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Edge effects on nesting success of cavity-nesting birds in fragmented forests
Biological Conservation 126 (2005) 363–370 www.elsevier.com/locate/biocon
Edge eVects on nesting success of cavity-nesting birds in fragmented forests Wen-Hong Deng a
a,¤
, Wei Gao
b
Ministry of Education Key Laboratory for Biodiversity Sciences and Ecological Engineering, College of Life Sciences, Beijing Normal University, Beijing, 100875, China b College of Life Sciences, Northeast Normal University, Changchun, 130024, China Received 11 February 2005 Available online 21 July 2005
Abstract Forest fragmentation leads to the creation of isolated forest patches and habitat edges with subsequent impact on forest-interior bird species. Although the eVects of fragmentation and edge on avian nesting success are well documented for open cup-nesting species in eastern deciduous forests in North America, it is unclear whether these eVects are common for all birds nesting in predominantly forested landscapes. In particular, edge eVects on nesting success of cavity-nesting birds are poorly understood. Using natural cavity nests, we examined nesting success of four species of cavity-nesting birds (two nonexcavators and two excavators), the yellow-rumped Xycatcher (Ficedula zanthopygia), the great tit (Parus major), the great spotted woodpecker (Picoides major), and the grey-faced woodpecker (Picus canus) in relation to forest edges in Zuojia Nature Reserve, Jilin province, northeastern China. Our primary objective was to assess whether distance to the edge of agricultural lands was related to nesting success for cavity-nesting birds in fragmented forests. A total of 439 natural cavity nests of the four species were located and monitored during four breeding seasons. Probability of nest success was inXuenced by distance to forest edge for nonexcavators, but not for excavators. The rate of nesting success of the two nonexcavators, yellow-rumped Xycatcher and the great tit, increased with distance from the edges. For all cavity nests, nesting success was 0.43 at 0–100 m, 0.56 at 101–200 m, 0.68 at 201–300 m, 0.61 at 301–400 m, 0.77 at 401–500 m from the edges. Nesting success ranged from 0.57 for the yellow-rumped Xycatcher to 0.89 for the Grey-faced Woodpecker. Failed nests were often occupied by nest-site competitors (accounting for 68%). However, predation only accounted for 20% of all nest failures. Our results suggest that negative edge eVects do exist for some cavity-nesting birds, especially for nonexcavator species. 2005 Elsevier Ltd. All rights reserved. Keywords: Cavity-nesting birds; Nesting success; Edge eVects; Nest-site competition; Forest fragments
1. Introduction Forest fragmentation aVects the distribution and abundance of organisms by reducing the amount and proximity of remnant patches of suitable habitat and increasing the amount of edges (Andrén, 1992; Boulinier * Corresponding author. Tel.: +86 10 58805121; fax: +86 10 58807721. E-mail address: [email protected] (W.-H. Deng).
0006-3207/$ - see front matter 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2005.06.013
et al., 1998; Ford et al., 2001; Maina and Jackson, 2003). Edges may aVect the organisms by causing changes in the biotic and abiotic conditions some distance into the forest, such as increased amounts of sunlight, high wind speeds, and larger Xuctuations in temperature and humidity (Saunders et al., 1991; Murica, 1995). Avian species may respond to one or a combination of these changes in the landscape as a result of diVerent biological mechanisms (Robinson et al., 1995; Donovan et al., 1997). Species that require forest interior may avoid
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edges due to altered microclimate, vegetation structure, or high density of predators or brood parasites (Yahner and Scott, 1988; Malcolm, 1994; Marini et al., 1995; Pasitschniak-Arts et al., 1998; Stephens et al., 2003). On the other hand, although predators and brood parasites may be more abundant or active in the adjacent habitat and edge, some bird species were concentrated near to edge areas. This paradox of high bird abundance and richness but low nesting success near edges was termed an ecological trap by Gates and Gysel (1978). Many studies have tested the occurrence of edge eVects on nesting success of forest birds and concluded that high predation and brood parasitism rates near edges were main causes of nest failures (Hannon and Cotterill, 1998; Manolis et al., 2002). However, an edge eVect has not been found in all studies (Angelstam, 1986; Santos and Telleria, 1992; Hanski et al., 1996; Morrison and Bolger, 2002). Early studies suggested that abrupt or permanent edges generally were thought to be associated with higher rates of predation and parasitism than gradual or regenerating edges (Suarez et al., 1997; Deng et al., 2003), but many contradictory results exist, particularly in forest landscapes (Yahner and Scott, 1988; Rodewald, 2002). These conXicting results may be explained in part by the mediation of edge eVects by life history traits of organisms (e.g., open- vs. cavity-nesting bids) and landscape characteristics. Most early studies were completed on open cup-nesting birds. However, nest predation and brood parasitism are unlikely to provide a general explanation for the edge eVects on bird species that nest in more protected sites such as cavities (Matthysen and Adriaensen, 1998). Nesting success of cavity-nesting birds near edges may be inXuenced by other factors such as changes in competition for nest sites (Deng, 2001). Very few studies have assessed nesting success of cavity-nesting birds near edges in fragmented forests (Nour et al., 1993; Matthysen and Adriaensen, 1998). Many studies of eVects on nesting success have used artiWcial nests (Wilcove, 1985; Picman and Schriml, 1994; Hartley and Hunter, 1998; Githiru et al., 2005). Such studies can identify general patterns of variation in nest predation intensity (Haskell, 1995; Sloan et al., 1998). However, predation and brood parasitism rates on artiWcial nests may be poorly or inconsistently correlated with predation and parasitism rates on real nests (Ortega et al., 1998; Moore and Robinson, 2004). Here, we examine edge eVects on nesting success for natural nests of four cavity-nesting bird species (two excavators and two nonexcavators) in a forested landscape in which edges were created by farmland reclamation. We also used data from these four species to determine whether life history characteristics (excavators vs. nonexcavators) aVect the relationship between nest success and distances to edge.
