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The effects of hoarding habitat selection of Eurasian red squirrels (Sciurus vulgaris) on natural regeneration of the Korean pines
Acta Ecologica Sinica 29 (2009) 362–366
Contents lists available at ScienceDirect
Acta Ecologica Sinica journal homepage: www.elsevier.com/locate/chnaes
The effects of hoarding habitat selection of Eurasian red squirrels (Sciurus vulgaris) on natural regeneration of the Korean pines Zong Cheng a, Ma Ying a, Rong Ke a,b, Ma Jian-Zhang a,*, Cheng Zhi-Ben a a b
College of Wildlife Resources, Northeast Forest University, Harbin 150040, China School of Life Science and Chemistry, Hulunbeier College, Hailar 021008, China
a r t i c l e
i n f o
Keywords: Eurasian red squirrels (Sciurus vulgaris) Korean pine (Pinus koraiensis) Hoarding behavior Habitat selection Cone-core
a b s t r a c t Cone-cores discarded by Eurasian red squirrels were used to study the habitat selection of Korean pine-seeds hoarding, in forest patch Nos. 16 and 19 in Liangshui Nature Reserve, China. Ten transects with a total length of 15 km were uniformly set, and data from 343 valid samples were collected in a 369 hm2 area. One hundred and eighty four were hoarding samples which were determined according to the cluster analysis based on the number of the cone-cores, while the other 159 were control samples. The principal component analysis, using 11 habitat factors, suggested that the distance from Korean pine forest, forest type, number of Korean pine seedlings, density and type of bush significantly influenced the habitat selection of hoarding by Eurasian red squirrels. The results of Bailey’s method indicated that the squirrels showed (1) preference for natural coniferous forest, natural fir and spruce forest and planted spruce forest; (2) avoidance of planted Korean pine forest and planted larch forest; and (3) random use of natural Korean pine forest. Moreover the distance from the Korean pines in the range of 150–600 m showed no effect on the habitat selection of hoarding by the Eurasian red squirrels. More than 50% of the cone-cores were discarded in either fringe or gap of the Korean pine forest with more cone-cores found at <300 m than at 300 m away (One-Way ANOVA; df = 3, 183, F = 5.76, p = 0.0009). This demonstrated that the Eurasian red squirrels could take the cone-cores out of the Korean pine forest. The density of bushes in samples of hoarding area was significantly lower than that in control samples (Kruskal–Wallis test; df = 1, v2 = 83.99, p < 0.0001). The number of the Korean pine seedlings in samples of hoarding area was significantly higher than that in the control samples (Kruskal–Wallis test; df = 1, v2 = 104.13, p < 0.0001). This illustrated that the hoarding habitat favoured the germination of the Korean pine seedlings. In conclusion the behavior of hoarding Korean pine seeds by the Eurasian red squirrels can promote the regeneration and dispersal of the Korean pines. Ó 2009 Ecological Society of China. Published by Elsevier B.V. All rights reserved.
1. Introduction Broad-leaved Korean pine forest ecosystem is climax community in Xiaoxing’an Mountains, and it is very significant for the maintenance of ecological safety of Northeast China [1]. The natural regeneration of Korean pine (Pinus koraiensis) is almost absolutely dependent on the hoarding behavior of animals, because of the structural characteristics of Korean pine seeds. Korean pine seeds hoarded by animals as winter food became the potential seed bank for the natural regeneration of Korean pine [2,3]. Eurasian red squirrel (Sciurus vulgaris) is a kind of scatter hoarding animals which store a large number of Korean pine seeds as over-wintering food [4]. However, there is still controversy on the role of squirrel in natural regeneration process of Korean pine. * Corresponding author. E-mail address: [email protected] (J.-Z. Ma).
Hutchins and Lu considered that the hoarding behavior of squirrels will not promote the diffusion of Korean pine [3,5], and Ma considered that squirrels can disperse and spread Korean pine seeds simultaneously [6]. To determine whether squirrels can promote the diffusion of Korean pine, it is necessary to solve two problems: (1) whether squirrels disperse seeds out of Korean pine forest and (2) whether the hoarding habitat is suitable for the establishment of Korean pine seedlings. The results from Ma [6] showed that hoarding habitats preferred by squirrels was suitable for growth of Korean pine seedlings which answered part of these questions based on the micro-habitat characteristics. In this paper, we used the cone-cores discarded by squirrels and the seedlings of Korean pine as index to analyse the character of hoarding habitat of squirrels and to determine the role of squirrels on the regeneration and diffusion of Korean pines.
1872-2032/$ - see front matter Ó 2009 Ecological Society of China. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.chnaes.2009.09.018
C. Zong et al. / Acta Ecologica Sinica 29 (2009) 362–366
2. Study area The field work was done in Liangshui National Nature Reserve (128°480 800 –128°550 4600 E, 47°70 1500 – 47°140 3800 N) in Xing0 an Mountains of Heilongjiang Province of northeastern China. The average elevation of the study site is 400 m with 10-15° slope. Natural vegetation is deciduous broad-leaved forest dominated by Korean pine (Pinus koariensis). The original Korean pine forest is approximately 2375 hm2. Study sites were located in two forest patches: Nos. 16 and 19, total area of 369 hm2 in Liangshui Nature Reserve. All forest types of Liangshui Nature Reserve are distributed in these two patches and the impacts of pine seed collection activities by people were comparatively less.
3. Study methods Based on the observation results of hoarding behavior of squirrel since 2003, the cone-cores discarded by squirrels were significantly different from the cones discarded by other animals. We use discarded cone-cores as the index to indicate hoarding sites and reflect hoarding amount of squirrels [6]. From 15th October to 10th November 2008, 10 transects along east–west direction were set in forest patch Nos. 16 and 19 to cover all kinds of forest types of Nature Reserve, with 1.5 km length and 150 m interval distance. Circular samples with 10 m radius and 50 m interval distance were established on each transect, and one sample was added when the forest type changed; the total number of samples is 344. The cone-cores discarded by squirrels in all samples were counted, and forest type, number of conifers, bush type, bush density, ground cover type, canopy, slope aspect, slope position, number of Korean pine seedlings, ubiety relative to Korean pine forest, distance from Korean pine forest were measured. The detailed methods are the following: The forest type includes nine natural Korean pine forests, natural coniferous forest, natural broad-leaved forest, natural mixed coniferous and broad-leaved forest, natural birch forest, natural fir and spruce forest, planted Korean pine forest, planted larch forest, planted spruce forest. Number of conifers means the number of Korean pine, spruce and fir and other coniferous trees. Bush type was named by dominated shrub in samples and includes five types: no shrub, Acanthopanax senticosus shrub, Evonymus sacrosancta shrub, Lonicera sp. shrub, Actinidia kolomikta shrub. To determine shrub density, five small circular samples (1 m radius) on centre, and east, west, south, north direction of big samples (10 m radius) were established, and the number of shrub branches in these five small samples was counted, and the average value of shrub branch numbers in five small samples was regarded as shrub density [7]. Ground covers include three types: conifer fall-leaves, broadleaved fall-leaves and fogs. Canopy of sample was determined by visual methods. Slope aspect was measured by geological compass, and was divided into three types: shade slope (N67.5°W–N22.5°E), sunny slope (S67.5°E–S22.5°W) and semi-sunny slope (N22.5°E–S67.5°E and S22.5°W–N67.5°W). Slope position was divided into five types: ridge, top slope, mid slope, below slope and valley. The number of Korean pine seedlings was calculated as the number of seedlings and young trees within 30a. The ubiety relative to Korean pine forest was divided into three types: inside Korean pine forest, outside Korean pine forest and in gaps of Korean pine forest.
