of water. The elevation of the normal water level is 2171.7 m, and the maximum water depth is 5.0 m. Caohai belongs to the subtropical plateau monsoon climate, with the yearly average temperature of 10.9 ℃ and the coldest monthly average (January) temperature of 2.1 ℃. Every winter, more than 80 species of waterbirds and 80, 000 individual birds live in Caohai Wetland (Zhang et al. 2014).

    Because the Caohai Wetland is close to Caohai County, the competition for living space between human beings and birds is more intense than other wintering areas. In recent years, construction for urban expansion plus a reduction in traditional tillage and increases in human activities have decreased the amount of farmland, especially after the construction of a 29.5 km road circling the lake in 2014, Caohai is divided into two parts by this road, i.e., the inner lakeshore area and the outer residential and farming area (see Fig. 1). This has led to a more prominent situation.

    Figure  1.  Land use map of farming areas around the Caohai wetland

    The field survey was conducted in two winter periods of 2016‒2017 and 2017‒2018. According to the duration of Black-necked Crane overwintering and local meteorological conditions, we divided each winter into three stages, namely, early winter (11th of November to 31st of December, EW), mid-winter (1st of January to 20th of February, MW) and late winter (21st of February to 31st of March, LW). We surveyed from 08:00‒17:00 every day in sunny, windless weather conditions, for at least 15 days in each stage. This pattern was repeated for both winters. To locate all foraging sites of Black-necked Cranes in farmland around the wetland, we used ArcGIS (version 10.3.0) software to define a 500 m × 500 m grid to investigate each grid square (see Fig. 1). In one grid, we tried to stay in the highlands to observe the Black-necked Crane foraging behavior using a monocular telescope (Magnification 20‒60 ×) without disturbing the birds. If the site has foraging behavior without interference and is continuously foraged for more than 15 min, we located and recorded this site as a foraging site, and recorded the landuse type here.

    To study habitat selection, we sampled the foraging points for the investigation of habitat environmental factors. After the Black-necked Crane left here to forage elsewhere, we set up a large quadrat (5 m × 10 m) in the center of each crop patch where a foraging point was located and 5 small quadrats (1 m × 1 m) at the center and the 4 corners of the patch. See Table 1 for a list of all variables investigated. A total of 98 large quadrats were defined during the study periods (early winter: 23; mid-winter: 32; late winter: 43).

    Table  1.  Sampling variables for the selection of foraging habitats
    Category Variables Description
    Topographic factors Slope degree (°) Large quadrat: < 10° = 1, 10°‒20° = 2, 20°‒30° = 3, > 30° = 4
    Slope aspect Large quadrat: shady slope = 1 (‒67.5° to 67.5°), sunny slope = 2 (112.5°‒247.5°), semi-sunny slope = 3 (67.5°‒112.5°, 247.5°‒292.5°)
    Slope position Large quadrat: upper = 1, middle = 2, lower = 3
    Human disturbance factors Distance to water (m) Straight-line distance (m) between the center of a large quadrat and the nearest water (ditch, canal, brook, or pool)
    Distance to settlement (m) Straight-line distance (m) between the center of a large quadrat and the nearest residence
    Distance to road (m) Straight-line distance (m) between the center of a large quadrat and a road
    Distance to tillagers (m) Straight-line distance (m) between the center of a large quadrat and the nearest farmer working at a site
    Food factors Types of food Type of crop: corn, potato, radish, cabbage, rape, shallot, green manure, tobacco
    Food richness If more than two kinds of crops were in a large quadrat: yes = 1, no = 0
    Crop remains (g/m2) The crop remains (g/m2): the average of 5 small quadrats, measured by an electronic balance
    Tillage methods Whether the crop patch was plowed by machine: yes = 1, no = 0
     | Show Table
    DownLoad: CSV

    Using the Landsat OLI dataset from 2017, the data were corrected with the error control at 0.5 pixels. Additionally, using SPOT digital orthophoto images as references, we used ERDAS (ver.10.0) software for mask extraction to obtain the qualified images of our study area using the 1954 Beijing Projection Coordinate System. Finally, ArcGIS10.3.0 is used to map land use types. During the mapping process, the data were corrected according to the classification of land use status (GB/t201010-2017) and the environmental conditions of field investigation. We classified the study area into five classes: farmland, woodland, water, construction land, and natural grasslands. Additionally, farmland was divided into different patches: corn, potato, radish, cabbage, rape, shallot, green manure, tobacco, machine-plowed or non-machine-plowed (Fig. 1).

