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Basic and Applied Ecology 14 (2013) 574–584

acilitation vs. competition: Does interspecific interaction affect droughtesponses in Sphagnum?

hao-Jun Bua,b,d,∗, Xing-Xing Zhenga, Håkan Rydinc, Tim Moored, Jinze Maa

Institute for Peat and Mire Research, Northeast Normal University, State Environmental Protection Key Laboratory of Wetland Ecology andegetation Restoration, Renmin 5268, Changchun 130024, ChinaInstitute of Grassland Sciences, Northeast Normal University, Key Laboratory for Vegetation Ecology, Ministry of Education, Renmin 5268,hangchun 130024, China

Department of Plant Ecology and Evolution, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18D, SE-752 36 Uppsala,wedenDepartment of Geography and Global Environmental & Climate Change Centre, McGill University, 805 Sherbrooke Street West, Montreal,C, Canada H3A 0B9

eceived 30 January 2013; accepted 4 August 2013vailable online 31 August 2013

bstract

The stress-gradient hypothesis (SGH) predicts that the relative importance of competition decreases and facilitation increasesith an increase in abiotic stress. In peatlands, Sphagnum faces the threat of drought and differentiates into hummock species

drought-tolerant) and hollow species. Whether interspecific interaction affects the influence of drought on bryophyte compo-ition in peatlands is unknown. We established an experiment by simulating drought and building bryophyte communities withwo hummock species (S. palustre and S. capillifolium) and one hollow species (S. fallax). In all three species, drought decreasediomass production, height increment and side-shoot production. Sphagnum stores water in the hyaline cells, and leaf hyalineell percentage (HCP) in the two hummock species increased with drought while no effect was found in S. fallax, suggesting

the hollow species. Morphological traits and carbon and nitrogen

hat adjusting HCP is not an effective response to drought for ontents in hummock species responded more to drought than in the hollow species, indicating a rapid response in phenotypiclasticity is an important strategy to resist drought in the hummock species. The presence of neighboring Sphagnum species,ather than drought, decreased carbon content for all three species. All three bryophytes showed interaction between droughtnd neighbor in two or more plant traits. Our study, however, did not support SGH, and there were no changes from competitionnder wet to facilitation under dry treatments in any of the six species combinations. On the contrary, when S. fallax was thearget species, a change from facilitation under wet to competition under dry treatments was observed. The results suggesthat hummock species can facilitate hollow species in wet environments but they could suppress hollow species under droughtonditions by competing for water resources. Both drought and strong competition are the probable reasons why hollow speciesarely grow in hummocks.

∗Corresponding author at: Institute for Peat and Mire Research, Northeast Normal University, State Environmental Protection Key Laboratory of Wetlandcology and Vegetation Restoration, Renmin 5268, Changchun 130024, China. Tel.: +86 431 85098982; fax: +86 431 87628607.

E-mail address: buzhaojun@nenu.edu.cn (Z.-J. Bu).

439-1791/$ – see front matter © 2013 Gesellschaft für Ökologie. Published by Elsevier GmbH. All rights reserved.ttp://dx.doi.org/10.1016/j.baae.2013.08.002

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Z.-J. Bu et al. / Basic and Applied Ecology 14 (2013) 574–584 575

usammenfassung

Die Stress-Gradient-Hypothese (SGH) besagt, dass bei erhöhtem abiotischen Stress die relative Wichtigkeit interspezifischeronkurrenz abnimmt und die facilitation zunimmt. In Mooren, begegnet die Gattung Sphagnum der Gefahr der Austrocknungit der räumlichen Differenzierung in Bult- (trockenheitstolerant) und Schlenkenarten. Ob interspezifische Interaktion denffekt von Trockenheit auf die Artenverteilung in Bulten direkt beeinflusst, ist unbekannt. Ein Experiment zur Erforschunger Reaktion zweier Bultarten (S. palustre and S. capillifolium) und einer Schlenkenart (S. fallax) auf simulierte Trockenheiturde eingerichtet. Die Moose wurden zu Gemeinschaften zusammengestellt. Alle drei Arten reagierten mit verringertemiomassezuwachs, Höhenwachstum und Seitenastanlage. Sphagnum speichert Wasser in den Hyalinzellen. Als Reaktion aufie Trockenheit nahm der Anteil des Volumens der Hyalinzellen in den Blättern bei den beiden Bultarten zu, während keineeränderung bei S. fallax festgestellt werden konnte. Das lässt darauf schließen dass die Anpassung des Volumenanteils der Hya-