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GPS (GARMIN eTrex Venture) was applied for measuring and recording the position of sample and Korean pine trees with seeds, and ArcGIS software was used to determine the shortest distance from sample to Korean pine forest, and the distances were divided into four levels: 0–150, 150–300, 300–450, and 450–600 m. 3.1. Data analysis JMP 7.02 (SAS Institute Inc., 2007) software was applied for data analysis. All the quantitative data were described as mean ± standard error, and the significant level was 0.05. 3.2. Standard of data eliminating Mahalanobis Distance methods were applied for eliminating the sample in which the number of cone-cores is beyond control limit, and 343 effective samples were obtained after one sample was eliminated. 3.3. Standard of determining hoarding sample and control sample According to our observation and research results of Stapanian and Smith [8]: (1) squirrels usually scatter hoarded food in a relatively concentrated region [9]; (2) squirrels sometimes will discard some cone-cores in hoarding course when disturbed by a person or other animals, it is believed that the sample with a low number of cone-cores is not a hoarding sample. Therefore, we used an average method to carry out cluster analysis of cone-core numbers in samples, and samples with more cone-cores were regarded as hoarding samples, the others were regarded as control samples. 3.4. Influencing factors of hoarding habitat selection of squirrels Data of 11 habitat factors was dealt with a conversion to nondimensional value by average value methods. Covariance matrix was calculated for principal component analysis to determine the main factors that influence the hoarding selection of squirrels [10]. 3.5. Main hoarding habitat factors selection of squirrels Shapiro–Wilk W method was applied to inspect whether the number of cone-cores, shrub density and the number of seedlings in samples are consonant with normal distribution or not. According to the results of principal component analysis, Bailey’s method was applied to determine if the factors, such as distance to Korean pine forest, forest type and conifers, can influence the hoarding behavior of squirrels in natural broadleaved forests [11,12]. One-Way ANOVA was applied to compare the effects of distance to Korean pine forest on hoarding amount of squirrels. Kruskal– Wallis test method was applied to analyze the effect of seedling number and shrub density on hoarding habitat of squirrels. 4. Results 4.1. Determining hoarding samples and control samples The cluster analysis result of cone-core numbers in samples indicated that the samples with P17 cone-cores were clustered into one category, and other samples were clustered into another category. It was determined that samples with P17 cone-cores were hoarding samples, the total number was 184; other samples were control samples, the total number was 159.
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Table 1 Results of the principal component (PC) analysis of habitat factors effected the hording habitat selection of Sciurus vulgaris.
Forest type Number of the conifers Bush type Bush density Floor cover type Canopy Slope aspect Slope position Number of the Korean pine seedlings Ubiety relative to the Korean pine forest Distance from the Korean pines Eigenvalue Total variance (%) Accumulated variance (%)
PC I 0.1535 0.0259 0.0615 0.0527 0.0196 0.0060 0.0664 0.0473 0.0602 0.0109 0.9790 5.8756 72.476 72.476
PC II
Out of the Korean pine forest Gap in the Korean forest
PC III
0.7186 0.1040 0.1768 0.1576 0.0940 0.0361 0.0776 0.1218 0.5770 0.1397 0.1822 0.6530 8.054 80.530
35
0.0913 0.0171 0.5217 0.8214 0.0538 0.0150 0.1172 0.1647 0.0184 0.0004 0.0136 0.4894 6.036 86.567
30
Number of cone-cores in a sample
Habitat factors and statistical parameters
In Korean pine forest
4.2. Main factors influencing hoarding habitat selection of squirrels Three principal components were obtained from the principal component analysis for habitat factors of hoarding samples, and the cumulative contribution rate was 86.57 (Table 1). We defined the first principal component as the seed resources factor, its factor loading capacity was >0.5; the second principal component as the forest type factor, the main influencing variables were forest type and number of Korean pine seedlings; and the third principal component as the impact factor, the main influencing variables were shrub type and density. The results of the principal component analysis showed that environment factors influencing hoarding habitat selection of squirrels were distance to Korean forest, forest type, number of Korean pine seedlings, shrub density and shrub types. 4.3. Effect of distance to Korean pine forest on hoarding habitat selection of squirrels Analysis of hoarding sample numbers with varied distances from Korean pines showed that the longer distance to Korean pine forest had no effect on hoarding habitat selection of squirrels, though squirrels preferred to hoard Korean pine seeds in gaps of Korean pine forest (Table 2). The number of cone-cores in hoarding samples with varied distances from Korean pines showed that the number of cone-cores discarded by squirrels in the hoarding samples with a distance of 150–300 m from Korean pine trees was significantly more than those in other hoarding samples. A large number of cones were carried by squirrels from Korean pine forest to forest gap and forest edge, and thus were dispersed far from Korean pine forest (OneWay ANOVA; df = 3, 183, F = 5.76, p = 0.0009, Fig. 1). 4.4. Hoarding selection of squirrels on different forest types The presence of conifers in samples influenced hoarding habitat selection of squirrels. Squirrels preferred to hoard seeds inside nat-
25 20 15 10 5 0 0-150
150-300
300-450
>450
Distance from the Korean pines (m) Fig. 1. Impact of distance from the Korean pines on the number of hoarding cones by Sciurus vulgaris (means with SE bars).
ural coniferous forest, natural fir and spruce forest and planted spruce forest, and avoided hoarding seeds inside natural broadleaved forest, natural birch forest, planted Korean pine forest and planted larch forest (Table 3). If the broad-leaved forest was taken as analysis object for hoarding habitat selection of squirrels, squirrels preferred to hoard seeds inside the broad-leaved forest with conifers (Table 4).
