Forestry College, Guizhou University, Guizhou 550025, China
2.
Research Center for Biodiversity and Natural Conservation, Guizhou University, Guizhou 550025, China
3.
College of Life Sciences, Guizhou University, Guizhou 550025, China
4.
Key Laboratory of Plant Resources Conservation and Germplasm Innovation in Mountainous Region (Guizhou University), Ministry of Education, Guizhou 550025, China
5.
Guizhou Institute of Biology, Guizhou 550005, China
Funds:
following projects: National Natural Science Foundation of China (NSFC)31860610
following projects: National Natural Science Foundation of China (NSFC)31400353
Provincial Key Science and Technology Project of Guizhou[2016]3022-1
Provincial Science and Technology Plan of Guizhou[2014]7682
Provincial Science and Technology Plan of Guizhou[2019]1068
Science and Technology Plan of Education Administration of Guizhou Province[2018]102
Science and Technology Plan of Education Administration of Guizhou Province[2015]354
Understanding how overwintering birds choose foraging habitats is very important for conservation management. The overwintering Black-necked Crane (Grus nigricollis) feeds on crop remains in farmlands; thus, reasonable conservation management of this type of farmland that surrounds wetlands is critical for the overwintering populations of the Black-necked Crane; however, it is not clear how the Black-necked Crane chooses the foraging land in the farmland.
Methods
A thorough field positioning survey of all foraging sites in farmland areas around the Caohai Wetland and a sampling analysis of habitat selection by the Black-necked Crane were conducted during the winters from 2016-2017 and 2017-2018.
Results
Multiple factors contributed to the selection of foraging habitat in farmlands, i.e., food factors (crop remains and tillage methods) > human disturbance factors (distance to road and settlement) > topography factors (slope aspect), listed according to the strength of influence. Additionally, Black-necked Cranes tend to choose farmland sites where there was no machine tillage, the crop remains were > 500 g/m2, the distance to residences ranged from 100 to 500 m, the distance to roads ranged from 50 to 100 m, and the slopes exhibited western or eastern aspects. As the winters progressed, the volume of the edible crop remains declined, and the influences of the other main factors also changed, i.e., the factors of human disturbance (distance to road and settlement) became less important, while the effect of the food factor (crop remains) was strengthened. Thus, the foraging sites near the road became more important.
Conclusion
The farming area surrounding the Caohai Wetland is very important for the overwintering Black-necked Crane. Food factors and human disturbance factors are the main factors that influence the choice of feeding ground.
Understanding how habitat fragmentation affects the persistence of plant populations is a central component of forest ecology and management (Taubert et al. 2018; Liu et al. 2019; Peters et al. 2019). In the case of fleshy-fruited trees, plant regeneration in remnant forest patches depends on the coupling of seed dispersal and seedling recruitment processes (Cordeiro and Howe 2003; Bregman et al. 2016; Farwig et al. 2017). Empirical evidence suggests that habitat fragmentation could disrupt plant regeneration by altering seed dispersal processes and reducing the availability of suitable microhabitat for regeneration (Bomfim et al. 2018; Emer et al. 2018; Simmons et al. 2018; Marjakangas et al. 2019). Nevertheless, the fundamental question remains of whether recruitment failure in fragmented forests is caused by a greater limitation of seeds available for dispersal or by post-dispersal processes (i.e., seedling establishment and germination) (Donoso et al. 2016; Schupp et al. 2017; García-Cervigón et al. 2018).
For bird-dispersed plants, birds transporting seeds away from the mother plants affect seed deposition in fragmented forests (Schupp et al. 2017; Li et al. 2020) and, hence, patterns of plant regeneration (Donoso et al. 2016; García-Cervigón et al. 2018). Often, birds exhibit complex behavioral pattern in response to forest fragmentation, depending on the distribution of food and other resources (e.g. shelter, nesting, vigilance or resting sites; Cody 1985; Côrtes and Uriarte 2013). For example, the loss of food resources by fragmentation might cause the number of frugivorous bird species to decline, thus reducing the amount of seeds removed and disrupting seed dispersal process (Pérez-Méndez et al. 2015; Farwig et al. 2017; Zwolak 2018). After foraging, birds often exhibit highly specific microhabitat selection. Consequently, a disproportionate number of seeds are deposited at sites selected by bird dispersers, negatively impacting future plant regeneration (Sasal and Morales 2013; Li et al. 2019).
