Livestock grazing, plateau pikas and the conservation of avian biodiversity on the Tibetan plateau

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Livestock grazing, plateau pikas and the conservation of avian biodiversity on the Tibetan plateau Anthony D. Arthura,*, Roger P. Pecha,1, Chris Daveya, Jiebub, Zhang Yanmingc, Lin Huid a

CSIRO Sustainable Ecosystems, GPO Box 284, Canberra ACT 2601, Australia Tibet Academy of Agriculture and Animal Sciences, Lhasa, Tibet 850023, People’s Republic of China c Northwest Plateau Institute of Biology, Chinese Academy of Sciences, Xining, Qinghai 810001, People’s Republic of China d Tibet Bureau of Agriculture and Animal Husbandry, Lhasa, Tibet 850000, People’s Republic of China b

A R T I C L E I N F O

A B S T R A C T

Article history:

On the Qinghai–Tibet plateau increased livestock numbers have resulted in degradation of

Received 8 January 2008

the grasslands with potential impacts on native biodiversity. Concurrently, perceived

Received in revised form

increases in populations of native small mammals such as plateau pikas (Ochotona curzoniae)

15 May 2008

have led to poisoning programs, with uncertain impacts on species such as ground-nesting

Accepted 17 May 2008

birds. We explored the relationships between the local seasonal abundance of small birds

Available online 7 July 2008

and (1) the density of pika burrows; (2) livestock grazing practices; and (3) local poisoning of pikas. Around Naqu prefecture, central Tibet, we used a nested experimental design to

Keywords:

collect data from areas rested from grazing over summer, nearby areas with year-round

Snowfinch

grazing and areas subjected to pika poisoning. Additional data were collected from a site

Burrow

where grazing had not occurred for at least 4 years prior to the study. Poisoning pikas in

Ground-nesting

spring had no detectable effect on the local abundance of birds the following autumn. How-

Grassland

ever, two ground-nesting species, white-rumped and rufous-necked snowfinches, showed

Passerine

positive associations with the density of pika burrows, indicating that long-term pika poisoning could reduce the density of these species by reducing the density of pika burrows. Rufous-necked snowfinches and non ground-nesting species including horned larks and common hoopoes showed positive responses to reduced grazing pressure from livestock, particularly in the long-rested site, indicating current grazing levels could be having a negative impact on these species. Conservation of small passerine biodiversity in this system will require changed management practices for livestock and pikas that consider the complex three-way interaction between livestock grazing, pikas and small birds.  2008 Elsevier Ltd. All rights reserved.

1.

Introduction

Livestock grazing has major impacts on native biodiversity throughout the world (Milchunas et al., 1998; Fuller and Gough, 1999; Martin and Possingham, 2005). Birds seem particularly susceptible to the changes that occur when grazing

pressure increases, with proposed mechanisms including loss of preferred vegetation type and structure, alteration of food supplies and alteration of predation pressure. The high alpine grasslands of the Qinghai–Tibetan plateau have supported pastoralism of domesticated yaks (Bos grunniens) and Tibetan sheep (Ovis aries) for approximately 2200

* Corresponding author: Tel.: +61 2 6242 1793; fax: +61 2 6242 1565; mobile: + 61 419 402 278. E-mail addresses: [email protected] (A.D. Arthur), [email protected] (R.P. Pech), [email protected] (C. Davey), [email protected] ( Jiebu), [email protected] (Z. Yanming). 1 Present address: Landcare Research, P.O. Box 40, Lincoln 7640, New Zealand. 0006-3207/$ - see front matter  2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2008.05.010

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years (Goldstein and Beall, 1990; Miller, 1995). In recent decades numbers of livestock have increased rapidly (Jing et al., 1991; Dong et al., 2004) and grassland degradation characterised by reduced above-ground plant biomass, loss of the hard turf layer leading to exposure of loose subsoil and an increase in the prevalence of toxic plants, has become a major problem on the plateau (Lang et al., 1997; Zhang et al., 1998; Zhou et al., 2005). During this period the abundance of medium-to-large native mammals has been greatly reduced (MacKinnon et al., 1996), while outbreaks of indigenous small mammals such as plateau pikas (Ochotona curzoniae), plateau zokors (Myospalax fontanierii), plateau voles (Pitymys irene), and Himalayan marmots (Marmota himalayana) are thought to have increased (Liu et al., 1991; Fan et al., 1999). In other words, some components of this natural ecosystem have suffered, while others may have benefited from increased grazing. The indigenous small mammals have come to be regarded as pests, competing with livestock for scarce food resources and contributing to soil erosion by burrowing (Liu et al., 1980; Xia, 1984; Fan et al., 1999). In response, extensive poisoning programs using poisons such as zinc phosphide, NHþ 4 -fluoroacetate, anticoagulants and most recently botulin toxin C have been used to control them on the Tibetan plateau since 1958 (Fan et al., 1999). Plateau pikas in particular have been targeted by control programs, which in some areas have resulted in populations being reduced to less than 5% of their pre-controlled densities (Lai and Smith, 2003). Plateau pikas (hereafter called pikas) are small lagomorphs (approximately 120–170 g for females and 150–210 g for males) endemic to parts of the Tibetan Plateau (Zhang et al., 1998; Smith and Foggin, 1999; Bagchi et al., 2006). They are social animals that tend to be spatially clumped (Smith and Wang, 1991; Zong et al., 1991) and can reach very high population densities of >350 ha1 (Wang et al., 1997). They are typically diurnal and interact with their environment through foraging and digging activities and by recycling nutrients, which contributes to plant community dynamics; as prey for a suite of top predators; and by constructing burrows that are used as shelter and nest sites by other species (Zhang, 2002; Lai and Smith, 2003; Zhang et al., 2005; Bagchi et al., 2006). Predatory species, such as the upland buzzard (Buteo hemilasius), and ground-nesting species which use pika burrows such as Hume’s groundpecker (Pseudopodoces humilis), white-rumped snowfinch (Pyrgilauda taczanowskii) and rufous-necked snowfinch (P. ruficollis) appear to suffer negative impacts from pika control programs, which has led to suggestions that plateau pikas are a keystone species with a pivotal role in the community dynamics of these high-altitude grasslands (Smith and Foggin, 1999; Lai and Smith, 2003). Hence, on the Qinghai–Tibetan plateau livestock grazing may advantage some bird species by promoting increases in pika populations and their burrows, while disadvantaging others by removing food or altering the physical structure of the grasslands. In this paper we use data collected on the abundance of small birds in one spring and two autumns at 17 sites in Naqu County, central Tibetan plateau (altitude ca. 4500 m) to assess whether abundance or presence was related to pika burrow density or to vegetation characteristics generated by different livestock grazing practices. The most common passerines ob-

