relationships between productivity, number of shoots and number of species in bryophytes and...

Journal of Ecology

2001

89

, 920–929

© 2001 British Ecological Society

Blackwell Science Ltd

Relationships between productivity, number of shoots and number of species in bryophytes and vascular plants

A. BERGAMINI, D. PAULI*, M. PEINTINGER* and B. SCHMID*

Institut für Systematische Botanik, Universität Zürich, Zollikerstrasse 107, CH-8008 Zürich, Switzerland,

*

Institut für Umweltwissenschaften, Universität Zürich, Winterthurerstrasse 190, CH-8057 Zürich, Switzerland

Summary

1

We measured species density, biomass and shoot density for both bryophytes andvascular plants in 90 small plots in 18 calcareous fens. In addition, we recorded leaf areaindex and litter mass of vascular plants. Our goals were: (a) to compare the relationshipbetween biomass and species density for the two taxonomic groups, (b) to test whetherbiomass and species density of bryophytes and vascular plants are related to their shootdensity, and (c) to assess the degree to which biomass, shoot and species density ofbryophytes are correlated with characteristics of the vascular plant layer.

2

For bryophytes there was a positive linear relationship between biomass and speciesdensity. Vascular plant species density was not related to biomass. Furthermore, bryophytebiomass and species density were linearly and positively related to bryophyte shoot density.For vascular plants, only biomass but not species density was related to shoot density.

3

We concluded that a bryophyte favourability gradient existed along which biomassand shoot and species density increased. This gradient was attributed to positive inter-actions within dense bryophyte stands, high clonal fragmentation, absence of competitivehierarchies and to the limited ability of larger bryophyte species to replace small speciesalong this favourability gradient.

4

Since species density for vascular plants varied independently from biomass andshoot density, there was no such favourability gradient as for bryophytes. Large sizevariation, predominantly negative interactions between species, and clonal integrationof species (e.g. tussock-forming grasses and sedges) may be responsible for the differentbehaviour of the two taxonomic groups.

5

Bryophyte favourability decreased with increasing vascular plant biomass. Concerninglight availability, we found highest bryophyte favourability at intermediate levels where thecombination of radiation and moisture seems to be optimal for bryophytes. No relationshipwas found between bryophyte favourability and vascular plant shoot density and litter mass.

6

The negative relationship between bryophyte favourability and vascular plant biomassis important for bryophyte conservation. Stands of low vascular plant production arethose with the potential for highest species richness, and should therefore receive con-servation priority.

Key-words

:

above-ground biomass, favourability gradient, positive interaction, speciesdiversity, wetlands

Journal of Ecology

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Introduction

Bryophytes are a major component of many plantcommunities in terms of both biomass and species

diversity (e.g. Vitt & Pakarinen 1977; Rieley

et al

. 1979;Longton 1984; Russel 1990). For example, in wet habitatssuch as fens and bogs, their biomass may exceed that ofvascular plants (e.g. Longton 1984; Wheeler & Shaw1991). Above-ground biomass or ‘productivity’ has beenconsidered to be one of the most important determinantsof species richness (Grime 1973, 1979; Rosenzweig &Abramsky 1993), and while for vascular plants this rela-tionship has received much attention since the studies

Correspondence: Ariel Bergamini, Institut für SystematischeBotanik, Universität Zürich, Zollikerstrasse 107, CH-8008Zürich, Switzerland (tel. + 41 1634 84 11; fax + 41 1634 84 03;e-mail [email protected]).

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of Grime (1973, 1979) and Al-Mufti

et al

. (1977), it ispoorly understood for bryophytes with the notableexception of rheophytic communities (Muotka &Virtanen 1995; Virtanen

et al

. 2001). We therefore focusupon the relationship between species number, biomassand shoot density of both bryophytes and vascularplants in 18 Swiss montane calcareous fens.

Species richness per unit area (hereafter calledspecies density following Magurran 1988) of vascularplants at the level of small plots (

≤

1 m

2

) is often reportedto be highest at intermediate levels of biomass. Thisleads to a ‘hump-shaped’ relationship between speciesdensity and biomass (reviewed in Grace 1999). Althoughthis pattern is perhaps not as widespread as was previ-ously thought (Waide

et al

. 1999), there is good evidenceto suggest that very high biomass values are antagonisticto high species densities (Marrs

et al

. 1996; Grace 1999).Furthermore, plot biomass depends on the number ofindividuals (or ramets for clonal plants) growing in aplot. Fisher

et al

. (1943) and Preston (1962), by linkingthe number of species to the number of individuals,proposed that the number of species should increasewith the number of individuals by a probabilistic effectof drawing different numbers of individuals from asingle pool. However, does this hold for systems, such ascalcareous fens, where most plant species grow clonallyand for bryophytes as well as for vascular plants?

Most bryophytes are ectohydric (Buch 1947), i.e.they neither possess roots nor an internal vascularsystem, and since water and nutrient uptake occursover the whole shoot surface, their size is restricted.Also, since bryophytes cannot regulate water loss, theyfrequently dry out and enter a physiologically inactivestate and, thus, are considered to be poikilohydricplants (Walter 1962). Physiological activity is prolongedwhere shoot density is high, because evaporative waterloss is reduced (Proctor 1982) and growth is thereforeoften best in dense stands (Bates 1988; Økland &Økland 1996; but see also Zamfir & Goldberg 2000).Such a positive effect of density on plant performanceis less common for vascular plants and may occur mostlyin communities growing in rather harsh environments(Callaghan 1987; Bertness & Callaway 1994).

