Bryophyte community composition and habitat specificity in the naturalforests of Terceira, Azores

R. Gabriel1,* and J.W. Bates2

1Universidade dos Açores, Dep. Ciências Agrárias, 9701-851 Angra do Heroísmo, Portugal; 2Department ofBiological Sciences, Imperial College London, Silwood Park Campus, Ascot, Berkshire SL5 7PY, UK;*Author for correspondence

Recieved 8 August 2003; accepted in revised form 24 May 2004

Key words: Biodiversity, DCA, Laurisilva, Lichens, Substratum-specificity, TWINSPAN

Abstract

In order to characterize the main areas of natural forest on Terceira Island �Azores�, some of the most interestingEuropean forests due to their rich and diverse flora of endemic as well as relict species, six forest stands werestudied and their flora inventoried using 226 randomized quadrats, which revealed one anthocerote, 64 liver-worts, 41 mosses and 16 macrolichen taxa. The alpha-diversity of the samples is particularly species-rich, somequadrats �30 � 30 cm� including more than 25 bryophyte species. A quantitative analysis of the vegetation-environment relationships consistently showed that the distributions of the native forest bryophytes and lichensof Terceira are governed by a complex set of factors related to water availability, the status of the substrata andthe influences of the vascular plant community. Considering the generally high values of the Sørensen indicesand the low number of specialist species found with Lloyd’s index, the differences are more in terms of domi-nance of species than in terms of species composition. In fact, substratum type was clearly important in the DCAand TWINSPAN analysis using species cover abundance values, largely explaining the distribution of bryophytespecies between Juniperus brevifolia �Seub.� Antoine and Laurus azorica �Seub.� Franco bark. The eight putativeplant community type groupings achieved with these multivariate methods were able to elucidate some majorbryophyte – substratum relationships, that had not previously been considered and they offer a framework forfuture research.

Introduction

The evergreen forests of the Azores offer a great va-riety of habitats for bryophytes and lichens, owing tothe diversity of microhabitats and available substrata,and to the hyper-humid conditions they provide.Cryptogamic species are thus a conspicuous and eco-logically significant component of these forests, anda continuous cover of bryophytes may be observed onsoil, lava rocks, living and dead trunks, branches,leaves and fern fronds. Nevertheless, quantitativestudies of these communities within Azorean forestsare lacking, although several techniques of numericalclassification have been used with success for overall

vegetation classification in Macaronesia as for vascu-lar plants �Oliveira 1989; Dias 1996� and for bryo-phytes �González-Mancebo 1991�.

No attempts to classify the bryophyte communitiesof the Azores were made until the study of Allorgeand Allorge �1946� and the literature on the subject isscarce �Hübschmann 1974; Sjögren 1978, 1990,1993, 1995a, 1996, 1997, 2003�. Azorean lichenshave also not been extensively studied until recently�Navás 1909; Degelius 1941; Abbayes 1948; Tavares1953; Aptroot 1989; Arvidsson 1990; Purvis et al.1996�, and the communities present have not been themain focus. Previous studies �Hübschmann 1974;Sjögren 1978, 2003� suggest that the bryophyte veg-

Plant Ecology �2005� 177:125–144DOI 10.1007/s11258-005-2243-6 © Springer 2005

etation presents complex patterns of distribution ow-ing to: 1� the large number of species, their wideecological ranges and their poorly pronounced sub-stratum preference in the archipelago; 2� the frequentparticipation of endemic species in the communitiesproducing a large number of endemic bryo-commu-nities; 3� the difficulties in selecting differential spe-cies due to climatic differences within individualislands with increasing altitude, and among islands inthe archipelago, from East to West. It was consideredthat a study based on objective sampling methods andemploying numerical analysis of community datamight be able to clarify the relationships between thecryptogamic flora and the various environmental var-iables.

Bryophytes and lichens inhabit the same vegetationstratum in forests and almost all have the commontrait of being poikilohydric. The distribution of bryo-phytes and lichens is influenced primarily by macro-climatic factors like rainfall and temperature �Pitkin1975; Sveinbjörnsson and Oechel 1992�, by microen-vironmental features of shade, humidity and tempera-ture �Yarranton and Beasleigh 1969; Alpert 1985,1991�, by site factors such as age, composition of theforest, moisture regime �McCune 1993; Sillett andNeitlich 1996�, and by substratum characteristics likepH and nutrient status �Wolseley and Aguirre-Hudson1997; Batty et al. 2003�. Nevertheless, since there aremajor taxonomic, morphological and ecological dif-ferences between bryophytes and lichens �Robinsonet al. 1989� they respond in different ways to thesevariables and often achieve maximum abundance indifferent habitats �McCune 1993; Pharo and Beattie1997�.

The studies reported here are based on Terceira, thethird largest island in the Azores archipelago and onewhere substantial areas of native forests survive andwhere there are considerable internal variation in cli-matic factors and vegetation types �Dias 1996; Diaset al. 2004�.

Our aims are: 1� to characterize the main areas ofnatural forest on Terceira in terms of their epiphytic,epilithic and epigeic vegetation; 2� to detect correla-tions of environmental factors with the compositionof the flora; 3� to subject the hypothesis thatbryophytes show reduced substratum affinities in theAzorean forests, to scrutiny. Bryophytes, lichens andvascular species have been included in the presentstudy because these groups occur in mixed commu-nities in nature, and it would thus be misleading to

study any one of these groups independently �Bates1982�.

Methods

Study area

The field study was conducted on Terceira Island�38°40� N; 27°20� W; maximum elevation 1021 m�in the Azores Archipelago �Portugal�. In order to en-compass a wide diversity of potential communities onTerceira, all six major areas of remaining native for-est were sampled. The locations of each site areshown in Figure 1 and their main characteristics areshown in Table 1. These are located at different alti-tudes, with different precipitation regimes and differ-ent degrees of exposure. The natural evergreen forests�laurisilva� include a number of broadleaf species,with native Laurus azorica �Seub.� Franco andendemic Juniperus brevifolia �Seub.� Antoine, beingthe most abundant trees. One of the main differencesbetween native Azorean forests and those studiedelsewhere is the absence of large trees, since themaximum height of trees on Terceira is currently ap-proximately 10 m. The trees are also uniformlyspaced, the distance between two tree neighbours be-ing always less than 3 m. In addition there is a richunderstory of shrub species �e.g., Myrsine africanaL., Vaccinium cylindraceum Smith� and some spec-tacular ferns �Ormonde 1990, 1991� allowing for avery closed canopy, that causes low light and highhumidity values. Bryophyte cover generally reachesthe tallest branches and even includes the leaves,which is only possible due to the high and unvaryingvalues of relative humidity �Veneklaas 1990; Sjögren1997�.

Sampling

Two hundred and twenty six quadrats were sampledduring the month of June 1998. Greater sampling ef-forts were made on the larger forest areas, such asSerra de Santa Bárbara and Terra Brava. The substrataexamined included tree bark of the commonest spe-cies �Laurus azorica and Juniperus brevifolia�, soiland rock. The trunks were sampled in predeterminedsegments of 30 cm, regarded as quadrats, from thesoil to 180 cm height and extending halfway roundthe trunk. The size of the quadrat varied with the di-ameter of each tree sampled. In order to avoid exces-

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sive dispersion of data, trees with girths less than 20cm at 150 cm from the soil were excluded; these,usually younger, trees also had a less abundant epi-phyte flora than the larger trees. A complementaryquadrat, included in the analysis, was recorded at thesame height but on the opposite side of the trunk. Soiland rock quadrats �30 � 30 cm� were recorded in theimmediate vicinity �from 25 cm� of each tree,although in some cases it was not possible to locateany suitable rock exposures in a 2 m perimeter of thetree. A scale with ten classes of percentage cover wasused to estimate the abundance of each species withineach quadrat in the field �Table 2�. From each quad-rat, samples of the species present �bryophytes, mac-

Figure 1. The study area in Terceira Island �Açores�. Dots represent sample sites. M, Matela; P, Pico Rachado; N, Mistérios Negros; L,Lomba; T, Terra Brava; S, Serra de Santa Bárbara.

