Distribution, Abundance and Biomass of Epiphyte-lianoid Communities

Distribution, abundance and biomass ofepiphyte-lianoid communities in a New Zealandlowland Nothofagus-podocarp temperaterain forest: tropical comparisonsRobert G. M. Hofstede1, Katharine J. M. Dickinson2 and Alan F. Mark2 1Proyecto PaÂramo ±

Ecopar Ecuador, Institute for Biodiversity and Ecosystem Dynamics (IBED-FGB), University

of Amsterdam, Amsterdam, The Netherlands and 2Botany Department, University of Otago,

Dunedin, New Zealand

Abstract

Aim In tropical rain forests, epiphytes can contribute signi®cantly to species diversityand biomass, a feature not generally associated with temperate forest systems. This studyinvestigates epiphyte-liane diversity and biomass on three host trees (two Dacrycarpusdacrydioides [Podocarpaceae] and one Nothofagus menziesii [Fagaceae]).

Location These trees were of varying architecture on different sites in a New Zealandlowland temperate rain forest at 45°43¢ S.

Methods Cover of epiphytic and lianoid species (vascular and non-vascular) wasrecorded in 5 m vertical height segments (trunk), on four aspects (north, south, east andwest); and in four sections (inner, middle, outer branches and branch extremes) on fourbranch faces (positions: topside, both sides, underside) on each tree. Inclination, branchface, and diameter of branch/trunk substrate, height above ground, duff thickness, andlocation on tree (trunkfoot, main trunk, inner branches, middle branches, outerbranches, branch extremes) were all recorded in 359 samples. Epiphytic biomass wasderived for one tree.

Results Sixty-one vascular and ninety-four non-vascular taxa were recorded. Eightcommunities associated with the highly vegetated inner branches and main trunk, andseven indicative of the less vegetated middle to outer branches and branch extremes wererecognized. Thirteen of the ®fteen communities were present on a forest interiorD. dacrydioides tree, nine on a riverside D. dacrydioides tree and seven on a N. menziesiitree. Most of the seven measured environmental variables were statistically signi®cant inrelation to ordination analyses of the samples. Dry mass per unit area and dry bulkdensity recorded were 350 � 125 and 118 � 13 g dm±2, respectively (trunkbase), and206 � 21 and 91 � 4 g dm±2, respectively (inner and middle branches combined).

Main conclusions Epiphytic community analyses that do not include non-vascular ¯oraeither as generalized categories or as individual taxa are incomplete. Values for epiphyticdry weight for the trunkfoot of one tree appear to exceed comparable ®gures recordedfrom tropical rain forest systems. Epiphytic communities and biomass within at leastsome temperate rain forests can be validly compared with those of tropical rain forests.

Keywords

Biomass, bryophytes, epiphytes, lianes, lichens, phorophyte, temperate rain forest,tropical rain forest.

Correspondence: Katharine J. M. Dickinson, Botany Department, University of Otago, PO Box 56, Dunedin, New Zealand.

E-mail: [email protected]

Journal of Biogeography, 28, 1033±1049

Ó 2001 Blackwell Science Ltd

INTRODUCTION

Forest canopies are purported to contain a major proportionof the diversity of organisms on earth and constitute the bulkof photosynthetically active biomass in forest ecosystems(Lowman & Wittman, 1996). The importance of epiphytes interms of both biomass and diversity has been emphasized forseveral distinctive tropical rain forest types in the world(Benzing, 1990). However, relatively little attention hasbeen given to vascular epiphytes in temperate rain forestsystems despite evidence of their importance (Dawson, 1988;Dickinson et al., 1993) although some attention has been paidto non-vascular species (Nadkarni, 1984a; Dickinson et al.,1993; McCune, 1993; Clement & Shaw, 1999). This paperadds to the ®eld of epiphyte forest ecology which is still young(Bergstrom & Tweedle, 1998), yet critical to the full appraisalof rain forest biodiversity. Several studies have been conduc-ted to determine epiphyte diversity patterns (Gentry &Dodson, 1987; Van Leerdam et al., 1990; Wolf, 1993a, b,1994), and the contribution of epiphytes to ecosystemfunction in terms of biomass and nutrient partitioning (PoÂ cs,1980; Nadkarni, 1984; Hofstede et al., 1993; see Lowman& Wittman, 1996 for summary). However, quantitativeinformation is generally lacking on the composition andstructure of epiphytic communities in rain forests, and thein¯uence of environmental variables on their diversity,abundance and distribution on host trees or phorophytes(Dickinson et al., 1993; Wolf, 1994; Hietz & Hietz-Seifert,1995a).

Water supply is the most powerful environmental deter-minant of vascular and non-vascular epiphyte distribution(Benzing, 1998). For the development of a high load ofepiphytic material on trees, continuous high atmospherichumidity is required. These conditions are typically encoun-tered in tropical mountain rain forests, which grow at thealtitudes of the condensation zone and where mist or lowcloud occurs almost daily. Continuously humid environmentsalso occur outside the tropics but studies of epiphytes herehave been few in comparison with those in tropical forestsystems (Nadkarni, 1984a; Dickinson et al., 1993; McCune,1993; Clement & Shaw, 1999). Epiphytic communities insouthern hemisphere temperate rain forests are particularlyunder-investigated although they constitute a signi®cant anddistinctive assemblage of species (Gentry & Dodson, 1987;Dawson, 1988; Dickinson et al., 1993) and contributeconsiderable organic loads. These forest types are typicallyfound near the western coasts of New Zealand, Tasmaniaand southern South America. The prevailing westerly windsof the southern temperate regions cross large oceans, result-ing in the western coasts of the land masses tending toexperience very high precipitation. Climates here are oceanic,being continuously humid (although with negligible fog) withmild winters and cool summers. In these conditions, a highdiversity and biomass of epiphytes can develop (Oliver, 1930;Dawson, 1988; Dickinson et al., 1993).

The ¯ora of southern temperate rain forests is distinct fromthat of tropical rain forests and northern temperate forests,

re¯ecting the distinctive geological history of the hemisphere(Enting & Molloy, 1982; Dawson, 1988; Stevens et al.,1988), and the generally low ratio of land to sea. Ancientelements, their origins associated with the supercontinent ofGondwanaland, dominate the forests in temperate SouthAmerica and Australasia. Genera in the gymnosperm familyPodocarpaceae and species in the dicotyledonous genusNothofagus (Fagaceae) are especially characteristic. This isparticularly true of the Nothofagus-podocarp-broadleavedrain forests of New Zealand which, prior to human occupa-tion about 1 ka ago, were widespread on the three mainislands, North, South and Stewart Islands. Through substan-tial clearance, these rain forests are now of much reducedextent with their largest remaining areas being on the westcoast of South Island (Stevens et al., 1988). Tree taxaassociated with these rain forests generally possess a distinc-tive architecture. The form of those in Podocarpaceae variesfrom tall, generally straight, slightly tapered trunks with somebroad branches yet generally tight canopies above the mainforest layer (see Dickinson et al., 1993), to a spreadingarchitecture, associated with growth in more open conditions.In these latter cases, large horizontal branches through toupright broad branches emerge from a shorter section oftrunk. They are long-lived, some may exceed 1 ka, and arecharacteristically emergent over an angiosperm-dominatedcanopy (Dawson, 1988; Ogden, 1988). The shorter-livedNothofagus taxa (Ogden, 1988) are not generally emergent,but form part of the angiosperm canopy (Dawson, 1988).Individuals tend towards a wider crown, with layered bran-ches, the actual form again being in¯uenced by the particularenvironmental circumstances, and history of the site.