4.5. Effect of Korean pine seedling on hoarding habitat selection of squirrels The number of Korean pine seedlings in the hoarding samples was significantly more than those in the control samples in all types of forests (Kruskal–Wallis test; df = 1, v2 = 104.13, p < 0.0001; Fig. 2).
4.6. Effect of shrub on hoarding habitat selection of squirrels The shrub density in the hoarding samples was significantly lower than that in the control samples in all types of forests (Kruskal–Wallis test; df = 1, v2 = 83.99, p < 0.0001; Fig. 3), which showed that squirrels avoided hoarding seeds in high density shrub habitats.
Table 2 Impact of distance from the Korean pines on the hoarding habitat selection of Sciurus vulgaris. Ubiety relative to the Korean pine forest
Distance from the Korean pines (m)
Pw Expected proportion used (n = 159)
Pi Actual proportion used (n = 184)
Bailey’s 95% confidence interval for Pi
Preference
In the Korean pine forest Gap in the Korean forest Out of the Korean pine forest Out of the Korean pine forest Out of the Korean pine forest Out of the Korean pine forest
0–150 0–150 0–150 150–300 300–450 450–600
0.277 0.314 0.151 0.145 0.082 0.031
0.250 0.413 0.152 0.120 0.043 0.022
0.168 6 Pi 6 0.341 0.315 6 Pi 6 0.51 0.088 6 Pi 6 0.232 0.063 6 Pi 6 0.193 0.012 6 Pi 6 0.097 0.002 6 Pi 6 0.066
o + o o o o
+: Observed use is significantly higher than expected (preference). : Observed use is significantly lower than expected (avoidance). o: Observed use in proportion to its availability (random use).
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C. Zong et al. / Acta Ecologica Sinica 29 (2009) 362–366 Table 3 Selection of various forest type of hoarding habitat selection of Sciurus vulgaris. Forest type
Pw Expected proportion used (n = 159)
Pi Actual proportion used (n = 184)
Bailey’s 95% confidence interval for Pi
Preference
Natural Korean pine forest Natural coniferous forest Natural broad-leaved forest Natural mixed coniferous and broadleaved forest Natural birch forest Natural fir and spruce forest Planted Korean pine forest Planted larch forest Planted spruce forest
0.277 0.094 0.283 0.031
0.250 0.429 0.130 0.033
0.165 6 Pi 6 0.345 0.326 6 Pi 6 0.531 0.068 6 Pi 6 0.210 0.006 6 Pi 6 0.085
o + o
0.151 0.006 0.025 0.126 0.006
0.033 0.060 0 0.011 0.054
0.006 6 Pi 6 0.085 0.020 6 Pi 6 0.122 – 0 6 Pi 6 0.05 0.017 6 Pi 6 0.115
+ +
+: Observed use is significantly higher than expected (preference). : Observed use is significantly lower than expected (avoidance). o: Observed use in proportion to its availability (random use).
Table 4 Impact of the conifers on the hoarding habitat selection of Sciurus vulgaris. Forest type
Contain the conifers?
Pw Expected proportion used (n = 69)
Pi Actual proportion used (n = 30)
Bailey’s 95% confidence interval for Pi
Preference
Natural broad-leaved forest Natural broad-leaved forest Natural birch forest Natural birch forest
True
0.449
0.767
0.506 6 Pi 6 0.915
+
False
0.203
0.033
0 6 Pi 6 0.205
o
True False
0.072 0.275
0.200 0
0.048 6 Pi 6 0.424 –
o
+: Observed use is significantly higher than expected (preference). : Observed use is significantly lower than expected (avoidance). o: Observed use in proportion to its availability (random use).
5. Discussion 5.1. Characteristics of hoarding habitat selection of squirrels Squirrels preferred to hoard Korean pine seeds in broad-leaved habitat with conifers, there are three reasons possibly (Tables 3
and 4): Firstly, this will improve the efficiency of hoarding to reduce the energy consumption when recovering in winter. The research of Stapanian and Smith indicated that fox squirrels (Sciurus niger) transported foods along the direction of nest trees, which can enhance their ability to control foods [8]. The nests of red squirrels are all on the conifers, especially on fir trees [13].
Sample of hoarding area
Sample of hoarding area Control sample 70
Bush density in a sample (number /m2)
Number of the Korean pine seedlings in a sample
Control sample 40
30
20
10
0 NK
NC
NL
NM
NB
NF
PK
PL
PS
Forest type *
60 50 40 30 20 10 0 NK
NC
NL
NM
NB
NF
PK
PL
PS
Forest type * Fig. 2. Impact of the Korean pine seedling number on the hoarding habitat selection by Sciurus vulgaris (means with SE bars). *NK, natural Korean pine forest; NC, natural coniferous forest; NL, natural broad-leaved forest; NM, natural mixed coniferous and broad-leaved forest; NB, natural birch forest; NF, natural fir and spruce forest; PK, planted Korean pine forest; PL, planet larch forest; PS, planted spruce forest.
Fig. 3. Impact of bush density on the hoarding habitat selection by Sciurus vulgaris (means with SE bars). *NK, natural Korean pine forest; NC, natural coniferous forest; NL, natural broad-leaved forest; NM, natural mixed coniferous and broad-leaved forest; NB, natural birch forest; NF, natural fir and spruce forest; PK, planted Korean pine forest; PL, planet larch forest; PS, planted spruce forest.