Clearly, seed deposition patterns by birds depend on their behavioral decisions (Schupp 1993; Jordano and Schupp 2000; Cousens et al. 2010). Key behavioral processes include seed removal and post-foraging microhabitat use (Schupp et al. 2017). However, while the regeneration of plant populations in fragmented forest depends on where seeds are deposited by birds (Spiegel and Nathan 2007; Lehouck et al. 2009; Carlo et al. 2013), sites must also be suitable for the early regeneration of plants (Puerta-Piñero et al. 2012; Schupp et al. 2017). Although many studies have highlighted the role of birds in seed removal and seed deposition in fragmented forests (Farwig et al. 2017; Bomfim et al. 2018; Marjakangas et al. 2019), empirical evidence of the consequence of bird microhabitat use on seed germination in fragmented forests is lacking.
In Southeast China, the endangered Chinese Yew, Taxus chinensis (Pilger) Rehd, is a dominant tree species in fragmented forests, and it mainly depends on bird dispersal for regeneration (Li et al. 2019). Over 80% seeds of T. chinensis were removed by the Black Bulbul, Hypsipetes leucocephalus (J. F. Gmelin, 1789) (resident species in Fujian, weight: 41-62 g), indicating that it is the most important species in T. chinensis-bird mutualism (Li et al. 2015). Here, we evaluated whether post-foraging microhabitat selection by H. leucocephalus impacts the early recruitment T. chinensis in a fragmented forest over a 4-year period (2011–2012, 2018–2019). Specifically, we examined: (1) which factors determine bird microhabitat use; and (2) how the microhabitat selection of H. leucocephalus impacts the early recruitment of T. chinensis in a fragmented forest. The results of this study are expected to demonstrate the importance of frugivores in facilitating the regeneration of tree species, with implications on conservation and management practices in remnant fragmented forests.
Methods
Species and study site
T. chinensis is a dioecious and wind-pollinated species that is distributed in evergreen broadleaf forests. Every year, female plants bear axillary cones which, in autumn, develop into fleshy arils (commonly, although incorrectly, referred to as "fruits") that contain a single seed. An average tree bears more than 4000 of these "fruits" (Li et al. 2015, 2019).
This study was conducted in a yew ecological garden (elevation 895–1218 m above sea level [a.s.l.], slope gradient 27°), located in the southern experimental area of the Meihua Mountain National Nature Reserve (25°15′–25°35′N, 116°45′–116°57′E) in the west part of Fujian Province, China. This site contains the largest natural population of T. chinensis in China (approximately 490 adults, distributed in the evergreen broadleaf forest), including 200 trees that are > 500 years old. A national forest garden of 15 ha was established by the government in 2003 to protect these endangered trees. Due to long-term of human use, the vegetation around the forest garden is highly fragmented. The remnant evergreen broadleaf forest patch is interlaced with bamboo patches and mixed bamboo and broadleaf patches to form a fragmented forest. The dominant tree species of the remnant evergreen broad-leaved forest is T. chinensis (Additional file 1: Fig. S1).
Microhabitat selection by Hypsipetes leucocephalus
To study post-foraging microhabitat selection of H. leucocephalus, field observations were made after the birds departed mature T. chinensis plants. We observed the post-foraging perching position of H. leucocephalus using a field scope (Leica 70, Germany) at distances of 50–100 m from the opposite mountain slopes. When the position of birds was recorded, we collected regurgitated seeds in the canopy of bird preferred microhabitats (regurgitated seeds refer to cleaned seeds without any aril/coat that had been totally digested by birds). Because we tried to show the relationship between bird habitat use and plant recruitment, we chose the site with regurgitated seeds as bird-preferred microhabitat and set 1 m×1 m quadrats. To test whether bird selected habitat, we also set the quadrats in other available areas, and the position were confirmed by random number table. Totally, 30 used and 30 available quadrats were set to collect information on microhabitat factors in 2011. To exclude year-to-year variation in bird habitat selection, we recorded perching frequency at these 60 sites in the other study years (2012, 2018-2019).
