Lindbergia, 30(3): 125-142 Jägerbrand, A., Jonsdottir, I ...698428/FULLTEXT01.pdf · Citation for the or iginal published paper (ver sion of record): ... data on whole-plant char-acters

http://www.diva-portal.org

This is the published version of a paper published in Lindbergia.

Citation for the original published paper (version of record):

Jägerbrand, A., Jonsdottir, I., Økland, R. (2005)

Phenotypic variation at different spatial scales in relation to environment in two circumpolar

bryophyte species.

Lindbergia, 30(3): 125-142

Access to the published version may require subscription.

N.B. When citing this work, cite the original published paper.

Permanent link to this version:http://urn.kb.se/resolve?urn=urn:nbn:se:vti:diva-6787

LINDBERGIA 30:3 (2005) 125

LINDBERGIA 30: 125–142. Lund 2005

Phenotypic variation at different spatial scales in relation toenvironment in two circumpolar bryophyte species

Annika K. Jägerbrand, Ingibjörg S. Jónsdóttir and Rune H. Økland

Jägerbrand, A. K., Jónsdóttir, I. S. and Økland, R. H. 2006. Phenotypic varia-tion at different spatial scales in relation to environment in two circumpolarbryophyte species. – Lindbergia 30: 125–142.

Morphology, physiology and biomass in two widespread bryophyte species,Hylocomium splendens and Racomitrium lanuginosum, were studied to ex-amine the extent to which different species exhibit similar phenotypic varia-tion patterns within and across regions. Analyses of nine morphological varia-bles, chlorophyll content, nitrogen content, C/N ratio and biomass were con-ducted in samples from five sites in two geographically separated and climat-ically different regions, Iceland and northern Sweden. Both species exhibitedlarge between-site variation in morphology, physiology and biomass, but with-in-site variation in morphology was substantially higher in Hylocomium splen-dens than Racomitrium lanuginosum. Morphological patterns were partly sim-ilar, partly different between the species, indicating that the two species re-spond morphologically to external factors on different scales. The lowest con-centrations of chlorophyll and nitrogen were found at the same sites for bothspecies, while the site of highest concentration was not the same. In Hyloco-mium splendens, chlorophyll content was positively correlated with biomass.Many of the observed relationships between morphological, physiological vari-ables and biomass were species-specific. Our results demonstrate that the twobryophytes exhibit different phenotypic responses to environmental variation.

A. K. Jägerbrand ([email protected]), Dept of Plant and Envi-ronmental Sciences, Göteborg Univ., Box 461, SE- 405 30 Göteborg, Sweden.– I. S. Jónsdóttir, Univ. Centre in Svalbard, UNIS, P.O. Box 156, NO-9171Longyearbyen, Norway. – R. H. Økland, Dept. of Botany, Natural History Mu-seum, Univ. of Oslo, P.O. Box 1172 Blindern, NO-0318 Oslo, Norway.

Accepted 27 April 2006

Copyright © LINDBERGIA 2006

Bryophyte species generally have wide distributionsand many bryophytes are cosmopolitan in their distri-bution (Watson 1964). The relative importance ofbryophytes generally increases towards higher lati-tudes and altitudes (Vitt and Pakarinen 1977, Wielgo-laski et al. 1981), and in many taiga, tundra and po-lar ecosystems bryophytes are important in terms ofcover, species richness, production, energy flow, bio-mass and nutrient cycling (Vitt and Pakarinen 1977,

Longton 1982, 1984, 1997, Matveyeva and Chernov2000). Widely distributed species are exposed to arange of climatic and other environmental conditions,to which the phenotype must be able to respond ade-quately. Accordingly, many bryophytes exhibit pro-nounced phenotypic variation across climatic gradi-ents, in terms both of morphology and physiology(Longton 1979) either due to genetic variation or plas-tic response to the environment.

At high altitudes and latitudes plants grow moreslowly and reach lower maximum size than elsewhere.Accordingly, bryophytes exhibit progressive reduc-tion of annual growth, leaf length and leaf number,

Lindbergia 30 - 3.pmd 12-06-2006, 10:40125

126 LINDBERGIA 30:3 (2005)

and are shorter and more compact towards higherlatitudes and altitudes in both hemispheres (Longton1979).

Significant relationships between morphology andenvironmental gradients such as temperature, lati-tude and altitude have been demonstrated for select-ed species (Montagnes and Vitt 1991, Heegaard 1997,Ross et al. 2001). Variation at regional (climate) andlocal scale (edaphic and microclimatic) in the branch-ing pattern of bryophyte species that proliferate asex-ually without specialised organs, may give importantclues as to how responsive different species are toenvironmental change. Furthermore, improved know-ledge of the patterns of variation and of the mecha-nisms underlying these patterns, are likely to contri-bute significantly to bryophyte ecology in general, andto our understanding of the role of bryophytes in ter-restrial ecosystems in particular.

However, several aspects of how bryophyte mor-phology varies along environmental gradients arepoorly understood. Firstly, data on whole-plant char-acters like growth patterns (e.g. number of lateralbranches) are sparse (Ross et al. 2001), but such in-formation is needed to address questions related toclonality and growth form of bryophytes (Bates 1998),which in turn affects how bryophytes influence co-oc-curring plants and affect ecosystem processes. Sec-ondly, few studies have addressed the scales of mor-phological variation in bryophytes, i.e. from individ-ual via community to geographical region. Finally, itis not well known to which extent bryophytes exhibitspecies- or group-specific morphological constraintssuch as fixed branching patterns that may limit theirability to respond phenotypically to environmentalvariation (During 1990).

Bryophyte populations from different sites oftenrespond physiologically to temperature variation inremarkably similar ways (Kallio and Heinonen 1973,Longton 1979). However, the physiological responsesof bryophytes in contrasting environments have beenaddressed in relatively few studies (but see Kallio andHeinonen 1973, Baddeley 1991), and the sparse lit-erature available demonstrate apparently contradic-tory patterns among species (Baddeley 1991, Nakat-subo et al. 1997). These observations suggest bothspecies-specific, as well as interspecific variation inphysiological reaction norms and point to our gener-al lack of knowledge of relationships between phe-notypic physiological variation and environment inbryophyte species.

This paper aims at describing phenotypic variationin two perennial clonal bryophytes in northern eco-systems at different spatial scales, using a range ofmorphological and physiological variables in addi-tion to biomass. Two widely distributed species dif-fering considerably in morphology, physiology as well

as ecology, Hylocomium splendens (Hedw.) Schimp.and Racomitrium lanuginosum (Hedw.) Brid., wereselected for the study.

Specifically, we address the following questions:

(1) do different species exhibit similar morphological,physiological and biomass variation within andacross regions? If response patterns to environ-mental variation are similar in both species, wepredict phenotypic variation to be expressed onthe same scale in both studied species.

(2) are patterns of variation in morphology, physio-logy and biomass related to each other?

