Competition among three dune species: the impact of water availability onbelow-ground processes

A. Weigelt1,2,*, T. Steinlein1 and W. Beyschlag1

1Chair of Experimental and Systems Ecology, University of Bielefeld, 33501 Bielefeld, Germany; 2Currentaddress: Chair of Biogeography, University of Bayreuth, Bayreuth, 95440, Germany; *Author forcorrespondence (fax: +49 921 552315; e-mail: alexandra.weigelt@uni-bayreuth.de)

Received 21 March 2003; accepted in revised form 12 January 2004

Key words: Below-ground competition, Log response ratio, Root: shoot ratio, Sand dunes, Specific root length,Water availability

Abstract

We studied competitive interactions among three species �Corynephorus canescens, Hieracium pilosella andCarex arenaria� of different early successional stages on sand dunes. Our study focused on the influence of com-petition and water availability on biomass allocation patterns and the plasticity of root responses. Plants weregrown for one growing season in a simple additive �target-neighbour� design under low or ambient water supply.Overall competition intensity �e.g., above- and below-ground�, as well as root competition alone, were comparedusing control plants grown without competitors. Our results show high competition intensity leading to an aver-age target plant biomass reduction of 56% relative to controls. Competition was mostly below-ground. With in-creasing water availability, the competitive effect of H. pilosella on both of the other species decreasedsignificantly. All other tested species combinations were not influenced by water availability. Soil moistureseemed to be a key factor determining the plasticity of root responses. Under limited water availability, strongcompetitors caused a significant decrease of response ratio �lnRR� based on root: shoot ratios for H. pilosella andC. arenaria and a decrease in lnRR based on specific root length �SRL� for C. arenaria. Under sufficient watersupply, however, there was no significant effect of competition on root: shoot ratios for any of the species andonly C. arenaria in competition with C. canescens showed a lower lnRR based on SRL. These water-related,species-specific changes of root morphology and allocation patterns may point to an adaptive response to com-petition.

Introduction

Below-ground processes, and root competition inparticular, are very important in resource-poor habi-tats �Berendse 1979, 1982; Wilson 1993a, b; Grubb1994; Caldwell et al. 1996; Casper and Jackson 1997;Coomes and Grubb 2000�. One possible effect of be-low-ground competition could be changes in biomassallocation �Bleasdale 1966�. In many studies that havereported effects of competition on below-ground bio-mass, the direction of change was inconsistent anddiffered among species �e.g., Goldberg 1987; Gure-

vitch et al. 1990; Wilson and Tilman 1995; Casper etal. 1998�. More recent work points toward an increasein root biomass of competing plants �Gersani 2001;Wardle and Peltzer 2003�. Müller et al. �2000� foundthat biomass allocation was purely a matter of indi-vidual plant size with small plants having larger root:shoot ratios and postulated that any factor that influ-ences plant size will thereby change allocation. Incontrast, the results of Shipley and Meziane �2002�supported the balanced-growth hypothesis, whereplants will preferentially allocate biomass to organsharvesting the most limiting resource. Testing these

Plant Ecology �2005� 176:57-68© Springer 2005

contrasting theories for competing plants, Cahill�2003� showed that there was an increase in root:shoot ratios, which was due to reduced plant sizerather than adaptive plasticity. According to this re-sult, competition is just one factor reducing plant size.Whether the effect of competition on allocationchanges with resource availability is unknown.

Even if competition leads to a proportional increaseof root biomass, this may still not necessarily resultin an increase of total root length or surface area,which would be one precondition for higher resourceuptake capacities �Drew and Nye 1969; Itoh and Bar-ber 1983�. Other possibilities that might lead to en-hanced resource capture include physiologicalchanges in uptake rates or nutrient use efficiencies�Casper and Jackson 1997�. Studies measuring com-petition intensity between single plant species that in-clude detailed root measurements are rare though andmainly provided data for pot experiments. Presum-ably, this is due to methodological constraints ofquantitative harvest of roots and their telling apart fordifferent species – a virtually impossible attempt inmost field situations. Nevertheless, we fully agreewith Zobel and Zobel �2002� that below-ground pro-cesses cannot be neglected in competition experi-ments. The homogeneous sandy soil of sand dunesand the limited number of species with partly differ-ing root morphology provides an opportunity to studythese problems.

Plant communities on sand dunes often form quitestable early successional stages on a rather small spa-tial scale. With ongoing succession from bare sandysoil to a heathland community, resource availabilityand soil moisture content increase significantly�Lache 1976; Rode et al. 1993; Van Rheenen et al.1995; Weigelt et al. 2000�. Increasing water availabil-ity supports a trend towards higher competitionintensity in dry ecosystems �Kadmon 1995; Callawayand Walker 1997; Holmgren et al. 1997�. Alterna-tively, competitive hierarchies may vary with wateravailability �e.g., Jones and Walker 1993; Briones etal. 1998; Davis et al. 1999�. Direct effects of wateravailability on competition processes have mainlybeen studied in desert ecosystems leading to the fa-cilitation concept �Brooker and Callaghan 1998; Cal-laway 1997, 1998�. Fewer experiments, however,revealed an influence of water supply on thecompetitive strength of species where water is notnecessarily limited �Collet et al. 1996; Davis et al.1998; Weigelt et al. 2000� and some of these studiesfound no change in competition intensity with vary-

ing water availability �Reader and Best 1989; Belcheret al. 1995; Wetzel and Van der Valk 1998�.

