Effects of Fragment Size and Habitat Heterogeneity on Cryptogam Diversity in the Low-boreal Forest of Western Canada

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Effects of Fragment Size and Habitat Heterogeneity on Cryptogam Diversity in theLow-boreal Forest of Western CanadaAuthor(s) L Dennis Gignac and Mark R T DaleSource The Bryologist 108(1)50-66 2005Published By The American Bryological and Lichenological Society IncDOI httpdxdoiorg1016390007-2745(2005)108[50EOFSAH]20CO2URL httpwwwbiooneorgdoifull1016390007-2745282005291085B503AEOFSAH5D20CO3B2

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The Bryologist 108(1) pp 50 66Copyright q 2005 by the American Bryological and Lichenological Society Inc

Effects of Fragment Size and Habitat Heterogeneity on Cryptogam Diversity inthe Low-boreal Forest of Western Canada

L DENNIS GIGNAC

Faculte Saint-Jean University of Alberta 8406 91 Street Edmonton Alberta T6C 4G9 Canada e-mail dgignacualbertaca

MARK R T DALE

Department of Biological Sciences University of Alberta Edmonton Alberta T6G 2E9 Canada e-mailmarkdaleualbertaca

Abstract The effects of fragmentation of the sub-humid low-boreal forest in agro environmentson bryophyte and lichen diversity were analyzed on 44 woodlots in three regions of northernAlberta Canada Woodlots were selected to cover a wide variety of shapes and sizes in eacharea Several microclimatic variables which included temperature at three different heights abovethe forest floor relative humidity and the amount of light penetration were measured in five mdiameter circular sample plots along transects that covered the length and the width of eachfragment The number of microhabitats that included living trees with creviced and smooth barkstanding dead different decay classes of downed woody debris soil and rock were tabulated ateach sample plot Bryophyte and lichen presence was noted for all microhabitats found withineach plot There was a trend of decreasing temperature and light intensity and increasing humidityup to 15 m from the edge of the fragments A multiple regression analysis revealed that thedistance from edge and the habitat heterogeneity were the most important variables affectingbryophyte and lichen species richness Further analysis indicated that edge effects were significantfor bryophytes but not for lichens The size and shape of fragments had a significant effect onhabitat heterogeneity and bryophyte and lichen diversity Although there was a distinction be-tween the floras in each region the effects of fragment size and habitat heterogeneity were similarAn indicator species analysis selected several indicators of large medium and small fragmentsthat were also indicators of habitat heterogeneity and species richness The presence or absenceof several indicator species is used to produce performance benchmarks for habitat heterogeneityand species richness The use of indicator species offers an inexpensive and relatively easy methodto evaluate edge effects and habitat heterogeneity on bryophyte and lichen diversity in woodlots

Keywords Agro-environments edge effects forest fragmentation habitat heterogeneity in-dicator species microclimate microhabitat

Forest fragmentation results from the clear cut-ting of large tracts for a variety of purposes includ-ing forestry agriculture andor urban developmentAt its most extreme clear cutting leaves only smallisolated remnants of the native original forestwoodlots hedgerows or stream banks of varyingsize surrounded on all sides by other types of hab-itats Landscape fragmentation caused by defores-tation is one of the main causes of decline in world-wide biological diversity (Wilcox amp Murphy 1985)

The decrease in the area of the remnants of thenative forest increases edge effects Vegetation inthe fragments is more exposed to wind and highersolar radiation that produce drier and warmer grow-ing conditions than in the original forest (Camargoamp Kapos 1995 Chen et al 1995 de Casenave etal 1995 Malcolm 1998 Sillett et al 1995) As a

result shade tolerant vascular plant species alongthe edge are replaced by species that are found inopen areas (Lovejoy et al 1986) Edge effects fur-ther reduce the area within the fragment occupiedby the original forest species As the size of thefragment is reduced it reaches a critical thresholdbelow which all parts of the fragment become edg-es thus eliminating many of the original shade tol-erant species and reducing diversity (With amp Crist1995) Thus although the size of long and narrowfragments may be above the critical threshold di-versity may be adversely affected because all areaswithin the patch are influenced by higher insolationand wind

Effects of forest fragmentation resulting from ag-ricultural land use in North America have beenstudied for many animal taxa particularly birds as

2005] 51GIGNAC amp DALE CRYPTOGAM DIVERSITY

well as forest-dwelling plants including the treesthemselves (Boutin amp Jobin 1998 Burke amp Nol1998 Cunningham 2000 Jobin et al 1997 Ma-tlack 1994 Weaver amp Kelman 1981) Howeveronly a few studies of native plant species in agro-ecosystems have focused on bryophytes and lichens(Merrifield 2000 Zechmeister 2003) Converselyseveral studies have focused on effects of clear cut-ting conifer-dominated forests for forestry purposeson diversity patterns of bryophytes (Frisvoll ampPrestoslash 1997 Gustafsson amp Hallingback 1998McGee amp Kimmerer 2002 Soderstrom 1989) andlichens (Boudreault et al 2000 Coxson amp Marsh2001 Dettki amp Esseen 1998 Kuusinen 1994 1996Lessica et al 1991 McCune et al 2000 Neitlichamp McCune 1997 Rosso amp Rosentreter 1999 Sod-erstrom 1988)

Clear cutting in agro-environments differs fromthat in forestry because 1) it produces relativelypermanent boundaries that are likely to last for cen-turies over extensive areas of the landscape 2) itproduces an extremely high density of roads thatfurther fragment the remaining forest creating aneven patchier landscape with a great deal of forest-edge habitat and 3) agricultural development islargely unregulated and there are no clear manage-ment strategies to conserve diversity (Hobson et al2002) Thus studies of bryophyte and lichen di-versity in forestry environments do not necessarilyapply to agro-environments

As a result of the lack of focus on fragments inagricultural ecosystems effects on bryophyte andlichen diversity are not clear For example Honnayet al (1999) found that fragment size was a redun-dant variable in explaining plant diversity in forestpatches in Belgium They attributed changes in spe-cies richness within fragments to habitat diversityConversely Sillett et al (1995) found that epiphiticbryophyte species richness decreased on isolatedtrees when compared to trees within the intact for-est Grashof-Bokdam (1997) also found that plantspecies diversity increased with increasing frag-ment size and that shade tolerant species disap-peared in smaller forest fragments in the Nether-lands

Apart from fragmentation and edge effects sev-eral studies have demonstrated that bryophyte andlichen diversity in forest environments are affectedby habitat heterogeneity at different scales At thelandscape or regional level the number of availablemesohabitats (physiographic and physiognomicforms) (Vitt amp Belland 1997 Vitt et al 1995) playsan important role in determining the species rich-ness and abundance At the local level within a for-est or forest fragment the presence of such sub-strate habitats as rocks and mineral soil (Coxson ampMarsh 2001 Fenton et al 2003 Pharo amp Vitt 2000

Ross-Davis amp Frego 2002) living and dead stand-ing trees (Kuusinen 1994 1996 McCune et al2000 McGee amp Kimmerer 2002 Ruchty et al2001 Sheard amp Jonescu 1974) and downed woodymaterial (McAlister 1995) will also affect diversityAt the microhabitat scale such factors as thesmoothness of the bark (Hazell et al 1998) or de-composition classes of downed woody material(Crites amp Dale 1998 Kruys et al 1999 Soderstrom1988 1989) affect the diversity of both taxa Thusa study of forest fragmentation in agro-environ-ments must also attempt to separate effects ofwoodlot size and shape from those produced byvariations in habitat heterogeneity

In many areas of the Prairie Provinces of Canadathe sub-humid low-boreal forest has been clearcutto allow agriculture Peak deforestation occurredapproximately 90 years ago (Ramankutty amp Foley1999) but deforestation is ongoing with estimatedlosses between 121 and 176 per year (Fitzsim-mons 2002 Hobson et al 2002) In the southernportions there is little forest left leaving a patch-work of woodlots and fragments of varying sizeson the landscape Although the northern portionsare more heavily forested they have recently ex-perienced some of the highest rates of deforestationpresently found in the world (Hobson et al 2002)

