Influence of tree composition upon epiphytic ...

Influence of tree composition upon epiphytic macrolichens and bryophytes in old forests of Acadia National Park, Maine Author(s): Natalie L. Cleavitt, Alison C. Dibble, and David A. Werier Source: The Bryologist, 112(3):467-487. 2009. Published By: The American Bryological and Lichenological Society, Inc. DOI: http://dx.doi.org/10.1639/0007-2745-112.3.467 URL: http://www.bioone.org/doi/full/10.1639/0007-2745-112.3.467

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Influence of tree composition upon epiphytic macrolichens and bryophytes in old forests of Acadia National Park, Maine NATALIE L. CLEAVITT Department of Natural Resources, 8F Fernow Hall, Cornell University, Ithaca, NY 14853, U.S.A. e-mail: [email protected] ALISON C. DIBBLE School of Biology and Ecology, 119 Deering Hall, University of Maine, Orono, ME 04469, U.S.A. e-mail: [email protected] DAVID A. WERIER 30 Banks Road, Brooktondale, NY 14817, U.S.A. e-mail: [email protected] ABSTRACT. To better understand associations between epiphytes and old forests, lichens and bryophytes that grow on tree bark were quantified in relatively undisturbed stands of Acadia National Park (ACAD). Four plots were dominated by hardwoods and eight by spruce. To obtain data from upper boles, we climbed four maple trees per plot (eight plots) and four spruce trees per plot (four of the eight plots). We found 85 macrolichen species and 62 bryophyte taxa (60 species, two varieties). Eight macrolichens are newly documented from ACAD. At the state-level, Acadia NP plots were notably species-rich including 15 species not found in 50 other plots in Maine surveyed using the USDA FS Forest Inventory and Analysis Program (FIA) lichen protocol. At the plot-level, the epiphyte flora of spruce-dominated plots differed significantly from that of hardwood-dominated plots, although species richness was comparable. At the tree-level, the epiphyte flora of maple trees was significantly influenced by tree composition within the surrounding stand. Mixed composition of tree species in the stand correlated with higher epiphyte diversity. Cyanolichens were more likely to occur on large hardwood trees in hardwood-dominated plots. Fruticose lichen occurrence was influenced by interactions between tree size, plot and tree species. Using comprehensive tree tally searches in combination with climbing of four maples per plot, we found that we missed an average of 15% of the macrolichen flora in the search area using only the two-hour timed survey required by the FIA protocol. This study serves as an important baseline for detecting future changes in the epiphyte flora of ACAD and further highlights the importance of mature mixed stands to epiphyte conservation in northern forests of eastern North America. KEYWORDS. Acadia National Park, Maine, bryophyte, macrolichen, FIA, tree composition, epiphytes, conservation.

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The Bryologist 112(3), pp. 467–487 Copyright E2009 by The American Bryological and Lichenological Society, Inc.

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Lichen and bryophyte epiphyte assemblages have drawn curiosity since the mid 1900s (e.g., Barkman 1958; Culberson 1955; Hale 1952, 1965; Oksanen 1988). These early studies established the broad framework of factors that may influence epiphyte occurrence including climate, plot factors such as microclimate, light availability and moisture regime, tree species, bark chemistry and texture, tree age and size and height on the tree bole. Later studies explored the relative importance of tree species, forest composition and climate to epiphyte assemblages (Adams & Risser 1971; Oksanen 1988; Palmer 1986; Studlar 1982). The general conclusion from these studies was that epiphytes sort out along gradients of bark chemistry and moisture regimes and are not specific to a given tree species. However, the importance of a given variable was reliant largely on either the gradients included or the scale of the studies. For instance, Studlar (1982) found evidence of specificity to tree species in a limited region of Virginia, while Palmer (1986) found importance of bark chemistry irregardless of tree species over a broader geographic region. Adams and Risser (1971) found rainfall to be the major determinant in an area with a sharp precipitation gradient. In a recent study examining several scales (within regions and across regions), the fidelity of the epiphyte indicator upon a given tree species was found to be scale-dependent shifting depending on the landscape-scale analysed (Will-Wolf et al. 2006). Most recent studies of epiphytes have focused largely on the effects of stand age (e.g., Neitlich & McCune 1997; Root et al. 2007b; Selva 1994) and air pollution on epiphyte assemblages (e.g., Bates 1992; Farmer et al. 1991; Gauslaa 1995). Two groups of macrolichens have repeatedly been recognized as ‘‘sensitive’’ to both disturbances by forest management and air pollution: epiphytic fruticose lichens (e.g., Usnea, Bryoria, Ramalina, etc.) and cyanolichens (e.g., Lobaria, Collema, Leptogium, etc.). Epiphytic fruticose lichens tend to reach higher abundances in conifer-dominated forests and are indicators of both air quality (Gilbert 1970; Otnyukova 2007; Zambrano-Garcı´a et al. 2000) and stand age (Boudreault et al. 2002; Neitlich & McCune 1997; Selva 1994). Cyanolichens are sensitive to substrate pH and generally require bark close to pH