inzellen kein effektives Mittel zur Reaktion auf Trockenheitsperioden für Schlenkenarten ist. Morphologische Eigenschaftennd Kohlenstoff- und Stickstoff-Anteile veränderten sich ebenfalls mehr in den Bultarten als in der Schlenkenart. Dass lässtarauf schließen, dass phänotypische Plastizität eine wichtige Strategie der Bultarten ist um Trockenheit zu überstehen. Dieräsenz von in der Nachbarschaft befindlichen Sphagnum-Arten spielt wahrscheinlich eine größere Rolle für die Abnahme derohlenstoffkonzentration, als die Trockenheit. Alle drei Arten zeigten eine Interaktion zwischen Trockenheit und Nachbararten

n zwei oder mehreren Pflanzeneigenschaften. Unsere Untersuchung konnte dennoch die SGH nicht bestätigen, da kein Wandelon Konkurrenz zur facilitation beim Wechsel von feuchten zu trockeneren Bedingungen in allen sechs Artenkombinationenestgestellt werden konnte. Im Gegenteil, wenn S. fallax die Zielart war, wurde ein Wechsel von Anpassung unter feuchtenedingungen hin zu Konkurrenz unter trockenen Bedingungen beobachtet. Die Ergebnisse lassen vermuten, dass Bultartennter feuchten Bedingungen Schlenkenarten begünstigen aber sie bei Trockenheit durch ihre morphologische Flexibilität unter-rücken. Beide Faktoren, die Trockenheit und Konkurrenz, sind wahrscheinliche Gründe warum Schlenkenarten wenig in Bultenachsen.

2013 Gesellschaft für Ökologie. Published by Elsevier GmbH. All rights reserved.

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eywords: Drought-tolerance; Facilitation; Stress gradient hypothe

ntroduction

Plant–plant interaction includes competition and facilita-ion, both being key processes in building plant communities.he importance of facilitation in ecological processes had noteen paid much attention until the stress gradient hypothe-is (SGH) was proposed by Bertness and Callaway (1994).GH predicts that plant–plant interaction will shift from com-etition in benign environments to facilitation in stressedcosystems. The hypothesis set off an upsurge in studies toest interaction shift along stress gradients (e.g. Callawayt al. 2002) but few experiments have tested the SGHith bryophytes, the second largest group of plants (Spitale009).Bryophytes are poikilohydric plants and their water con-

ent is controlled by their environment. Hence, the growthBragazza 2008) and cover (Bates, Thompson, & Grime005) of bryophytes often decrease under drought condi-ions, and they usually grow densely to increase capillaritynd decrease water losses. SGH predicts that facilitationmong bryophytes should be more common than amongascular plants and many studies have shown facilitation inryophytes. For example, both yield and mean life expec-ation of Polytrichum alpestre increased with density in

he Antarctic (Collins 1976) and Polytrichum strictum, as

nurse plant, promoted Sphagnum establishment in peat-xtracted peatlands (Groeneveld, Massé, & Rochefort 2007).he greatest growth and productivity were observed in the

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rbon content; Nitrogen content

ensest colonies of Rhytidiadelphus triquetrus (Bates 1998).edersen, Hanslin, and Bakken (2001) found plant-plant

nteraction shifted along a gradient of aridty stress: underumid conditions, the growth rate in Dicranum majus andhytidiadelphus loreus decreased with density, and it peakedt an intermediate density due to facilitation in close pack-ng. In constructed bryophyte communities, an increase inpecies richness resulted in biomass increase in a droughtreatment, while no relationship was found in a moist envi-onment (Mulder, Uliassi, & Doak 2001).

Sphagnum is the dominant genus in peatlands, and anmportant function of carbon sink in peatlands is attributed tophagnum as the main peat-forming plant (Rydin & Jeglum006). Sphagnum grows in wet habitats and even may reachts maximum growth in over-wet conditions (Harris 2008;auhiainen & Silvola 1999; Schipperges & Rydin 1998).rought, however, is not rare in peatlands and drought-

olerance, including desiccation tolerance and desiccationvoidance (Glime 2007), is a strategy necessary for Sphag-um to face the threat from daily drought in midday duringummers or seasonal drought outside the rainy season. Sphag-um can avoid desiccation by virtue of its outstandingapillarity and water-holding ability (Glime 2007; Li, Glime,

Liao 1992; Rydin 1985). The individuals of Sphagnumrow closely with dense branches and leaves to hold more

ater and reduce water loss (Clymo & Hayward 1982). More

mportantly, there are two types of cells in the leaves ofphagnum, dead hyaline cells and living chlorophyllose cells.