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served on all occasions were snowfinches, particularly whiterumped snowfinches and rufous-necked snowfinches, which are burrow nesters and predominantly eat seeds and small insects (Clement, 1999). All other species were observed in small numbers and/or inconsistently across the three sampling occasions. They included Hume’s groundpecker, a burrow/cavity nester that eats ground insects and larvae; common hoopoe (Upupa epops) which also eats ground insects and larvae; and Richard’s pipit (Anthus richardi) and horned lark (Eremophila alpestris) which feed on insects and seeds. We used paired sites for our grazing practice treatment (continuous vs. summer-rested at most sites) and pika burrow densities across the sites ranged from ca. 400 to 2300 (Pech et al., 2007). Fencing is now used by local people to restrict grazing of short alpine meadow over summer in some areas, which results in an increase in sward height by September, compared with other areas that are grazed continuously (Pech et al., 2007). By the end of winter almost all above-ground biomass has been removed in both areas but there are still detectable differences between continuously grazed and ‘summer-rested’ areas (Pech et al., 2007). With these data we used a model selection and inference approach (Burnham and Anderson, 1998) to assess support for the following hypotheses and associated predictions (more detailed descriptions of the a priori specified models tested are shown in Table 1): In spring, at the start of the breeding season, the birds are associated with their breeding territories/areas rather than occurring in flocks and hence: 1. Burrow nesting birds are limited by the availability of pika burrows. The relationship between bird density and burrows could be: (i) directly linear increasing – no other resource becomes limiting over the range of burrow densities observed; (ii) asymptotic – bird density increases up to a point where some other resource not influenced by pikas becomes limiting. 2. Burrow nesting birds are limited by resources (most likely food) and hence more birds will be found in summerrested areas than in continuously grazed areas. 3. Burrow nesting birds are limited by interactions between burrows and resources. We tested this with a range of interaction models which are described in detail in Table 1. 4. Birds that do not nest in burrows will be associated with greater food resources and hence they will occur at higher densities or be detected more commonly in summerrested areas than in continuously grazed areas. In autumn, at the end of the breeding season, snowfinches begin to form flocks (Clement, 1999). It is not known whether or how far snowfinches move from their breeding areas, but species such as the white-winged snowfinch (Montifringilla nivalis) are known to move away from breeding areas over winter (Cramp 1994). In our study white-rumped snowfinches still appeared to be associated with their breeding areas in both autumns. Rufous-necked snowfinches had begun to form flocks, particularly in the second autumn. We do not know whether the birds in flocks were associated with their breeding sites or not, so we tested the same set of hypotheses

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Table 1 – A priori specified models for the density of birds seen on the sites derived from the hypotheses and predictions in the introduction Model

Model description

Burrow

Linear relationship between bird density and spring burrow count. For autumn bird data the burrow count from the preceding spring was used because this reflects the burrows available when breeding commences Different bird densities between continuously grazed and ‘summer-rested’ areas Standard interaction model Standard additive model Asymptotic relationship between bird density and spring burrow count where: asym is the maximum density reached; lrc is the log of the rate constant which determines the shape of the relationship (log used to enforce positivity of the estimated rate constant); and Co is the burrow count below which the density of birds is zero Different maximum density depending on grazing ‘treatment’ Different shape depending on grazing ‘treatment’ Different burrow count below which the density of birds is zero depending on grazing ‘treatment’ Different densities in the following autumn on sites where pikas were poisoned in spring vs. sites where pikas were not poisoned Standard interaction model Standard additive model Intercept only model

Graze

Burrow · Graze Burrow + Graze asym (1-exp(-lrc(Burrow-C0)))

asymgraze (1-exp(-lrc(Burrow-C0))) asym (1-exp(-lrcgraze(Burrow-C0))) asym (1-exp(-lrc (Burrow-C0 graze))) Poison

Burrow · Poison Burrow + Poison Null

and predictions as those in spring considering (i) only birds not seen in flocks; and (ii) all birds seen. During the study pikas were poisoned on some of the sites by local people with once-off application of botulin toxin C distributed on wheat bait in spring (Pech et al., 2007). This control produced immediate pika population reductions of over 90%, but populations recovered rapidly over the following summer, returning to uncontrolled densities by autumn (Pech et al., 2007). While pika populations recovered, pika burrow counts in the autumn following poisoning were 33% lower than in the spring when poisoning occurred (Pech et al., 2007). Poisoning was carried out after we counted birds in spring, and birds were not counted immediately after poisoning. If poisoning had a direct impact on birds and if local populations at poisoned sites could not recover before the following autumn (most likely through immigration), then we expected to see lower populations on poisoned sites. This was an additional prediction tested with autumn data (Table 1). Finally, we also collected data at a unique site where livestock grazing had not occurred for 4 years when the study

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commenced. While this part of the study could not be replicated, we consider these data less formally as a possible indicator of what much lower livestock grazing pressure might mean to the avian biodiversity of the plateau.