The purpose of this study is to determine the im-portance of the size and shape of forest fragmentson lichen and bryophyte diversity in the remnantsof the sub-humid low-boreal forest compared tohabitat heterogeneity Habitat heterogeneity is ad-dressed at different spatial scales microhabitatssubstrate habitats within a patch a patch or frag-ment a landscape formed by a group of patchesand different groups of patches from different land-scapes defining a regional scale Because edge ef-fects will be more prominent in smaller than inlarger patches the importance of fragmentation canonly be determined by comparing the size of thefragments with the number of microhabitats foundin them The results will separate effects of frag-mentation from the number of microhabitats andthat a critical threshold can be established for thedifferent taxa If taxa differ in their requirementsfor successful establishment survival and repro-duction then the number of taxa present in a givenarea will be determined more by microhabitat di-versity than by the size of the fragment Howeverincreasing the geographical area sampled generallyincreases the number of microhabitats consequent-ly area should have a positive influence on taxadiversity This information can also be used to iden-tify species that are indicative of fragment sizehigh species diversity and high habitat heteroge-neity

52 [VOL 108THE BRYOLOGIST

FIGURE 1 Locations of the 44 fragments in three regions of northern Alberta Shaded areas indicate the extent ofthe sub-humid low-boreal forest in western Canada Dots indicate study sites in the Athabasca area triangles sites inthe Peace River area and asterisks sites in the Manning area

METHODS

Study area The sub-humid low-boreal forest forms aband between the mid-boreal forest and the transitionalgrassland of continental western Canada (EcoregionsWorking Group 1989) (Fig 1) This band extends diago-nally in a southeast to northwest direction from Manitobato British Columbia east of the Rocky Mountains Theupland vegetation on most sites within that forest is dom-inated by deciduous trees rather than by coniferous spe-cies particularly in the southern portions of the forest(Rowe 1972)

Forty-four upland aspen-dominated fragments werestudied in three different regions within the sub-humidlow-boreal forest of northern Alberta (Fig 1) 18 between54 and 558 N latitude and between 112 and 1148 W lon-gitude (Athabasca area) 15 between 55 and 568 N latitudeand 116 and 1178 W longitude (Peace River area) and 11between 56 and 578 N latitude and 117 and 1188 W lon-gitude (Manning area) The forest in the Athabasca andPeace River areas was cleared approximately 90 to 100years ago while the Manning area was deforested ap-proximately 60 years ago

The mean annual precipitation in the study area variesbetween 446 mm in the south at Athabasca and 517 mmin the north at Manning and annual mean temperature be-tween 11 in the north and 148C in the south (Environ-ment Canada 1980) Elevations range between 530 and580 m above sea level The soil parent material is sedi-mentary rock and the soils are generally clay loam Theterrain is more undulating in the Athabasca area becauseof glacial moraines while the areas surrounding PeaceRiver and Manning are relatively flat The natural over-story vegetation in upland areas in the three regions isdominated by Populus tremuloides Michx but other treespecies such as Picea glauca (Moench) Voss and Populusbalsamifera L also reach moderate abundances Theshrub layer typically consists of Rosa acicularis LindlAlnus crispa (Ait) Pursh Lonicera involucrate (Richards)Banks and Ribes oxyacanthroides L (Ecoregions Work-ing Group 1989)

Site selection The woodlots that were selected rangedin size from individual trees to small (between 0002 andone hectares) to large (covering up to 17 hectares) Par-ticular care was used to select stands of different shapesfrom circular to linear rectangular to square as well ascomplex for each of the different size classes in eachgeographic region Fragments that were extensivelygrazed by livestock were omitted since intense grazingcan seriously affect the environmental conditions within astand by opening up the understory either by grazing orby paths through the fragment Also since bryophyte andlichen diversity is dependant on the age of the stand (Cri-tes amp Dale 1998) and maximum diversity occurs in maturestands only older fragments (approx 70 years) wereanalyzed in this study Old fragments were identified bythe height of the canopy (20 m) and by the diameter ofthe boles (Diameter at Breast Height 25 cm) Selectionwas also based in part on ease of access and the absenceof non-agricultural human disturbances as gas and oilwells and pipelines

Data collection Within each fragment that containedmore than two trees a minimum of two line transects werelocated as follows one transect running along the length(the longest axis from the trunks of the trees on the edges)and the other the width (the longest axis at right anglesto the length) For bigger woodlots or those with irregularshapes two additional transects running parallel to thewidth transect were also sampled The distance betweeneach parallel transect depended on the size of the frag-ment but were equidistant to the longest axis at right an-gles to the length and never placed within five m of ad-jacent transects We gathered data quantifying the perim-eter and shape of the fragment by walking around the edgeand marking points with a Garmin Model 12 Global Po-sitioning System (GPS) unit that had a typical positionalerror of five m The perimeter and area of each fragmentwere calculated from the GPS points using a GeographicInformation System (Arcview) Physical dimensions ofeach fragment were expressed as perimeter area and ashape index (Forman amp Godron 1986) The shape index


(D) was calculated as D 5 P2(PS)12 where P is the siteperimeter and S is the site area All distance area andshape index values were natural log transformed to im-prove the normality of the distribution

The vegetation was sampled at five m intervals alongeach transect using a five m diameter circular sample plotThe presence of bryophytes and lichens was noted foreach microhabitat found within each plot All microhabi-tats within each quadrat were counted and catalogued andthe presence of each species was noted for each micro-habitat Microhabitat classes for downed woody materialwere defined as 1) log whole and undecayed bark intact2) log sound wood hard with 50 of bark remaining 3)wood soft in places with 50 of bark remaining 4) woodsoft with crevices little or no bark remaining 5) largewood fragments lost outline of trunk slightly deformed6) wood mostly well decayed 7) humification nearly100 (Soderstrom 1988) Microhabitat classes for theground were 1) leaf litter and humus 2) moose or deerdung 3) exposed mineral soil and 4) rocks Exposed min-eral soil in the fragments was only encountered wheretrees had overturned exposing roots and the soil belowthem and as a result formed discrete units Microhabitatsfor epiphytic species were defined by the tree species oras standing dead as well as the presence of smooth orcreviced bark up to a height of two m above the groundMicrohabitats present at each sample plot were also notedregardless of whether mosses or lichens were growing onthem Each fragment was also carefully searched for ad-ditional species and microhabitats that were not previouslyrecorded in the quadrat sampling and if a new species wasfound its microhabitat was recorded Nomenclature most-ly follows Crosby et al (1999) for mosses Paton (1999)for liverworts and Brodo et al (2001) for lichens

The following microclimatic measurements were takenat the center of each plot as well as outside the fragmentsimultaneously relative humidity measured with a Bach-arach sling psychrometer at one m above the soil irradi-ation measured with a VWR Traceable photometer at onem above the soil and air temperatures measured withthermistors at three heights (at the level of the soil and 1m and 2 m above the soil) Measurements outside thefragments were taken in adjacent fields along the sameline as each transect a minimum of 20 m from the firsttree encountered in the fragment All microclimatic valueswere expressed as the difference between measurementsoutside the fragment and at each plot Microclimatic mea-surements were taken once per quadrat during the summermonths of 2000 for Athabasca of 2001 for Peace Riverand of 2002 for Manning in full sunshine between 1000and 1400 hours and at least two or more days after rainbecause moisture levels are strongly affected by precipi-tation (Camargo amp Kapos 1995) Measurements wereplotted as means 6 one standard deviation against thedistance from the fragment edge and exponential curveswere fit to the means The curves were fit in order todetermine the distance from the margin that the edge af-fected each microclimatic variable

Data analyses Microhabitat heterogeneity was quan-tified using Simpsonrsquos heterogeneity index (D 5 Spi

2where pi is the ith habitat class in the plot or fragment) andsubtracting it from one (Magurran 1988) This index takesthe number and evenness of distribution of microhabitatsinto account and has highest value when there are manyclasses and all substrate habitats and microhabitat classesare found in equal proportions Stepwise forward selectedmultiple linear regressions were used to examine the re-lationship between species richness and microclimatic var-iables distance from the margin and habitat heterogeneity

at the sample plot level as well as species richness andthe size and shape and habitat heterogeneity at the frag-ment level

Microclimatic measurements were log transformed toimprove normality Habitat heterogeneity was measuredas the total number of different microhabitats found in afragment regardless of the size of the microhabitat Todetermine if there is a critical area or shape threshold thataffects species diversity a second order polynomial wasincluded in the regressions and tested for significance