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76 Z.-J. Bu et al. / Basic and A

he hyaline cells are much larger than chlorophyllose cellsnd they serve as water reservoirs to avoid desiccation inphagnum (Andrus 1986; Glime 2007). Water stored in hya-ine cells and capillary spaces among branches and leaves isalled “external water”, amounting to at least 50% of totalater volume in Sphagnum shoots (Hájek & Beckett 2008).

n peatlands, a hummock-hollow microtopography is com-on, with hummock mounds mainly formed by Sphagnum

pecies with strong vertical growth and slow decomposi-ion while hollows are depressions among the hummocksRydin & Jeglum 2006). According to their general distribu-ion along the hummock-hollow gradient, Sphagnum speciesan be termed hummock, lawn or hollow species. In contrasto hummock species, hollow species are more vulnerable torought because of their quicker drying (Li et al. 1992; Rydin,985). In mixed Sphagnum communities, hummock speciesith a higher water content (Wagner & Titus 1984) could

reate a wet microhabitat to facilitate hollow species (Glime007; Rydin 1985).Congeners of Sphagnum share morphological and physio-

ogical traits, but they differ in niche breadth and life historytrategy (Andrus 1986; Bragazza 1997; Gignac 1992; Rydin985). The congeners are ideal plants to test SGH sincehey could reduce confounding effects of other traits (He,ui, Bertness, & An 2012). Grime (1979) classified plant

trategies as trade-offs between competitive, stress-tolerantnd ruderal. Within Sphagnum, the drought-tolerant hum-ock species such as S. fuscum signal a stress-tolerancehile hollow species such as S. fallax and S. subsecundumave been regarded more as competitors (Bragazza 1997;ignac 1992; Laine, Juurola, Hájek, & Tuittila 2011). Itas been suggested that hummock species rarely grow closeo the water table because they are out-competed by hol-ow species, while hollow species hardly grow in hummocksue to their intolerance of drought (Bragazza 1997; Rydin985).Sphagnum is well known for its phenotypic plasticity in

esponse to environmental change. For example, ammoniuman decrease the cross-sectional area of leaf hyaline cells in S.apillifolium (Manninen, Woods, Leith, & Sheppard 2011).o reduce damage by drought, the volume of leaf hyalineells in S. magellanicum and S. papillosum increases, per-itting them to store more water under drought conditions

Li et al. 1992). It has also been observed that shoot den-ity increases with growth height above the water table inollow species, but not in hummock species (Rydin 1995).iochemical traits in Sphagnum can also respond to envi-

onmental change. In S. capillifolium, N concentration and:N ratio increased and decreased with shading, respectively

Manninen et al. 2011). According to the classical theory oflant life history strategy, competitors tend to have a higherrowth rate and phenotypic plasticity (Grime 1979). Hollow

pecies usually responded to water level rapidly in biomassnd height growth (Andrus 1986; Clymo & Hayward 1982)hile some hummock species such as S. fuscum showedo response (Mulligan & Gignac 2001). Drawdown of the

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cology 14 (2013) 574–584

ater level led to an increase of leaf length in the lawnnd low hummock species S. papillosum but showed noffect on leaf length in the hummock species S. magel-anicum (Li et al. 1992). In S. angustifolium, shoots fromollow habitats had long branches and high growth rates com-ared to shoots from dry habitats (Såstad, Pedersen, & Digre999).

Vascular plants generally allocate more C to non-tructural carbohydrates to resist severe abiotic stressGruber, Pirkebner, Florian, & Oberhuber 2012). Underrought conditions, the concentration of non-structural car-ohydrates increased in drought-tolerant clones or speciesut decreased in drought-susceptible clones or species (Piper011; Regier et al. 2009). Drought may greatly decrease

acquisition in vascular plants by affecting physiologicaletabolism and then decrease C:N ratio (Herms & Mattson