The epiphytic ¯ora in New Zealand itself contains manyGondwanan elements with a high degree of endemism(Oliver, 1930). Dickinson et al. (1993), in a comprehensivestudy of epiphytes and lianes on one podocarp (Dacrycarpusdacrydioides) individual on the South Island's west coast,established that the subtleties of microclimate, in combina-tion with other environmental variables such as branchorientation and duff (humus) depth, were re¯ected inthirteen lianoid-epiphytic communities. Zonation of thesecommunities was indicated only for the canopy withcomplex patterns of associations occurring within thecrown. Tree architecture through branch orientation, time,microclimate and epiphyte life-form were all involved indetermining these communities formed from the twenty-eight vascular species found on this single host.

Our paper builds on this work of Dickinson et al. (1993)by testing the wider applicability of their ®ndings onepiphyte community distribution and the analogies withtropical rain forest features (Dawson & Sneddon, 1969;Dawson, 1988) and communities. We test the hypothesesthat the vascular epiphytic ¯ora of perhumid temperate rainforest is of equivalent diversity and biomass to tropical rainforest systems; and that vascular plant distribution can beused as a surrogate for bryophyte and lichen distribution inthe derivation of epiphyte communities. In particular, wetested the importance of host tree speci®city and tree

Ó Blackwell Science Ltd 2001, Journal of Biogeography, 28, 1033±1049

1034 R. G. M. Hofstede, K. J. M. Dickinson and A. F. Mark

architecture; through non-destructive sampling of the fullcomplement of vascular and non-vascular taxa and weassessed biomass, including duff loadings, through low-impact destructive sampling of organic matter accumulation.This was executed by thoroughly traversing three host trees,involving two species of varying architecture, within an areaof c. 20 ha. Our study is in similar lowland rain forest to thestudy tree of Dickinson et al. (1993) albeit somewhat moredistant from the coast (c. 2 km vs. 80 m).

Study area

Our study was conducted in a mixed Nothofagus-podocarp-broadleaved rain forest in south-west New Zealand, on acoastal alluvial terrace along the Moeraki river, at c. 2 kminland (45°43¢ S, 169°14¢ E) and c. 8 km north of the ColeCreek study location of Dickinson et al. (1993). Both sitesare located within the Haast Ecological District (McEwen,1987). This is characterized by extensive ¯uvio-glacialoutwash plains up to 10 km wide with some isolated ice-smoothed granite domes, and an intermittent series ofvegetated Holocene sand dunes and associated swalesextending inland for up to 2 km (Dickinson & Mark,1994). The indigenous vegetation, which persists over muchof the Haast Ecological District, contains extensive stands oflowland podocarp-broadleaved and mixed Nothofagus-podocarp-broadleaved rain forests interspersed withswamps, mires and lagoons (Mark & Smith, 1975; Scott& Rowley, 1975; Mark & Lee, 1985; Robertson et al.,1991; Dickinson & Mark, 1994). Most of the ecologicaldistrict is protected for its conservation values, and formspart of the 2.8 million ha Southwest New Zealand WorldHeritage Area (Hutching & Potton, 1987; Department ofConservation, 1989; Mark, 1998).

The forest comprises a continuous main canopy layer,c. 20 m tall, consisting of Nothofagus menziesii and otherbroadleaved species, dominantly Weinmannia racemosa.Above this layer, podocarps (Dacrycarpus dacrydioides,Dacrydium cupressinum, Prumnopytis ferruginea) up to42 m emerge. There is a subcanopy layer, c. 12 m tall, withWeinmannia racemosa, the tree fern Dicksonia squarrosaand sapling podocarps frequent, while the understoreyconsists of a discontinuous layer of shrubs and herbs.Bryophytes dominate the ground layer. Trees in the forestsupport a considerable load of epiphytic material whilelianes, notably Metrosideros spp., climb vigorously over andthrough the epiphytic cloak (Dickinson et al., 1993).

The Haast Ecological District is characterized by astrongly perhumid mesothermal climate. This results fromthe high and well-distributed precipitation (3455 mm year±1

spread over 178 rain days (� 1.00 mm rain) at Haast Beach,4 m a.s.l. and 23 km south-west of the study site), as well asgenerally low rates of evapotranspiration (Dickinson et al.,1993) and proximity to the coast. Mean rain days per monthvary only from thirteen in mid-winter (June) to seventeen inspring (October and November). Relative humidity (09.00-hvalues) averages 83% on an annual basis, and ranges frommonthly means of 79% in late winter to 86% in autumn

(March and April). Sunshine levels, however, are relativelyhigh (1853-h annually at Haast Beach or 44% of thepossible total). Winds from the south-west and east areusually associated with clear, dry weather with most of therain resulting from depressions from the north-west whichapproach across the Tasman Sea. Temperatures are generallymild with a mean annual air temperature of 11.3 °C andlittle seasonal or diurnal ¯uctuations: mean monthly valuesrange from 14.9 °C in February to 7.4 °C in July, while themean daily range on an annual basis is 8.0 °C. Air frosts(between May and October) are infrequent, occurring only7.4 days per year on average, while ground frosts occur on55.4 days throughout the year. Fog and snow are bothuncommon, occurring on 6.6 and 0.8 days per year,respectively (Hessell, 1982; New Zealand MeteorologicalService, 1983).

METHODS

Tree selection and sampling

In January 1996, we selected three trees in the study area, twoDacrycarpus dacrydioides and one Nothofagus menziesii. Allhad signi®cant buildup of organic matter at the base of theirtrunks resulting in an organic `talus' slope. The growth formsassociated with the three individuals re¯ected their differ-ent positions in the forest. One host was an emergentD. dacrydioides tree (30 m tall; d.b.h. 1.9 m; trunkfootdimensions 2.85 ´ 1.21 m) growing on a riverbank (here-after termed D-d R). Because of its more freestandingposition this tree had an extensive branching pattern, result-ing in a large crown. To contrast, another D. dacrydioidestree was selected (37 m tall; d.b.h. 1.6 m; trunkfoot1.5 ´ 1.3 m), which was growing as an emergent withinintact closed forest (hereafter termed D-d I). This tree had alarge erect trunk and a tighter but emergent crown with fewerspreading branches. The third tree was a Nothofagusmenziesii in the main canopy. This specimen (22 m tall;d.b.h. 122 cm; trunkfoot diameter 2 m) (hereafter termedN-m) had a large and spreading crown and was also locatedon the riverbank <100 m north-east of the D-d R.

