Detection probability and abundance estimation of epiphytic lichens

based on height-limited surveys

Victor Johansson, Tord Snall, Per Johansson & Thomas Ranius

AbstractQuestions: What are the detection probabilities ofepiphytic crustose lichens on oak (Quercus robur)when only the lowest 2m of the trunk are surveyed?How does the abundance of lichen species changewith height above the ground, and is the changerelated to tree age? How well can total abundance(0-6m) be predicted based on data from the lowest2m? Which tree characteristics explain the verticaldistribution of the study species?Location: Southeast Sweden.Methods: The occurrence and abundance of eightcrustose lichen species were recorded on 35 oaks, 0-6m from the ground.Results: The detection probability was high (496%)for seven out of the eight species. The abundance ofsix species declined significantly with increasingheight. For five species, 469% of the total abun-dance (0-6m) was recorded on the lowest 2m. Theproportion of the total abundance present above 2mincreased significantly with age for three species.Models predicting total abundance based on datafrom the lowest 2m and diameter explained 480%of the deviance for all except one species. The verticaldistribution of the study species was explained bybark fissure depth, area and cover of macrolichens.Conclusions: For crustose lichens associated withold oaks, surveying only the lowest 2m of the trunkyields reliable occurrence data and fairly goodestimates of total abundance. However, before in-terpreting data from the lowest 2m, knowledge ofspecies vertical distribution, and how the distribu-tion changes with tree age is essential.

Keywords: Crustose lichens; Epiphyte; Indicator spe-cies; Quercus robur; Tree age; Vertical distribution.

Nomenclature: Santesson et al. (2004).

Introduction

In recent decades, increasing attention has beenpaid to epiphytic lichens and bryophytes asindicators of biodiversity or environmental condi-tions (Hawksworth & Rose 1976; Nilsson et al.1995; Gustafsson et al. 1999; Lindenmayer et al.2000), and as model species for increasing our un-derstanding of metapopulation dynamics amongdynamic patches (Snall et al. 2003, 2005). Epiphytesurveys are, for practical reasons, often only per-formed on the lowest 2m of the trunk (e.g. Dettki &Esseen 1998; Kantvilas & Jarman 2004; Johanssonet al. 2007; Glimskar et al. 2008). For protrudingand easily identified species, this is sometimes com-plemented by a survey of the rest of the tree usingbinoculars (e.g. Hedenas & Ericsson 2000; Jo-hansson & Ehrlen 2003; Ockinger et al. 2005). Formany epiphytic species, however, it is unlikely thatall occurrences will be detected if only the lowest 2mof the tree is surveyed (Fritz 2009). Furthermore,limiting the survey to the lowest 2m should reducethe accuracy of measures of epiphyte abundance ontrees. We are not aware of any study that has calcu-lated detection probabilities of epiphytic lichenspecies caused by limiting the survey to the lowest2m, or that has developed models for predicting thetotal abundance on trees using data from only thelowest 2m of the trunk.

The vertical distribution of an epiphyte de-termines how well whole-tree distribution isrepresented by only collecting data from the lowest2m of the trunk. Canopy studies have revealed thatthe vertical distribution of epiphytes is affected byboth succession and environmental gradients ofmoisture and light (e.g. McCune 1993; McCuneet al. 1997; Lyons et al. 2000). The succession ofepiphytes on tree trunks is likely to be related to thevertical gradient of substrate age; the bark on thelower part of a trunk is the oldest (Harris 1971a;Yarranton 1972; Rogers 1988; Fritz 2009). Treevariables related to age affect the occurrence andabundance of many epiphytes (Gustafsson et al.1992; Gu et al. 2001; Johansson & Ehrlen 2003;Snall et al. 2004; Ranius et al. 2008; Johansson et al.in press). Species that exhibits a positive correlation

Johansson, V. (corresponding author, victor.johansson@

ekol.slu.se), Snall, T. (Tord.Snall@ekol.slu.se) &

Ranius, T. (Thomas.Ranius@ekol.slu.se): Department

of Ecology, Swedish University of Agricultural

Sciences, P.O. Box 7044, SE–750 07 Uppsala, Sweden.