992). The global drought-affected area has increased inhe past four decades (Dai, Trenberth, & Qian 2004), and

ore frequent and intense droughts are expected in the futureIPCC 2007). Drought may affect 50% of Canada’s peatlandsTarnocai 2009) and negatively impact peatland bryophytese.g. Bragazza 2008). It is unknown if the effect of drought on

allocation and acquisition in vascular plants are also impor-ant for Sphagnum species. The general aim of this study iso test whether drought will affect performance and interspe-ific interactions among Sphagnum species, in the contextf the SGH. We took two hummock species, S. palustre, aeak competitor (Bu, Chen, & Rydin 2011), and S. capilli-

olium, and one hollow species, S. fallax, to test the followingypotheses:

1) drought will negatively affect all growth processesincluding biomass production, height increment andside-shoot production;

2) drought will increase the proportion of the leaves occu-pied by hyaline cell;

3) drought will decrease C content and C:N ratio;4) hollow species will show more responses to drought in

morphological traits (biomass production, height incre-ment, side-shoot production and hyaline cell proportion)and biochemical traits (C, N content and C:N ratio);

5) hollow species will inhibit hummock species throughtheir high competitive ability under wet conditions;

6) facilitation will occur in dry treatments where hum-mock species will reduce the effect of drought on hollowspecies.

aterials and methods

Sphagnum shoots were collected from Hani Peatland42◦13′ N, 126◦31′ E) in the Changbai Mountains, North-

ast China. The peatland is located in the temperate zone withrecipitation rate of 757–930 mm year−1. Mean temperaturesor January and July are −15.7 and 22.5 ◦C, respectivelyBu et al. 2011). Plant communities are diverse, and

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Z.-J. Bu et al. / Basic and A

phagnum, such as S. palustre L., S. capillifolium (Ehrh.)edw., S. magellanicum Brid., S. fuscum (Schimp.) Klinggr.

nd S. fallax (H. Klinggr.) H. Klinggr., are dominant in sometands.

In early October 2009, we collected Sphagnum shoots fromypical mono-specific hummock habitats for S. palustre and S.apillifolium and hollow habitats for S. fallax (voucher spec-mens were deposited at Northeast Normal University withollection numbers Bu 2009010001-3). After being cut to.0 cm, the shoots were inserted at a natural density into trans-arent cylindrical PVC pots with 6.3 cm inner diameter and6 cm height. To accurately measure performance includingiomass production, height increment and side-shoot produc-ion of the bryophytes, we prepared shoot bundles for eachpecies. Ten vigorous shoots, 9.0 cm long, of each speciesithout side-shoots or multiple capitula were bound with a

hin rubber band. The shoot bundles were inserted into thephagnum pots after removing a corresponding number ofhoots to retain the original density. We used a full factorialesign with three levels of species (S. palustre, S. capilli-olium and S. fallax), two levels of neighbor (mono- and

ixed culture) and two levels of drought (wet and dry) withve replicates.The bryophyte pots were cultured in a HPG-400HX

rowth chamber (Harbin Donglian Electronic & Technol-gy Development Co. Ltd). Similar to the climate in Hanieatland in July, we set the growth chamber at 27/20 ◦Cday/night), 180 mol m−2 s−1 PAR, and a 16-h photoperiod.

e established wet and dry conditions by manipulatingelative humidity (40% for both) and water table (6 and

cm for wet and dry conditions, respectively). Every sec-nd day we sprayed 4 ml distilled water to capitula to avoidevere drought and infused distilled water into the pots toaintain their initial water level. Every week we added

ml of Rudolph’s nutrient medium (Rudolph, Kirchhoff, &liesmann 1998) and the medium was renewed every foureeks.After 11 weeks of culture, we randomly chose 3 non-arked shoots and took a branch leaf 0.5 cm below the

apitulum for each shoot. One hundred and fifty leaf slicesere stained with crystal violet and we took digital photos forranch leaves from the convex surface under a microscopet a magnification of 400× for S. palustre and 1000× for. capillifolium and S. fallax. After colors were transformednto double primary colors and color threshold was adjusted,otal leaf hyaline cell area was measured and its percent-ge (HCP) was calculated with Adobe Photoshop software.ince Sphagnum leaves are one cell layer thick, HCP willeflect the relative volume of hyaline cells in the leaf. Heightncrement of shoot bundles was measured and side-shootsere counted. The parts between capitula and lower 8 cm

tems in the 10 shoots were cut off, oven dried at 70 ◦C for

4 h and represented biomass production. All the capitulaor one species in each pot were used to determine C and

content with dichromate oxidation and Kjeldahl methods,espectively.