Climbing ropes, assembled by using a sling-shot, allowedaccess to the trees and enabled us to sample the whole trunkand most of the branches. The epiphytic vegetation on thetrees was sampled as completely as possible, depending onaccessibility and visibility. The three trees were sampled in asimilar manner to Dickinson et al. (1993), that is withoutpredetermined zones. The trunk was subdivided into asloping base (trunkfoot), and then into 5 m vertical seg-ments, in which four faces (north, south, east and west) weresampled separately, resulting in four samples per 5 m heightsegment. In each height segment, where possible, twobranches were completely sampled. The main part of thebranches (from the origin to the point where the mainbranch divided into numerous smaller branches and twigs)was then subdivided into three equally long sections: innerbranch, middle branch and outer branch. In each of thesesections, four positions were sampled, one from each face


Epiphytic-lianoid communities in temperate rainforest 1035

(topside, both sides, underside). The branch extremes (twigs)were sampled separately. Because of their inaccessibility,many outer branches and twigs were sampled by usingbinoculars, less accurately; a few were removed with ropesfor closer examination. In all, 150 samples were recorded onthe D-d R, 114 on the D-d I and 95 on the N-m tree.

In each sample, the inclination, position (face) on thebranch (topside, both sides, underside), diameter of thebranch/trunk substrate, height above the ground, duffthickness and location on the tree (trunkfoot, main trunk,inner branch, middle branch, outer branch, branch extreme)was recorded. The percentage cover (projection on to barksurface) of all species of epiphytic and lianoid vascularplants, bryophytes, and foliose and fruticose lichens wasestimated. The combined cover of crustose lichens wasestimated as they were not easily differentiated or readilyidenti®able. Percentage covers of dead material, bare barkand litter also were recorded.

Epiphytic biomass was estimated only on the D-d R treebecause of its easier overall accessibility. Twenty-®vebiomass samples (including dead and living material) weretaken randomly from the inner and outer branches of thecrown using a 12-cm long tube with a sharp cutting edge(diameter 6 cm; volume 339 cm3). Four samples weresimilarly taken from each of four faces (north, south, east,west) of the trunk foot. These samples were dried (48 hours,70 °C) and weighed to calculate their dry bulk density,which was applied per unit area of surface (g dm±2) bymultiplication with the duff thickness. These ®gures wereaveraged for the samples from the canopy (inner and middlebranches) and the trunk foot.

Data analysis

As we were primarily interested in the relationships ofepiphyte diversity, distribution and abundance amongst thethree trees, the data collected from each were combined foranalysis. Using the percentage cover data of the vascular andnon-vascular taxa collectively, and also of the vascular taxaalone, the quadrats were initially classi®ed using theprogram TWINSPANTWINSPAN, which executes a polythetic, divisiveclassi®cation based on reciprocal averaging (Hill, 1979) andindicator species analysis (Hill et al., 1975). Pseudospeciescut levels were 0%, 2%, 10% and 50%. We then performeda detrended correspondence analysis (Hill & Gauch, 1980)on the combined vascular and non-vascular cover data, usingthat facility within the package CANOCOCANOCO (ter Braak, 1987).This ordination was related to the environmental variablesmeasured (inclination, position on the branch, height abovethe ground, location in the tree, thickness of duff layer, anddiameter of substrate) through the process of vector ®ttingwhich incorporates a Monte Carlo permutation procedure(Minchin, 1994). Vector ®tting, or rotational correlation,®nds the direction of maximum correlation for a givenvariable across the ordination, and is formally equivalent toa multiple linear regression of the environmental variablesonto the set of ordination axes (Dargie, 1984; Dickinson &Mark, 1999). Performing an ordination on just the commu-

nity data, then secondarily relating the ordination to theenvironmental variables, followed by an independent assess-ment of the importance of the environmental variables inthis way allows an expression of pure community gradients(McCune, 1997).

The degree of similarity between the epiphytic ¯ora foundon each of the three trees was established using Sùrenson'sCommunity Coef®cient, SCC � 2s/a + b, where a � num-ber of species found at site (tree) A; b � number of speciesfound at site B; s � number of species found at both sites(Sùrenson, 1948).

RESULTS

Species diversity

Overall, using the differentiation of Benzing (1989), thevascular ¯ora comprised fourteen holo-epiphytes, forty-onefacultative epiphytes and six hemi-epiphytes (lianes). Sixty-one vascular species (twenty-three shrubs or small treesincluding ®ve conifers together with six lianes, ®ve orchids,four other forbs, three graminoids and twenty ferns or fernallies) and ninety-four non-vascular species (twenty-eightlichens, thirty-®ve mosses and thirty-one liverworts) wererecorded from the three trees (Table 1). All taxa areindigenous to New Zealand. One hundred and one species(forty-nine vascular and ®fty-two non-vascular: elevenlichens; twenty-two mosses; nineteen liverworts) wererecorded on the D-d R tree, ninety (thirty-seven and®fty-three (fourteen lichens, ®fteen mosses, twenty-four liver-worts), respectively) on the D-d I and ninety-eight (forty-oneand ®fty-seven (seventeen lichens, twenty-three mosses, seven-teen liverworts), respectively) on the N-m tree (Table 2). Ofthese, forty-seven species (30%) occurred on all three trees,forty-one (27%) on two and sixty-seven (43%) on one treeonly. When compared for all species, the D-d I and D-d Rtrees displayed the greatest similarity (Sùrenson's Commu-nity Coef®cient 67%) and the D-d I and N-m trees the least(59%) (see Table 2). Amongst the non-vascular species, thegreatest similarity was also displayed between the twoD. dacrydioides trees (64%), whereas amongst the vascularspecies the D-d R tree appeared equally similar to the D-d Iand the N-m trees (72% and 73%, respectively).

Community analysis

Fifteen general vegetation groups (communities) weredifferentiated from the cover-abundance data of all thevascular plant and non-vascular cryptogamic taxa from the359 samples from all three hosts (Communities I±XV),associated with fourteen Species Classes (A±N). Eightcommunities (I±VIII) comprising a mixture of samples(202 in total) from the three hosts initially split from theremaining seven (IX±XV) which are more clearly differen-tiated by the host tree. The former are associated with themain trunk and highly vegetated inner branches, while thelatter are indicative of the less well vegetated habitats ofthe middle to outer branches and branch extremes. The



Table 1 List of the sixty-one vascular plant and ninety-four non-vascular taxa sampled on three host trees in Nothofagus-podocarp lowlandtemperate rainforest, South Westland, New Zealand. The species class (Fig. 1) for each taxon is listed together with the names of the four mostimportant of the ®fteen communities, ordered in relation to their importance. Communities shown in bold indicate a cover of � 2% of the taxonin the particular community. Epiphyte classes: L � Liane (hemi-epiphyte); F � Facultative epiphyte and O � holo-epiphyte. Nomenclaturefollows Connor & Edgar (1987) or references therein for angiosperms and gymnosperms, Brownsey & Smith-Dodsworth (1989) for ferns andfern allies, Beever et al. (1992) for mosses, Allison & Child (1975) for liverworts, and Malcolm & Galloway (1997) for lichens, except where anauthority is given

Species Species class Community Epiphyte class

Dicotyledons

ApocynaceaeParsonsia heterophylla J II IV X IX L

AraliaceaePseudopanax anomalous A I II FP. colensoi C VI V I III FP. crassifolius A I VII V VI FP. edgerleyi B VI FSchef¯era digitata B V F