2.

Methods

2.1.

Study site and design

The Tibetan Plateau occupies 2.5 million km2 in the southwest of the People’s Republic of China, approximately 25% of the country’s area with an average elevation >4000 m. An estimated 70% is high altitude grassland and pastoralism is the primary land use (Ekvall, 1968; Miller, 1995; Miller and Craig, 1997). The climate is strongly seasonal with an annual mean temperature <0 C (Xia, 1988). There is no frost-free season and extensive areas of permafrost occur in mountains and grasslands (Smith et al., 1986). Principal soil types are Mat Cryic Cambisols and Mol Cryic Cambisols (CSTC, 1995). The major plant communities are alpine meadow, alpine shrub, alpine prairie and alpine steppe meadow and the dominant forms are Carex spp., Kobresia spp., Stipa spp., Achantherum splendens, and Potentilla fruticosa (Xia 1988). This study was conducted near Naqu (elevation 4500– 4600 m), approximately 330 km north of Lhasa, the capital of the Tibet Autonomous Region, from April 2004 to September 2005 (Pech et al., 2007). At Naqu the mean annual temperature is 1.9 C (ranging from 22.6 C in July to 41.2 C in January), and the mean annual precipitation is 430 mm, 70% of which occurs between June and August. Personnel from the local Grassland Station provided assistance in selecting study sites where (1) pikas were perceived to be a problem; (2) the history of pika control was known; and (3) pika control could be applied by local villagers during the period of our study. All study sites consisted of gently undulating terrain with low, sparse alpine meadow comprised mainly of Kobresia capollifolia grazed by yaks and Tibetan sheep. They had limited amounts of wetter areas where the dominant species is the longer, coarser Stipa purpurea; in areas dominated by this habitat type pikas are not considered a problem by local people. Plateau pika densities in autumn ranged from 30 to 50 ha1 (Pech et al., 2007), while counts of their predators during road-based surveys, particularly upland buzzards where counts ranged from 21 to 35 per 100 km, indicated the study sites were representative of the general area around Naqu (Arthur et al., 2007). Nine sites were identified with varying histories of pika control (Table 2). Maps of the study area are shown in Pech et al., 2007. At each site, with one exception, we selected paired areas: one area inside a paddock fenced to conserve forage for winter grazing, which we refer to hereafter as ‘rested’, and one area outside the paddock where there is year-round grazing by livestock, which we refer to hereafter as ‘continuously grazed’ (Table 2). At site 1 there was no ‘continuously grazed’ area with pika control to match the rested area. We also found one site (Site 7), where grazing by livestock had not occurred for at least 4 years prior to the study. Each core area which was used for gathering data was ca. 15 ha and was located at least 40 m from the fence separating

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Table 2 – Sites for monitoring plateau pika populations, birds and alpine meadow in areas with different histories of pika poisoning Site number

Grazing treatmenta

1 2b

Rested Rested Continuous Rested Continuous Rested Continuous Rested Continuous Rested Continuous Rested for P4 years Continuous Rested Continuous Rested Continuous

3 4 5 6 7c 8 9

Pika control

Pika burrows ha1 (April 05)

2003 2002 2002 none none 2005 2005 none none 2002, 2005 2002, 2005 2003 2003 2004 2004 2004 2004

455 835 410 1510 810 1605 1425 2285 2010 925 870 1460 655 1600 1000 1365 1045

Maps of the site locations are available in Pech et al. 2007. a Rested areas are grazed only in winter and continuous areas are grazed year-round. b The two areas at this site were not immediately adjacent to each other. c There was a unique paddock at this site that had been ungrazed by livestock for at least 4 years.

rested and continuously grazed areas. Pikas were controlled on sites 8 and 9 in the spring of 2004 and on sites 4 and 6 in the spring of 2005 using botulin C on wheat bait placed down pika burrows (Pech et al., 2007) (Table 1). Control was applied by villagers under the direction of staff from the Naqu Grasslands Station over ca. 35 ha either side of the fences separating continuously grazed and rested areas to ensure it extended beyond each core area of ca. 15 ha. For each core area we counted the abundance of plateau pikas (results presented in Pech et al., 2007) in April and September 2004 and in April and September 2005, the abundance of pika burrow entrances in April and September 2005, and the abundance of birds in September 2004 and in April and September 2005. We also assessed the vegetation in each area in April and September 2004 and in April and September 2005.