(twS

cology 14 (2013) 574–584 577

To test neighbor effect and interaction type, we used thendex of relative neighbor effect (RNE) (Callaway et al.002):

NE = BW − B0

max(BW, B0)(1)

here BW and B0 correspond, respectively, to performance oflants with neighbors and without neighbors. Positive RNEalues indicate positive neighbor effects (facilitation) andegative values indicate negative neighbor effects (competi-ion). We calculated RNE with biomass production for eachair.

ata analysis

All statistical analyses were performed with SPSS for win-ows 13.0 (SPSS Inc., USA). Two-way ANOVA was used toxamine the main effects and interactive effect of drought andnterspecific interaction on plant traits of each species. Theffect of neighbor on plant traits and the effects of drought onNE were determined with one-way ANOVA, and the dif-

erence between RNE and zero was determined with a t-test.ukey HSD post hoc tests were used to identify interspecificifferences.

esults

ffect of drought

Drought decreased biomass production (P < 0.001 for all),eight increment (P < 0.001 for all) and side-shoots (P < 0.05or S. palustre, P < 0.01 for S. capillifolium and P < 0.001 for. fallax) (Fig. 1A–C, Table 1). All of them decreased by50% or more. HCP in the two hummock species increasedith drought (P < 0.001 for both) while no effect of droughtas found in S. fallax (Fig. 1D, Table 1). HCP in S. capil-

ifolium was higher than in S. palustre in both wet and dryreatments, while it was higher than in S. fallax only in thery treatment (P < 0.001 for all). In the wet treatment, HCPas lower in S. palustre than in S. fallax (P < 0.01), but theifference disappeared in the dry treatment. Drought had noffect on C content in any of the three species, whereas Nontent decreased and the C:N ratio increased in the dry treat-ent for S. palustre (P < 0.05) and S. capillifolium (P < 0.01)

Fig. 1E–G, Table 1).

ffect of neighbors

Interspecific neighbor decreased biomass productionP < 0.001) and side-shoot production (P < 0.05) in S. palustre

Fig. 2A and C, Table 1). Height increment of S. palus-re was smaller when growing with S. capilliflolium thanhen growing with S. fallax (P = 0.014) (Fig. 2B) HCP in. capillifolium was higher when growing with S. palustre or

578 Z.-J. Bu et al. / Basic and Applied Ecology 14 (2013) 574–584

Fig. 1. Main effect of drought on biomass production (A), height increment (B), side-shoot production (C), leaf hyaline cell area percentage(HCP) (D), C content (E), N content (F) and C:N ratio (G) of three Sphagnum species, S. palustre (Pal), S. capillifolium (Cap) and S. fallax(Fal). Biomass and side-shoot production are dry weight increase and number of side-shoots produced per 10 shoots. Data are mean ± 1SE( rence.

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n = 5). *P < 0.05; **P < 0.01; ***P < 0.001; ns, no significant diffe

rowing alone than when growing with S. fallax (P < 0.001or both) (Fig. 2D, Table 1). Interspecific neighbors signifi-antly decreased C content for all 3 species (P < 0.01 for S.alustre, P < 0.001 for S. capillifolium and P < 0.05 for S. fal-ax) (Table 1, Fig. 2E). Neighbor S. capillifolium increased

content of S. fallax (P = 0.002) (Fig. 2F). Both S. capilli-olium (P < 0.001) and S. fallax (P < 0.01) showed an effectf neighbor on C:N ratio (Fig. 2G, Table 1).

nteractive effect of drought and neighbor

All three species showed interactions between drought andeighbor in two or more plant traits. The negative neighborffect of S. fallax (P = 0.000) on biomass of S. palustre dis-ppeared in the dry treatment (Fig. 3A, Table 1). The positiveeighbor effect on height increment of S. palustre (P = 0.016)nd S. fallax (P = 0.000) on S. capillifolium was lost in thery treatment (Fig. 3B). The drought resulted in a positive

eighbor effect on HCP of S. fallax (P = 0.009) on S. palustreFig. 3C). In the wet treatment neighbor S. fallax decreasedCP of S. capillifolium, but the effect disappeared in dry

reatment (Fig. 3D). Although no drought effect was found

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n mono-populations, the HCP during drought of S. fallaxas significantly higher when S. palustre was a neighbor thanhen S. capillifolium was a neighbor (P = 0.014) (Fig. 3E).