5.0 (Farmer et al. 1991; Gauslaa 1995; Goward & Arsenault 2000; Richardson & Cameron 2004), which makes them particularly sensitive to air pollution effects because of acidification. In addition, they are important indicators of advanced stand age in mixed and hardwood-dominated forests (Selva 1994; Sillett & Neitlich 1996). Glenn et al. (1998) noted that the overlaying of air pollution effects may disrupt the usefulness of epiphytes as indicators of forest integrity. Indeed, given the complexity of factors affecting epiphyte assemblages, the most defendable use of epiphytes as indicators of forest integrity would require plotspecific baseline data from which to evaluate the magnitude and direction of future change (Poikolainen et al. 1998). One of the key aims of our work was to provide such a baseline for understanding epiphyte floras and for documenting change in epiphyte distribution in Acadia National Park (ACAD), Maine. In addition to providing a baseline, we used a unique combination of timed ground-level, complete ground-level and vertical tree surveys to examine partitioning of epiphyte diversity and the relationship between species composition and measured plot or tree variables. Our methodology allowed a comparison to protocols used for the lichen indicator at Forest Health Monitoring Plots in the nation-wide Forest Inventory and Analysis (FIA) program (USDA 1999). Specific questions we addressed included: 1) Does species richness of epiphytes at the plot-level increase with frequency of hardwood trees, particularly Acer. spp.? 2) Is treelevel epiphyte composition on maples affected by the plot-level tree composition, particularly dominance of conifer or hardwood trees? 3) What are the predictors for sensitive species occurrence, specifically cyanolichens and fruticose lichens? 4) Are some species found mostly above 2 m high on the trees? 5) How do ACAD plots compare and contrast with other FIA plots in Maine? 6) How efficient is the two-hour timed epiphytic lichen survey used by FIA in capturing total lichen species richness?

METHODS All primary study plots are in Acadia National Park (ACAD), Hancock County, Maine (Fig. 1

Cleavitt et al.: Epiphyte ecology in Maine

Figure 1. Location of plots used in plot-level ordination of macrolichen composition in forests of Maine. Plots are coded as: circles for Maine FIA plots, square for the Bear Brook plots (10 plots in close juxtaposition) and triangles for plots in Acadia National Park (ACAD). Plots that have . 50% hardwoods are shown with closed symbols and those with . 50% conifers with open symbols. The expanded inset shows our 12 study plots in ACAD on Mount Desert Island, Maine using the same plot coding.

inset). In 2005, eight red spruce (Picea rubens)dominated plots were selected to include a range of atmospheric deposition inputs based on data of Weathers et al. (2006). Weathers et al. (2006), who took throughfall measurements of sulfur and nitrogen at 285 plots in ACAD on 7 Jun–18 Sep 2000. We were provided with their plot information including precise GPS locations and annual deposition at each plot. We were then able to select four paired plots in spruce-dominated forests of ACAD. The plots were paired by proximity with one plot having relatively lower annual sulfur deposition (6.2–10.8 kg/ha/yr) and the other plot having relatively higher sulfur deposition (15.6–23.6 kg/ha/ yr). Surprisingly, we did not find compositional differences to correlate to throughfall deposition