2.2. Counts of birds, plateau pika burrows and assessment of vegetation Birds were counted during 3 ‘sessions’, one in spring (17–25 April 2005) and two in autumn (10–15 September 2004, 13–21 September 2005). The spring count preceded the pika control carried out in April 2005; we did not have the resources to do an immediate post-control count of birds to look for immediate non-target effects on birds. Walked transects were used to measure the abundance of birds, identified to species, in the core areas. They were conducted simultaneously by two observers, one in the continuously grazed area and the other in the rested area at a site, from midday to early afternoon. Each observer counted all birds in a 50 m wide (25 m either side of centre line) by 1 km long belt transect comprised of

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10 approximately contiguous 100 m long straight sections, for each core area. As an example, a sample could involve three contiguous sections heading north, a fourth section heading approximately east which started 30–50 m away from the end of the previous section to avoid sampling the same area twice, three sections heading approximately south, another section heading approximately east and two final sections heading approximately north. The exact direction chosen in each case was based on locating a distant fixed object to ensure the observer walked in a straight line. Birds were observed easily in the relatively flat terrain with vegetation sward height generally much less than 3 cm, so we assumed all birds within the strip were observed to derive a density estimate for presentation of results (count per unit area). For each session, the birds in each area were counted on two occasions, once by each of the two observers to account for observer bias. However, we found no evidence of observer bias in the collected data. The exact location of each walked transect was not fixed but followed the same general route on each occasion. Similarly, belt transects of 10 contiguous 4 m · 100 m strips were use to count burrow entrances at each core area in April and September 2005. The step-point technique (Evans and Love, 1957) was used to measure the percentage cover of vegetation, vegetation litter and bare soil at each site in April and September 2004, and in April and September 2005. At least 400 step-point readings were recorded at each core area. Each point was two steps apart, i.e. with a spacing of 1.0–1.5 m. Each point was assigned to an exclusive category of either ‘vegetation’, which included dry grass stems still attached to the roots, ‘litter’, which included all detached plant material lying on the surface and ‘bare soil’, which included stones, small rocks and cryptogam or lichen crusts on the surface. After each set of 10 step points, the height of the sward within 1 m of the observer was estimated at that point. A training period was conducted at the start of each session to ensure consistent use of these categories and measurement protocols by observers.

2.3.

Analyses

We used a model selection and inference approach to assess the support for the predictions (Burnham and Anderson, 1998). Each model shown in Table 1 was fitted as model + error assuming normally distributed errors, with adjusted Akaike information criteria (AICc) calculated from the minimised negative log-likelihood using standard formulas (Burnham and Anderson, 1998). Residuals were checked to ensure that normal errors were appropriate for the data. The probability of each model conditional on both the data and all models in the set was calculated as described in Burnham and Anderson (1998). Models were fitted in program R (R Development Core Team, 2007).

3.

Results

3.1.

Effect of grazing practices on vegetation structure

There was less bare ground in autumn following the growing season than in early spring (F4,48 = 76.73, P < 0.0001), and less

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bare ground in rested areas than in continually grazed areas (F1,5 = 13.9, P = 0.014; Fig. 1a). On average, vegetation sward was taller in autumn following the growing season than in spring (F3,58 = 521.0, P < 0.0001), and taller in rested areas than in continually grazed areas (F1,5 = 18.21, P = 0.008; Fig. 1b). The area that had not been grazed by livestock for four years prior to the start of our study had much less bare ground than other areas in spring 2004, less bare ground than other areas in spring 2005 and a slightly taller sward than average in both springs (Fig. 1). In autumn 2004 the sward there was over twice the height compared with areas rested over summer only, while the amount of bare ground was about the same (Fig. 1). This area was grazed over the summer of 2005, so that by the autumn of 2005 the sward was as low as continuously grazed areas, but there was still less bare ground than in continuously grazed areas (Fig. 1).

a

80 70

Bare ground (%)

60

3.2.

General observations on birds

The most common species of bird seen across the sites was the white-rumped snowfinch with average seasonal densities ranging from 2 to 3 ha1. Average seasonal densities of rufous-necked snowfinches ranged from 0.5 to 1.2 ha1. In general these species were not observed in flocks, except the rufous-necked snowfinch for which 41% of the total count in both spring 2005 and autumn 2005 was made up of birds in flocks. All other species had average seasonal densities less than 0.25 ha1. Plain-backed snowfinches (P. blanfordi) were only seen in low densities in autumn, with most observations in autumn 2005. Tibetan snowfinches (Montifringilla adamsi) were only seen in low densities in spring 2005, with one flock of eight accounting for the majority of the records. Hume’s groundpeckers and Richard’s pipits (Anthus richardi) were seen in low densities in autumn 2004, and very rarely in autumn 2005. Horned larks (Eremophila alpestris) were seen at low densities in all sessions while common hoopoes (Upupa epops) were seen at low densities in both autumns. Two white wagtails (Motacilla alba) and one Saker falcon (Falco cherrug) were also seen at the sites. Upland buzzards were observed commonly around all sites (C. Davey, R. Pech and T. Arthur, personal observations).

3.3. Relationships between the abundance of snowfinches and burrows, grazing, or pika control

50 40

3.3.1.