We studied the influence of competition and wateravailability on biomass allocation patterns and theplasticity of root responses. We conducted a field-likeexperiment with pair-wise competition treatments ofthree early successional species of sand dunes. Thesespecies dominate early successional stages with dif-fering soil water availability. The main objectives ofour study were to test the effect of water availabilityon competitive interactions of these species, and tostudy the effect of below-ground competition on bio-mass allocation to roots and root morphology.

Methods

Species description

Competitive interactions were studied using Coryne-phorus canescens �L.� P. Beauv., Hieracium pilosellaL. and Carex arenaria L. All three species are abun-dant on European coastal dunes as well as inland sanddunes not associated with the sea, where they arepredominantly found in early successional stages. C.canescens �Grey Hair-grass� is a tufted wintergreenperennial grass that occurs on open sand. The specieshas a finely divided, fibrous root system without rhi-zomes. Its roots grow mainly downwards �Marshall1967�. H. pilosella �Mouse-ear Hawkweed� is astoloniferous perennial, with extended clonal growth,often found in denser vegetation. H. pilosella forms afine, web-like, rather superficial root system with in-tensive lateral growth �personal observation�. Thethird species, C. arenaria �Sand Sedge� is a sympo-dial plant that forms an extensive perennial rhizomesystem. C. arenaria is generally more abundant in drygrasslands and sometimes in open pine forests onsand. A distinctive morphological feature of the spe-cies is root dimorphism. Each shoot has one or twolarge sinker roots along with several finer roots�Noble 1982�.

Experimental design

To study above- and below-ground competitive inter-actions, the three species were grown together in anexperimental “sand pit” �20 m long, 6 m wide, 1.2 mdeep�, divided into four chambers �6 m long, 5 mwide�, filled with sieved sand �mean nutrient contentin 0 � 30 cm: 0.003 total N % d.wt; 0.10 mg NO3-N

58

* kg–1; 0.03 mg NH4-N * kg–1; 0.099 total C % d.wt�.The sand pit was located in a common garden areanext to the University of Bielefeld, Germany. Differ-ences between the separated chambers of the sand pitwere tested in the year 2000, when no water or othertreatment was imposed on the site. We found no sig-nificant differences between the four chambers forNH4-N �Anova, F � 0.20, p � 0.90, n � 34�, NO3-N�Anova, F � 0.41, p � 0.74, n � 34� and pH CaCl2�Anova, F � 0.17, p � 0.92, n � 34�.

Plants of all species were grown from seeds col-lected from approximately 20 maternal plants from anarea of 100 � 20 m with patchy vegetation of allearly successional stages, at the “Senne”, a sand dunearea near Bielefeld �08°40’E 51°57�N�. They weresown for germination 3 months prior to the start ofthe experiment. Mean total dry weight ��/- s.e.� perplant at the start of the experiment was equal for H.pilosella �0.38 �/- 0.02 g� and C. canescens �0.32 �/-0.02 g� while C. arenaria plants had less mass �0.13�/- 0.00 g� although they were equal or greater inheight. After planting �19-22 April 1999�, plants weregrown in a one-factorial randomised block designwith water availability as the variable factor. Toachieve differences in water supply �low vs. ambientwater availability� a rainout-shelter was constructedto cover two of the four sand pit chambers. The shel-ter was a semi-transparent plastic that was fixed on aflexible, stainless steel tube and rope construction. Itwas closed manually during heavy rainfall events andeffectively reduced the amount of rain in the low wa-ter treatment chambers �sum of precipitation over thevegetation period: 103.8 mm; mean ��/- s.e.� soilwater content 2.85 �/- 0.33% d.wt� compared to thechambers with ambient water supply �321.2 mm; 3.95�/- 0.25% d.wt�. This treatment mimicked an inten-sive drought period, which had been previously mea-sured in the field �Weigelt et al. 2000� and was started6 weeks after planting. Before this, sufficient waterwas provided to the plants in all chambers. Thedrought treatment never exceeded potentially naturalconditions e.g., dry periods of over 10 � 14 days andthe plants never showed indications of wilting. Dur-ing drought periods, the plants which received ambi-ent water supply were additionally watered withcollected rainwater, thus simulating a rather wet sum-mer.

Competition plots were planted as a target-neigh-bour design with one target plant and 6 border plantsseparated by 9 cm. In order to measure the effect ofbelow-ground competition alone, a net tied back the

shoots and leaves of neighbouring plants so that atarget in the centre of the net was not shaded byneighbours, but was surrounded by neighbour roots.Plastic net �40 � 40 cm; mesh: 1.0 � 1.0 cm� wasfastened to the soil surface at the centre of the plotusing four bamboo poles each 15 cm long. The cen-tre portion �5 � 5 cm� of the net was cut out for thetarget plant. The outer corners of the net were held10-15 cm above the soil surface using bamboo polesof 30 cm length. Nets were installed during planting.Another treatment, planted to measure abovegroundcompetition, failed due to methodological difficultiesand is not reported. We planted 12 species combina-tions �i.e., control, intra- and interspecific competitionfor the three species� in two competition treatments�total- or below-ground competition� with or withoutwater. Each single treatment was replicated 8 times,with 4 replicates in a randomized block design perchamber, resulting in a total of 384 plots.