    We used the principal component analysis to reveal the main factors (slope degree, slope aspects, slope position, distance to water, distance to settlement, distance to road, distance to tillagers, food richness, crop remains, tillage methods) influencing the foraging habitat selection by Black-necked Crane in farmland. We retained the principal components with eigenvalues greater than or equal to 1.0 and determined the main factors that contributed the most to habitat selection.

    We also used selectivity coefficients (Wi) and the selectivity index (Ei) (Vanderploeg and Scavia 1979) to determine how Black-necked Cranes chose foraging patches under the influences of the main factors. The formulas are as follows:

    Ei=(Wi1/n)/(Wi+1/n)
    (1)
    Wi=(ri/pi)/(ri/pi)
    (2)

    where i is the level of a feature of the eco-factor (variables); n is the number of levels; pi is the proportion of samples with feature level i in all samples in the whole study areas; ri is the proportion of samples with feature level i in all samples in the foraging land of the overwintering Black-necked Cranes. Ei= - 1 represents no choice, expressed as NP; - 1 < Ei < 0 represents a tendency to avoid, expressed as NP; Ei = 0 or approaching 0 represents a random choice, expressed as R; 0 < Ei < 1 represents a positive choice, expressed as S; and Ei = 1 represents a highly positive choice, expressed as SP (Wei et al. 1996).

    To analyze the influencing patterns of the main factors that varied during the different stages in winter, one-way ANOVA and LSD multi-comparisons were used for the continuous variables, while a Chi square test was applied to discrete variables. In the analysis, P < 0.01 means an extremely significant difference; 0.01 < P < 0.05 means a significant difference; and P ≥ 0.05 represents no significant difference.

    All statistical analyses were conducted by using R 3.6 (R Core Development Team 2019) and SPSS software.

    Four components (eigenvalue > 1.0) were determined to have a 65.83% cumulative contribution explaining the PCA results, reflecting the main factors influencing the selection of foraging habitats by Black-necked Crane. According to the scores of the load factors, we focused on the variables with significantly high scores and renamed them. In the first principal component (PC), tillage methods (- 0.875) and crop remains (0.771) were renamed as the food factor; in the second and third PCs, the distance to residences (0.678), distance to tillagers (0.631), and distance to roads (0.698) were renamed as the distance factor; and in the fourth PC, the slope (0.639) was renamed as the topographic factor (see Table 2).

    Table  2.  Contributions of habitat factors to the principal components in foraging areas in the farming areas
    Factors PC-1 (27.525) PC-2 (42.899) PC-3 (55.785) PC-4 (65.827)
    Slope aspect - 0.259 0.484 - 0.214 0.639
    Slope degree (°) - 0.680 0.254 - 0.008 - 0.286
    Slope position 0.351 - 0.463 - 0.221 - 0.007
    Distance to road (m) 0.092 0.388 0.698 0.016
    Distance to water (m) 0.661 - 0.053 0.175 - 0.232
    Distance to tillagers (m) 0.426 0.189 0.631 0.240
    Distance to settlement (m) 0.187 0.678 - 0.433 - 0.048
    Tillage methods - 0.875 0.130 0.170 - 0.064
    Crop remains (g/m2) 0.771 0.283 - 0.235 0.188
    Food richness - 0.281 - 0.527 0.075 0.600
     | Show Table
    DownLoad: CSV

    The selectivity coefficients (Wi) and selectivity indexes (Ei) showed that Black-necked Crane preferred to choose farmland patches as foraging sites, and these patches were located on semi-sunny slopes, with distances to roads ranging from 50‒100 m, distances to a residence within 100‒500 m, and crop remains of greater than 500 g/m2, and the preferred patches were not machine-plowed (see Table 3).

