- Open Access
The importance of willow to the Chinese Grouse: evidence from analysis on their breeding territories at Lianhuashan, China
© The Author(s) 2017
- Received: 26 October 2017
- Accepted: 24 November 2017
- Published: 11 December 2017
The habitat features of breeding territory have important adaptive significance for the survival and reproduction of territory holders. The Chinese Grouse (Tetrastes sewerzowi) is a rare and endemic species with relatively small distribution range and decreasing population trend. It is important to elucidate breeding territory habitat requirements of the Chinese Grouse for habitat management and conservation actions.
Using radio-telemetry and field observations, we determined the core areas of 65 breeding territories of males. Two to three samples were selected in each core breeding territory as used sites and compared with nearby sites with no grouse occurrence using logistic regression.
Our model showed a high accuracy in prediction of core breeding territory used by males, which preferred stands with more small deciduous trees (0.5 m ≤ height < 5 m), more small willow trees (Salix spp., 0.5 m ≤ height < 5 m), greater willow cover, and greater herb cover. The number of small willow trees had the greatest influence on males’ core breeding territory selection. Dense shrubs were also chosen compared with unused sites. Tall conifer trees was an important determinant in the distribution of Chinese Grouse at the landscape scale, and was relatively important in the univariate model, but not included in our final multivariable model.
Male Chinese Grouse established territories at sites with abundant food resources. At the landscape scale, the Chinese Grouse occurred in alpine conifer forest. At the territory scale, small willow trees had the most important effect on males’ core breeding territory selection. We suggest that the forest gaps in dense conifer forest are important for improving the occurrence of willows and facilitating breeding territory establishment for the Chinese Grouse.
- Salix spp.
- Chinese Grouse
- Core area
- Conifer forest
- Logistic regression
The distribution of animals depends on interactions between the distributions of required resources and their ability to acquire these resources (Morris 2003; Jones and Siefferman 2014; Akresh et al. 2015). In monogamous bird species, breeding territory habitat selection determines their distributions in the breeding season (Boves et al. 2013; Reiley et al. 2013). Breeding territory habitat features have an important adaptive significance for the survival and fecundity of their owners, as they not only provide food and shelter, but also influence mate acquisition and offspring survival (Holt et al. 2011; Chalfoun and Schmidt 2012; Rahman et al. 2012). Thus, breeding territory habitat selection affects population sustainability and dynamics (Nystrand et al. 2010; Hollander et al. 2011). Elucidating and understanding the breeding habitat features of rare avian species is pivotal for their conservation.
In a heterogeneous breeding territory, the owner makes differential use of the parts of the territory according to its life purposes (e.g. feeding, nesting, Barg et al. 2006). Core areas of a territory are sites that are used most frequently, and are potentially important to their owners (Barg et al. 2006). These areas are thought to be most important for breeding territory selection and draw a great deal of attentions from researchers, because these are where individuals are most frequently found (Liu 1987; Barg et al. 2004). As core areas only occupy a small part in a breeding territory, and acquires most intensive use, they have great conservation value and are important for the habitat management of focal species, especially rare species.
With a decreasing population trend and distribution confined to alpine conifer forests along the east edge of the Qinghai-Tibetan Plateau (elevation range 2400–4300 m), the endemic Chinese Grouse (Tetrastes sewerzowi) is considered as “near threatened” by IUCN (2013 version) and is listed as a category I national protected animal by the Chinese government (Zheng and Wang 1998; Sun 2004). As a monogamous bird (Bergmann et al. 1996; Sun and Fang 1997), male Chinese Grouse hold territories and females choose males to pair with and they nest in the males’ territories (Sun and Fang 1997; Sun et al. 2003). Territory quality is thought to play an important role in the fitness of males (Sun and Fang 2010), and thus might have important effects on its population sustainability and dynamics. However, information regarding the features of male breeding territories is lacking, although this knowledge is valuable for population recovery.
In this study, we compared habitat features of core areas in males’ territories with areas outside of males’ territories. We predicted that willow shrubs would an important factor as willow buds constitute the most important food resource during pairing and egg laying periods (Wang et al. 2010). In addition, predation risk also influences the birds’ habitat selection, we thus expected that core areas of territories would have good concealment, i.e., greater shrub cover. Finally, as the distributions of Chinese Grouse corresponds with alpine conifer forest (Sun 2000), we expected the occurrence and density of conifer trees would also play an important role in territory selection.