Johansson, P. (Per.Johansson@lansstyrelsen.se):

County Administration Board, SE-791 84 Falun,

Sweden.

Journal of Vegetation Science 21: 332–341, 2010DOI: 10.1111/j.1654-1103.2009.01146.x& 2009 International Association for Vegetation Science

between occurrence/abundance and tree age can beexpected to establish on the lower parts, and thenexpand upwards on the trunk as the tree ages(Barkman 1958; Rogers 1988).

Pendunculate oak (Quercus robur) grows largerand lives longer than most other tree species inNorthern Europe (Nilsson 1997), and constitutes akey substrate for many species. In Sweden, about300 lichen species grow on oaks (Hultengren et al.1997), and the characteristic coarse bark of old oaksconstitutes a habitat for many rare and Red-listedcrustose lichens (Thor & Arvidsson 1999). Thesespecies are commonly used as indicators of highconservation value (Nitare 2000; Glimskar et al.2008). In a study of three wind-felled oaks, severalspecies of conservation interest occurred only above2m (Johansson et al. 2003). In a survey of a singleoak tree, Hultengren (1995) showed that speciesrichness was greatest on the lowest 2m. However,some species occurred only on the lower part of thetrunk, and some species only on the upper part. It isdifficult to draw general conclusions from these stu-dies because of the small sample sizes, but bothindicate that species of conservation interest maynot be detected when limiting the survey to the low-est 2m.

The first aim of this study is to quantify the de-tection probabilities of eight crustose lichen species(given that they occur on the tree) if a survey is re-stricted to the lowest 2m of the tree trunk. In thisstudy, detection probability is based on a single sur-vey, and is defined as the proportion of occupiedtrees where the species was found on the lowest 2m.The second aim is to investigate how the abundanceof different species changes with increasing heightabove the ground, and how this is related to tree age.Third, we develop models to predict the total abun-dance on a tree using only species abundance andtree characteristics recorded for the lowest 2m.Fourth, we test whether the effect of height on lichenabundance is an effect of tree characteristics that arecorrelated to height above ground.

Methods

Study site and trees

The study was conducted in September andOctober 2007 at ‘‘Brokinds skolhage’’ (581120N,151390E), which is a pasture with widely spaced oakssituated in southeast Sweden. Thirty-five oak trees(Q. robur) were randomly chosen from pre-

determined age classes that cover the range of agesof trees present in the pasture.

Study species

We studied eight crustose lichen species thatdiffer in their frequency and abundance on oaks(Ranius et al. 2008; pers. obs.): Cliostomum corru-gatum (Ach.:Fr.) Fr., Lecanographa amylacea(Ehrh. ex Pers.) Egea & Torrente, Chaenothecaphaeocephala (Turner) Th. Fr., Calicium adspersumPers.,Calicium salicinum Pers.,Calicium viride Pers.,Chrysothrix candelaris (L.) J.R. Laundon and Per-tusaria flavida (DC.) Laundon. The first four speciesrepresent old oak specialists of conservation inter-est. They mainly occur on old oaks and are used asindicators of old oak continuity (Nitare 2000). Thefirst two of these are Red-listed (Gardenfors 2005).The last four species were chosen as a contrast to thefirst four. They are relatively common, and fre-quently also occur on other deciduous tree species.

Sampling and field measurements

For each tree (tree level henceforth), we estimatedtree age from tree cores (25 available from Raniuset al. 2008, and 10 new using the same method), thatranged between 40-435 years. We also measured treediameter at breast height (dbh), and these rangedfrom 27-166 cm. Each tree was then divided intovertical segments by attaching ropes from a height of6m down to the ground. This was done on four sidesof the trees: SE, SW, NE and NW. The ropes weremarked every meter, where each marking constitutedcorners of plots, giving a total of 24 plots per tree thattogether covered the whole trunk surface from theground up to 6m (Fig. 1).

For each plot, we recorded the abundance ofeach study species on a log scale: 0, o1, 1-10 cm2,etc. The lowest plots (0-2m) were surveyed whilestanding on the ground, while the upper 4m weresurveyed using a ladder. The time spent on each plotwas usually approximately 10min, but at some plotswe spent more time for species identification of smallor atypical thalli. Unidentified thalli were collectedand later identified in the lab. Before surveying thestudy species on the upper 4m from the ladder, wejudged their abundance in each plot above 2m fromthe ground using a pair of binoculars (�10).