    Table  3.  Selective parameters of major habitat factors for foraging habitats
    Factors I Pi Ri Wi Ei Preference
    Slope aspect Shady slope 0.400 0.347 0.867 - 0.106 R
    Sunny slope 0.360 0.265 0.737 - 0.186 R
    Semi-sunny slope 0.240 0.388 1.616 0.202 S
    Distance to road (m) < 50 0.389 0.388 0.998 - 0.002 R
    50-100 0.303 0.347 1.145 0.067 S
    > 100 0.309 0.265 0.860 - 0.076 R
    Distance to settlement (m) < 100 0.263 0.031 0.116 - 0.773 NP
    100‒500 0.389 0.592 1.523 0.253 S
    > 500 0.349 0.378 1.083 0.088 R
    Tillage methods Yes 0.657 0.531 0.807 - 0.148 R
    No 0.343 0.469 1.369 0.114 S
    Crop remains (g/m2) < 100 0.486 0.306 0.630 - 0.299 NP
    100‒500 0.366 0.449 1.228 0.025 R
    > 500 0.149 0.245 1.648 0.170 S
    R random choice, S normal choice, SP highly positive choice, NP tending to avoid
     | Show Table
    DownLoad: CSV

    We analyzed the results of the Chi square test and LSD multi-comparison tests that compare the main factors of the crop remains, distance to roads and distance to residences during different stages of winter. These three main factors showed extremely significant differences in late winter (P < 0.01) compared to those in mid- and late winter, but there was no significant difference between those in mid- and early winter. Crop remains were greater than 500 g/m2 in early winter but decreased to less than 200 g/m2 in late winter (see Tables 4 and 5).

    Table  4.  LSD multiple comparisons for the main influencing factors between different stages
    Factors Stages of time (Ⅰ) Stages of time (Ⅱ) Mean difference (Ⅰ-Ⅱ) Standard error P Mean ± SD
    EW MW LW
    Crop remains (g/m2) EW MW 75.25 81.27 0.357
    LW 354.68 76.80 0.000** 512.04 ± 359.56 436.79 ± 400.18 157.36 ± 118.33
    MW LW 279.43 69.41 0.000**
    Distance to road (m) EW MW 88.33 19.71 0.000**
    LW 76.94 18.63 0.000** 151.52 ± 89.86 63.19 ± 66.80 74.58 ± 65.08
    MW LW - 11.39 16.83 0.500
    Distance to settlement (m) EW MW - 169.05 49.65 0.001**
    LW - 44.7 46.92 0.343 354.39 ± 163.77 523.44 ± 156.48 399.09 ± 206.16
    MW LW 124.34 42.41 0.004**
    EW early winter, MW mid-winter, LW late winter
    **P < 0.01
     | Show Table
    DownLoad: CSV
    Table  5.  Chi square tests for the main influencing factors between different stages
    Type Stages of time (Ⅰ) Stages of time (Ⅱ) P
    Tillage methods (df=1) EW MW 0.023
    LW 0.000**
    MW LW 0.008**
    EW MW 0.473
    Slope aspect (df=2) LW 0.561
    MW LW 0.004**
    EW early winter, MW mid-winter, LW late winter
    **P < 0.01
    *P < 0.05
     | Show Table
    DownLoad: CSV

    The 3D scatter plot (see Fig. 2) shows that due to the changes in crop remains, the foraging sites were evenly distributed in terms of the main factors of the distance to roads and the distance to residences in early winter. However, in mid-winter, all foraging sites were close to roads (the average was 63.19 m), and some sites with relatively high crop remains were close to residences, but some were far from residences due to low crop remains (the average was 523.44 m). During late winter, when the crop remains were approaching their lowest levels, more foraging sites were close to both roads and residences, without any grouping.

    Figure  2.  Scatter plot of the sampling plots of foraging habitats

    Factors contributing to the first principal component in the PCA were named the food factor, which is also the first factor that influenced when Black-necked Cranes chose a crop patch as a foraging site, as shown in our study. Researchers have previously mentioned that food is the most important factor contributing to habitat selection for animals, especially the nutrition obtained from food resources (Langvatn and Hanley 1993; Storch 1993). The feeding efficiency of Black-necked Cranes often depends to some extent on the soil density of the cultivated farmland of foraging sites, because cranes can use only their beaks and claws when searching for food (Jia et al. 2013). Overwintering Black-necked Cranes in the Huizhe Wetland, Yunnan Province, preferred to forage in plowed land because of the lower soil density and shallowly buried food (Li et al. 2009). Nonetheless, we obtained the opposite result, and Black-necked Cranes in Caohai tended to feed in non-plowed and food-abundant farmlands, although the soil density was higher than that of plowed locations. In recent years, local mechanized tillage has become more popular and will eventually completely replace traditional tillage methods. We found that the crop remains in farmlands plowed by machines were lower than those of patches plowed by traditional methods (P < 0.01); therefore, Black-necked Cranes perhaps preferred non-plowed land over plowed land because of the more abundant food they were able to obtain. Some cases concerning Red-crowned Crane (Grus japonensis) and White-naped Crane (Grus vipio) were reported in farmlands near the Demilitarized Zone dividing North and South Korea, where many cranes foraged in non-machine-plowed farmland because machine-plowing resulted in few crop remains (Li et al. 2009).