In both bird-use and available quadrats, we measured three qualitative factors: aspect (shade slope; sunny slope), vegetation type (bamboo forest; Chinese Yew forest; farmland; mixed bamboo and broadleaf forest) and heterogeneous tree species (other tree species, except T. chinensis trees). Moreover, we also measured 15 quantitative factors: elevation, slope, distance to water, distance to light gap, distance to roads, distance to nearest T. chinensis tree, distance to nearest heterogeneous tree, distance to nearest T. chinensis mature tree, distance to fallen dead tree, herb cover, herb density, shrub cover, shrub density, tree cover, and leaf litter cover.
For analyzing microhabitat selection by birds, we first compared three qualitative factors by Chi square test. The other 15 quantitative factors evaluated between bird used, and available quadrats were first analyzed by a t-test. All quantitative variables were evaluated with Principal Component Analysis (PCA) based on their correlation matrix with a varimax rotation to screen out the key factors in microhabitat selection of H. leucocephalus. PCA is a multivariate technique that produces a simplified, reduced expression of the original data with complex relationships, and has been widely applied in studies of wildlife habitats (Fowler et al. 1998). We also used logistic regression to explore the role of microhabitat factors for bird habitat selection.
Effects of microhabitat selection by birds on the early recruitment of Taxus chinensis
Independent of the seed dispersal study, seedling emergence was assessed experimentally in 2017 and 2018 beneath the 30 sites used by H. leucocephalus. At each site, 200 seeds were sown at a depth of 1 cm to avoid predation by rodents. The germinated seedlings were monitored weekly from spring to fall of the following year. Plant early recruitment was computed as the fraction of germinated seedlings that survived to the end of the first fall.
To study the effects of bird microhabitat selection on the early recruitment of plants, we used the t-test to compare the seedling emergence rate in the fragmented forest with natural conditions (seedling emergence rate: 10.86%, with 1000 seeds sowing under the canopy of 10 microhabitats in the natural habitat; Gao 2006). Random Forest model is an ensemble machine-learning method for classification and regression that operates by constructing a multitude of decision trees. It is appropriate for illustrating the nonlinear effect of variables, can handle complex interactions among variables and is not affected by multicollinearity. Random Forest can assess the effects of all explanatory variables simultaneously and automatically ranks the importance of variables in descending order. Then, we used the Random Forest (RF) algorithm to evaluate the quadrat habitat factors selected by birds in relation to the number of germinated seedlings (R package Random Forest) (Breiman 2001).
Results
After foraging, H. leucocephalus exhibited strong microhabitat selection. The Chi square test showed that vegetation type (Chi square test: χ2= 6.300, p = 0.043) and slope aspect (Chi square test: χ2= 9.600, p = 0.002) varied between microhabitats used by birds and those that were available. H. leucocephalus preferred shade slope and bamboo patches. Highly significant differences were detected between microhabitats used by birds and those that were available when considering distance to the nearest T. chinensis tree, distance to the nearest heterogeneous tree, distance to the nearest T. chinensis mature tree, shrub density, and leaf litter cover (Table 1).
Table
1.
Characteristics of H. leucocephalus-preferred microhabitats and other available sites in the yew ecological garden representing a fragmented forest in Southeast China
Importantly, the PCA results highlighted that the main factors affecting H. leucocephalus microhabitat selection were distance to the nearest T. chinensis mature tree, herb cover, herb density, leaf litter cover, and vegetation type. Distance to light gaps and nearest heterogeneous trees were also important for bird microhabitat selection (Table 2). Moreover, the results by logistic regression showed habitat selection of birds was only affected by elevation, distance to light gap and roads, tree cover (Table 3; the other eleven factors did not affect habitat selection, All p > 0.05).
Table
2.
Principal Component Analysis (eigenvalues ≥ 0.60) for microhabitat factors used by Hypsipetes leucocephalus in the yew ecological garden representing a fragmented forest in Southeast China
Table
3.