Canonical Correspondence Analysis (CCA) was used todetermine the relative effects of increased fragmentationregional differences and habitat heterogeneity on bryo-phyte and lichen species distribution at the fragment levelThe relative abundance of each species in each fragmentas measured by the number of sample plots on which aspecies was found divided by the total number of plotssampled in the fragment was ordinated using such dis-turbance metrics as fragment area fragment perimeterarea ratio and shape index Regional differences were ex-plored by assigning a region variable with value of 1 forall fragments found in the Athabasca area two for allfragments in the Peace River area and three for those inthe Manning area We used the Indicator Species Analysis(ISA) function in PC-ORD (McCune amp Mefford 1997) toidentify species indicative of fragment size ISA calculatesthe indicator value (iv 5 of perfect indication) for eachspecies in each pre-defined group by multiplying the spe-ciesrsquo proportional abundance by its proportional frequencyfor that group (Dufrene amp Legendre 1997) Fragmentswere classified into three groups depending on the loga-rithm of their shape index small fragments five inter-mediate fragments between five and ten large fragmentsten Only species having ISA values $64 in one ormore of the three shape classes were retained as indica-tors

RESULTS

Environmental variables Graphic representa-tions of the relationship between microclimatic var-iables that were measured as differences betweenvalues inside and outside each fragment showedwide variations at each distance from the edgewhenever there were several measurements taken(Fig 2) These graphs indicated a trend of dimin-ishing mean temperature and mean light intensityand increasing mean humidity with increasing dis-tance from the margin The exponential curves fitto the means were all significant (p 0001) andindicated that mean air temperature at ground leveland one m above the surface as well as light inten-sity stabilized at between 12 and 15 m from themargin The relative humidity stabilized at approx-imately 30 m from the margin Differences betweeninside and outside air temperatures at two m abovethe soil (not shown) also decreased with distanceand equilibrated at approximately 12 m from theedge Air temperatures at ground level indicateddifferences of up to 158C between temperatures in-side and outside the fragment while those at one mand two m above the soil were smaller 78C and68C respectively

The three temperature variables were significant-


FIGURE 2 Relationship between air temperature atground level air temperature one m above the soil surfacerelative humidity and light intensity and the distance fromthe edge of the fragment Microclimatic measurements aremeans 6 1 standard deviation and were calculated as dif-ferences between values inside and outside the fragmentthat were taken simultaneously

ly correlated with each other (Table 1) Light inten-sity was significantly positively correlated withtemperatures at ground level and one m above thesurface while relative humidity was not signifi-cantly correlated with any of the variables Thetemperature at ground level was significantly neg-atively correlated with distance from the edge andthe number of different microhabitats was positive-ly related to the distance

There were 27 microhabitat classes identified inthis study Some classes such as dung and rocks

were relatively rare whereas others such as aspentrees with creviced bark were common to almostall sample plots Values for Simpsonrsquos heterogene-ity index at the plot level ranged between zero and093 Among the 520 plots 28 had values greaterthan 090 67 had values between 080 and 090and only 5 had values less than 080

Fragment area varied between 25 and 172800m2 perimeter between 74 and 2280 m and the logshape index between 291 and 1693 Fragment pe-rimeter area and shape index were highly signifi-cantly correlated with each other (p 00001)Habitat heterogeneity values at the fragment levelranged between zero to 094 and 62 of the frag-ments had values greater than 09 29 had valuesbetween 08 and 09 and the remaining 9 hadvalues less than 08 There was a significant posi-tive linear relationship (p 0001) between thenumber of different microhabitats found in eachfragment and the shape of the fragments (Fig 3)

Bryophyte and lichen diversity We identified74 bryophytes (Table 2) and 57 lichens (Table 3)in this study Several species such as Amblystegiumserpens Brachythecium campestre Pylaisiellapolyantha Caloplaca holocarpa Candelariella vi-tellina Parmelia sulcata Physcia adscendens andP aipolia were found on a large proportion of sam-ple plots in all three regions Eleven mosses fourliverworts and eight lichens were found on onlyone plot The abundance of several species includ-ing Brachythecium velutinum Drepanocladusaduncus Caloplaca cerina C holocarpa Candel-lariella vitellina Peltigera canina Physcia adscen-dens and Ramalina dilacerata increased from themore southerly area at Athabasca to the more north-erly area at Manning Conversely the abundance ofHaplocladium microphyllum Biatora vernalis Hy-pogymnia physodes Parmelia sulcata and Xan-thoria polycarpa decreased from Manning to Ath-abasca

The multiple regression analysis of species rich-ness at the sample plot level and distance from theedge microclimatic variables as well as the numberof different microhabitats (Table 4) revealed thatdistance from the edge and the number of differentmicrohabitats were consistently the most importantvariables affecting the diversity of bryophytes andlichens in each region Distance from the marginwas the most important variable affecting bryo-phyte species richness for two of the three regionswhereas the number of microhabitats was the mostimportant for the third region and when all plotswere pooled The number of microhabitats wasconsistently the most important variable affectinglichen richness although the relationship is not sig-nificant for two of the three areas Slopes for theregressions of both the number of different micro-


TABLE 1 Correlation matrix between distance from the edge the number of different microhabitats (Habitats) airtemperatures at ground level (temp 0m) and at one m (temp 1m) and two m (temp 2m) above the soil surface relativehumidity and light intensity measured on 520 sample plots in 44 woodlots in northern Alberta 5 p 005 5 p 001 5 p 0001

Temp (0m) Temp (1m) Temp (2m) Humidity Distance Habitats

Temp (0m)Temp (1m) 0536Temp (2m) 0379 0524Humidity 20045 0023 0042Distance 20215 20155 0024 0067Microhabitats 0089 0014 0069 20070 0233Light 0249 0219 0137 0111 20101 20109

FIGURE 3 Relationship between the number of different microhabitats and the shape of 44 fragments of the sub-humid low-boreal forest in northern Alberta

habitats and distance from the margin and speciesrichness were all positive

There were significant linear relationships (p 005) between species richness for bryophytes andlichens and the shape of the fragments in all areas(Fig 4) R2 values ranged between 068 for lichensand mosses to 071 for all species Significant linearrelationships also existed between species richnessand fragment shape when fragments were analyzedby region (Table 5) R2 values for those relation-ships ranged between 070 for bryophytes in theAthabasca area and 095 for mosses in the Manningarea Relationships were not greatly improved by

the addition of a second-order polynomial (Table5)

The CCA analysis of the relative abundance ofspecies in each fragment revealed that all environ-mental variables with the exception of habitat het-erogeneity were significantly correlated (p 5 005)with axis one (eigenvalue 5 053) The regionalgradient had the highest correlation with axis onewhile habitat heterogeneity had the highest corre-lation among all variables with axis two (eigenval-ue 5 026) The ordination revealed that fragmentswere separated along the regional gradient with themore southerly sites in the Athabasca area on the


TABLE 2 Percent abundance of bryophytes in fragments from three different areas of the sub-humid low-borealforest in north central Alberta Abundance was measured as the number of sample plots on which a species wasencountered divided by the total number of plots analyzed in the area