    The disturbance factor was also a main influencing factor that contributed to habitat selection by Black-necked Cranes (Jiang et al. 2017; Zhang et al. 2017). Many types of human activities in the farming areas around Caohai depend on roads (Sun et al. 2018). The local government has constructed many roads (especially hard-packed tractor roads between farmlands) to facilitate the agricultural industry, which has shaped a network covering the farming area. Black-necked Crane alert behavior is reliant on the positions of Black-necked Crane individuals (Kuang et al. 2014). Obviously, areas that are farther from roads and residences are more beneficial to foraging Black-necked Cranes due to reduced human disturbance. However, according to the results of the selectivity coefficients (Wi), most of the foraging sites are located within 50‒100 m to the road, rather than farther away from the road, because the farmland in Caohai is divided into small blocks by the road network, and the straight-line distance between most of the roads is within 100 m, which makes the foraging sites distributed near the roads without other options. The distance to water was not a significant influencing factor for Black-necked Cranes in our study, which indicated that Black-necked Cranes do not depend on the water when foraging in the farmland areas.

    Environmental conditions affecting wildlife survival often gradually vary with time during the winter. During the overwintering period in Caohai, foraging choice of Black-necked Crane also varied with changes in the environmental conditions of the foraging habitats during the three different stages of winter (Wu and Li 1985). The main factor, crop food remains, declined sharply over time in winter in Caohai, especially in late winter, when it was only one-third of that available in early winter (mean: 512 g/m2 in early winter, 157 g/m2 in late winter). Due to the changes in food factors, influences from disturbance factors also changed. With the arrival of Black-necked Cranes in early winter, they often showed more alert behaviors because they had to adapt to the relatively new environment (Wu and Li 1985) and preferred to choose crop patches that were far from roads and residences. Upon the onset of mid-winter, weather conditions were more severe, and Black-necked Cranes needed more energy from food, but the crop remains decreased; therefore, the influences of disturbance factors, especially the distance to roads, began to weaken. Black-necked Cranes began to choose crop patches with abundant food remains that were far from residences (the average distance to residences was 500 m in mid-winter) as foraging sites. Black-necked Cranes have difficulty avoiding disturbances from roads because of the developed road networks in farmland areas. We found that foraging sites in this stage were comprised of two groups, as demonstrated on the scatter plot (see Fig. 2). One group of sites was not far from roads but had low crop remains and was used mainly by families of Black-necked Cranes, with a family often consisting of parents and one or two juveniles, meaning that they needed less food than non-family Black-necked Crane groups (Kuang et al. 2014; Zhang et al. 2017) and show more territorial behavior and loyalty to their used foraging sites (Yang et al. 2016; Che et al. 2018). Another group of sites was farther from roads but had higher crop remains and was occupied mainly by non-family Black-necked Crane groups who needed large crop patches to meet their food demands. In late winter, after the last 10 days of February, crop remains decreased to their lowest level. When preparing to fly back to breeding sites, the cranes had to complete fat accumulation and migration excitation, which demands more energy than usual (Zheng 2012; Sun et al. 2018). Therefore, during this stage, influences of disturbance factors, especially those from residences, decreased further, and many foraging sites were distributed close to residences. In early March, local farmers begin spring sowing in Caohai, thus it seems that Black-necked Cranes would obtain more food. However, in contrast, Black-necked Crane foraging sites provide less food at this time because farmers do not allow cranes to damage their cultivated land, and crop patches are reduced due to spring sowing. In the meantime, some Black-necked Cranes have begun to gradually migrate from the Caohai Wetland.