Results by logistic regression for microhabitat selection by Hypsipetes leucocephalus in the yew ecological garden representing a fragmented forest in Southeast China
As a consequence of bird habitat selection, the sowing experiment first showed a 5%–15.5% seedling emergence rate in the H. leucocephalus microhabitat, which was not significantly different from natural conditions (t = 1.679, p = 0.104). Considering the seed germination related to habitat selection, the Random Forest model showed that seedling emergence rate increased with leaf litter cover and distance to fallen dead trees, but decreased in relation to herb cover, slope, and elevation (Random Forest: 62.43% of germinated seedlings could be explained by five variables) (Fig.1).
Figure
1.
Microhabitat selection by Hypsipetes leucocephalus and how these parameters (distance to fallen dead tree, distance to leaf litter cover, herb cover, slope, and elevation) affect the seedling emergence rate of Taxus chinensis in a yew ecological garden representing a fragmented forest in Southeast China. Results were determined using the Random Forest algorithm, and show the partial effects of the five independent variables on seedling emergence rate
After foraging, H. leucocephalus exhibited strong microhabitat selection. Consequently, H. leucocephalus microhabitats influence the early recruitment of T. chinensis.
Because microhabitat characteristics vary in fragmented forests, they influence the microhabitat selection of birds. An optimum suitable microhabitat provides safe shelter for bird to avoid predation and an opportunity to access reliable food resources (Cody 1985). With forest fragmentation, the remnant microhabitat was important for the ecology and management of the fragmented forest. In our fragmented forest, bamboo patches and shrub density potentially supply safe shelter for H. leucocephalus. Microhabitats close to T. chinensis trees, heterogeneous trees, and T. chinensis mature trees could meet the two requirements of safety and food for H. leucocephalus. The requirement for optimum temperature is also an important component in the strategy of bird habitat selection (Moore 1945). Suitable microhabitat temperature is maintained by shrubs and herbs, providing shelter from wind and rain (Kelty and Lustick 1977; Cody 1985). In the current study, shrub density, distance to light gaps, herb cover, herb density, and leaf litter cover were preferred by H. leucocephalus, possibly because they supply suitable microhabitat temperature.
The remnant microhabitats selected by birds were important for plant recruitment (García-Cervigón et al. 2018). The seed emergence rate of T. chinensis beneath the microhabitats used by birds showed no significant difference to natural conditions; thus, H. leucocephalus is likely important for the early recruitment of T. chinensis. Furthermore, the emergence of T. chinensis seeds was influenced by bird microhabitat factors. Sites with low herb cover facilitated seed emergence, due to the low competitive ability of trees. T. chinensis (Li et al. 2015). Living with dense leaf litter cover could also provide an important supply of nutrients for seed germination. Because of the requirements for T. chinensis seedlings to germinate (Li et al. 2015), shaded slopes might supply a shaded microenvironment for seed germination.
Conclusions
This study demonstrated the microhabitats used by H. leucocephalus affected the early recruitment of T. chinensis. Our results also highlight the importance of remnant microhabitats in fragmented forest for sustaining forest ecology and enhancing management practices. The contribution of habitats used by birds to sites of plant recruitment could be used to determine how frugivore species facilitate plant regeneration. Such information could be incorporated in future conservation and management practices to facilitate the regeneration of fragmented forests. However, our study partially reflected the consequence of bird habitat selection on plant recruitment, owing to sowing the seeds in bird preferred habitat. Researchers need to consider in future studies including the sowing experiment in both bird preferred and available habitat with bird regurgitated seeds and natural fallen seeds. Furthermore, future studies also need to compare how bird habitat selection affect plant recruitment in both fragmented and continuous habitat, which could explore the effects of habitat fragmentation on bird-plant mutualism.
We thank Shuai Zhang for providing assistance in the field. We also thank Prof. Xian-Feng Yi, Prof. Xin-Hai Li and Dr. Si-Chong Chen for constructive suggestions.
Authors' contributions
NL, ZW and LZ conceived and designed this study. NL and ZW performed the study. NL and LZ analyzed the data. ZW and NL wrote the paper. All authors read and approved the final manuscript.
Availability of data and materials
The datasets used in the present study are available from the corresponding author on reasonable request.