Taxon Athabasca Peace River Manning

Amblystegium serpens (Hedw) Schimp 749 888 849Aulacomnium palustre (Hedw) Schwagr 08 224 66Barbula convoluta Hedw 04 00 00Brachythecium acuminatum (Hedw) Austin 00 00 38Brachythecium campestre (Mull Hal) Schimp 510 615 500Brachythecium digastrum Mull Hal amp Kindb 00 06 09Brachythecium reflexum (Starke) Schimp 04 19 00Brachythecium rivulare Schimp 00 12 00Brachythecium salebrosum (Web amp Mohr) Schimp 335 466 217Brachythecium sp 00 12 00Brachythecium starkii (Brid) Schimp 116 441 236Brachythecium velutinum (Hedw) Schimp 08 180 340Bryoerythrophyllum recurvirostre (Hedw) P C Chen 00 93 09Bryum argenteum Hedw 04 00 09Bryum caespiticium Hedw 48 379 358Bryum pseudotriquetrum (Hedw) P Gaertn B Mey amp Scherb 00 230 38Campylium chrysophyllum (Brid) Lange 247 242 57Campylium hispidulum (Brid) Mitt 143 155 75Campylium polygamum (Schimp) C E O Jens 00 06 00Campylium radicale (P Beauv) Grout 12 00 00Campylium stellatum (Hedw) C E O Jens 00 19 00Cephalozia lunulifolia (Dumort) Dumort 00 12 00Ceratodon purpureus (Hedw) Brid 151 354 330Climacium dendroides (Hedw) F Web amp D Mohr 00 06 00Cratoneuron filicinum (Hedw) Spruce 04 00 00Dicranum flagellare Hedw 04 25 00Dicranum fragilifolium Lindb 00 19 00Dicranum fuscescens Turner 04 56 19Dicranum polysetum Sw 04 06 09Dicranum scoparium Hedw 08 50 09Drepanocladus aduncus (Hedw) Warnst 00 106 189Encalypta ciliata Hedw 00 00 09Eurhynchium pulchellum (Hedw) Jenn 223 472 132Haplocladium microphyllum (Hedw) Broth 522 267 104Helodium blandowii (F Web amp D Mohr) Warnst 08 06 00Hylocomium splendens (Hedw) Schimp 28 217 208Hypnum pratense Spruce 08 12 19Isopterygiopsis pulchella (Hedw) Z Iwats 04 00 00Jamesoniella autumnalis (DC) Steph 08 37 09Leptobryum pyriforme (Hedw) Wilson 20 31 00Leskea polycarpa Hedw 00 00 09Lophocolea heterophylla (Schrad) Dumort 00 31 00Lophozia longidens (Lindb) Macoun 04 00 00Lophozia ventricosa (Dicks) Dumort 04 06 00Mnium spinulosum Bruch amp Schimp 04 19 09Oncophorus wahlenbergii Brid 52 863 94Orthotrichum elegans Nees 402 621 283Orthotrichum obtusifolium Brid 526 584 415Plagiomnium cuspidatum (Hedw) T J Kop 386 702 283Plagiomnium ellipticum (Brid) T J Kop 76 68 00Plagiomium sp 16 00 00Plagiothecium denticulatum (Hedw) Schimp 04 00 00Plagiothecium laetum Schimp 00 06 00Platydictya jungermannioides (Brid) H A Crum 16 00 00Platygyrium repens (Brid) Schimp 88 373 245Pleurozium schreberi (Brid) Mitt 100 193 47Pohlia cruda (Hedw) Lindb 00 19 09Pohlia nutans (Hedw) Lindb 16 174 28Polytrichum juniperinum Hedw 00 12 00Ptilidium ciliare (L) Hampe 00 06 00Ptilidium pulcherrimum (Weber) Vainio 28 155 66Ptilium crista-castrensis (Hedw) De Not 112 75 00Pylaisiella polyantha (Hedw) Grout 968 975 925Rhizomnium punctatum (Hedw) T J Kop 00 06 00


TABLE 2 Continued


Sanionia uncinata (Hedw) Loeske 124 590 462Sarmenthypnum sarmentosum (Wahlenb) Tuom amp T J Kop 00 06 00Scapania apiculata Spruce 00 00 09Scapania glaucocephala (Taylor) Austin 00 06 00Syntrichia ruralis (Hedw) F Web amp D Mohr 00 00 19Thuidium recognitum (Hedw) Lindb 04 137 28Timmia megapolitana Hedw 04 00 00Tomentypnum nitens (Hedw) Loeske 00 06 00Tortula mucronifolia Schwagr 12 06 00Trichodon cylindricus (Hedw) Schimp 04 00 00

right side of the ordination and the more northerlysites on the left side (Fig 5) Within each regionsites were ordinated with the smaller less hetero-geneous fragments containing the fewest number ofmicrohabitats at the bottom and the largest andmost heterogeneous sites at the top

Indicator species analyses The Indicator Spe-cies Analysis (ISA) revealed that several species in-cluding Amandinea punctata Caloplaca holocarpaPhaeophyscia orbicularis Physcia adscendens Py-laisiella polyantha and Xanthoria fallax had highindicator values (70) for the smaller fragments(Table 6) However all of those species were alsoindicators of medium-sized and large fragmentsNone of the species were indicators of only smallfragments There were several indicators of mediumand large fragments that were not indicators ofsmaller fragments Indicators of medium and largefragments were Brachythecium salebrosum B star-kei Orthotrichum elegans O obtusifolium Arthoniapatellulata Caloplaca cerina Candellariella vitel-lina Parmelia sulcata and Physcia aipolia How-ever none of those species had high indicator values($64) only in the intermediate class Brachythe-cium campestre Campylium chrysophyllum C his-pidulum Eurynchium pulchellum Hylocomiumsplendens Oncophorus wahlenbergii Plagiomniumcuspidatum Pleurozium schreberi Sanionia uncin-ata Biatoria vernalis Candelaria concolor Everniamesomorpha Hypogymnia physodes Melanelia al-bertana Peltigera canina P neopolydactyla Usneahirta Vulpicida pinastri and Xanthoria polycarpareached high indicator values only in the larger frag-ments Only Peltigera canina had high indicator val-ues in the larger fragments and was not found infragments of the other two size classes

Several indicator species were chosen from the listin Table 6 Selection of indicators for medium andlarge fragments was based on low indicator valuesfor small fragments but high values for medium andlarge fragments Indicators for large fragments hadlow values for small and medium fragments but highvalues for large fragments Relative abundance ofseveral indicators of medium- and large-sized frag-

ments was then plotted against the number of mi-crohabitats (Fig 6) and species richness (Fig 7) Thepresence or absence of indicators of medium andlarge fragments produced a benchmark for fragmentsthat contained more than nine different microhabitatsand 19 bryophyte and lichen species Indicators oflarge-sized fragments produced a benchmark forfragments that contained more than 12 different mi-crohabitats and over 40 species

DISCUSSION

Edge effects Values for all microclimatic var-iables varied considerably at each distance from theedge Since the temperature and humidity outsidethe fragments varied depending on the regional cli-mate the magnitude of the difference between mea-surements inside and outside the fragments alsovaried For example on a cool day the differencebetween temperatures inside and outside the frag-ment at 15 m from the edge was relatively smallwhile the difference in temperatures taken on a hotday at the same distance was relatively large Thesame also applied for humidity measurementsLight intensity at different distances depended onthe canopy structure For example if the canopycover at 15 m was almost complete light intensitymeasurements were low but if there was a gap inthe cover produced by a fallen tree the measure-ments at the same distance were relatively high

The trend of decreasing mean temperatures andlight intensity extending up to 15 m into the frag-ments was similar to those encountered in otherstudies Burke and Nol (1998) who studied decid-uous forests in Ontario found that edge effects ontemperature and soil moisture extended up to 20 mfrom the edge Matlack (1993) found that edge ef-fects extended between 10 and 35 m for light and13 to 24 m for temperature in a deciduous forest inPennsylvania Matlack (1993) also found that edgesaffected humidity up to 50 m from the margin Thetrends of decreasing mean temperatures and lightintensity and increasing mean relative humidity upto 15 and 30 m encountered in this study fell within


TABLE 3 Percent abundance of lichen species in fragments from three different areas of the sub-humid low-borealforest in north central Alberta Abundance was measured as the number of sample plots on which a species wasencountered divided by the total number of plots analyzed in the area


Amandinea punctata (Hoffm) Coppins amp Scheid 335 758 632Arthonia patellulata Nyl 402 901 660Biatora vernalis (L) Fr 876 416 217Bryoria fusescens (Gyelnik) Brodo amp Hawksw 04 81 09Bryoria lanestris (Ach) Brodo amp Hawksw 04 50 00Bryoria simplicior (Vainio) Brodo amp Hawksw 00 137 09Bryoria sp 00 12 00Caloplaca cerina (Erhr) Th Fr 570 584 660Caloplaca holocarpa (Hoffm) Wade 833 925 943Candelaria concolor (Dicks) Stein 60 416 47Candelariella vitellina (Hoffm) Mull Arg 661 863 896Cladina mitis (Sandst) Hustich 00 12 19Cladonia cenotea (Ach) Schaer 00 00 09Cladonia chlorophaea (Florke) Spreng 00 273 66Cladonia coniocraea (Florke) Spreng 44 205 75Cladonia cornuta (L) Hoffm 08 19 00Cladonia cristatella Tuck 00 25 00Cladonia fimbriata (L) Fr 04 25 19Cladonia gracilis (L) Willd 08 130 19Cladonia macilenta Hoffm 00 43 00Cladonia multiformis Merr 20 06 38Cladonia phyllophora Hoffm 00 06 00Cladonia pyxidata (L) Hoffm 08 81 57Cladonia sp 36 06 28Cladonia squamosa Hoffm 00 06 00Cladonia subulata (L) Wigg 00 06 00Cladonia uncialis (L) Wigg 08 236 19Evernia mesomorpha Nyl 72 410 292Flavopunctelia flaventior (Stirt) Hale 76 00 28Hypogymnia physodes (L) Nyl 785 348 123Lecanora circumborealis Brodo amp Vitik 00 06 00Melanelia albertana (Ahti) Essl 80 503 208Melanelia exasperatula (Nyl) Essl 12 484 311Pannaria pezizoides (Web) Trev 04 00 00Parmelia sulcata Tayl 845 839 726Parmeliopsis ambigua (Wulf) Nyl 00 19 00Peltigera aphthosa (L) Willd 00 62 28Peltigera canina (L) Willd 36 149 160Peltigera didactyla (With) Laundon 00 93 00Peltigera leucophlebia (Nyl) Gyelnik 00 06 00Peltigera neopolydactyla (Gyelnik) Gyelnik 147 292 09Peltigera sp 08 00 00Phaeophyscia orbicularis (Neck) Moberg 713 795 434Physcia adscendens (Fr) Oliv 757 994 1000Physcia aipolia (Humb) Furnr 570 919 717Ramalina dilacerata (Hoffm) Hoffm 20 224 302Ramalina farinacea (L) Ach 00 19 00Tuckermannopsis americana (Sprengel) Hale 00 00 09Umbilicaria hyperborea (Ach) Hoffm 08 00 00Usnea hirta (L) Wigg 76 547 349Usnea lapponica Vainio 00 255 170Usnea scabrata Nyl 00 12 00Usnea subfloridana Stirt 84 168 94Vulpicida pinastri (Scop) Mattson amp Lai 16 379 94Xanthoria elegans (Link) Th Fr 00 25 28Xanthoria fallax (Hepp) Arn 745 807 377Xanthoria polycarpa (Hoffm) Rieber 259 193 28