CornaceaeGriselinia littoralis B I VI II VII FG. lucida G XIII XIV V IV O

CunoniaceaeWeinmannia racemosa B V I II VI F

FagaceaeNothofagus menziesii C I V VI F

MyrsinaceaeMyrsine australis B II VI IV VII FM. divaricata A I II F

MonimiaceaeHedycarya arborea A II I VI F

MyrtaceaeMetrosideros diffusa B I IV II VII LM. perforata D VIII VII VI I LNeomyrtus pedunculatus A I II V VI F

PolygonaceaeMuehlenbeckia australis A II I IV VIII L

RosaceaeRubus cissoides B IV III L

RubiaceaeCoprosma foetidissima C I II VI FC. lucida C V VI FC. rhamnoides D II VII FC. rotundifolia A I FNertera depressa A I FN. dichondraefolia A II F

ViolaceaeMelicytus rami¯orus A II IV VII F

Monocotyledons

CyperaceaeUncinia angustifolia A I II FU. uncinata A II F

LiliaceaeAstelia solandri D VI V IX VII OLuzuriaga parvi¯ora C V XIII I VI F



Table 1 Continued


OrchidaceaeAporostylis bifolia L XIV FBulbophyllum pygmaeum N XI X XIII XII ODendrobium cunninghamii M XIV XIII X XI OEarina autumnalis N XII X XI XIII FE. mucronata L XIV V O

PoaceaeMicrolaena avenacea A I F

SmilacaceaeRipogonum scandens A I II L

Gymnosperms

PodocarpaceaeDacrycarpus dacrydioides C I II V VI FDacrydium cupressinum G I V VI FManoao colensoi (Hook.) Molloy B VI FPodocarpus hallii M XII FPrumnopitys ferruginea A II I IV VI F

Ferns and fern allies

AspleniaceaeAsplenium bulbiferum A II I FA. ¯accidum B V VIII VI VII OA. polyodon B VII VI V III O

DicksoniaceaeDicksonia squarrosa A II F

DryopteridaceaeRumohra adiantiformis A II F

GrammitidaceaeCtenopteris heterophylla M XV X XI XIV FGrammitis billardierei B I V VII F

HymenophyllaceaeHymenophyllum ferruginea A II OH. ¯abellatum G XIII V XV VII OH. lyallii D XIII II XI V OH. multi®dum L XIV XV V XIII FH. rarum L XIII XIV XV V OH. revolutum B V I VI VII OH. sanguinolentum N X XI IX I FH. scabrum B VI OTrichomanes reniforme D IX VI VIII VII F

PolypodiaceaePhymatosorus diversifolius D VII VI IV VIII FP. scandens M X FPyrrosia eleagnifolia I XII X IV VII F

PsilotaceaeTmesipteris tannensis D V III XII VIII O

Bryophytes

MossesAchrophyllum quadrifarium A I II VCamptochaete sp. A II ICampylopus cf. clavatus B VIIICladomnion ericoides M XI XII XV XCyathophorum bulbosum C I V VI IIDicnemon calycinum M XI X XIV XVD. dixonianum L XIV V



Table 1 Continued


Dicranoloma billardierei G I XIV V XIIID. menziesii B V VII XIII ID. robustum G I XIV VHampeella pallens A II VIIHolomitrium perichaetiale L XIVHypopterygium rotulatum A ILeucobryum candidum B I VII VI VMacomitrium longipes L XIV XM. microstomum M X XI XII VIIIM. submucronifolium L XIIIMesotus celatus L XV XIII XIV XIIPapillaria crocea M XP. ¯avo-limbata L XV XIV XI XIIIPhilonotis sp. A IIPtychomniom aciculare A IIPyrrhobryum bifarium A IRhizogonium distichum A IR. novae-hollandiae B I VI VII VSematophyllum amoenum D VII VIII XII IVS. leucocytus B IV VII VIII VISematophyllum sp. B VThuidium sparsum A II IV VIITrachyloma diversinerve B VIIWeymouthia cochlearifolia F VIII X VII VIW. mollis N XV XI III XII

Moss sp. `very light green' B V VI

Moss sp. `very ®ne' A I

Moss sp. `speckled green' B I V

Liverworts

Aneura alterniloba B VII II IV VIArchilejeunea olivacea A IBazzania adnexa B V I VIBazzania tayloriana D VIII VII XII VIChandonanthus squarrosus M XV IX XI XChiloscyphus coalitus F II X VICololejeunea sp. B VII VIIIFrullania patula B III VII XIGeocalyx caledonica M XIIHeteroscyphus sp. A II IV I VHymenophyton ¯abellatum A ILejeunea sp. A J X VIII VI VIILejeunea sp. B D III VI XII VIILejeunea sp. C B VII III VIII VLepidolaena clavigera F X VII VIIIL. taylorii M XII XV XI VMastigophora ¯agellifera H I XII III VIIIMetzgeria decipiens B VII VIII X VIPlagiochila banksiana A II IP. circinalis K XV XIV XIII IP. deltoidea A IIP. fasciculata F VI VII XI VP. radiculosa M XII X XI VIIIP. strombifolia N XI IX VIII XPodomitrium phyllanthus I II XII IPorella elegantula M XII IX VIII XSchistochila appendiculata A II



major separation of communities I±VIII is indicated byMetrosideros diffusa an endemic climber, Trichomanesreniforme the endemic rhizomatous `kidney' fern, and thependant fern Asplenium polyodon; and communitiesIX±XV by the endemic orchids Dendrobium cunninghamiiand Earina autumnalis, as well as the austral foliose lichenPseudocyphellaria faveolata and the common epiphyticmoss Dicnemon calycinum (Fig. 1).

Community I derives from six trunk-foot samples from theN-m (5) and D-d I (1) trees, and is characterized by SpeciesClasses (SC) A, C, G, K and H (Fig. 1). In this particularcommunity, the dominants are the woody species Neomyr-

tus pedunculata, Pseudopanax crassifolius, and Ripogonumscandens plus the bryophytes Achrophyllum quadrifariumand Trichocolea mollissima (SC A); Dacrycarpusdacrydioides, and Cyathophorum bulbosum (C); Dicrano-loma billardierei and D. robustum (G), Plagiochila circinalis(K) and Mastigophora ¯agellifera (H). Community II isbased on ten trunk-foot and lower main trunk samples fromthe D-d I (8) and D-d R (2) hosts, with a predominance ofAsplenium bulbiferum, Dicksonia squarrosa, Muehlenbec-kia australis, Rumohra adiantiformis, Heteroscyphus sp.,Trichocolea mollissima and Schistochila appendiculata (A).Community III, all from the upper main trunk of D-d I (eight

Table 1 Continued


Teleranea praenitens A ITeleranea tetradactyla A IITrichocolea mollissima A II I VZoopsis leitgebiana D VII VIII X I

Other bryophytes N III II XI XII

Lichens

Bundophoron australe H XIII VIICladina sp. M XIV XI XII XIIICladonia sp. A F VIII XIII VII XCladonia sp. B F VIII XCladonia sp. C M XI XII V VICladonia sp. D C V XIII VI VIIClathroporina sp. B IVLei®dium tenerum B VII VIII VLepraria cf. incana B VPertusaria sp. H III XII XI XVPhyllopsora microdactyla B III IVPseudocyphellaria cinnamonea J X VIII IX VP. degelii M XII XIP. faveolata N XI XII IX XV