Many studies have examined interactions amongbryophytes (recently reviewed by Rydin 1997) and effectsof bryophytes upon seedling emergence (e.g. Zamfir2000) but very few studies have considered how theperformance of the bryophyte layer is dependent uponstructural properties of the vascular plant layer (Watson1960; Sveinbjörnsson & Oechel 1992; Økland 1994).Nevertheless, structural properties of the vascular plantlayer, such as biomass, shoot density, leaf area index(LAI) and litter mass, seem likely to be important sincebryophytes are much smaller than most vascular plantsand interactions for light are thus asymmetric (Rydin1997). Light absorption of the vascular plant layerdepends mainly on the cumulative leaf area (Monsi &Saeki 1953) and, in addition to the effect of living tissues,a thick, persistent litter layer will inhibit the development

of a vigorous bryophyte layer (Cornish 1954; Wheeler& Giller 1982; van Tooren

et al

. 1988), mainly by heavyshading (Sveinbjörnsson & Oechel 1992). Dense standsof vascular plants could, however, benefit bryophytegrowth if they reduce evaporative water loss by increasedshading. Such contrasting effects could produce aunimodal relationship between biomass and shootdensity of bryophytes and variables related to vascularplant productivity. Moreover, if bryophyte speciesdensity is unimodally related to bryophyte biomass, thenbryophyte species density will be lowest at intermediatevascular plant productivity.

We asked the following specific questions:

1

Is their biomass an adequate predictor of the speciesdensity of bryophytes and vascular plants, and what isthe shape of each relationship?

2

Do biomass and species density of bryophytes andvascular plants depend upon their shoot density?

3

What is the relationship between the properties ofthe bryophyte community (biomass, shoot density andspecies density) and those of the vascular plant layer(biomass, shoot density, LAI and litter mass)? Whichvariable or combination of variables best explainsbryophyte variation?

Methods

We studied 18 montane wetlands located in the pre-Alpsof north-eastern Switzerland. The sites were randomlyselected from the inventory of Swiss fenlands (BUWAL1990). They are situated between 800 and 1400 m a.s.l.and distributed over an area of 3500 km

2

. The use ofextensive management practices (mowing once a yearin September) means that these montane wetlands canbe considered to be semi-natural communities. Annualprecipitation is relatively high throughout the studyregion (1500–2800 mm, Uttinger 1967). Sites have pre-dominantly north to north-western aspects and rangein size from 1 to 9.1 ha. The underlying bedrock con-sists of various calcareous sediments of tertiary andmesozoic age (Spicher 1972). Soil pH ranges from 5.4 to7.2 (mean 6.2) and the vegetation belongs mainly to theCaricion davallianae alliance (vegetation classificationafter Ellenberg 1996).

Species richness of both bryophytes and vascularplants is high (Peintinger 1999; Bergamini

et al

. 2001).Graminoids, such as

Carex davalliana

Sm.,

C. panicea

L.,

Molinia caerulea

Moench and

Festuca rubra

L., andforbs, such as

Potentilla erecta

(L.) Räuschel,

Trifoliumpratense

L.,

Lotus corniculatus

L.s.l. and

Succisa pratensis

Moench, are common (Plattner 1996; Peintinger 1999),and the bryophytes are usually dominated by pleuro-carpous mosses, with

Calliergonella cuspidata

(Hedw.)Loeske,

Climacium dendroides

(Hedw.) Web. & Mohr,

Campylium stellatum

(Hedw.) J. Lange & C. Jens,

Bryumpseudotriquetrum

(Hedw.) Schwaegr.,

Drepanocladuscossonii

(Schimp.) Loeske and

Plagiomnium elatum


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(B. & S.) T. Kop. being prominent components (Bergamini

et al

. 2001).Data were collected during August 1997 (i.e. at peak

vascular plant biomass) in five randomly selected plots,each of 20

×

20 cm (0.04 m

2

), at each site (total

n

= 90).Leaf area index (LAI) of vascular plants was used as anindicator of light availability for bryophytes and wasmeasured, using a LAI-2000 Plant Canopy Analyser(LI-COR Inc., Lincoln, Nebraska, USA), at four pointsfor each plot: one just above the vascular plant canopyand three within the canopy just above the bryophytelayer. LAI measurements are only available for 84 plotsdue to technical problems. We then clipped vascularplants just above the bryophyte layer and recorded thenumber of species and total shoot number (rametsrather than shoots were counted for clonal plants and,as these formed the majority of vascular plants, shootnumber did not equal genet number). Next, all bryo-phytes were collected, including their brown parts, andalso the litter of vascular plants. Litter was defined asunattached above-ground vascular plant material. Aprovisional list of bryophyte species was prepared inthe field and species identity was subsequently checkedin the laboratory after separation of litter and bryophytematerial. The dry weight of bryophytes (hereafter ‘bryo-mass’), vascular plants and litter was recorded afterdrying for at least 24 h at 70

°

C.After drying, a random subsample (compasing 100–

130 shoots) was taken from each bryophyte samplefrom each plot. Shoot number, including lateral branchesof indeterminate growth (offshoots, equivalent to themain shoot) greater than 10 mm, was counted beforeweighing and extrapolating to the whole sample (togive bryophyte shoot density in each plot).