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C. Zong et al. / Acta Ecologica Sinica 29 (2009) 362–366
Secondly, this will reduce the risk of being preyed when squirrels hoard and retrieve seeds. As strictly arboreal animals [14], hoarding and retrieving seeds on the ground will increase the threat of squirrels to be preyed. In this investigation, we observed that squirrels were preyed by raptors such as goshawk (Accipiter gentilis) and common buzzard (Buteo buteo) several times. Conifers with intensive branches will help squirrels to avoid natural enemies. Squirrels always jump to the nearest conifer when they are disturbed by other animals in the process of hoarding and retrieving. Thirdly, the ground cover under conifer forest was composed of a mixture of fog and defoliation of broad-leaved trees, which will benefit to conceal pine seeds when hoarding and reduce the difficulty in retrieving in winter [15]. Squirrels hoard Korean pine seeds by peeling off scales of cones, carrying it in their mouth and running on the ground. Because the gross withered in hoarding season, the shrub becomes the obstructing factor influencing squirrels’ activities on ground, and shrub density will directly influence the hoarding and retrieving of squirrels. Accordingly, squirrels prefer to hoard seeds in shrub habitat with lower density. Field observation showed that squirrels always put Korean pine cone-cores on the base of one tree (mainly conifers), and fetch some seeds from the cone and hoard them under the fall-leaves litter of ground, and then return and fetch other seeds and jump to another direction near the tree. After making several caches in one site, squirrels transport the cone to the base of other trees, and repeat the above-mentioned procedure, so the seeds of one cone hoarded near different trees. When recovering seeds in winter, squirrels directly jump to the caches and retrieve seeds after they get down to the ground from the tree [9], so it can be presumed that the trees, especially conifers, maintain the spatial memory of squirrels to caches. In this study, in 184 hoarding samples, 15.2% of hoarding samples were situated outside Korean pine forest and within 150 m distance to trees, 41.3% hoarding samples were situated in gaps of Korean pine forest, these two were more than half of all hoarding samples and higher than the hoarding samples situated in Korean pine forest (25.0%) (Fig. 1). This result supported the Rapidsequestering hypothesis [16]. Some kinds of animals in Korean pine forest, such as chipmunk (Eutamias sibiricus), Korean field mouse (Apodemus speciosus), and wild pig (Sus scrofa), also forge, hoard and steal Korean pine seeds. Squirrels will avoid the intense competition for food and obtain most benefit by hoarding seeds outside Korean pine forest and in forest gaps where the density of other hoarding species is relatively lower [17]. 5.2. Can squirrels hoard seeds outside Korean pine forest? This study indicated that above 150 m distance to Korean pine trees did not impact hoarding habitat selection of squirrels (Table 2), and most caches were situated at an area with 150–300 m distance to Korean pine forest (Fig. 1). This showed that squirrels were able to transport and hoard massive seeds outside Korean pine forest. The results of cone placement test also supported this conclusion [18]. In hoarding season, squirrels were very vigilant, and it is difficult to directly observe the direction and distance of hoarding behavior, so it is suspected that the conclusion of Hutchins is educed by direct observation [3]. 5.3. Whether hoarding habitat of squirrels is a benefit for the establishment of Korean pine seedlings Korean pine seedlings not only reflect total results of hoarding habitat selection of hoarding animals, but also reveal hoarding
behavior of squirrels. The status of regeneration of seedlings within the hoarding samples was better than that within the control samples, which showed that the hoarding habitat is a benefit for the establishment of Korean pine seedlings in the temporal scale of 30a (Fig. 2). The Korean pine seedlings have a characteristic of liking shade, and the gap and edge of forest will be the most suitable site for regeneration [19]. Squirrels prefer to hoard massive seeds in these two kinds of habitats which show that the hoarding behavior of squirrels can promote regeneration (in gaps) and dispersal (in edge) of Korean pine (Fig. 1). Removing under-forest shrub aptly, artificially planting fastgrowing conifers to provide nest habitat for squirrels, and controlling the activity of artificial picking cone to a suitable extent will be a benefit for hoarding behavior of hoarding animals, and these promote the regeneration and dispersal of Korean pines. References [1] L. Wang, Chun Meng, Landscape diversity and stability of Korean pine broadleaved forest in Xiaoxing anling forest region, Chinese Journal of Applied Ecology 16 (12) (2005) 2267–2270. [2] D. Tao, D. Zhao, S. Zhao, et al., Dependence of natural regeneration or Korean pine on animals – an outclosure experiment, Chinese Biodiversity 3 (3) (1995) 131–133. [3] H.E. Hutchins, S.A. Hutchins, B. Liu, The role of birds and mammals in Korean pine (Pinus koraiensis) regeneration dynamics, Oecologia 107 (1) (1996) 120– 130. [4] H.-J. Su, J.-Z. MA, H.-F. Zou, et al., A field study on retrieved-caches of squirrel (Sciurus vulgaris) and their survival strategy in winter in Liangshui National Nature Reserve, Northeastern China, Acta Theriologica Sinica 26 (3) (2006) 262–266. [5] C.-H. Lu, B.-W. Liu, J.-P. Wu, Foraging and dispersing of Korean pine seed by animals in broad-leaved Korean pine forest, Journal of Northeast Forestry University 29 (5) (2001) 96–98. [6] J.-Z. MA, C. Zong, Q.-M. Wu, et al., Hoarding habitat selection of squirrels (Sciurus vulgaris) in Liangshui Nature Reserve, Acta Ecologica Sinica 26 (11) (2006) 3542–3548. [7] Q. Lu, J. Yu, X. Gao, et al., Winter habitat selection of Reeves’s muntjac and wild boars in the Qingliangfeng Mountains, Acta Theriologica Sinica 27 (1) (2007) 45–52. [8] M.A. Stapanian, C.C. Smith, A model for seed scatterhoarding: coevolution of fox squirrels and black walnuts, Ecology 59 (5) (1978) 884–896. [9] K. Rong, C. Zong, J.-Z. Ma, Behaviour tactics in overwintering Eurasian red squirrel in Liangshui Nature Reserve, China, Acta Theriologica Sinica 29 (2) (2009) 142–151. [10] R.f. Ji, Improvement of data processing method in principal component analysis, Journal of Shandong University of Science and Technology (Natural Science) 26 (5) (2007) 95–98. [11] D.L. Thomas, E.J. Taylor, Study designs and tests for comparing resource use and availability II, Journal of Wildlife Management 70 (2) (2006) 324– 336. [12] S. Cherry, A comparison of confidence interval methods for habitat useavailability studies, Journal of Wildlife Management 60 (3) (1996) 653– 658. [13] K. Rong, J.-Z. Ma, C. Zong, Nest-site selection by the Eurasian red squirrels in Liangshui Nature Reserve, Acta Theriologica Sinica 29 (1) (2009) 112– 119. [14] P.W.W. Lurz, G. John, M. Louise, Sciurus vulgaris, Mammalian Species (769) (2005) 1–10. [15] C. Zong, T. Chen, J.-Z. Ma, et al., Differences on hoarding habitat selection of squirrels (Sciurus vulgaris) and Eurasian nutcrackers (Nucifraga caryocatactes) in Liangshui Nature Reserve, Acta Theriologica Sinica 27 (2) (2007) 105– 111. [16] E.B. Hart, Food preferences of the cliff chipmunk, Eutamias dorsalis, in northern Utah, Great Basin Naturalist 31 (1971) 182–188. [17] A.L. Lisa, D. Martin, Food caching and differential cache pilferage: a field study of coexistence of sympatric kangaroo rats and pocket mice, Oecologia 128 (4) (2001) 577–584. [18] J.-Z. Ma, K. Rong, Q.-M. Wu, et al., Seed hoarding distance of Pinus koreansis by Sciurus vulgaris in Liangshui Nature Reserve, Chinese Journal of Zoology 43 (3) (2008) 45–49. [19] R. Zang, Z. Guo, W. Gao, Gap regeneration in a broadleaved Korean pine forest in Changbai Mountain Natural Reserve, Chinese Journal of Applied Ecology 9 (4) (1998) 349–353.
