Positive associations between the cushion plant Arenaria polytrichoides(Caryophyllaceae) and other alpine plant species increase with altitude

in the Sino-Himalayas

Yang Yang, Yang Niu, Lohengrin A. Cavieres & Hang Sun

AbstractQuestion: Does the facilitative effect of cushionplants increase with elevation as a result of increasesin environmental harshness? Does this hypothesisapply in the Sino-Himalayan Mountains?Location: Lakaka Pass on the Baima Snow Moun-tains (281200N, 991050E), SW China.Methods: We evaluated the spatial association ofseveral plant species with the cushion plant Arenariapolytrichoides (Caryophyllaceae) at two elevations(4500 m and 4700m) in the study site andmonitoredtemperature, moisture and nutritional status of soilbeneath and outside the cushions.Results: While 14 species grow more frequentlyassociated with the cushions at the higher elevation,at the lower site only three species were positivelyassociated with cushions. Eleven of the species thatoccurred at both elevations changed their spatialassociation from neutral or negative with cushionsat the lower site to positive at the higher elevationsite. Substrate temperatures were rather similarbetween the cushions and areas of bare ground.Cushions maintained higher moisture than areas ofbare ground at both elevations. Soils beneath cush-ions contained significantly more available nitrogenand potassium compared to open areas at the higherelevation.Conclusions: Our results show that facilitation by A.polytrichoides cushions increases with elevation inthe Sino-Himalayan region. This facilitation effect

of A. polytrichoides cushions is probably due to theimproved nutrient availability provided by cushionplants in the higher elevation, and these conditionsprobably permit increased plant recruitment,growth and survival.

Keywords: Alpine environment; Arenaria polytri-choides; Facilitation; Nurse effect; Sino-Himalayas.

Introduction

Many studies that have recently examined thebalance between positive and negative interactionsamong plants along environmental gradients haveargued that the importance of facilitation increasesalong with increasing abiotic harshness and de-creasing productivity (e.g. Bertness & Callaway1994; Brooker & Callaghan 1998; Brooker et al.2008). Alpine habitats are well known for theirstressful conditions (Korner 2003), where stress fac-tors such as low temperatures and substrate stabilitychange with altitude and can be easily quantified(Choler et al. 2001). Thus, alpine habitats are parti-cularly useful for evaluating the importance ofpositive interactions along environmental stressgradients (Callaway et al. 2002).

Recent studies have revealed that the distribu-tion and abundance of many species in highelevation communities is enhanced by the presenceof neighbours, where interactions are predominatelyfacilitative (Choler et al. 2001; Callaway et al. 2002).In many of these high-altitude sites the positive in-teractions involve nurse plants that facilitate theestablishment of other plant species within their ca-nopy, because they offer microhabitats that aremore favourable for seed germination and/or seed-ling recruitment than the surrounding environment(Cavieres et al. 2006, 2007). The ameliorative effectsof nurse plants typically include increased soilmoisture, protection against herbivores and greateravailability of nutrients (Callaway 2007).

Cushion plants are a common growth form inalpine habitats (Korner 2003). Their low stature andcompact form act as an efficient heat trap (Korner &

Yang, Y. (yangyang@mail.kib.ac.cn) Niu, Y. (new

youngs@126.com) & Sun, H. (corresponding author,

hsun@mail.kib.ac.cn): Key Laboratory of Biodiversity

and Biogeography, Kunming Institute of Botany, Chi-

nese Academy of Sciences, 132 Lanhei Road, 650204,

Kunming, Yunnan, People’s Republic of China.

Niu, Y.: Graduate School of the Chinese Academy of

Sciences, 100039, Beijing, People’s Republic of China.

Cavieres, L.A. (lcaviere@udec.cl): ECOBIOSIS,

Departamento de Botanica, Facultad de Ciencias Nat-

urales y, Oceanograficas, Universidad de Concepcion,

Concepcion, Chile, and Instituto, de Ecologıa y Biodi-

versidad (IEB), Santiago, Chile.

