2. 四川省草原科学研究院, 成都 611731；
3. 甘肃省林业科学研究院, 兰州 730020
2. Sichuan Grassland Science Academy, Chengdu 611731, China;
3. Gansu Forestry Science and Technology Research Academy, Lanzhou 730020, China
Plateau pikas(Ochotona curzoniae)are small lagomorphs, endemic to parts of the Tibetan Plateau in China, India and Nepal(Bagchi et al., 2006), their grazing, burrowing, mowing, caching behaviours and food selection overlap with local yak(Bos grunniens)and Tibetan sheep(Ovis aries)(Fan & Zong, 1991; Pech et al. , 2007).
In the past, plateau pikas have been traditionally viewed as competitors with domestic livestock for forage, and agents of pasture desertification, soil erosion and vegetation disturbances(Smith & Foggin, 1999； Zhang & Liu, 2003). On the other hand, plateau pikas also play a key role in maintaining ecosystem functions as a keystone species for providing a food resource for large mammalian predators such as foxes(Vulpes ferrilata), steppe polecats(Mustela eversmanni), Chinese mountain cats(Felis bieti), Pallas's cat(Otocolobus manul) and Eurasian lynx(Lynx lynx)(Smith & Foggin, 1999), and avian predators, such as golden eagles(Aquila chrysaetos), upland buzzards(Buteo hemilasius), saker falcons(Falco cherrug), goshawks(Accipiter gentiles), black kites(Milvus migrans)and little owls(Athene noctua)(Smith & Foggin, 1999; Lai & Smith, 2003; Zhang & Liu, 2003). Additionally, some abandoned tunnels provide homes for lizards, ground squirrels and native birds(Desmond & Savidge, 1996; Lai & Smith, 2003). An alternative view of plateau pikas is that they contribute to the overall health of alpine meadows by aerating the soilviatheir burrowing activities, promoting nutrient recycling within alpine ecosystems(Smith & Foggin, 1999; Li & Zhang, 2006).
Like other small herbivores, such as plateau zokors(Myospalax baileyi) , european rabbits(Oryctolagus cuniculus), pocket gophers(Thomomys bottae), prairie dogs(Cynomys ludovicianus)and water voles(Arvicola terrestris)in various grasslands types around the world, plateau pikas appear to have both detrimental and beneficial, direct and indirect, and long-term and short-term impacts on grassland ecosystems(Bagchi et al., 2006; Arthur et al., 2008; Delibes-Mateos et al ., 2011). When the pika populations reach a high density, eradication campaigns, mainly by putting poison baits in burrows, have been performed by Chinese local governments and organizations for many years(Fan et al., 1999; Zhang & Liu, 2003).
The positive or negative impact of pikas on grassland ecosystems have mainly been assessed with species abundance(Liu et al., 1980), however, researches on pika population survey method, high frequency activity and pika roles of "benefit-detrimental" transformation are limited and the results lack of quantitative evidences. We focused on plateau pika population survey method, biomass changes and herbivorous small mammal population effective management in the alpine meadow ecosystems.1 Methods 1.1 Study area
Tibetan Plateau is located in southwest China with a high altitude, harsh environment where the grassland ecosystems have complex, sensitive and vulnerable characteristics(Long, 2007; Arthur et al., 2008). The climate shows strong seasonality, with an annual mean temperature＜0 ℃, year-round frost and extensive areas of permafrost occur in mountains and grasslands. The major plant communities are alpine meadow, alpine swamp, alpine shrub, alpine prairie and alpine steppe meadow(Zhou et al., 2005; Wang et al., 2008).
This study was carried out on the south-eastern flank of Qinghai province, part of the Sanjiangyuan National Nature Reserve, which is one of the largest nature reserves in the world(Worthy & Foggin, 2008). Plateau pikas had never been eradicated in this area, and all study sites consisted of gently undulating terrain with low, sparse alpine meadow, comprised mainly of Kobresia humilis grazed by yaks and sheep in the cold season from September to the following May.1.2 Plateau pika burrow demography
Large circle sample(2 500 m2)method was used to investigate plateau pika burrow densities with the plugging tunnels method(PTM)in early May, 2008. We randomly selected 12 sites in alpine meadows within a similar habitat, where there were practically no subter-ranean zoker mounds and no zokers were trapped(Fig. 1), while the range of pika population abundance was deduced with active burrow ratio and the local burrow coefficient(Fig. 2: a, b). All surveys were conducted simultaneously at each site between 09∶ 00 and 11∶ 30(Sun et al., 2008; Zeng & Lu, 2009).