For each plot, we also recorded the potentialexplanatory variables, bark fissure depth (mm), plotarea (cm2), total macrolichen cover and total mosscover, the last two using the log scale describedabove. Bark fissure depth was measured by putting a

Detection probability and abundance estimation for lichens 333

metallic ruler into the fissure and reading it against astraight object held over the fissure. In the analyses,we used the mean depth of bark fissures, i.e. mean ofmeasures at three points (the furthest right, middleand furthest left fissure of the plot) at the meanheight of each plot. The upper and lower widths ofeach plot were used to calculate plot area. If the plotincluded branches, the 0.5m of the branches closestto the trunk were surveyed and taken to be part ofthe plot. In these cases, we recorded whether thestudy species either occurred (i) only on the trunk,(ii) on both the trunk and the branch or (iii) only onthe branch.

As a complement to the survey of standingtrees, we surveyed five recently wind-felled oaks. Foreach tree, we searched for our study species on thewhole tree and focused on ensuring that species ab-sent on the lowest 2m were absent also above 6m,and on the parts of the branches that were 40.5mfrom the trunk.

Data analysis

We tested the effect of height and tree age on theabundance of each species, and how the interaction

between height and tree age affected species abun-dance in three different analyses: (i) focal speciesabundance in relation to height above the ground;(ii) total focal species abundance in relation to treeage; and (iii) proportion of the total abundance thatwas recorded above 2m and its relationship to treeage. When examining effect of height above theground (i), we controlled for the effect of tree iden-tity, making it impossible to include tree age in thesame analysis.

In the first analysis (i), we tested the effect ofheight above the ground on focal species abundanceusing a generalized linear model (GLM, McCullagh& Nelder 1989) with an identity link function (linearregression). We calculated the response variable,species abundance at different heights (0-2, 2-4 and4-6m), as the sum of the abundance in all plots ateach height, using the geometric mean of the coverclass recorded in each plot. The response variablewas log-transformed to provide a better approx-imation to normality. Only trees where a focalspecies was present were included in this analysis.Tree identity was included as a categorical variableto avoid pseudoreplication at the tree level. Sinceage was also measured at the tree level (see Samplingand field measurements above), this variable couldnot be included in the same model.

In the second analysis (ii), we tested the effect ofage-related factors (age, mean bark fissure depthand dbh, all summarized to tree level) on the totalabundance of each study species using a GLM withan identity link function. The total abundance ofeach species was calculated by summing the abun-dance in all plots on the tree using the geometricmean of the cover class recorded in each plot. Thetotal abundance was divided by the total surfacearea of the trunk up to 6m to produce the responsevariable percentage cover, which was arcsine squareroot-transformed to provide a better approximationto normality.

In the third analysis (iii), we tested whether theproportion of the total abundance of each speciesthat was recorded above 2m varied with age-relatedfactors (age, mean bark fissure depth and dbh)measured at the tree level using a GLM with anidentity link function. The response variable, pro-portion of the total abundance recorded above 2m,was arcsine square root-transformed to provide abetter approximation to normality. Only trees onwhich the focal species was present were included inthe analyses. First we tested each independent vari-able (also its square if biologically reasonable)separately. Age was, if significant, used as the start-ing variable in building the model. The remaining

Fig. 1. Schematic representation of the sampling design.The lower 6m of the tree trunk was divided into six hor-izontal segments, at every meter. Each segment wasfurther divided vertically on four sides of the tree, SE, SW,NE and NW, giving a total of 24 smaller plots per tree,together covering the whole trunk up to 6m.

334 Johansson, Victor et al.

significant variables were then added one by one, inorder of explained deviance, and retained in themodel if they significantly improved the fit.