Journal of Vegetation Science 21: 1048–1057, 2010DOI: 10.1111/j.1654-1103.2010.01215.x& 2010 International Association for Vegetation Science

De Moraes 1979) and also enhances soil moistureand nutrient availability (Nunez et al. 1999;Cavieres et al. 2006, 2007, 2008). Therefore, cushionplants could facilitate recruitment of other plantspecies in alpine areas. This has been demonstratedby studies in high-elevation habitats in the southernAndes (e.g. Cavieres et al. 2002, 2006, 2007, 2008;Badano et al. 2007), where there are significantlymore plant species growing within cushions thanoutside them (Cavieres et al. 2002; Arroyo et al.2003), mostly due to the buffering of temperatureextremes and increased soil moisture (e.g. Caviereset al. 2006, 2007, 2008).

The role of facilitative interactions amongplants in determining the performance of plant in-dividuals and the composition of plant communitiesin the Himalayan region has only recently receivedattention (Song et al. 2006; Wang et al. 2008). Forinstance, a comparison of the interactions betweenroot and shoot within alpine meadow plants in theNE Tibetan Plateau, Song et al. (2006) suggestedthat interactions among neighbour species could befacilitative, competitive or neutral, depending on thetraits of the plant species involved. Wang et al.(2008) indicated that facilitation is the dominant in-teraction in a Tibetan alpine meadow, wherebiomass growth responses to facilitative effects arespecies-specific. However, these two studies wereconducted using a small subsample of the speciespresent at relative low elevations ( � 3500m) anddone with species that do not create as conspicuousa microclimate modification as that of cushionplants.

In alpine ecosystems (4500-5500m abovesea level) in the Sino-Himalayas, there are severalcushion-shaped plant species, e.g. Chionocharishookeri (Boraginaceae), Arenaria polytrichoides, A.bryophylla, Thylacospermum caespitosum (Caryo-phyllaceae) and Androsace tapete (Primulaceae).However, the importance of these cushions in fa-vouring the presence of other species has not beeninvestigated in this region. We selected A. poly-trichoides, which is abundant in alpine areas of theSino-Himalayan region, to test the hypothesis thatthis cushion species facilitates the recruitment ofother plant species at higher elevations and henceleads to proportionally higher species richness thanin open areas. We compared the number of plantspecies growing within cushions of A. polytrichoidesat 4500m and 4700m and measured temperature,moisture and nutrient content of soil beneath A.polytrichoides cushions and in the surrounding baresoil to gain insights into the mechanisms involved infacilitation.

Methods

Study site

The study site was located in the alpine zone atthe Lakaka Pass on the Baima Snow Mountains,Deqen County, Yunnan Province, SW China(281200N, 991050E). Two plant communities domi-nated by A. polytrichoides were selected, one at4500m and the other at 4700m, both on east-facingslopes. Both sites also contained some prostrateshrubs and perennial herbs, e.g. Rhododendron rupi-cola, Saxifraga melanocentra and Potentillacoriandrifolia at the lower elevation, and Saussureavelutina, Pleurospermum amabile and Meconopsishorridula at the higher elevation.

The climate of the study site is characterized by

the summer monsoon. Annual precipitation re-corded from 1982 to 1984 at the nearest

meteorological station (281230N, 991010E, altitude4290m), 10 km from the study site, was 680–

790mm, with 30mm in May, 130mm in June and

500mm between July and September. The annual

average precipitation in the study region increases

with altitude, at 36.3mm per 100m. The plantgrowth season commonly starts in mid-May at

snow-melt, and ends in mid-September when the

summer monsoon ceases (Yang & Sun 2009). Thus,

the growing season at the study site has two distinct

periods, namely a dry period from mid-May to mid-

June, and a wet period from mid-June to mid-Sep-

tember (Yang 2009). The annual average air

temperature is � 1.01C, with 21C in May, 61C inJune, 81C in July, 71C in August, 51C in September

and 11C in October. The difference in mean monthly

temperature between the coldest and the warmest

month is around 151C. The altitudinal lapse rate of

annual average temperature in the study region is

0.7781C per 100m. Mean wind speed is 2.9m s� 1 to

3.1m s� 1 (Wang 2006).The available nitrogen, phosphorus and po-

tassium in soil from the A0 (0–2 cm), AS (2–14 cm)and Ac (14–45 cm) layers in the sub-alpine zone (ca.4000–4500m) is 292–329–57.7 ppm (N), 11.7–10.9–1.3 ppm (P) and 226–215–110 ppm (K) per layer, re-spectively. In the alpine zone (ca. 4500–4800m), thenitrogen, phosphorus and potassium availability insoil A (0–5 cm) and AC (5–10 cm) layers decreases to38.7–40.7 ppm (N), 1.2–1.5 ppm (P) and 99–125.5 ppm (K) (Qiu et al. 2003).