2. Materials and methods 2.1. Study site Our study site, approximately 200 km2 in size, was located in Zuojia Nature Reserve and included the Tumengling Mountains and Zhujia Mountains ranging from the eastern Changbai Mountains to the western plain (126°1⬘127°2⬘N, 44°6⬘45°9⬘E). The climate is east monsoon, characterized by hot, dry summers and cold, snowy winters. Mean monthly temperatures ranged from ¡20.5 °C in January to 23.6 °C in August. Vegetation within the study area was quite diverse, although the forest type was secondary forest. The age of the forests is 40 years. The seven tree species mainly present on the study area were Mongolian oaks (Quercus mongolica), dahurian birchs (Betula davurica), Manchurian linden (Tilia mandschurica), Japanese elm (Ulmus japonica), Scotch pine (Pinus sylvestris), Korean larches (Pinus koraiensis) and masson pines (Pinus massoniana) (Deng et al., 2003). In the study area, Dahurian rose (Rosa dahurica), Korean rose (Rosa d oreana), willowleaf spiraea (Spiraea salicifolia), ural falsespiraea (Sorbaria sorbifolia), and sakhalin honeysuckle (Lonicera maximowiczii) dominated the shrub layer (Deng, 2001). We established six study plots (mean size D11.2 ha, range 7.6–32.8 ha) to evaluate edge eVects on nesting success of cavity-nesting birds. The six study plots were chosen because they had (1) similar vegetation characteristics (tree age, tree species, composition); (2) similar management histories; and (3) similar ectones (embedded farmland). The plot terrain was relatively Xat and elevation ranged from 325 to 388 m above sea level. We measured the distance from each nest to the forest edge by pacing, with a known meter, or by measuring the distance on a gridded map of each plot. 2.2. Nest monitoring Four to Wve people searched for nests daily in each study plot from mid-April to the end of July during 1998–2001. Nests were found by observing birds during nest building, food carrying and by searching tree holes. Workers distributed their search eVort as evenly as possible throughout the plots. The location of each nest was marked with a Xag that was usually placed at least 10 m from the nest. Upon Wnding a nest, we recorded the stage of nesting, location of the nest, and the species of the bird. Nests were revisited every three or four days and every other day near anticipated Xedging date to monitor the fate of the nests. We checked the cavities using a device consisting of mirrors and a torch. When checking nests, we strived to avoid damaging vegetation and making trails near nests. Nests that Xedged at least one young were considered successful. Observation of Xedging, Xedglings near nests, and parents feeding Xedglings
W.-H. Deng, W. Gao / Biological Conservation 126 (2005) 363–370
were taken as evidence of a successful nest. Nesting attempts were considered failed if (1) there was clear evidence of predation (broken egg, scattered feathers); (2) the cavity was empty before Xedging was possible; (3) chicks were never seen; (4) the cavity was taken over by other species. If those cues were not available to determine success or failure, the outcome was considered uncertain. Uncertain nest fate was rare in this study. We also noted when nests were abandoned before the Wrst egg was laid, although we did not consider these early abandonments in our analyses. Daily survival rates were estimated following MayWeld (1961, 1975). 2.3. Statistical analyses Nesting success rates were estimated using the MayWeld method (MayWeld, 1961, 1975). For nest fates considered uncertain, exposure period was terminated on the last day that nests were known to be active. For nests known to be successful or failed, exposure period was terminated on the midpoint between the last day the nest was observed as active and the Wrst day the nest was observed as inactive. Because nest success rates often vary between nesting stages, nest success was calculated separately for the incubation and nestling periods. Donovan et al. (1995) suggested if partial nest loss were common, MayWeld estimates of nest success might not be appropriate for calculating productivity. Partial nest loss in this study was rare (<3%). Comparisons of MayWeld nest success values between plots and years were done using the computer program Contrast, with a 2 analysis and multiple comparisons (Sauer and Williams, 1989). We grouped nests and compared nest success in two zones (0–200 m vs. 201–500 m) because these contained roughly equal numbers of nests for all species. Deng (2001) suggested that a threshold edge eVect on nesting success appears to exist for several bird species at approximately 200 m in the study area. We used contingency tables to test the hypothesis that nest success was diVerent in the two zones. While we recognize the importance of species-speciWc nest success as a unit of analysis, for some analyses, and to increase sample sizes, we pooled species according to bird life history traits (i.e., nonexcavator or excavator). For comparisons of nest success at diVerent distances from the edge, we ranked the six plots in order of plot-level nest success for each species. We then compared patterns of plot-level nest success for nonexcavators and excavators. Also, we tested for species-speciWc year and plot eVects using logistic regression models. For species that showed signiWcant diVerences among nest success in the two zones, we then grouped nests into smaller zones and tested multiple hypotheses related to eVects at 100 m intervals (0– 100, 101–200, 201–300, 301–400, 401–500 m) from forest edge. Because the number of nests further than 500 m
365
from the forest edges was small (<20 nests), we only used the nests within 500 m from forest edges in the analysis during this step. We used logistic regression to examine the inXuence of distance to forest edge on nest fate. This technique does not require that data from the independent variable be normally distributed (Flaspohler et al., 2001). For multi-species calculations of nest success, we used an average weighted by exposure days to estimate nest success for pooled groups of birds. For comparisons of nest success at distances from the edge, we used D 0.05. Data were given as means §1 SE. All logistic models were calculated with forward, backward, stepwise, and score methods to achieve the best model. All methods yielded similar results. To evaluate whether the relationship between nest success and distance to forest edge was independent of bird species, log-linear models were Wtted to three-way contingency tables for all species. For all logistic regression analyses, we used simple nest fate (success D 1 or failure D 0; unoccupied D 1, occupied D 0), either from a Wrst or a repeated nest. In all logistic regression models, we used an information-theoretic approach and calculated Akaike’s Information Criterion (AIC) based on log-likelihood values to identify the best models (Burnham and Anderson, 1998). The model with the smallest AIC is the best approximating model for the data. All statistical analyses were conducted using SAS (1990).