30 Rested

20

Continuously grazed 10

Rested for 4 years

0 April 04

b

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Sept 04

April 05

Sept 05

60 Rested

Spring densities (start of breeding season)

Only white-rumped snowfinches and rufous-necked snowfinches were seen in sufficient densities for analyses. Models with a positive relationship between the density of whiterumped snowfinches and pika burrows were overwhelmingly supported compared with the null model (Table 3 and Fig. 2). There was some evidence that for a given density of burrows, slightly higher densities of white-rumped snowfinches were present in summer-rested areas compared with areas grazed continuously by livestock (Table 3 and Fig. 2). Densities in the long-rested area were consistent with densities in summer-

50

Sward height (mm)

Continuously grazed 40

Table 3 – Model selection table for the relationship between snowfinch density and explanatory variables in spring 2005

Rested for 4 years 30

20

10

0 April 04

Sept 04

April 05

Sept 05

Fig. 1 – (a) The percentage of bare ground and (b) the average height of the sward, in grazed and rested areas throughout the study. Symbols indicate points when data were collected. Black symbols are from the statistical models. Rested areas were grazed by livestock mostly during winter and rested over summer. Grey symbols are from the area at site 7 where grazing had not occurred for four years prior to the start of the study; the area was grazed between April 2005 and September 2005.

Rank Model

N AICc

White-rumped snowfinch 1 Burrow 2 Burrow + Graze 3 asym(1-exp(-lrc(Burrow-C0))) 4 Burrow · Graze 5 asymgraze(1-exp(-lrc(Burrow-C0))) 6 asym(1-exp(-lrcgraze(Burrow-C0))) 7 asym(1-exp(-lrc(Burrow-C0 graze))) 8 Null 9 Graze

3 4 4 5 5 5 5 2 3

DAICc xi

114.28 0.00 117.24 2.96 118.09 3.81 118.57 4.29 120.20 5.92 120.24 5.96 121.93 7.65 123.47 9.19 124.97 10.69

0.61 0.14 0.09 0.07 0.03 0.03 0.01 0.01 0.00

N, number of parameters; AICc, Akaike information criteria adjusted for sample size; DAICc, the difference between the model and the ‘best’ model; xi, Akaike weight or probability of the model given the data and the models in the set. Parameters and variables are defined in Table 1.

White-rumped snowfinches ha -1(April 2005)

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Table 4 – Model selection table for the relationship between snowfinch density and explanatory variables in autumn 2005

5

4

3

2

1

0 0

500

1000

1500

2000

2500

Pika burrows ha-1(April 2005)

Fig. 2 – Observed (open symbols) and predicted (line) density of white-rumped snowfinches ha1 in spring (April 2005). The solid line is the most supported model (Burrow; Table 3). The line of large dashes is for summer-rested areas and the line of small dashes is for continually grazed areas (Model 2: Burrow + Graze; Table 3). The single closed square symbol is for the long-rested site which was not included in model selection. rested areas (Fig. 2). For rufous-necked snowfinches there was no clear pattern with the null model receiving three times the support of the next best model. In the long-rested area there were 5.8 rufous-necked snowfinches per hectare, which was over seven times the density of any other site. The estimate included a flock of eight and one of 30, while no flocks were observed in any other sites at this time.

3.3.2.

1977

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Autumn densities (end of breeding season)

We had two separate autumn counts to analyse. For autumn 2004 we did not have pika burrow counts from the preceding spring and we had to use the burrow counts from spring 2005 in this analysis. Given that pika poisoning was shown to reduce the count of burrows by 33% between spring 2005 and autumn 2005 (Pech et al., 2007) it is possible the burrow counts from spring 2005 did not accurately reflect the burrows available in spring 2004 for those sites poisoned in spring 2004. For autumn 2005 we had pika burrow counts from the preceding spring. Hence we consider the autumn 2005 data to be more reliable, while the 2004 data are presented as supporting evidence for the relationships indicated by the 2005 data. Models with a positive relationship between the density of white-rumped snowfinches and pika burrows were overwhelmingly supported for 2005 compared with the null model (Table 4 and Fig. 3a) while there was weaker support for a similar positive relationship in 2004 (Table 5 and Fig. 3b). Densities in the long-rested area were consistent with densities in summer-rested areas (Fig. 3a and b). For rufous-necked snowfinches three of the top four models, including the top two, indicated a positive relationship between their density and the density of pika burrows in summer-rested areas, but low densities in areas continually grazed by livestock (Table 4 and Fig. 4). However, the relationship was only evident when all birds, including those in flocks, were included. When birds in flocks were excluded no clear relationship was evident with the null model receiving three times the support

Rank Model

N AICc

White-rumped snowfinch 1 asym(1-exp(-lrc(Burrow-C0))) 2 Burrow 3 asym(1-exp(-lrc(Burrow-C0 graze))) 4 Null 5 asym(1-exp(-lrcgraze(Burrow-C0))) 6 Burrow + Graze 7 Burrow + Poison 8 asymgraze(1-exp(-lrc(Burrow-C0))) 9 Poison 10 Graze 11 Burrow · Poison 12 Burrow · Graze

4 3 5 2 5 4 4 5 3 3 5 5

Rufous-necked snowfinch (including birds in 1 asym(1-exp(-lrcgraze(Burrow-C0))) 2 asymgraze(1-exp(-lrc(Burrow-C0))) 3 Burrow 4 Burrow + Graze 5 Burrow + Poison 6 Graze 7 Null 8 asym(1-exp(-lrc(Burrow-C0))) 9 Poison 10 Burrow · Poison 11 asym(1-exp(-lrc(Burrow-C0 graze))) 12 Burrow · Graze

106.72 107.87 110.41 110.84 111.14 111.60 111.61 111.76 113.80 114.11 115.86 116.05