At the 4700m site we recorded ambient solarradiation (I), air temperature (Ta) and relative hu-midity (RH) at ca. 15 cm above the soil surface usingan integrated thermistor (1400–104 RH/Air tem-

Positive associations between Arenaria polytrichoides and other alpine plants 1049

perature sensor, LI-COR Inc., Lincoln, NE, USA)and a quantum sensor (Li-190SA quantum sensor,LI-COR) connected to a data logger (Li-1400 datalogger, LI-COR). Data were recorded every 15 minfrom 27 May to 2 June during the dry period andevery 5 min from 14 to 20 August during the rainyperiod (see supporting information).

Study species

The genus Arenaria is widely distributed intemperate to arctic regions and contains more than300 species classified in ten subgenera. A. poly-trichoides Edgeworth (subgenus Eremogone) is along-lived perennial herb that forms a hemisphericcushion, and is mainly found at high elevations inthe Sino-Himalayan region (Fig. 1). Vegetativegrowth of this plant starts as soon as the groundthaws, and flowering occurs from late May to earlyJune (Authors’ personal observations).

Vegetation sampling in patches dominated byArenaria polytrichoides

At both elevations, 50 A. polytrichoides cushionsof different sizes were selected randomly. Previously,metallic hoops of 20 cm, 30 cm, 40 cm and 50 cm dia-meter were prepared. At each selected cushion, ametallic hoop of similar diameter was placed on thesurface of the cushion and individual plants foundinside the hoop were identified and recorded. Then,the same metallic hoop was placed at random on theopen ground at least 1m away from the cushion,where again we identified and recorded all plants. At4500m, ten cushions of 20-cm, 19 of 30-cm, 17 of 40-cm and four of 50-cm diameter were recorded. At4700m, these numbers were 15, 27, seven and one forcushions of 20-, 30-, 40- and 50-cm diameter, respec-tively. Hence, 30-cm diameter was the most abundantsize class at both elevations. Vegetation sampling wasdone on 15 and 16 August 2008, when most plantswere in flower, thus facilitating the identification ofspecimens to species level. Voucher specimens weredeposited in the herbarium of Kunming Institute ofBotany, Chinese Academy of Sciences (KUN).

To statistically test for positive associations ofindividual plant species for either cushion plant orbare ground, we performed randomization tests(Slade & Hall 1999) using RESAMPLING STATS(Resampling Stats Inc., Arlington, VA, USA, 1990-95). For this, from the total abundance of a parti-cular species, we randomly redistributed the totalnumber of individuals between the within and out-side cushion habitats. For each species weperformed 1000 runs of random re-distributions,and calculated the probability of the observed fre-quency within cushions being generated by chance(see also Cavieres et al. 2002, 2006).

Microclimate measurements

At each elevation we characterized the microcli-matic changes induced by the presence of A.polytrichoides cushions by measuring the substratetemperature and water content. Measures were takenover two intervals from 26 May to 2 June and from14 to 20 August 2008, which correspond to the typi-cal dry and rainy periods during the growing season.In addition, the nitrogen, phosphorus and potassiumavailability in soil samples beneath cushions andfrom bare ground was measured at each elevation.

Temperature

At each elevation, four cushions of ca. 30 cm indiameter were randomly selected along with a point

Fig. 1. Upper: Arenaria polytrichoides cushion showingapproximately hemispherical growth form (this cushion isca. 30-cm diameter). Lower: Landscape of the communitydominated byA. polytrichoides cushions at high elevationsin the Sino-Himalayas.