We address these questions by recording nine mor-phological variables, three physiological variables(chlorophyll content, nitrogen content, C/N ratio, i.e.variables that reflect the outcome of physiologicalactivity) and biomass of individual shoots as well asper unit area, at five sites from different altitudes, foreach species. Material was collected from two regions,western Iceland with an oceanic climate and north-ern Sweden with a more continental climate.

Material and methodsThe studied speciesDistribution and autecologyHylocomium splendens and Racomitrium lanugino-sum are among the best studied moss species (Tamm1953, Tallis 1958, 1959a, 1959b, Kallio and Heinonen1973, Baddeley 1991, Jónsdóttir et al. 1995, R. Øk-land 1995, 1997, 2000, R. Økland and T. Økland1996, Cronberg et al. 1997, Rydgren et al. 1998).Both are perennial stayers in the life-strategy classi-fication of During (1979) and both are widespread.Hylocomium splendens occurs from the temperatezone to the High Arctic (Nyholm 1965, Schofield1985) and is common over the Northern Hemisphere(Persson and Viereck 1983); Racomitrium lanugino-sum is cosmopolitan (Tallis 1958). Hylocomiumsplendens prefers mesic habitats, and is a prominentspecies in boreal coniferous forests (T. Økland 1996).Racomitrium lanuginosum is favoured by a cold ocea-nic climate and becomes more common with increas-ing climatic humidity and towards higher altiduesand latitudes (Tallis 1964). Racomitrium lanugino-sum prefers more exposed habitats (Vitt and Marsh1988) such as summits, upland grasslands and heaths,and peatland hummocks (Tallis 1958).

MorphologyBoth species display extensive morphological varia-bility across their distributional range and across a

Lindbergia 30 - 3.pmd 12-06-2006, 10:40126

LINDBERGIA 30:3 (2005) 127

wide range of habitats within a region [for Hyloco-mium, see reviews by Persson and Viereck (1983) andCallaghan et al. (1997); for Racomitrium, see Tallis(1959a)]. Hylocomium splendens is a weft-formingpleurocarpous bryophyte with sympodial or monopo-dial growth and primary, secondary and tertiary bran-ching (La Farge-England 1996). New growing pointsusually arise sympodially, but monopodial growingpoints are also occasionally found, arising by contin-ued growth of the main axis (R. Økland 1995, Rosset al. 2001). Branching mode, monopodial or sym-podial, is primarily determined by the environment,but also has a genetic component (Ross et al. 1998,2001). In temperate areas, Hylocomium splendens hasa modular growth pattern that provides distinct in-nate markers of the annual growth, regardless of bran-ching mode (Callaghan et al. 1978, R. Økland 1995,Callaghan et al. 1997, Ross et al. 1998, 2001). Typi-cally, one new segment is initiated every year (Tamm1953) but aberrant branching patterns are also com-mon (R. Økland 1995).

The proportion of sympodially arising segments andthe annual growth rate decrease significantly as en-vironmental conditions become harsher, e.g. with in-creasing altitude and/or latitude (Zechmeister 1995,Ross et al. 2001). With decreasing growth rates in-nate markers of annual growth gradually disappearin monopodially branching shoot chains, and seg-ment-based variables can no longer be used. In thisstudy we therefore used morphological variables thatcould be recorded irrespective of branching mode anddistinctness of innate markers of annual growth.

Racomitrium lanuginosum is cladocarpous withmonopodial growth (La Farge-England 1996) and hasan elongated main stem with a variable number oflateral primary branches (Tallis 1959a, 1959b). Thegrowth-form variability of Racomitrium lanuginosumis high, and several different “morphotypes” may bediscerned along a continuum from long shoots withfew branches to short compact shoots with manybranches. Tallis (1959a) suggests that this variationmay be environmentally induced. Racomitrium lanug-inosum propagates clonally by prolonged growth oflateral branches and subsequent detachment by de-composition. The two species are phylogenetically un-related (belong to different orders; Buck and Goffi-net 2000) and have basically different morphologies,although functionally equivalent units can be distin-guished that can be used in comparative morpholo-gical analyses.

PhysiologyPrevious studies on the physiology of Hylocomiumsplendens and Racomitrium lanuginosum indicatesubstantial differences. Hylocomium splendens has

been shown to exhibit relatively large physiologicalintegration (Eckstein and Karlsson 1999), with con-siderable acropetal transport of nitrogen (Eckstein2000), whereas studies in Racomitrium lanuginosumhave showed that the nitrogen required for growthsolely comes from precipitation (Nakatsubo 1990,Baddeley 1991). Redistribution of nitrogen in Raco-mitrium lanuginosum is most likely externally by cap-illary action (Jónsdóttir et al. 1995, Soares and Pear-son 1997) and nitrogen concentrations are extremelylow (Vitt and Pakarinen 1977, Baddeley 1991,Jónsdóttir et al. 1995, Soares and Pearson 1997). Themean nitrogen residence time and annual nitrogenproductivity of Hylocomium splendens are compara-ble with those of woody evergreen vascular plants(Eckstein 2000).

Hylocomium splendens and Racomitrium lanugi-nosum have different temperature optima for the rela-tive growth rate: Hylocomium splendens grows mostrapidly at 15–25 °C (Furness and Grime 1982) where-as temperature optima of 8–10 °C (Tallis 1959a) and13–15 °C (Tallis 1964) have been reported for Raco-mitrium lanuginosum originating from different sites.Hylocomium splendens and Racomitrium lanugino-sum also have different temperature responses of netassimilation and dark respiration (Dilks and Proctor1975).

The nomenclature follows Söderström and Hedenäs(1998).

Study sitesSites were chosen to represent areas with oceanic orcontinental climate as well as different altitudes. Theywere situated in two geographically separated subar-ctic regions; on western Iceland with an oceanic cli-mate (cool summers and mild winters) and in theAbisko area in northern Sweden with a relativelymore continental climate.

Three sites at different altitudes were chosen in eachregion (Table 1). The Icelandic site Thingvellir is oce-anic and subarctic (cold tempered) and has high pre-cipitation whereas Armansfell and the west Icelan-dic highland site Audkuluheidi are subarctic-alpinewith high and moderate precipitation, respectively.The lowest-situated Swedish site, Abisko, is subarc-tic with extremely low precipitation whereas the twoother Swedish sites (Latnjajaure low elevation andLatnjajaure high elevation) are typical, subarctic-al-pine sites with high orographic precipitation. Avail-ability of meteorological data was used as an addi-tional criteron for selection of sites.

Lindbergia 30 - 3.pmd 12-06-2006, 10:40127

128 LINDBERGIA 30:3 (2005)

SamplingAt each site, a 19-m transect running in west–eastdirection was selected with high occurrence of ho-mogeneous moss turfs and/or carpets for each of thestudied species that was present. Two paired cores(diameter 7 cm) were collected systematically at eve-ry meter along each transect. One sample in eachpair was used for biomass per unit area measurements(n = 10 or 20 depending on species and site, Table 1),the other alternatively for morphological and indi-vidual shoot biomass measurements (n = 10), and/orphysiological analyses (chlorophyll n = 10; nitrogenand C/N ratio, n = 6–8).