Peak biomass (excluding the bottom layer of approx.3 cm) was used as a measure of vascular plant produc-tivity. Although bryomass is the result of accumulationand decomposition of biomass over several years, thereis good evidence that it is closely related to bryophyteproductivity (Wielgolaski

et al

. 1981; see also van Tooren

et al

. 1988). This was confirmed by our analyses of thedata of Rieley

et al

. (1979) and Pande & Singh (1988),both of which resulted in a highly significant positivelinear regression of bryophyte production on bryomass(

R

2adj.

= 87.2%,

P

< 0.001,

n

= 14, and

R

2adj.

= 85.3%,

P

< 0.001,

n

= 18, respectively).

We used regression models in which ‘site’ was included asblock factor. Plot values were thus adjusted for differ-ences between sites. Plots without LAI values (see above)were omitted from analyses of the effect of vascularplant variables on bryophyte variables, but the whole dataset was used otherwise. Variables were log-transformed(indicated in tables) whenever necessary to obtainnormally distributed residuals and/or to achieve homo-scedastic distributions of points around regressionlines. Both linear and quadratic terms were fitted but

only linear regressions are presented where the quadraticterm was not significant (

P

> 0.05). Irrespective ofsignificance, the quadratic term is then included to assesswhether the widely cited ‘hump-shaped’ relationshipapplies to bryophytes and vascular plants in this study.

To find the most parsimonious regression explainingvariation in bryophyte variables (bryomass, speciesdensity or shoot density), we used the forward selectionstrategy after Payne

et al

. (1993) with the inratio set to 4(criterion for including a variable in the multiple regres-sion equation). Since bryomass and log (bryophyte shootdensity) were unimodally related to LAI (see Results),the variables LAI and LAI

2

were treated as if they wereone variable in the forward selection. Data were evaluatedfor collinearity by the standard procedure provided byGENSTAT 5.0 program, release 3.2 (Payne

et al

. 1993).As a guide to the fit of the regression models we used

the adjusted

R

2

statistic after Payne

et al

. (1993), expressedas a percentage:

R

2adj.

= 100

×

(1

−

(residual mean squares/total mean squares))

All analyses were carried out with the GENSTAT5.0 program, release 3.2 (Payne

et al

. 1993).

Results

The bryophyte layer of the studied wetlands was gen-erally well developed, forming a continuous cover withbare soil rarely visible. Bryophyte species density perplot varied from 3 to 18 (mean 8.5

±

0.26, plot area =0.04 m

2

) and bryomass from 0.04 g to 13.2 g (6.3 g

±

0.39).Vascular plant species density (20.3

±

0.54; range 8–32)was higher than that of bryophytes. Mean biomass wasalso higher for vascular plants (15.9 g

±

1.27; range4.6–92.0.g) but in 19 plots, distributed over 12 sites,bryomass exceeded vascular plant biomass.

Shoot densities of bryophytes and vascular plantswere both very variable (8–45 946, mean 1421.4

±

107.1and 83–579, mean 248.7

±

10.4, respectively). Littermass was low, varying from 0.7 to 6.0 g per plot (mean2.4 g

±

0.10).There were significant (

P

≤

0.05) or marginally sig-nificant (

P

≤

0.1) effects of site in most regressions(Tables 1 and 2), indicating large-scale variability.

There was a positive relationship between speciesdensity and biomass (Table 1a, Fig. 1), but it was linearrather than unimodal (quadratic term not significant).In contrast, vascular plant species density was unrelatedto biomass (Table 1b, Fig. 1).

Species density of bryophytes increased with increasingshoot density, even when four outlying plots with lowdensities (Fig. 1) were omitted, but species density wasunrelated to shoot density in vascular plants (Table 1,Fig. 1).

Biomass was positively related to shoot density forboth groups (Fig. 1), although the relationship forvascular plants should be interpreted with caution,


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Table 1

Linear or quadratic regressions for the relationships between species density, biomass and shoot density for bryophytes andvascular plants. Percentage variance accounted for by each regression is the adjusted

R

2

statistic. *

P

≤

0.05, **

P

≤

0.01, ***

P

≤

0.001

Dependent variable Source of variation d.f. SS

F

-ratio

R

2adj.

(a) BryophytesSpecies density Site 17 141.60 2.33**

Bryophyte biomass 1 146.59 41.02***[Bryophyte biomass]

2

1 0.05 0.01Residuals 70 250.15 40.9%

Species density Site 17 141.60 1.95*Log [Bryophyte shoot density] 1 93.15 21.78***Residuals 71 303.65 29.3%

Log [Biomass] Site 17 6.09 12.84***Log [Bryophyte shoot density] 1 9.53 341.91***Residuals 71 1.98 85.9%

(b) Vascular plantsSpecies density Site 17 1135.69 4.21***

Log [Vascular plant biomass] 1 36.20 2.28(Log [Vascular plant biomass] )

2

1 40.67 2.56Residuals 70 1109.93 39.2%

Species density Site 17 1135.69 4.01***Log [Vascular plant shoot density] 1 3.24 0.19Residuals 71 1183.56 36.1%

Log [Biomass] Site 17 1.38 2.39**Log [Vascular plant shoot density] 1 0.25 7.27**Residuals 71 2.41 25.1%

Table 2

Linear or quadratic regressions for the relationships between properties of the vascular plant layer (biomass, shootdensity, litter mass and LAI) and bryophyte variables (biomass, shoot density and species density). Percentage variance accountedfor by each regression is the adjusted

R

2

statistic. †

P

≤

0.1, *

P

≤

0.05, **

P

≤

0.01, ***

P

≤

0.001

Dependent variable Source of variation d.f. SS

F

-ratio

R

2adj.