1050 Yang, Y. et al.

on the bare ground located at least 3m away in arandom direction from the cushion. A temperatureprobe (3.0-mm diameter and an active tip lengthof 5mm, Center Technology Corp., Taiwan) wasinserted to a depth of 2 cm in the centre of eachselected cushion. Additional probes were insertedat 2-cm depth on the selected spots on the bareground (Cavieres et al. 2005, 2008). The probeswere calibrated in ice-cold water before use, toconfirm stability and accuracy (deviation fromzero o1.01C, commonly o0.71C). Because one ofthe probes was damaged in the field, we measuredsoil temperature only at three points on the bareground at the lower elevation between 26 Mayand 2 June. All probes were connected to a four-channel thermocouple data logger (Center 309, datalogger thermometer, Center Technology) pro-grammed to record temperature every 150 sthroughout the measurement periods. The differ-ences between temperatures within cushions andthose on bare ground were analysed with a one-sample t-test.

Substrate water content

As several species depend on water available inthe top few centimeters of ground for germinationand early growth, we measured the water content ofcushions and open ground.

On 29 May and 17 August 2008, at each eleva-tion, five cushion plants ca. 30-cm diameter werecollected and stored in a stainless steel container. Inaddition, five soil samples were randomly collectedfrom the bare ground to ca. 15-cm deep using a tro-wel. Soil samples were immediately sealed instainless steel containers. Both the plants and thesoil samples were transported to the laboratorywithin 24 h. The fresh weights of samples were mea-sured immediately and water content wasdetermined by reweighing samples after 72 h in a751C drying oven. Differences in water content be-tween cushions and bare ground were assessed usinga factorial two-way ANOVA, where altitude (higherand lower elevation) and position (within cushionsand bare soil) were the fixed factors, and time (dry orwet season) was used as a co-variable.

Nutrient content of soil

At each elevation, ca. 5000-g soil samples werecollected from a depth of 15 cm beneath four ran-domly selected cushion plants of ca. 30 cm diametereach and from four randomly selected positions onthe bare ground. One of these samples was taken on

16 August 2007 while the other three were taken on18 August 2008. Samples were sealed in plastic bagsand sent to the Laboratory for Soil Analyses at theAgricultural Institute of Yunnan, where availablenitrogen (NH4

1, NO3� ), phosphorus and potassium

were measured. Data were not normally distributedso they were analysed using a Mann-Whitney non-parametric test.

Results

Species association patterns

A total of 37 and 34 plant species were recordedat the lower and the higher elevation sites, respec-tively (Table 1). Fourteen species were found only atthe lower elevation, while 11 species were only pre-sent at the higher elevation. At 4500m, 24 plantspecies were found growing within cushions of A.polytrichoides and 36 on the bare ground; at 4700m,those figures were 26 and 29, respectively. At thelower elevation, one species, Primula sinopurpurea,was found only within cushions, while 13 specieswere found growing only on bare ground. At thehigher elevation site these figures were five and eight,respectively (Table 1).

At 4500m, three plant species (8.1% of the totalfound at this elevation) were shown to be positivelyassociated with cushions, while 13 plant species(35.1%) were found more frequently outside thecushions (Table 1). In contrast, at 4700m, 14 plantspecies (41.2%) were found to be positively asso-ciated with cushions, and 11 plant species (32.4%)grew more frequently outside the cushions (Table 1).

Of the 23 species that were found at both eleva-tions, 11 changed the nature of their spatialassociation with A. polytrichoides in relation to ele-vation. Anaphalis nepalensis, Carex atrata,Potentilla arbuscula, Saxifraga aristulata, S. mela-nocentra, S. moorcroftiana and Trollius farrerichanged from a negative association with cushionsat 4500m to a positive association at 4700m.Meconopsis horridula, Potentilla hypargyrea, Rho-dodendron tapetiforme and Saxifraga wardii changedfrom a neutral interaction with cushions at 4500mto a positive association at 4700m. However, onespecies (Rhodiola nobilis) that had a positive re-lationship with cushions at 4500m changed to anegative relationship at 4700m. In addition, twospecies, Arenaria barbata and Corydalis adrienii, hada neutral interaction to cushions at 4500m thatchanged to a negative association with cushions at4700m.

Positive associations between Arenaria polytrichoides and other alpine plants 1051

Environmental modification by cushions

Substrate temperatureDuring the dry period, while temperatures

within cushions did not differ to those in bareground at the higher site (mean difference5 0.0143,t5 0.401, P5 0.688; Fig. 2a), cushions in the lowersite maintained significantly lower temperaturesthan those in surrounding areas (t5 � 61.060,

Po0.01; Fig. 2b). However, the mean differencebetween cushion and bare ground temperature wasonly of 1.71C. Bare ground and cushion tempera-tures at both elevations never exceeded 301C (Fig. 2aand b).