3. Results 3.1. Nest success by distance to forest edge A total of 439 cavity nests of four species were located and monitored during 1998–2001 (Table 1). Of this total, 422 nests were entered into our analysis of edge eVects. Nests abandoned before egg laying (n D 12) or of uncertain outcome (n D 5) were excluded from analyses. Nest success rates of each cavity-nesting bird did not vary between years (2 D 6.13, df D 3, P D 0.11) and plots (2 D 9.08, df D 5, P D 0.91). However, nest success rates among species within years were signiWcantly diVerent. Nest success varied among individual species, with the lowest value for yellow-rumped Xycatcher and the highest for grey-faced woodpecker (Table 2). On all six plots, excavator species had higher nest success than non-excavator species (Table 2). For four years of pooled data, nest success was lower in the 0–200 m zone than in the 201–500 m zone from the forest edge for the nonexcavators (2 D 6.94, df D 1, P < 0.01), but not for excavators (2 D 2.89, df D 1, P D 0.09). Logistic regression models including a distance to forest edge variable provided a better Wt to nest fate data for the yellow-rumped Xycatcher and the great tit (Table 3), but not for the great spotted woodpecker and the grey-faced woodpecker. The best models for yellow-rumped Xycatcher
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Table 1 Nest fates of cavity-nesting birds in Zuojia Nature Reserve, Northeastern China, 1998–2001 Species and year
Total nests in analysis
Total nests failed
Number (percentage) of nest failures, by cause Occupationa
Yellow-rumped Xycatcher 1998 1999 2000 2001 All years
19 27 26 23 95
9 12 10 7 38
7 (78) 6 (50) 7 (70) 5 (71) 25 (66)
Great tit 1998 1999 2000 2001 All years
18 21 20 25 84
8 9 5 10 32
5 (62) 7 (78) 3 (60) 5 (50) 20 (63)
Great spotted woodpecker 1998 1999 2000 2001 All years
26 27 31 34 118
2 6 4 5 17
4 (67) 3 (75) 5 (100) 12 (70)
Grey-faced woodpecker 1998 1999 2000 2001 All years
28 30 35 32 125
2 3 5 4 14
2 (100) 2 (67) 3 (60) 3 (75) 10 (72)
a b c
Abandonmentb
Predation 2 (22) 2 (17) 3 (30) 7 (16) 2 (25) 1 (20) 2 (20) 5 (16)
Uncertainc
3 (25)
1(8)
2 (25) 5 (13)
1 (5)
1 (13) 2 (22) 1 (20) 1 (10) 5 (16)
2 (20) 2 (5)
2 (100) 2 (33) 1 (25) 4(24)
1 (6)
1(20)
1 (20)
1 (7)
1 (7)
1 (33) 1(25) 2 (14)
Nests were re-occupied by another species after laying. Abandonment prior to laying. If cues were not available to determine success or failure.
Table 2 Nest success estimates of cavity-nesting birds in Zuojia Nature Reserve, northeastern China, 1998–2001 Species Yellow-rumped Xycatcher Great tit Great spotted woodpecker Grey-faced woodpecker a b c
Nest success § SEa 1998
1999
2000
2001
All yearsb
0.67 § 0.08 (19)c 0.72 § 0.12 (18) 0.86 § 0.03 (26) 0.91 § 0.02 (28)
0.64 § 0.06 (27) 0.69 § 0.09 (21) 0.83 § 0.05 (27) 0.88 § 0.06 (30)
0.71 § 0.11 (26) 0.79 § 0.06 (20) 0.69 § 0.17 (31) 0.84 § 0.09 (35)
0.66 § 0.04 (23) 0.66 § 0.12 (25) 0.87 § 0.04 (34) 0.90 § 0.11 (32)
0.67 § 0.09 (95) 0.73 § 0.10 (84) 0.84 § 0.04 (118) 0.89 § 0.10 (125)
MayWeld (1961, 1975) nest success values calculated from exposure. 2 comparison of diVerences species for all years nest success (P > 0.05). Number of nests.
included just the single predictor log distance to forest edge, but for great tits, log distance and year were the predictors that produced the best-Wtting model (Table 3). The probability of failure for yellow-rumped Xycatcher nests decreased with increasing distance to the edge in a roughly linear function (Fig. 1), but this trend was not apparent for other cavity-nesting species. 3.2. Causes of nest failure Potential predators on cavity-nesting birds (eggs, nestlings, adults) that were observed on the study plots during four years were Eurasian sparrow hawk (Accipiter nicus), besra sparrow hawk (Accipiter virgatus), longeared owl (Asio otus), Siberian weasel (Mustela aibirica),
Siberian chipmunk (Tamias sibiricus), and beauty snake (Elaphe taeniura). The white-cheeked starling (Sturnus cineraceus) was the most important nest-site competitor for the four cavity-nesting bird species. A total 101 failure nests occurred in our analyses. Failed nests were often a results of nest-site competitors (competitors which accounted for 68% of such losses). Occupation rate by nest-site competitors was higher (66%, n D 46) during the egg period than during the nestling period (34%, n D 22). Seventy percent of nests lost to competitors were lost to white-cheeked starlings. In contrast, nest predation only accounted for 20%. The four species also suVered from nest site occupation by the white-backed woodpecker (Picoides leucotos) and sometimes by Siberian chipmunk. Also, the occupation rate
W.-H. Deng, W. Gao / Biological Conservation 126 (2005) 363–370
AIC
Yellow-rumped Xycatcher FDC 1 FDC+D 2 F D C + LD 2 F D C + LD + Y 3 F D C + LD + P 8 F D C + LD + P + Y 9
¡81.32 ¡78.26 ¡77.49 ¡77.28 ¡76.11 ¡73.37
164.64 160.52 158.98 160.56 168.22 164.74
Great tit FDC FDC+D F D C + LD F D C + LD + Y F D C + LD + P F D C + LD + P + Y
¡65.43 ¡64.26 ¡64.11 ¡63.05 ¡61.57 ¡59.44
132.86 132.52 132.22 132.10 139.14 136.88
1 2 2 3 8 9
F indicates nest fate; C indicates constant; D indicates distance to forest edge; LD indicates log10 (D); Y indicates studying years; P indicates plots; AIC indicates Akaike’s Information Criterion. F D C + LD is the best Wt for the yellow-rumped Xycatcher; F D C + LD + Y is the best Wt for the great tit.
by the white-cheeked starlings was signiWcantly greater for the yellow-rumped Xycatcher in the 0–200 m zone than the 201–500 m (2 D 5.16, df D 1, P D 0.02). Nest predation did not follow this same trend (2 D 1.18, df D 1, P D 0.29) when comparing between the two zones. Lastly, we did not Wnd nest parasitism in this study.