Table 1. Denominations �abbreviations� and main characteristics of the studied sites. UTM coordinates, coordinates from the ‘Carta MilitarNacional, 1: 25000’. N, number of total samples recorded at each site. Dominant phorophytes: Laurus, L. azorica; Erica, E. azorica; Juni-perus, J. brevifolia; Ilex, I. perado sp. azorica. Altitude �m�, minimum and maximum altitude sampled at the site. Rainfall �mm�, averageprecipitation values measured by the nearest meteorological stations in 1997 and 1998 by F. C. Rodrigues �Universidade dos Açores, DCA�.pH, pH values measured for the different substrata under study. L. a., Laurus azorica; J. b., Juniperus brevifolia.

Sites �abbreviations� UTM coordinates N Dominant phorophytes Altitude Rainfall pH

�m� �mm� soil rock L. a. J. b.

Matela �M� �4.77, 42.83� 32 Laurus, Erica 430-480 1242 5.4 5.7 5.2 4.3Pico Rachado �P� �4.72–4.73, 42.89–42.90� 44 Juniperus, Laurus 580-620 2535 4.3 5.1 4.8 4.1Mistérios Negros �N� �4.75, 42.87� 34 Juniperus 560-660 3028 4.1 4.4 3.8Lomba �L� �4.74, 42.87� 16 Laurus 760-780 3028 4.7 5.3 5.0Terra Brava �T� �4.82–4.83, 42.86–42.87� 61 Laurus, Juniperus, Ilex 630-700 3828 4.4 5.2 5.5 4.1Sta. Bárbara �S� �4.71–4.72, 42.87–42.88� 39 Juniperus 810-970 4705 4.1 4.7 4.1

Table 2. Classes of percentage cover used in the study of the na-tive Terceira forests.

Classes Cover

1 Present, but total area amounting to less than 1cm2

2 Total area at least 1cm2 but less than 1% cover ofthe quadrat’s area.

3 Cover at least 1% but � 5%4 Cover at least 5% but � 10%5 Cover at least 10% but � 15%6 Cover at least 15% but � 25%7 Cover at least 25% but � 35%8 Cover at least 35% but � 50%9 Cover at least 50% but � 75%

10 Cover at least 75% but � 100%

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rolichens and vascular plants� were collected forfurther examination and the bryophyte and lichenspecimens are deposited in the Herbarium of the Uni-versity of the Azores �AZU�.

Nomenclature and identification

Nomenclature follows Corley et al. �1981� withmodifications of Corley and Crundwell �1991� andHedenäs �1992� for mosses and Schumacker andVáña �2000� for liverworts. Vascular plants wereidentified using the floras of Franco �1971, 1984� andFranco and Afonso �1994, 1998�. Lichens were iden-tified by P. Carvalho �LISU, Lisbon University� andnomenclature followed Haffelner �1995�. Prof. R.Schumacker �University of Liège� confirmed or iden-tified the Lejeuneaceae and Dr. C. Sérgio �LISU,University of Lisboa� confirmed or identified the spe-cies from the genus Thamnobryum and Fissidens.Prof. E. Sjögren �University of Uppsala� helped withthe identification of several species.

Environmental variables

The environmental variables are listed in Table 3.Mean annual precipitation �rainfall� used for each sitefollows Rodrigues and Rodrigues �2003�. Altitudewas measured using an altimeter, and the slope of thesampled surface �90° � vertical� using a clinometer.Isolation of the tree in the forest �m� was assessed asthe average of the distances to the nearest trees on itsNorth, South, East and West sides. The distance to thesoil �cm� and the distance to the canopy �cm� weremeasured for each patch. The distance to the canopywas measured using 1 m lengths of plastic electricityconduit, which were light to carry and simple to con-

nect, for measurements in the field. The pH valueswere measured for soil, rock and bark: a sample wascollected in the field, stored in paper bags, air driedand analysed in the laboratory about three monthslater. All samples were pulverized prior to analysis�Farmer et al. 1990�. An aliquot sample was extractedand diluted in distilled water �1 : 2, sample : water�,shaken for one hour and pH measured with a WTWMicroprocessor pH meter, pH 537. Substratum, refersto bark of Juniperus brevifolia �j� or Laurus azorica�l�, or to soil �s� or rock �b�. The following variableswere recorded as ordinal. Evaporation shelter: 1 –completely sheltered, cave; 2 – Sphagnum cushionsover the patch; 3 – dense vascular vegetation in front;4 � open vascular vegetation in front; 5 – fully ex-posed to wind. Moisture available: 1 – only indirectwater, caves; 2 – water only during rain, substrata notadjacent to soil; 3 – water available for a short periodof time after rain, mostly tree trunks or well-drainedsoil; 4 – water available for a longer period of timeafter rain, mostly soil with impermeable layer at lowdepth; 5 – water permanently available, bogs, Sphag-num cover. Light: 1 – deeply shaded, cave or underrock; 2 – more than 1.5 m height of vegetation infront; 3 – less than 1.5 m height of vegetation in front,4 � just a few twigs in front; 5 – fully exposed tosky.

Data analysis

The Sørensen Similarity Index �SSI� was used tocompare the groups of taxa found on the four differ-ent substrata in the sampled native forests on Terceira,and was calculated as: SSI � 2w / �m � n�, where mis the total number of species in the first sample, nthe total number in the second sample, and w thenumber of species common to both samples �South-wood and Hendersen 2000�. The index was calculatedseparately for the total number of species, total num-ber of bryophytes, mosses, liverworts, lichens andvascular plants in the possible pairs of substrata.

The assessment of substratum-specificity of cryp-togamic species was performed using the Lloyd In-dex of Patchiness �L� �Lloyd 1967�. This index hasbeen used for animal populations �Southwood andHenderson 2000� in order to determine the speciesmean crowding per quadrat. The index is relativelyinsensitive to sample size, performs well in a varietyof situations �Basset 1999� and is calculated as: L ��Sx

2 – x / x2� �1, where Sx2 and x are respectively the

variance and mean of the samples in the four

Table 3. Environmental variables measured, with abbreviations,units and the data type each variable represents.

Environmental variable �abbreviations� Units Data type

Rainfall mm continuousAltitude m continuousSlope degree continuousIsolation m continuousDistance to soil �d.soil� cm continuousDistance to canopy �d.canopy� cm continuouspH continuousSubstratum ordinalShelter ordinalMoisture ordinalLight ordinal

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substrata. The application of this index in vegetationstudies is not common, but in the current situation isadequate since it is intended to evaluate the frequencyof occurrence of different bryophyte and lichen spe-cies in different substrata �substrate specificity insteadof host specificity�. The calculation was made onlyfor the species represented by a minimum of fourquadrats, because the species could be collected fromfour possible substrata. To standardize the samplingeffort among the substrata, the number of quadratswhere the species were found was divided by the to-tal number of quadrats made in those substrata, priorto applying the index. A species was considered to bea specialist �as opposed to a generalist� on a particu-lar substrata if L � 3.0. The value of the index in-creases for more specialized species.