During the rainy period, at both elevations,temperatures within cushions were significantlylower than those in surrounding areas (4700m:mean difference5 � 1.7506, t5 � 92.454, Po0.01;

Table 1. Frequency of species withinArenaria polytrichoides cushions and in surrounding bare soil at two elevations (4500mand 4700m) in the Sino-Himalayas. P-values are from a randomization test. 1, significant positive association with cushion(a5 0.05); � , significant negative association with cushion. Abbreviations: An, Annual species; PH, Perennial herb; PRH,Perennial rhizomatous herb; PS, Perennial sedge.

Species Life form Within4500m

Outside4500m

Total Prob Within4700m

Outside4700m

Total Prob

Ajania khartensis PH 22 22 0 �Anaphalis nepalensis PRH 7 26 33 0 � 22 10 32 0.021 1

Arenaria barbata PH 19 10 29 0.072 40 65 105 0.006 �Arenaria trichophora PH 22 22 0 �Astragalus acaulis PH 4 4 0.059Carex atrata PS 99 149 248 0 � 327 39 366 0 1

Chrysosplenium griffithii RH 1 16 17 0 � 1 1 2 0.76Corydalis adrienii PRH 1 1 0.5 21 21 0 �Cremanthodium humile PH 3 39 42 0 �Cyananthus macrocalyx PH 55 98 153 0.001 �Delphinium likiangensis PH 2 2 0.24Draba alpina PH 1 2 3 0.515 1 12 13 0.003 �Eriophyton wallichii PRH 2 30 32 0 �Gentiana atuntsiensis PRH 4 4 0.059 4 1 5 0.175Gentiana ludlowii An 1 1 0.5 1 1 0.517Juncus leucomelas PRH 17 17 0 � 1 19 20 0 �Lagotis praecox PRH 1 1 0.517Lamiophlomis rotata PRH 4 4 0.059Meconopsis horridula An 2 2 0.24 13 3 16 0.014 1

Oxygraphis glacialis PH 2 2 4 0.062Pedicularis roylei PH 8 10 18 0.379 3 6 9 0.265Pedicularis trichoglossa PH 2 2 0.24Pleurospermum amabile PH 8 22 30 0.013 � 31 66 97 0 �Pleurospermum nanum PH 8 2 10 0.058Polygonum macrophyllum PRH 80 42 122 0.002 1 129 18 147 0 1

Potentilla arbuscula Shrub 2 10 12 0.016 � 7 7 0.012 1

Potentilla eriocarpa var.tsarongensis

PH 5 5 0.04 �

Potentilla hypargyrea PH 66 67 133 0.524 84 8 92 0 1

Primula sinopurpurea PH 2 2 0.24Pyrethrum tatsienense PH 7 3 10 0.158Ranunculus dongregensis PH 1 1 0.517Rheum delavayi PH 11 15 26 0.267Rhodiola fastigiata PRH 9 9 0.005 1

Rhodiola nobilis PH 26 1 27 0 1 6 30 36 0 �Rhododendron tapetiforme Shrub 9 12 21 0.343 26 4 30 0 1

Saussurea quercifolia PH 8 8 0.004 �Saussurea stoliczkae PH 123 32 155 0 1 64 64 0 1

Saussurea superba PH 1 2 3 0.515Saussurea velutina PH 2 2 0.24Saxifraga aristulata PH 15 70 80 0 � 60 19 79 0 1

Saxifraga flagellaris PH 3 3 0.137Saxifraga melanocentra PH 5 25 30 0 � 16 6 22 0.03 1

Saxifraga moorcroftiana PH 2 41 43 0 � 30 1 33 0 1

Saxifraga wardii PH 2 2 0.24 27 3 30 0 1

Sibbaldia cuneata PH 3 3 6 0.662Solms-Laubachia

linearifoliaPH 2 9 11 0.04 �

Trollius farreri PH 28 28 0 � 35 35 0 1

Viola delavayi PH 2 2 0.24

1052 Yang, Y. et al.

4500m: mean difference5 � 0.929, t5 � 3.379,Po0.01; Fig. 2c and d). Bare ground and cushiontemperatures did not drop below 01C or rise above251C at either elevation (see Fig. 2c and d).