4. Discussion
Nest success
Log-likelihood
yellow-rumped flycatcher
0.8
0.6 25
21
14
19
16
0.4 1
Nest success
Number of parameters
great tit
0.8
0.6 23
20
12
16
13
0.4
great spotted woodpecker 1
Nest success
Models
1
0.8 0.6
31
26
22
19
20
0.4
grey-faced woodpecker 1
Nest success
Table 3 Logit transformation models of the nest fate for the yellow-rumped Xycatcher and great tit during four breeding seasons in northeastern China
367
0.8
0.6
29
39
12
22
23
0.4
4.1. Edge eVects on cavity-nesting birds We found some evidence for an edge eVect on nesting success of cavity-nesting species near anthropogenic edges, especially for nonexcavator species. Our results concur with Wndings from several recent studies on open-cup nesting species (Flaspohler et al., 2001; Manolis et al., 2002). Our results are also consistent with Wndings from several studies of cavity-nesting birds. Denny and Summers (1996) found that cavity birds were aVected by edge-related factors. Huhta and Jokimaki (2001) found pairing success and nesting success of two hole-nesting passerines, the pied Xycatcher (Ficedula hypoleuca) and the cavity-nesting redstart (Phoenicurus phoenicurus), were aVected by proximity to edge. However, Matthysen and Adriaensen (1998) reported that reproductive success of the great tit was not aVected by forest fragmentation in western Europe. Most early studies of edge-related nest success of avian species suggested that high nest predation and parasitism rates were main causes of high nest failure near edges (Gates and Gysel, 1978; Gibbs, 1991; Eriksson et al., 2001; Manolis
0-100
101-200
201-300
301-400
401-500
Distance to edge (m) Fig. 1. MayWeld nest success for the four cavity-nesting species in relation to distance to the forest edge in Zuojia Nature Reserve, Northeastern China, 1998–2001. The number of nests used to estimate nest success is given inside each histogram bar.
et al., 2002). However, in our study, the main cause of nest failure near edges was not nest predation or parasitism, but rather, competition for nest sites among cavity nesters. We also found that the rate of nesting success of yellow-rumped Xycatcher and the great tit increased with distance from the edges, but the great spotted woodpecker and the grey-faced woodpecker did not follow the same trend. This indicates local scale habitat perturbations can have species-speciWc eVects on nesting success of cavity-nesting birds. Several ideas have been proposed to explain the absence of edge-related nest predation in forested landscapes. Angelstam (1986) suggested that edge-related nest predation rates could be explained by diVerences in productivity of the adjacent habitats. This explanation
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indicated that an edge eVect on nest predation is most likely to occur where there is a steep gradient in primary productivity across the edge and is least likely to occur where this gradient is less pronounced (Lahti, 2001). Lack of predation may also occur if there is no increase in prey density along edges or if predators are habitat specialists (i.e., they do not move between habitats and cross edges) (Rodewald, 2002). Morrison and Bolger (2002) suggested that the lack of edge eVect on nest predation rate of Rufous-crowned Sparrow (Aimophila ruWceps) appeared to be due to a lack of edge sensitivity of snakes. Excavator species (the great spotted woodpecker and the grey-faced woodpecker) had signiWcantly higher nest success than nonexcavator species (the yellow-rumped Xycatcher and the great tit). Nonexcavator species are generally smaller than excavator species. This smaller size may reduce ability to compete for high quality nests. Nonexcavator species may have had relatively low nest success in part because they tend to nest in old cavities and nest closer to the ground (Sonerud, 1985; Li and Martin, 1991). 4.2. Nest-site competitors Numerous studies of avian reproductive success have concluded that the destruction of eggs and nestlings by predators is the most signiWcant inXuence on avian nest success (Askins, 1995). But in our results, nest predation was not the main causes of nest failures and accounted for only 20% of all nest failures. Most of the failed nests (68%) were attributable to nest-site competitors. Indeed, nest takeovers by the white-cheeked starlings were common both in edge and interior habitats. A potential cost of cavity-nesting birds is increased competition for nest sites, especially for nonexcavator species. Raphael and White (1984) found a signiWcant correlation between cavity density and nonexcavator species density in the coniferous forests of the Sierra Nevada, suggesting densities were limited by nest site availability. In our study area, because the forest age was only about 40 years, lack of natural tree cavities probably was the main reason for drastic competition among the species, although we did not investigate cavity resources throughout the study area. Some researchers found that some cavity-nesting birds prefer edges and open understories in forested landscapes (Belles-Isles and Picman, 1986; Finch, 1989). Dobkin et al. (1995) explained that birds that use multiple habitat types might nest on edges to reduce commuting time between resources. Cavity nesters may select nest sites with open understories to increase their ability to detect approaching predators (Finch, 1989). We did not Wnd the same phenomenon during our study period. The number of cavity nests was roughly equal between edge and interior habitat.
Brush (1983) observed Xycatchers, starlings, and other species competing for nest cavities, but the starlings had no eVect on other species because abundant alternate nest sites were available. However, the potential for interference competition seems greatest in habitats where nest sites are limited, as was the case in our studies. Weitzel (1988) reported that starlings were serious competitors for certain native birds in Nevada. Kerpez and Smith (1990) found evidence for competition and a negative relationship between starlings and gila woodpeckers (Melanerpes uropygialis) in Arizona. Ingold (1998) suggested that the European Starling (Sturnus vulgaris) was having a signiWciantly adverse eVect on the reproductive success of northern Xickers (Colaptes auratus). Despite these clear examples of starling having detrimental eVects on many cavity-nesting species, Koenig (2003) did not Wnd that starlings had had a severe impact on populations of native cavity-nesting birds in a study of 27 species in America. Starlings may nest in forest, but they do not feed in forests (Feare, 1984). They commute to open habitats from their nest sites where they forage, just as does the brown-headed cowbird (Molothrus ater) of North America. It seems likely that starlings prefer to nest near edges because it reduces their travel costs from their breeding areas to their feeding areas. Like the parasitic cowbird phenomenon, this is a clear example of a situation in which the matrix surrounding a fragment directly aVects birds nesting within the fragment. The disturbed landscape supports a nest “pirate” that depends on the matrix for food, but nest in forests. Our results suggest that local land-use practices or natural events can have a profound inXuence on the nesting success of birds that depend upon disturbed habitats for nesting. Our results also suggest that forest management strategies should consider not only stands in forest planning, but also the edges.
Acknowledgments We thank Yan-Hui Li, Yang Liu, Zheng-Xin Sun, Ren-Kai Song, Gui-Quan Xiang, Hai-Tao Wang, JingRun Cheng, Nan Li, Quan Zhao, and Long Sun for their involvement in the collection of Weld data. We thank the teachers and students who are in Department of Wildlife, Special Plant and Animal College that they found and monitored the success of the nests. Members of the ecology team, Beijing Normal University, were extremely patient and helpful in providing assistance with data analysis. We thank fund of National Nature Science of China to support this research (No. 30470300). We also thank anonymous reviewers for their helpful and excellent remarks on this paper.