nterspecific neighbors tended to switch the effect of droughtn C content from negative to null (Fig. 3F and H, Table 1)r even positive (Fig. 3G), independent of the target species.rought increased the C: N ratio of S. capillifolium when S.alustre was its neighbor (P = 0.016) (Fig. 3I).

elative neighbor effect (RNE)

There were no indications of a shift from competition underhe wet treatment to facilitation in the dry treatment for allhe six species combinations (Fig. 4). On the contrary, when. fallax was a target species and S. palustre was the neigh-or, there was a change from facilitation (P = 0.003) underhe wet treatment to competition (P < 0.001) under the dryreatment. When S. palustre was a target species, droughtecreased and increased RNE when S. capillifolium and S.

allax, respectively, were neighbors (P < 0.01 for both). Nonterspecific interaction occurred when S. capillifolium was

target species.

Z.-J. Bu et al. / Basic and Applied Ecology 14 (2013) 574–584 579

Table 1. Two-way ANOVA for effects of drought and neighbor on performance of three Sphagnum species. Neighbor effect denotes adifference among performances with and without a different neighboring species.

Species Index Drought Neighbor Drought × neighbor

F P F P F P

S. palustre Biomass production 178.321 <0.001 17.208 <0.001 10.678 <0.001Height increment 115.078 <0.001 5.152 0.014 0.140 0.870Side-shoot production 5.026 0.034 5.383 0.012 0.565 0.576HCP 63.721 <0.001 1.496 0.244 5.887 0.008C content 3.313 0.081 7.907 0.002 9.279 0.001N content 4.921 0.036 1.894 0.172 0.945 0.403C:N ratio 8.009 0.009 2.027 0.154 0.450 0.643

S. capillifolium Biomass production 44.694 <0.001 0.634 0.539 0.213 0.810Height increment 106.230 <0.001 2.969 0.070 3.512 0.046Side-shoot production 10.025 0.004 0.205 0.816 0.205 0.816HCP 40.250 <0.001 24.318 <0.001 9.791 0.001C content 0.647 0.429 13.347 <0.001 37.839 <0.001N content 12.743 0.002 1.329 0.283 2.663 0.090C:N ratio 16.506 <0.001 3.767 0.038 4.021 0.031

S. fallax Biomass production 79.930 <0.001 0.412 0.667 1.817 0.184Height increment 52.401 <0.001 0.795 0.463 0.055 0.946Side-shoot production 42.702 <0.001 0.673 0.519 2.747 0.084HCP 1.216 0.281 0.285 0.754 7.680 0.003C content 1.034 0.319 4.262 0.026 5.635 0.010N content 1.217 0.281 8.067 0.002 1.694 0.205C:N ratio 0.010 0.920 7.532 0.003 0.288 0.752

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iscussion

rowth responses to drought and phenotypiclasticity

Decreased water availability can reduce photosynthesisr biomass production in bryophytes (e.g. Harris 2008;auhiainen & Silvola 1999; Wagner & Titus 1984). In ourtudy, drought decreased not only biomass production butlso height increment and side-shoot production in all threepecies, with the decrease in the latter two traits attributedo less biomass allocation and confirming hypothesis 1. Gen-rally, once an individual of Sphagnum grows higher thants neighbors it will lose more water by evaporation (Rydin993a), thus lessening height increment is a response torought by decreasing water loss. High side-shoot produc-ion would increase density and decrease the openness ofphagnum colonies and hence also reduce water losses. How-ver, with a decline in biomass production it will be difficultor Sphagnum to increase side-shoot production.

Higher HCP in S. capillifolium than the other two specieseflects a higher water holding capacity in this hummock

pecies. HCP change could reflect water content change andven adaptation to drought in Sphagnum. Partially consistentith our second hypothesis, the simulated periodical droughtnly increased HCP in hummock species, suggesting that the

pip

ollow species is incapable of phenotypically adjusting itsCP in response to drought. When we consider the neighbor

ffect on HCP, the two hummock species were quite differ-nt. Under wet conditions, both of them facilitated the growthf S. fallax (Fig. 4), and S. capillifolium decreased its HCPhen it was neighbored by S. fallax, but S. palustre had no

uch effect. It is possible that water loss in the two Sphag-um species occurred in different parts: under wet conditions,. palustre lost water mainly from capillary spaces while S.apillifolium from both capillary spaces and hyaline cells.