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
Beest FMV, Mysteru A, Loe LE, Milner JM. Forage quantity, quality, and depletion as scale-dependent mechanisms driving habitat selection of a large browsing herbivore. J Anim Ecol. 2010;79:910-22
Bishop MA, Li FS. Effects of farming practices in Tibet on wintering black-necked crane (Grus nigricollis) diet and food availability. Biodivers Sci. 2002;10:393-8.
Che Y, Yang L, Li ZQ. Vigilance synchronization of wintering Black-necked crane (Grus nigricollis) families in Tibet. Acta Ecol Sin. 2018;38:1375-81 (in Chinese).
Davis JB, Guillemain M, Kaminski RM, Arzel C, Eadiem JM, Rees EC. Habitat and resource use by waterfowl in the northern hemisphere in autumn and winter. Wildfowl. 2014;4:17-69.
Goss-Custard JD, Stillman RA, West AD, Caldow RWG, McGrorty S. Carrying capacity in overwintering migratory birds. Biol Conserv. 2002;105:27-41.
Jia Y, Jiao S, Zhang Y, Zhou Y, Lei G, Liu G. Diet shift and its impact on the foraging behavior of Siberian crane (Grus leucogeranus) in Poyang Lake. PLoS ONE. 2013;8:e65843.
Jiang Z, Li F, Ran J, Liu W, Zhao C, Zhang B, et al. Nest building duration and its contributing factors for black-necked cranes (Grus nigricollis) at Ruoergai, Sichuan. China. Acta Ecol Sin. 2017;37(3):1027-34 (in Chinese).
Jones J. Habitat selection studies in avian ecology: a critical review. Auk. 2001;118:557-62.
Kaminski RM, Elmberg J. An introduction to habitat use and selection by waterfowl in the northern hemisphere. Wildfowl. 2014;4:9-16.
Kuang FL, Li FS, Liu N, Li F. Effect of flock size and position in flock on vigilance of Black-necked cranes (Grus nigricollis) in winter. Waterbirds. 2014;37:94-8.
Langvatn R, Hanley TA. Feeding-patch choice by red deer in relation to foraging efficiency. Oecologia. 1993;95:164-70.
Li FS. Foraging habitat selection of the wintering Black-necked Cranes in Caohai, Guizhou, China. Chin Biodiversity. 1999;4:257-62 (in Chinese).
Li ZM, Li FS. Black-necked crane research. Shanghai: Shanghai Science and Technology Education Press; 2005 (in Chinese).
Li FS, Nie H, Ye C. Microscopic analysis on herbivorous diets of wintering black-necked cranes at Caoha, China. Zool Res. 1997;18:51-7 (in Chinese).
Li WJ, Zhang KX, Wu ZL, Jiang P. A study on the available food for the wintering Black-necked crane (Grus nigricollis) in Huize nature reserve, Yunnan. J Yunnan Univ. 2009;31:644-8 (in Chinese).
Qian FW, Wu HQ, Gao LB, Zhang HG, Li FS, Zhong XY, et al. Migration routes and stopover sites of Black-necked cranes determined by satellite tracking. J Field Ornithol. 2009;80:19-26.
R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2019; . Accessed 30 Mar 2019.
Ran JC, Meng WP, Su HJ, Zhang MM. The impact of environmental problems on Black-necked crane (Grus nigricollis) and the management strategies at Caohai Wetland, Guizhou, China. J Wildlife. 2017;38:35-9 (in Chinese).
Redpath SM, Gutiérrez RJ, Wood KA, Young JC. Conflicts in conservation: navigating towards solutions. 1st ed. Cambridge: Cambridge University Press; 2015.
Storch I. Habitat selection by capercaillie in summer and autumn: is bilberry important? Oecologia. 1993;95:257-65.
Sun X, Zhang M, Hannah L, Hu CS, Su HJ. Field observations on the behavior of wintering Black-necked cranes (Grus nigricollis) at roosting sites in Caohai, Guizhou. Chin J Zool. 2018;2:180-90 (in Chinese).