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The effects of hoarding habitat selection of Eurasian red squirrels (Sciurus vulgaris) on natural regeneration of the Korean pines Zong Cheng a, Ma Ying a, Rong Ke a,b, Ma Jian-Zhang a,*, Cheng Zhi-Ben a a b
College of Wildlife Resources, Northeast Forest University, Harbin 150040, China School of Life Science and Chemistry, Hulunbeier College, Hailar 021008, China
a r t i c l e
i n f o
Keywords: Eurasian red squirrels (Sciurus vulgaris) Korean pine (Pinus koraiensis) Hoarding behavior Habitat selection Cone-core
a b s t r a c t Cone-cores discarded by Eurasian red squirrels were used to study the habitat selection of Korean pine-seeds hoarding, in forest patch Nos. 16 and 19 in Liangshui Nature Reserve, China. Ten transects with a total length of 15 km were uniformly set, and data from 343 valid samples were collected in a 369 hm2 area. One hundred and eighty four were hoarding samples which were determined according to the cluster analysis based on the number of the cone-cores, while the other 159 were control samples. The principal component analysis, using 11 habitat factors, suggested that the distance from Korean pine forest, forest type, number of Korean pine seedlings, density and type of bush significantly influenced the habitat selection of hoarding by Eurasian red squirrels. The results of Bailey’s method indicated that the squirrels showed (1) preference for natural coniferous forest, natural fir and spruce forest and planted spruce forest; (2) avoidance of planted Korean pine forest and planted larch forest; and (3) random use of natural Korean pine forest. Moreover the distance from the Korean pines in the range of 150–600 m showed no effect on the habitat selection of hoarding by the Eurasian red squirrels. More than 50% of the cone-cores were discarded in either fringe or gap of the Korean pine forest with more cone-cores found at <300 m than at 300 m away (One-Way ANOVA; df = 3, 183, F = 5.76, p = 0.0009). This demonstrated that the Eurasian red squirrels could take the cone-cores out of the Korean pine forest. The density of bushes in samples of hoarding area was significantly lower than that in control samples (Kruskal–Wallis test; df = 1, v2 = 83.99, p < 0.0001). The number of the Korean pine seedlings in samples of hoarding area was significantly higher than that in the control samples (Kruskal–Wallis test; df = 1, v2 = 104.13, p < 0.0001). This illustrated that the hoarding habitat favoured the germination of the Korean pine seedlings. In conclusion the behavior of hoarding Korean pine seeds by the Eurasian red squirrels can promote the regeneration and dispersal of the Korean pines. Ó 2009 Ecological Society of China. Published by Elsevier B.V. All rights reserved.
1. Introduction Broad-leaved Korean pine forest ecosystem is climax community in Xiaoxing’an Mountains, and it is very significant for the maintenance of ecological safety of Northeast China [1]. The natural regeneration of Korean pine (Pinus koraiensis) is almost absolutely dependent on the hoarding behavior of animals, because of the structural characteristics of Korean pine seeds. Korean pine seeds hoarded by animals as winter food became the potential seed bank for the natural regeneration of Korean pine [2,3]. Eurasian red squirrel (Sciurus vulgaris) is a kind of scatter hoarding animals which store a large number of Korean pine seeds as over-wintering food [4]. However, there is still controversy on the role of squirrel in natural regeneration process of Korean pine. * Corresponding author. E-mail address: [email protected] (J.-Z. Ma).
Hutchins and Lu considered that the hoarding behavior of squirrels will not promote the diffusion of Korean pine [3,5], and Ma considered that squirrels can disperse and spread Korean pine seeds simultaneously [6]. To determine whether squirrels can promote the diffusion of Korean pine, it is necessary to solve two problems: (1) whether squirrels disperse seeds out of Korean pine forest and (2) whether the hoarding habitat is suitable for the establishment of Korean pine seedlings. The results from Ma [6] showed that hoarding habitats preferred by squirrels was suitable for growth of Korean pine seedlings which answered part of these questions based on the micro-habitat characteristics. In this paper, we used the cone-cores discarded by squirrels and the seedlings of Korean pine as index to analyse the character of hoarding habitat of squirrels and to determine the role of squirrels on the regeneration and diffusion of Korean pines.
1872-2032/$ - see front matter Ó 2009 Ecological Society of China. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.chnaes.2009.09.018
C. Zong et al. / Acta Ecologica Sinica 29 (2009) 362–366
2. Study area The field work was done in Liangshui National Nature Reserve (128°480 800 –128°550 4600 E, 47°70 1500 – 47°140 3800 N) in Xing0 an Mountains of Heilongjiang Province of northeastern China. The average elevation of the study site is 400 m with 10-15° slope. Natural vegetation is deciduous broad-leaved forest dominated by Korean pine (Pinus koariensis). The original Korean pine forest is approximately 2375 hm2. Study sites were located in two forest patches: Nos. 16 and 19, total area of 369 hm2 in Liangshui Nature Reserve. All forest types of Liangshui Nature Reserve are distributed in these two patches and the impacts of pine seed collection activities by people were comparatively less.
3. Study methods Based on the observation results of hoarding behavior of squirrel since 2003, the cone-cores discarded by squirrels were significantly different from the cones discarded by other animals. We use discarded cone-cores as the index to indicate hoarding sites and reflect hoarding amount of squirrels [6]. From 15th October to 10th November 2008, 10 transects along east–west direction were set in forest patch Nos. 16 and 19 to cover all kinds of forest types of Nature Reserve, with 1.5 km length and 150 m interval distance. Circular samples with 10 m radius and 50 m interval distance were established on each transect, and one sample was added when the forest type changed; the total number of samples is 344. The cone-cores discarded by squirrels in all samples were counted, and forest type, number of conifers, bush type, bush density, ground cover type, canopy, slope aspect, slope position, number of Korean pine seedlings, ubiety relative to Korean pine forest, distance from Korean pine forest were measured. The detailed methods are the following: The forest type includes nine natural Korean pine forests, natural coniferous forest, natural broad-leaved forest, natural mixed coniferous and broad-leaved forest, natural birch forest, natural fir and spruce forest, planted Korean pine forest, planted larch forest, planted spruce forest. Number of conifers means the number of Korean pine, spruce and fir and other coniferous trees. Bush type was named by dominated shrub in samples and includes five types: no shrub, Acanthopanax senticosus shrub, Evonymus sacrosancta shrub, Lonicera sp. shrub, Actinidia kolomikta shrub. To determine shrub density, five small circular samples (1 m radius) on centre, and east, west, south, north direction of big samples (10 m radius) were established, and the number of shrub branches in these five small samples was counted, and the average value of shrub branch numbers in five small samples was regarded as shrub density [7]. Ground covers include three types: conifer fall-leaves, broadleaved fall-leaves and fogs. Canopy of sample was determined by visual methods. Slope aspect was measured by geological compass, and was divided into three types: shade slope (N67.5°W–N22.5°E), sunny slope (S67.5°E–S22.5°W) and semi-sunny slope (N22.5°E–S67.5°E and S22.5°W–N67.5°W). Slope position was divided into five types: ridge, top slope, mid slope, below slope and valley. The number of Korean pine seedlings was calculated as the number of seedlings and young trees within 30a. The ubiety relative to Korean pine forest was divided into three types: inside Korean pine forest, outside Korean pine forest and in gaps of Korean pine forest.