Harvest

During October 11-14, after 5 ½ months of growth,all plots were harvested completely and plants werecarefully washed and separated in the lab. The rootstructure and morphology of the three species is verydifferent, thus enabling us to separate them. Above-and below-ground parts of single plants were driedfor at least 72 h at 70 °C. Total root length and aver-age root diameter were determined before drying.Root measurements were performed with a transpar-ency scanning module �Snap Scan 1236, Agfa� com-bined with specialised software �WIN Rhizo 4.0regular, Instruments Régent INC, also see Bouma etal. 2000�. Because of their enormous number and finestructure, dry weight only was determined for rootsof C. canescens.

Data analysis

To quantify competition intensity the log ResponseRatio �lnRR, Goldberg et al. 1999� was calculated as

lnRR � ln�Pcontr ⁄ Pmix� �1�

where Pcontr represents performance of a single targetplant grown alone �control� and Pmix represents per-formance of a target plant grown in intra- or interspe-cific competition �see Weigelt and Jolliffe 2003 for acomparison of this index with other competition in-

59

dices�. Here performance is total biomass, root: shootratio, specific root length or total root length. LnRRwas calculated separately for plants with root compe-tition alone, where control and competing targetsgrown with netting were compared, and for plants intotal competition using the targets grown withoutnetting.

Differences in biomass allocation patterns depend-ing on the competition treatments were assessed us-ing root: shoot ratios, where rhizome dry weight ofC. arenaria was included as root biomass �accordingto Noble et al. 1979� while stolons of H. pilosellawere considered to be shoot biomass.

All biomass, length and calculated variables weretested for differences between species and treatmentsusing factorial Anova in General Linear Models�GLM; independent variables: water availability andcompetition treatments� and post-hoc Tukey �HSD�tests. All statistical analyses were performed withStatistica for Windows �Version 5.5, Statsoft Tulsa�.

Results

To assess differences among species, we used a com-petition index �lnRR�, but for an easier comparisonwith other studies and future meta-analysis, the origi-nal data might be more suitable. Table 1 thereforeprovides means of all parameters for each treatment.

Biomass and log Response Ratio

Mean lnRR values based on total biomass of targetsof C. canescens, H. pilosella and C. arenaria revealedsubstantial competitive interaction with significantlydiffering magnitudes between the target species andvarying neighbours � Figure 1�. Under both, high andlow water availability, C. canescens was always themost effective competitor while C. arenaria had onlya minor effect. The position of H. pilosella in this hi-erarchy, however, varied with changing water avail-ability. In general, H. pilosella had an equally highcompetitive effect as C. canescens, but under suffi-cient water supply, targets of C. canescens and C.arenaria were significantly less affected by neigh-bours of H. pilosella. On average, the presence ofneighbouring plants reduced biomass production oftarget plants by 56% compared to control plants.

The treatment to distinguish between the influencesof total versus below-ground competition had no ef-fect on the total biomass of neighbours �Table 2�. Ta

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60

Hence, the differences measured for target plantsgrown either with or without netting, was due to thereduced shading or below-ground competition byneighbours, as intended, and not to a lower neighbourbiomass. For target plants, Table 3 compares the re-sults of root and total competition for all target spe-cies giving mean total biomass of plants growingalone �control� or in an intra- or interspecific mixture.For all combinations of target and neighbouring spe-cies, no significant difference between total competi-tion and root competition alone could be detected.

Root: shoot ratio and log Response Ratio

Within single competition treatments and for controls,higher water supply led to an increase in root: shootratios in many cases �Table 1�. However, lnRR basedon root: shoot ratio was low, indicating a minor effectof competition on root: shoot ratio under high wateravailability with a few exceptions �Figure 2�.

Intraspecific competition in C. canescens and compe-tition of H. pilosella with C. arenaria resulted in adecrease in root: shoot ratio �positive lnRR� whilecompetition with H. pilosella as neighbours for H.pilosella and C. arenaria as targets, caused anincrease in root: shoot ratio and negative lnRR.

Low water availability, in contrast, caused an in-crease in root: shoot ratio only in highly competitiveenvironments, resulting in negative lnRR values�Figure 2�. This was most obvious for H. pilosella,where both competition with conspecifics and C. ca-nescens had a significantly higher effect on root:shoot ratios than all other treatments. For C. arenaria,only competition with C. canescens had a signifi-cantly higher effect than intraspecific competition,while H. pilosella as neighbour had an intermediateeffect on root: shoot ratio changes. C. canescens wasgenerally less affected with only small changes ofroot: shoot ratio relative to control plants. However,the effect of competition on root: shoot ratio was sig-

Figure 1. Log response ratio �lnRR, see methods� based on total biomass of target plants of Corynephorus canescens �Cc�, Hieracium pi-losella �Hp� and Carex arenaria �Ca� with the same three species as neighbours. Given are means � � SE� of total and below-ground com-petition treatments for low �open bars� and sufficient �closed bars� water availability. Different letters indicate significant differences withineach diagram �MANOVA, post-hoc Tukey �HSD� test p � 0.001 for all but C. canescens, where p � 0.05, n � 16�. Note the difference inscales between the diagrams.