Tsamchue D, Yang L, Li JC, Yangjaen D. Current status of conservation and research on Black-necked cranes. Sichuan J Zool. 2008;27:449-53 (in Chinese).
Vanderploeg HA, Scavia D. Calculation and use of selectivity coefficients of feeding: zooplankton grazing. Ecol Model. 1979;7:135-49.
Wei FW, Zhou A, Jin C, Wang W, Yang G. Habitat selection by giant pandas in Mabian Dafengding Reserve. Acta Theriol Sin. 1996;16:241-5 (in Chinese).
Wiens JA. Pattern and process in grassland bird communities. Ecol Monogr. 1973;43:237-70.
Wood KA, Newth JL, Brides K, Harrison AL, Heaven S, et al. Are long-term trends in Bewick's swan Cygnus columbianus bewickii numbers driven by changes in winter food resources? Bird Conserv Int. 2019;29:479-96.
Wu Z, Li R. A preliminary study on the overwintering ecology of Black-necked cranes. Acta Ecol Sin. 1985;5:71-6 (in Chinese).
Yang Y, Wen JB, Hu DF. A review on avian habitat research. Sci Silvae Sin. 2011;47(11):172-80 (in Chinese).
Yang L, Zhuom CJ, Li Z. Group size effects on vigilance of wintering Black-necked cranes (Grus nigricollis) in Tibet China. Waterbirds. 2016;39:108-13.
Zhang HB, Su HJ, Liu W, Li ZM, Zhang MM. Relationship of community structure of main waterfowl with habitat in Caohai National Nature Reserve in winter. J Ecol Rural Environ. 2014;30:601-7.
Zhang L, An B, Shu M, Yang X. Nest-site selection, reproductive ecology and shifts within core-use areas of Black-necked cranes at the northern limit of the Tibetan Plateau. PeerJ. 2017;5:e2939.
Zheng GM. Ornithology. Beijing: Beijing Normal University Press; 2012 (in Chinese).
Xingyi Zhang, Zhenhua Zhong, Maolin Zhang, et al. Analysis of anthropogenic disturbance and spatial and temporal changes of bird communities in plateau wetlands fusing bird survey and nighttime light remote sensing data. Journal of Environmental Management, 2025, 375: 124349.
DOI:10.1016/j.jenvman.2025.124349
2.
Insan Kurnia, Harnios Arief, Ani Mardiastuti, et al. Nilai Willingness To Pay Birdwatching di Indonesia. Jurnal Ilmu Lingkungan, 2024, 22(2): 302.
DOI:10.14710/jil.22.2.302-312
3.
Samuel T. Turvey, Heidi Ma, Tonglei Zhou, et al. Local ecological knowledge and regional sighting histories of Hainan Peacock-pheasant Polyplectron katsumatae: pessimism or optimism for a threatened island endemic?. Bird Conservation International, 2023, 33
DOI:10.1017/S095927092200020X
4.
Xiongwei Huang, Congtian Lin, Liqiang Ji, et al. Species inventories from different data sources “shaping” slightly different avifauna diversity patterns. Frontiers in Ecology and Evolution, 2023, 11
DOI:10.3389/fevo.2023.1121422
5.
Ying Ding, Lichuan Xiong, Fandi Ji, et al. Using citizen science data to improve regional bird species list: A case study in Shaanxi, China. Avian Research, 2022, 13: 100045.
DOI:10.1016/j.avrs.2022.100045
6.
Puyue Gong, Yuanzhi Cai, Zihan Zhou, et al. Investigating spatial impact on indoor personal thermal comfort. Journal of Building Engineering, 2022, 45: 103536.
DOI:10.1016/j.jobe.2021.103536
Table
1.
Characteristics of H. leucocephalus-preferred microhabitats and other available sites in the yew ecological garden representing a fragmented forest in Southeast China
Table
2.
Principal Component Analysis (eigenvalues ≥ 0.60) for microhabitat factors used by Hypsipetes leucocephalus in the yew ecological garden representing a fragmented forest in Southeast China
Table
3.
Results by logistic regression for microhabitat selection by Hypsipetes leucocephalus in the yew ecological garden representing a fragmented forest in Southeast China
DownLoad:
Email Alerts
RSS Feeds