    It is critical for migratory birds to have foraging habitats of sufficient quality for overwintering survival (Davis et al. 2014; Wood et al. 2019). Presently, there are severe conflicts between birds and humans and an ecological imbalance of the wetland system in Caohai (Ran et al. 2017). These can also lead to conflicts between groups of people over how such issues should be managed (Redpath et al. 2015). As a result of the shrinkage of the lakeshore, including the farmlands within it, Black-necked Cranes are becoming more dependent on the outer farmlands surrounding the wetland; hence, protecting and managing the farmlands is critical to Black-necked Crane conservation. It is of great concern that the farmlands relied on by Black-necked Cranes are vanishing for the following reasons: more agricultural development projects are occurring, more areas of farmland reduction are arising, road construction and car owners are becoming more common, the plastic house culture is prevalent, machine tillage is becoming popular, and the traditional crop compositions are being altered. Therefore, we suggest that local authorities control the expansion of construction in farmland areas; partly recover and retain traditional agricultural production, for example, traditional tillage methods and sufficient cultivation of potatoes and buckwheat; and reduce disturbances from human activities to meet the demands by Black-necked Cranes for foraging habitats of sufficient quality for successful overwintering.

    We are very grateful to Mr. Fengshan Li for his valuable comments on the paper.

    DW conceived the study, collected and analysed the data, and wrote the manuscript. HS supervised the research and provided multiple revisions of the writing. CH conducted research method guidance for the article. MZ and ZL implemented the field surveys and collected the data. All authors read and approved the final manuscript.

    The datasets generated and/or analysed during the current study are available from the corresponding author upon reasonable request.

    The investigations comply with the current laws of China, where they were performed.

    Not applicable.

    The authors declare that they have no competing interests.