P. glabra D VIII IX V VIIP. homoeophylla M XII XI VIIPsoroma durietzii N XII XI VI VIIIRoccellinastrum neglectum B I VII II VSticta lacera L XIV XIII XV VSticta subcaperata M XI XII V XV

Lichen sp. `green globular' B III

Lichen sp. `pink globular' B III

Lichen sp. `powdery lichen' M XII

Lichen sp. `small dangly' M X IX VIII V

Lichen sp. `tight green' B V

Lichen sp. `white fruticose' F X VIII VII IV

Lichen sp. `white powdery' B V

Lichen sp. `other crustose' M XV XIV XII XI

Non-plant groups

Bare bark E IV III XV VIIDead material B III VI VII VLitter B I II VI VRoots F IV III VII II



samples), is dominated by bare bark (E), Pertusaria sp. (H)and Pseudocyphellaria faveolata, Weymouthia mollis andòther bryophytes' (N). Community IV comprises mid maintrunk and inner branch samples from D-d I (eight) and D-dR (six) trees with a predominance of bare bark (E) andPyrrosia eleagnifolia (I). Metrosideros diffusa is one of thefew species in SC B that is dominant in Communities III andIV. It also has a major presence in Communities I and II.Community V occupies the middle to upper main trunk plusthe inner and middle branches on all three hosts, but mostlyon N-m (thirty-six). This community also has a predomin-ance of bare bark (E) together with Hymenophyllum¯abellifolium and Dicranoloma billardierei (G). Forty-threesamples from the middle and inner branches of all three hosttrees form Community VI. Fifty samples from the maintrunk plus inner and middle branches, and twenty-ninesamples from the upper main trunk plus inner to outerbranches, form Communities VII and VIII, respectively, andare found mainly on D-d R (forty-eight and twenty-eight).These three communities are characterized by Trichomanesreniforme, Phymatosorus diversifolius, and Astelia solandri(D) in varying order of importance. The bryophytes Semat-ophyllum amoenum and Zoopsis leitgebiana (also D) as wellas bare bark are prominent in VII, and Dendrobiumcunninghamii (M) together with Earina autumnalis (N) inVIII. Metrosideros diffusa has a major presence in the twolatter communities.

Dealing with the other main cluster of communities, IXderives from sixteen samples on the middle to outer branchesof both D-d trees, and is characterized by Earina autumnalis,Hymenophyllum sanguinolentum and Pseudocyphellariafaveolata (N) as well as Trichomanes reniforme (D).Community X, with twenty-eight mid to outer branch andbranch extreme samples, mostly on D-d R (27), is charac-terized by Pseudocyphellaria cinnamonea (J), Pyrrosia elea-gnifolia (I), Earina autumnalis and Hymenophyllumsanguinolentum (N), along with Dendrobium cunninghamii,an unidenti®ed lichen sp. `small dangling' and Ctenopterisheterophylla (M). Forty-two samples, mainly from the outerbranches and branch extremes of D-d I (41) form Commu-nity XI with Earina autumnalis, Pseudocyphellaria faveolata,Hymenophyllum sanguinolentum and Weymouthia mollis(N) all prominent, along with the mosses Dicnemon calyc-inum and Cladomnion ericoides (forming much of the large`moss balls' up to 50 cm diameter), and the liverwort

Chandonanthus squarrosus (M). Twenty-two samples, allfrom the inner to outer branches of D-d I form CommunityXII and are characterized by Earina autumnalis, Pseudo-cyphellaria faveolata and òther bryophytes' (N), Pyrrosiaeleagnifolia (I), Mastigophora ¯agellifera (S) and bare bark(E). By contrast, Community XIII comprises mostly N-msamples (seventeen) on middle to outer branches with the®lmy ferns Hymenophyllum ¯abellifolium (G), H. rarum (L),the liverwort Plagiochila circinalis (K), Dendrobium cun-ninghamii (M) and Earina autumnalis (N) all prominent.Samples in Community XIV are exclusive to the inner toouter branches of N-m and are typi®ed by a predominanceof bare bark (E), Hymenophyllum multi®dum, H. rarum andSticta lacera (L) and Plagiochila circinalis (K). CommunityXV, with ten mid to outer branch and branch extremesamples, mostly from N-m, is dominated by bare bark (E),Hymenophyllum ¯abellifolium (G), Plagiochila circinalis(K), H. rarum, Papillaria ¯avo-limbata, Mesotus celatus (L),Dendrobium cunninghamii (M), Weymouthia mollis, Earinaautumnalis, Pseudocyphellaria faveolata and òther bryo-phytes' (N).

The similarities and differences between the three hosts isshown in Fig. 2 with respect to the ®rst two axes of the DCAordination of the samples. Considerable overlap between thehosts is apparent with the N-m tree showing the least spreadon Axis 1 (eigenvalue � 0.492). The spread of samples onAxis 2 (eigenvalue � 0.295) is similar for the three trees.Thirteen communities derived from the TWINSPANTWINSPAN classi®-cation are represented on the D-d I, nine on the D-d R andseven on the N-m tree (Figs 1 & 2).

Environmental relationships

Vector ®tting of the measured environmental variables tothe sample scores for the D-d I tree reveal that location onthe tree, height and diameter are all highly signi®cant(P � 0.001) and closely aligned with Axis 1 (Fig. 2a). Theformer two are negatively associated, whilst the lattershows a strong positive association with this axis. Duffthickness (P � 0.001) and branch inclination (P � 0.01)are more closely associated with Axis 2, but in opposingdirections. Position on the branch is important but not assigni®cant as the other variables (P � 0.05), and holds acentral position when displayed in relation to the ®rst twoaxes of the ordination (Fig. 2a).

Table 2 Number of epiphytic vascular and non-vascular species recorded on the three trees sampled: Dacrycarpus dacrydioides riverside(D-d R); D. dacrydioides forest interior (D-d I); and Nothofagus menziezii (N-m) in New Zealand temperate rainforest. The number of speciesoccurring on all three trees, two trees and one tree only, are also indicated, as well as Sùrenson's Community Coef®cients (Sùrenson, 1948) forthe between-tree comparisons

No. species present (tree) Sùrenson's community coef®cient

D-d R D-d I N-m 3 2 1 D-d R : D-d I D-d R : N-m D-d I : N-m

Vascular 49 37 41 24 19 19 72 73 67Non-vascular 52 53 57 23 22 48 64 50 54

Total 101 90 98 47 41 67 67 61 59



Figure 1 Summary of the two-way table resulting from the TWINSPANTWINSPAN classi®cation of the cover-abundance data from the 359 samplesanalysed from the three host trees. Dendrograms of the associations between the ®fteen communities (quadrat groups) and fourteen speciesclasses (with number of taxa plus categories, e.g. roots) in each class are displayed, together with the indicator species (for the communitydendrogram) and eigenvalues for each division. Values in italics correspond to percentage presence in each cell (i.e. 100% implies all species inthis species class occur in all samples in this quadrat group). Upper values in each cell give the percentage of the total possible cover for thatcombination of quadrat group and species class.