The study was conducted at Lianhuashan Nature Reserve (34°40′67″N, 103°30′84″E), Gansu, China, 2009–2012. With an area of 11,691 ha, this reserve was set up in 1983 to protect various natural forest ecosystems. Vegetation types comprised original conifer forests (Abies fargesii, Picea purpurea, P. crassifolia), deciduous forests (Betula platyphylla, B. albosinensis, B. utilis, Populus davidiana), conifer deciduous mixed forests, shrubs (Salix oritrepha, S. caprea, S. cupularis, Hippophae rhamnoides, Rosa hugonis, Berberis kansuensis, Rhododendron anthopogonoides, R. rufum, R. przewalskii, Sorbus koehneana), alpine meadows, farmlands, villages, rocks and rivers (Klaus et al. 1996). Vegetation types change dramatically along altitudes from 2000 to 3500 m. We conducted our research in an area of about 4 km2 in the western part of the reserve, where original conifer forests are distributed and has the highest population density in the reserve. In the remaining conifer forests, trees had been cut selectively and roads were constructed to facilitate timber transport before the reserve was established. In such areas, deciduous trees, such as willows and birches, were interspersed in the conifer forests, which constituted favorite spots for the Chinese Grouse. For detailed description of climate and vegetation, please see Sun et al. (2003).
Male Chinese Grouse core breeding territories were confirmed by two methods, from 48 radio-tracked males and from observations of unmarked males from the last 10 days of April to first 20 days of May. This was before incubation started and when males exhibited most extensive territory behaviors during 2009–2012. Males were caught using ground nets or walk in traps in April, and released after being measured and fitted with necklace radio-transmitters (Holihil; Model RI-2B). Transmitters weighed about 9 g (less than 3% of the bird’s body weight) and had an expected battery life of 12 months. We radio tracked males between 6:30 to 10:00 am and 15:00 to 17:30 pm, 1–2 times per day using a 2-element Yagi antenna (Biotrack Ltd., Dorset, UK). Radio-tracked males’ positions were acquired using the triangulation method (White and Garrott 1990). Territories were described using the Geospatial Modeling Environment (Beyer 2012). We used the 50% fixed kernel method to determine the core areas of a territory. During radio tracking, we spot mapped males without transmitters. We validated an untagged male’ territory when we observed a male at the same site at least 5 times during 20 April to 20 May in each year. We used this method because males were sedentary in their territories and easy to observe with conspicuous territory behaviors in this period. All capture, radio-tagging, and tracking procedures used in the present study had received prior approval and were supervised by the Animal Care and Use Committee of the Institute of Zoology, the Chinese Academy of Sciences (Project No. 2008/73)
Variables that were used to characterize core breeding territory habitat sites (20 m × 20 m) and unused sites of male Chinese Grouse, at Lianhuashan, Gansu, China, 2009–2012
Slope aspect in °
Slope gradient in °
Distance to edge
Length between forest and gaps/clearance in m
Distance to water
Length between forest and creek/water hole
Tall deciduous trees
Number of deciduous trees (≥ 5 m) per ha
Small deciduous trees
Number of deciduous trees and bushes (height: ≥ 0.5 m, < 5 m) per ha
Tall coniferous trees
Number of coniferous trees (≥ 5 m) per ha
Small coniferous trees
Number of coniferous trees (height: ≥ 0.5 m, < 5 m) per ha
Tall willow trees
Number of willow trees (≥ 5 m) per ha
Small willow trees
Number of willow trees (height: ≥ 0.5 m, < 5 m) per ha
Area covered by willow trees ≥ 0.5 m, estimated in 10% steps
Number of rowan trees (≥ 0.5 m) per ha
Area covered by crowns, estimated in 10% steps
Area covered by shrub layer (≥ 0.5 m, < 5 m) in 10% steps
Area covered by grass, estimated in 10% steps
Area covered by herbaceous, estimated in 10% steps
Area covered by fern, estimated in 10% steps
Area covered by moss, estimated in 10% steps
Stand structure in four categories
1 = one layered
2 = two layered
3 = three layered
4 = multi-layered
Stem distribution in four categories
1 = crowed, defined as canopy closure (≥ 0.8)
2 = normal, defied as canopy closure (≥ 0.3, < 0.8)
3 = spare, defined as canopy closure (≥ 0.1, < 0.3)
4 = grouped, defined as canopy closure (≥ 0, < 0.1)