In sites where one of the species was sparselypresent the number of sample pairs was reduced to10 (Table 1) and morphological and physiologicalvariables were recorded in the same sample to obtain10 replicate measurements. At some sites, chlorophyllcontent was recorded in one sample subset while theother subset was used for recording morphology, shootbiomass, nitrogen content and C/N ratio. For Hylo-comium splendens this applies to Abisko and Latnja-jaure low elevation, for Racomitrium lanuginosumto Thingvellir, Audkuluheidi, and Latnjajaure highelevation. For Racomitrium lanuginosum at Latnja-jaure high elevation every other sample was used foreither morphological or physiological analyses as thevariation in morphology was large, and adequate cov-erage of within-site variation in morphology andphysiology was the specific aim. Sampling was car-ried out in Iceland in June 1996 and in Sweden inAugust 1996. The samples were dried at room tem-perature and stored dry in the dark

Morphological measurementsFor each species, nine morphological variables wererecorded on ten randomly selected moss shoots fromeach sample and site. Morphological variables relat-ed to branching patterns that were believed to bestrongly influenced by external conditions during de-velopment were identified and preferentially select-ed, resulting in eight morphological variables com-mon to both species. In addition, one species-specif-ic variable was recorded for each of the species (Fig.1, Table 2).

All segments were recorded, irrespective of age orphysiological state. This variable might thus be in-fluenced by differences in decomposition rates. ForRacomitrium lanuginosum we recorded the numberof green primary branches as an indicator of the po-tential physiological activity.

Tabl

e 1.

Geo

grap

hic

and

envi

ronm

enta

l da

ta,

sam

ple

size

and

the

mos

t do

min

ant

vasc

ular

pla

nts

for

the

site

s.

Lindbergia 30 - 3.pmd 12-06-2006, 10:40128

LINDBERGIA 30:3 (2005) 129

Physiological measurementsThe physiological variables analysed were chloro-phyll, nitrogen content and C/N ratio. The first twowere selected because of their role in photosynthesis.The C/N ratio gives further indication of nutrient sta-tus and how easily moss litter is decomposed (Nakat-subo et al. 1997). Analyses of chlorophyll were per-formed on green moss parts from each of the ten sam-ples (of each species from each site). Each samplewas milled, weighed (at room temperature; 0.05 mgaccuracy), and split into three subsamples. Two ofthe subsamples were analysed for chlorophyll con-tent and the mean value for the sample was used insubsequent statistical analyses. The third subsamplewas used for dry weight determination.

All chlorophyll analyses were completed within atwo-week period in November 1996, to minimiseamong-sample variation in the degradation of chlo-rophyll. Ten ml of 80% acetone were added to eachsample and the mixture was hand-shaken for 15 sec-onds before being centrifuged for 7 min at 3000 g.Light absorbance at wavelengths of 720 nm, 663 nm,and 645 nm was measured by a spectrophotometer(UV-visible recording spectrophotometer UV-240,Shimadzu Corp., Japan). Chlorophyll content wascalculated according to Arnon (1949). Analyses ofnitrogen and carbon were performed using eight sam-ples of each species from each site, chosen at randomfrom the samples used for analyses of morphology,except in Racomitrium lanuginosum at Latnjajaurehigh elevation (se above).

Nitrogen and carbon contents were analysed on theapical 2 cm of five shoots. Material from the mossshoots was ground in liquid nitrogen to a fine-grainedpowder and dried to constant dry weight at 60 °C for24 h. Samples of 2 mg were analysed on a CN-ana-lyser (Carlo Erba Elementaranalysator model 1106,Carlo Erba Strumentazione, Milano). The C/N ratioof the shoots was calculated and the N content wascalculated as mg N g–1 dry weight.

Biomass measurementsBiomass was measured both for individual shoots andas biomass per unit area based on the whole sample.Mean shoot biomass (cut to 2 cm length) on 10 com-bined shoots was measured for each of the 10 sam-ples from each site, on the samples from morpholog-ical measurements. Measurements were made afterdrying to constant weight at 75 °C for 24 h. For eachspecies, biomass measurements per unit area weremade on 10 or 20 samples from each site (Table 1),after drying to constant dry weight at 75 °C (3 d).

Data analysesPrior to analyses, all variables were transformed tozero skewness to achieve homogeneity of variancesand meet normality assumptions (R. Økland et al.2001, 2003). Variation in morphology was analysedseparately for each species using (1) the first fouraxes of a principal component analysis (PCA; terBraak 1983) of the data matrix of all 500 shoots × 9morphological variables, and (2) the morphologicalvariables themselves. PCA was applied to centred andstandardised variables, with axes scaled to optimisefit to inter-variable correlations. ANOVAs were usedto test for between-site and within-site differences,followed by Fisher’s post-hoc test for between-site

Fig. 1. A schematic representation of the morphologicalvariables used in the analyses. For code explanations, seeTable 2.

Table 2. Morphological characters measured for Hyloco-mium splendens and Racomitrium lanuginosum, with ab-breviated code. For explanations see Fig. 1.

Lindbergia 30 - 3.pmd 12-06-2006, 10:40129

130 LINDBERGIA 30:3 (2005)

Lindbergia 30 - 3.pmd 12-06-2006, 10:40130

LINDBERGIA 30:3 (2005) 131

Lindbergia 30 - 3.pmd 12-06-2006, 10:40131

132 LINDBERGIA 30:3 (2005)

Lindbergia 30 - 3.pmd 12-06-2006, 10:40132

LINDBERGIA 30:3 (2005) 133

Fig. 2. Box plots of morphological characters of Hylocomium splendens in Iceland and northern Sweden. The median isindicated by the centred line in the box, the box indicate the 25th and 75th percentiles, the bars indicate the 10th and90th percentile and single dots other observations. Sites with different letters were significantly different (Fisher’sPLSD) at P < 0.05. n = 500.

Lindbergia 30 - 3.pmd 12-06-2006, 10:40133

134 LINDBERGIA 30:3 (2005)

differences (Sokal and Rohlf 1995). For physiologi-cal variables, shoot biomass and biomass per unit area,between-site differences were tested by ANOVA fol-lowed by the Tukey-Kramer post-hoc test (suitablefor unequal sample sizes; Sokal and Rohlf 1995).Within-site variation in the physiological variablesand biomass could not be statistically tested (as therewere only 6-10 samples), and we therefore expressedthe relative variation as coefficients of variation(Sokal and Rohlf 1995, Zar 1996).