DAICc xi 0.00 1.15 3.70 4.12 4.43 4.88 4.89 5.04 7.08 7.39 9.14 9.34

0.44 0.25 0.07 0.06 0.05 0.04 0.04 0.04 0.01 0.01 0.00 0.00

flocks) 5 111.33 0.00 5 111.56 0.23 3 112.08 0.75 4 112.91 1.58 4 115.01 3.68 3 115.19 3.86 2 115.74 4.40 4 115.90 4.57 3 118.34 7.01 5 119.30 7.97 5 125.02 13.69 5 nc nc

0.28 0.25 0.19 0.13 0.04 0.04 0.03 0.03 0.01 0.01 0.00

N, number of parameters; AICc, Akaike information criteria adjusted for sample size; DAICc, the difference between the model and the ‘best’ model. xi, Akaike weight or probability of the model given the data and the models in the set. Parameters and variables are defined in Table 1; nc, model would not converge.

of the next best model. Flocks were only seen in rested areas; four flocks of seven individuals, one of nine individuals, one of 12 individuals and one of 22 individuals were seen. In autumn 2005 the long-rested area had over twice as many rufous-necked snowfinches as summer-rested sites. The density estimate included a flock of 19 individuals. No clear model for rufous-necked snowfinches was supported for autumn 2004 data. There was no evidence that poisoning pikas in spring 2005 affected the densities of either species of snowfinch in autumn 2005 (Table 4).

3.3.3. Relationships between the abundance of other bird species and grazing practices The low densities and seasonal variation in the abundance of other species observed restricted the inferences that could be made about them. For Hume’s groundpeckers, which are also burrow/ground nesters, no clear relationships were evident. Grouping species into foraging and/or nesting guilds did not produce any clear patterns; however there was some evidence of a positive association with reduced grazing for some of the species. The density of Richard’s pipits tended to be higher in summer-rested areas (0.26 ha1) than in continuously grazed areas (0.16 ha1) but there was no strong support for this relationship (AICc rested = 71.94 vs. AICc null = 69.73) in autumn 2004. All 16 observations of common hoopoes made during

1978

Table 5 – Model selection table for the relationship between snowfinch density and explanatory variables in autumn 2004

6

5

4

3

2

1

0 0

500

1000

1500

2000

2500

White-rumped snowfinches ha-1(Sep 2004)

Rank Model

N AICc

DAICc xi

White-rumped snowfinch 1 Burrow 2 Burrow + Graze 3 Null 4 asym(1-exp(-lrc(Burrow-C0))) 5 Graze 6 asymgraze(1-exp(-lrc(Burrow-C0))) 7 Burrow · Graze 8 asym(1-exp(-lrcgraze(Burrow-C0))) 9 asym(1-exp(-lrc(Burrow-Co graze)))

3 4 2 4 3 5 5 5 5

0.00 2.62 2.64 3.27 3.82 6.01 6.66 6.88 7.28

113.71 116.33 116.36 116.98 117.54 119.72 120.37 120.59 121.00

0.49 0.13 0.13 0.10 0.07 0.02 0.02 0.02 0.01

N, number of parameters; AICc, Akaike information criteria adjusted for sample size. DAICc, the difference between the model and the ‘best’ model. xi, Akaike weight or probability of the model given the data and the models in the set. Parameters and variables are defined in Table 1.

Pika burrows ha-1 (April 2005)

b

1 4 1 ( 2 0 0 8 ) 1 9 7 2 –1 9 8 1

5

4

3

2

1

0 0

500

1000

1500

2000

2500

Pika burrows ha-1 (April 2005)

Fig. 3 – Observed (open symbols) and predicted (line) density of white-rumped snowfinches ha1 in autumn. (a) September 2005; the solid line is the most supported model and the dashed line is the 2nd ranked model (Table 4). The grey shaded outlier was excluded during model selection. This was the only poisoned site where the burrow density did not appear to decline between April 2005 and September 2005 which may indicate an error was made with the April 2005 burrow count – this would shift the point to the right. The single closed square symbol is for the long-rested site which was not included in model selection. (b) September 2004; the solid line is the most supported model (Table 5). The single closed square symbol is for the long-rested site which was not included in model selection.

the study were in rested areas. Of the 49 observations of horned larks made during the study, 51% were made at the long-rested site; on average there were 16 times as many horned larks there as other sites. Outside the long-rested site, for horned larks no clear preference between summer-rested and continuously grazed sites was apparent.

4.

Discussion

4.1.

Ground-nesting snowfinches

The most common species around Naqu were white-rumped and rufous-necked snowfinches. At the start of the breeding season in spring the density of white-rumped snowfinches

Rufous-necked snowfinches ha-1 (Sep 2005)

White-rumped snowfinches ha-1 (Sep 2005)

a

B I O L O G I C A L C O N S E RVAT I O N

5.5 5.0 4.5 4.0 3.5 3.0 2.5 2.0 1.5 1.0 0.5 0.0 0

500

1000

1500

2000

2500

Pika burrows ha-1 (April 2005)

Fig. 4 – Observed (open symbols) and predicted (line) density of rufous-necked snowfinches in autumn 2005. Models ranked 1 and 2 (Table 4) gave similar predictions and those from model 1 are shown. While these models were notionally asymptotic, the parameter estimates produce essentially straight line fits over the range of the data. The solid line and open triangles are summer-rested sites. The dashed line and open squares are continuously grazed sites. The single closed square symbol is for the long-rested site which was not included in model selection.