  • Bartoń K. Package MuMIn. R package version 1.43.6. 2019. . Accessed 27 Oct. 2019.
    Batáry P, Báldi A. Evidence of an edge effect on avian nest success. Conserv Biol. 2004;18:389–400.
    Blackmer AL, Ackerman JT, Nevitt GA. Effects of investigator disturbance on hatching success and nest-site fidelity in a long-lived seabird, Leach's storm-petrel. Biol Conserv. 2004;116:141–8.
    Bocz R, Szép D, Witz D, Ronczyk L, Kurucz K, Purger JJ. Human disturbances and predation on artificial ground nests across an urban gradient. Anim Biodivers Conserv. 2017;40:153–7.
    Briskie JV, Martin PR, Martin TE. Nest predation and the evolution of nestling begging calls. Proc R Soc Lond B-Biol Sci. 1999;266:2153–9.
    Burnham KP, Anderson DR, Huyvaert KP. AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol. 2011;65:23–35.
    Carey MJ. The effects of investigator disturbance on procellariiform seabirds: a review. N Z J Zool. 2009;36:367–77.
    Carey MJ. Investigator disturbance reduces reproductive success in Shorttailed Shearwaters Puffinus tenuirostris. Ibis. 2011;153:363–72.
    Chalfoun AD, Ratnaswamy MJ, Thompson FR. Songbird nest predators in forest-pasture edge and forest interior in a fragmented landscape. Ecol Appl. 2002;12:858–67.
    Collias NE. On the origin and evolution of nest building by passerine birds. Condor. 1997;99:253–70.
    Dinsmore SJ, Dinsmore JJ. Modeling avian nest survival in program MARK. Stud Avian Biol. 2007;34:73–83.
    Ellenberg U, Setiawan AN, Cree A, Houston DM, Seddon PJ. Elevated hormonal stress response and reduced reproductive output in Yellow-eyed penguins exposed to unregulated tourism. Gen Comp Endocrinol. 2007;152:54–63.
    Emery RB, Howerter DW, Armstrong LM, Anderson MG, Devries JH, Joynt BL. Seasonal variation in waterfowl nesting success and its relation to cover management in the Canadian prairies. J Wildl Manage. 2005;69:1181–93.
    Gibson D, Blomberg EJ, Atamian MT, Sedinger JS. Observer effects strongly influence estimates of daily nest survival probability but do not substantially increase rates of nest failure in Greater Sage-Grouse. Auk. 2015;132:397–407.
    Götmark F. The effects of investigator disturbance on nesting birds. In: Power DM, editor. Current Ornithology. Boston: Springer; 1992. p. 63–104.
    Grant TA, Shaffer TL, Madden EM, Pietz PJ. Time-specific variation in passerine nest survival: new insights into old questions. Auk. 2005;122:661–72.
    Guan H, Wen Y, Wang P, Lv L, Xu J, Li J. Seasonal increase of nest height of the Silver-throated Tit (Aegithalos glaucogularis): can it reduce predation risk? Avian Res. 2018;9:42.
    Gutzwiller KJ, Riffell SK, Anderson SH. Repeated human intrusion and the potential for nest predation by gray jays. J Wildl Manage. 2002;66:372.
    Herranz J, Yanes M, Suárez F. Does photo-monitoring affect nest predation? J Field Ornithol. 2002;73:97–101.
    Ibáñez-Álamo JD, Sanllorente O, Soler M. The impact of researcher disturbance on nest predation rates: a meta-analysis. Ibis. 2012;154:5–14.
    Ibáñez-Álamo JD, Soler M. Investigator activities reduce nest predation in blackbirds Turdus merula. J Avian Biol. 2010;41:208–12.
    Jacobson MD, Tsakiris ET, Long AM, Jensen WE. No evidence for observer effects on Lark Sparrow nest survival. J Field Ornithol. 2011;82:184–92.
    Jehle G, Adams AA, Savidge JA, Skagen SK. Nest survival estimation: a review of alternatives to the Mayfield estimator. Condor. 2004;106:472–84.
    Klett AT, Johnson DH. Variability in nest survival rates and implications to nesting studies. Auk. 1982;99:77–87.
    Laake JL. RMark: An R interface for analysis of Capture-Recapture data with MARK. Seattle: National Marine Mammal Laboratory, Alaska Fisheries Science Center; 2013.
    Laake JL, Rexstad E. R code for MARK analysis. R package version 2.2.6. 2019. . Accessed 14 Aug. 2019.
    Ledwoń M, Betleja J, Neubauer G. Different trapping schemes and variable disturbance intensity do not affect hatching success of Whiskered Terns Chlidonias hybrida. Bird Study. 2016;63:136–40.
    Leech SM, Leonard ML. Begging and the risk of predation in nestling birds. Behav Ecol. 1997;8:644–6.
    Li J, Lv L, Wang Y, Xi B, Zhang Z. Breeding biology of two sympatric Aegithalos tits with helpers at the nest. J Ornithol. 2012;153:273–83.
    Li J, Wang Y, Lv L, Wang P, Hatchwell BJ, Zhang Z. Context-dependent strategies of food allocation among offspring in a facultative cooperative breeder. Behav Ecol. 2019;30:975–85.
    Lloyd P, Plagányi ÉE. Correcting observer effect bias in estimates of nesting success of a coastal bird, the White-fronted Plover Charadrius marginatus. Bird Study. 2002;49:124–30.