The environmental variables for the D-d R host (Fig. 2b)display similar relationships to that of the D-d I tree. Heightand location on the tree are both signi®cantly (P � 0.001)negatively related to Axis 1 with diameter of the branch/trunk (P � 0.001) having an opposing relationship. Positionon the branch on this host is more highly signi®cant(P � 0.01) and more clearly associated with Axis 1 (vectorlength 0.806) than for the D-d I tree. With this tree,however, although still highly signi®cant (P � 0.001), theinclination of branch and duff thickness are both alignednegatively with Axis 2. However, inclination, at vectorlength ±0.351 on Axis 2, is more clearly related with Axis 3of the ordination (diagram not shown: vector length ±0.928).

For the N-m host, again location on the tree and height aresigni®cantly (P � 0.001) negatively associated with Axis 1and diameter (P � 0.001) positively associated (Fig. 2c).Only on this tree does aspect of the branch assumesigni®cance, because position on the branch assumes agreater relationship with Axis 2 (vector length 0.964;P � 0.01) than for the two D. dacrydioides hosts. Diameter,inclination and duff thickness at P � 0.001, are highlysigni®cant, with the two former variables being closelyrelated to Axis 1 of the ordination (Fig. 2c).

Figure 3 displays the ordination of all the samples for thethree hosts according to the ®fteen recognized communitygroups (Q.G. I±XV). When ®tted against all the samplescores together, six of the seven measured environmentalvariables are signi®cant at P � 0.001. The spread of samplesin relation to Axis 1 is clearly being driven by height andlocation on the hosts. These two parameters have anopposite relationship to the four remaining variables, diam-eter and inclination of branches, position on the branch, andduff thickness. Overall, Axis 1 generally re¯ects a complexof environmental variables which produce a gradient fromthe trunk and highly vegetated inner branches, and thoseindicative of the less well covered middle to outer branches.Communities I and II are the most clearly separated, with theother thirteen communities displaying a certain degree ofoverlap in relation to both axes. Essentially, the lower theinclination of the branch and the larger its diameter,the greater is the duff thickness, and the more signi®cant isthe position on the branch. Conversely, with increasingheight on the host, the location towards the middle to outerbranches, and the steeper the inclination, the smaller is thediameter, the less signi®cant is the position on the branch,and the lesser is the duff thickness.

Biomass

On the D-d R tree we found an average of 350 � 125 g dryweight dm±2 of material attached to the trunkbase, and206 � 21 g dm±2 on the inner and middle branches. Ourbulk density values show considerable consistency withrelatively small standard errors, thus implying that theinformation on biomass, expressed per unit area (g dm±2), isprimarily a function of duff thickness (Table 4). The latteraveraged 33 � 13 cm on the trunkbase and 24 � 3 cm onthe inner and middle branches. By contrast, epiphytic

Figure 2 Ordination and vector diagrams for the statisticallysigni®cant (*P � 0.05; **P � 0.01; ***P � 0.001) environmentalvariables ®tted to the individual host sample scores resulting fromthe collective ordination. Communities recognized followingTWINSPANTWINSPAN classi®cation occurring on each of the three trees areshown. (a) Dacrycarpus dacrydioides forest interior (D-d I); (b) D.dacrydioides riverside (D-d R); (c) Nothofagus menziesii (N-m).



material was negligible on the outer branches and branchextremes except occasional `moss balls' up to 15 cm thick.

DISCUSSION

Biodiversity and community patterns

The twenty-eight vascular species on a single host recordedby Dickinson et al. (1993) has been eclipsed by the currentstudy with forty-nine vascular species recorded on the D-d Rtree. Furthermore, this number exceeds the thirty-six speciesfound on an Agathis australis (kauri) tree in northern NewZealand by Harrison-Smith (1938). Our ®gure is of the sameorder as the forty-®ve recorded from 0 to 20 m on anemergent Prumnopitys exigua in Bolivian cloud forest(S.R.P. Halloy, K.J.M. Dickinson and I. Vargas, unpublisheddata) but is however, exceeded by the sixty-®ve vascular taxarecorded on a single tree both in Costa Rica by Ingram &Nadkarni (1993) and in French Guyana by Freiberg (1996).

Trees in Nothofagus-dominated forests in New Zealandare not generally associated with a proli®c development of

epiphytes. Of the species that are present here, non-vascularepiphytes tend to predominate. It could be hypothesized thatthe bark of Nothofagus is chemically and/or physicallyunsuitable for the accumulation of vascular epiphytes inparticular. Our study, however, discounts this hypothesis,favouring climatic conditions and perhaps time as theunderlying explanation. Indeed, Scott & Rowley (1975)could ®nd no evidence for the restriction of bryophytes tothe trunks of particular host species, in their study of a rangeof hosts, including Nothofagus menziesii and Dacrycarpusdacrydioides, in a mixed N. menziesii-podocarp forest insouth-westland. The individual N. menziesii tree in ourstudy is characteristic of numerous old-growth trees in thismixed forest stand, all growing in climatic conditions highlyconducive to epiphyte establishment and build-up. Thisshorter host tree (22 m) was equally laden and not readilydistinguished in terms of diversity or abundance, fromnearby hosts of a mature podocarp, in this caseD. dacrydioides, a species more usually associated withlarge and diverse epiphyte loads. N. menziesii appears to be

Figure 3 Two-dimensional ordination of the 359 samples based on detrended correspondence analysis of the cover-abundance data. Samplesare coded according to the ®fteen TWINSPANTWINSPAN communities (I±XV). Envelopes essentially prescribe the limits of the distribution of thecommunities differentiated at level two of the TWINSPANTWINSPAN classi®cation (Fig. 1).



the most long-lived (reaching 500±600 years), and shadetolerant of the four Nothofagus species in New Zealandaccording to Ogden (1988). The conifers in New Zealandare generally slower growing and achieve greater ®nal sizesand longevities than the associated angiosperms (Ogden &Stewart, 1995). Figures quoted in Ogden and Stewart (seeTable 5.2; 1995) indicate that New Zealand conifers havemean longevities ranging from 51% to 87% (mean differ-ence 190±457 years) greater than angiosperms.

In our study the ®rst division of the classi®cation analysislargely differentiates seven communities associated with themiddle to outer crown on the basis of the host tree. Bycontrast, the particular eight communities associated withthe lower and inner portions of the trees' trunk and innerbranch systems are not as clearly split on the basis of host(Fig. 1; Table 3). These results imply that the epiphyticcommunities in the canopies are more distinct between thetrees even within a single species, than those found on theinner branches and trunk, which have greater similarityamong the three trees. The outer branches have little or noduff and in these circumstances epiphytes have more directcontact with the host. In contrast, duff often forms ablanket in the interior of the tree and in effect becomes ahomogenizing substrate where any host species effects arelikely to be masked. Dickinson et al. (1993) showed thatzonation of lianoid-epiphytic communities can only bejusti®ed for the outer portions of the canopy with the morecentral portions portraying complex community patterns.This situation is mirrored in the present study for all threehosts. By contrast, Wolf (1994) found host-tree speci®ccommunities on the inner branches and non-speci®c com-munities on the branch extremes. This pattern may beattributable to the unifying effect of persistent fog at histropical study site.