Relationships between morphological variables(mean value from a sample) and other variables meas-ured in the same sample were expressed as matricesof Pearson’s product-moment correlations, separate-ly for each species. The Z-statistic was used to obtainp values for tests of independence (Zar 1996). Corre-lation coefficients between chlorophyll content andother variables were based on a lower number of ob-servations. Relationships between morphological andother variables measured in the same sample (the datasets used for correlation analyses but with chloro-phyll content excluded) were further analysed by or-dination. We initially used detrended correspondenceanalysis (DCA; Hill 1979) to check if the variableswere likely to be linearly or unimodally related to theaxes (R. Økland 1990). Short axes (< 3 SD units)suggested predominantly linear relationships andmotivated use of the linear ordination method PCAto describe the patterns of variation (ter Braak andŠmilauer 1998). The same options were used as inthe PCA of morphological variables.

Principal component analysis was performed by useof CANOCO 4.02 (ter Braak and Šmilauer 1998),for all other analyses, the Statview ® 5.0.1. softwarepackage was used.

ResultsVariation between and within sitesHylocomium splendensFor Hylocomium splendens, the first four axes of thePCA of morphological variables explained 31.1, 17.7,13.9 and 10.0% of the variation, respectively (a totalof 72.8%). High positive loadings on PCA1 were ob-tained for branch lengths, apex length, and high neg-ative loadings were obtained in the near-apicalnumber of branches, whereas high negative loadingson PCA2 were obtained for the number of sub-apicalbranches. The four axes showed significant segrega-tion of sites (Table 3), and also of variation withinall sites (80%; or 16 out of 20 site-times-axes combi-nations). All single morphological variables were sig-nificantly different between sites (ANOVA; Table 3),and significant variation among samples within siteswas found for 33 out of 45 (73%) site-times-charac-

ter combinations (ANOVA; Table 3). Apex length andthe number of segments differed significantly amongsamples within all five sites, and in the Audkuluhei-di site all morphological variables differed signifi-cantly among samples (Table 3).

The ANOVA followed by Fisher’s post-hoc testshowed that the apex and the first and the secondbranch from apex were significantly longer in Thing-vellir and Latnjajaure high elevation (Fig. 2a–c),whereas the third branch was significantly longer inThingvellir, Audkuluheidi and Latnjajaure high ele-vation (Fig. 2d). The length of the longest primarybranch was highest in Abisko and the lowest in Lat-njajaure high elevation (Fig. 2e). The near-apicalbranches (Nrb1) were significantly more numerousat Audkuluheidi than at Thingvellir and Latnjajaurehigh elevation (Fig. 2f). The number of sub-apicalbranches (Nrb2) were the highest in Latnjajaure highelevation, and lowest in Abisko (Fig. 2g), and thenumber of sub-apical branches (Nrb3) was also low-est in Abisko whereas Latnjajaure low elevation andhigh had the highest numbers (Fig. 2h). The numberof segments was significantly higher in Thingvellirand Abisko, compared to the other sites (Fig. 2i).

Between-site differences were found for the physi-ological variables and biomass per unit area (ANO-VA; Table 3), but not for shoot biomass. Coefficientsof variation revealed high variation in physiologicalvariables (Table 3). Abisko differed from all othersites by having significantly higher chlorophyll con-tent, highest nitrogen content, and lowest C/N ratio,whereas Audkuluheidi had lowest nitrogen content,highest C/N ratio, and significantly higher biomassper unit area (Tukey-Kramer post-hoc test; Fig. 4).

Racomitrium lanuginosumFor Racomitrium lanuginosum, the first four axes ofthe PCA of morphological variables explained 28.3,22.2, 11.8 and 8.9% of the variation (a total of 71.1%),and showed significant differences between sites(ANOVA; Table 4). High negative loadings on PCA1were obtained for the number of branches and greenbranches, and positive loading was found for apexlength (59%). The apex and branch lengths all ob-tained high positive loadings on PCA2, while nega-tive loading was obtained for the near-apical numberof branches. Within-site variation in sample scoreswas low for all four PCA axes; significant for a totalof 4 out of 20 (20%) of the site-times-axes combina-tions (ANOVA; Table 4). Significant differences be-tween sites were found in all morphological variables(ANOVA; Table 4), and significant variation amongsamples within sites was found for 16 out of 45 site-times-character combinations (36%) for Racomitriumlanuginosum (ANOVA; Table 4). Length of the sec-

Lindbergia 30 - 3.pmd 12-06-2006, 10:40134

LINDBERGIA 30:3 (2005) 135

Fig. 3. Box plots of morphological characters of Racomitrium lanuginosum in Iceland and northern Sweden. The medi-an is indicated by the centred line in the box, the box indicate the 25th and 75th percentiles, the bars indicate the 10thand 90th percentile and single dots other observations. Sites with different letters were significantly different (Fisher’sPLSD) at P < 0.05. n = 500.

Lindbergia 30 - 3.pmd 12-06-2006, 10:40135

136 LINDBERGIA 30:3 (2005)

ond branch from apex was the only morphologicalvariable for which no significant within-site varia-tion was found for any of the sites (Table 4).

Significant differences among some pairs of siteswere found for all morphological variables (revealedby Fisher’s post-hoc test; Fig. 3). Lengths of apex andthe first, second and third branch were consistentlylower in Audkuluheidi when compared to Thingvel-lir, although the longest third branches were foundin Latnjajaure high elevation (Fig. 3a-d). However,the length of the longest primary branch did not fol-low these patterns, instead Armansfell had the long-est branches and Latnjajaure low elevation had theshortest branches (Fig. 3e). The number of brancheswas higher in Audkuluheidi, and lower in Latnja-jaure high elevation (Nrb1), and Latnjajaure low ele-vation (Nrb2, 3; Fig. 3 f-h). The number of greenbranches was higher in Thingvellir than in Lat-njajaure low elevation and Audkuluheidi (Fig. 3i).

Differences between sites were found in the physi-ological variables, shoot biomass and biomass per unitarea (ANOVA; Table 4). High coefficients of varia-tion were obtained for many physiological and bio-mass variables (Table 4). Armansfell and Latnjajaurehigh elevation differed from the other sites by hav-ing higher chlorophyll, nitrogen content and lowerC/N ratio (Tukey-Kramer post-hoc test; Fig. 4). Shootbiomass was highest in Audkuluheidi and lowest inLatnjajaure high elevation, whereas biomass per unitarea was highest in Thingvellir (Fig. 4).

Correlations between morphological andphysiological and biomass variablesHylocomium splendensFor Hylocomium splendens apex and distal branchlengths made up a group of strongly, positively, cor-related variables (Table 5) with which the length ofthe longest primary branch was weakly, but not sig-nificantly correlated. The number of branches in sub-apical sections (Nrb2 and Nrb3) were strongly corre-lated, and weakly so also with the number of near-apical branches (Nrb1). These two groups of vari-ables were negatively related to each other; apicaland distal branch lengths most strongly with thenumber of near-apical branches, the length of thelongest primary branch with numbers of branches inall sections (Table 5). As expected, a strong correla-tion was observed between nitrogen content and theC/N ratio. Few correlations were found between mor-phological and physiological variables, but thenumber of sub-apical branches (Nrb2) was positivelycorrelated with the C/N ratio and shoot biomass, andnegatively correlated with nitrogen content (Table 5).A significantly positive correlation was found between

chlorophyll content and biomass per unit area.The first three axes of the principal component anal-

ysis (PCA; Fig. 5a) for Hylocomium splendens ex-plained 31.6, 24.1, and 9.9% (a total of 65.6%) ofthe variation, respectively. The highest loadings onPCA1 were obtained for apex, distal branch lengths,length of the longest primary branch (positive) andnumbers of branches in near-apical sections (Nrb1;negative), whereas the highest loadings on PCA2were obtained for nitrogen content, number of seg-ments (positive), and C/N ratio, number of sub-api-cal branches (Nrb2, 3; negative; Fig. 5a). Abisko wasdistinctly separated in the PCA ordination, whereasthe other sites overlapped, especially near the originof the PCA ordination space.