    MaCivor LH, Melvin SM, Griffin CR. Effects of research activity on piping plover nest predation. J Wildl Manage. 1990;54:443.
    Mainwaring MC, Reynolds SJ, Weidinger K. The influence of predation on the location and design of nests. In: Deeming DC, Reynolds SJ, editors. Nests, eggs, and incubation: new ideas about avian reproduction. New York: Oxford University Press; 2015. p. 50–64.
    Major RE. The effect of human observers on the intensity of nest predation. Ibis. 1990;132:608–12.
    Martin TE, Geupel GR. Nest-monitoring plots methods for locating nests and monitoring success. J Field Ornithol. 1993;64:507–19.
    Martin TE, Scott J, Menge C. Nest predation increases with parental activity: separating nest site and parental activity effects. Proc R Soc B-Biol Sci. 2000;267:2287–93.
    McDonald PG, Wilson DR, Evans CS. Nestling begging increases predation risk, regardless of spectral characteristics or avian mobbing. Behav Ecol. 2009;20:821–9.
    Meixell BW, Flint PL. Effects of industrial and investigator disturbance on arcticnesting geese. J Wildl Manage. 2017;81:1372–85.
    Monroe AP, Martin JA, Riffell SK, Burger LW. Effects of measuring nestling condition on nest success in the dickcissel (Spiza americana). Wildl Soc Bull. 2014;38:401–6.
    Mouton JC, Martin TE. Nest structure affects auditory and visual detectability, but not predation risk, in a tropical songbird community. Funct Ecol. 2019;33:1973–81.
    Moynahan BJ, Lindberg MS, Rotella JJ, Thomas JW. Factors affecting nest survival of greater sage-grouse in northcentral Montana. J Wildl Manage. 2007;71:1773–83.
    Orzechowski SCM, Shipley JR, Pegan TM, Winkler DW. Negligible effects of blood sampling on reproductive performance and return rates of Tree Swallows. J Field Ornithol. 2019;90:21–38.
    R Development Core Team. R: A language and environment for statistical computing version 3.1.6. Vienna, Austria: R Foundation for Statistical Computing; 2019. .
    Richardson TW, Gardali T, Jenkins SH. Review and meta-analysis of camera effects on avian nest success. J Wildl Manage. 2009;73:287–93.
    Rodway MS, Montevecchi WA, Chardine JW. Effects of investigator disturbance on breeding success of Atlantic puffins Fratercula arctica. Biol Conserv. 1996;76:311–9.
    Ropert-Coudert Y, Knott N, Chiaradia A, Kato A. How do different data logger sizes and attachment positions affect the diving behaviour of little penguins? Deep Res Part Ⅱ-Top Stud Oceanogr. 2007;54:415–23.
    Rosenberg KV, Dokter AM, Blancher PJ, Sauer JR, Smith AC, Smith PA, et al. Decline of the North American avifauna. Science. 2019;366:120–4.
    Segura LN, Reboreda JC. Nest survival rates of Red-crested Cardinals increase with nest age in south-temperate forests of Argentina. J Field Ornithol. 2012;83:343–50.
    Stein A, Young MJ, Seddon PJ, Darby JT, van Heezik Y. Investigator disturbance does not reduce annual breeding success or lifetime reproductive success in a vulnerable long-lived species, the yellow-eyed penguin. Biol Conserv. 2017;207:80–9.
    Steven R, Pickering C, Guy Castley J. A review of the impacts of nature based recreation on birds. J Environ Manage. 2011;92:2287–94.
    Stien J, Ims RA. Absence from the nest due to human disturbance induces higher nest predation risk than natural recesses in Common Eiders Somateria mollissima. Ibis. 2016;158:249–60.
    Sutherland WJ, Newton I, Green R. Bird ecology and conservation: a handbook of techniques. Oxford and New York: Oxford University Press; 2004. p. 62–4.
    Touihri M, Charfi F, Villard MA. Effects of landscape composition and native oak forest configuration on cavity-nesting birds of North Africa. For Ecol Manage. 2017;385:198–205.
    Walker J, Lindberg MS, Maccluskie MC, Petrula MJ, Sedinger JS. Nest survival of scaup and other ducks in the boreal forest of Alaska. J Wildl Manage. 2005;69:582–91.
    Weidinger K. Nest monitoring does not increase nest predation in opennesting songbirds: inference from continuous nest-survival data. Auk. 2008;125:859–68.
    White GC, Burnham KP. Program MARK: survival estimation from populations of marked animals. Bird Study. 1999;46:S120–39.
    Yu J, Wang PC, Lü L, Zhang ZW, Wang Y, Xu JL, et al. Diurnal brooding behavior of long-tailed tits (Aegithalos caudatus glaucogularis). Zool Res. 2016;37:84–9.
    Zar JH. Biostatistical analysis. 5th ed. Essex: Pearson Education Limited; 2014.
    Zhao JM, Yang C, Lou YQ, Shi M, Fang Y, Sun YH. Nesting season, nest age, and disturbance, but not habitat characteristics, affect nest survival of Chinese grouse. Curr Zool. 2020;66:29–37.
  • Related Articles