469

levels of sulfur (Cleavitt, unpublished data). Therefore in 2006, we broadened the study to include four hardwood-dominated plots that had not burned during an extensive fire in 1947 (Table 1). The extent of hardwood-dominated forest in ACAD is much more restricted than conifer-dominated forest within ACAD, and we limited our plots to mature forests that were in some proximity to our existing study plots (Fig. 1). Important hardwoods on all 12 plots included maple species (red maple, Acer rubrum, and some sugar maple, A. saccharum, on hardwooddominated plots) and birch species (Betula alleghaniensis, B. papyrifera, B. cordifolia) (Table 2). American beech (Fagus grandifolia) was the prevalent hardwood at the hardwood-dominated plots D1–D3. All study plots were circular with a 34.7 m radius and 0.38 ha area. Plot locations and elevations were recorded at plot center with a Magellan SporTrak Pro GPS unit. Plot center and one boundary point are marked permanently with large plastic, orange survey stakes. We conducted epiphyte surveys of the macrolichens according to a modification of the Forest Inventory and Analysis (FIA) lichen monitoring protocol as described in McCune et al. (1997a). This modification simply allows use of circular study plots, which is less complex than the full FIA plot setup. Within each plot, two-hour timed surveys were conducted to document presence/ absence of macrolichen species that were on woody substrata: above 0.5 m from the ground on live and dead tree boles and shrubs, and on the ground over recently fallen boles, branches and twigs (McCune et al. 1997a; USDA 1999). Voucher specimens were made for each new species (specimens will be deposited at COA) and abundance ratings were assigned based on the frequency of lichen occurrence (scale of 1–4 used by FIA protocol; USDA 1999, 2004; Appendix A). To complement the lichen surveys, a one-hour survey for bryophyte epiphytes was also conducted in the plots. The two-hour lichen surveys at the eight spruce-dominated plots were conducted twice, once in 2005 and again in 2006. Identifications of difficult lichen specimens were verified by experts. Nomenclature for lichens follows Hinds and Hinds (2007; which retains Melanelia sensu lato). Nomenclature for bryophytes follows

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Table 1. Characteristics for 12 sites at Acadia National Park, Maine, that were used in an ordination of sites by macrolichen species composition for timed survey data only (see Fig. 2). A complete list of species for each site is provided in Appendix A. Sites in bold were further used in the tree-level surveys.

Location name

Site code

Western Mt.

11

Western Mt.

18

Hadlock Bk.

66

Hadlock Bk.

67

Sargent Mt.

160

Sargent Mt.

162

Pemetic Mt.

284

Pemetic Mt.

285

Hadlock Bk.

D1

Bubble Pond

D2

Bubble Rock

D3

Amphitheatre

D4

UTM zone 19 NAD 83 550966E 4906137N 550054E 4905698N 557797E 4909201N 557639E 4909074N 557646E 4906720N 557685E 4906943N 560164E 4909631N 560189E 4909819N 557530E 4909064N 561078E 4909094N 559661E 4910214N 558215E 4907887N

Tree Elevation density (m) (stems ha21)

Hardwood (%)

Macrolichen richness

Cyanolichen (%)

Fruticose Bryophyte (%) richness

287

2278

8.6

32

0

307

1897

0.5

32

0

9.8

4

262

1140

13.9

36

1.4

6.5

23

211

1024

26.6

38

2.3

12.4

26

104

1939

30.8

35

2

39.4

23

148

1664

27

40

2.8

19.4

18

359

1526

27

38

0

11.1

22

338

1373

20.8

34

0

6.3

11

198

1399

61.8

40

10.8

2.3

34

128

1167

86.6

33

10.2

0.5

30

135

1503

82

30

20

0.5

27

96

1093

50.8

33

14.3

6.8

31

Crosby et al (1999) for mosses and Schuster (1966– 1992) for liverworts. In addition, at all 12 plots (Table 1) we tallied all trees . 2 cm diameter at breast height by species and size class (5 cm interval), and noted canopy position, whether or not the crown was associated with a gap, extent of crown breakage or dieback (if . 50% the tree branches were not foliated then the tree was tallied as unhealthy), as well as presence of cyanolichens and fruticose lichens. During these complete tree tallies, macrolichens new to the plot list were also noted and rated for abundance in the plot. Complete tree tally surveys allowed for examination of predictors for the presence of cyanolichens and fruticose lichens as well as providing valuable tree composition data for the plots. The predictability of occurrence for sensitive lichen taxa, cyanolichens and fruticose lichens, was