We employed whether the site was a used core breeding territory or an unused area as a response variable and habitat features as predictor variables to build models using logistic regression (Janzen and Stern 1998; Keating and Cherry 2004). We reduced the independent variable set in three steps, because a large variable set risk overfitting the model and consequently lose generality and interpretability (Schäublin and Bollmann 2011; Ludwig and Klaus 2016). In a first step, we assessed bivariate correlation, because multicollinearity could cause problems in logistic regression (Hosmer and Lemeshow 2000). In cases with correlations r ≥ 0.7 (Spearman/Pearson rank correlation), the variable with least explanatory potential was excluded from further analysis (Schäublin and Bollmann 2011). In a second step, we analyzed univariate logistic models for each independent variable and significant variables (p < 0.05) were retained for further analysis. In a third step, we constructed a full model containing all significant independent variables left in the second step, and then reduced them in a stepwise manner using logistic regression based on Akaike’s information criterion (Akaike 1974; Burnham and Anderson 2002). We assessed model fit by calculating AUC, the area under the receiver operating characteristic curve (ROC), which can vary between 0.5 (worst fit) and 1 (best fit) (Hosmer and Lemeshow 2000; Dussault et al. 2005). Parameter estimates with standard errors and odds ratio were also calculated. Finally, we calculated means and standard errors of all variables that contributed significantly to a model of territory occupancy probability.
All statistics were performed on SAS 9.1 (SAS institute, Cary, NC), with all results presented with mean ± standard error.
Results of core territory characteristics of Chinese Grouse using logistic regression, with their regression estimate coefficients β, p values and R 2 values presented
Small deciduous trees
Small willow trees
Tall deciduous trees
Tall willow trees
Tall coniferous trees
Standardized coefficient regression estimation and odds ratio of variables in the most important model of core territory characteristics of Chinese Grouse
95% Wald CI
Small deciduous trees
Small willow trees
For the first time, we quantitatively described core breeding territory characteristics for the Chinese Grouse. Small willow trees, small deciduous trees, willow cover, and herb cover were the most important variables determined core breeding territory selection by the Chinese Grouse, and all four parameters had positive effects. Abundant small willow trees and big willow cover provided males the most important food resources in the pairing and prelaying periods, i.e., willow catkins, leaves, twigs, and buds, which constitute 98% of the wet contents of males’ crops (Wang et al. 2010). In addition, territories with abundant small deciduous trees, and herb cover could supply the potential mates with more nutritious food, such as herb leaves and insects (Wang et al. 2010). Dense shrub layers could also decrease the detectability of predators as the grouse feed.
Previous studies have found that willows are important in determining the habitat selection of Chinese Grouse during spring (Ji et al. 2005), brood rearing (Zhao et al. 2015), and winter seasons (Yang et al. 2011). We found that willows were important in determining males’ core territories during paring and egg-laying periods in this study. A much higher number of small willow trees (2328/ha) was found in core breeding territory than winter habitat (570–1820/ha) (Yang et al. 2011). Males were more sedentary after occupying territories in spring; however, many males moved around in winter when most food resources in their territories were covered by deep snow. In such situations, the Chinese Grouse might lower their willow use and feed on other foods, such as the fruits of Sea Buckthorn (Hippophae rhamnoides) on sunny slopes (Sun et al. 2003). The number of willows in our results was also greater than in spring habitat selection, which was 1583 willows/ha (Ji et al. 2005). We can explain this, based on two aspects. One was that our used sites were at core areas of a male’s territory, where a great deal of time was spent feeding on willows. The sample sites of Ji et al. (2005) were in the entire territories and less willows existed in noncore areas, such as nest sites at the peripheries of territories (Sun et al. 2007). Another explanation was that the areas examined by Ji et al. (2005) might have contained areas outside the territory, because females are not territoriality before pairing and nesting in a male’s territory in spring (personal observation). Thus, we could summarize that the Chinese Grouse was willow dependent, and it relied on willows year round. During the pairing and egg-laying periods, willow selection by territorial males reached a peak, because of shortage of other food resources. Dependence on certain food sources in territory habitat selection has also been found in other Galliform species. Examples include Aspen (Populus spp.) for Ruffed Grouse (Tetrastes umbellus, Bump et al. 1947; Gullion 1977), Sagebrush (Artemisia spp.) for Greater Sage-grouse (Centrocercusu urophasianus, Wallestad and Schladweiler 1974; Leonard et al. 2000), Bilberry (Vaccinium spp.) for Capercaillie (Tetrao urogallus, Wegge et al. 2005), Alder (Alnus spp.) for Hazel Grouse (Tetrastes bonasia, Swenson 1993), and Daphniphyllum macropodum for Cabot’s Tragopan (Tragopan caboti, Young et al. 1991).