Table 2. Mean total biomass of border species per plot � � SE� across all treatments with total competition �above and below-ground com-petition; no netting� and with below-ground competition alone �netting mounted around the target plant to tie back neighbour shoots� for allthree study species.

Neighbours root � shoot competition root competition df t p

C. canescens 30.19 � 1.29 29.64 � 1.21 98 0.311 0.757H. pilosella 21.58 � 1.17 23.98 � 1.37 98 � 1.329 0.187C. arenaria 6.58 � 0.90 6.62 � 0.61 96 � 0.867 0.388

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nificantly different between low and high water avail-ability for intraspecific competition and lnRR wassignificantly lower in high �intraspecific� compared tolow �with C. arenaria� competition.

Root morphology and log Response Ratio

Figure 3 �A, B� shows the mean lnRR based on spe-cific root length �SRL� for targets of C. arenaria andH. pilosella under low and high water availability. It

reveals different changes of SRL with increasingcompetition intensity for both species.

C. arenaria showed a significant decrease of lnRR,suggesting strong competitive interactions � Figure3A�. High competition intensity, e.g., with C. cane-scens or with H. pilosella under dry conditions, ledto a significant increase of SRL and therefore a highlynegative lnRR based on this parameter. Lower com-petition, e.g., with H. pilosella in high wateravailability or with intraspecific neigbours, resulted insignificantly lower changes of SRL and higher lnRR.

Table 3. Total biomass �mean � SE� of target plants of C. canescens, H. pilosella and C. arenaria growing either alone �control� or incompetition with the same three species as neighbours. The table compares total competition with root competition alone. Different superiorletters indicate significant differences for each target species �ANOVA, post-hoc Tukey �HDS� test p � 0.05; n � 16�.

root � shoot competition root competition

target: C. canescensneighbour species control 16.65 � 1.57 a 16.87 � 1.60 a

C. arenaria 13.57 � 1.24 ab 15.59 � 1.04 a

H. pilosella 9.77 � 1.29 bc 9.96 � 1.55 bc

C. canescens 3.95 � 0.53 d 5.13 � 0.64 cd

target: H. pilosellaneighbour species control 7.94 � 0.83 a 11.43 � 1.02 a

C. arenaria 8.47 � 0.84 a 7.96 � 0.71 a

H. pilosella 2.39 � 0.34 c 2.14 � 0.35 bc

C. canescens 1.24 � 0.15 c 1.72 � 0.25 bc

target: C. arenarianeighbour species control 4.40 � 0.75 a 4.32 � 0.67 a

C. arenaria 2.06 � 0.41 ab 3.63 � 0.63 a

H. pilosella 1.07 � 0.22 b 1.05 � 0.22 b

C. canescens 0.39 � 0.12 c 0.32 � 0.05 c

Figure 2. Log response ratio �lnRR� based on root: shoot ratio of target plants of C. canescens �Cc� H. pilosella �Hp� and C. arenaria �Ca�with the same three species as neighbours. Given are means � � SE� of total and below-ground competition treatments for low �open bars�and sufficient �closed bars� water availability. Different letters indicate significant differences within each diagram �MANOVA, post-hoc Tukey�HSD� test p � 0.05; n � 16�. Note the difference in scales between diagrams.

62

Overall, SRL of C. arenaria was strongly affected bycompetition. Particularly in drier conditions, this spe-cies developed not only proportionally more, but alsolonger roots per dry weight in highly competitivesituations. In contrast, H. pilosella revealed only mi-nor changes of root morphology � Figure 3 B�. Onlythe effect of competition with C. canescens in highwater availability differed significantly from lnRR indrier conditions, but the absolute values of lnRR werevery small. For H. pilosella, the allocation towardsmore root biomass was not concurrent with modifi-cations in root structure.

Total root length of both species was reduced un-der competition �Table 1�. In consequence, lnRRbased on total root length significantly increased withincreasing competitive strength of neighbouring spe-cies �Fig 3 C, D�. For H. pilosella as target, compe-tition with C. canescens and intraspecific neighboursunder both high and low water supply resulted in asignificantly higher lnRR than competition with C.

arenaria �Figure 3 D�. However, targets of C.arenaria under low water availability showed no sig-nificant increase of lnRR for differing neighbour spe-cies, while there was a significant difference betweenC. arenaria and C. canescens as neighbours underhigh water availability � Figure 3 D�. Overall, the ef-fect of competition on total root length reduction washigher for H. pilosella than for C. arenaria.

For a comparison of the effect of competition ontotal biomass with its effect on root structure, Figure4 gives a regression of lnRR based on total biomasson lnRR based on root: shoot ratio �A�, SRL �B� androot length �C�. Figure 4 �A� shows that there is nosignificant relationship between the effect of compe-tition on biomass and its effect on root: shoot ratiofor C. arenaria, where very high lnRR based on bio-mass results in only minor changes of root: shoot ra-tio for both high and low water supply. The sameholds for H. pilosella in high water availability, whilein low water supply the relative changes of total bio-

Figure 3. Log response ratio �lnRR� based on specific root length �SRL� and total root length for targets of C. arenaria �A, C� and H.pilosella �B, D� in competition with C. canescens �Cc�, H. pilosella �Hp� or C. arenaria �Ca�. Given are means � � SE� of total and below-ground competition treatments for low �open bars� and sufficient �closed bars� water availability. Different letters indicate significant differ-ences within each diagram �MANOVA, post-hoc Tukey �HSD� test p � 0.05; n � 16�. Note the difference in scales between diagrams.