(a) Bryophyte biomass Site 16 318.82 2.41**Log [Vascular plant biomass] 1 209.07 25.30***Residuals 66 545.39 36.1%

Bryophyte biomass Site 16 318.82 1.88*Vascular plant shoot density 1 55.89 5.28*Residuals 66 698.57 18.1%

Bryophyte biomass Site 16 318.82 2.13*LAI 1 35.44 3.78†LAI

2

1 109.79 11.71***Residuals 65 609.23 27.5%

Bryophyte biomass Site 16 318.82 1.75†Litter mass 1 1.11 1.10Residuals 66 753.36 11.7%

(b) Bryophyte shoot density Site 16 20859232 1.65†Log [Vascular plant biomass] 1 16214755 20.53***Residuals 66 52133429 26.5%

Log [Bryophyte shoot density] Site 16 4.90 1.78†Vascular plant shoot density 1 0.29 1.71Residuals 66 11.34 13.7%

Log [Bryophyte shoot density] Site 16 4.90 1.95*LAI 1 0.15 0.92LAI

2

1 1.26 8.00**Residuals 65 10.23 21.0%

Log [Bryophyte shoot density] Site 16 4.90 1.74†Litter mass 1 0.01 0.04Residuals 66 11.62 11.6%

(c) Log [Bryophyte species density] Site 16 0.391 1.76†Log [Vascular plant biomass] 1 0.076 5.50*Residuals 66 0.914 16.8%

Bryophyte species density Site 16 137.26 1.59†Vascular plant shoot density 1 19.67 3.65†Residuals 66 355.88 12.7%

Bryophyte species density Site 16 137.260 1.51LAI 1 0.001 0.00LAI

2

1 9.858 1.75Residuals 65 375.549 8.9%

Bryophyte species density Site 16 137.26 1.51Litter mass 1 0.46 0.08Residuals 66 375.10 8.0%


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since biomass was more variable at high densities thanlow densities. Omitting the three plots with the lowestbiomass did not influence the outcome of the regressionfor bryophytes, which showed a much closer relation-ship than vascular plants (

R

2adj .

= 85.9% vs. 25.1%).The relationship between bryomass and the vascular

plant layer depended on the variable considered (Table 2a,Fig. 2a). Bryomass was negatively related to vascularplant biomass and vascular plant shoot density, butweakly unimodally related to LAI and unrelated to littermass.

Bryophyte shoot density was related only to vascularplant biomass (linear decrease) and LAI (unimodal,although this must be interpreted with caution, sinceshoot density was more variable at high and low lightavailability than at intermediate light availability(Table 2b, Fig. 2b)).

Bryophyte species density also declined with vascularplant biomass (Table 2c, Fig. 2c). Highest and lowest spe-cies densities were reached at intermediate light availabil-ity (Fig. 2C). Unlike for bryomass and bryophyte shootdensity this relationship was therefore not significant.

Fig. 1 Relationships between species density, biomass and number of shoots for two plant groups (bryophytes and vascularplants). Dependent variables are adjusted for the effects of site (see Methods). Regression lines are only drawn for significantrelationships (P ≤ 0.05).


Fig. 2 Relationships between bryophyte variables (a, biomass; b, shoot density; and c, bryophyte species density) and properties of the vascular plant layer (vascular plant biomass, vascular plant shoot density,LAI, and litter mass). Dependent variables are adjusted for the effects of sites (see Methods). Regression lines are only drawn for significant (P ≤ 0.05) relationships.

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For both bryomass and bryophyte species density,stepwise multiple regression showed that vascularplant biomass and light availability (LAI + LAI

2

) werethe best explanatory variables, although in the oppositeorder (Table 3). Both regressions explained only about40% of the variation of the dependent variables, indicat-ing that there are other major sources of variation. Bio-mass was the only vascular plant variable significantlycontributing to the explanation of bryophyte speciesdensity (Table 2c).

Discussion

,

The two taxonomic groups showed different biomass-species density relationships: there was a positive linearrelationship for bryophytes but no significant correla-tion in vascular plants. Neither showed the expectedunimodal relationship between biomass and speciesdensity as predicted by Grime (1973), Tilman & Pacala(1993) and Huston (1994).

No comparable data are available for wetland bryo-phytes. Virtanen

et al

. (2001), studying the relationshipbetween biomass and species density in rheophyticbryophyte assemblages, found three different patterns:a positive linear relationship in two streams (out of 14),a unimodal relationship in five streams, and no relationat all in seven streams. Unimodal relationships occurredonly in streams with largely different microhabitatsthat allowed for small-scale community diversification.

Our results for vascular plants were consistent withthe findings of some previous wetland studies (e.g.Vermeer & Verhoeven 1987; Moore & Keddy 1989),although others have detected a humped relationshipin such habitats (e.g. Wheeler & Giller 1982; Moore

et al

.1989; Garcia

et al

. 1993).A comprehensive review by Waide

et al

. (1999) showedthat only 30% of the studies investigating the biomass-species density relationship revealed a unimodal pattern

and there is growing evidence that this depends uponthe spatial scale that is studied (Moore & Keddy 1989;Waide

et al

. 1999; Weiher 1999; Gross

et al

. 2000;Virtanen

et al

. 2001). When studies within plant com-munities are considered, only 24% reveal a unimodalpattern, with 42% showing no relationship and 22% apositive one (Waide

et al

. 1999). The limited range ofbiomass values within a community may be too narrowto demonstrate an underlying unimodal relationship(Rosenzweig & Abramsky 1993; Grace 1999), consistenthere with the two plots with the highest vascular plantbiomass showing low species density but not with thebryophyte data (highest biomass in plots with highestnumber of species, Fig. 1). The influence of other variables(e.g. successional age or edaphic conditions of sites) mayalso affect productivity and thus the species density-biomass relationship (Gough

et al

. 2000; Loreau 2000).