A Pearson correlation coefficient was calculatedbetween the species richness �total bryophytes,mosses, liverworts and lichens; alpha-diversity� andthe vascular plant cover calculated as the sum ofcover �%� of each quadrat.

The whole abundance data set of abundances of139 species in 226 quadrats was classified using aclustering algorithm, Two-Way-Indicator SpeciesAnalysis �TWINSPAN; Hill 1979; Gauch and Whit-taker 1981� that classifies vegetation communities ac-cording to their floristic similarity. The classificationwas carried out using a PC-based software package,Community Analysis Package �CAP 1999; PiscesConservation Ltd. http://www.irchouse.demon-.co.uk/�.

The vegetation data matrix �abundance of 139 spe-cies� was ordinated using Detrended CorrespondenceAnalysis �DCA� �CAP 1999� employing default op-tions. A non parametric correlation method �Spear-man rank correlation� was used to correlate thesample axes �DCA scores� and levels of environmen-tal variables �STATVIEW SE Graphics�. A conserva-tive Bonferroni test was applied to control for type Ierrors that appear when performing multiple tests�Sokal and Rohlf 1995�. The accepted level ofsignificance is thus �’ � � / k, where � � 0.05 and k� 10, the number of environmental variables.Significance of the correlation was inferred from ap-propriate tables �Zar 1984�.

Results

Species richness

Two hundred and twenty six quadrats were obtainedfrom the four substrata �bark of Laurus azorica andJuniperus brevifolia, basalt rock and soil� and 139species identified �Table 4�. Among these there were16 lichen taxa, eight fern species, 11 flowering plantsand 106 bryophyte species �one hornwort, 64 liver-worts and 41 mosses�. Among the ten most frequentlyrecorded species �Table 5�, seven were liverworts�Plagiochila bifaria, Frullania tamarisci, Lejeunealamacerina, Diplophyllum albicans, Scapania graci-lis, Cephalozia crassifolia and Calypogeia muelleri-ana�, two species were mosses �Hypnum uncinulatumand Thuidium tamariscinum� and one was a fern �Hy-menophyllum tunbrigense�. Twenty two cryptogamicspecies were present in only one of the quadrats, nineliverworts �e.g., Heteroscyphus denticulatus, Lep-toscyphus cuneifolius, Plagiochila longispina, Radulawichurae, Tylimanthus azoricus�, eight mosses �e.g.,Fissidens coacervatus, F. papillosus, F. taxifolius,Hookeria lucens, Zygodon viridissimus�, and five li-chens �e.g., Dimerella pineti, Parmelia tiliacea, Stictadufourii�.

The average number of species per quadrat �spe-cies richness� was highest on rock �12.1�, followed bysoil �10.7� and Juniperus brevifolia bark �10.2� andlowest on Laurus azorica bark �8.6�. The number ofvascular species per quadrat was highest on soil �1.7�,but with comparable values on rock �1.1� and J.brevifolia bark �0.9� and the lowest on L. azorica bark�0.4�. The highest number of bryophyte species perquadrat occurred on rock �10.7�, followed by J.brevifolia bark �9.0�, soil �8.5� and L. azorica bark�7.6�. Lichens were the only group that presentedhigher values on L. azorica bark �0.6� than on theother substrata.

No correlations were obtained between the bryo-phyte species richness and vascular plant cover �r �0.08, p � 0.05�, between the lichen species richnessand the vascular plant cover �r � 0.00, p � 0.05� orbetween the bryophyte and lichen richness of species�r � 0.00, p � 0.05�.

Species similarity

Table 6 compares the similarities of species betweenthe four substrata studied in Terceira native forestsusing the Sørensen index. The values obtained are

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Table 4. A list of the taxa recognized in this study of six nativeforest stands in Terceira island �Azores� with abbreviations laterused in tables and figures. 107 bryophytes �1 hornwort, 64 liver-worts and 41 mosses�, 16 lichen taxa and 17 vascular species.

Abbreviations Species

Hornwortsanca Anthoceros caucasicus

Liverwortsacwi Acrobolbus wilsoniiadde Adelanthus decipiensapmi Aphanolejeunea microscopicaapsi Aphanolejeunea sintenisiibaat Barbilophozia attenuatabaaz Bazzania azoricabltr Blepharostoma trichophyllumcaar Calypogeia argutacafi Calypogeia fissacamu Calypogeia muellerianacebi Cephalozia bicuspidatacecr Cephalozia crassifoliacelu Cephalozia lunulifoliachce Cheilolejeunea cedercreutziicomi Cololejeunea minutissimacoca Colura calyptrifoliacoco Conocephalum conicumdial Diplophyllum albicansdrha Drepanolejeunea hamatifoliafrmi Frullania microphyllafrta Frullania tamariscifrte Frullania teneriffaegegr Geocalyx graveolanshamo Harpalejeunea moelleriheaz Herbertus azoricushtde Heteroscyphus denticulatusjuhu Jubula hutchinsiaejugr Jungermannia gracillimaleec Lejeunea ecklonianalefl Lejeunea flava ssp. mooreilehi Lejeunea hibernicalela Lejeunea lamacerinalepa Lejeunea patensleaz Lepidozia azoricalecu Lepidozia cupressinalere Lepidozia reptanslpaz Leptoscyphus azoricuslpcu Leptoscyphus cuneifoliuslobi Lophocolea bidentatalosp Lophozia sp.love Lophozia ventricosamama Marchesinia mackaiimefu Metzgeria furcatamele Metzgeria leptoneuramnfu Mnioloma fuscumnocu Nowellia curvifoliaodpr Odontochisma prostratumpaly Pallavicinia lyelliipeep Pellia epiphyllaplal Plagiochila longispina

Table 4. Continued.

Abbreviations Species

plbi Plagiochila bifariaplex Plagiochila exiguapoca Porella canariensispoob Porella obtusataraaq Radula aquilegiaraca Radula carringtoniiraho Radula holtiirawi Radula wichuraerich Riccardia chamaedryfoliarimu Riccardia multifidasavi Saccogyna viticulosascgr Scapania gracilistene Telaranea nematodestyaz Tylimanthus azoricus

Mossesanbe Andoa berthelotianaatun Atrichum undulatumbrru Brachythecium rutalsilumcamp Campylopus sygnaeuscyla Cyclodictyon laetevirensdast Daltonia stenophylladisc Dicranum scottianumdisp Ditrichum sp.ecpr Echinodium prolixumecre Echinodium renauldiieupr Eurhynchium praelongumeusp Eurhynchium speciosumfias Fissidens asplenioidesfico Fissidens coacervatusfilu Fissidens luisieriifipa Fissidens papillosusfipo Fissidens polyphyllusfise Fissidens serrulatusfita Fissidens taxifoliushehe Heterocladium heteropterumholu Hookeria lucenshysp Hylocomium splendenshyun Hypnum uncinulatumlevi Lepidopilum virensleju Leucobryum juniperoideummyho Myurium hochstetteriplun Plagiomnium undulatumplne Plagiothecium nemoralepoco Polytrichum communepofo Polytrichum formosumpsel Pseudotaxiphyllum eleganspsla Pseudotaxiphyllum laetevirensscpu Scleropodium purumsesu Sematophyllum substrumulosumsppa Sphagnum palustrespsu Sphagnum subnitenstefo Tetrastichium fontanumthal Thamnobryum alopecurumthma Thamnobryum maderensethat Thuidium tamariscinumzyvi Zygodon viridissimus

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generally above 0.40 and most above 0.60, i.e., thespecies composition is similar among the substrata.The two most similar ones are rock and soil, exceptwith lichens, where L. azorica bark and soil havehigher values. Generally, the two most different sub-strata are the bark of L. azorica and J. brevifolia, ex-cept for vascular plants where L. azorica bark androck present a lower value �0.25�. The lichen florashows some low Sørensen index values, with the barkof Juniperus brevifolia harbouring a more specificflora of lichens than Laurus azorica �0.13�, rock�0.25� or soil �0.14�.