Considering the major grassland types of alpine meadow, and the status of site habitat and utilization, combined with cluster analysis, 4 degrees with active burrow densities were defined as approximately zero-density(AZD), low-density(LD), medium-density(MD), and high-density(HD)sites, respectively(Table 1; Fig. 2: b), then fenced with 50 m×50 m square to avoid livestock grazing and human activity.
|Total burrows/(hm-2)||102||1 124||2 124||2 780|
|Active burrows/(hm-2)||48±8||512±54||864±85||1 360±152|
|Altitude/m||3 771||3 769||3 740||3 751|
|Notes: burrow density: AZD. approximately zero-density, LD. low-density, MD. medium-density, HD. high-density.|
In each site, 5 random quadrats of 25 cm×25 cm were identified and the following parameters were recorded: plant species, overall vegetation cover and height in late August. Aboveground vegetation was sorted into four functional groups(grasses, sedges, forbs and litter)and clipped at ground level(Wang et al., 2008). After aboveground biomass harvest, belowground biomass was estimated from 10 cm×10 cm soil cores collected to 30 cm depth with each section 10 cm, because nearly all of Kobresiameadows roots were concentrated in this depth. At each sampling, 3 soil cores were collected on each plot. Mud and soil were carefully removed by rinsing with water, and the roots were divided into 2 parts: living and dead(Sun et al., 2008; Wang et al., 2010). All biomass materials were stored in paper bags, oven dried at 75 ℃ for 48 h and weighed.2 Discussion 2.1 Plateau pika population survey
It is vital to collect the counts of plateau pikas accurately, to provide detailed information on population dynamics, to allow effective management measures to be implemented(Zhong & Fan, 2002). At present, there are many methods used in small animal surveys, such as active and inactive burrow counts, mark-resight, mark-recapture and live-capture methods with belt transects on plateau pikas, plateau zokers, European rabbits, pocket gophers, prairie dogs and water voles(Dobson et al., 1998; Brown et al., 2006). Active and inactive burrows are considered by some as the best indicator of intensity for herbivorous small mammal control(Desmond & Savidge, 1996; Desmond et al., 2000; Pech et al., 2007), but it is difficult to distinguish active and inactive entrances unambiguously through small herbivores footprint or/and fecal material(Pech et al., 2007). It seems that capturing individuals or mark-resight may be very close to the actual species abundance, yet it is not practical to use for a number of large experimental sites(Ma et al., 2002).
This study indicates that, in alpine meadow ecosystems, the active burrow count to represent plateau pika abundance, using the plugging tunnel method is accurate, operable and practical. Within the active burrow ratios of our survey sites, where the mean active burrows ratio and the burrow coefficient were 42.8% and 3.3, over the counts of 200 pika and/or 1 360 active burrows per hectare could be the "high-density" in Guoluo pasture. However, the relationship between pika population and the total burrows(Pech et al., 2007)was not good. The causes may be that pika abundance show large seasonal and regional variations related to microhabitat, vegetation, precipitation and grasslands utilization(Ma et al., 2002; Sun et al., 2010).
In short, the demography of plateau pika is a direct indicator to evaluate the impacts of pika populations on grasslands, and whether their impacts are beneficial or detrimental in alpine meadow ecosystems. Pikas have the natural characteristics of transferring and moving frequently for food and exercises(Smith & Foggin, 1999), but the active burrows, as dwelling homes, still are their activities assembly area. Through large-scale active burrow ratio and burrow coefficient investigation, active burrow densities could be more objectively and truly reflected the pika population fluctuations.2.2 Plant functional groups, aboveground and belowground biomass allocation
Fig. 3 demonstrates that aboveground, belowground and total biomass varied with seasons. Total biomass is made up of aboveground and belowground biomass components. Overall there were significant differences in aboveground biomass(F=1 026.366, P＜0.001)and belowground biomass(F=23 754.111, P＜0.001).
Aboveground biomass increased to the maximum in August(LD, MD and HD)and September(AZD)then declined rapidly in October, yet the sequence of mean seasonal aboveground biomass was AZD(278.2 g·m-2)＞ MD(137.1 g·m-2)＞HD(106.7 g·m-2)＞LD(93.5 g·m-2)(Fig. 3: a). The minimum belowground biomass occurred in August, and the sequence of mean seasonal belowground was AZD(6 084.2 g·m-2)＞LD(3 436.0 g·m-2)＞HD(2 748.5 g·m-2)＞MD(2 197.0 g·m-2)(Fig. 3: b).