Favourability gradients

The denser bryophytes grow, the more biomass theyproduce in total and the more species live together insmall plots (see Fig. 1). Økland (1994) was the first totalk about such bryophyte ‘favourability gradients’whereby the water content of the shoots rises as theirdensity increases (Proctor 1982) and bryophytes aretherefore able to remain photosynthetically active for agreater part of the growing season and show greaterbiomass production (Bates 1988). This positive density-dependent relationship appears to be a common phe-nomenon in bryophyte assemblages (e.g. Økland &Økland 1996; Økland 2000) and, in combination withhigh clonal fragmentation and the absence of competitivehierarchies (at least in comparable bryophyte commu-nities in chalk grasslands, During & van Tooren 1988),this is probably responsible for the parallel increases inbiomass, shoot density and species density.

In contrast, vascular plants showed no such favour-ability gradient. Although denser growing shoots pro-duced more biomass, species density was not related tobiomass or shoot density. Tilman & Pacala (1993) haveexplained decreases in vascular plant species density at

Table 3 Best multiple regressions for the relationships between properties of the vascular plant layer and bryophyte biomass orshoot density, respectively. For bryophyte species density the most parsimonious regression was on site and log [vascular plantbiomass]. Results of this regression are already presented in Table 2c. Percentage variance accounted for by each regression is theadjusted R2 statistic. *P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.001

Dependent variable Source of variation d.f. SS F-ratio R2adj.

(a) Bryophyte biomass Site 16 318.82 2.72**Log [Vascular plant biomass] 1 209.07 28.49***LAI 1 0.17 0.02LAI2 1 75.55 10.29**Residuals 64 469.67 43.2%

(b) Bryophyte shoot density Site 16 20859232 2.03*LAI 1 7284222 11.34***LAI2 1 11996153 18.68***Log [Vascular plant biomass] 1 7960968 12.39***Residuals 64 41106841 40.2%


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high levels of productivity as a response to light limita-tion. Under these conditions, slow-growing species areoutcompeted by a few highly competitive fast-growingspecies: according to an extension of the self-thinninglaw to thinning in mixed communities, larger speciesreplace smaller species under more productive conditions(Bazzaz & Harper 1976; Schmid 1991; but see Stevens& Carson 1999b). Although this may be true for somevascular plant communities, it seems unlikely for bryo-phytes, whose shoot size is much more restricted bymorphological and physiological constraints (cf. thetall herb

Angelica sylvestris

vs. the small grass Festucarubra). Thus, under more productive conditions, theincrease of bryomass per plot is likely to be mainly aneffect of increased shoot density, leading to the very closerelationship between these variables in bryophytes butnot in vascular plants.

Effects of clonality

The domination of the vegetation in these wetlands byclonal plants (personal observation) may have import-ant consequences for the relationship between speciesdensity and biomass. Specifically, the probability oftwo neighbouring shoots belonging to the same speciesis much higher than in communities dominated by non-clonal species, where species density and shoot densityare often found to be closely related (Condit et al. 1996;Stevens & Carson 1999a). The lack of a relationship forvascular plants was therefore as expected.

Most bryophytes exhibit clonal growth patterns(During 1990) and experimental evidence is growingthat physiological integration of ramets in ectohydricbryophytes may reach levels comparable with those ofclonal vascular plants (Alpert 1989; Økland et al. 1997;Eckstein & Karlsson 1999). There was, nevertheless, aclose relationship between bryophyte species densityand shoot density, suggesting dominance of non-clonalplants (cf. Stevens & Carson 1999a). Light limitation indense stands and therefore browning of shoots in thelower strata of the bryophyte canopy (van der Hoeven& During 1997), may lead to earlier physical disintegra-tion of connections between ramets and parent plants inbryophytes than in many clonal vascular plants, suchas tussock-forming grasses and sedges, so that physio-logical integration is unlikely to regulate bryophyteshoot density. Even in vascular plants, whether regula-tion of shoot density operates via physiological inte-gration or via external factors, is still a matter of debate(Suzuki & Hutchings 1997; Meyer & Schmid 1999).

Of all the measured variables of the vascular plantlayer, biomass was the best single predictor of each ofthe three, intercorrelated bryophyte variables, with bry-ophyte favourability decreasing with increasing vascular

plant biomass. There was a unimodal relationship betweenbryophyte favourability and light availability, mostlikely caused by a combination of optimal radiationand moisture at intermediate light levels, which leads tolonger periods of photosynthetic activity for the ecto-and poikilohydric bryophytes and, thus, to their highergrowth rates (Callaghan et al. 1978; Bates 1988; Økland& Økland 1996; Økland 2000). However, scatter in ourdata was high, indicating that important sources ofvariation were not included in our restricted set ofexplanatory variables. Marrs et al. (1996) proposedthat such variable data sets should be characterized byboundary conditions rather than by regression analysesthat obscure valuable information. This would includethe observation that values of bryophyte biomass, shootdensity and species density were particularly unpredictableat intermediate light levels, although favourability wasconsistently low at both ends of the gradient.