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Edge eVects on nesting success of cavity-nesting birds in fragmented forests Wen-Hong Deng a
a,¤
, Wei Gao
b
Ministry of Education Key Laboratory for Biodiversity Sciences and Ecological Engineering, College of Life Sciences, Beijing Normal University, Beijing, 100875, China b College of Life Sciences, Northeast Normal University, Changchun, 130024, China Received 11 February 2005 Available online 21 July 2005
Abstract Forest fragmentation leads to the creation of isolated forest patches and habitat edges with subsequent impact on forest-interior bird species. Although the eVects of fragmentation and edge on avian nesting success are well documented for open cup-nesting species in eastern deciduous forests in North America, it is unclear whether these eVects are common for all birds nesting in predominantly forested landscapes. In particular, edge eVects on nesting success of cavity-nesting birds are poorly understood. Using natural cavity nests, we examined nesting success of four species of cavity-nesting birds (two nonexcavators and two excavators), the yellow-rumped Xycatcher (Ficedula zanthopygia), the great tit (Parus major), the great spotted woodpecker (Picoides major), and the grey-faced woodpecker (Picus canus) in relation to forest edges in Zuojia Nature Reserve, Jilin province, northeastern China. Our primary objective was to assess whether distance to the edge of agricultural lands was related to nesting success for cavity-nesting birds in fragmented forests. A total of 439 natural cavity nests of the four species were located and monitored during four breeding seasons. Probability of nest success was inXuenced by distance to forest edge for nonexcavators, but not for excavators. The rate of nesting success of the two nonexcavators, yellow-rumped Xycatcher and the great tit, increased with distance from the edges. For all cavity nests, nesting success was 0.43 at 0–100 m, 0.56 at 101–200 m, 0.68 at 201–300 m, 0.61 at 301–400 m, 0.77 at 401–500 m from the edges. Nesting success ranged from 0.57 for the yellow-rumped Xycatcher to 0.89 for the Grey-faced Woodpecker. Failed nests were often occupied by nest-site competitors (accounting for 68%). However, predation only accounted for 20% of all nest failures. Our results suggest that negative edge eVects do exist for some cavity-nesting birds, especially for nonexcavator species. 2005 Elsevier Ltd. All rights reserved. Keywords: Cavity-nesting birds; Nesting success; Edge eVects; Nest-site competition; Forest fragments
1. Introduction Forest fragmentation aVects the distribution and abundance of organisms by reducing the amount and proximity of remnant patches of suitable habitat and increasing the amount of edges (Andrén, 1992; Boulinier * Corresponding author. Tel.: +86 10 58805121; fax: +86 10 58807721. E-mail address: [email protected] (W.-H. Deng).
0006-3207/$ - see front matter 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2005.06.013
et al., 1998; Ford et al., 2001; Maina and Jackson, 2003). Edges may aVect the organisms by causing changes in the biotic and abiotic conditions some distance into the forest, such as increased amounts of sunlight, high wind speeds, and larger Xuctuations in temperature and humidity (Saunders et al., 1991; Murica, 1995). Avian species may respond to one or a combination of these changes in the landscape as a result of diVerent biological mechanisms (Robinson et al., 1995; Donovan et al., 1997). Species that require forest interior may avoid
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edges due to altered microclimate, vegetation structure, or high density of predators or brood parasites (Yahner and Scott, 1988; Malcolm, 1994; Marini et al., 1995; Pasitschniak-Arts et al., 1998; Stephens et al., 2003). On the other hand, although predators and brood parasites may be more abundant or active in the adjacent habitat and edge, some bird species were concentrated near to edge areas. This paradox of high bird abundance and richness but low nesting success near edges was termed an ecological trap by Gates and Gysel (1978). Many studies have tested the occurrence of edge eVects on nesting success of forest birds and concluded that high predation and brood parasitism rates near edges were main causes of nest failures (Hannon and Cotterill, 1998; Manolis et al., 2002). However, an edge eVect has not been found in all studies (Angelstam, 1986; Santos and Telleria, 1992; Hanski et al., 1996; Morrison and Bolger, 2002). Early studies suggested that abrupt or permanent edges generally were thought to be associated with higher rates of predation and parasitism than gradual or regenerating edges (Suarez et al., 1997; Deng et al., 2003), but many contradictory results exist, particularly in forest landscapes (Yahner and Scott, 1988; Rodewald, 2002). These conXicting results may be explained in part by the mediation of edge eVects by life history traits of organisms (e.g., open- vs. cavity-nesting bids) and landscape characteristics. Most early studies were completed on open cup-nesting birds. However, nest predation and brood parasitism are unlikely to provide a general explanation for the edge eVects on bird species that nest in more protected sites such as cavities (Matthysen and Adriaensen, 1998). Nesting success of cavity-nesting birds near edges may be inXuenced by other factors such as changes in competition for nest sites (Deng, 2001). Very few studies have assessed nesting success of cavity-nesting birds near edges in fragmented forests (Nour et al., 1993; Matthysen and Adriaensen, 1998). Many studies of eVects on nesting success have used artiWcial nests (Wilcove, 1985; Picman and Schriml, 1994; Hartley and Hunter, 1998; Githiru et al., 2005). Such studies can identify general patterns of variation in nest predation intensity (Haskell, 1995; Sloan et al., 1998). However, predation and brood parasitism rates on artiWcial nests may be poorly or inconsistently correlated with predation and parasitism rates on real nests (Ortega et al., 1998; Moore and Robinson, 2004). Here, we examine edge eVects on nesting success for natural nests of four cavity-nesting bird species (two excavators and two nonexcavators) in a forested landscape in which edges were created by farmland reclamation. We also used data from these four species to determine whether life history characteristics (excavators vs. nonexcavators) aVect the relationship between nest success and distances to edge.
