Plateau Pika Population Survey and its Control Threshold in the Alpine Meadow Ecosystems of the Tibetan Plateau

SUN Feida， GOU Wenlong， LI Fei， ZHU Can， LU Hui， CHEN Wenye

(1. College of Animal Science and Technology， Sichuan Agricultural University， Chengdu 611130， China;2. Sichuan Grassland Science Academy， Chengdu 611731， China;3. Gansu Forestry Science and Technology Research Academy， Lanzhou 730020， China)

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Plateau Pika Population Survey and its Control Threshold in the Alpine Meadow Ecosystems of the Tibetan Plateau

SUN Feida1， GOU Wenlong2， LI Fei1， ZHU Can1， LU Hui1， CHEN Wenye3

(1. College of Animal Science and Technology， Sichuan Agricultural University， Chengdu 611130， China;2. Sichuan Grassland Science Academy， Chengdu 611731， China;3. Gansu Forestry Science and Technology Research Academy， Lanzhou 730020， China)

Understanding the roles of plateau pikas (Ochotonacurzoniae) on grassland degradation is essential for improving the management of pika populations in alpine meadow ecosystem. In this study， 4 degrees of active burrows densities from 12 survey sites were defined to evaluate the interactions between pika populations and biomass changes. We conclude that pika activities may not be the cause but act as a symptom of grassland degradation， and the high-frequency of pika activities can promote to the process of reverse succession. Therefore， some comprehensive measures such as reduction of livestock numbers， variable grazing system， restorative management techniques， and community participation in co-management of the meadows are likely to effectively improve grassland productivity and prevent the outbreaks of pikas. Furthermore， pika population fluctuations should be monitored. When the population of pikas exceeds the economic threshold or reaches high-density， integrated management strategies should be implemented to prevent damage.

control threshold; plant biomass; rodents control; rangeland management

Plateau pikas (Ochotonacurzoniae) are small lagomorphs， endemic to parts of the Tibetan Plateau in China， India and Nepal (Bagchietal.， 2006)， their grazing， burrowing， mowing， caching behaviours and food selection overlap with local yak (Bosgrunniens) and Tibetan sheep (Ovisaries)(Fan & Zong， 1991; Pechetal., 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 (Vulpesferrilata)， steppe polecats (Mustelaeversmanni)， Chinese mountain cats (Felisbieti)， Pallas’s cat (Otocolobusmanul) and Eurasian lynx (Lynxlynx) (Smith & Foggin， 1999)， and avian predators， such as golden eagles (Aquilachrysaetos)， upland buzzards (Buteohemilasius)， saker falcons (Falcocherrug)， goshawks (Accipitergentiles)， black kites (Milvusmigrans) and little owls (Athenenoctua)(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 (Myospalaxbaileyi)， european rabbits (Oryctolaguscuniculus)， pocket gophers (Thomomysbottae)， prairie dogs (Cynomysludovicianus) and water voles (Arvicolaterrestris) 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 (Bagchietal.， 2006; Arthuretal.， 2008; Delibes-Mateosetal., 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 (Fanetal.， 1999; Zhang & Liu， 2003).

The positive or negative impact of pikas on grassland ecosystems have mainly been assessed with species abundance (Liuetal.， 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; Arthuretal.， 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 (Zhouetal.， 2005; Wangetal.， 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 ofKobresiahumilisgrazed 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 (Sunetal.， 2008; Zeng & Lu， 2009).

Table 1 Geographical， plateau pika abundance and burrows counts of survey sites

Notes： burrow density： AZD. approximately zero-density， LD. low-density， MD. medium-density， HD. high-density.

Fig. 1 Survey scheme for plateau pika burrows demography by large circle sample (r=28.2 m) with plugging tunnels method

Make O as fixed centre of a circle， then carefully look for burrows along anticlockwise direction from A to B， C， D， A， or clockwise direction from A to D， C， B， A.

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.