Hietz & Hietz-Seifert (1995b) found that a highlyspecialized group of epiphytes is restricted to the stem base,and they presumed this to be because of requirements forhigh atmospheric humidity. They included species ofHymenophyllaceae in this group, which they maintained,for their study at least, are essentially incapable of regulatingwater through lack of stomatal control. Eight species ofHymenophyllum were present in our study but these werenot con®ned to the trunk base although they were generallyabsent from the outer branches.

Our present results further emphasize the importance ofsampling complete trees (McCune, 1990; Clement & Shaw,1999), rather than assuming that trunk-based epiphytesre¯ect the total epiphytic diversity. Moreover, our analysesalso indicate the importance of including both vascular andnon-vascular taxa in the differentiation of epiphytic com-munities. We found ninety-four non-vascular taxa on thethree host trees and if we had relied on the sixty-one vasculartaxa alone, the community patterns would have beenincomplete (cf. Pharo et al., 1999) and the Sùrensen simi-larity indices would be notably higher. Undoubtedly, thenon-vascular taxa contribute substantially to epiphyticbiodiversity (and productivity) in rain forests. However, apertinent issue is the extent to which the vascular ¯ora alonecan reveal epiphytic community patterns and the contribu-tion of non-vascular epiphytic taxa to such patterns. In orderto test this issue, separate classi®cations were derived for thevascular taxa alone and for the combined data. Interpret-ation of these analyses to an equivalent ®fteen-group level tothat derived for the entire epiphytic data set, revealed thathalf of the samples were grouped differently at level three ofthe classi®cation. Moreover, 30 of the 359 samples (8.7%)changed their association at the ®rst division that, with thefull analysis, had essentially separated the interior and

Table 3 Mean values for seven coded environmental variables in the ®fteen epiphytic communities (quadrat groups) differentiated in theTWINSPANTWINSPAN classi®cation of the samples from the three hosts combined. Codes for location in tree: Trunkfoot � 1, Main trunk � 2, Innerbranch � 3, Middle branch � 4, Outer branch � 5, Branch extremes � 6. Codes for aspect of branch in tree: N � 3, E and W � 2, S � 1. Codesfor position on branch: Topside � 3, Side � 2, Underside � 1

Quadratgroup

No. ofsamples

Locationin tree

Height(m)

Branchaspect

Positionon branch

Inclination(degrees)

Diameter(cm)

Duffthickness (cm)

I 6 1.2 1.3 2.2 2.0 80.3 133.3 21.7II 10 1.4 1.3 2.1 2.0 59.7 166.0 6.1III 8 2.5 20.1 2.0 1.9 80.6 90.6 7.5IV 14 2.4 12.0 1.9 2.0 67.5 114.5 2.1V 42 3.0 10.8 2.0 2.0 69.6 57.2 6.9VI 43 3.6 14.3 2.1 2.1 53.1 37.6 18.9VII 50 3.1 13.0 2.0 2.0 62.3 63.6 12.6VIII 29 4.0 17.8 1.8 2.0 83.5 27.8 10.4IX 16 3.9 22.5 2.2 2.1 60.3 20.6 12.4X 28 4.3 23.2 2.0 2.0 39.5 15.3 2.9XI 42 4.5 27.2 2.0 2.1 60.7 14.9 2.0XII 22 3.5 26.2 1.9 2.1 54.5 31.2 5.5XIII 18 4.1 13.4 2.0 1.8 59.4 29.4 2.6XIV 21 3.7 15.7 2.1 2.0 54.0 25.0 1.4XV 10 5.2 15.5 2.0 1.9 22.2 12.7 4.8



trunkfoot samples from those associated with the middle andouter branches. Of these thirty samples, twenty-six actuallytransferred from the peripheral (Q.G. IX±XV) to the interior(Q.G. I±VIII) communities. Inclusion of non-vascular abun-dance data was therefore in¯uential to the communitydifferentiation.

Given the added dif®culty of including detailed sampling ofnon-vascular epiphytes, particularly in rain forests, general-ized categories as used by Dickinson et al. (1993) or functionalgroups (sensu McCune, 1993) are preferable to their totalexclusion. McCune (1993) proposed the use of four epiphytefunctional groups to aid the interpretation of epiphytedistribution in Pseudotsuga menziesii coniferous northerntemperate rain forest by dividing macro-epiphytes (non-crustose forms) into: cyanolichens, alectorioid lichens, `otherlichens' (mainly green-algal foliose lichens) and bryophytes.

Non-vascular species, particularly lichens, tended topredominate in the crown of the trees we studied. The treestructural variables of height, crown length, trunk, limb andfoliage regions, as well as the abundance and distribution ofsmall, medium and large limbs, can play an important role inthe abundance and vertical occurrence of non-vascularepiphytic functional groups as in old-growth Pseudotsugamenziesii trees in rain forest in the Paci®c Northwest ofNorth America (Clement & Shaw, 1999). Furthermore, theymaintained that the tall, structurally diverse, old-growthtrees with well-distributed large limbs and long crowns hadenhanced biodiversity. This conclusion is consistent with our®ndings, particularly as humid forests also may display ®nerniche partitioning and a higher diversity because of a moreconstant environment that, according to Gentry & Dodson(1987) when addressing vascular species, may favour within-community microhabitat specialization by epiphytes.

Rain forests offer a favourable environment for epiphyticlichens but these organisms are constrained by the interplaybetween light levels, humidity, liquid water and desiccation(Lange et al., 1993) which affect the particular lichens thatcan persist and in what abundance. Surplus water has beenshown to reduce lichen photosynthetic productivity (Langeet al., 1986, 1993), and in rain forests, high lichen cover isoften concentrated in relatively drier microhabitats such as inthe upper canopy (Wolf, 1993a, b, 1994), as in the presentstudy. Lichens can colonize these extreme sites because oftheir ability to photosynthesize at low water potentials, and totake advantage of minimal water and, in the case of greenalgal lichens, high relative humidity. It appears that lichens,particularly those containing green algae as the photobiont,can occupy habitats that are unfavourable to either vascularspecies or bryophytes. In a study in a mixed Nothofagus-podocarp temperate rain forest in North Island, NewZealand, Green et al. (1993) found that the green algalcomponent of the lichens studied, had a large photosyntheticadvantage when thallus water contents were low and thethalli were in equilibrium with atmospheric humidity. Thecyanobacterial component performed better under the verywet conditions common in these forests. The distribution oflichens generally re¯ects preferences for microsites withoutlengthy suprasaturation (Lange et al., 1993). Of the lichens

recorded in our study, the majority have green algal or bothgreen algal and cynanobacterial components, with seeminglyonly one which is purely cynanobacterial (Pseudocyphelleriacinnamonea), according to Galloway (1985). Cyanolichenscan ®x nitrogen and are indicators of `long ecologicalcontinuity' (Clement & Shaw, 1999). They are also negativelyaffected by high light exposure (Gauslaa & Solhaug, 1996).However, we recorded P. cinnamonea only on the D-d R tree,and predominantly in Communities X and VIII (Table 1) onmiddle to outer branches. This would seem a patterninconsistent with what we might have predicted as the morefavoured habitat for this species in this functional group.