63

mass and biomass allocation are strongly correlated�r2 � 0.99, F � 1211.2, p � 0.018�. For SRL and C.arenaria as target species, there is a significant cor-relation including both water treatments �r2 � 0.95, F� 69.33, p � 0.001�, while here H. pilosella showsno relationship whatsoever � Figure 4 B�. The effectof competition on total root length is significantlycorrelated to its effect on overall biomass for bothspecies �Hp: r2 � 0.97, F � 111.6, p � 0.0005; Ca:r2 � 0.90, F � 36.98, p � 0.004�. The slope of thisregression, however, is higher for H. pilosella �a �

0.74� than for C. arenaria �a � 0.38�, indicating alower effect of intense competition on root length forC. arenaria � Figure 4 C�.

Discussion

Competition intensity above and below-ground

The experiment revealed intense competition for allthree species � Figure 1� with C. canescens being themost effective and C. arenaria the weakest competi-tor. The result of the competitive hierarchy might ap-pear to be a density or biomass effect, because theoverall plant biomass of the species follows the sameorder as the competitive effect of species �Table 1�. Aprevious paper on the same experiment, however,clearly demonstrated that the competitive effect isspecies specific rather than purely related to biomass�Weigelt et al. 2002�.

As a further overall result we found no significantdifference between total and below-ground competi-tive interactions �Table 2�. Although shoot and rootcompetition are often assumed to have additiveeffects on plant growth, some studies provideevidence to the contrary �e.g., Casper and Jackson1997�. Cahill �1999, 2002�, however, suggested thatthere should be no interaction between the two com-petitive forms in unproductive sites. We thereforeconclude that the reduction of species biomass in thepresent experiment is due to significant below-groundcompetitive interactions, while aboveground interfer-ence for light was not detectable despite of consider-able overlap and shading of target plants in thecontrol treatment without netting.

The effect of water availability

Low compared to ambient water supply mainly de-creased the competitive effect of H. pilosella on theother species and decreased its competitive responsebased on root: shoot ratio. To explain this situation, itis important to remember that sand dunes are inher-ently nutrient poor. Although water availability wasthe variable factor in this experiment, the study spe-cies may also have been nutrient limited to differingextents. Field observations show that, with ongoingsuccession from bare sandy soil to a heathland com-munity, there is a significant increase in soil watercontent, organic material and total nitrogen content�Lache 1976; Van Rheenen et al. 1995; Weigelt et al.

Figure 4. Regression plots of lnRR based on root: shoot ratio �A�,specific root length �B� and total root length �C� against lnRR basedon total biomass for targets of C. arenaria �grey� and H. pilosella�black� in competition with the neighbour species C. canescens�triangle�, H. pilosella �circle� or C. arenaria �square�. Given aremeans over total and below-ground competition treatments for low�open symbols� and sufficient �closed symbols� water availability.Lines show significant regressions for C. arenaria �grey lines� andH. pilosella �black line�. Note the difference in scales betweendiagrams.

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2000�. Although occurring together in several inter-mediate stages, the species studied here grow mostvigorously in different successional stages in the field.C. canescens most effectively colonises open, inher-ently nutrient poor sand areas, while C. arenariagrows more vigorously on moister, but still nutrientpoor, downhill sites. In contrast, H. pilosella ratherdominates on drier, but less nutrient poor grasslandstages, where it forms dense plaques of rosettes. Anearlier competition study on a more nutrient richsandy soil revealed a high competitive strength of H.pilosella under favourable nutrient conditions �datanot shown�. For this reason, under the high water andlow nutrient conditions of our experiment, H.pilosella was most likely primarily nutrient limited,while both grasses were able to use additional waterfor higher biomass production. Overall, water is cer-tainly an important factor affecting competitive bal-ances in sand dunes, but it is unlikely to be theexclusive force driving plant community changesduring succession in this system. Rather, the close in-terplay between water and nutrient supply finally de-termines single stages of vegetation and theirdevelopment over time.

Effect of competition on root: shoot ratio

Cahill �2003� found an increased root: shoot ratio un-der competition for 10 grassland species and demon-strated that this was due to reduced plant size ratherthan adaptive plasticity. According to this result,competition is just one factor reducing plant size. Thisis certainly true for the current study where below-ground competition led to a mean target biomass re-duction of over 50%. More specifically, there was asignificant increase of lnRR based on total biomassfor all targets in response to C. canescens at low andhigh water availability, and in response to H. pilosellaat low water availability. In contrast, none of the tar-gets in competition with C. canescens showed a sig-nificant change in lnRR based on root: shoot ratio athigh water availability. There was, however, apronounced effect in drier conditions for two of thetree study species �C. arenaria and H. pilosella�,which showed a significant increase in root: shoot ra-tio in response to strong competitors �H. pilosella, C.canescens� under drought conditions �Figure 2�. As aresult, competition intensity based on root: shoot ra-tio was significantly correlated with that based on to-tal biomass only for H. pilosella in the low watertreatment �Figure 4 A�, thereby indicating that alloca-

tion shift might be at least partly adaptive rather thansolely biomass dependent. Of course, having dataonly from three species, care should be taken in gen-eralizing these results, but they show at least for somespecies, that biomass allocation is not simply a mat-ter of plant size and that resource availability, specifi-cally water, could interfere with a plant’s allocationresponse to competition.