was positively related to the density of pika burrows, with predicted densities ranging from ca. 0.5 ha1 at burrow densities of ca. 500 ha1 to ca. 3 ha1 at burrow densities of ca. 2000 ha1 (Fig. 2), suggesting that breeding densities of this species may be limited by the availability of pika burrows. All the most supported models indicated a positive relationship between the density of white-rumped snowfinches and pika burrows (Table 3) and there was some evidence that higher densities occurred in areas rested from livestock grazing over summer compared with areas grazed continuously for a given burrow density (Fig. 2), but this effect was small relative to the effect of pika burrow density. Vegetation cover and presumably food for snowfinches was much higher in the

B I O L O G I C A L C O N S E RVAT I O N

area rested from grazing for four years prior to the start of our study, but the density of white-rumped snowfinches in this area still seemed to be determined mainly by the density of pika burrows (Fig. 2). In mid-September at the end of both the 2004 and 2005 breeding seasons white-rumped snowfinches were still spread in the landscape and presumably still associated with their breeding territories. At these times models with a positive relationship between their densities and the densities of pika burrows were still supported, but there was some evidence in 2005 that the relationship might be asymptotic (Table 4 and Fig. 3). An asymptotic relationship could arise at the end of the breeding season if recruitment is less successful due to intra- or inter-specific (with pikas) competition in populations of white-rumped snowfinches that are high at the start of the breeding season, but more data are required to test this. There was no evidence that livestock grazing treatments (summer-rested vs. continuous) affected the autumn densities of white-rumped snowfinches and the density in the long-rested area also appeared to be determined mainly by the density of pika burrows (Table 4 and Fig. 3). In summary, both the spring and autumn data for white-rumped snowfinches suggest their densities are largely determined by the density of pika burrows in the landscape. The relationship between the local density of snowfinches and the local density of pika burrows is not surprising given that these species nest primarily in pika burrows (MacKinnon and Phillipps 2000). In other systems similar relationships have been observed. For example, burrowing owls (Athene cunicularia) have a significant positive association with blacktailed prairie dog (Cynomys ludovicianus) towns (Smith and Lomolino, 2004). However, we have not found any other studies that suggest that both the breeding abundance and post breeding abundance of a bird is so closely linked to the burrow density provided by another species as our study does. In contrast to white-rumped snowfinches, the density of rufous-necked snowfinches appeared to be influenced by livestock grazing practices. At the start of breeding in spring we could find no clear relationship between the density of rufous-necked snowfinches and the variables we tested with the null model receiving three times the support of the next best model, but birds were seen in flocks in the long-rested area. At the end of the breeding season in autumn 2005 we found a positive relationship between the density of rufousnecked snowfinches and the density of pika burrows in areas rested from grazing over summer, but numbers were consistently low in continuously grazed areas (Fig. 4). Three of the four top models included the grazing treatment effect (Table 4). The relationship was only evident when birds in flocks were included in the analysis. If birds from the local area were forming into these flocks then this would suggest that pika burrow density is an important determinant of rufous-necked snowfinch density, but we do not know whether this is the case and further data are required to test this. In the longrested area the density of rufous-necked snowfinches in autumn 2005 was much higher than at any other site (Fig. 4) and flocks were only seen in this area and at summer-rested sites. No flocks were seen in continuously grazed sites. These data suggest that livestock grazing practices affect

1 4 1 ( 2 0 0 8 ) 1 9 7 2 –1 9 8 1

1979

resources, probably food, that is important to rufous-necked snowfinches. We found no evidence that local poisoning of pikas in spring directly affected the local abundance of either species of snowfinch in the following autumn with very limited support for models including poisoning (Table 4). We did not have the resources to measure bird populations in spring immediately following pika poisoning, so we do not know whether local bird populations were reduced by poisoning but recovered by the following autumn, or whether there was no direct affect of poisoning on the birds. Populations of ground-nesting birds including snowfinches are much lower in large areas that have been subjected to extensive pika poisoning compared with areas where pika populations are intact (Lai and Smith, 2003). In the poisoned areas Lai and Smith (2003) observed only 51 partially collapsed burrows ha1 and no active (open) burrows. In our study area local poisoning in spring reduced the density of pika burrows by about 33% by the following autumn (Pech et al., 2007). Pika populations recovered rapidly, but more extensive and sustained pika control would probably produce the same sorts of impact on pikas and hence the density of their burrows as observed by Lai and Smith (2003). From our results we would expect this to have a large impact on the densities of white-rumped snowfinches and possibly rufous-necked snowfinches.

4.2.

Other species

Most other species seen in our study were seasonal migrants (del Hoyo et al., 2001; del Hoyo et al., 2004) and they generally occurred at much lower densities than the two more common species of snowfinch. There was some evidence that these species responded positively to reduced grazing by livestock. Common hoopoes were never seen at continuously grazed sites and over 50% of the observations of horned larks throughout the study were in the long-rested area. On the shortgrass steppe of the North American Great Plains, horned larks are widespread and replace lark buntings (Calamospiza melanocorys) when the system moves from low grazing intensity by livestock to high grazing intensity (Milchunas et al., 1998). While this appears to contrast with our results, the high grazing intensity employed in the Milchinas et al., study was experimentally imposed to remove 60% of maximum standing herbage, compared with the complete removal of standing herbage that occurs over winter with current grazing practices around Naqu. Richard’s pipits also tended to occur at higher densities in summer-rested areas than in continuously grazed areas. All of these species may be responding to greater food resources in the form of seeds and possibly insects which we presume were associated with rested areas. Changes in food supply in terms of quantity or composition, as well as changes in the physiognomy of the plant community have all been suggested as mechanisms for bird community responses to livestock grazing (Milchunas et al., 1998; Fuller and Gough, 1999; Martin and Possingham, 2005) and could explain the patterns we observed. For example, in Scotland the breeding abundance of the meadow pipit (Anthus pratensis) was found to be highest under low intensity grazing from cattle and sheep rather than sheep alone, the authors proposing that mixed grazing generated greater heterogene-