Substratum specificity

The most common 10% of species �14� did notpresent a clear substratum preference behaving con-sistently as generalists. However, if the substrata aregrouped as bark and non-bark, the liverwort Plagio-chila bifaria occurred in 88% of the bark samples�only 12% as non-bark� and two species behaved asnon-epiphytic, i. e. Thuidium tamariscinum �84%�and Calypogeia muelleriana �85%�. The Lloyd indi-ces �L� are in Table 5. The moss Fissidens serrulatus�L � 3.04� showed specificity towards the rock, andone lichen species, Lobaria virens �L � 3.27�, wasmore faithful to Laurus azorica bark. The largestgroup of species, liverworts, also presented the larg-est number of specialist species, seven. Three liver-worts were most commonly found on Juniperusbrevifolia bark: Lepidozia azorica �L � 3.23�, Lep-toscyphus azoricus �L � 3.01� and Nowellia curvifo-lia �L � 3.87� while two liverworts, Frullaniamicrophylla �L � 4.63� and Radula cf. jonesii �L �4.44� were collected only on Laurus azorica bark.Two liverworts, Calypogeia arguta �L � 3.49� andPellia epiphylla �L � 3.06� were commonly found onrock.

Floristic ordination

The DCA ordination of the full floristic datasetyielded four primary axes with eigenvalues of 0.62,0.48, 0.36 and 0.28. The species ordination ispresented in Figure 2 �axis 1 and 2� and the ordina-tion of quadrats is in Figure 3 �axis 1 and 2�. Spear-man rank correlation coefficients �rs�, calculatedbetween the sample axes and environmental variables�Table 7�, indicate the following relationships: Axis 1reflects mainly the water gradient exhibited by thedifferent samples with an important negative correla-tion with rainfall, altitude and shelter. Positive corre-lations of Axis 1 are found with pH, distance to thesoil and light. Axis 2 exhibits positive correlationswith pH and distance to the canopy and negative cor-relations with distance to soil and slope. The stron-gest relationships of the firs two axis are representedin Figure 4.

The species ordinations �Figure 2� show meaning-ful ecological orderings of the bryophytes. Figure 2shows taxa characteristic of the wettest sites �e.g.,Bazzania azorica, Calypogeia arguta, C. muelleriana,Fissidens luisierii, Geocalyx graveolens, Hookerialucens, Jungermannia gracillima, Leucobryum juni-

Table 4. Continued.

Abbreviations Species

LichensClCo Cladonia g. coccifera �L.� Willd.Clsp Cladonia spp.DiPi Dimerella pineti �Ach.� VezdaHeLe Heterodermia leucomelos �L.� PoeltLeSp Lepraria spp.LoVi Lobaria virens �With.� LaundonNoPu Normandina pulchella �Borrer� Nyl.PaEn Parmelia endochlora Leight.PaSp Parmelia spp.PaTi Parmelia tiliacea �Hoffm.� Ach.PeSp Peltigera spp.PhSp Physcia spp.PsLa Pseudocyphellaria lacerata Degel.StCa Sticta canariensis �Ach.� Bory ex DeliseStDu Sticta dufourii DeliseStFu Sticta fuliginosa �Hoffm.� Ach.

Vascular plantsASPL Asplenium onopteris L.BLEC Blechnum spicant �L.� RothCULC Culcita macrocarpa K. Presl.DRYO Dryopteris azorica �Christ� AlstonELAP Elaphoglossum paleaceum �Hook. and

Grev.� SledgeERIC Erica azorica Hochst. ex Seub.HOLC Holcus lanatus L.HYME Hymenophyllum tunbrigense �L.� Sm.ILEX Ilex perado Ait. ssp. azorica �Loes.� Tut.LUZU Luzula purpureo-splendens Seub.LYSI Lysimachia azorica Hornem. ex Hook.MYRS Myrsine africana L.PTER Pteridium aquilinum �L.� KuhnSELA Selaginella kraussiana �Kunze� A.BraunSIBT Sibthorpia europaea L.TRIC Trichomanes speciosum Willd.VACC Vaccinium cylindraceum Sm.

131

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altic

rock

�n�

38�

Soil

�n�

64�

Perc

enta

geof

occu

rren

ce

Liv

erw

orts

adde

Ade

lant

hus

deci

pien

s1.

752

00

21.

8ap

mi

Aph

anol

ejeu

nea

mic

rosc

opic

a1.

2310

63

39.

7ap

siA

phan

olej

eune

asi

nten

isii

0.96

34

45

7.1

baat

Bar

bilo

phoz

iaat

tenu

ata

2.39

05

02

3.1

baaz

Baz

zani

aaz

oric

a1.

480

2411

1321

.2ca

arC

alyp

ogei

aar

guta

3.49

00

72

4.0

cafi

Cal

ypog

eia

fissa

1.44

23

612

10.2

cam

uC

alyp

ogei

am

uell

eria

na1.

742

719

3226

.5ce

crC

epha

lozi

acr

assi

foli

a1.

302

2514

2127

.4co

mi

Col

olej

eune

am

inut

issi

ma

1.42

17

13

5.3

coca

Col

ura

caly

ptri

foli

a1.

953

30

02.

7co

coC

onoc

epha

lum

coni

cum

2.47

00

32

2.2

disc

Dip

loph

yllu

mal

bica

ns1.

776

4710

931

.9dr

haD

repa

nole

jeun

eaha

mat

ifol

ia1.

2613

244

821

.7fr

mi

Fru

llan

iam

icro

phyl

la4.

636

00

02.

7fr

taF

rull

ania

tam

aris

ci1.

2445

2710

2446

.9fr

teF

rull

ania

tene

riff

ae1.

142

94

48.

4ge

grG

eoca

lyx

grav

eola

ns2.

230

27

45.

8ha

mo

Har

pale

jeun

eam

oell

eri

2.45

91

20

5.3

juhu

Jubu

lahu

tchi

nsia

e2.

494

01

02.

2le

flL

ejeu

nea

flava

ssp.

moo

rei

2.02

212

12

7.5

lela

Lej

eune

ala

mac

erin

a1.

0832

2016

1938

.5le

paL

ejeu

nea

pate

ns1.

640

72

24.

9le

azL

epid

ozia

azor

ica

3.23

018

12

9.3

lecu

Lep

idoz

iacu

pres

sina

1.72

126

413

19.5

lere

Lep

idoz

iare

ptan

s1.

750

144

49.

7lp

azL

epto

scyp

hus

azor

icus

3.01

120

04

11.1

mam

aM

arch

esin

iam

acka

ii2.

539

11

15.

3m

efu

Met

zger

iafu

rcat

a1.

976

12

04.