14

10

examined using logistic regression. In the results section we provide the Wald statistic, which is a test of significance of the regression coefficient and is tested against the Chi-square distribution. The regressions were run using conditional forward selection from a full model of tree characters in SPSS version 15.0. In addition, on the eight cyanolichen plots (bolded in Table 1), tree-specific lichen and bryophyte data were collected for four maple trees . 20 cm diameter at breast height (DBH). At the four spruce-dominated plots, four spruce trees . 20 cm DBH were also surveyed. For each tree, a complete survey of macrolichens was conducted around the bole at 0.5–1.5 m height. In this area, abundance of each species was rated on a 6 point scale: 1) 1–4 thalli; 2) 5–10 thalli; 3) 11–20 thalli; 4) 21–30 thalli; 5) 31–50 thalli; 6) . 50 thalli. These data are referred


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Table 2. Basal area by tree species and total basal area across sites, with a summary of additional parameters by site from the tree tally surveys at eight sites in Acadia National Park, Maine. Acer spp. included A. saccharum and A. rubrum; Betula spp. included B. alleghaniensis, B. papyrifera and B. cordifolia. Other hardwoods included: Acer pensylvanicum, Sorbus americana, Amelanchier spp., Populus grandidentata and unspecified dead standing boles. Other conifers included: unspecified dead standing boles. Site: Basal area by tree taxa (m2/ha): Abies balsamea Acer spp. Betula spp. Fagus grandifolia Fraxinus americana Picea rubens Pinus strobus Thuja occidentalis Tsuga canadensis Other conifers Other hardwoods Dead unknown Total Density (tree # per plot) Trees in gaps (%) Dead trees (%) Unhealthy trees (%) Dominant/co-dominant trees (%)

D1

D2

D3

0.09 7.44 5.76 6.61 0.10 2.98

0.21 6.00 2.49 10.03 1.07 0.66

5.53 4.45 8.61 0.47 2.05

2.76 0.79

0.86

23.77

24.09

529 20.2 15.5 12.9 20.8

372 5.6 19.4 9.9 23.9

to as the ‘‘total abundance survey.’’ Abundance and diversity were also quantified by marking the circumference starting at due west at 1.5 m height, and tallying all lichens every centimeter around the circumference of the tree, such that the number of total tallies varied with the girth of the tree. These data are referred to as the ‘‘circumference survey.’’ The same maples were also climbed for tree bole surveys to two-thirds of tree height and these data are referred to as ‘‘canopy surveys’’ to distinguish them from lower bole surveys even though they are not comprehensive canopy surveys. Tree heights were taken using a digital hypsometer. Trees were climbed using a closed rope system with mechanical ascenders. When climbing, we did not go beyond the two-thirds height nor out on the limbs of the trees for safety reasons. Plot checklists (Appendix A) were made from a combination of two-hour plot surveys, plot tree tally surveys and the three categories of climbed tree surveys (cyanolichen plots only). Species and environmental data were analyzed using Non-metric Multidimensional Scaling (NMS) in PC-ORD (ver. 4.27). The NMS analysis is an