1980

B I O L O G I C A L C O N S E RVAT I O N

ity in vegetation structure which modified prey availability, resulting in a greater abundance of birds (Evans et al., 2006). In the same study the egg size of the meadow pipit was found to be maximised under intermediate grazing pressure from sheep rather than high or no grazing, probably because their ability to obtain food was maximised (Evans et al., 2005). While our observations apply to local abundance, clearly food availability is likely to play a key role in survival and breeding success in harsh environments like those on the Tibetan plateau, so it is likely grazing practices have significant effects on the overall populations of these species. There is some evidence from other studies that impacts of grazing on biodiversity are greater when large herbivores are introduced into systems which evolved without similar large herbivores, compared with systems where free-living large herbivores, for example bison, are part of their recent history (Milchunas et al., 1998). However, even in the latter situation, which is more analogous to the situation on the Tibetan plateau, large impacts on particular components of the community, such as birds, are still observed when grazing pressure gets too high. This is consistent with the results of our study.

4.3. Implications for the conservation of avian biodiversity on the Tibetan plateau Our results indicate that different species of small birds respond in different ways to both the presence of pika burrows and hence pikas, as well as the differential effects of grazing practices employed around Naqu, probably mediated through effects on the food supply. Given that the current supposedly high density pika populations are thought to have arisen in response to increased grazing pressure from livestock (Liu et al., 1991; Fan et al., 1999), this creates a complex system in which to manage avian biodiversity on the plateau. No other studies on grazing impacts on birds appear to consider this three way interaction. Clearly management practices which either remove pikas from the system, or permanently reduce their abundance to very low levels will have serious consequences for the small birds that rely on pika burrows for breeding, as observed directly by Lai and Smith (2003). Reducing grazing pressure from livestock may increase the food supply for some bird species and ultimately their abundance; we have some evidence that reducing grazing pressure quite significantly, as was done with the long-rested site in our study may have large effects, but additional studies are required to test this relationship further. At present around Naqu most areas are grazed continuously and a relatively small proportion of available grazing land is fenced to restrict access by livestock over summer: so far, approximately 2.2% of grassland has been fenced in TAR compared to 20–30% around Qinghai Lake in the northern part of the plateau (Wu, 2005). But regardless of the grazing treatment, the majority of above ground biomass is still removed in most areas throughout winter (Fig. 1 and Pech et al., 2007). Paradoxically, reducing grazing pressure may reduce pika populations and hence the abundance of some avian species like the white-rumped snowfinch that rely on pika burrows. However, the relationship between pika densities and livestock grazing pressure is far from certain. High levels of livestock grazing could benefit pika populations by increasing

1 4 1 ( 2 0 0 8 ) 1 9 7 2 –1 9 8 1

erosion and creating additional burrowing opportunities for pikas and a positive relationship between the level of erosion and the number of pika burrows has been observed (Arthur et al., 2007). However, it is also plausible that high pika populations caused the higher levels of erosion. At the local scale, under the heavy livestock grazing pressure seen around Naqu, pika populations benefited from reduced summer grazing by livestock with higher density populations in summer-rested areas adjacent to continuously grazed areas (Pech et al., 2007). This provides some evidence that grazing pressure could be reduced without having negative impacts on the density of pika populations, but further studies will be required to determine properly the relationship between livestock grazing intensity and pika abundance. As Lai and Smith (2003) suggested, the interactions between livestock grazing practices and the plateau’s biodiversity must be understood in order to properly manage the system. Plateau pikas play a key role, providing food for large avian predators and habitat for small-ground-nesting birds (Lai and Smith, 2003), as well as mediating plant community dynamics through disturbance (Bagchi et al., 2006). Their presence is likely to be required for long-term sustainable management of this system. Currently the system seems overgrazed mainly by livestock, which have increased rapidly in recent decades (Jing et al., 1991; Dong et al., 2004) and reducing this grazing pressure would also alleviate some of the other problems of degradation that have been associated with it, such as erosion and an increase in the prevalence of toxic plants (Lang et al., 1997; Zhang et al., 1998; Zhou et al., 2005). It appears likely that reducing grazing pressure will also have significant benefits for biodiversity.

Acknowledgements This project was co-funded by the Australian Centre for International Agricultural Research (ACIAR), AusAID, the Chinese Academy of Sciences and CSIRO. This research was conducted under animal ethics approval 02/03-30 (CSIRO Sustainable Ecosystems Animal Ethics Committee). Steve Henry, Eddie Gifford, Tony Sinclair, Song Xiaoping, Cai Hai Jian, Baima Cuo, Lydia Li, Jin Li and members of the Grassland Station, Naqu Bureau of Agriculture and Animal Husbandry, provided valuable assistance with data collection and manipulation. Wang Guanglin, Lydia Li and Baima Cuo assisted with essential translation skills. The project could not have been completed without the friendship and co-operation of people at the villages of Duo Su, Qi long Nang ba, Gen ma, Ke ma, Na ka quk and Sang long. David Westcott and Eric Doerr provided useful comments on an early draft of the manuscript which was also improved by the input of two anonymous referees.

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