0m

nfu

Mni

olom

afu

scum

1.87

117

43

11.1

nocu

Now

elli

acu

rvif

olia

3.87

120

01

9.7

odpr

Odo

ntoc

hism

apr

ostr

atum

1.50

06

32

4.9

peep

Pel

lia

epip

hyll

a3.

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020

1013

.3pl

biP

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ochi

labi

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a1.

0239

4418

3158

.4pl

exP

lagi

ochi

laex

igua

1.69

2131

25

26.1

poca

Por

ella

cana

rien

sis

1.11

20

11

1.8

poob

Por

ella

obtu

sata

1.55

70

33

5.8

raaq

Rad

ula

aqui

legi

a1.

6416

25

512

.4

132

Tabl

e5.

Con

tinue

d.

Spec

ies

code

Iden

tifica

tion

Llo

yd’s

inde

xL

auru

s�n

�56

�Ju

nipe

rus

�n�

68�

Bas

altic

rock

�n�

38�

Soil

�n�

64�

Perc

enta

geof

occu

rren

ce

raca

Rad

ula

carr

ingt

onii

1.11

20

11

1.8

raho

Rad

ula

holt

ii2.

708

02

04.

4ri

chR

icca

rdia

cham

aedr

yfol

ia2.

720

14

12.

7sa

viSa

ccog

yna

viti

culo

sa1.

784

114

1916

.8sc

grSc

apan

iagr

acil

is2.

091

444

1829

.6te

neTe

lara

nea

nem

atod

es1.

431

1615

2525

.2

Mos

ses

anbe

And

oabe

rthe

loti

ana

1.98

260

78

18.1

atun

Atr

ichu

mun

dula

tum

2.23

00

49

5.8

cyla

Cyc

lodi

ctyo

nla

etev

iren

s1.

542

04

65.

3di

alD

icra

num

scot

tian

um2.

330

01

42.

2ec

prE

chin

odiu

mpr

olix

um1.

4919

78

316

.4eu

prE

urhy

nchi

umpr

aelo

ngum

1.90

20

53

4.4

fias

Fis

side

nsas

plen

ioid

es1.

651

03

33.

1fil

uF

issi

dens

luis

ieri

i2.

470

03

22.

2fis

eF

issi

dens

serr

ulat

us3.

042

010

26.

2he

heH

eter

ocla

dium

hete

ropt

erum

2.18

10

31

2.2

hyun

Hyp

num

unci

nula

tum

1.30

1551

925

44.2

levi

Lep

idop

ilum

vire

ns1.

833

210

69.

3le

juL

euco

bryu

mju

nipe

roid

eum

1.48

016

1425

24.3

myh

oM

yuri

umho

chst

ette

ri2.

1339

27

1126

.1pl

unP

lagi

omni

umun

dula

tum

2.46

00

43

3.1

plne

Pla

giot

heci

umne

mor

ale

2.07

40

20

2.7

poco

Pol

ytri

chum

com

mun

e2.

140

13

106.

2po

foP

olyt

rich

umfo

rmos

um2.

410

21

95.

3ps

elP

seud

otax

iphy

llum

eleg

ans

1.43

211

1415

18.6

sppa

Spha

gnum

palu

stre

2.36

10

518

10.6

spsu

Spha

gnum

subn

iten

s2.

710

03

137.

1te

foTe

tras

tich

ium

font

anum

2.36

20

30

2.2

thal

Tha

mno

bryu

mal

opec

urum

2.34

130

41

8.0

that

Thu

idiu

mta

mar

isci

num

1.68

93

2537

32.7

Lic

hens

LoV

iL

obar

iavi

rens

3.27

50

01

2.7

NoP

uN

orm

andi

napu

lche

lla

2.56

30

01

1.8

PsL

aP

seud

ocyp

hell

aria

lace

rata

1.19

20

23

3.1

StC

aSt

icta

cana

rien

sis

2.56

130

31

7.5

133

peroideum, Pallavicinia lyellii, Polytrichum com-mune, P. formosum, Sphagnum palustre, S. subnitens�clustered at the negative end of axis 1 and thesegrade, with increasingly positive scores to taxa whichare recognizable as much less reliant on permanentwater supply �e.g., Frullania microphylla,Marchesinia mackaii, Metzgeria furcata, Thamno-bryum alopecurum, and the lichens Sticta canarien-sis, S. fuliginosa�. The second axis distinguishesspecies found on higher pH substrata �Calypogeia

fissa, Cyclodictyon laetevirens, Fissidens coacerva-tus, F. serrulatus� from acidophilous species on thenegative part �e.g., Acrobolbus wilsonii, Cheilolejeu-nea cedercreutzii, Herbertus azoricus, Lepidoziaazorica, Leptoscyphus azoricus, L. cuneifolius, Mnio-loma fuscum, Nowellia curvifolia�. This latter groupis also characteristic of more upland areas. On the leftside of the species ordination �Figure 2� there seemsto be a clustering of the epigeic and epilithic species

Table 6. Mutual similarity �Sørensen’s indices� between pairs of substrate type for the different taxonomic groups among the four substrataconsidered in the native forests of Terceira Island. The higher the similarity of species composition between the pairs of substrata, the closerthe index becomes to 1.00.

Substrata Total Bryophytes Mosses Liverworts Lichens Vascular plants

Laurus azorica – Juniperus brevifolia 0.54 0.58 0.38 0.67 0.13 0.62Laurus azorica � basaltic rock 0.62 0.68 0.68 0.69 0.43 0.25Laurus azorica – soil 0.64 0.65 0.63 0.66 0.80 0.42Juniperus brevifolia – basaltic rock 0.60 0.63 0.44 0.71 0.25 0.53Juniperus brevifolia – soil 0.60 0.64 0.46 0.73 0.14 0.64Basaltic rock – soil 0.75 0.78 0.73 0.82 0.50 0.72

Figure 2. First two axis of a DCA ordination of a vegetation survey of Terceira Island �Azores� for 139 forest species �abbreviations as inTable 4; group symbols: ��� hornworts; �*� liverworts; ��� mosses; �□� lichens; �–� vascular plants�. The first axis goes from wet to dryconditions and the second axis is positively correlated with and pH and negatively correlated with the distance to the soil.

134

whereas epiphytes are found mostly on the right sideof axis 2.

The DCA ordination of samples employing the firsttwo axes is in Figure 3. The first axis shows a gradi-ent of samples from the wettest conditions: soil on

Serra de Santa Bárbara, Mistérios Negros, TerraBrava through the rock substrata to the drier environ-ment of Laurus azorica bark at Matela. Samples fromJuniperus brevifolia bark occupy a medium positionon axis one but are generally better separated by thesecond axis, where they form a coherent group on thenegative part of the axis, with the acidic pH values.Soil samples of the lowest altitude site �Matela� oc-cupy the other extreme of that axis.

Classification

Based on TWINSPAN cluster analysis, the 226 quad-rats and 139 species of bryophytes, lichens and vas-cular species occurring in the native forests ofTerceira Island were divided into eight ecologicallymeaningful putative community groups, A – H �Fig-ure 5�. The community types identified here are hy-pothetical, as they have not been placed into existingtypes or categories �Mueller-Dombois and Ellenberg1974�. Environmental conditions regarding the differ-ent groups are reported in Table 8.

Figure 3. First two axis of a DCA ordination of a vegetation survey of Terceira Island �Azores� for 226 forest quadrats �site abbreviations asin Table 1; substrata symbols: �x� basaltic rock; �"� Juniperus brevifolia bark; ��� Laurus azorica bark; �◊� soil�. The first axis goes fromwet to dry conditions and the second axis is positively correlated with and pH and negatively correlated with the distance to the soil.