D4

66

67

0.32 2.56 0.68

0.16 4.77 1.96 0.08

1.71 5.37 2.32

1.37 6.18 0.66

35.15

26.76 0.18

16.47 2.20 0.02

17.70 1.56 1.33

1.07

0.91 8.73 5.84 0.12 5.60 1.34 1.52 2.60 0.13

1.02 0.07 23.29

0.31 0.08 27.17

0.02 0.02

0.07 0.04 0.01 34.03

0.23 0.51 0.05 28.90

0.65 0.35

495 20.4 18.4 8.3 27.5

415 14.9 13.5 16.6 29.2

38.75 394 11.9 25.4 15.5 41.9

384 7.0 13.8 17.2 45.6

160

709 10.9 15.5 16.9 35.3

162

29.78 622 11.9 16.1 11.1 35.4

ordination method that uses an iterative search for rankings and placement of the analyzed variables to find the solution which minimizes stress (McCune & Mefford 1999). Because NMS uses ranks, it can be considered a non-parametric form of ordination with relaxed assumptions on data structure that are usually more applicable to ecological data (McCune & Mefford 1999). All NMS analyses were run using Sorensen’s distance measure with 40 runs using real data and 50 runs of randomized data. The instability criterion was 0.00001 with 400 as the maximum number of iterations. The final solution was chosen based on the dimensionality with the lowest mean stress from a run comparing randomized to real data (McCune & Mefford 1999). The indicator value of species for conifer- and hardwood-dominated forests at three scales was examined using Indicator Species Analysis in PC-ORD. This analysis uses the relative frequency and abundance of species in a pre-defined grouping (here conifer- or hardwood-dominated forest) to calculate an indicator value for each species. The significance of this indicator value is then determined through comparison with indicator

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values obtained from data randomization. We used the default settings of random seed number based on time of the run and 1000 randomizations (McCune & Mefford 1999). Three ordinations of species composition patterns were run: 1) Plot-level, ACAD plots only: 12 plots with complete plot-level lichen and bryophyte data; 2) Tree-level: four maple trees on each of eight of the ACAD plots (32 trees) with both lichen and bryophyte species included; and 3) Plot-level, Mainewide: data set of 62 plots in Maine where macrolichens only were surveyed using the FIA protocol. The first ordination was run to examine which plot variables best explained the differences in epiphyte species composition of the ACAD plots. Specifically, how does stand dominance affect epiphyte composition of the plot? Variables used as overlays for the plot-level species patterns included tree density (number of trees), percent hardwoods (by stems), lichen richness, percent of species that were cyanolichens, percent of species that were fruticose lichens and elevation (m). These variables are independent of the species composition pattern itself and are used to look at correlation of environmental variables to the existing patterns. The second ordination was run to examine how tree-level variables corresponded to differences in epiphyte composition. In particular, how does stand composition affect tree-level epiphyte composition? Variables used as overlays in the NMS analysis for the tree-level species composition patterns included tree height (m), circumference (cm) at 1.37 m from ground, number of canopy epiphyte species, number of fruticose lichen species, number of species in the circumference sample, total number of species for tree, abundance survey at tree base (0.5–1.5 m bole survey with abundance ratings) and plot location. The third ordination sought to provide a context for the ACAD plots compared to samples from elsewhere across forested areas of Maine. We used the publicly available FIA lichen data for Maine available online at http://fia.fs.fed.us/. This data set included 41 plots with macrolichen collections. In addition, we entered published data for the 10 reference plots in the Bear Brook watershed, Hancock Co., Maine (Eckhoff & Wiersma 2002) that were sampled using the FIA protocol except that distance between plots

was much closer than standard FIA plots. During exploratory analysis, one of the Maine FIA plots was excluded as an outlier with very low richness. Therefore the final NMS analysis included the 12 ACAD plots, 10 Bear Brook plots and 40 FIA plots for a total of 62 plots (Fig. 1). Plot information available for all the plots included percent hardwoods, elevation, and approximate latitude and longitude.

RESULTS Plot-level surveys. A total of 147 taxa of epiphytes were found on the 12 plots in ACAD. These included 85 macrolichen species and 62 bryophyte taxa (60 species, 2 varieties) (Appendix A). In hardwood-dominated plots, bryophytes comprised an average of 44% of the epiphyte diversity, while in spruce-dominated plots they comprised 29% and were much less abundant (Appendix A). Of the 12 plots, the highest epiphyte diversity was on plot D1 with 82 species, while the lowest was on plot 18 with 39 species. Four of the spruce-dominated plots did not have any cyanolichens, while two of the deciduous plots had fruticose lichens present on only 0.5% of the trees (Table 1). The following eight species of macrolichens are additions to the most recent list of lichens for ACAD (Sullivan 1996): Candelaria concolor, Hypotrachyna afrorevoluta, H. revoluta, Parmelia fertilis, Parmotrema reticulatum, Physconia leucoleiptes, Usnea glabrescens and U. subscabrosa. There was no strong correlation between lichen species richness in a plot and frequency of hardwood trees; however, there was a significant difference in lichen species composition between plots (Fig. 2). Macrolichen species richness at the plot-level based on two-hour survey data was 30–40 species (Table 1: note Appendix A; this was increased to 34–50 species with additional survey data). Species richness in the hardwood-dominated plots was comparable to that of the conifer-dominated plots. Among hardwood plots, highest diversity was in plots that had about 25–30% conifers (Table 1). The hardwooddominated plots had a higher percentage of trees with cyanolichens and a lower percentage of trees with fruticose lichens. In direct contrast, sprucedominated plots were generally low in cyanolichens,