At the landscape scale, the distribution of Chinese Grouse coincides with the distribution of alpine conifer forest (Sun 2000, 2004; Sun et al. 2006). At the territory scale, tall coniferous trees were relatively important in univariate models, but were not entered into our final model (see Table 2). This confirmed that habitat selection was scale dependent (Sergio et al. 2003; Mayor et al. 2009). In our study area, territories were all near conifer trees or in conifer forest gaps, where willows were abundant. We found that sites with more tall coniferous trees lacked shrubs and willows, which were important food sources and for concealment of Chinese Grouse. But, we could not rule out the importance of conifer trees in males’ territory selection. Seeds of conifer trees were important food for their paired mates in the prelaying period, accounted for more than 40% of wet crop food content, the same percent as willows (Wang et al. 2010). Conifer trees also provide shelter for Chinese Grouse, such as roosting sites and refuge from predators (Swenson et al. 1995; Bergmann et al. 1996; Klaus et al. 1996), and a large portion of females nested at the bases of conifer trees in males’ territories (Sun et al. 2007). Similar results have also been also found for the Giant Panda (Ailuropoda melanoleuca), which selects bamboo abundant sites at the microhabitat scale. However, older forests are as important as bamboo at the landscape scale (Zhang et al. 2011). In Chinese Grouse, larger conifer trees in core territories might also have contributed to breeding success and thus had a positive effect on the fitness of territory owners. We speculate that males should first guarantee an adequate amount of small willow trees, then as many tall coniferous trees as possible to attract females. Seeds of coniferous trees changed dramatically between years (Koenig and Knops 2000), so males might change the number of tall conifer trees in their core breeding territory annually in relation to conifer seed production.
Herbs had not sprouted when territories were established in late April and early May. They constituted a small part of the food for paired females (Wang et al. 2010). However, it could attract more arthropod animals (Wegge et al. 2005), which could provide important nutrients for females before egg laying (Wang et al. 2010).
In conclusion, the most important features that determined male core breeding territory selection were food acquirements for males, and probably also for paired females. Males established territories at sites with abundant small willow trees. Dense small deciduous shrubs were also preferred, probably for concealment. Greater herb cover could provide additional foods for females. However, subalpine conifer forest was the most important determination of Chinese Grouse habitat selection at the landscape scale. In our study at the scale of territories, conifer trees were less important than willows. However, all willow trees were in gaps of conifer forests in our study area, so males must seek a balance between enough small willow trees and some conifer trees to occupy a territory. In hazel Grouse, natural rejuvenation in gaps after windfalls, insect calamities, or avalanches could enlarge habitat area in mountain forests (Schäublin and Bollmann 2011; Ludwig and Klaus 2016). For the Chinese Grouse, the naturel or anthropogenic enlargement of conifer forest gaps to facilitate growth of small willow trees would promote male Chinese Grouse to colonize, which in turn should promote fecundity and population growth.
JMZ and YHS conceived and designed the idea. YF, YHM and JMZ performed the field work. JMZ and YHS analyzed the data. JMZ and YHS wrote the paper. All authors read and approved the final manuscript.
We are grateful to Yahui Li, Yingqiang Lou, Mei Shi and Yang Hong for assistance in the field. We appreciate the support of the Lianhuashan Nature Reserve Authority. We are grateful to Prof. Jon E. Swenson for his help with English.
The authors declare that they have no competing interests.
Availability of data and materials
The datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request.
Consent for publication
All capture, radio-tag and tracking procedures on Chinese Grouse used in the present study had been given prior approval and were supervised by the Animal Care and Use Committee of the Institute of Zoology, the Chinese Academy of Sciences (Project No. 2008/73).
This research was supported by grants from the National Natural Science Foundation of China (NSFC, 31520103903).
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
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