Table 7. Spearman’s rank correlation coefficients �rS� computedbetween the axes of the DCA ordination of the samples collectedinside the native Azorean forests and the values of the quantitativeenvironmental variables. s, significant correlation after a Bonfer-roni test ��’�0.05/10�.

AX1 AX2 AX3 AX4

rainfall � 0.520 s � 0.181 � 0.283 s 0.287 sshelter � 0.316 s 0.109 0.236 s 0.023d.canopy 0.130 0.445 s 0.513 s 0.061d.soil 0.339 s � 0.485 s � 0.360 s � 0.118altitude � 0.401 s � 0.070 � 0.273 s 0.387 sisolation 0.117 0.143 0.027 0.049moisture � 0.064 0.195 � 0.206 s � 0.028slope 0.031 � 0.348 s � 0.031 � 0.079pH 0.498 s 0.460 s 0.200 s 0.085light 0.272 s � 0.157 -0.387 s 0.062

135

In groups A and B Dicranum scottianum, Hypnumuncinulatum and Scapania gracilis aggregate most ofthe Juniperus brevifolia quadrats �60 out of 68� aswell as five soil and rock quadrats.

Group A is discriminated by Leucobryum juniper-oideum, and includes 33 medium altitude samples�average altitude, 621 m�, of Juniperus brevifolia barkand 3 samples of soil.

Group B, is positively separated by the presence ofBazzania azorica, Mnioloma fuscum and the fern Hy-menophyllum tunbrigense; it includes a great numberof interesting liverwort species such as Aphanolejeu-nea sintenisii, Cheilolejeunea cedercreutzii, Lejeuneapatens, Lepidozia azorica, Leptoscyphus azoricus andNowellia curvifolia as preferentials. This groupincludes most of the Serra de Santa Bárbara Junipe-rus samples �23 out of 25�, at an average altitude, of889 m altitude. Besides altitude and its related varia-bles �e.g., precipitation, direct and occult, tempera-ture, wind speed� other differences between theenvironmental conditions of groups A and B, are re-lated to the physiognomy of the forests. Generally,Santa Bárbara Juniperus forest has lower trees, thatare closer to each other, with trunks better lit and withless shelter from evaporation.

Groups C, D and E include the ground samples�soil and rock� of the medium and higher altitude for-ests. In contrast to groups A and B, these vegetationtypes include a high number of moss species.

Group C is indicated by the presence of Calypo-geia muelleriana but other liverworts such as Bazza-nia azorica, Calypogeia arguta, Cephalozia crassifo-lia and Geocalyx graveolens are also strong positivedifferential species. This group, as well as group E,has similar proportions of quadrats from rock andsoil.

Group D encompasses the soil samples from Serrade Santa Bárbara, Terra Brava and Mistérios Negros�average altitude 769 m�. It is characterized by a rela-tively low number of bryophyte species, and a highcover of Sphagnum species. This is a homogeneousgroup, with Sphagnum palustre and two endemicvascular species, Lysimachia azorica and Luzula pur-pureo-splendens, as indicator species. Other commonspecies are Sphagnum subnitens, Polytrichum com-mune and P. formosum. Not surprisingly, owing to thepresence of Sphagnum, the moisture values are thehighest obtained �average 4� and pH values are low�average 4.3 units�.

Group E is discriminated by Pellia epiphylla andThuidium tamariscinum. Other faithful species in-

Figure 4. Relationships between the sample scores of the DCA ordination axis and the environmental variables: a� rainfall; b� pH; c� distanceto the canopy �d.canopy� and d� distance to the soil �d.soil�. Non transformed Y values were used in the figure.

136

Figure 5. TWINSPAN dendrogram of site associations based on a survey of bryophytes, lichens and vascular species in the native forests ofTerceira Island. n, number of samples on each category. Substrata: b, basalt rock; j, Juniperus brevifolia bark; l, Laurus azorica bark; s, soil.Sites: M, Matela; T, Terra Brava; L, Lomba; N, Mistérios Negros; P, Pico Rachado; S, Serra de Santa Bárbara.

137

Tabl

e8.

Env

iron

men

tal

vari

able

s�a

vera

gean

dst

anda

rder

rors

�an

dnu

mbe

rof

spec

ies

char

acte

rist

icof

each

TW

INSP

AN

grou

p�A

toH

�.n,

num

ber

ofqu

adra

tsin

clud

edin

each

com

-m

unity

.

A,

n=

36B

,n

=29

C,

n=

30D

,n

=21

E,

n=

37F,

n=

49G

,n

=14

H,

n=

9

seav

erag

ese

aver

age

seav

erag

ese

aver

age

seav

erag

ese

aver

age

seav

erag

ese

aver

age

Alti

tude

�m�

621

9.4

889

24.9

695

22.2

769

33.7

643

18.7

643

11.4

495

25.0

444

3.7

Rai

nfal

l�m

m�

4617

137.

858

5514

6.5

4972

140.

353

0918

7.2

4303

176.

141

9610

9.3

2597

253.

222

300.

0

Isol

atio

n�m

�2.

30.

181.

80.

092.

00.

072.

50.

192.

50.

192.

40.

292.

90.

152.

90.

60Pe

rim

eter

at5

cm79

3.1

623.

152

2.8

521.

432

2.2

Peri

met

erat

150

cm40

1.3

301.

932

1.5

381.

127

1.4

Dis

tanc

eto

the

cano

py�c

m�

261

19.7

145

17.5

388

29.2

307

40.1

466

25.4

361

22.8

415

40.0

356

54.3

Dis

tanc

eto

the

soil

�cm

�72

8.9

579.

617

5.1

136.

17

3.5

897.

120

8.0

6323

.2Sl

ope

�deg

ree �

103

10.4

858.

166

7.4

3310

.861

8.9

765.

286

11.8

901.

0

pH4.

00.

044.

10.

044.

30.

104.

30.

075.

00.

085.

20.

085.

40.

115.

30.

07Sh

elte

r3.

20.

122.

80.

153.

90.

133.

20.

143.

40.

183.

00.

112.

70.

223.

30.

29M

oist

ure

1.2

0.11

1.2

0.13

3.0

0.20

4.0

0.23

2.5

0.13

1.1

0.05

1.8

0.15

1.1

0.11

Lig

ht2.

70.

143.

10.

152.

10.

132.

80.

172.

30.

152.

90.

143.

10.

162.

80.

17

Num

ber

ofliv

erw

ort

spec

ies

3235

3522

3441

2219

Num

ber

ofm

oss

spec

ies

89

1913

3017

1913

Num

ber

oflic

hen

taxa

43

24

39

45

Num

ber

ofva

scul

arsp

ecie

s3

89

910

58

2

138

clude Cyclodictyon laetevirens, Fissidens luisierii, F.serrulatus, Pseudotaxiphyllum elegans, Riccardiachamaedryfolia, Saccogyna viticulosa, Scapania gra-cilis and Telaranea nematodes. Average pH �5.0units� is higher than in group C �4.3 units� and wateravailability is lower for group E than for group C.

Groups F, G and H include most of the samplesfrom Laurus azorica communities �53 out of 54� aswell as the ones from lower altitude.