473

Table 3. Correlations of site characters to Axes for ordination of sites (N5 12). Significance of the correlation coefficients are shown by: * p , 0.05 and ** p , 0.005. The corresponding ordination is shown as Fig. 2.

Figure 2. Ordination of 12 plots by species composition from timed-surveys of epiphytes. Plots labeled as in Table 1. Plot traits that were significantly correlated to the axes are shown as vectors that increase in the direction of their labels. Abbreviations are: fruti 5 percent of trees with fruticose lichens, tree den 5 tree density, elev 5 plot elevation, cyano 5 percent of trees with cyanolichens, and hardwood 5 percent hardwoods. The percent variation explained is given in parentheses beside each axis label. Further details relating to this ordination are given in Tables 2–4.

but higher in fruticose lichens; their lichen richness was higher overall if hardwoods comprised at least 25–30% of the stand. Hence, mixed stands harbored the highest macrolichen diversity at these plots. The NMS ordination explained 98.4% of the variability in the macrolichen flora between plots (Fig. 2). The ordination had low stress and instability (2.89 5 final stress for 2-dimensional solution; 0.00001 5 final instability) indicating a robust ordination. The percent of hardwood trees and the number of trees with cyanolichens were the two strongest correlates to the patterns found in the macrolichen species composition (Table 3). Twentyone macrolichen taxa were exclusive to the coniferdominated plots. While macrolichen diversity was comparable between the two stand types, bryophyte diversity was much higher in the hardwooddominated plots, as evidenced by the greater number of bryophyte species that were associated with hardwoods (Table 4) than those that were strongly associated with conifers. Predicting presence of sensitive species. Tree distribution varied by plot for the eight plots where the presence of sensitive species, i.e., cyanolichens

Axis 1

Axis 2

Site trait

Pearson’s r

Pearson’s r

Tree density Percent hardwood trees Percent of trees with cyanolichens Percent of trees with fruticose lichens Species richness Site elevation

20.605* 0.864** 0.809** ns ns 20.825**

0.662* 0.897** 0.772** 20.691* ns ns

and fruticose lichens, were examined (Table 2). For ACAD plots 66, 67, 160 and 162, red spruce (Picea rubens) comprised over half of the basal area and percent of hardwoods was lowest for plot 66 (Tables 1, 2). For plots D1–D3, the dominant species was American beech (Fagus grandifolia), which in ACAD and much of Maine is heavily impacted by beech bark scale disease complex (Nectria spp.). Other important tree species in the plots were red maple, sugar maple, yellow birch, paper birch and white ash (Fraxinus americana) (Table 2). Conifers were typically present, especially red spruce with northern white cedar (Thuja occidentalis) important at plot D4. Cyanolichen species encountered on the plots were: Collema subflaccidum, Dendriscocaulon intricatulum, Leptogium cyanescens, Lobaria pulmonaria, L. quercizans, L. scrobiculata, Nephroma parile, Protopannaria pezizioides, Parmeliella triptophylla and Peltigera spp. (Appendix A). Cyanolichens occurred mainly on hardwood tree species, but some also occurred on cedar (Thuja occidentalis). Therefore, red spruce and balsam fir trees were not included in the analysis. The cyanolichen analyses included data for 1,843 trees. Cyanolichen occurrence was best predicted by a model including the interaction between tree size and species (Wald 5 53.6, df 5 6, p , 0.001; Fig. 3a), tree size (Wald 5 36.3, df 5 1, p , 0.001) and plot (Wald 5 47.3, df 5 7, p , 0.001; Fig. 3b) (overall model: X2 5 485.621, df 5 14, p , 0.001; 86.5% correctly predicted). For most tree species with