We developed GLMs (identity link function) fortotal abundance (absolute cover 0-6m) of the focalspecies using abundance data from the lowest 2m ofthe trunk, and variables measured at the tree level(see Sampling and field measurements above). Totalabundance was log-transformed to provide a betterapproximation to normality, while the abundanceon the lowest 2m was log-transformed to improvemodel fit. For species that were absent from thelowest 2m on some trees, a constant (0.01 cm2) wasadded to make log transformation possible. Tomake the models user-friendly, we used trunk dia-meter (dbh) instead of age, since this is easier tomeasure.

We assessed the correlation between plot vari-ables and height above the ground using Spearman’scorrelations. Plot area and bark fissure depth foreach plot were taken as the proportion of the meanfor each tree in order to remove the effect of differ-ences between trees. Bryophyte and macrolichencover were taken as percentage cover in each plotusing the geometric mean of the cover class recordedin each plot.

In order to test whether the effect of heightabove the ground on lichen abundance found (seeResults) was an effect of substrate characteristicscorrelated to height, we used ordinal regression(Agresti 2002) because of the ordinal response vari-able. Three variables, tree identity, plot area andconnectedness (see below), were always included inthe model, irrespective of whether they were sig-nificant or not. Tree identity was included as acategorical variable to avoid pseudoreplication atthe tree level. Plot area was included to remove theeffect of plot size differences between trees. Con-nectedness was calculated as the sum of theabundance in adjacent plots (eight for all plots ex-cept those at ground level and at 6m, where only fiveplots were adjacent), and included in all models to

remove the effect of closely situated plots having si-milar properties (Besag 1975).

Statistical analyses were conducted using R2.6.2 (R Development Core Team 2008), with theadd-on library MASS 7.2-40 (Venables & Ripley2002).

Results

Detection probability of lichens when surveying fromthe ground

The probability of detecting a species (giventhat it was present on the tree) was high when onlythe lowest 2m of the tree trunk were surveyed; forsix of the study species, all occurrences at the treelevel were detected. For the remaining two species,detection probability was high for C. phaeocephalabut relatively low for C. salicinum (Table 1). Ontrees where these species occurred only above 2m,they remained undetected from the ground evenwhen binoculars were used.

In plots with branches, the focal lichens oc-curred most often only on the trunk. However, twospecies also occurred quite frequently on branches,C. viride and C. candelaris, which were present onbranches in 31% and 41%, respectively, of the plotswith branches and in which the species were pre-sent. Furthermore, five species were occasionallyfound only on a branch: C. adspersum (2.7%), C.viride (6.0%), C. phaeocephala (5.3%), C. candelaris(2.8%) and P. flavida (1.8%). At the tree level, nospecies were only found on branches, and a speciesoccurring on a branch was always also present onthe lowest 2m of the trunk. On the five recentlywind-felled trees, considered individually, no spe-cies (out of the eight study species) in addition tothose found on the lowest 2m of the trunk, weredetected above 6 or40.5m away from the trunk onbranches.

Table 1. The proportion of oaks (n5 35) on which species were recorded (i) in the range 0–6m, (ii) below 2m and (iii) below2m1using binoculars. Detection probabilities are the proportion of trees where the species was found on the lowest 2m outof all trees where the species was recorded in the height range 0–6m.

Caliciumadspersum(%)

Caliciumsalicinum(%)

Caliciumviride(%)

Chaenothecaphaeocephala(%)

Chrysothrixcandelaris(%)

Cliostomumcorrugatum(%)

Lecanographaamylacea(%)

Pertusariaflavida(%)

0–6m 71.4 40.0 82.9 65.7 97.1 45.7 8.6 88.6Below 2m 71.4 28.6 82.9 62.9 97.1 45.7 8.6 88.6With binoculars 71.4 28.6 82.9 62.9 97.1 45.7 8.6 88.6Detection probability 100 71 100 96 100 100 100 100

Detection probability and abundance estimation for lichens 335

Lichen abundance at different heights, in total, and itsrelationship with tree age

Abundance decreased with increasing height forsix out of the eight species (Fig. 2). The proportionof total abundance found at different heightsdiffered between the species. For C. adspersum,C. candelaris, C. corrugatum, L. amylacea and P.flavida, 69-84% of the total abundance was foundon the lowest 2m (Fig. 2). C. salicinum abundancetended to decrease with height, while C. viride andC. phaeocephala were more evenly distributed up thetrunk.