the ranges for those studies As a result a squarefragment must cover a minimum of 900 m2 in orderto protect the microclimate in the interior

The multiple linear regression analysis of speciesrichness indicated that distance from the margin

played an important role on bryophyte and lichendiversity (Table 4) However results were con-founded by the number of different microhabitatsthat seemed to have a more important role in de-termining richness particularly for lichens Dis-


TABLE 4 Stepwise forward selection multiple linear regression analyses between the number of bryophyte andlichen species and distance from the edge the number of different microhabitats air temperatures at ground level (temp0m) at one m (temp 1m) and two m (temp 2m) above the soil surface relative humidity and light intensity forfragments in three different areas of northern Alberta 5 p 005 5 p 0001 ns 5 not significant

All species

Variable R2

Bryophytes

Variable R2

Lichens

Variable R2

All plots (n 5 520)microhabitats 037 microhabitats 025 microhabitats 031distance 048 distance 041 distance 034humidity 050 humidity 042 humidity 037light 051 temp 1m 042 light 037

Athabasca area (n 5 255)microhabitats 019 distance 027 microhabitats 011 nsdistance 027 microhabitats 031 distance 012 nstemp 1m 028 temp 2m 032 light 013 nshumidity 029 temp 0m 033 temp 0m 014 ns

Peace River area (n 5 156)microhabitats 031 microhabitats 020 microhabitats 030distance 044 distance 029 distance 043humidity 048 temp 1m 031 humidity 050temp 1m 028 humidity 031 temp 0m 052

Manning area (n 5 109)distance 021 distance 030 microhabitats 008 nsmicrohabitats 035 microhabitats 041 distance 012 nshumidity 040 temp 1m 041 humidity 015temp 1m 040 temp 2m 042 temp 1m 024

FIGURE 4 Relationship between the number of bryophyte and lichen species and the shape of 44 fragments of thesub-humid low-boreal forest in northern Alberta


TABLE 5 R2 values for linear and second order polynomial regressions between species richness and the log shapeindex of fragments of the sub-humid low-boreal forest in three regions of northern Alberta

Taxa

Athabasca

linear polynomial

Peace River

linear polynomial

Manning

linear polynomial

All species 088 088 076 076 075 077Bryophytes 095 096 070 070 070 071Lichens 071 071 078 078 075 079

FIGURE 5 CCA plot of the scores for 44 fragments of the sub-humid low-boreal forest in northern Alberta basedon the relative abundance of bryophyte and lichen species The insert shows the scores for four environmental variablesalong each axis Habitat heterogeneity 5 the number of different microhabitats found in each fragment Microhabitats5 the total number of microhabitats found in each fragment Shape 5 the log shape index value for each fragmentRegion 5 the three regions in which the fragments were studied (Athabasca Peace River and Manning) Fragments1 2 and 3 are large fragments 4 5 and 6 are medium-sized and fragments 7 8 and 9 are small Fragments 1 4and 7 are in the Manning area fragments 2 5 8 are in the Peace River area and fragments 3 6 and 9 are in theAthabasca area

tance from the edge was significantly positivelycorrelated with habitat heterogeneity making it dif-ficult to separate effects of one from the otherHowever if microhabitats were removed from theregression analysis distance from the edge was sig-nificantly related (p 005) to bryophyte species

richness but not lichen richness Therefore therewas an edge effect on bryophytes where the num-ber of species was reduced close to the edge sincethe slopes for the relationships between distanceand bryophyte richness were positive A more de-tailed analysis of the distance from the margin on


TABLE 6 Percent indicator values for bryophytes andlichens in small medium and large fragments of the sub-humid low-boreal forest in northern Alberta

Taxon Small Medium Large

BryophytesAmblystegium serpens 36 86 100Brachythecium campestre 27 57 100Brachythecium salebrosum 9 64 95Brachythecium starkii 0 64 89Campylium chrysophyllum 0 36 74Campylium hispidulum 0 36 79Eurhynchium pulchellum 9 57 100Haplocladium microphyllum 0 36 100Hylocomium splendens 0 14 65Oncophorus wahlenbergii 18 36 74Orthotrichum elegans 18 71 100Orthotrichum obtusifolium 45 86 95Plagiomnium cuspidatum 9 50 89Pleurozium schreberi 0 14 65Pylaisiella polyantha 82 93 100Sanionia uncinata 0 50 79

LichensAmandinea punctata 73 86 100Arthonia patellulata 55 86 100Biatora vernalis 9 57 95Caloplaca cerina 45 93 95Caloplaca holocarpa 91 100 100Candelaria concolor 9 36 74Candelariella vitellina 64 93 100Evernia mesomorpha 0 43 89Hypogymnia physodes 36 64 95Melanelia albertana 18 50 95Parmelia sulcata 55 100 100Peltigera canina 0 0 65Peltigera neoplydactyla 9 29 79Phaeophyscia orbicularis 91 93 100Physcia adscendens 91 93 100Physcia aipolia 64 100 100Usnea hirta 9 57 89Vulpicida pinastri 0 21 65Xanthoria fallax 82 100 100

bryophyte species richness indicated that edge ef-fects extended between 15 and 20 m (Fig 8) Edgeeffects were particularly evident in smaller frag-ments where bryophytes were not found on downedwoody debris at any decay stage Downed woodydebris that is exposed to full sunlight is drier andharder than debris that is sheltered (Lumley et al2001) The establishment phase of bryophytes onlogs requires moist conditions (Soderstrom 1988)which may explain the lack of bryophytes alongedges or in small fragments

Habitat heterogeneity and species richnessFragment perimeter area and shape index werehighly significantly autocorrelated Since the shapeindex incorporated both the values for perimeterand area it was used to demonstrate effects of frag-mentation on habitat heterogeneity and speciesrichness The linear relationships between the shapeindex and habitat heterogeneity and species rich-

ness also apply to the length of the perimeter andthe size of the fragment

Most of the rare species encountered in this studywere associated with substrate habitats that werenot commonly found in the fragments For exam-ple Brachythecium rivulare Sarmentypnum sar-mentosum Campylium polyganum Campyliumstellatum Climacium dendroides and Tomentyp-num nitens were all found in a wet area or alongthe banks of an ephemeral stream that traversed oneof the fragments Other rare species were found onhabitats that were created by humans For exampleBarbula convoluta Timmia megapolitana and Um-bilicaria hyperborea were found on piles of rocksthat were collected from fields and discarded in thefragments Normally rocks in the study area do notprotrude much above the soil surface and are usu-ally covered by leaf litter Although bryophyteswere occasionally found growing on deciduous leaflitter lichens were never found on that microhabi-tat Propagules of other rare species may have beentransported into the study area by human activityFor example Leskea polycarpa an eastern NorthAmerican species that is rare in Alberta (Vujnovicamp Gould 2002) was found in a fragment that wasadjacent to a tree nursery and experimental orchardthat had imported several plants from eastern NorthAmerica That fragment also contained several non-native vascular plants such as Lonicera tatarica L