Litter mass of vascular plants accounted for only asmall part of the bryophyte variation, possibly due tothe low levels maintained by yearly mowing.

Although biomass is a rather crude descriptor of thestructure of the vascular plant layer (Spehn et al. 2000)and thus of the environment experienced by bryophytes(Watson 1960; Sveinbjörnsson & Oechel 1992), the neg-ative relationship is important for bryophyte conserva-tion: stands of low vascular plant production are richerin bryophytes. Since vascular plant growth in fens ismainly controlled by the availability of phosphorusand nitrogen (Verhoeven & Schmitz 1991; Pauli 1998),it is crucial to curb supply of these nutrients in order tomaintain bryophyte diversity.

Acknowledgements

We are grateful to the nature conservancy authoritiesof the cantons of Schwyz, Glarus, St Gallen andAppenzell-Ausserrhoden and to the land owners of theinvestigated sites who allowed us to conduct this study.We thank E. Urmi, P. Alpert, R. Økland and one anon-ymous referee for various comments which improvedearlier versions of the manuscript considerably,M. Naegeli for helping with the very time-consumingseparation of vascular plant litter and bryophytes, andM. Matthews for linguistic aid.

References

Al-Mufti, M.M., Sydes, C.L., Furness, S.B., Grime, J.P. &Band, S.R. (1977) A quantitative analysis of shoot phenologyand dominance in herbaceous vegetation. Journal of Ecology,65, 759–791.

Alpert, P. (1989) Translocation in the nonpolytrichaceous mossGrimmia laevigata. American Journal of Botany, 76, 1524–1529.

Bates, J.W. (1988) The effect of shoot spacing on the growthand branch developement of the moss Rhytidiadelphustriquetrus. New Phytologist, 109, 499–504.

Bazzaz, F.A. & Harper, J.L. (1976) Relationship betweenplant weight and numbers in mixed populations of Sinapisalba (L.) Rabenh. & Lepidium sativum L. Journal of AppliedEcology, 13, 211–216.


928A. Bergamini et al.

© 2001 British Ecological Society, Journal of Ecology, 89, 920–929

Bergamini, A., Peintinger, M., Schmid, B. & Urmi, E. (2001)Effects of management and altitude on bryophyte speciesdiversity and composition in montane calcareous fens.Flora, 196, 180–193.

Bertness, M.D. & Callaway, R. (1994) Positive interactions incommunities. Trends in Ecology and Evolution, 9, 191–193.

Buch, H. (1947) Über die Wasser und Mineralstoffversorgungder Moose I, II. Societas Scientiarium Fennica Commenta-tiones Biologicae, 9 (16), 1–44, 9 (20), 1–49.

BUWAL (1990) Inventar der Flachmoore Von NationalerBedeutung. Entwurf für die Vernehmlassung. Bundesamt fürUmwelt, Wald und Landschaft (BUWAL), Bern, Germany.

Callaghan, T.V. (1987) Plant population processes in arcticand boreal regions. Ecological Bulletins, 38, 58–68.

Callaghan, T.V., Collins, N.J. & Callaghan, C.H. (1978) Photo-synthesis, growth and reproduction of Hylocomium splendensand Polytrichum commune in Swedish Lapland. Oikos, 31,73–88.

Condit, R., Hubbel, S.B., Lafrankie, J.V., Sukumar, R.,Manokaran, N., Foster, R.B. & Ashton, P.S. (1996) Species-area and species-individual relationships for tropical trees:a comparison of three 50-ha plots. Journal of Ecology, 84,549–562.

Cornish, M.W. (1954) The origin and structure of the grass-land types of the central North Downs. Journal of Ecology,42, 359–374.

During, H.J. (1990) Clonal growth patterns among bryo-phytes. Clonal Growth in Plants: Regulation and Function(eds J. van Groenendael & H. de Kroon), pp. 153–176. SPBAcademic Publishing, The Hague, The Netherlands.

During, H.J. & van Tooren, B.F. (1988) Pattern and dynamics inthe bryophyte layer of a chalk grassland. Diversity and Patternof Plant Communities (eds H.J. During, M.J.A. Werger &J.H. Willems), pp. 195–208. SPB Academic Publishing, TheHague, The Netherlands.

Eckstein, R.L. & Karlsson, P.S. (1999) Recycling of nitrogenamong segments of Hylocomium splendens as comparedwith Polytrichum formosum: implications for clonal integra-tion in an ectohydric bryophyte. Oikos, 86, 87–96.

Ellenberg, H. (1996) Vegetation Mitteleuropas Mit Den Alpenin Ökologischer, Dynamischer und Historischer Sicht. Ulmer,Stuttgart.

Fisher, R.A., Corbet, A.S. & Williams, C.B. (1943) The relationbetween the number of species and the number of individualsin a random sample of an animal population. Journal ofAnimal Ecology, 12, 42–58.

Garcia, L.V., Maranon, T., Moreno, A. & Clemente, L. (1993)Above-ground biomass and species richness in a Mediter-ranean salt marsh. Journal of Vegetation Science, 4, 417–424.

Gough, L., Shaver, G.R., Carroll, J., Royer, D.L. & Laundre, J.A.(2000) Vascular plant species richness in Alaskan arctictundra: the importance of soil pH. Journal of Ecology, 88,54–66.