Racomitrium lanuginosumCorrelation patterns among morphological variableswere largely the same for Racomitrium lanuginosumas for Hylocomium splendens (Table 5), but differedin: the weaker (but still positive) relationships amongapex and distal branch lengths; the stronger positiverelationships among branch number variables; andthe affiliation of the longest primary branch with thegroup of apex and branch lengths by the significantpositive correlation with the length of the third branch(Leb3). The apex and distal branch lengths were pos-itively correlated with the number of green branch-es. The number of branches 1–2 cm below the apexwas positively correlated with the length of the long-est primary branch. A positive correlation was alsofound between the shoot biomass and the numbers ofnear-apical and sub-apical branches. Further, posi-tive correlations were found between apex length andbiomass per unit area, branch length of the firstbranch and C/N ratio, length of the longest primarybranch and nitrogen content. Chlorophyll content waspositively correlated with many variables, i.e. thelength of the third branch from apex, the length ofthe longest primary branch, the number of branches1–2 cm from apex, and the number of green branch-es (Table 5).

Facing page:Fig. 4. Box plots of chlorophyll content (mg g-1 dry weight),nitrogen content (mg g-1 dry weight), C/N ratio, shoot bio-mass (mg) and biomass per unit area (kg m-2) of Hyloco-mium splendens and Racomitrium lanuginosum. The me-dian is indicated by the centred line in the box, the boxindicate the 25th and 75th percentiles, the bars indicatethe 10th and 90th percentile and single dots other obser-vations. Sites with different letters were significantly dif-ferent (Tukey-Kramer post-hoc tests) at P < 0.05. n = 50(A, B, G, H); 34 (C, E); 38 (D, F) 70 (I) 90 (J).

Lindbergia 30 - 3.pmd 12-06-2006, 10:40136

LINDBERGIA 30:3 (2005) 137

Lindbergia 30 - 3.pmd 12-06-2006, 10:40137

138 LINDBERGIA 30:3 (2005)

The first three axes of the principal component anal-ysis (PCA; Fig. 5b) for Racomitrium lanuginosum ex-plained 29.8, 25.4, and 17.4% (a total of 72.6 %) ofthe variation, respectively. Highest loadings on PCA1were obtained for near-apical number of branches(positive, Nrb1), and lengths of the first and secondbranch from apex, apex length, C/N ratio and bio-mass per unit area (all negative). Highest negativeloadings on PCA2 were obtained for length of thelongest primary branch, the number of sub-apicalbranches (Nrb2, 3) shoot biomass (Sbi), length of thethird branch from apex (Leb3) and the number ofgreen branches (Gren). Sites were more distinctly se-

parated in the PCA ordination for Racomitrium lanu-ginosum than for Hylocomium splendens (Fig. 5).

DiscussionVariation between and within sitesOur results show patterns of morphological variationin the two species Hylocomium splendens and Raco-mitrium lanuginosum that are partly similar, partlysignificantly different. Variables reflecting recentgrowth show similar trends among sites in the twospecies, whereas other variables (likely to reflectgrowth over longer time-scales), show inconsistentpatterns of variation. This demonstrates the difficul-ties involved in relating morphology to environment;aggravated by large within-site variation and com-plex patterns of variation.

Despite similar proportions of morphological var-iation explained by the first four PCA axes in bothspecies, morphological variation is much higher inHylocomium splendens. Species may show morpho-logical variability at the population and regionalscales (Vitt 1980) that varies from very high to insig-nificant. In Hylocomium splendens, numerous fac-tors may influence the patterns of morphological var-iation, e.g. fine-scaled experimental disturbance (Ry-dgren et al. 1998), or site differences (R. Økland 1997,2000, R. Økland and Bakkestuen 2004). Furthermore,Hylocomium splendens has been shown to have highgenetic variation within populations as well as be-tween populations (Cronberg et al. 1997; Cronberg2004). Thus, Hylocomium splendens is not only ahighly genetically differentiated moss species, but itis also capable of exhibiting complex patterns ofmorphological variation, expressed at several spatialscales and in relation to variation in the environment.Our results show that Hylocomium splendens showshigh morphological variation which may be either aresult of its large genetic variation within sites, ormay be due to a wide phenotypic plasticity.

Tallis (1959a) suggested that the many varietiesand forms (i.e. growth patterns) of Racomitriumlanuginosum represent environmental modifications.Vitt and Marsh (1988) report regional differences infine-scaled morphological characters in Racomitriumlanuginosum as well as within-population morpho-logical variation along moisture gradients, which in-dicate responsiveness to microclimatic variation. Ourresults clearly show that between-site differences ex-ist, but leaves open how much of the morphologicalvariation that originates from environmental modi-fications and genetical differences, respectively.

We predicted a relationship between the number ofbranches and the environmental conditions of thesites, in accordance with the observations of a pro-

Fig. 5. Principal component analysis (PCA) bi-plot dia-grams on Hylocomium splendens and Racomitrium lanug-inosum from Iceland and northern Sweden. The length anddirection of arrows indicate the realtive importance of thevariables. (A) Hylocomium splendens. The diagram ex-plains 55.7% of the variation. n = 34. (B) Racomitriumlanuginosum. The diagram explains 55.1% of the varia-tion. n = 31. For morphological code explanations, seeTable 2, and N=nitrogen content, C/N=C/N ratio, Sbi=shootbiomass, Bio=biomass pe

Lindbergia 30 - 3.pmd 12-06-2006, 10:40138

LINDBERGIA 30:3 (2005) 139

gressive morphological reduction towards higher al-titudes and latitudes (Longton 1979). However, ourresults indicate that the two species show differentpatterns of morphological variation in relation to theenvironment. In Hylocomium splendens we expect-ed environmental conditions to modify the numberof segments, but contrary to the findings of Ross etal. (2001), we found no such trends. This indicatesthat other factors than the environment also affectthe number of segments (Økland 1997).