The multiple linear regression analysis indicatedthat habitat heterogeneity affected the distributionof both bryophytes and lichens at the sample plotand fragment levels (Tables 4ndash5) Effects were par-ticularly important for lichen species richnessThose results were consistent with findings fromother studies of bryophyte and lichen diversitystudies in deciduous forests where diversity in-creased as the complexity of microhabitats in-creased (Holz et al 2002 Peck 2004) Thereforeplots that contain a wide variety of microhabitatsincluding such unusual substrate habitats as rockpiles ephemeral streams or wet low-lying areas aswell as all of the log decay classes would harborthe greatest diversity

The CCA analysis indicated that there was a dif-ference between fragments from the three regions(Fig 5) Those differences were probably caused bythe following factors 1) a climatic difference wherethe southern area near Athabasca was warmer anddrier than the northern area near Manning 2) theterrain was undulating to moderately hummocky(glacial moraines) in the Athabasca area and flatterand less well drained in the Peace River and Man-ning areas and 3) soil in the Athabasca area wasrockier than in the other two areas Because sites inthe Athabasca area were generally drier than the oth-er two areas it produced a slightly different suite of


FIGURE 6 Habitat heterogeneity performance benchmarks for species indicators of medium and large-sized frag-ments (top) and large fragments (bottom) of the sub-humid low-boreal forest in northern Alberta


FIGURE 7 Bryophyte and lichen species richness performance benchmarks for indicators of medium and large-sized fragments (top) and large fragments (bottom) of the sub-humid low-boreal forest in northern Alberta


FIGURE 8 Relationship between distance from theedge and bryophyte species richness in 44 woodlots innorthern Alberta

species that did not include species found in wetareas As a result of a colder wetter climate in thenorthern area the abundance of conifers and aldersgenerally increased and that produced a slightly dif-ferent suite of species particularly for epiphytic li-chens The rocky soil in the Athabasca area resultedin the creation of rock piles in fragments a habitatthat was not found in the other areas and that con-tained several species not found elsewhere

Although there were regional differences in bryo-phyte and lichen diversity habitat heterogeneity re-mained an important factor affecting the abundanceof both taxa at the fragment level (Fig 5) Fragmentswithin each region were ordinated in the same man-ner small woodlots were separated from medium-sized fragments that were separated from large-sizedones Thus the more heterogeneous sites weregrouped together and the smaller less heterogeneoussites were separate for each region This indicatesthat regardless of the differences between floras inthe different areas diversity within fragments wasregulated by habitat heterogeneity

Indicator species The eight indicators of frag-ments of all sizes (indicator values $64 for all sizes)were mostly epiphytic species that inhabited aspentrees with creviced bark (Table 5) The distributionof those species was not affected by edge effects andbecause their habitat was always present in thisstudy it was not affected by habitat heterogeneityAmong indicators of medium and large fragmentsthere were five bryophytes and four lichens All ofthe species were corticolous that either grew at thebase of the trees along the trunks or on the bark offallen trees Indicators of medium and large frag-ments were susceptible to edge effects but were notrestricted to the interior For example Vitt et al(1988) considered that Vulpicida pinastri (as Ce-traria pinastri) only grew on branches and twigs thatwere at or below maximum snow depth Wind swept

conditions may limit snow accumulations along theedges and in smaller fragments thus limiting the dis-tribution of that species However effects of snowaccumulation may not extend more than a few me-ters inside a fragment and as a result Vulpicida pi-nastri is not restricted only to the interior

Bryophyte indicators of large fragments were gen-erally found on later decay stages of downed woodydebris Such species as Pleurozium schreberi andHylocomium splendens have been shown to be sen-sitive to high light conditions and to drying in thestudy area (Gignac et al 1991) The microclimaticconditions that can support those species were onlyfound in larger fragments where there was an inte-rior that was protected from edge effects Amonglichen indicator species two were found only on de-cayed logs that were close to the ground surfacePeltigera canina and P neopolydactyla two werependant from trees Evernia mesomorpha and Usneahirta and the remainder were epiphytes Althoughprevious analyses demonstrated that there were nosignificant edge effects on lichen species richnessthe indicator species analysis showed that severalspecies were only found in the interior Edge effectson lichen diversity were probably masked by the rel-atively large number of epiphytes that grew on aspenalong the edges and in small fragments

Results of this study demonstrated that there wereedge effects on the microclimate and bryophyte di-versity that extended up to 15 m into a fragmentThus to conserve bryophyte and lichen diversity ef-fectively fragments that have a minimum area of 900m2 or an interior area that is not within 15 m of anedge should be retained on the landscape Since frag-ments often had complex shapes it was not alwayseasy to determine if enough of the interior was pro-tected from edge effects or contained enough micro-habitats to protect species diversity The indicator spe-cies method developed in this study offers an inex-pensive and relatively easy method that can be usedto monitor effects of fragmentation on bryophyte andlichen diversity in mature upland aspen-dominatedcommunities in agricultural and urban environmentsThe method bypasses the necessity of identifying allspecies in each fragment and uses only a few speciesthat are relatively easy to identify Thus landownersif they so desire can assess the conservation value ofwoodlots on their property and adjust their manage-ment accordingly However not all indicators werepresent on all fragments that had greater numbers ofmicrohabitats and species than the benchmarks Forexample Vulpicida pinastri an indicator for mediumand large fragments was not found on woodlots thatcontained 10 11 or 12 microhabitats (Fig 7) There-fore indicators must be used as a suite of specieswhere the presence of one or more would indicatethat a fragment was above the benchmark We rec-


ommend that at least one mature aspen-dominatedfragment containing Pleurozium schreberi Hylocom-ium splendens or Peltigera canina remain on thelandscape until other such communities reach matu-rity in order to protect as much bryophyte and lichendiversity as possible in an area

CONCLUSION

Agricultural development in the Prairie Provinc-es of western Canada is largely unregulated Mostof the land is held by private ownership and manylandowners in the area clearcut forested areas anduse the proceeds to finance the costs of preparingthe land for agriculture Although the province doesmanage some forested land in the region theselands are often used for grazing cattle There arealso provincial and national parks where loggingand grazing are not permitted but these cover onlya small portion of the landscape Thus effectiveconservation of biodiversity in the agriculturalzones must be achieved on the privately ownedlands This study offers an inexpensive and rela-tively easy method that private landowners can usewith a minimum of training to evaluate some of theconservation value of their woodlots

ACKNOWLEDGMENTS

We wish to thank the following field personnel for theircontributions to this project Sherri Nash Pierre RobinsonNatalie Tashe Abigail Vandebergh and Natasha YoungWe would also like to thank Martina Krieger and SuzanneMills for the identification of the bryophytes We are in-debted to Dorothy Fabian of the Department of BiologicalSciences of the University of Alberta for her help in iden-tifying vascular plants The Sustainable Forest Manage-ment Network and a Stanley Greene Research Awardfrom the International Association of Bryologists grantedto L D Gignac and an NSERC Research Grant to M RT Dale provided funding for this project

LITERATURE CITED

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BOUTIN C amp B JOBIN 1998 Intensity of agriculturalpractices and effects on adjacent habitats EcologicalApplications 8 544ndash557

BRODO I M S D SHARNOFF amp S SHARNOFF 2001 Li-chens of North America Yale University Press NewHaven CT

BURKE D M amp E NOL 1998 Edge and fragment sizeeffects on the vegetation of deciduous forests in On-tario Canada Natural Areas Journal 18 45ndash53

CAMARGO J L C amp V KAPOS 1995 Complex edge effectson soil moisture and microclimate in central Amazonianforest Journal of Tropical Ecology 11 205ndash221

CHEN J J F FRANKLIN amp T A SPIES 1995 Growing-season microclimatic gradients from clearcut edgesinto old-growth Douglas-fir forests Ecological Appli-cations 5 74ndash86

COXSON D S amp J MARSH 2001 Lichen chronosequence(postfire and postharvest) in lodgepole pine (Pinuscontorta) forest of northern interior British ColumbiaCanadian Journal of Botany 79 1449ndash1464

CRITES S amp M R T DALE 1998 Diversity and abun-dance of bryophytes lichens and fungi in relation towoody substrate and successional stage in aspen mix-edwood boreal forests Canadian Journal of Botany76 641ndash651

CROSBY M R R E MAGILL B ALLEN amp S HE 1999Checklist of the Mosses Missouri Botanical GardenSt Louis MO

CUNNINGHAM S A 2000 Effects of habitat fragmentationon the reproductive ecology of four plant species inmallee woodland Conservation Biology 14 758ndash768

DE CASENAVE J L J P PELOTTE amp J PROTOMASTRO1995 Edge interior differences in vegetation structureand composition in Chaco semi-arid forest ArgentinaForest Ecology and Management 73 61ndash69