Fig. 4 presents the proportions of sedges, grasses, forbs and litter group biomass of the four sites. The sequences of seasonal average plant functional group biomass proportions were as follows, sedges: LD(36.9%)＞AZD(25.3%)＞HD(6.6%)＞MD(3.1%); grasses: LD(20.1%)＞AZD(15.0%)＞HD(13.2%)＞MD(8.0%); forbs: MD(57.7%)＞HD(57.4%)＞AZD(27.2%)＞LD(23.3%); litter: AZD(32.6%)＞MD(31.6%)＞HD(22.5%)＞LD(19.7%); moreover, palatable herbage: LD(57.0%)＞AZD(40.2%)＞HD(19.8%)＞MD(11.0%).
The consumption of vegetation and burrowing can affect aboveground(shoots)and belowground(roots), which could in turn affect plant community composition, aboveground biomass allocation and root system characters(Pokorny et al., 2005). Sedges and grasses are the dominant palatable forages resources, but forbs, which are usually considered to be toxic, are not palatable forage for livestock.
In alpine meadows, perennial plants turn green in May and absolutely withered and yellow in October. For sedges, however, the dominant functional group did change with altitude, site habitat, degradation and reverse succession(Wang et al., 2008). In this study, pika burrowing activities may increase the plant species richness(Smith & Foggin, 1999)was not appeared, maybe it will take long-term controlled experiments to evaluate the full relationship between plateau pikas and plant diversity. However, certain plants such asLigularia virgaurea, Aconitum pendulum, Euphorbia ftscheriana, and Anaphalis lactealonly grow on the burrows and/or off-burrows.
Above- and below-ground biomass allocation is a central issue in plant ecology, however, the strategies of allocation in plants remain contentious(Yang et al., 2009). R∶ S ratios increased with belowground competition, suggesting that it is an adaptive response, but it could have been affected by the activity of herbivorous animals rather than adaptive plasticity(Craine, 2006). Plants can also alter their living root growth in response to the presence of external disturbance, and a plant adaptation strategy could alter plant rooting depths(Yang et al., 2009). In our study, R∶ S ratios were widely dispersed and the lowest value occurred in site HD, which were higher than those of analogous research on alpine meadows with different conditions such as degradation, altitude and areal extent(Wang et al., 2008; Yang et al., 2009). Pika transfers and activities disturbed the grassland habitat and increased the prevalence of community species but decreased biomass and palatable forage.2.3 Implications for the grasslands integrated management of plateau pika populations on the Tibetan Plateau
Many studies indicate that if the small mammal population reaches high density, control measures are necessary(Zhang & Liu, 2003; Jing et al., 2006). However, "high density" is an ill-defined concept animal density frequently changes. Researchers have accepted that plateau pikas may have both beneficial and detrimental effects on alpine meadow ecosystems(Smith & Foggin, 1999), yet at present it is not clear how pika density impacts upon biomass and grassland degradation.
Our central question concerns whether plateau pika induce beneficial and/or detrimental impacts. Plateau pikas act as a keystone species due to burrowing activities(Lin et al., 2008). The temporary reduction in pika abundance through poison control programmes have limited effect, because populations can recover in one breeding season(Delibes-Mateos et al., 2011); also there was no apparent increase in forage production in areas where plateau pikas were controlled(Pech et al., 2007). However, pika control with poison did lead to depletion of prey and secondary poisoning, so may therefore present problems for populations of numerous other animals, even to humans(Delibes-Mateos et al., 2011), which may have implications for food safety and ecological incidents.
To rodent pests, management will need to move away from the broadly destructive current approach of chemical eradication toward ecologically-based solutions(Dickman, 1999). Based on the current pastoral policy in China of "retire livestock, restore pasture" and an economic compensation programme, reduction of livestock number and rational rotational grazing are important, while the feeding of livestock indoors, or greenhouse feeding in winter, increases the income of nomadic herders and improve their livelihoods. Therefore, alternate methods such as establishing artificial or semi-artificial grassland are used to manage high-density alpine meadows. After restoring the vegetation, the alpine meadow is no longer a suitable habitat for plateau pikas and the grasslands function well and self-rehabilitate, which is the key to regulating and controlling pika density, and to promoting the healthy development of alpine meadows.3 Main conclusion
In our study sites, we concluded that pika activities at high-density(＞200 pikas or/and 1 360 active burrows per hectare)was likely to have detrimental impacts, and that low-densities(15~110 pikas and/or 48~512 active burrows per hectare)may be safe with potential beneficial impacts on grassland ecosystems. On the contrary, we highlighted that medium-density(110~200 pikas or/and 512~864 active burrows per hectare)was a key stage because it sat between high and low-density, and at these densities, succession direction is in the balance.
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