Substrate water contentWater content of A. polytrichoides cushions was

significantly higher than that of soil samples frombare ground at both elevations (F5 93.360,Po0.01) and between dates within the growing sea-son (F5 48.877, Po0.01) (Fig. 3). During both thedry and wet periods, the water content of cushionsand of soil samples from bare ground did not differbetween the two elevations (dry period: cushions:P5 0.973, bare ground: P5 0.963; rainy period:cushions: P5 0.779, bare ground: P5 0.807; Fig. 3aand b).

Nutrient content of soils

While at 4500m the soil beneath A. poly-trichoides cushions and that from open areas did not

differ in nitrogen, phosphorus and potassiumavailability (nitrogen: Z5 � 0.577, P5 0.564;phosphorus: Z5 � 0.866; P5 0.386; potassium:Z5 � 1, P5 1; Table 2), at 4700m the differencesin nitrogen and potassium were significant (nitrogen:Z5 � 2.021, P5 0.043; potassium: Z5 � 2.309;P5 0.029; Table 2), with soils beneath cushionscontaining more available nitrogen and potassiumcompared to open areas. No significant differences insoil phosphorus were found between cushions andbare ground at the higher elevation site (Z5 0.145,P5 0.885; Table 2). In addition, there were no sig-nificant differences in nitrogen availability in soilbeneath cushions or from bare ground between thetwo elevations (cushions: Z5 � 0.289, P5 0.773,open areas: Z5 � 0.866, P5 0.386; Table 2). A si-milar pattern was observed with respect tophosphorus content (cushions: Z5 0.289, P5 0.773;open areas: Z5 0.577, P5 0.564; Table 2). By con-trast, the availability of potassium in soil samplesfrom bare ground at the lower site was significantlyhigher than in soil samples from bare ground at the

Fig. 2. Temperature recorded during the dry (a, b) and rainy (c, d) periods of the growing season within cushions ofArenariapolytrichoides and on bare ground in the Sino-Himalayas. (a), (c): Temperature at the higher elevation site; (b), (d): Tem-perature at the lower elevation site.

Positive associations between Arenaria polytrichoides and other alpine plants 1053

higher site (Z5 2.021, P5 0.043; Table 2). Theavailable potassium in soil beneath cushions did notsignificantly differ between the two elevations(Z5 � 0.289; P5 0.773; Table 2).

Discussion

Cushions of A. polytrichoides contain morespecies than equivalent open spaces in alpine areasof the Sino-Himalayas, suggesting that they act asnurse species for other plants in this stressful habi-tat. The increased percentage of plant species

positively associated with cushions in the higherelevation site indicates that the facilitative effect ofA. polytrichoides cushions increases with elevation.Similar results were reported for Bolax gummifera(Apiaceae) and Azorella monantha (Apiaceae), bothinhabiting sub-antarctic alpine regions in the Andes(Cavieres et al. 2002; Arroyo et al. 2003).

The increased association of plant species withcushions of A. polytrichoides at the higher elevationis likely due to several factors acting in concert.Previous studies on sub-antarctic mountains haveshown that cushions provide warmer habitats thanthe surrounding bare ground (Arroyo et al. 2003;Korner 2003). In addition, nurse cushions at highelevation in sub-tropical mountains generate a mi-crohabitat having fewer low temperatures thannearby bare ground (Cavieres et al. 2007). By con-trast, A. polytrichoides cushions at both elevationsmaintained similar or even lower temperatures thanopen areas, suggesting that mitigation of low tem-peratures cannot be regarded as an importantmechanism of facilitation by cushions in our studysite. However, cushions at low elevations in sub-tropical mountain areas create microhabitats with alower frequency of extreme high temperatures thanfound in bare ground (Cavieres et al. 2006, 2008).Bare ground temperatures in such habitats com-monly reach 35-401C (Cavieres et al. 2006, 2008),which is lethal for many alpine plant species (Korner2003), but bare soil temperatures in our sites neverexceeded 301C.