Effect of competition on root structure

Other than biomass allocation, below-ground compe-tition could also change morphological characteris-tics, notably specific root length �Aerts et al. 1991;Aerts and Chapin 2000�. So far, studies have shownthat low allocation of biomass to roots may be com-pensated for by a higher SRL �Berendse and Elberse1989; Boot and Den Dubbelden 1990; Aerts et al.1991� and that nutrient shortages might lead tochanges in SRL �Christie and Moorby 1975; Boot andMensink 1990�. The results of the present study shownot only a higher allocation to roots but also an in-crease in SRL in response to a high competitive ef-fect from neighbouring plants �Figure 3 A�. Thisplasticity in root growth, however, was found only forC. arenaria and, again, was more pronounced underlow water availability. H. pilosella showed no signif-icant changes of SRL in response to differing neigh-bour species. Total root length was reduced in bothspecies, leading to a significant increase of competi-tion intensity based on this factor with increasingcompetitive strength of neighbouring species �Figure3 C, D and Figure 4 B, C�. This effect was less pro-nounced for C. arenaria where both, biomass alloca-tion and higher SRL compensated for the reductionin root length due to competition, which could be animportant factor for the remaining resource acquisi-tion of this species.

In combination with plant competition, changes inroot density in response to plant interactions havebeen assessed �Caldwell et al. 1991, 1996� and rootlength data has been measured in some pot experi-ments �Hartley and Amos 1999; Genney et al. 2000;Leuschner et al. 2000; Wardle and Peltzer 2003�.Other studies provide results on root proliferation inresponse to nutrient patches �Jackson and Caldwell1989; Fransen et al. 1998; Robinson et al. 1999;Hodge et al. 1999, 2000; Fransen et al. 2001�. To ourknowledge, only two studies included the measure-ment of root length in field experiments on plantcompetition, and both found a species specific

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increase of SRL in the presence of interspecificneighbours �Jastrow and Miller 1993; Huber-San-nwald et al. 1996�. Both, however, measured compe-tition relative to monocultures and therefore quanti-fied the difference in intra- versus interspecificcompetition, rather than to plants growing alone. Likethe ability to allocate more biomass to root structuresin competitive situations, variation in root morphol-ogy is highly species-specific. As a possible responseto strong competition, it might be a decisive factor forthe acquisition of water and nutrients on resource-poor soils.

Conclusion

Our results show a significant effect of below-groundcompetition on all three dominant plant species fromsand dunes, whereas water availability significantlyaltered the competitive effect of only one of the spe-cies. However, soil moisture seemed to be a key fac-tor determining the plasticity of root responses tosevere competition. We found species-specificchanges in biomass allocation to roots and in rootmorphology in response to competition that dependedon soil water supply. These results might point to anadaptive response of root morphology and allocationpatterns to competition rather than a mere biomassdependency at least for some species. Further studiescombining the measurement of below-ground struc-tures with plant competition are needed to gathermore insight into the processes of below-ground plantinteractions and their effects in different plant com-munities.

Acknowledgements

We are grateful to Elke Furlkröger and ChristineSchlüter for field and laboratory assistance and to Ul-lrich Richhardt and Gerd Drexler for technical sup-port. Kate A. Harrison and two anonymous reviewersprovided useful comments on an earlier version of themanuscript.

References

Aerts R., Boot R.G.A. and Van der Aart P.J.M. 1991. The relationbetween above- and belowground biomass allocation patternsand competitive ability. Oecologia 87: 551–559.

Aerts R. and Chapin F.S. 2000. The mineral nutrition of wild plantsrevisited: a re-evaluation of processes and patterns. Advances inEcological Research 30: 1–67.

Belcher J.W., Keddy P.A. and Twolan-Strutt L. 1995. Root andshoot competition intensity along a soil depth gradient. Journalof Ecology 83: 673–682.

Berendse F. 1979. Competition between plant populations withdifferent rooting depths. Oecologia 43: 19–26.

Berendse F. 1982. Competition between plant populations withdifferent rooting depths. III. Field experiments. Oecologia 53:50–55.

Berendse F. and Elberse W.T. 1989. Competition and nutrientlosses from the plant. In: Lambers H., Cambridge M.C. andKonings H. �eds�, Causes and consequences in variation ingrowth rate and productivity of higher plants, pp. 269-284. Aca-demic Publishing, The Hague, The Netherlands.

Bleasdale J.K.A. 1966. Plant growth and crop yield. Journal ofEcology 52: 665–676.

Boot R.G.A. and Den Dubbelden K.C. 1990. Effects of nitrogensupply on growth, allocation and gas exchange characteristics oftwo perennial grasses from inland dunes. Oecologia 85:115–121.

Boot R.G.A. and Mensink M. 1990. Size and morphology of rootsystems of perennial grasses from contrasting habitats as affectedby nitrogen supply. Plant and Soil 129: 291–299.

Bouma T.J., Koutstaal B., Van Dongen M. and Nielsen K.L. 2000.Coping with low nutrient availability and inundation: rootgrowht responses of three halophytic grass species from differ-ent elevations along a flooding gradient. Oecologia 126: 472–481.