The total abundance (as a proportion of totalarea surveyed) of five species increased with in-creasing tree age, while the abundance ofmacrolichens decreased with increasing age (Table2). For three species, all age-related variables hadpositive effects on the proportion of the totalabundance that occurred above 2m, when analysed

as separate variables. However, since all these vari-ables were strongly correlated, only age wassignificant in the final model (Table 2). This meansthat on young trees compared to old trees, more ofthe total abundance of these species was found onthe lowest 2m.

For most species, the total abundance on thetree was best predicted using only the abundanceon the lowest 2m as an explanatory variable(Table 3). For two species, C. adspersum andP. flavida, the models were improved by also in-cluding dbh of the tree (as an easily obtained proxyfor age). For all species except C. salicinum, theexplained deviance (which is an analogue to R2)was high (480%).

It was difficult to survey the study species on theupper 4m of the trunk (2-6m) using binoculars; formost specieso25% of the abundance between 2 and6m could be recorded from the ground. For twospecies, the proportion visible from the ground was

Calicium adspersumP < 0.001, N = 75

Calicium salicinumP = 0.033, N = 42

Calicium virideP = 0.082, N = 87

Chaenotheca phaeocephalaP = 0.416, N = 69

Chrysothrix candelarisP < 0.001, N = 102

Cliostomum corrugatumP < 0.001, N = 48

Lecanographa amylaceaP = 0.016, N = 9

Pertusaria flavidaP < 0.001, N = 93

Macrolichens

0.0 0.2 0.4 0.6 0.8 1.0Proportion ± SE

4-6 m

2-4 m

0-2 m

Fig. 2. The proportion of the total abundance of eight crustose lichen species, and the group of macrolichens at differentheights from the ground. P-values are from tests for difference in proportional abundance between heights. SignificantP-values (o0.05) are written in bold.

336 Johansson, Victor et al.

higher: C. candelaris (58.7%) and L. amylacea(100.0%).

Tree characteristics correlated to height and theirrelationship with lichen abundance

Three plot characteristics were correlated withheight above the ground (Table 4). The correlationwith bark fissure depth and plot area was negative,while the correlation with macrolichen cover waspositive. For two of the study species, abundancedecreased with increasing macrolichen cover (Table5). Bark fissure depth had a significant effect on theabundance of five species. For three of these speciesthere was a significant interaction between bark fis-sure depth and height, indicating that the effect ofbark fissure depth differed along the vertical gra-

dient: the positive effect of bark fissure depth wasmost pronounced at greater heights. The negativeeffect of height remained in models including othervariables related to height for all species (Table 5).

Discussion

Detection probability of lichens when surveying fromthe ground

For seven out of the eight species, the detectionprobability was high when the survey was limited tothe lowest 2m of the trunk, and for the four in-dicator species, only one occurrence at tree level (outof 67) was not represented on the lowest 2m. Thismeans that, for most of our study species, surveyslimited to the lowest 2m of oak trunks yield accu-

Table 2. The relationship between tree age and total abundance and the proportional abundance above 2m for differentlichens. P-values and relationships are from linear regression models. A negative relationship with Age2 means that theincrease in abundance flattens out at high ages. Significant P-values (o0.05) are written in bold.

Total abundance Proportional abundance 42m

Relationship P-value Relationship P-value

Calicium adspersum Age 1 o0.001 1 o0.001

Calicium salicinum Age (� ) 0.308Calicium viride Age (� ) 0.819Chaenotheca phaeocephala Age 1 o0.001

Age2 � 0.001

Chrysothrix candelaris Age 1 o0.001 1 0.001

Age2 � o0.001 � 0.006

Cliostomum corrugatum Age 1 o0.001

Lecanographa amylacea Age (1) 0.087Pertusaria flavida Age 1 0.006 1 o0.001

Age2 � 0.027

Macrolichens (as a group) Age � o0.001

Table 3. Model coefficients and P-values for linear regression models for the total abundance (cm2 cover, 0–6m) of differentcrustose lichen species, using abundance data from the lowest 2m and tree diameter at breast height (dbh). SignificantP-values (o0.05) are written in bold.