In our study, contrary to the fourth hypothesis, the hum-ock species responded to drought by reducing N content

nd increasing HCP and C:N ratio, while no such effectsere found in S. fallax. It seems that the relationship between

ife history strategy and phenotypic plasticity described inascular plants is not applicable to Sphagnum, and a rapidesponse in phenotypic plasticity is an important strategy toesist drought in the hummock species (Rice, Aclander, &anson 2008). The three Sphagnum species showed different

esponses of phenotypic plasticity to interspecific neighbors:he two hummock species showed plasticity in both mor-hological and biochemical traits, while only plasticity iniochemical traits was observed in the hollow species. In mor-

hological traits, interspecific neighbors affected S. palustren its biomass production, length increment and side-shootroduction but affected S. capillifolium in its HCP.

580 Z.-J. Bu et al. / Basic and Applied Ecology 14 (2013) 574–584

Fig. 2. Main effect of neighbors on biomass production (A), height increment (B), side-shoot production (C), leaf hyaline cell area percentage(HCP) (D), C content (E), N content (F) and C:N ratio (G) of three Sphagnum species, S. palustre (Pal), S. capillifolium (Cap) and S. fallax( nd numm differe

C

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Fal). Biomass and side-shoot production are dry weight increase aean ± 1 SE (n = 5). Bars with different letters indicate significant

arbon, nitrogen and interspecific interaction

In Sphagnum species, there are specific patterns of resourcellocation to non-structural and structural carbohydrates:ompared to hummock species, hollow species possess a highercentage of non-structural carbohydrates (Turetsky, Crow,vans, Vitt, & Wieder 2008) which may help hollow species

esist drought. In our experiment, drought did not affect Content in neither drought-tolerant nor drought-susceptiblepecies. This suggests that possible changes in non-structuralarbohydrates need not affect C content in Sphagnum.

Sphagnum is rich in secondary phenolic compounds,hich may suppress the growth of many vascular plants

n peatlands (Van Breemen 1995; Verhoeven & Liefveld997). Our experiment found a negative effect of neighborn Sphagnum growth and, to our knowledge, this is the firsteport on neighbor effects on C content and C:N ratio inryophytes. Neighbors may force target species to excreteore C-rich phenolic compounds (Verhoeven & Liefveld

997) to suppress neighbors, resulting in a decrease in their content. In addition, N content in S. fallax showed no

esponse to drought while it decreased in the two hummockpecies, probably suggesting an advantage of N uptaken S. fallax over its neighbors especially S. capillifoliumFig. 2F). The unexpected effect of interspecific interaction

Sfi2a

ber of side-shoots produced per 10 shoots, respectively. Data arences analyzed by Tukey HSD tests (P < 0.05).

n C content, C:N ratio and the difference in resource com-etition between hummock and hollow species may have aar-reaching effect on carbon accumulation in peatlands.

rought, interspecific interaction and SGH

Contrary to our fifth and sixth hypotheses, RNE showedhat under wet conditions the hollow species S. fallaxnhibited the hummock species S. palustre but not S.apillifolium, and facilitation never appeared in all six com-inations in the dry treatment. Although there were nohanges from competition to facilitation along the droughttress gradient, changes from facilitation to competitionere observed. Under wet conditions, the two hummock

pecies, S. palustre and S. capillifolium, facilitate S. fallaxhile they compete with S. fallax under dry conditions.aestre and Cortina (2004) observed a similar pattern in

Mediterranean semi-arid area with a shift from facilita-ion under medium drought conditions to competition at highater stress level. In a simulated water level experiment,

capania undulata maintained competition with Warnstor-a exannulata all through a stable drought gradient (Spitale,009). In a post-mined peatland of Hokkaido, facilitationmong several vascular plants disappeared in an extreme

Z.-J. Bu et al. / Basic and Applied Ecology 14 (2013) 574–584 581

Fig. 3. Significant interactions between drought and neighbor in biomass production (A), height increment (B), leaf hyaline cell area percentageH pecies.m perform*

dmmoatiws

shdhS&

FpP*

CP (C–E), C content (F–H) and C:N ratio (I) of three Sphagnum sean ± 1SE (n = 5). Asterisks denote significant difference among