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GPS (GARMIN eTrex Venture) was applied for measuring and recording the position of sample and Korean pine trees with seeds, and ArcGIS software was used to determine the shortest distance from sample to Korean pine forest, and the distances were divided into four levels: 0–150, 150–300, 300–450, and 450–600 m. 3.1. Data analysis JMP 7.02 (SAS Institute Inc., 2007) software was applied for data analysis. All the quantitative data were described as mean ± standard error, and the significant level was 0.05. 3.2. Standard of data eliminating Mahalanobis Distance methods were applied for eliminating the sample in which the number of cone-cores is beyond control limit, and 343 effective samples were obtained after one sample was eliminated. 3.3. Standard of determining hoarding sample and control sample According to our observation and research results of Stapanian and Smith [8]: (1) squirrels usually scatter hoarded food in a relatively concentrated region [9]; (2) squirrels sometimes will discard some cone-cores in hoarding course when disturbed by a person or other animals, it is believed that the sample with a low number of cone-cores is not a hoarding sample. Therefore, we used an average method to carry out cluster analysis of cone-core numbers in samples, and samples with more cone-cores were regarded as hoarding samples, the others were regarded as control samples. 3.4. Influencing factors of hoarding habitat selection of squirrels Data of 11 habitat factors was dealt with a conversion to nondimensional value by average value methods. Covariance matrix was calculated for principal component analysis to determine the main factors that influence the hoarding selection of squirrels [10]. 3.5. Main hoarding habitat factors selection of squirrels Shapiro–Wilk W method was applied to inspect whether the number of cone-cores, shrub density and the number of seedlings in samples are consonant with normal distribution or not. According to the results of principal component analysis, Bailey’s method was applied to determine if the factors, such as distance to Korean pine forest, forest type and conifers, can influence the hoarding behavior of squirrels in natural broadleaved forests [11,12]. One-Way ANOVA was applied to compare the effects of distance to Korean pine forest on hoarding amount of squirrels. Kruskal– Wallis test method was applied to analyze the effect of seedling number and shrub density on hoarding habitat of squirrels. 4. Results 4.1. Determining hoarding samples and control samples The cluster analysis result of cone-core numbers in samples indicated that the samples with P17 cone-cores were clustered into one category, and other samples were clustered into another category. It was determined that samples with P17 cone-cores were hoarding samples, the total number was 184; other samples were control samples, the total number was 159.
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Table 1 Results of the principal component (PC) analysis of habitat factors effected the hording habitat selection of Sciurus vulgaris.
Forest type Number of the conifers Bush type Bush density Floor cover type Canopy Slope aspect Slope position Number of the Korean pine seedlings Ubiety relative to the Korean pine forest Distance from the Korean pines Eigenvalue Total variance (%) Accumulated variance (%)
PC I 0.1535 0.0259 0.0615 0.0527 0.0196 0.0060 0.0664 0.0473 0.0602 0.0109 0.9790 5.8756 72.476 72.476
PC II
Out of the Korean pine forest Gap in the Korean forest
PC III
0.7186 0.1040 0.1768 0.1576 0.0940 0.0361 0.0776 0.1218 0.5770 0.1397 0.1822 0.6530 8.054 80.530
35
0.0913 0.0171 0.5217 0.8214 0.0538 0.0150 0.1172 0.1647 0.0184 0.0004 0.0136 0.4894 6.036 86.567
30
Number of cone-cores in a sample
Habitat factors and statistical parameters
In Korean pine forest
4.2. Main factors influencing hoarding habitat selection of squirrels Three principal components were obtained from the principal component analysis for habitat factors of hoarding samples, and the cumulative contribution rate was 86.57 (Table 1). We defined the first principal component as the seed resources factor, its factor loading capacity was >0.5; the second principal component as the forest type factor, the main influencing variables were forest type and number of Korean pine seedlings; and the third principal component as the impact factor, the main influencing variables were shrub type and density. The results of the principal component analysis showed that environment factors influencing hoarding habitat selection of squirrels were distance to Korean forest, forest type, number of Korean pine seedlings, shrub density and shrub types. 4.3. Effect of distance to Korean pine forest on hoarding habitat selection of squirrels Analysis of hoarding sample numbers with varied distances from Korean pines showed that the longer distance to Korean pine forest had no effect on hoarding habitat selection of squirrels, though squirrels preferred to hoard Korean pine seeds in gaps of Korean pine forest (Table 2). The number of cone-cores in hoarding samples with varied distances from Korean pines showed that the number of cone-cores discarded by squirrels in the hoarding samples with a distance of 150–300 m from Korean pine trees was significantly more than those in other hoarding samples. A large number of cones were carried by squirrels from Korean pine forest to forest gap and forest edge, and thus were dispersed far from Korean pine forest (OneWay ANOVA; df = 3, 183, F = 5.76, p = 0.0009, Fig. 1). 4.4. Hoarding selection of squirrels on different forest types The presence of conifers in samples influenced hoarding habitat selection of squirrels. Squirrels preferred to hoard seeds inside nat-
25 20 15 10 5 0 0-150
150-300
300-450
>450
Distance from the Korean pines (m) Fig. 1. Impact of distance from the Korean pines on the number of hoarding cones by Sciurus vulgaris (means with SE bars).
ural coniferous forest, natural fir and spruce forest and planted spruce forest, and avoided hoarding seeds inside natural broadleaved forest, natural birch forest, planted Korean pine forest and planted larch forest (Table 3). If the broad-leaved forest was taken as analysis object for hoarding habitat selection of squirrels, squirrels preferred to hoard seeds inside the broad-leaved forest with conifers (Table 4).