DETTKI H amp P A ESSEEN 1998 Epiphytic macrolichensin managed and natural forest landscapes A compar-ison of two spatial scales Ecography 21 613ndash624

DUFRENE M amp P LEGENDRE 1997 Species assemblagesand indicator species the need for a flexible asymmet-rical approach Ecological Monographs 67 345ndash366

ECOREGIONS WORKING GROUP 1989 Ecoclimatic regionsof Canada First approximation Sustainable Devel-opment Branch Canadian Wildlife Service Conser-vation and Protection Environment Canada Ecologi-cal Land Classification Series No 23

ENVIRONMENT CANADA 1980 Canadian Climate Normals1951ndash1980 Temperature and Precipitation Environ-ment Canada Atmospheric Environment ServiceDownsview ON

FENTON N J K A FREGO amp M R SIMS 2003 Changesin forest floor bryophyte (moss and liverwort) com-munities 4 years after forest harvest Canadian Journalof Botany 81 714ndash731

FORMAN R T T amp M GODRON 1986 Landscape Ecol-ogy John Wiley amp Sons NY

FITZSIMMONS M 2002 Estimated rates of deforestation intwo boreal landscapes in central Saskatchewan CanadaCanadian Journal of Forest Research 32 843ndash851

FRISVOLL A A amp T PRESToslash 1997 Spruce forest bryo-phytes in central Norway and their relationship to en-vironmental factors including modern forestry Ecog-raphy 20 3ndash18

GIGNAC L D D H VITT S C ZOLTAI amp S E BAYLEY1991 Bryophyte response surfaces along climaticchemical and physical gradients in peatlands of west-ern Canada Nova Hedwigia 53 27ndash71

GRASHOF-BOKDAM C 1997 Forest species in an agricul-tural landscape in the Netherlands effects of habitatfragmentation Journal of Vegetation Science 8 21ndash28

GUSTAFSSON L amp T HALLINGBACK 1998 Bryophyte floraand vegetation of managed and virgin coniferous for-ests in South-West Sweden Biological Conservation44 283ndash300

HAZELL P O KELLNER H RYDIN amp L GUSTAFSSON1998 Presence and abundance of four epiphytic bryo-phytes in relation to density of aspen (Populus tre-mula) and other stand characteristics Forest Ecologyand Management 107 147ndash158

HOBSON K A E M BAYNE amp S L VAN WILGENBURG2002 Large-scale conversion of forest to agriculturein the Boreal Plains of Saskatchewan ConservationBiology 16 1530ndash1541

HOLZ I S R GRADSTEIN amp J HEINRICHS 2002 Bryo-phyte diversity microhabitat differentiation and dis-


tribution of life forms in Costa Rican upper montaneQuercus forest THE BRYOLOGIST 105 334ndash348

HONNAY O M HERMY amp P COPPIN 1999 Effects of areaage and diversity of forest patches in Belgium on plantspecies richness and implications for conservation andreforestation Biological Conservation 87 73ndash84

JOBIN B C BOUTIN amp J-L DESGRANGES 1997 Effectsof agricultural practices on the flora of hedgerows andwoodland edges in southern Quebec Canadian Journalof Plant Science 77 293ndash299

KUUSINEN M 1994 Epiphytic lichen flora and diversityon Populus tremula in old growth and managed forestsof southern and middle boreal Finland Annales Bo-tanici Fennici 31 245ndash260

mdashmdashmdash 1996 Cyanobacterial macrolichens on Populustremula as indicators of forest continuity in FinlandBiological Consevation 75 43ndash49

KRUYS N C FRIES B G JONSSON T LAMAS amp GSTAHL 1999 Wood-inhabiting cryptogams on deadNorway spruce (Picea abies) trees in managed Swed-ish boreal forests Canadian Journal of Forest Research29 178ndash186

LESSICA P B MCCUNE amp W S HONG 1991 Differencesin lichen and bryophyte communities between old-growth and managed second-growth forests in theSwan Valley Montana Canadian Journal of Botany69 1745ndash1755

LOVEJOY T E R O BIERREGARD JR H B RYLANDS JR MALCOLM C E QUINTELA L H HARPER K SBROWN JR A H POWELL G V N POWELL H OR SCHUBERT amp M B HAYS 1986 Edge and othereffects of isolation on Amazonian forest fragmentspp 257ndash285 In M Soule (ed) Conservation BiologySinauer Associates Sunderland MA

LUMLEY T C L D GIGNAC amp R S CURRAH 2001 Mi-crofungus communities of white spruce and tremblingaspen logs at different decay stages in disturbed andundisturbed sites in the boreal mixedwood region ofAlberta Canadian Journal of Botany 79 76ndash92

MALCOLM J R 1998 A model of conductive heat flowin forest edges and fragmented landscapes ClimateChange 39 487ndash502

MAGURRAN A E 1988 Ecological Diversity and Its Mea-surement Princeton University Press Princeton NJ

MATLACK G R 1993 Microenvironment variation withinand among forest edge sites in the eastern UnitedStates Biological Conservation 66 185ndash194

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MCALISTER S 1995 Species interactions and substratespecificity among log-inhabiting bryophyte speciesEcology 76 2184ndash2195

MCCUNE B amp M J MEFFORD 1997 PC-ORD Multi-variate Analysis of Ecological Data Version 32 MJMSoftware Design Glenedon Beach OR

mdashmdashmdash R ROSENTRETER J M PONZETTI amp D C SHAW2000 Epiphytic habitats in an old conifer forest inwestern Washington USA THE BRYOLOGIST 103417ndash427

MCGEE G G amp R W KIMMERER 2002 Forest age andmanagement effects on epiphytic bryophyte commu-nities in Adirondack northern hardwood forests NewYork USA Canadian Journal of Forest Research 321562ndash1576

MERRIFIELD K 2000 Bryophytes on isolated Quercusgarryana trunks in urban and agricultural settings inthe Willamette Valley Oregon THE BRYOLOGIST 103720ndash724

NEITLICH P N amp B MCCUNE 1997 Hotspots of epiphyticlichen diversity in two young managed forests Con-servation Biology 11 172ndash182

PATON J A 1999 The liverwort flora of the British IslesHarley Books Colchester

PECK J E J GRABNER D LADD amp D R LARSEN 2004Microhabitat affinities of Missouri Ozark lichens THE

BRYOLOGIST 107 47ndash61PHARO E J amp D H VITT 2000 Local variation in bryo-

phyte and macro-lichen cover and diversity in mon-tane forests of western Canada THE BRYOLOGIST 103455ndash466

RAMANKUTTY N amp J A FOLEY 1999 Estimating histor-ical changes in land cover North American croplandsfrom 1850 to 1992 Global Ecology and Biogeography8 381ndash396

ROSS-DAVIS A L amp K A FREGO 2002 Comparison ofplantations and naturally regenerated clearcuts in theAcadian Forest forest floor bryophyte community andhabitat features Canadian Journal of Botany 80 21ndash33

ROSSO A amp R ROSENTRETER 1999 Lichen diversity andbiomass in relation to management practices in forestsof northern Idaho EVANSIA 16 97ndash104

ROWE J S 1972 Forest Regions of Canada CanadianForestry Service Bulletin No 1300

RUCHTY A A L ROSSO amp B MCCUNE 2001 Changes inepiphyte communities as the shrub Acer circinatumdevelops and ages THE BRYOLOGIST 104 274ndash281

SHEARD J W amp M E JONESCU 1974 A multivariateanalysis of the distribution of lichens on Populus tre-muloides in west-central Canada THE BRYOLOGIST 77514ndash530

SILLET S C S R GRADSTEIN amp D GRIFFIN 1995 Bryo-phyte diversity of Ficus tree crowns from cloud forestand pasture in Costa Rica THE BRYOLOGIST 98 218ndash227

SODERSTROM L 1988 Sequence of bryophytes and li-chens in relation to substrate variables of decaying co-niferous woods in northern Sweden Nordic Journal ofBotany 8 89ndash97

mdashmdashmdash 1989 Regional distribution patterns of bryophytespecies on spruce logs in northern Sweden THE BRY-OLOGIST 92 349ndash355

VITT D H amp R J BELLAND 1997 Attributes of rarityamong Alberta mosses Patterns and prediction of spe-cies diversity THE BRYOLOGIST 100 1ndash12

mdashmdashmdash Y LI amp R J BELLAND 1995 Patterns of bryo-phyte diversity in peatlands of continental westernCanada THE BRYOLOGIST 98 218ndash227

mdashmdashmdash J E MARSH amp R B BOVEY 1988 Mosses Li-chens and Ferns of Northwest North America LonePine Publishing Edmonton AB