Estimate SE P-value N Explained deviance (%)

Calicium adspersum Intercept 1.07 0.37 25 99.4Abundance o2m 1.00 0.021 o0.001

dbh � 0.031 0.0079 o0.001

dbh2 � 0.00021 0.000037 o0.001

Calicium salicinum Intercept 0.45 0.27 14 31.5Abundance o2m 0.24 0.10 0.037

Calicium viride Intercept 1.68 0.41 29 84.6Abundance o2m 0.89 0.073 o0.001

Chaenotheca phaeocephala Intercept 2.45 0.30 23 80.9Abundance o2m 0.68 0.072 o0.001

Chrysothrix candelaris Intercept 0.19 0.12 34 99.2Abundance o2m 1.04 0.017 o0.001

Cliostomum corrugatum Intercept 0.97 0.39 16 91.5Abundance o2m 0.90 0.074 o0.001

Lecanographa amylacea 3Pertusaria flavida Intercept � 0.32 0.30 31 90.8

Abundance o2m 0.89 0.067 o0.001

dbh 0.013 0.0029 o0.001

Detection probability and abundance estimation for lichens 337

rate data on species occurrence at the tree level.Moreover, this accuracy is not increased when usingbinoculars: not a single occurrence only representing2-6m above the ground was found when standingon the ground. Only one species, C. salicinum, hadrelatively low detection probability. One explana-tion is its very low abundance up to 6m (median0.9 cm2 per occupied tree) compared to the abun-dance of the other species (median of species-wisemedians: 99.6 cm2).

The detection probability when the lowermostparts of the trunk are surveyed should differamong epiphyte species, and should also depend onthe environment being studied. For instance, indense and tall forests, vertical gradients of moist-ure and light availability, in combination withsuccessional changes restrict several species tohigher levels in the canopy (e.g. McCune 1993;McCune et al. 1997; Lyons et al. 2000), obviouslyresulting in lower potential detection probabilityfrom the ground. Under more open conditions,such as oak pastures, the detection probabilityfrom the ground may differ between early and latesuccessional species. Late successional species (e.g.the crustose lichen species in this study) are likelyto occur and be found on the lower (oldest) parts of

the trunk (Table 5, discussion below), while thepopulation of earlier successional species maymove upwards on the trunk as the tree ages (He-denas & Ericsson 2000). This results in higherdetection probabilities from the ground for latethan for early successional species. This is for-tunate from a conservation point of view sincethreatened species are often confined to old trees(Berg et al. 1994) and thereby are late successional.The reason why they are threatened is that forestryremoves trees before they become old enough tohave become suitable for many late successionalspecies (Thor 1998; Fritz et al. 2008).

The detection probabilities presented may beoverestimates, because we only surveyed the trunkup to 6m, and the inner 0.5m of the branches.However, on the five recently wind-felled oaks wefound no occurrences above 6m of species that wereabsent on the lower 2m. Young parts of the tree (thetrunk area above 6m and branches) are likely to beless suitable for these species (see below), and there-fore we believe that such occurrences are rare.

Lichen abundance at different heights, in total, and itsrelationship with tree age

It is difficult to measure the total abundance ofepiphytic species on standing trees. Consequently,there is a need for abundance estimates based ondata measured solely from the ground. For five outof the eight study species, most (469%) of the to-tal abundance on the tree trunk up to 6m wasfound below 2m (Fig. 2). This suggests that theabundance below 2m alone constitutes a fairlygood estimate of total abundance. However, forthree species the proportion of the total abundancethat occurred above 2m increased with tree age(Table 2). This implies that, for old trees, the

Table 4. Spearman correlation coefficients between plotcharacteristics and height (n5 840). In the correlations,measures of plot area and bark fissure depth were calcu-lated as proportions of the mean for each tree. Formacrolichens and bryophytes, the percentage cover ineach plot was used. Significant P-values (o0.05) are writ-ten in bold.

Height P-value

Plot area � 0.90 o0.001

Bark fissure depth � 0.66 o0.001

Macrolichen cover 0.21 o0.001

Bryophyte cover � 0.04 0.24

Table 5. Likelihood ratio tests of relationships (Rel.) between lichen abundance and plot characteristics correlated to heightabove the ground based on ordinal regression models. Significant P-values (o0.05) are written in bold.