Fig. 2 The total， active burrows counts and their ratios of active burrow of 12 survey sites (a) and 4 degrees of pika population sites (b)

Burrow density： AZD. approximately zero-density, LD. low-density, MD. medium-density, HD. high-density; capital and lowercase letters for a given variable indicate there is a significanr difference in the same plant speciece (P<0.05) and (P<0.01) among different treatments; the same below.

1.3 Plant composition and biomass

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 (Wangetal., 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 ofKobresiameadows 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 (Sunetal.， 2008; Wangetal.， 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 (Dobsonetal.， 1998; Brownetal.， 2006). Active and inactive burrows are considered by some as the best indicator of intensity for herbivorous small mammal control (Desmond & Savidge， 1996; Desmondetal.， 2000; Pechetal.， 2007)， but it is difficult to distinguish active and inactive entrances unambiguously through small herbivores footprint or/and fecal material (Pechetal.， 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 (Maetal.， 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 (Pechetal.， 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 (Maetal.， 2002; Sunetal.， 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

Fig. 3 Seasonal fluctuations of aboveground (a) and belowground (b) biomass at different sites

Thick dash lines describe their own mean seasonal biomass, e.g.， MAZD is the abbreviation of mean seasonal biomass of site AZD， etc.

Fig. 4 Seasonal fluctuations of plant functional groups of sedges， grasses， forbs and litter biomass at different sites

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 (Pokornyetal., 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 (Wangetal.， 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 asLigulariavirgaurea，Aconitumpendulum，Euphorbiaftscheriana， andAnaphalislactealonly 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 (Yangetal.， 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 (Yangetal.， 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 (Wangetal.， 2008; Yangetal.， 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; Jingetal.， 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 (Linetal.， 2008). The temporary reduction in pika abundance through poison control programmes have limited effect， because populations can recover in one breeding season (Delibes-Mateosetal.， 2011); also there was no apparent increase in forage production in areas where plateau pikas were controlled (Pechetal.， 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-Mateosetal.， 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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河南省鳥(niǎo)類新紀(jì)錄——黑眉柳鶯

2016年4月2日10∶00左右，在河南省洛陽(yáng)市吉利區(qū)開(kāi)展鳥(niǎo)類資源調(diào)查期間，于河陽(yáng)新村西花園(112°36′53.31″E，34°53′56.20″N，133 m)發(fā)現(xiàn)2只柳鶯屬Phylloscopus鳥(niǎo)類。其上體橄欖綠色，中央冠紋淡綠黃色自額基延伸至后頸，側(cè)冠紋黑色，明顯粗于緊鄰其下的黃色眉紋，貫眼紋黑色，較眉紋為細(xì)。左右翅各有2道淡黃色翼斑，靠前者較靠后者細(xì)弱且明顯暗淡不顯；下體鮮黃色，有亮感，兩脅染淺灰綠。頸及背橄欖綠色染以灰色細(xì)紋。上喙褐色，端處淺紅黃色，下喙色同上喙先端處。綜上，鑒定該鳥(niǎo)為黑眉柳鶯P.ricketti(約翰·馬敬能等，2000；曲利明等，2014)。檢索相關(guān)文獻(xiàn)資料、觀鳥(niǎo)記錄、《中國(guó)鳥(niǎo)類分類與分布名錄(第二版)》(鄭光美，2011)和《河南省鳥(niǎo)類原色圖鑒》(吳國(guó)新，劉玉卿，2016)，確認(rèn)該鳥(niǎo)為河南省鳥(niǎo)類分布新紀(jì)錄。

觀測(cè)當(dāng)日天氣晴朗，該鳥(niǎo)與黃腰柳鶯P.proregulus集小群活躍于槐樹(shù)Sophorajaponica、構(gòu)樹(shù)Broussonetiapapyrifera和柳樹(shù)Salixbabylonica的樹(shù)冠基部，在樹(shù)枝間移動(dòng)鳴叫，極少見(jiàn)于樹(shù)冠頂端；不甚懼人，與觀測(cè)者最近距離僅4～5 m。