Briones O., Montana C. and Ezcurra E. 1998. Competition inten-sity as a function of resource availability in a semiarid ecosys-tem. Oecologia 116: 365–372.

Brooker R.W. and Callaghan T.V. 1998. The balance between posi-tive and negative plant interactions and its relationship to envi-ronmental gradients: a model. Oikos 81: 196–207.

Cahill J.F. 1999. Fertilization effects on interactions betweenabove- and belowground competition in an old field. Ecology 80:466–480.

Cahill J.F. 2002. Interactions between root and shoot competitionvary among species. Oikos 99: 101–112.

Cahill J.F. 2003. Lack of relationship between below-ground com-petition and allocation to roots in 10 grassland species. Journalof Ecology 91: 532–540.

Caldwell M.M., Manwaring J.H. and Durham S.L. 1991. The mi-croscale distribution of neighbouring plant roots in fertile soilmicrosites. Functional Ecology 5: 765–772.

Caldwell M.M., Manwaring J.H. and Durham S.L. 1996. Speciesinteractions at the level of fine roots in the field: influence ofsoil nutrient heterogeneity and plant size. Oecologia 106: 440–447.

Callaway R.M. and Walker L.R. 1997. Competition and facilita-tion: a synthetic approach to interactions in plant communities.Ecology 78: 1958–1965.

Callaway R.M. 1997. Positive interactions in plant communitiesand the individualistic-continuum concept. Oecologia 112: 143–149.

Callaway R.M. 1998. Competition and facilitation on elevationgradients in subalpine forests of the northern Rocky Mountains,USA. Oikos 82: 561–573.

66

Casper B.B. and Jackson R.B. 1997. Plant competition under-ground. Annual Review of Ecology and Systematics 28: 545–570.

Casper B.B., Cahill J.F. and Hyatt L.A. 1998. Above-ground com-petition does not alter biomass allocated to roots in Abutilontheophrasti. New Phytologist 140: 231–238.

Christie E.K. and Moorby J. 1975. Physiological responses ofsemi-arid grasses I. The influence of phosphorus supply ongrowth and phosphorus absorption. Australian Journal of Agri-cultural Research 26: 423–436.

Collet C., Guehl J.M., Frochot H. and Ferhi A. 1996. Effect of twoforest grasses differing in their growth dynamics on the waterrelations and the growth of Quercus petraea seedlings. CanadianJournal of Botany 74: 1562–1571.

Coomes D.A. and Grubb P.J. 2000. Impacts of root competition inforests and woodlands: A theoretical framework and review ofexperiments. Ecological Monographs 70: 171–207.

Davis M.A., Wrage K.J. and Reich P.B. 1998. Competition betweentree seedlings and herbaceous vegetation: support for a theory ofresource supply and demand. Journal of Ecology 86: 652–661.

Davis M.A., Wrage K.J., Reich P.B., Tjoelker M.G., Schaeffer T.and Muermann C. 1999. Survival, growth, and photosynthesisof tree seedlings competing with herbaceous vegetation along awater-light- nitrogen gradient. Plant Ecology 145: 341–350.

Drew M.C. and Nye P.H. 1969. The supply of nutrient ions by dif-fusion to plant roots in soil. II the effect of root hairs on the up-take of potassium by roots of ryegrass �Lolium multiflorum�.Plant and Soil 31: 407–424.

Fransen B., De Kroon H. and Berendse F. 1998. Root morphologi-cal plasticity and nutrient acquisition of perennial grass speciesfrom habitats of different nutrient availability. Oecologia 115:351–358.

Fransen B., De Kroon H. and Berendse F. 2001. Soil nutrient het-erogeneity alters competition between two perennial grass spe-cies. Ecology 82: 2534–2546.

Genney D.R., Alexander I.J. and Hartley S.E. 2000. Exclusion ofgrass roots from soil organic layers by Calluna: the role of eri-coid mycorrhizas. Journal of Experimental Botany 51: 1117–1125.

Gersani M., Brown J.S., O�Brien E.E., Maina G.M. and AbramskyZ. 2001. Tragedy of the commons as a result of root competi-tion. Journal of Ecology 89: 660–669.

Goldberg D.E. 1987. Neighborhood competition on an old-fieldplant community. Ecology 68: 1211–1223.

Goldberg D.E., Rajaniemi T., Gurevitch J. and Stewart-Oaten A.1999. Empirical approaches to quantifying interaction intensitycompetition and facilitation along productivity gradients. Ecol-ogy 80: 1118–1131.

Grubb P.J. 1994. Root competition in soils of different fertility: aparadox resolved? Phytocoenologia 24: 495–505.

Gurevitch J., Wilson P., Stone J.L., Teese P. and Stoutenburgh R.J.1990. Competition among old-field perennials at different levelsof soil fertility and available space. Journal of Ecology 78: 727–744.

Hartley S.E. and Amos L. 1999. Competitive interactions betweenNardus stricta L. and Calluna vulgaris �L.� Hull: the effect offertilizer and defoliation on above- and belowground perform-ance. Journal of Ecology 87: 330–340.

Hodge A., Robinson D., Griffiths B.S. and Fitter A.H. 1999. Whyplants bother: root proliferation results in increased nitrogen

capture from an organic patch when two grasses compete. Plant,Cell and Environment 22: 811–820.