Height Bark Macrolichen Bark�height Variables included in all models

AreaConnectedness Tree ID

Rel P Rel P Rel P Rel P Rel P Rel P P

Calicium adspersum � NA � NA � 0.026 1 o0.001 � 0.058 0.929 o0.001

Calicium salicinum � NA � NA 1 0.025 0.110 0.366 0.279Chrysothrix candelaris � o0.001 1 o0.001 � 0.002 0.082 1 0.028 o0.001

Cliostomum corrugatum � 0.016 1 o0.001 0.186 1 o0.001 o0.001

Lecanographa amylacea � 0.006 � 0.040 0.329 0.126Pertusaria flavida � NA � NA 1 o0.001 1 o0.001 1 0.004 o0.001

Macrolichens 1 NA 1 NA � 0.015 0.633 1 o0.001 o0.001

338 Johansson, Victor et al.

abundance measures based on species cover ononly the lowest 2m might underestimate totalabundance more markedly. These estimates can,however, be improved by including dbh or someother age-related variable in the prediction model(Table 3).

Tree characteristics correlated to height and theirrelationship with lichen abundance

As expected, the abundance of most speciesdecreased with height above the ground (Fig. 2).This can be explained by decreasing substrate suit-ability up along the trunk: age-related factors, suchas bark fissure depth and bark area, are knownpredictors of lichen occurrence and abundance(e.g. Gustafsson et al. 1992; Gu et al. 2001;Johansson & Ehrlen 2003; Snall et al. 2004; Raniuset al. 2008; Fritz 2009; Johansson et al. in press),and these can be expected to change along thetrunk. Our results suggest (Table 2) that speciesthat are positively affected by age-related variablesestablish on the lower (oldest) parts of the trunkand then expand upwards as the tree ages. In con-trast to the crustose study species, the cover ofmacrolichens increased up along the trunk (Table4), indicating that young bark is more suitable forthis group of species.

The decline along the vertical gradient was, formost species, not only related to declining area, barkfissure depth and increasing cover of macrolichens.Some other not measured variable may also explainthe abundance decline with increasing height abovethe ground, e.g. changing moisture conditions alongthe vertical gradient (Harris 1971b). Some speciesmay grow closer to the ground because of greatermoisture availability e.g. due to reduced wind ex-posure. C. viride and C. phaeocephala, which wereboth unrelated to height above the ground, do exhibita positive correlation to sun exposure (Hultengren1995; Rydberg 1997). Therefore, these species may bemore tolerant to lower moisture conditions.

Conclusion

Surveys performed on only the lowest 2m of thetree trunk were sufficient to detect most occurrences,and to obtain fairly good estimates of total abun-dance (0-6m) of eight crustose lichens associatedwith old oaks. Four of these species are re-presentatives of crustose old oak specialists that allprobably have similar substrate requirements. Thissuggests that also other species in this group have

high detection probabilities. The result probablyalso applies to other lichens associated with old treesin open environments. However, different epiphyticspecies have different vertical distributions. There-fore, surveys of the lowest 2m of the trunk mayprovide poor estimates of occurrence and abun-dance on the whole tree, depending on species andsituation. For this reason, analyses of the verticaldistribution of the focal species should precede in-terpretation of data recorded on the lowest parts ofthe trunk. Information about the relationship be-tween substrate characteristics related to height(here e.g. bark fissure depth) and the distribution ofepiphytes can be helpful when predicting the verticaldistribution of the species.

Acknowledgements. Lena Gustafsson, Jens Astrom, Katja

Fedrowitz and Josefine Liew provided valuable comments

on the manuscript. We also thank the landowner, Henric

Falkenberg of Brokinds gods. Financial support came

from Formas (a grant to Thomas Ranius for the project

‘‘Evaluation of strategies to maintain lichen populations

connected to oak using metapopulation and landscape

modelling’’) and Stiftelsen Eklandskapsfonden i Linkop-

ings kommun (to Thomas Ranius). TS received financial

support from Formas.

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Received 5 March 2009;

Accepted 29 October 2009.

Co-ordinating Editor: Dr. Sara Cousins.

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