Group F, with 41 bark quadrats, mainly includesthe samples from Terra Brava, Lomba and PicoRachado, at medium to high altitude �average 643 m�.A high number of liverworts �41� and lichens �9�characterizes this group, with Plagiochila bifaria asthe main indicator species. The mosses Myuriumhochstetteri, Andoa berthelotiana and Hypnumuncinulaturm, and the liverworts Frullania tamarisci,Lejeunea lamacerina and Plagiochila exigua are alsocommon within this group, including mainly largetrees �circumference at the base: 52 cm�.

Group G, includes 14 quadrats, mainly fromMatela �12�, the lowest lying area investigated �aver-age 444 m�, on a mixture of substrata, seven on rock,three on soil and four on Laurus azorica bark. Thisgroup is characterized by the presence of threemosses, Echinodium prolixum, Thuidium tamarisci-num, Plagiomnium undulatum. Other positive prefer-ential species include Andoa berthelotiana, Myuriumhochstetteri and Frullania tamarisci. The pH valuesare higher �5.4 units� than on other soil and rockgroups and the samples are among the best lit.

Finally, Group H is a smaller �9 quadrats�, homo-geneous group on Laurus azorica bark, with fewerspecies �19 liverworts and 13 mosses�, and includesonly samples from Matela. The liverwort Marchesiniamackaii is a positive indicator species for this group,but the lichen Sticta canariensis is also a positivepreferential. Group H includes the samples withPorella canariensis, Radula carringtonii, Semato-phyllum substrumulosum and Zygodon viridissimus.Laurus trees from this group are among the smallestsampled, with average circumferences at the base of32 cm.

Discussion

In many parts of the world, forests with bryophyteand lichen epiphytes have been highly disturbed andit is known that man’s influence on epiphyte commu-nities leads to their simplification �Schmitt and Slack

1990; Rose 1992; Sim-Sim et al. 1995; Sjögren1995b�. The native evergreen forests of Terceira, incontrast, are essentially undisturbed by man and farfrom industrial zones. The occurrence, abundance andluxuriance of bryophytes in the Terceira forests arethus expected to show the natural condition of themature forests in the Azores. While the phytosocio-logical analysis of Sjögren �2003� includes commu-nities in a greater number of islands and indicatesdifferences among the islands, Terceira is generallyrecognized as having some of the richest and largestnatural forest areas of the archipelago �Sjögren 1973,1978, 2003; Borges 1990, 1992; Gabriel 1994; Dias1996�. Therefore, these results may, with caution, becompared with the earlier analyses.

One of the most striking features of this study wasthe large number of taxa identified, 139, including 17vascular species �eight ferns�. The region is charac-terized by a higher proportion of liverworts �64 spe-cies� than mosses �41 species� and of bryophytescompared with macrolichens �16 taxa� �Table 4�.Studies from Australian forests �Pharo and Beattie1997�, inspecting a similar range of substrata,revealed far fewer bryophyte species �77�, especiallyliverworts �only 20 species�, but a higher number oflichen species �69�. Studies of tropical rainforeststhough, have shown higher proportions of liverwortsthan mosses and lichens �Rhoades 1995; Richards1996�. For instance, the analysis of epiphytes in alowland rain forest of Guyana identified 52 mosses,82 liverworts and 36 lichens �Cornelissen and Grad-stein 1990�. The high number and frequency of liver-worts is typical of hyper-humid environments, suchas are experienced in the Azorean forests all yearround. The alpha-diversity of the samples is also out-standing: some quadrats �30 � 30 cm� include morethan 25 bryophyte species. These results corroboratethe present complexity and importance of the exist-ing Azorean forests, probably due to a set of favour-able conditions: temperate climate and high level ofhumidity �Gabriel 2000�, and purity of the air.

Our data do not reveal any correlation betweenspecies richness of macrolichens and bryophytes, andcover of vascular plants, contrasting with the compar-ative study carried out by Pharo and Beattie �1997�,where a negative correlation between species richnessof the groups was observed, bryophytes preferring thewettest sites. Studies in North American forests havealso shown that bryophytes and lichens occupy dif-ferent vertical zones of the trunks �McCune 1993;Sillett 1995; Sillett and Neitlich 1996; McCune et al.

139

1997� with bryophytes dominating near the ground�more humid habitats� and cyanolichens and othermacrolichens �mainly foliose chlorolichens� dominat-ing progressively higher zones in the canopy �Mc-Cune and Antos 1982; McCune 1993; Ellyson andSillett 2003�. The lack of correlation between lichensand bryophytes in the Azores may be due to the smallnumber of quadrats with lichen species �36%�, therelatively low number of lichen taxa found and theirlow cover values. According to a recent survey �Pur-vis et al. 1996�, Azorean forests are characteristicallylow in lichen biodiversity, although containingseveral rare and endemic species �e.g., Ramoniaazorica, a crustose lichen, restricted to Juniperusbrevifolia�. Closed canopies, smooth fluctuations inhumidity and temperature providing optimal condi-tions for bryophyte growth �Peck et al. 1995� butmany lichens are probably constrained by it �During1992�. Thus, lichen cover was higher in the drier andlower altitude site, Matela.

The hypothesis that bryophytes show reduced sub-stratum affinities in the Azores, �Sjögren 1978, 2003;R. Schumacker pers. comm.� is in part corroboratedby the reduced number of specialist species found foreach substratum �Lloyd Index, Table 5� and the highsimilarity values found for the bryophytes in the foursubstrata �Sørensen Index, Table 6�. Notwithstanding,these comparisons consider only the species compo-sition �presence / absence�, they are not based onquantitative data showing dominance relationships.When these quantitative data are considered, as in or-dinations �Figure 2, Figure 3� or TWINSPAN classi-fication �Table 8�, bryophyte communities do in factseparate by substrata. Schmitt and Slack �1990� whencomparing bryophytes and lichens occurring on fivetree species in North America found a similar result.So, in the Azores, although very few species havehost / substratum-specificity, groupings of specieswere found to be characteristic for the different sub-strata analysed inside the forest: Laurus azorica andJuniperus brevifolia bark, soil and rock.

Two epiphytic alliances were described in theAzores by Sjögren: Echinodion Sjn. 93, a very inclu-sive alliance, for all native cloud-zone forest types�Sjögren 1993, 2003� and Marchesinion Sjn. 96, de-scribed for trunks at low altitude �below 400 m��Sjögren 1996, 2003�. Lepidozia cupressina, consid-ered by Sjögren �1993� as differential towards theEchinodion Sjn. 93 and several other species �e.g.,Dicranum scottianum, Hypnum uncinulatum, Bazza-nia azorica) regarded as differential for associations,

are also included in the present classification analy-sis, mainly discriminating epiphyte groups on Junipe-rus brevifolia bark �TWINSPAN groups A and B�.Group A, at medium altitude �621 m�, is separated bythe moss Leucobryum juniperoideum, which, al-though not specially mentioned for Echinodion Sjn.93 was actually picked out by Hübschmann �1974� inone of the epiphyte communities he described Leuco-bryum juniperoideum – ‘Gesellschaft’. The other Ju-niperus brevifolia epiphyte group, �group B andnegative extreme of DCA axis 2� includes samplesfrom higher altitude �889 m� and was separated by theliverworts Bazzania azorica, Mnioloma fuscum, andthe fern Hymenophyllum tunbrigense. It supports anextraordinary number of mountainous, endemic orrare species �e.g., Acrobolbus wilsonii, Bazzaniaazorica, Cheilolejeunea cedercreutzii, Herbertusazoricus, Lepidozia azorica, Leptoscyphus azoricus,Mnioloma fuscum� seldom if ever found in other con-ditions �ECCB 1995�.