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WEAVER M amp M KELLMAN 1981 The effects of forestfragmentation on woodlot tree biotas in southern On-tario Journal of Biogeography 8 199ndash210

WILCOX B A amp D D MURPHY 1985 Conservationstrategy the effects of fragmentation on extinctionAmerican Naturalist 125 897ndash887

WITH K A amp T O CRIST 1995 Critical thresholds inspecies responses to landscape structure Ecology 762446ndash2459

ZECHMEISTER H G A TRIBSCH D MOSER J PETERSEIL ampT WRBK 2003 Biodiversity lsquohot spotsrsquo for bryophytesin landscapes dominated by agriculture in Austria Ag-riculture Ecosystems and Environment 94 159ndash167

ms received July 20 2004 accepted Nov 9 2004

0007-274505$1850

The Bryologist 108(1) pp 50 66Copyright q 2005 by the American Bryological and Lichenological Society Inc

Effects of Fragment Size and Habitat Heterogeneity on Cryptogam Diversity inthe Low-boreal Forest of Western Canada

L DENNIS GIGNAC

Faculte Saint-Jean University of Alberta 8406 91 Street Edmonton Alberta T6C 4G9 Canada e-mail dgignacualbertaca

MARK R T DALE

Department of Biological Sciences University of Alberta Edmonton Alberta T6G 2E9 Canada e-mailmarkdaleualbertaca

Abstract The effects of fragmentation of the sub-humid low-boreal forest in agro environmentson bryophyte and lichen diversity were analyzed on 44 woodlots in three regions of northernAlberta Canada Woodlots were selected to cover a wide variety of shapes and sizes in eacharea Several microclimatic variables which included temperature at three different heights abovethe forest floor relative humidity and the amount of light penetration were measured in five mdiameter circular sample plots along transects that covered the length and the width of eachfragment The number of microhabitats that included living trees with creviced and smooth barkstanding dead different decay classes of downed woody debris soil and rock were tabulated ateach sample plot Bryophyte and lichen presence was noted for all microhabitats found withineach plot There was a trend of decreasing temperature and light intensity and increasing humidityup to 15 m from the edge of the fragments A multiple regression analysis revealed that thedistance from edge and the habitat heterogeneity were the most important variables affectingbryophyte and lichen species richness Further analysis indicated that edge effects were significantfor bryophytes but not for lichens The size and shape of fragments had a significant effect onhabitat heterogeneity and bryophyte and lichen diversity Although there was a distinction be-tween the floras in each region the effects of fragment size and habitat heterogeneity were similarAn indicator species analysis selected several indicators of large medium and small fragmentsthat were also indicators of habitat heterogeneity and species richness The presence or absenceof several indicator species is used to produce performance benchmarks for habitat heterogeneityand species richness The use of indicator species offers an inexpensive and relatively easy methodto evaluate edge effects and habitat heterogeneity on bryophyte and lichen diversity in woodlots

Keywords Agro-environments edge effects forest fragmentation habitat heterogeneity in-dicator species microclimate microhabitat

Forest fragmentation results from the clear cut-ting of large tracts for a variety of purposes includ-ing forestry agriculture andor urban developmentAt its most extreme clear cutting leaves only smallisolated remnants of the native original forestwoodlots hedgerows or stream banks of varyingsize surrounded on all sides by other types of hab-itats Landscape fragmentation caused by defores-tation is one of the main causes of decline in world-wide biological diversity (Wilcox amp Murphy 1985)

The decrease in the area of the remnants of thenative forest increases edge effects Vegetation inthe fragments is more exposed to wind and highersolar radiation that produce drier and warmer grow-ing conditions than in the original forest (Camargoamp Kapos 1995 Chen et al 1995 de Casenave etal 1995 Malcolm 1998 Sillett et al 1995) As a

result shade tolerant vascular plant species alongthe edge are replaced by species that are found inopen areas (Lovejoy et al 1986) Edge effects fur-ther reduce the area within the fragment occupiedby the original forest species As the size of thefragment is reduced it reaches a critical thresholdbelow which all parts of the fragment become edg-es thus eliminating many of the original shade tol-erant species and reducing diversity (With amp Crist1995) Thus although the size of long and narrowfragments may be above the critical threshold di-versity may be adversely affected because all areaswithin the patch are influenced by higher insolationand wind

Effects of forest fragmentation resulting from ag-ricultural land use in North America have beenstudied for many animal taxa particularly birds as











METHODS















RESULTS

























TABLE 2 Continued







DISCUSSION












All species

Variable R2

Bryophytes

Variable R2

Lichens

Variable R2








Taxa

Athabasca

linear polynomial

Peace River

linear polynomial

Manning

linear polynomial






























CONCLUSION


ACKNOWLEDGMENTS


LITERATURE CITED














































































METHODS















RESULTS

























TABLE 2 Continued







DISCUSSION












All species

Variable R2

Bryophytes

Variable R2

Lichens

Variable R2








Taxa

Athabasca

linear polynomial

Peace River

linear polynomial

Manning

linear polynomial






























CONCLUSION


ACKNOWLEDGMENTS


LITERATURE CITED






































































METHODS















RESULTS

























TABLE 2 Continued







DISCUSSION












All species

Variable R2

Bryophytes

Variable R2

Lichens

Variable R2








Taxa

Athabasca

linear polynomial

Peace River

linear polynomial

Manning

linear polynomial






























CONCLUSION


ACKNOWLEDGMENTS


LITERATURE CITED













































































RESULTS

























TABLE 2 Continued







DISCUSSION












All species

Variable R2

Bryophytes

Variable R2

Lichens

Variable R2








Taxa

Athabasca

linear polynomial

Peace River

linear polynomial

Manning

linear polynomial






























CONCLUSION


ACKNOWLEDGMENTS


LITERATURE CITED


























































































TABLE 2 Continued







DISCUSSION












All species

Variable R2

Bryophytes

Variable R2

Lichens

Variable R2








Taxa

Athabasca

linear polynomial

Peace River

linear polynomial

Manning

linear polynomial






























CONCLUSION


ACKNOWLEDGMENTS


LITERATURE CITED


















































































TABLE 2 Continued







DISCUSSION












All species

Variable R2

Bryophytes

Variable R2

Lichens

Variable R2








Taxa

Athabasca

linear polynomial

Peace River

linear polynomial

Manning

linear polynomial






























CONCLUSION


ACKNOWLEDGMENTS


LITERATURE CITED









































































TABLE 2 Continued







DISCUSSION












All species

Variable R2

Bryophytes

Variable R2

Lichens

Variable R2








Taxa

Athabasca

linear polynomial

Peace River

linear polynomial

Manning

linear polynomial






























CONCLUSION


ACKNOWLEDGMENTS


LITERATURE CITED





































































TABLE 2 Continued







DISCUSSION












All species

Variable R2

Bryophytes

Variable R2

Lichens

Variable R2








Taxa

Athabasca

linear polynomial

Peace River

linear polynomial

Manning

linear polynomial






























CONCLUSION


ACKNOWLEDGMENTS


LITERATURE CITED













































































All species

Variable R2

Bryophytes

Variable R2

Lichens

Variable R2








Taxa

Athabasca

linear polynomial

Peace River

linear polynomial

Manning

linear polynomial






























CONCLUSION


ACKNOWLEDGMENTS


LITERATURE CITED






































































All species

Variable R2

Bryophytes

Variable R2

Lichens

Variable R2








Taxa

Athabasca

linear polynomial

Peace River

linear polynomial

Manning

linear polynomial






























CONCLUSION


ACKNOWLEDGMENTS


LITERATURE CITED






































































Taxa

Athabasca

linear polynomial

Peace River

linear polynomial

Manning

linear polynomial






























CONCLUSION


ACKNOWLEDGMENTS


LITERATURE CITED





























































































CONCLUSION


ACKNOWLEDGMENTS


LITERATURE CITED


















































































CONCLUSION


ACKNOWLEDGMENTS


LITERATURE CITED
















































































CONCLUSION


ACKNOWLEDGMENTS


LITERATURE CITED














































































CONCLUSION


ACKNOWLEDGMENTS


LITERATURE CITED






































































CONCLUSION


ACKNOWLEDGMENTS


LITERATURE CITED














































































































Documents

Effects of Fragment Size and Habitat Heterogeneity on Cryptogam Diversity in the Low-boreal Forest of Western Canada