Patterns of between-site variation in chlorophyll,nitrogen, C/N ratio, shoot biomass and biomass perunit area are mostly significantly different betweenthe two species. For instance, the lowest concentra-tions of chlorophyll and nitrogen are found at thesame sites for both species, whereas the highest con-centrations do not occur at the same site for both spe-cies. Nevertheless, our results for Hylocomium splen-dens accord with those of Bazzaz et al. (1970), whofound lower concentrations of chlorophyll at an al-pine than a lowland site for Polytrichum juniperi-num, and the study by Nakatsubo et al. (1997) onHylocomium splendens; lower nitrogen concentra-tions are reported from sites with lower mean tem-perature. Our results for the nitrogen content ofRacomitrium lanuginosum do, on the other hand,accord with those of Baddeley (1991) for the samespecies; he found increasing nitrogen concentrationswith increasing altitudes.

We do not know if the observed species-specificdifferences apply to the species in general, reflectingcontrasting relationships of the two species to the en-vironment, or if they are idiosyncratic, brought aboutby particularities of our study sites (and those of thestudies above, providing supporting results). How-ever, bryophytes are known for their species-specificecophysiology, e.g. in their growth rates and temper-ature responses (Furness and Grime 1982). It there-fore seems very likely that such physiological differ-ences will be reflected in different patterns of varia-tion in variables like those recorded in our study. Dif-ferences between the species were also found in themagnitudes and the amount of variation of the phys-iological variables. Our results therefore indicate thatbryophyte species may differ in their responses toenvironmental variation, a result quite opposite ofthose normally recorded for vascular plants. For ex-ample, in vascular plants, the effects (a smaller finalsize) of a lower temperature on growth on plants athigh altitudes and latitudes are well known (Billingsand Mooney 1968, Chapin and Shaver 1985), andthere is a clear relationship between increased nitro-gen content with increasing altitude and latitude(Körner 1989).

The collection of samples at different time pointsduring the growing season might, in theory, influ-

ence the variation in chlorophyll content in this study.However, significant differences between sites ratherthan between regions indicate that the time point ofcollection was probably of minor importance, in ac-cordance with the well-known ability of bryophytesto withstand long periods of desiccation (Proctor1981, 1982).

We expected dry weight and biomass per unit areato decrease with increasing latitude or environmen-tal harshness, but our results do not show any specif-ic trends in that direction, apart from some indica-tions of lower shoot biomass of Racomitrium lanug-inosum in northern Sweden than in Iceland. For bio-mass per unit area, our results fail to comply withgeneral predictions of decreasing bryophyte biomasswith increasing latitude in the Arctic and Antarctic(Russell 1990). Many factors may confound the pat-tern expected, e.g. interference by local environmen-tal gradients (Russell 1990), decomposition, and otherfactors such as volcanic ash content and grazing.Furthermore, the biomass in a single sample unit mostoften comprises both intact and dead parts of the mosswhen innate growth markers are not used to stand-ardise the length of periods over which the biomasshas accumulated (R. Økland 1995).

Relationships between morphological andphysiological variables and biomassBoth species show high separation between sites whenanalysed by the multivariate method PCA, this is moststrongly seen for Racomitrium lanuginosum. Com-pared with Hylocomium splendens, Racomitriumlanuginosum exhibits less within-site morphologicalvariation, but in Racomitrium lanuginosum the phys-iological variables explain somewhat more of the to-tal variation in morphological variables, physiologi-cal variables and biomass than in Hylocomium splen-dens. Racomitrium lanuginosum also shows strong-er relationships among morphological variables,physiological variables and biomass, as well as strong-er variability in general. Some of our results indicatethat bryophyte phenotypes are shaped by external,most probably environmental factors, as the same twogroups of positively correlated variables (apex andbranch lengths, and branch numbers) are identifiedby correlation analysis of the morphological variablesfor both species.

Even though we find both coincident and diver-gent correlation patterns, most correlations are spe-cies-specific. Congruent patterns are found in quitebasic characteristics such as the number of branchesand shoot biomass, and nitrogen content and C/Nratios. Opposing patterns for the two species are foundin the length of the longest primary branch and the

Lindbergia 30 - 3.pmd 12-06-2006, 10:40139

140 LINDBERGIA 30:3 (2005)

number of branches (0-2 cm from apex), probablyreflecting complex differences in the morphologicalconstitution of the species.

Chlorophyll content is an estimate of the photo-synthetic capacity (Kallio and Valanne 1975) and is,in vascular plants, highly correlated with light andnutrient conditions (Seemann et al. 1987). In bryo-phytes photosynthesis is strongly dependent on wa-ter availability (Kallio and Kärenlampi 1975, Proc-tor 1990) so that climate and especially precipitationmay play a large role for the chlorophyll content. Wetherefore expected chlorophyll or nitrogen content topeak at the same sites as biomass per unit area, aschlorophyll and nitrogen are usually assumed to beindirectly responsible for growth. This is supportedby a positive correlation between biomass per unitarea and chlorophyll content in Hylocomium splen-dens, and in Racomitrium lanuginosum by a positivecorrelation between the number of green branchesand chlorophyll content.

Our results thus demonstrate a clear and interpret-able pattern of photosynthetic capacity and biomassper unit area in Hylocomium splendens, while no re-lationship between nitrogen content and biomass isobserved in any species. In fact, the opposite is found:the lowest nitrogen content and the highest C/N ra-tio are observed in the sites with highest biomass perunit area for both species. This contrasts with theclose relationship in vascular plants between nitro-gen supply and increases in biomass (Larcher 1995),and the answer may be that vascular plants and bryo-phytes have somewhat different physiology and ecol-ogy, and that bryophytes are usually not limited intheir growth by nitrogen, but by water availability.

The observed patterns and its implicationsOur results demonstrate that the two bryophytes ex-hibit different phenotypic responses to the environ-ment at the two different scales explored. An impor-tant implication is that to be able to predict respons-es of the important bryophyte-dominated ecosystemsto environmental change, e.g. climatic change. Suchspecies-specific responses of the dominating speciesneed to be considered. The large phenotypic varia-tion among and within sites as well as among spe-cies observed by us indicate that site-specific ecosys-tem responses to environmental change are likely tooccur.

Several studies (Potter et al. 1995, R. Økland, 1995,1997, 2000, T. Økland et al. 2004) report predictableresponses of bryophyte growth to external, notablyclimatic, factors, and recommend use of bryophytesare sensitive indicators of climatic conditions. Our

results seemingly indicate that the relationship be-tween phenotypes of bryophytes and the environmentis too complicated to allow simple generalisations,over species, over morphological and physiologicalcharacters, and over broad-scaled climatic gradients.Therefore, generalisations of bryophyte phenotypicvariation beyond the simple relationship betweengrowth and the length of the effective growing sea-son should be made with great care.

Acknowledgements – Norm Kenkel, Einar Heegaard andMargit Fredriksson are thanked for different kinds of help.This study was supported by Swedish Natural Science Re-search Council (to ISJ), and by Abisko stipendiefond, Adler-bertska forskningsfonden, Kapten Carl Stenholms, LarsHiertas Minnesfond, Th. Kroks, Wilhelm och Martina Lun-dgrens fond, Överskottsfonden, Jubileumsfonden (Göte-borg University) and NorFA. All of these are gratefullyacknowledged.