Hodge A., Stewart J., Robinson D., Griffiths B.S. and Fitter A.H.2000. Competition between roots and soil micro-organisms fornutrients from nitrogen-rich patches of varying complexity.Journal of Ecology 88: 150–164.

Holmgren M., Scheffer M. and Huston M.A. 1997. The interplayof facilitation and competition in plant communities. Ecology78: 1966–1975.

Huber-Sannwald E., Pyke D.A. and Caldwell M.M. 1996.Morphological plasticity following species-specific recognitionand competition in two perennial grasses. American Journal ofBotany 83: 919–931.

Itoh S. and Barber S.A. 1983. Phosphorus uptake by six plant spe-cies as related to root hairs. Agronomy Journal 75: 457–461.

Jackson R.B. and Caldwell M.M. 1989. The timing and degree ofroot proliferation in fertile-soil microsites for three cold-desertperennials. Oecologia 81: 149–153.

Jastrow J.D. and Miller R.M. 1993. Neighbor influences on rootmorphology and mycorrhizal fungus colonization in talgrassprairie plants. Ecology 74: 561–569.

Jones R.E. and Walker R.H. 1993. Effect of interspecific interfer-ence, light intensity and soil moisture on soybean �Glycine max�,common cocklebur �Xanthium strumarium�, and sicklepod �Cas-sia obtusifolia� water uptake. Weed Science 41: 534–540.

Kadmon R. 1995. Plant competition along soil moisture gradients:a field experiment with the desert annual Stipa capensis. Journalof Ecology 83: 253–262.

Lache D.W. 1976. Umweltbedingungen von Binnendünen- undHeidegesellschaften im Nordwesten Mitteleuropas. Scripta Geo-botanica 11: 5–96.

Leuschner C., Hertel D., Coners H. and Büttner V. 2000. Rootcompetition between beech and oak: a hypothesis. Oecologia126: 276–284.

Marshall J.K. 1967. Biological Flora of the British Isles – Coryne-phorus canescens. Journal of Ecology 55: 207–220.

Müller I., Schmid B. and Weiner J. 2000. The effect of nutrientavailability on biomass allocation patterns in 27 species of her-baceous plants. Perspectives in Plant Ecology, Evolution andSystematics 3/2: 115–127.

Noble J.C., Bell A.D.and Harper J.L. 1979. The population biol-ogy of plants with clonal growth I. The morphology and struc-tural demography of Carex arenaria. Journal of Ecology 67:983–1008.

Noble J.C. 1982. Biological Flora of the British Isles: Carexarenaria L. Journal of Ecology 70: 867–886.

Reader R.J. and Best B.J. 1989. Variation in competition along anenvironmental gradient: Hieracium floribundum in an abandonedpasture. Journal of Ecology 77: 673–684.

Reynolds H.L. and D’Antonio C.M. 1996. The ecological signifi-cance of plasticity in root weight ratio in response to nitrogen:Opinion. Plant and Soil 185: 75–97.

Robinson D., Hodge A., Griffiths B.S. and Fitter A.H. 1999. Plantroot proliferation in nitrogen-rich patches confers competitiveadvantage. Proceedings of the Royal Society of London, B 266:431–435.

Rode M.W., Leuschner C., Clauß C., Danner E., Gerdelmann V.,Margraf S. and Runge M. 1993. Changes in nutrient availabilityand nutrient turnover during heathland-forest succession in NWGermany. Scripta Geobotanica 21: 85–96.

67

Shipley B. and Meziane D. 2002. The balanced-growth hypothesisand the allometry of leaf and root biomass allocation. FunctionalEcology 16: 326–331.

Van Rheenen J.W.A., Werger M.J.A., Bobbink R., Daniels F.J.A.and Mulders W.H.M. 1995. Short-term accumulation of organicmatter and nutrient contents in dry sand ecosystems. Vegetatio120: 161–171.

Wardle D.A. and Peltzer D.A. 2003. Interspecific interactions andbiomass allocation among grassland plant species. Oikos 100:497–506.

Weigelt A., Röttgermann M., Steinlein T. and Beyschlag W. 2000.Influence of water availability on competitive interactionsbetween plant species on sandy soils. Folia Geobotanica 35:169–178.

Weigelt A., Steinlein T. and Beyschlag W. 2002. Is plant competi-tion more biomass or species dependent? Basic and AppliedEcology 3: 85–94.

Weigelt A. and Jolliffe P.A. 2003. Indices of plant competition.Journal of Ecology 91: 707–720.

Wetzel P.R. and Van der Valk A.G. 1998. Effects of nutrient andsoil moisture on competition between Carex stricta, Phalarisarundinacea, and Typha latifolia. Plant Ecology 138: 179–190.

Wilson S.D. 1993. Competition and resource availability in heathand grassland in the Snowy Mountains of Australia. Journal ofEcology 81: 445–451.

Wilson S.D. 1993. Belowground competition in forest and prairie.Oikos 68: 146–150.

Wilson S.D. and Tilman D. 1995. Competitive responses of eightold-field plant species in four environments. Ecology 76: 1169–1180.

Zobel K. and Zobel M. 2002. Studying plant competition: fromroot biomass to general aims. Journal of Ecology 90: 578–580.

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