2. Materials and methods 2.1. Study site Our study site, approximately 200 km2 in size, was located in Zuojia Nature Reserve and included the Tumengling Mountains and Zhujia Mountains ranging from the eastern Changbai Mountains to the western plain (126°1⬘127°2⬘N, 44°6⬘45°9⬘E). The climate is east monsoon, characterized by hot, dry summers and cold, snowy winters. Mean monthly temperatures ranged from ¡20.5 °C in January to 23.6 °C in August. Vegetation within the study area was quite diverse, although the forest type was secondary forest. The age of the forests is 40 years. The seven tree species mainly present on the study area were Mongolian oaks (Quercus mongolica), dahurian birchs (Betula davurica), Manchurian linden (Tilia mandschurica), Japanese elm (Ulmus japonica), Scotch pine (Pinus sylvestris), Korean larches (Pinus koraiensis) and masson pines (Pinus massoniana) (Deng et al., 2003). In the study area, Dahurian rose (Rosa dahurica), Korean rose (Rosa d oreana), willowleaf spiraea (Spiraea salicifolia), ural falsespiraea (Sorbaria sorbifolia), and sakhalin honeysuckle (Lonicera maximowiczii) dominated the shrub layer (Deng, 2001). We established six study plots (mean size D11.2 ha, range 7.6–32.8 ha) to evaluate edge eVects on nesting success of cavity-nesting birds. The six study plots were chosen because they had (1) similar vegetation characteristics (tree age, tree species, composition); (2) similar management histories; and (3) similar ectones (embedded farmland). The plot terrain was relatively Xat and elevation ranged from 325 to 388 m above sea level. We measured the distance from each nest to the forest edge by pacing, with a known meter, or by measuring the distance on a gridded map of each plot. 2.2. Nest monitoring Four to Wve people searched for nests daily in each study plot from mid-April to the end of July during 1998–2001. Nests were found by observing birds during nest building, food carrying and by searching tree holes. Workers distributed their search eVort as evenly as possible throughout the plots. The location of each nest was marked with a Xag that was usually placed at least 10 m from the nest. Upon Wnding a nest, we recorded the stage of nesting, location of the nest, and the species of the bird. Nests were revisited every three or four days and every other day near anticipated Xedging date to monitor the fate of the nests. We checked the cavities using a device consisting of mirrors and a torch. When checking nests, we strived to avoid damaging vegetation and making trails near nests. Nests that Xedged at least one young were considered successful. Observation of Xedging, Xedglings near nests, and parents feeding Xedglings
W.-H. Deng, W. Gao / Biological Conservation 126 (2005) 363–370
were taken as evidence of a successful nest. Nesting attempts were considered failed if (1) there was clear evidence of predation (broken egg, scattered feathers); (2) the cavity was empty before Xedging was possible; (3) chicks were never seen; (4) the cavity was taken over by other species. If those cues were not available to determine success or failure, the outcome was considered uncertain. Uncertain nest fate was rare in this study. We also noted when nests were abandoned before the Wrst egg was laid, although we did not consider these early abandonments in our analyses. Daily survival rates were estimated following MayWeld (1961, 1975). 2.3. Statistical analyses Nesting success rates were estimated using the MayWeld method (MayWeld, 1961, 1975). For nest fates considered uncertain, exposure period was terminated on the last day that nests were known to be active. For nests known to be successful or failed, exposure period was terminated on the midpoint between the last day the nest was observed as active and the Wrst day the nest was observed as inactive. Because nest success rates often vary between nesting stages, nest success was calculated separately for the incubation and nestling periods. Donovan et al. (1995) suggested if partial nest loss were common, MayWeld estimates of nest success might not be appropriate for calculating productivity. Partial nest loss in this study was rare (<3%). Comparisons of MayWeld nest success values between plots and years were done using the computer program Contrast, with a 2 analysis and multiple comparisons (Sauer and Williams, 1989). We grouped nests and compared nest success in two zones (0–200 m vs. 201–500 m) because these contained roughly equal numbers of nests for all species. Deng (2001) suggested that a threshold edge eVect on nesting success appears to exist for several bird species at approximately 200 m in the study area. We used contingency tables to test the hypothesis that nest success was diVerent in the two zones. While we recognize the importance of species-speciWc nest success as a unit of analysis, for some analyses, and to increase sample sizes, we pooled species according to bird life history traits (i.e., nonexcavator or excavator). For comparisons of nest success at diVerent distances from the edge, we ranked the six plots in order of plot-level nest success for each species. We then compared patterns of plot-level nest success for nonexcavators and excavators. Also, we tested for species-speciWc year and plot eVects using logistic regression models. For species that showed signiWcant diVerences among nest success in the two zones, we then grouped nests into smaller zones and tested multiple hypotheses related to eVects at 100 m intervals (0– 100, 101–200, 201–300, 301–400, 401–500 m) from forest edge. Because the number of nests further than 500 m
365
from the forest edges was small (<20 nests), we only used the nests within 500 m from forest edges in the analysis during this step. We used logistic regression to examine the inXuence of distance to forest edge on nest fate. This technique does not require that data from the independent variable be normally distributed (Flaspohler et al., 2001). For multi-species calculations of nest success, we used an average weighted by exposure days to estimate nest success for pooled groups of birds. For comparisons of nest success at distances from the edge, we used D 0.05. Data were given as means §1 SE. All logistic models were calculated with forward, backward, stepwise, and score methods to achieve the best model. All methods yielded similar results. To evaluate whether the relationship between nest success and distance to forest edge was independent of bird species, log-linear models were Wtted to three-way contingency tables for all species. For all logistic regression analyses, we used simple nest fate (success D 1 or failure D 0; unoccupied D 1, occupied D 0), either from a Wrst or a repeated nest. In all logistic regression models, we used an information-theoretic approach and calculated Akaike’s Information Criterion (AIC) based on log-likelihood values to identify the best models (Burnham and Anderson, 1998). The model with the smallest AIC is the best approximating model for the data. All statistical analyses were conducted using SAS (1990).