4.5. Effect of Korean pine seedling on hoarding habitat selection of squirrels The number of Korean pine seedlings in the hoarding samples was significantly more than those in the control samples in all types of forests (Kruskal–Wallis test; df = 1, v2 = 104.13, p < 0.0001; Fig. 2).
4.6. Effect of shrub on hoarding habitat selection of squirrels The shrub density in the hoarding samples was significantly lower than that in the control samples in all types of forests (Kruskal–Wallis test; df = 1, v2 = 83.99, p < 0.0001; Fig. 3), which showed that squirrels avoided hoarding seeds in high density shrub habitats.
Table 2 Impact of distance from the Korean pines on the hoarding habitat selection of Sciurus vulgaris. Ubiety relative to the Korean pine forest
Distance from the Korean pines (m)
Pw Expected proportion used (n = 159)
Pi Actual proportion used (n = 184)
Bailey’s 95% confidence interval for Pi
Preference
In the Korean pine forest Gap in the Korean forest Out of the Korean pine forest Out of the Korean pine forest Out of the Korean pine forest Out of the Korean pine forest
0–150 0–150 0–150 150–300 300–450 450–600
0.277 0.314 0.151 0.145 0.082 0.031
0.250 0.413 0.152 0.120 0.043 0.022
0.168 6 Pi 6 0.341 0.315 6 Pi 6 0.51 0.088 6 Pi 6 0.232 0.063 6 Pi 6 0.193 0.012 6 Pi 6 0.097 0.002 6 Pi 6 0.066
o + o o o o
+: Observed use is significantly higher than expected (preference). : Observed use is significantly lower than expected (avoidance). o: Observed use in proportion to its availability (random use).
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C. Zong et al. / Acta Ecologica Sinica 29 (2009) 362–366 Table 3 Selection of various forest type of hoarding habitat selection of Sciurus vulgaris. Forest type
Pw Expected proportion used (n = 159)
Pi Actual proportion used (n = 184)
Bailey’s 95% confidence interval for Pi
Preference
Natural Korean pine forest Natural coniferous forest Natural broad-leaved forest Natural mixed coniferous and broadleaved forest Natural birch forest Natural fir and spruce forest Planted Korean pine forest Planted larch forest Planted spruce forest
0.277 0.094 0.283 0.031
0.250 0.429 0.130 0.033
0.165 6 Pi 6 0.345 0.326 6 Pi 6 0.531 0.068 6 Pi 6 0.210 0.006 6 Pi 6 0.085
o + o
0.151 0.006 0.025 0.126 0.006
0.033 0.060 0 0.011 0.054
0.006 6 Pi 6 0.085 0.020 6 Pi 6 0.122 – 0 6 Pi 6 0.05 0.017 6 Pi 6 0.115
+ +
+: Observed use is significantly higher than expected (preference). : Observed use is significantly lower than expected (avoidance). o: Observed use in proportion to its availability (random use).
Table 4 Impact of the conifers on the hoarding habitat selection of Sciurus vulgaris. Forest type
Contain the conifers?
Pw Expected proportion used (n = 69)
Pi Actual proportion used (n = 30)
Bailey’s 95% confidence interval for Pi
Preference
Natural broad-leaved forest Natural broad-leaved forest Natural birch forest Natural birch forest
True
0.449
0.767
0.506 6 Pi 6 0.915
+
False
0.203
0.033
0 6 Pi 6 0.205
o
True False
0.072 0.275
0.200 0
0.048 6 Pi 6 0.424 –
o
+: Observed use is significantly higher than expected (preference). : Observed use is significantly lower than expected (avoidance). o: Observed use in proportion to its availability (random use).
5. Discussion 5.1. Characteristics of hoarding habitat selection of squirrels Squirrels preferred to hoard Korean pine seeds in broad-leaved habitat with conifers, there are three reasons possibly (Tables 3
and 4): Firstly, this will improve the efficiency of hoarding to reduce the energy consumption when recovering in winter. The research of Stapanian and Smith indicated that fox squirrels (Sciurus niger) transported foods along the direction of nest trees, which can enhance their ability to control foods [8]. The nests of red squirrels are all on the conifers, especially on fir trees [13].
Sample of hoarding area
Sample of hoarding area Control sample 70
Bush density in a sample (number /m2)
Number of the Korean pine seedlings in a sample
Control sample 40
30
20
10
0 NK
NC
NL
NM
NB
NF
PK
PL
PS
Forest type *
60 50 40 30 20 10 0 NK
NC
NL
NM
NB
NF
PK
PL
PS
Forest type * Fig. 2. Impact of the Korean pine seedling number on the hoarding habitat selection by Sciurus vulgaris (means with SE bars). *NK, natural Korean pine forest; NC, natural coniferous forest; NL, natural broad-leaved forest; NM, natural mixed coniferous and broad-leaved forest; NB, natural birch forest; NF, natural fir and spruce forest; PK, planted Korean pine forest; PL, planet larch forest; PS, planted spruce forest.
Fig. 3. Impact of bush density on the hoarding habitat selection by Sciurus vulgaris (means with SE bars). *NK, natural Korean pine forest; NC, natural coniferous forest; NL, natural broad-leaved forest; NM, natural mixed coniferous and broad-leaved forest; NB, natural birch forest; NF, natural fir and spruce forest; PK, planted Korean pine forest; PL, planet larch forest; PS, planted spruce forest.