Grace, J.B. (1999) The factors controlling species density inherbaceous plant communities: an assessment. Perspectivesin Plant Ecology, Evolution and Systematics, 2, 1–28.

Grime, J.P. (1973) Competitive exclusion in herbaceous vegeta-tion. Nature, 242, 344–347.

Grime, J.P. (1979) Plant Strategies and Vegetation Processes.Wiley, London.

Gross, K.L., Willig, M.R., Gough, L., Inouye, R. & Cox, S.B.(2000) Patterns of species density and productivity atdifferent spatial scales in herbaceous plant communities.Oikos, 89, 417–427.

van der Hoeven, E.C. & During, H.J. (1997) The effect of densityon size frequency distributions in chalk grassland bryo-phyte populations. Oikos, 80, 533–539.

Huston, M.A. (1994) Biological Diversity. The Coexistence ofSpecies on Changing Landscapes. Cambridge University Press,Cambridge, UK.

Longton, R.E. (1984) The role of bryophytes in terrestrialecosystems. Journal of the Hattori Botanical Laboratory,55, 147–163.

Loreau, M. (2000) Biodiversity and ecosystem functioning:recent theoretical advances. Oikos, 91, 3–17.

Magurran, A.E. (1988) Ecological Diversity and its Measure-ment. Princeton University Press, Princeton, USA.

Marrs, R.H., Grace, J.B. & Taylor, L. (1996) On the relation-ship between plant species diversity and biomass: a commenton a paper by Gough, Grace and Taylor. Oikos, 75, 323–326.

Meyer, A.H. & Schmid, B. (1999) Experimental demographyof the old-field perennial Solidago altissima: the dynamics ofthe shoot population. Journal of Ecology, 87, 17–27.

Monsi, M. & Saeki, T. (1953) Über den Lichtfaktor in denPflanzengesellschaften und seine Bedeutung für die Stoff-produktion. Japanese Journal of Botany, 14, 22–52.

Moore, D.R.J. & Keddy, P.A. (1989) The relationship betweenspecies richness and standing crop in wetlands: the import-ance of scale. Vegetatio, 79, 99–106.

Moore, D.R.J., Keddy, P.A., Gaudet, C.L. & Wisheu, I.C. (1989)Conservation of wetlands: do infertile wetlands deserve ahigher priority? Biological Conservation, 47, 203–217.

Muotka, T. & Virtanen, R. (1995) The stream as a habitattemplet for bryophytes: species’ distribution along gradientsin disturbance and substratum heterogeneity. FreshwaterBiology, 33, 141–160.

Økland, R.H. (1994) Patterns of bryophyte associations atdifferent scales in a Norwegian boreal spruce forest. Journalof Vegetation Science, 5, 127–138.

Økland, R.H. (2000) Population biology of the clonal mossHylocomium splendens in Norwegian boreal spruce forests.5. Vertical dynamics of individual shoot segments. Oikos,88, 449–469.

Økland, R.H. & Økland, T. (1996) Population biology of theclonal moss Hylocomium splendens in Norwegian borealspruce forests. II. Effects of density. Journal of Ecology, 84,63–69.

Økland, R.H., Steinnes, E. & Økland, T. (1997) Element con-centrations in the boreal forest moss, Hylocomium splendens:variation due to segment size, branching patterns and pig-mentation. Journal of Bryology, 19, 671–684.

Pande, N. & Singh, J.S. (1988) Bryophyte biomass of dominantspecies and net production of different communities in varioushabitats of the Nainital hills, NW Himalaya. Lindbergia,14, 155–161.

Pauli, D. (1998) Plant species diversity and productivity inwetland communities: patterns and processes. PhD thesis,Universität Zürich, Zurich, Switzerland.

Payne, R.W., Lane, P.W., Digby, P.G.N., Harding, S.A.,Leech, P.K., Morgan, G.W., Todd, A.D., Thompson, R.,Tunicliffe Wilson, G., Welham, S.J. & White, R.P. (1993)Genstat 5 Reference Manual. Clarendon Press, Oxford, UK.

Peintinger, M. (1999) The effects of habitat area, managementand altitude on species diversity in montane wetlands. PhDthesis, Universität Zürich, Zurich, Switzerland.

Plattner, M. (1996) Diversität und Artenzusammensetzung derVegetation in Flachmooren in Abhängigkeit von Nutzung,Höhenlage, Flächengrösse und verschiedenen Bodenparame-tern. Diploma thesis, Universität Basel, Basel, Switzerland.

Preston, C.M. (1962) The canonical distribution of common-ness and rarity: part I. Ecology, 43, 185–215.

Proctor, M.C.F. (1982) Physiological ecology: water relations,light and temperature responses, carbon balances. BryophyteEcology (ed. A.J.E. Smith), pp. 333–382. Chapman & Hall,Cambridge, UK.

Rieley, J.O., Richards, P.W. & Bebbington, A.D.L. (1979) Theecological role of bryophytes in a North Wales woodland.Journal of Ecology, 67, 497–527.

Rosenzweig, M.L. & Abramsky, Z. (1993) How are diversityand productivity related? Species Diversity in Ecological

JEC_613.fm 28 Wednesday, November 21, 2001 1:11 PM

929Productivity, shoot number, and species number

© 2001 British Ecological Society, Journal of Ecology, 89, 920–929

Communities – Historical and Geographical Perspectives(eds R.E. Ricklefs & D. Schluter), pp. 52–65. University ofChicago Press, Chicago, USA.