Ecophysiological studies of corticolous non-vascular cryp-togams have shown the importance of radiation intensityand moisture availability to their vertical distribution in trees(Hokosawa et al., 1964). In the wettest habitats, bryophytespredominate, apparently because they are better able to copewith a surfeit of liquid water whilst maintaining a reasonablelevel of photosynthesis (Green & Lange, 1993 cited in Langeet al., 1993). In their study of old-growth Pseudotsugamenziesii trees, Clement & Shaw (1999) found that mossesand liverworts were very sparse in the upper canopy andabundant in the lower canopy but that they were noticeablyabundant on larger limbs regardless of height. The distribu-tion of canopy cryptogams is in¯uenced by both microcli-mate and succession, and the vertical zonation of species willre¯ect gradients in both microclimate and distribution ofbranch size (bark age) (Pentecost, 1998). In our analysis, thependant mosses Weymouthia cochlearifolia, W. mollis andPapillaria ¯avo-limbata were indicator species associatedwith the communities of the outer branches (Q.G. IX±XV).The mosses in this family (Meteoriaceae) are usuallyepiphytes, characteristically forming veils hanging frombranches and twigs in wet forest (Beever et al., 1992).Further indication is provided by large thick `moss balls' thatinclude Cladomnion ericoides (Ptychomniaceae), on thelarger inner to outer branches.

Biomass

Neotropical montane cloud forests are considered to supporta higher biomass of epiphytes than any other forest type(Gentry & Dodson, 1987; Benzing, 1998). Our study of amixed Nothofagus-podocarp temperate rainforest challengesthis convention. High elevation tropical forests have beenshown to support up to 44 kg ha±1 of suspended organicmatter (only a small proportion of which was living;Hofstede et al., 1993). The organic matter can reach athickness of 30 cm on the upper sides of branches (Nadkarni& Matelson, 1991). We found duff (humus) buildup inexcess of 50 cm depth on the topside and the underside ofsome branches (see also Dickinson et al., 1993). Ourbiomass values for epiphytic material at the trunkbase andon inner and middle branches on the D-d R tree (350 and206 g dm±2, respectively), are higher than those reported byHofstede et al. (1993) for a Colombian upper montane rainforest (137.8 and 130.4 g dm±2, respectively), and muchhigher than those found by Nadkarni (1984b) in Costa Rica



(Table 4). The high values found at our site may be are¯ection of the extremely thick cloak of suspended, deadmaterial interwined with liane roots (average 33 � 12.6 and24 � 2.7 cm depth for the trunkbase, and inner and middlebranches, respectively) and a higher bulk density of the dufflayer. The higher density of duff might be explained by thedifference of the dominant duff-forming, and accumulating,growth forms ± ferns and lianes in New Zealand vs.bryophytes in Colombia. However, in our study, somesigni®cant biomass loads were associated with only a fewspecies of bryophytes. In particular, mosses such asCladomnion ericoides locally made a substantial contribu-tion to the epiphytic biomass. Nadkarni et al. (2000) suggestthat as a tree grows and its epiphyte load increases, itsretention of epiphyte fragments, and thereby recruitment,also increases. Given the longevity of the trees in our study,the time for epiphytes to establish and for duff to accumulatemust be a signi®cant factor in explaining these biomassresults (probably >500 years in our case vs. 215 � 15 yearsfor the Weinmannia mariquitae study tree in Colombia:Hofstede et al., 1993).

If our value for biomass per unit surface area of bark isextrapolated to the entire trunkfoot (150 cm long, 230 cmdiameter), we estimate a dry weight of 400 kg of epiphyticmaterial here. This ®gure is much higher than the estima-tions made by Hofstede et al. (1993) and Nadkarni(1984b) for entire trees (115 and 141 kg DW, respectively).As our D. dacrydioides is much taller than either theColombian W. mariquitae and the Costa Rican Clusia alatatrees, we might expect extremely high total biomass valuesfor our entire tree, allowing this temperate rain forest torank with tropical rain forest systems in terms of epiphyticbiomass on a single host.

CONCLUSIONS

Dickinson et al. (1993), in their study of a single coastalDacrycarpus dacrydioides host tree in New Zealand podo-carp-broadleaved lowland temperate rain forest, revealedthe complexity of epiphytic communities and also thesubtleties of microclimatic habitats on this tree. We havecon®rmed their conclusions for three other host trees,

including another species, growing under similar conditionswithin c. 8 km of the previous study area. Comprehensivequantitative epiphyte studies, incorporating a suite ofenvironmental factors in relation to diversity and abun-dance, are globally in their infancy. This is particularly truefor the southern hemisphere temperate rain forests. Hietz &Hietz-Seifert (1995b), in a study in the cloud forests inMexico, reinforce the fact that more than a single one-dimensional gradient is responsible for the distinctiveness ofcanopy microhabitats. Their work, however, did notincorporate a full range of relevant environmental factorsbut did acknowledge that, although tedious, such anapproach was likely to be rewarding. We can but concur.Our study has revealed the high epiphytic-lianoid diversityand biomass of this temperate rain forest, a condition moretypically associated with tropical rain forest areas. Weencourage more comprehensive quantitative studies ofepiphytic communities in relation to the full range ofrelevant environmental factors, including microclimate. Wealso emphasize that features of tropical rain forest epiphyticsystems, notably ¯oristic diversity and biomass, may haveanalogues in the perhumid climates of temperate latitudes,particularly in the southern hemisphere.

ACKNOWLEDGMENTS

We thank Bec Stanley and Liz Radford for help in the ®eld,Barbara Polly, David Glenny and David Galloway foridenti®cation of mosses, liverworts and lichens, respectively,Jennifer Bannister for some advice on lichens, as well asDr Jan Wolf and two anonymous reviewers for helpfulcomments on the manuscript. This study was approved bythe Department of Conservation and substantially funded byan Otago University Research Grant. The visit of RGMH toNew Zealand was funded by the Miss E.L. HellabyIndigenous Grasslands Research Trust.

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Table 4 Epiphytic biomass (live and dead)data from the present study compared withrelevant studies elsewhere

Dry bulkdensity (g dm)3)

Mass per unitarea (g dm)2)

Duffthickness (cm)

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Hofstede et al. (1993) ColombiaTrunkbase 137.8Inner branches 130.4Middle branches 32.4Outer branches 1.5

Nadkarni (1984b) Costa RicaInner branches 22.9



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BIOSKETCHES

Robert Hofstede is the Coordinador General of theProyecto PaÂramo±Proyecto EcoPar programme based inQuito, Ecuador which is af®liated with and supported bythe Institute for Biodiversity and Ecosystem Dynamics atthe University of Amsterdam, the Netherlands. Hisresearch extends from epiphytic communities in Colom-bian rain forest to the ecology and sustainable manage-ment of the high-Andean paÂramo ecosystems.

Katharine Dickinson and Alan Mark are Senior Lecturerand Professor, respectively, at the University of Otago.They have collaborated with Robert in ecologicalresearch in grassland and rain forest ecosystems in NewZealand and Ecuador.



Distribution, Abundance and Biomass of Epiphyte-lianoid Communities

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