**P < 0.001, and ns means no significant difference.

rought year (Koyama & Tsuyuzaki 2012). SGH should beodified from a monotonic increase of facilitation to non-onotonic changes with a peak in the intermediate levels

f stress along a gradient of stress, and negative inter-ctions will be predominant again once stress becomesoo high (Kawai and Tokeshi 2007). In our experiment,

t seemed that the culture condition in the wet treatmentas wet for the hummock species but not the hollow

pecies. Hence, hummock species may facilitate hollow

pci

ig. 4. Relative neighbor effect (RNE) of the neighbors on Sphagnum paluairs indicate interactions: for example, “PC” indicates the effect of specie-values denote significance of differences between the wet and dry treatP < 0.05, **P < 0.01, ***P < 0.001, and ns means no significant differenc

Biomass production is dry weight increase per 10 shoots. Data areances under different neighbor conditions. *P < 0.05, **P < 0.01,

pecies by helping maintain a wet microhabitat but suppressollow species under drought conditions by absorbing waterirectly from hollow species due to their strong water-olding ability (Robroek, Limpens, Breeuwer, Crushell, &chouten 2007; Robroek, Limpens, Breeuwer, van Ruijven,

Schouten 2007). It probably means that the benefits

rovided by the benefactor, the hummock species, over-ome its own resource uptake when the limiting resources too scarce. Strong competition under drought conditions

stre (P), S. capillifolium (C) and S. fallax (F). Letters above columns C (neighbor) on the target species P. Data are mean ± 1SE (n = 5).ments, and asterisks denote RNE significantly different from zero.e.

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B

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82 Z.-J. Bu et al. / Basic and A

uggests that drought will make hummock species with strongater competitive advantage suppress co-existing hollow

pecies.RNE showed that S. palustre and S. fallax exerted

o neighbor effect on S. capillifolium suggesting strongrought-tolerance in S. capillifolium. It is similar to thetress-tolerant S. fuscum, which is nearly indifferent to allnvironmental factors including water level and bryophyteabitat (Mulligan & Gignac 2001). The low competi-ive ability of the stress-tolerant species brought about

positive effect on the competitor S. fallax under lowtress levels. However, unlike S. fuscum, which showed

weak competitive ability when close to the water tableGranath, Strengrom, & Rydin 2010; Rydin, 1993b), S.apillifolium still holds a competitive ability since itompeted with S. palustre under both wet and dry condi-ions.

Interspecific interaction could interact with environmen-al change and mediate the effect of environmental changen plants (Brooker 2006; Bu et al. 2011). In our experiment,he effect of neighbor on plant traits was dependent on theater status, including production of S. palustre, height incre-ent of S. capillifolium, HCP and C content of all the three

pecies and C: N ratio of S. fallax. In this experiment, inter-pecific neighbors marginally reduced the disfavored effectf drought on plant morphological traits, no matter whichas the target species. Drought lessened the neighbor effectn biomass production of S. palustre and height increment of. capillifolium. It also lessened the effect of neighbors on Content of all the three species. On the whole, there are fewrowth interactions between neighbors and drought as thereas no facilitation under dry conditions. Strong competitionade the performance of S. palustre and S. fallax under dry

onditions much poorer.The ecological differences between hummock and hol-

ow species have been studied for at least four decadese.g. Andrus 1986; Bragazza 1997; Clymo & Hayward982; Clymo & Reddaway 1971; Gignac 1992; Hájek &eckett 2008; Rydin 1985, 1993b; Wagner & Titus 1984)et there still are some disputes on the drought-tolerance ofhe two ecological groups of Sphagnum (Rydin, Gunnarsson,

Sundberg 2006). Although drought decreased growth ofhe three bryophyte species similarly in this study, hum-

ock species showed a higher phenotypic plasticity andhis advantage will emerge in the long run. The resultsodify the view that hummock species facilitate hollow

pecies in retaining water (Rydin 1985, 1993b; Wagner &itus 1984) and hummock species hold not only drought-

olerance but also competitive ability under dry conditions.nder severe stress conditions, a trade-off between stress-

olerance and competitive ability in Sphagnum seemed toe ineffective, and competition should be integrated into the

echanism of Sphagnum distribution on both ends of the

radient of water level. Both drought and strong competitionrobably are the reasons why hollow species rarely grow inummocks.

G

cology 14 (2013) 574–584

cknowledgements

This study was funded by the Natural Science Founda-ion of China (Contract No. 30700055 and No. 40971036)nd Operation Expenses for Universities’ Basic Scientificesearch of Central Authorities (No. 11GJHZ003). We thankaolin Zhao for plant material collection in the field, Hanguoiu for the lab work and Annett Thiele for German abstract

ranslation.

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