Russel, S. (1990) Bryophyte production and decomposition intundra ecosystems. Botanical Journal of the Linnean Society,104, 3–22.

Rydin, H. (1997) Competition among bryophytes. Advancesin Bryology, 6, 135–168.

Schmid, B. (1991) Konkurrenz bei Pflanzen. Populationsbiologieder Pflanzen (eds B. Schmid & J. Stöcklin), pp. 201–210.Birkhäuser, Basel, Switzerland.

Spehn, E., Joshi, J., Diemer, M., Schmid, B. & Körner, C. (2000)Aboveground resource use increases with plant speciesrichness in experimental grassland ecosystems. FunctionalEcology, 14, 326–337.

Spicher, A. (1972) Geologie. Atlas der Schweiz (ed. E. Imhof ),Tafel 4. Eidgenössische Landestopographie, 1965–78, Bern-Wabern, Germany.

Stevens, M.H.H. & Carson, W.P. (1999a) Plant density deter-mines species richness along an experimental fertilitygradient. Ecology, 80, 455–465.

Stevens, M.H.H. & Carson, W.P. (1999b) The significance ofassemblage-level thinning for species richness. Journal ofEcology, 87, 490–502.

Suzuki, J. & Hutchings, M.J. (1997) Interactions betweenshoots in clonal plants and the effects of stored resources onthe structure of shoot populations. The Ecology and Evolutionof Clonal Plants (eds H. de Kroon & J. van Groenendal),pp. 311–329. Backhuys Publishers, Leiden, The Netherlands.

Sveinbjörnsson, B. & Oechel, W.C. (1992) Controls on growthand productivity of bryophytes: environmental limitationsunder current and anticipated conditions. Bryophytesand Lichens in a Changing Environment (eds J.W. Bates &A.M. Farmer), pp. 77–102. Oxford University Press,Clarendon Press, Oxford, UK.

Tilman, D. & Pacala, S. (1993) The maintenance of speciesrichness in plant communities. Species Diversity in Ecolog-ical Communities – Historical and Geographical Perspectives(eds R.E. Ricklefs & D. Schluter), pp. 13–25. University ofChicago Press, Chicago, USA.

van Tooren, B.F., den Hertog, J. & Verhaar, J. (1988) Cover,biomass and nutrient content of bryophytes in Dutch chalkgrasslands. Lindbergia, 14, 47–54.

Uttinger, H. (1967) Klima und Wetter II. Atlas der Schweiz(ed. E. Imhof), Tafel 12. Eidgenössische Landestopographie,1965–1978, Bern-Wabern, Germany.

Verhoeven, J.T.A. & Schmitz, M.B. (1991) Control of plantgrowth by nitrogen and phosphorus in mesotrophic fens.Biogeochemistry, 12, 135–148.

Vermeer, J.G. & Verhoeven, J.T.A. (1987) Species compositionand biomass production of mesotrophic fens in relation tothe nutrient status of the organic soil. Acta Oecologica/Oecologia Plantarum, 8, 321–330.

Virtanen, R., Moutka, T. & Saksa, M. (2001) Species richness–standing crop relationship in stream bryophyte communities:patterns across multiple scales. Journal of Ecology, 89, 14–20

Vitt, D.H. & Pakarinen, P. (1977) The bryophyte vegetation,production, and organic components of Truelove Lowland.Truelove Lowland, Devon Island, Canada: a High Arctic Eco-system (ed. L.C. Bliss), pp. 225–244. University of AlbertaPress, Edmonton, Canada.

Waide, R.B., Willig, M.R., Steiner, C.F., Mittelbach, G.,Gough, L., Dodson, S.I., Juday, G.P. & Parmenter, R. (1999)The relationship between productivity and species richness.Annual Reviews of Ecology and Systematics, 30, 257–300.

Walter, H. (1962) Grundlagen Des Pflanzenlebens. Eugen Ulmer,Stuttgart, Germany.

Watson, E.V. (1960) A quantitative study of the bryophytes ofchalk grassland. Journal of Ecology, 48, 397–414.

Weiher, E. (1999) The combined effects of scale and productivityon species richness. Journal of Ecology, 87, 1005–1011.

Wheeler, B.D. & Giller, K.E. (1982) Species richness ofherbaceous fen vegetation in Broadland, Norfolk in relationto the quantity of above-ground plant material. Journal ofEcology, 70, 179–200.

Wheeler, B.D. & Shaw, S.C. (1991) Above-ground crop massand species richness of the principal types of herbaceousrich-fen vegetation of lowland England and Wales. Journalof Ecology, 79, 285–301.

Wielgolaski, F.E., Bliss, L.C., Svoboda, J. & Doyle, G. (1981)Primary production of tundra. Tundra Ecosystems: a Com-parative Analysis (eds L.C. Bliss, O.W. Heal & J.J. Moore),pp. 187–225. Cambridge University Press, Cambridge, UK.

Zamfir, M. (2000) Effects of bryophytes and lichens onseedling emergence of alvar plants: evidence from green-house experiments. Oikos, 88, 603–611.

Zamfir, M. & Goldberg, D.E. (2000) The effect of initialdensity on interactions between bryophytes at individualand community levels. Journal of Ecology, 88, 243–255.

Received 2 October 2000 revision accepted 19 March 2001


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