3. Results 3.1. Nest success by distance to forest edge A total of 439 cavity nests of four species were located and monitored during 1998–2001 (Table 1). Of this total, 422 nests were entered into our analysis of edge eVects. Nests abandoned before egg laying (n D 12) or of uncertain outcome (n D 5) were excluded from analyses. Nest success rates of each cavity-nesting bird did not vary between years (2 D 6.13, df D 3, P D 0.11) and plots (2 D 9.08, df D 5, P D 0.91). However, nest success rates among species within years were signiWcantly diVerent. Nest success varied among individual species, with the lowest value for yellow-rumped Xycatcher and the highest for grey-faced woodpecker (Table 2). On all six plots, excavator species had higher nest success than non-excavator species (Table 2). For four years of pooled data, nest success was lower in the 0–200 m zone than in the 201–500 m zone from the forest edge for the nonexcavators (2 D 6.94, df D 1, P < 0.01), but not for excavators (2 D 2.89, df D 1, P D 0.09). Logistic regression models including a distance to forest edge variable provided a better Wt to nest fate data for the yellow-rumped Xycatcher and the great tit (Table 3), but not for the great spotted woodpecker and the grey-faced woodpecker. The best models for yellow-rumped Xycatcher
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Table 1 Nest fates of cavity-nesting birds in Zuojia Nature Reserve, Northeastern China, 1998–2001 Species and year
Total nests in analysis
Total nests failed
Number (percentage) of nest failures, by cause Occupationa
Yellow-rumped Xycatcher 1998 1999 2000 2001 All years
19 27 26 23 95
9 12 10 7 38
7 (78) 6 (50) 7 (70) 5 (71) 25 (66)
Great tit 1998 1999 2000 2001 All years
18 21 20 25 84
8 9 5 10 32
5 (62) 7 (78) 3 (60) 5 (50) 20 (63)
Great spotted woodpecker 1998 1999 2000 2001 All years
26 27 31 34 118
2 6 4 5 17
4 (67) 3 (75) 5 (100) 12 (70)
Grey-faced woodpecker 1998 1999 2000 2001 All years
28 30 35 32 125
2 3 5 4 14
2 (100) 2 (67) 3 (60) 3 (75) 10 (72)
a b c
Abandonmentb
Predation 2 (22) 2 (17) 3 (30) 7 (16) 2 (25) 1 (20) 2 (20) 5 (16)
Uncertainc
3 (25)
1(8)
2 (25) 5 (13)
1 (5)
1 (13) 2 (22) 1 (20) 1 (10) 5 (16)
2 (20) 2 (5)
2 (100) 2 (33) 1 (25) 4(24)
1 (6)
1(20)
1 (20)
1 (7)
1 (7)
1 (33) 1(25) 2 (14)
Nests were re-occupied by another species after laying. Abandonment prior to laying. If cues were not available to determine success or failure.
Table 2 Nest success estimates of cavity-nesting birds in Zuojia Nature Reserve, northeastern China, 1998–2001 Species Yellow-rumped Xycatcher Great tit Great spotted woodpecker Grey-faced woodpecker a b c
Nest success § SEa 1998
1999
2000
2001
All yearsb
0.67 § 0.08 (19)c 0.72 § 0.12 (18) 0.86 § 0.03 (26) 0.91 § 0.02 (28)
0.64 § 0.06 (27) 0.69 § 0.09 (21) 0.83 § 0.05 (27) 0.88 § 0.06 (30)
0.71 § 0.11 (26) 0.79 § 0.06 (20) 0.69 § 0.17 (31) 0.84 § 0.09 (35)
0.66 § 0.04 (23) 0.66 § 0.12 (25) 0.87 § 0.04 (34) 0.90 § 0.11 (32)
0.67 § 0.09 (95) 0.73 § 0.10 (84) 0.84 § 0.04 (118) 0.89 § 0.10 (125)
MayWeld (1961, 1975) nest success values calculated from exposure. 2 comparison of diVerences species for all years nest success (P > 0.05). Number of nests.
included just the single predictor log distance to forest edge, but for great tits, log distance and year were the predictors that produced the best-Wtting model (Table 3). The probability of failure for yellow-rumped Xycatcher nests decreased with increasing distance to the edge in a roughly linear function (Fig. 1), but this trend was not apparent for other cavity-nesting species. 3.2. Causes of nest failure Potential predators on cavity-nesting birds (eggs, nestlings, adults) that were observed on the study plots during four years were Eurasian sparrow hawk (Accipiter nicus), besra sparrow hawk (Accipiter virgatus), longeared owl (Asio otus), Siberian weasel (Mustela aibirica),
Siberian chipmunk (Tamias sibiricus), and beauty snake (Elaphe taeniura). The white-cheeked starling (Sturnus cineraceus) was the most important nest-site competitor for the four cavity-nesting bird species. A total 101 failure nests occurred in our analyses. Failed nests were often a results of nest-site competitors (competitors which accounted for 68% of such losses). Occupation rate by nest-site competitors was higher (66%, n D 46) during the egg period than during the nestling period (34%, n D 22). Seventy percent of nests lost to competitors were lost to white-cheeked starlings. In contrast, nest predation only accounted for 20%. The four species also suVered from nest site occupation by the white-backed woodpecker (Picoides leucotos) and sometimes by Siberian chipmunk. Also, the occupation rate
W.-H. Deng, W. Gao / Biological Conservation 126 (2005) 363–370
AIC
Yellow-rumped Xycatcher FDC 1 FDC+D 2 F D C + LD 2 F D C + LD + Y 3 F D C + LD + P 8 F D C + LD + P + Y 9
¡81.32 ¡78.26 ¡77.49 ¡77.28 ¡76.11 ¡73.37
164.64 160.52 158.98 160.56 168.22 164.74
Great tit FDC FDC+D F D C + LD F D C + LD + Y F D C + LD + P F D C + LD + P + Y
¡65.43 ¡64.26 ¡64.11 ¡63.05 ¡61.57 ¡59.44
132.86 132.52 132.22 132.10 139.14 136.88
1 2 2 3 8 9
F indicates nest fate; C indicates constant; D indicates distance to forest edge; LD indicates log10 (D); Y indicates studying years; P indicates plots; AIC indicates Akaike’s Information Criterion. F D C + LD is the best Wt for the yellow-rumped Xycatcher; F D C + LD + Y is the best Wt for the great tit.
by the white-cheeked starlings was signiWcantly greater for the yellow-rumped Xycatcher in the 0–200 m zone than the 201–500 m (2 D 5.16, df D 1, P D 0.02). Nest predation did not follow this same trend (2 D 1.18, df D 1, P D 0.29) when comparing between the two zones. Lastly, we did not Wnd nest parasitism in this study.