Laurus azorica bark was separated mainly inTWINSPAN groups F and H, by a coherent group ofspecies including Andoa berthelotiana, Frullaniatamarisci and Myurium hochstetteri often accompa-nied by Echinodium prolixum �differential species forthe alliance Echinodion Sjg. 93 �Sjögren 1993� andthe association Echinodietum prolixi Hbs. 74 �Hüb-schmann 1974��. Group F is reiterated in the DCAanalysis, positioned towards the positive end of axis1, relating to lower water availability and higher barkpH, shows a number of species �e.g., Plagiochila bi-faria, Lejeunea eckloniana, L. lamacerina, Metzgeriafurcata, Porella canariensis, Radula aquilegia, R.carringtonii� also characteristic of the epiphytic alli-ance Echinodion Sjn. 93. However the TWINSPANgroup H, also recognizable at the most positive ex-treme of DCA axis 1 �Figure 2� is in harmony withMarchesinion Sjn. 96 �Sjögren 1996, 2003�. The dif-ferential species Marchesinia mackaii, is the mostfaithful of the four differential species of the alliancebut Frullania microphylla, Cololejeunea minutissima,and the moss Zygodon viridissimus were alsorecorded in these samples.

Allorge and Allorge �1946� defined a high altitudeSphagnum region, where an important part of thenatural forests remains even today. Findings by Dias�1996� confirm the presence of Sphagnum in the na-tive forest types dominated by Juniperus brevifoliaand Ilex perado. A group dominated by Sphagnumwas equally found in both floristic analyses �TWIN-SPAN- group D; DCA- beginning of the first axis�,

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related to low pH and waterlogged soil samples onSerra de Santa Bárbara. The latter factor, �averagemoisture 4, in a subjective scale with 5 points, Table8� seems to be determinant supporting the high cov-ers of Sphagnum palustre and restraining the numberof other moss, liverwort and lichen species. Two otherspecies are often found growing in those conditions:Calypogeia muelleriana and Polytrichum commune.Several vascular species occur, including Luzula pur-pureo-splendens and Lysimachia azorica, with highcover degrees. Sjögren �2003� did not refer to such abryophyte community. The genus Sphagnum wasnamed in the bryophyte association Odontochisma-Sphagnum of the Andoa-Nardion Sjn. 95 alliance, butonly for open grassland vegetation and on wet soilescarpments at high altitudes �Sjögren 1995a, 2003�.

Apart from the well-defined group of soil samplesfrom Serra de Santa Bárbara, soil and rock have notseparated from each other clearly in any other floris-tic analysis. These results reflect the high values ofthe similarity indices found between these substrataand confirm the inherent difficulty of segregating‘ground’ in the Azores, when considering the plantcover. Previous analysis had led Hübschmann �1974�to describe a large number of associations �14�, withfew differential species. These included associationsthat were only locally frequent on an epigeic substra-tum in S. Miguel Island, and were not validated else-where. Sjögren �1995a, 2003� described seven asso-ciations within the epigeic alliance Andoae-NardionSjn. 95, mostly separated by the degree of wetness ofthe substratum. Two TWINSPAN groups �C, E� frommedium-high altitude �650 m� were discriminatedwith different values of pH and including a similarnumber of rock and soil quadrats. More acid condi-tions �average pH 4.3� support a community domi-nated by Calypogeia muelleriana and Bazzaniaazorica, with a relatively low number of moss spe-cies associated. On the other hand, Thuidium tama-riscinum and Pellia epiphylla strongly dominatedsubstratum with higher pH values �average 5.0�. Noneof these species is used as a differential of the epigeicor epilithic associations created by Sjögren �1995a,2003�, but this author had suggested that transitionalspecies combinations might be found especially innative cloud-zone forests where they can gradetowards epilithic or epixylic communities. TWIN-SPAN group G �also found towards the end of DCAaxis 1�, includes characteristic species of the epigeicalliance Andoae-Nardion Sjn. 95 such as Andoa ber-thelotiana, Echinodium prolixum, Myurium hochstet-

teri and Fissidens asplenioides, frequently found onrock, Laurus azorica bark and soil. These species arethus found on a variety of substrata with high pH�average pH, 5.4� and relatively low moisture condi-tions.

Although few environmental variables representsimple unimodal gradients �Bates 1992a; Rhoades1995; Eldridge and Tozer 1997�, water availabilityappears to be the most important environmental var-iable driving the separation of different bryophytecommunities in Terceira Island �Azores�. Dias �1996�,in a CCA ordination analysis of the vegetation typesof the archipelago, found that water availabilitywithin the soil was one of the most informative var-iables separating the vascular communities and waterregime was also suspected to be determinant for li-chen distribution �Purvis et al. 1996�. A wet-dry axiswas the major feature in the DCA ordination �Figure2�, and was also evident in the conditions supportedby the communities created by the TWINSPANanalysis �Table 8�. Nevertheless, a strong influence ofpH was also observed in the different ordinations,separating the samples. These results confirm thatmicroclimate is a determinant of bryophyte distribu-tion but that substrata chemistry, also affects the es-tablishment and growth of individual species andconsequently affects the composition of the commu-nities �see also Snäll and Persson 2000�. Actually, thedifferent chemistry of the barks, reflected by theranges of pH, 4.0 � 4.1 on J. brevifolia and 5.2 �5.4 on L. azorica, is probably among the most infor-mative variables able to discriminate among the setsof species preferring each substrata. Even at equiva-lent altitudes, therefore with similar air humidity, thespecies dominating on Juniperus brevifolia are differ-ent from the species dominating on Laurus azorica.

In summary, the distributions of the native forestbryophytes and lichens of Terceira are governed by acomplex set of factors related to water availability, thestatus of the substrata and the influences of the vas-cular plant community. The ordination analysis indi-cated some strong correlations between the distribu-tion of the species and the environmental variables,mainly water availability and the pH of substrata. ThepH values were found to be a reliable indicator ofbryophyte communities in the forests of Terceira Is-land. Thus, substratum type, which was underesti-mated in other analyses �cf. Allorge and Allorge 1946;Hübschmann 1974; Sjögren 1978, 1993, 1995a, 1996and 2003�, was clearly important in the TWINSPANand DCA analysis, especially the distribution between

141

Juniperus brevifolia and Laurus azorica bark. Con-sidering the generally high values of the Sørensen in-dices and the low number of specialist species foundwith Lloyd’s index, the differences are more in termsof dominance of species than in terms of speciescomposition. It is possible that other factors may alsobe important in the distribution of cryptogams, suchas bark porosity and fertility, nitrogen and phospho-rus levels, dispersal limitations and competition andtemporal evolution. Nevertheless, the groupingsachieved with these ordination methods were able toelucidate some major bryophyte – substratum rela-tionships, that had not previously been considered andthey offer a framework for future research.

Acknowledgements

This research was made possible by a studentshipawarded to R. Gabriel by the Calouste GulbenkianFoundation and was partly supported by CITAA. Weare very grateful to Cecília Sérgio and Palmira Car-valho �Lisbon�, Erik Sjögren �Uppsala�, René Schu-macker �Liége�, and Paulo Borges �Terceira� forhelpful discussions, revising of material and othervaluable inputs into this project. We thank PaulaVagueiro for her help in the field. We also would liketo thank to the anonymous referees who haveimproved the original manuscript.

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