ReferencesArnon, D. I. 1949. Copper enzymes in isolated chloroplasts.

Polyphenoloxidase in Beta vulgaris. – Plant Physiol.24: 1–15.

Baddeley, J. A. 1991. Effects of atmospheric nitrogen dep-osition on the ecophysiology of Racomitrium lanugi-nosum (Hedw.) Brid. – PhD thesis, Univ. of Manches-ter.

Bates, J. W. 1998. Is ‘life-form’ a useful concept in bryo-phyte ecology? – Oikos 82: 223–237.

Bazzaz, F. A., Paolillo, D. J. Jr. and Jagels, R. H. 1970.Photosynthesis and respiration of forest and alpine pop-ulations of Polytrichum juniperinum. – Bryologist 73:579–585.

Billings, W. D. and Mooney, H. A. 1968. The ecology ofarctic and alpine plants. – Biol. Rev. 43: 481–529.

Buck, W. R. and Goffinet, B. 2000. Morphology and clas-sification of mosses. – In: Shaw, A. J. and Goffinet, B.(eds), Bryophyte biology. – Cambridge Univ. Press pp.71–123.

Callaghan, T. V., Collins, N. J. and Callaghan, C. H. 1978.Photosynthesis, growth and reproduction of Hylocomi-um splendens and Polytrichum commune in SwedishLapland. Strategies of growth and population dynam-ics of tundra plants 4. – Oikos 31: 73–88.

Callaghan, T. V., Carlsson, B. Å., Sonesson, M. et al. 1997.Between-year variation in climate-related growth of cir-cumarctic populations of the moss Hylocomium splen-dens. – Funct. Ecol. 11: 157–165.

Chapin, F. S. III and Shaver, G. R. 1985. Arctic. – In:Chabot, B. F. and Mooney, H. A. (eds), Physiologicalecology of North American plant communities. Chap-man and Hall, pp. 16–40.

Cronberg, N. 2004. Genetic differentiation between popu-lations of the moss Hylocomium splendens from lowversus high elevation in the Scandinavian mountainrange. – Lindbergia 29: 64–72.

Cronberg, N., Molau, U. and Sonesson, M. 1997. Geneticvariation in the clonal bryophyte Hylocomium splen-dens at hierarchical geographical scales in Scandina-via. – Heredity 78: 293–301.

Lindbergia 30 - 3.pmd 12-06-2006, 10:40140

LINDBERGIA 30:3 (2005) 141

Dilks, T. J. K. and Proctor, M. C. F. 1975. Comparativeexperiments on temperature responses of bryophytes:assimilation, respiration and freezing damage. – J. Bry-ol. 8: 317–336.

During, H. J. 1979. Life strategies of Bryophytes: a pre-liminary review. – Lindbergia 5: 2–18.

During, H. J. 1990. Clonal growth patterns among bryo-phytes. – In: van Groenendal, J. and de Kroon, H. (eds),Clonal growth in plants: regulation and function. SPBAcademic Publishing, pp. 153–176.

Eckstein, R. L. 2000. Nitrogen retention by Hylocomiumsplendens in a subarctic birch woodland. – J. Ecol. 88:506–515.

Eckstein, L. R. and Karlsson, S. P. 1999. Recycling of ni-trogen among segments of Hylocomium splendens ascompared with Polytrichum commune: implications forclonal integration in an ectohydric bryophyte. – Oikos86: 87–96.

Furness, S. B. and Grime, J. P. 1982. Growth rate andtemperature responses in bryophytes. II. A comparativestudy of species of contrasted ecology. – J. Ecol. 70:525–536.

Heegaard, E. 1997. Morphological variation within An-dreaea blyttii in relation to the environment on Hardan-gervidda, western Norway: a quantitative analysis. –Bryologist 100: 308–323.

Hill, M. O. 1979. DECORANA – A FORTRAN programfor detrended correspondence analysis and reciprocalaveraging. – Cornell Univ.

Jónsdóttir, I. S., Callaghan, T. V. and Lee, J. A. 1995. Fateof added nitrogen in a moss-sedge Arctic communityand effects of increased nitrogen deposition. – Sci. To-tal Environ. 160/161: 677–685.

Kallio, P. and Heinonen, S. 1973. Ecology of Rhacomitri-um lanuginosum (Hedw.) Brid. – Rep. Kevo Subarct.Res. Stat. 10: 43–54.

Kallio, P. and Kärenlampi, L. 1975. Photosynthesis inmosses and lichens. – In: Cooper, J. P. (ed.), Photosyn-thesis and productivity in different environments. Theinternational biological programme. Cambridge Univ.Press, pp. 393–423.

Kallio, P. and Valanne, N. 1975. On the effect of continu-ous light on photosynthesis in mosses. – Ecol. Stud.16: 149–162.

Körner, C. 1989. The nutritional status of plants from highaltitudes. A worldwide comparison. – Oecologia 81:379–391.

La Farge-England, C. 1996. Growth form, branching pat-tern, and perichaetial position in mosses: cladocarpyand pleurocarpy redefined. – Bryologist 99: 170–186.

Larcher, W. 1995. Physiological plant ecology. Ecophysio-logical and stress physiology of functional groups. -Springer-Verlag.

Longton, R. E. 1979. Climatic adaptation of bryophytes inrelation to systematics. – In: Clarke, G. C. S. and Duck-ett, J. G. (eds), Bryophyte systematics. Syst. Ass. Spec.Vol. No. 14. Academic Press, pp. 511–531.

Longton, R. E. 1982. Bryophyte vegetation in polar re-gions. – In: Smith, A. J. E. (ed.), Bryophyte ecology.Chapman and Hall, pp. 123–165.

Longton, R. E. 1984. The role of bryophytes in terrestrialecosystems. – J. Hatt. Bot. Lab. 55: 147–163.

Longton, R. E. 1997. The role of bryophytes and lichensin polar ecosystems. – In: Woodin, S. J. and Marquiss,

M. (eds) Ecology of Arctic environments. Blackwell Sci-ence, pp. 69–96.

Matveyeva, N. and Chernov, Y. 2000. Biodiversity of ter-restrial ecosystems. – In: Nuttall, M. and Callaghan, T.V. (eds), The Arctic: environment, people, policy. Har-wood Academic Publishers, pp. 233–273.

Montagnes, R. J. S. and Vitt, D. H. 1991. Patterns of mor-phological variation in Meesia triquetra (Bryopsida:Meesiaceae) over an Arctic-boreal gradient. – Syst. Bot.16: 726–735.

Nakatsubo, T. 1990. Primary production and nitrogen econ-omy of Racomitrium lanuginosum at the subalpine la-va field of Mt. Fuji. – Proc. Bryol. Soc. Jpn 5: 65–70(in japanese with english summary).

Nakatsubo, T., Uchida, M., Horikoshi, T. et al. 1997. Com-parative study of the mass loss rate of moss litter inboreal and subalpine forests in relation to temperature.– Ecol. Res. 12: 47–54.