4. Discussion
Nest success
Log-likelihood
yellow-rumped flycatcher
0.8
0.6 25
21
14
19
16
0.4 1
Nest success
Number of parameters
great tit
0.8
0.6 23
20
12
16
13
0.4
great spotted woodpecker 1
Nest success
Models
1
0.8 0.6
31
26
22
19
20
0.4
grey-faced woodpecker 1
Nest success
Table 3 Logit transformation models of the nest fate for the yellow-rumped Xycatcher and great tit during four breeding seasons in northeastern China
367
0.8
0.6
29
39
12
22
23
0.4
4.1. Edge eVects on cavity-nesting birds We found some evidence for an edge eVect on nesting success of cavity-nesting species near anthropogenic edges, especially for nonexcavator species. Our results concur with Wndings from several recent studies on open-cup nesting species (Flaspohler et al., 2001; Manolis et al., 2002). Our results are also consistent with Wndings from several studies of cavity-nesting birds. Denny and Summers (1996) found that cavity birds were aVected by edge-related factors. Huhta and Jokimaki (2001) found pairing success and nesting success of two hole-nesting passerines, the pied Xycatcher (Ficedula hypoleuca) and the cavity-nesting redstart (Phoenicurus phoenicurus), were aVected by proximity to edge. However, Matthysen and Adriaensen (1998) reported that reproductive success of the great tit was not aVected by forest fragmentation in western Europe. Most early studies of edge-related nest success of avian species suggested that high nest predation and parasitism rates were main causes of high nest failure near edges (Gates and Gysel, 1978; Gibbs, 1991; Eriksson et al., 2001; Manolis
0-100
101-200
201-300
301-400
401-500
Distance to edge (m) Fig. 1. MayWeld nest success for the four cavity-nesting species in relation to distance to the forest edge in Zuojia Nature Reserve, Northeastern China, 1998–2001. The number of nests used to estimate nest success is given inside each histogram bar.
et al., 2002). However, in our study, the main cause of nest failure near edges was not nest predation or parasitism, but rather, competition for nest sites among cavity nesters. We also found that the rate of nesting success of yellow-rumped Xycatcher and the great tit increased with distance from the edges, but the great spotted woodpecker and the grey-faced woodpecker did not follow the same trend. This indicates local scale habitat perturbations can have species-speciWc eVects on nesting success of cavity-nesting birds. Several ideas have been proposed to explain the absence of edge-related nest predation in forested landscapes. Angelstam (1986) suggested that edge-related nest predation rates could be explained by diVerences in productivity of the adjacent habitats. This explanation
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indicated that an edge eVect on nest predation is most likely to occur where there is a steep gradient in primary productivity across the edge and is least likely to occur where this gradient is less pronounced (Lahti, 2001). Lack of predation may also occur if there is no increase in prey density along edges or if predators are habitat specialists (i.e., they do not move between habitats and cross edges) (Rodewald, 2002). Morrison and Bolger (2002) suggested that the lack of edge eVect on nest predation rate of Rufous-crowned Sparrow (Aimophila ruWceps) appeared to be due to a lack of edge sensitivity of snakes. Excavator species (the great spotted woodpecker and the grey-faced woodpecker) had signiWcantly higher nest success than nonexcavator species (the yellow-rumped Xycatcher and the great tit). Nonexcavator species are generally smaller than excavator species. This smaller size may reduce ability to compete for high quality nests. Nonexcavator species may have had relatively low nest success in part because they tend to nest in old cavities and nest closer to the ground (Sonerud, 1985; Li and Martin, 1991). 4.2. Nest-site competitors Numerous studies of avian reproductive success have concluded that the destruction of eggs and nestlings by predators is the most signiWcant inXuence on avian nest success (Askins, 1995). But in our results, nest predation was not the main causes of nest failures and accounted for only 20% of all nest failures. Most of the failed nests (68%) were attributable to nest-site competitors. Indeed, nest takeovers by the white-cheeked starlings were common both in edge and interior habitats. A potential cost of cavity-nesting birds is increased competition for nest sites, especially for nonexcavator species. Raphael and White (1984) found a signiWcant correlation between cavity density and nonexcavator species density in the coniferous forests of the Sierra Nevada, suggesting densities were limited by nest site availability. In our study area, because the forest age was only about 40 years, lack of natural tree cavities probably was the main reason for drastic competition among the species, although we did not investigate cavity resources throughout the study area. Some researchers found that some cavity-nesting birds prefer edges and open understories in forested landscapes (Belles-Isles and Picman, 1986; Finch, 1989). Dobkin et al. (1995) explained that birds that use multiple habitat types might nest on edges to reduce commuting time between resources. Cavity nesters may select nest sites with open understories to increase their ability to detect approaching predators (Finch, 1989). We did not Wnd the same phenomenon during our study period. The number of cavity nests was roughly equal between edge and interior habitat.
Brush (1983) observed Xycatchers, starlings, and other species competing for nest cavities, but the starlings had no eVect on other species because abundant alternate nest sites were available. However, the potential for interference competition seems greatest in habitats where nest sites are limited, as was the case in our studies. Weitzel (1988) reported that starlings were serious competitors for certain native birds in Nevada. Kerpez and Smith (1990) found evidence for competition and a negative relationship between starlings and gila woodpeckers (Melanerpes uropygialis) in Arizona. Ingold (1998) suggested that the European Starling (Sturnus vulgaris) was having a signiWciantly adverse eVect on the reproductive success of northern Xickers (Colaptes auratus). Despite these clear examples of starling having detrimental eVects on many cavity-nesting species, Koenig (2003) did not Wnd that starlings had had a severe impact on populations of native cavity-nesting birds in a study of 27 species in America. Starlings may nest in forest, but they do not feed in forests (Feare, 1984). They commute to open habitats from their nest sites where they forage, just as does the brown-headed cowbird (Molothrus ater) of North America. It seems likely that starlings prefer to nest near edges because it reduces their travel costs from their breeding areas to their feeding areas. Like the parasitic cowbird phenomenon, this is a clear example of a situation in which the matrix surrounding a fragment directly aVects birds nesting within the fragment. The disturbed landscape supports a nest “pirate” that depends on the matrix for food, but nest in forests. Our results suggest that local land-use practices or natural events can have a profound inXuence on the nesting success of birds that depend upon disturbed habitats for nesting. Our results also suggest that forest management strategies should consider not only stands in forest planning, but also the edges.
Acknowledgments We thank Yan-Hui Li, Yang Liu, Zheng-Xin Sun, Ren-Kai Song, Gui-Quan Xiang, Hai-Tao Wang, JingRun Cheng, Nan Li, Quan Zhao, and Long Sun for their involvement in the collection of Weld data. We thank the teachers and students who are in Department of Wildlife, Special Plant and Animal College that they found and monitored the success of the nests. Members of the ecology team, Beijing Normal University, were extremely patient and helpful in providing assistance with data analysis. We thank fund of National Nature Science of China to support this research (No. 30470300). We also thank anonymous reviewers for their helpful and excellent remarks on this paper.
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