Moisture content of the substrate, rather thancold conditions, was indicated to be the crucial fac-tor for successful germination of seeds of somepioneer plant species in alpine areas (Stocklin &Baumler 1996). Although the Sino-Himalayan re-gion experiences a wet monsoonal climate duringmost of the growing season, higher radiation com-bined with low rainfall characterize the earlygrowing season. An extended winter drought ofabout 1 month, which is not uncommon, couldproduce substantial water limitations for seed ger-mination and subsequent seedling growth at highelevations (Korner 2003). Chambers et al. (1990)

Fig. 3. Moisture conditions, assessed as water content(%), inside and outside of Arenaria polytrichoides cush-ions at the higher (4700 m) and lower sites (4500 m) in thedry (a) and rainy periods (b) during the growing season.Error bars indicate 1 SE. Water content is plotted as meanvalues of five cushions and five bare ground points. Barswith different letters are significantly different (P � 0.05).

Table 2. Nutrient content of soil beneath and outsideArenaria polytrichoides cushions at the lower and higher elevation sitesin the Sino-Himalayas. Data are mean � 1 SE. Different letters indicate significant differences (Po0.05).

Nutrients (mg/kg) 4500m 4700m

Beneath Outside Beneath Outside

ElevationNH4

11NO3� 233.63 � 73.58a 143.18 � 36.19ac 197.37 � 26.64a 93.96 � 16.71bc

P 3.82 � 0.30a 2.67 � 0.94a 3.23 � 1.22a 3.15 � 1.08a

K 180.34 � 48.32a 142.68 � 19.27a 153.18 � 20.43a 76.54 � 13.55b

1054 Yang, Y. et al.

and Forbis (2003) demonstrated that seedling re-cruitment and survival of many species at NiwotRidge, Colorado, was higher in wetter micro-sites.Thus, the higher moisture within cushions could bean important factor in the nurse effect of A. poly-trichoides. However, we acknowledge that thedifferences found between cushions and open areasshould be considered with caution because ourweighing procedure did not allow the separation ofwater within tissues (which is not available for otherplants) from water outside tissues that is actuallyavailable for use by other species. Nevertheless, theabsence of succulent leaves and stems in A. poly-trichoides suggests that most of the water within thecushions is contained in the dead plant material andorganic matter that accumulates within the cushioncanopy.

Alpine cushions can act as litter traps, andcombined with the more favourable microclimateconditions within the cushion, this can create a veryfavourable micro-environment for the activity ofmicrobial and decomposer organisms, resulting inlocally increased nutrient release beneath cushions(Korner 2003; Escudero et al. 2004; Cavieres et al.2008). This effect is particularly important in nu-trient-poor environments, such as alpine habitats.However, few studies have emphasized the role ofmicro-site differences in nutrients as a driver for apositive association with cushions. Our study showsthat at the lower elevation, there was no differencein soil nutrients between cushions and bare ground,but at the higher elevation, soils beneath cushionshad significantly more nitrogen and potassium thanbare ground. Nitrogen is the most common nutrientlimiting plant growth in alpine areas (Korner 2003),and fertilization of alpine plants stimulates theirgrowth (Heer & Korner 2002). Chambers et al.(1990) demonstrated that establishment and growthof alpine plant seedlings in dependent upon nitrogenavailability.

Although much less studied than nitrogen, po-tassium has been found to increase plant resistanceto drought, mainly due to its role in osmotic adjust-ment and reduced transpiration, leading to higherwater-use efficiency (Bradbury &Malcom 1977; vanden Driessche 1991; Egilla et al. 2001). The im-portance of potassium in facilitation has not beenhighlighted until recently (Gomez-Aparicio et al.2005; Cavieres et al. 2008). Gomez-Aparicio et al.(2005) attributed the facilitative effects of shrubs ontree seedling establishment in Mediterranean mon-tane ecosystems to shading and modification ofpotassium content by the benefactors. Cavieres et al.(2008) suggested that the difference in potassium

content beneath facilitator species was related tovariations in nurse effects of different cushion spe-cies in the central Chilean Andes. Hence A.polytrichoides cushions might generate ‘‘fertile is-lands’’ for establishment of other plant species at thehigher elevation by increasing availability of nitro-gen and potassium. However, the responses ofalpine plants to fertilizers are reported to be specificto certain species, life forms and habitats (Bowmanet al. 1993). Fast-growing plants, particular grami-noids (sedges, grasses and rushes), obtain thegreatest advantage from elevated nutrient avail-ability of NPK fertilizer in alpine areas (Bowman etal. 1995; Heer & Korner 2002). The large number ofsedge individuals (Carex atrata; Table 1) recordedon the surface of cushions at the higher elevationseems to be related to a species-specific response ofthis plant life form to the higher nutrient micro-siteprovided by A. polytrichoides cushions.