Nyholm, E. 1965. Illustrated moss flora of Fennoscandia.II. Musci. Fasc.5. – Gleerup, Lund.

Økland, R. H. 1990. Vegetation ecology: theory, methodsand applications with reference to Fennoscandia. – Som-merfeltia suppl. 1: 1–233.

Økland, R. H. 1995. Population ecology of the clonal mossHylocomium splendens in Norwegian boreal spruce for-ests. I. Demography. – J. Ecol. 83: 697–712.

Økland, R. H. 1997. Population biology of the clonal mossHylocomium splendens in Norwegian boreal spruce for-ests. III. Six-year demographic variation in two areas.– Lindbergia 22: 49–68.

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

Økland, R. H. and Bakkestuen, V. 2004. Fine-scale spa-tial patterns in populations of the clonal moss Hyloco-mium splendens partly reflect structuring processes inthe boreal forest floor. – Oikos 106: 565–575.

Økland, R. H. and Økland T. 1996. Population biology ofthe clonal moss Hylocomium splendens in Norwegianboreal spruce forests. II. Effects of density. – J. Ecol.84: 63–69.

Økland, R. H., Økland, T. and Rydgren, K. 2001. Vegeta-tion-environment relationships of south boreal spruceswamp forests in Østmarka nature reserve, SE Norway.– Sommerfeltia 29: 1–190.

Økland, R. H., Rydgren, K. and Økland, T. 2003. Plantspecies composition of boreal spruce swamp forests:closed doors and windows of opportunity. – Ecology84: 1909–1919

Økland, T. 1996. Vegetation-environment relationships ofboreal spruce forest in ten monitoring reference areasin Norway. – Sommerfeltia 22: 1–349.

Økland, T., Bakkestuen, V., Økland, R. H. et al. 2004.Changes in forest understory vegetation in Norway re-lated to long-term soil acidification and climatic change.– J. Veg. Sci. 15: 437–448.

Persson, H. and Viereck, L. A. 1983. Collections and dis-cussions of some bryophytes from Alaska. – Lindber-gia 9: 5–20.

Potter, J. A., Press, M. C., Callaghan, T. V. et al. 1995.Growth responses of Polytrichum commune and Hylo-comium splendens to simulated environmental changein the sub-arctic. – New Phytol. 131: 533–541.

Lindbergia 30 - 3.pmd 12-06-2006, 10:40141

142 LINDBERGIA 30:3 (2005)

Proctor, M. C. F. 1981. Physiological ecology of bryophytes.– Adv. Bryol. 1: 79–166.

Proctor, M. C. F. 1982. Physiological ecology: water rela-tions, light and temperature responses, carbon balance.– In: Smith, A. J. E. (ed.), Bryophyte ecology. Chap-man and Hall, pp. 333–381.

Proctor, M. C. F. 1990. The physiological basis of bryo-phyte production. – Bot. J. Linn. Soc. 104: 61–77.

Ross, S. E., Callaghan, T. V., Ennos, A. R. et al. 1998.Mechanics and growth form of the moss Hylocomiumsplendens. – Ann. Bot. 82: 787–793.

Ross, S. E., Callaghan, T. V., Sonesson, M. et al. 2001.Variation and control of growth-form in the moss Hylo-comium splendens. – J. Bryol. 23: 283–292.

Russell, S. 1990. Bryophyte production and decomposi-tion in tundra ecosystems. – Bot. J. Linn. Soc. 104: 3–22.

Rydgren, K., Økland, R. H. and Økland, T. 1998. Popula-tion biology of the clonal moss Hylocomium splendensin Norwegian boreal spruce forsts. 4. Effects of exper-imental fine-scale disturbance. – Oikos 82: 5–19.

Schofield, W. B. 1985. Introduction to Bryology. – Mac-millan.

Seemann, J. R., Sharkey, T. D., Wang, J. L. et al. 1987.Environmental effects on photosynthesis, nitrogen useefficiency and metabolic pools in leaves of sun andshade plants. – Plant Physiol. 84: 796–802.

Soares, A. and Pearson, J. 1997. Short-term physiologicalresponses of mosses to atmospheric ammonium and ni-trate. – Water Air Soil Pollution 93: 225–242.

Sokal, R. R. and Rohlf, F. J. 1995. Biometry, ed. 3. – Free-man.

Söderström, L. and Hedenäs, L. 1998. Checklista överSveriges mossor. – Myrinia 8: 58–90.

Tallis, J. H. 1958. Studies in the biology and ecology ofRhacomitrium lanuginosum Brid. I. Distribution andecology. – J. Ecol. 46: 271–288.

Tallis, J. H. 1959a. Studies in the biology and ecology ofRhacomitrium lanuginosum Brid. II. Growth, reproduc-tion and physiology. – J. Ecol. 47: 325–350.

Tallis, J. H. 1959b. Periodicity of growth in Rhacomitri-um lanuginosum. – J. Linn. Soc. Lond. 56: 212–217.

Tallis, J. H. 1964. Growth studies on Rhacomitrium lanu-ginosum. - Bryologist 67: 417-422.

Tamm, C. O. 1953. Growth, yield and nutrition in carpetsof a forest moss (Hylocomium splendens). – Medd. Stat-ens Skogsforskningsinst. 43: 1–140.

ter Braak, C. J. F. 1983. Principal components biplots andalpha and beta diversity. – Ecology 64: 454–462.

ter Braak, C. J. F. and Šmilauer, P. 1998. CANOCO refer-ence manual and user’s guide to Canoco for Windows:software for canonical community ordination (version4). – Microcomputer Power, 1–352.

Vitt, D. H. 1980. The Genus Macrocoma. II. Geographi-cal variation in the Macrocoma tenue-M. sullivantii spe-cies complex. – Bryologist 83: 437–450.

Vitt, D. H. and Marsh, C. 1988. Population variation andphytogeography of Racomitrium lanuginosum and R.pruinosum. – Nova Hedwigia 90: 235–260.

Vitt, D. H. and Pakarinen, P. 1977. The bryophyte vegeta-tion, production and organic components of TrueloveLowland. – In: Bliss, L. C. (ed.), Truelove Lowland,Devon island, Canada: a high arctic ecosystem. Univ.of Alberta Press, pp. 225–244.

Watson, E. V. 1964. The structure and life of bryophytes.– Hutchinson.

Wielgolaski, F. E., Bliss, L. C., Svoboda, J. et al. 1981.Primary production of tundra. – In: Bliss, L. C., Heal,O. W. and Moore, J. J. (eds), Tundra ecosystems: a com-parative analysis. Cambridge Univ. Press, pp.187–226.

Zar, J. H. 1996. Biostatistical analysis. 3d ed. – Prentice-Hall Int., Inc.

Zechmeister, H. G. 1995. Growth of five pleurocarpousmoss species under various climatic conditions. – J.Bryol. 18: 455–468.

Lindbergia 30 - 3.pmd 12-06-2006, 10:40142