  • Cited by

    Periodical cited type(16)

    1. Hongying Xu, Ru Jia, Hongrui Lv, et al. Habitat suitability and influencing factors of a threatened highland flagship species, the Black-necked Crane (Grus nigricollis). Avian Research, 2025, 16(2): 100243. DOI:10.1016/j.avrs.2025.100243
    2. Wanhui Cao, Qian Wang, Qianjin Cao. Fine-scale spatial genetic structure and gene dispersal in lake populations of submerged species. Journal of Oceanology and Limnology, 2025. DOI:10.1007/s00343-024-4111-z
    3. Yuxin Zhang, Shasha Liu, Yue Qiu, et al. New Insight into the Source Contribution of Dissolved and Particulate Organic Matter in a Typical Macrophyte-Dominated Lake Using Optical Spectroscopy, Stable Isotopes, and FT-ICR MS. ACS ES&T Water, 2025. DOI:10.1021/acsestwater.4c01216
    4. Lanyan Zhong, Yanfang Li, Yalong Li, et al. Hungry wintering birds and angry farmers: Crop damage and management implications in a protected wetland in China. Global Ecology and Conservation, 2025, 57: e03402. DOI:10.1016/j.gecco.2025.e03402
    5. Zhengxia Yang, Linzheng Hu, Ruidong Wu, et al. Multi-taxon species richness representation within national nature reserves is associated with spatial features, human disturbance and environmental factors in mountains region. Global Ecology and Conservation, 2024, 54: e03042. DOI:10.1016/j.gecco.2024.e03042
    6. Fusheng Chao, Xin Jiang, Xin Wang, et al. Water Level Fluctuation Rather than Eutrophication Induced the Extinction of Submerged Plants in Guizhou’s Caohai Lake: Implications for Lake Management. Water, 2024, 16(5): 772. DOI:10.3390/w16050772
    7. Ningjing Kou, Yalong Li, Linjia Pu, et al. Variations of gut microbiota in the wintering black-necked crane (Grus nigricollis) at local and regional scales and its management implications. Global Ecology and Conservation, 2024, 52: e02982. DOI:10.1016/j.gecco.2024.e02982
    8. Xiang Gao, Yiyin Liang, Yutian Zhu, et al. Habitat selection of wintering cranes in typical wetlands in the middle and lower reaches of the Yangtze River over the past 20 years, China. Environmental Science and Pollution Research, 2023, 30(20): 58466. DOI:10.1007/s11356-023-26504-5
    9. Lanyan Zhong, Yanhua Li, Yalong Li, et al. Local farmers' perceptions of ecosystem services and disservices provided by the Black-necked Crane (Grus nigricollis) and their conservation implications. Global Ecology and Conservation, 2023, 46: e02614. DOI:10.1016/j.gecco.2023.e02614
    10. Xuezhu Li, Falk Huettmann, Wen Pei, et al. Habitat selection across nested scales and home range assessments of the juvenile black-necked crane (Grus nigricollis) in the post-breeding period. Global Ecology and Conservation, 2022, 34: e02011. DOI:10.1016/j.gecco.2022.e02011
    11. Yunzhu Liu, Lan Wu, Jia Guo, et al. Habitat selection and food choice of White-naped Cranes (Grus vipio) at stopover sites based on satellite tracking and stable isotope analysis. Avian Research, 2022, 13: 100060. DOI:10.1016/j.avrs.2022.100060
    12. Xue Gou, Xijiao Sun, Romaan Hayat Khattak, et al. An inference of the wading depths of the cranes in wintering wetlands through photographic sampling: a case study of black-necked cranes (Grus nigricollis) in Caohai Wetland, China. Wetlands Ecology and Management, 2022, 30(2): 331. DOI:10.1007/s11273-022-09863-7
    13. Xinting Yan, Jiahao Liao, Xingxing Cao, et al. Temporal and spatial distribution characteristics and source analysis of dissolved organic nitrogen in the surface sediment of the Caohai Lake, southwest China. Environmental Science and Pollution Research, 2022, 30(5): 12844. DOI:10.1007/s11356-022-22953-6
    14. Yun Ruan, Yalong Li, Yuanping Xia, et al. Students’ knowledge of and conservation attitude toward the black-necked crane (Grus nigricollis) in Guizhou, China: insights for conservation. Journal of Ethnobiology and Ethnomedicine, 2022, 18(1) DOI:10.1186/s13002-022-00536-6
    15. Sen Yang, Youzheng Zhang, Wei Wu, et al. Birds and their habitat conditions in reed marshes with different cutting intervals at Chongming Dongtan along China’s coasts. Global Ecology and Conservation, 2021, 26: e01499. DOI:10.1016/j.gecco.2021.e01499
    16. Zhang Ming-Ming, Hu Can-Shi, Sun Xi-Jiao, et al. Seasonal Migration and Daily Movement Patterns of Sympatric Overwintering Black-Necked Cranes (Grus nigricollis) and Common Cranes (Grus grus) in Caohai, Guizhou, China. Waterbirds, 2021, 44(2) DOI:10.1675/063.044.0203

    Other cited types(0)

Catalog

    Figures(1)  /  Tables(3)

    Article Metrics

    Article views (1074) PDF downloads (8) Cited by(16)

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return