Despite our focus on the generality of the cush-ion effect, a number of other responses wereobserved related to establishment on A. poly-trichoides cushions. For example, at higherelevation, 14 species showed a preference for cush-ions, but 19 species did not. Such variation supportsprevious findings of Cavieres et al. (2002, 2006), whosuggested that nurse effects of alpine cushions arespecies-specific. Thus, even though cushions providethe necessary conditions for many species at thehigher elevation, they do not facilitate establishmentfor all species (see also Fajardo et al. 2008). Somespecies have higher establishment and survival onbare ground away from cushions and this is likelydue to differences in stress tolerance and the ecolo-gical optimal growing conditions of different plantspecies (Wang et al. 2008).

In conclusion, our results show that facilitationby A. polytrichoides cushions is frequent and im-portant in alpine areas of the Sino-Himalayas.Further, the degree of facilitation by A. poly-trichoides cushions is stronger at higher elevation,which is likely related to the increasingly harsh soil,microclimate and nutrient conditions at higher alti-tudes. This facilitative effect of A. polytrichoidescushions is probably due to the higher availability ofsoil nutrients induced within the cushion, and theseconditions promote seed germination, juvenile plantestablishment and subsequent plant growth. Ourresults support previous hypotheses that harsh en-vironments might restrict acquisition of resourcesby plants, and any amelioration of these conditionsfrom the presence of a neighbour will favour growthto the extent that it outweighs the negative effects ofcompetition (Brooker & Callaghan 1998; Callaway

Positive associations between Arenaria polytrichoides and other alpine plants 1055

et al. 2002). Thus, it can be concluded that by pro-viding a more suitable microhabitat for therecruitment of other plants, A. polytrichoides cush-ions play an important role in structuring alpineplant communities at high elevations in the Sino-Himalayas.

Acknowledgements. This research was supported by Yun-

nan Natural Science Foundation (2008CC013 to Sun H),

the Natural Science Foundation of China (30625004,

40930209 to Sun H; 30900084 to Yang Y), the Knowledge

Innovation Program of the Chinese Academy of Sciences

(KSCX2-YW-Z-1019) and the Western Light Talent Cul-

ture Project (to Yang Y). LAC thanks the BBVA

Foundation and funds from P05-002 F ICM CONICYT

PFB-023 supporting the Institute of Ecology and Biodi-

versity (IEB). We thank R. Turkington (Vancouver) for

his great help in editing and improving the English of this

manuscript. T. Lindsay (Zurich) and two anonymous re-

viewers are thanked for their helpful comments on our

writing and the experimental design.

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Supporting Information

Additional supporting information may befound in the online version of this article:

Photo S1. Arenaria polytrichoides (Caryophyllaceae)cushion facilitates the establishment and growth ofother plant species at high elevations of the Sino-Himalayas.

Table S1.Daytime (08:00–20:00 h) data of mean( � SD), maximum and minimum air temperature(Ta, 1C), solar radiation (I, mmol� 1m-2 s� 2), re-lative humidity (RH, %) above ground level(0.15m) during the experiment in the dry and rainyperiods of the growing season in 2008. Means pre-sented in the table are for 12 h of 15-min and 5-minrecording values for the measurements during thedry and rainy periods, respectively. Weather condi-tions during measurements in the dry periodincluded sun on 7 days and snow on 1 day. Formeasurements in the rainy period, there was rain on5 days and 2 days with cloud cover and some rainshowers.

Table S2. The patch (hoop) size and number ofspecies found within and outside Arenaria poly-trichoides cushions at 4500m and 4700m in theSino-Himalayas.

Please note: Wiley-Blackwell is not responsiblefor the content or functionality of any supportingmaterials supplied by the authors. Any queries(other than missing material) should be directed tothe corresponding author for the article.

Received 8 December 2009;

Accepted 16 July 2010.

Co-ordinating Editor: Dr. Lindsay Turnbull.

Positive associations between Arenaria polytrichoides and other alpine plants 1057