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Secondly, this will reduce the risk of being preyed when squirrels hoard and retrieve seeds. As strictly arboreal animals [14], hoarding and retrieving seeds on the ground will increase the threat of squirrels to be preyed. In this investigation, we observed that squirrels were preyed by raptors such as goshawk (Accipiter gentilis) and common buzzard (Buteo buteo) several times. Conifers with intensive branches will help squirrels to avoid natural enemies. Squirrels always jump to the nearest conifer when they are disturbed by other animals in the process of hoarding and retrieving. Thirdly, the ground cover under conifer forest was composed of a mixture of fog and defoliation of broad-leaved trees, which will benefit to conceal pine seeds when hoarding and reduce the difficulty in retrieving in winter [15]. Squirrels hoard Korean pine seeds by peeling off scales of cones, carrying it in their mouth and running on the ground. Because the gross withered in hoarding season, the shrub becomes the obstructing factor influencing squirrels’ activities on ground, and shrub density will directly influence the hoarding and retrieving of squirrels. Accordingly, squirrels prefer to hoard seeds in shrub habitat with lower density. Field observation showed that squirrels always put Korean pine cone-cores on the base of one tree (mainly conifers), and fetch some seeds from the cone and hoard them under the fall-leaves litter of ground, and then return and fetch other seeds and jump to another direction near the tree. After making several caches in one site, squirrels transport the cone to the base of other trees, and repeat the above-mentioned procedure, so the seeds of one cone hoarded near different trees. When recovering seeds in winter, squirrels directly jump to the caches and retrieve seeds after they get down to the ground from the tree [9], so it can be presumed that the trees, especially conifers, maintain the spatial memory of squirrels to caches. In this study, in 184 hoarding samples, 15.2% of hoarding samples were situated outside Korean pine forest and within 150 m distance to trees, 41.3% hoarding samples were situated in gaps of Korean pine forest, these two were more than half of all hoarding samples and higher than the hoarding samples situated in Korean pine forest (25.0%) (Fig. 1). This result supported the Rapidsequestering hypothesis [16]. Some kinds of animals in Korean pine forest, such as chipmunk (Eutamias sibiricus), Korean field mouse (Apodemus speciosus), and wild pig (Sus scrofa), also forge, hoard and steal Korean pine seeds. Squirrels will avoid the intense competition for food and obtain most benefit by hoarding seeds outside Korean pine forest and in forest gaps where the density of other hoarding species is relatively lower [17]. 5.2. Can squirrels hoard seeds outside Korean pine forest? This study indicated that above 150 m distance to Korean pine trees did not impact hoarding habitat selection of squirrels (Table 2), and most caches were situated at an area with 150–300 m distance to Korean pine forest (Fig. 1). This showed that squirrels were able to transport and hoard massive seeds outside Korean pine forest. The results of cone placement test also supported this conclusion [18]. In hoarding season, squirrels were very vigilant, and it is difficult to directly observe the direction and distance of hoarding behavior, so it is suspected that the conclusion of Hutchins is educed by direct observation [3]. 5.3. Whether hoarding habitat of squirrels is a benefit for the establishment of Korean pine seedlings Korean pine seedlings not only reflect total results of hoarding habitat selection of hoarding animals, but also reveal hoarding
behavior of squirrels. The status of regeneration of seedlings within the hoarding samples was better than that within the control samples, which showed that the hoarding habitat is a benefit for the establishment of Korean pine seedlings in the temporal scale of 30a (Fig. 2). The Korean pine seedlings have a characteristic of liking shade, and the gap and edge of forest will be the most suitable site for regeneration [19]. Squirrels prefer to hoard massive seeds in these two kinds of habitats which show that the hoarding behavior of squirrels can promote regeneration (in gaps) and dispersal (in edge) of Korean pine (Fig. 1). Removing under-forest shrub aptly, artificially planting fastgrowing conifers to provide nest habitat for squirrels, and controlling the activity of artificial picking cone to a suitable extent will be a benefit for hoarding behavior of hoarding animals, and these promote the regeneration and dispersal of Korean pines. References [1] L. Wang, Chun Meng, Landscape diversity and stability of Korean pine broadleaved forest in Xiaoxing anling forest region, Chinese Journal of Applied Ecology 16 (12) (2005) 2267–2270. [2] D. Tao, D. Zhao, S. Zhao, et al., Dependence of natural regeneration or Korean pine on animals – an outclosure experiment, Chinese Biodiversity 3 (3) (1995) 131–133. [3] H.E. Hutchins, S.A. Hutchins, B. Liu, The role of birds and mammals in Korean pine (Pinus koraiensis) regeneration dynamics, Oecologia 107 (1) (1996) 120– 130. [4] H.-J. Su, J.-Z. MA, H.-F. Zou, et al., A field study on retrieved-caches of squirrel (Sciurus vulgaris) and their survival strategy in winter in Liangshui National Nature Reserve, Northeastern China, Acta Theriologica Sinica 26 (3) (2006) 262–266. [5] C.-H. Lu, B.-W. Liu, J.-P. Wu, Foraging and dispersing of Korean pine seed by animals in broad-leaved Korean pine forest, Journal of Northeast Forestry University 29 (5) (2001) 96–98. [6] J.-Z. MA, C. Zong, Q.-M. Wu, et al., Hoarding habitat selection of squirrels (Sciurus vulgaris) in Liangshui Nature Reserve, Acta Ecologica Sinica 26 (11) (2006) 3542–3548. [7] Q. Lu, J. Yu, X. Gao, et al., Winter habitat selection of Reeves’s muntjac and wild boars in the Qingliangfeng Mountains, Acta Theriologica Sinica 27 (1) (2007) 45–52. [8] M.A. Stapanian, C.C. Smith, A model for seed scatterhoarding: coevolution of fox squirrels and black walnuts, Ecology 59 (5) (1978) 884–896. [9] K. Rong, C. Zong, J.-Z. Ma, Behaviour tactics in overwintering Eurasian red squirrel in Liangshui Nature Reserve, China, Acta Theriologica Sinica 29 (2) (2009) 142–151. [10] R.f. Ji, Improvement of data processing method in principal component analysis, Journal of Shandong University of Science and Technology (Natural Science) 26 (5) (2007) 95–98. [11] D.L. Thomas, E.J. Taylor, Study designs and tests for comparing resource use and availability II, Journal of Wildlife Management 70 (2) (2006) 324– 336. [12] S. Cherry, A comparison of confidence interval methods for habitat useavailability studies, Journal of Wildlife Management 60 (3) (1996) 653– 658. [13] K. Rong, J.-Z. Ma, C. Zong, Nest-site selection by the Eurasian red squirrels in Liangshui Nature Reserve, Acta Theriologica Sinica 29 (1) (2009) 112– 119. [14] P.W.W. Lurz, G. John, M. Louise, Sciurus vulgaris, Mammalian Species (769) (2005) 1–10. [15] C. Zong, T. Chen, J.-Z. Ma, et al., Differences on hoarding habitat selection of squirrels (Sciurus vulgaris) and Eurasian nutcrackers (Nucifraga caryocatactes) in Liangshui Nature Reserve, Acta Theriologica Sinica 27 (2) (2007) 105– 111. [16] E.B. Hart, Food preferences of the cliff chipmunk, Eutamias dorsalis, in northern Utah, Great Basin Naturalist 31 (1971) 182–188. [17] A.L. Lisa, D. Martin, Food caching and differential cache pilferage: a field study of coexistence of sympatric kangaroo rats and pocket mice, Oecologia 128 (4) (2001) 577–584. [18] J.-Z. Ma, K. Rong, Q.-M. Wu, et al., Seed hoarding distance of Pinus koreansis by Sciurus vulgaris in Liangshui Nature Reserve, Chinese Journal of Zoology 43 (3) (2008) 45–49. [19] R. Zang, Z. Guo, W. Gao, Gap regeneration in a broadleaved Korean pine forest in Changbai Mountain Natural Reserve, Chinese Journal of Applied Ecology 9 (4) (1998) 349–353.