黑眉柳鶯在我國(guó)分布于甘肅東南部、云南東南部、四川、重慶、貴州、湖北、湖南、江西、浙江、福建、廣東、廣西、香港(鄭光美，2011)。本次發(fā)現(xiàn)或?qū)斫獯饲盃?zhēng)議、明確其分類地位具有一定的意義。

黑眉柳鶯Phylloscopus ricketti (王大勇 攝)

馬朝紅1， 王文博2， 王大勇3， 趙海鵬4*

(1. 河南黃河濕地國(guó)家級(jí)自然保護(hù)區(qū)孟津管理局，河南孟津471100；

2.河南黃河濕地國(guó)家級(jí)自然保護(hù)區(qū)洛陽(yáng)濕地處，河南洛陽(yáng)471000；

3.中國(guó)石油化工股份有限公司洛陽(yáng)分公司水務(wù)中心，河南洛陽(yáng)471012；

4.河南大學(xué)生命科學(xué)學(xué)院，河南開(kāi)封475001)

*通信作者, 男, 博士, 副教授, 研究方向：動(dòng)物學(xué), E-mail：hpzhao1980@gmail.com

2016-04-05 接受日期：2016-08-18

國(guó)家自然科學(xué)基金項(xiàng)目(31100338); 四川省留學(xué)回國(guó)人員項(xiàng)目(03109148); 四川農(nóng)業(yè)大學(xué)“雙支計(jì)劃”項(xiàng)目

孫飛達(dá)(1978—)， 男， 副教授， 從事高寒草地生態(tài)學(xué)研究(小型食草動(dòng)物為主)， E-mail：sunfd08@163.com

Q959.837； Q958.1

A

1000-7083(2016)06-0825-08

青藏高原高寒草甸生態(tài)系統(tǒng)高原鼠兔種群調(diào)查及其防控閾值研究

孫飛達(dá)1， 茍文龍2， 李飛1， 朱燦1， 路慧1， 陳文業(yè)3

(1. 四川農(nóng)業(yè)大學(xué)動(dòng)物科技學(xué)院，成都611130； 2. 四川省草原科學(xué)研究院，成都611731；3. 甘肅省林業(yè)科學(xué)研究院，蘭州730020)

認(rèn)識(shí)高原鼠兔Ochotonacurzoniae在草地退化中的角色和地位，對(duì)于加強(qiáng)高寒草甸生態(tài)系統(tǒng)高原鼠兔種群管理具有重要的意義。以高原鼠兔有效洞穴密度為調(diào)查對(duì)象，根據(jù)所調(diào)查的12個(gè)樣地遴選出4個(gè)不同鼠洞等級(jí)的研究樣地去評(píng)估鼠兔數(shù)量和植物生物量變化之間的關(guān)系。主要結(jié)論如下：高原鼠兔活動(dòng)并非引起草地退化的原因，而是作為草地退化的標(biāo)志性信號(hào)，然而高頻度的鼠兔活動(dòng)會(huì)加劇草地逆向演替的進(jìn)程。因此，一些綜合措施諸如減少牲畜數(shù)量、動(dòng)態(tài)的輪牧、草地恢復(fù)管理技術(shù)、社區(qū)參與式管理等可以有效提高草地生產(chǎn)力和防止鼠害爆發(fā)。對(duì)各類型退化草地進(jìn)行綜合治理時(shí)，應(yīng)加強(qiáng)對(duì)害鼠種群動(dòng)態(tài)的監(jiān)測(cè)，當(dāng)種群密度超過(guò)經(jīng)濟(jì)閾值或達(dá)到高密度種群時(shí)，應(yīng)急性、常規(guī)性滅鼠工作才可以實(shí)施，為重度型退化草地重建、植被恢復(fù)和土壤發(fā)育提供可能性。

防控閾值；植物生物量；鼠害防控；草原管理

10.11984/j.issn.1000-7083.20160073