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Table 4. Indicator species for conifer- and hardwood-dominated sites based on FIA plot-level surveys for macrolichens and bryophytes at 12 study sites in Acadia National Park, Maine. Indicator values are derived from the relative frequency and abundance of species in each forest type (calculated using Indicator Species Analysis in PC-ORD). P-values indicate significantly higher indicator value than randomized data. Only species with p-values of # 0.051 are shown here. Conifer forest indicators Species

Indicator value

Bryoria furcellata Everniastrum catawbiense Evernia mesomorpha Hypogymnia krogiae Hypogymnia physodes Hypogymnia tubulosa Imshaugia aleurites Parmelia saxatilis Platismatia glauca Platismatia tuckermanii Tuckermanopsis spp. Usnea subfloridana

100 100 76.9 79.3 66.7 85.2 88.2 79.9 82.4 84.6 75 100

Hardwood forest indicators p

Species

Indicator value

p

100 76.9 80 83.3 86.7 92.3 60.4 94.7

0.003 0.036 0.014 0.007 0.013 0.008 0.036 0.004

100 75 75 85.7 81.2 87.5 75 92.3 100 77.4 80

0.003 0.02 0.019 0.013 0.011 0.006 0.02 0.003 0.003 0.035 0.031

Macrolichens 0.003 0.003 0.006 0.008 0.003 0.003 0.003 0.019 0.003 0.003 0.051 0.003

Collema subflaccidum Lobaria quercizans Melanelia subaurifera Parmotrema crinitum Phaeophyscia rubropulchra Physconia detersa Punctelia rudecta Pyxine sorediata

Bryophytes Ptilidium pulcherrimum

87.9

0.003

cyanolichens present, cyanolichens were more likely to be found on the larger trees (Fig. 3a). For striped maple (Acer pensylvanicum) and red maple, tree size was less useful as a predictor of cyanolichen occurrence. There was little variation in size for striped maple, which rarely grows to more than about 15 cm DBH. There was great variation in size of red maple trees where cyanolichens were absent (Fig. 3a). Cyanolichens were more likely to occur on trees in plots D3 and D4 (Fig. 3b). Fruticose lichens seen were: Bryoria furcellata, B. nadvornikiana, B. trichodes, Evernia mesomorpha, Pseudevernia consocians, P. cladonia, Ramalina americana, R. intermedia and 11 species of Usnea (Appendix A). Fruticose lichens did not occur with enough frequency on two of the deciduous plots (D2 and D3); therefore the analysis included six plots and

Anomodon attenuatus Leskeella nervosa Leucodon andrewsianus Metzgeria furcata Neckera pennata Orthotrichum sordidum Orthotrichum speciosum Porella platyphylla Pterigynandrum filiforme Pylaisia intricata Thuidium delicatulum

2,764 trees. Fruticose lichen occurrence was best predicted by a model including the interactions between tree size and plot (Wald 5 21.3, df 5 5, p 5 0.001; Fig. 4a), tree size and tree species (Wald 5 56.1, df 5 8, p , 0.001; Fig. 4b) and tree species and plot (Wald 5 74.3, df 5 31, p , 0.001; Figs. 4c, d) (overall model: X2 5 654.512, df 5 44, p , 0.001; 85.1% correctly predicted). The number of trees with fruticose species present was highest at plots 160 and 162 (Fig. 4c). There were nine tree species with fruticose lichens present with red spruce, balsam fir, red maple, paper birch and eastern white pine (Pinus strobus) as the most frequent hosts of fruticose lichens (Fig. 4d). As with the cyanolichens, the fruticose lichens tended to occur on larger trees; however, tree size was only a significant predictor at plot 160 where a


Figure 3. Differences in occurrence of cyanolichens found in full tree tallies at 8 plots in ACAD. A. Box plots of tree size differences for the seven tree species with cyanolichens; white boxes for trees lacking cyanolichens and gray boxes for trees with cyanolichens. Tree species are abbreviated by the first two letters of their genus and species. B. Bar graph of the percentage distribution of trees without (white) and with cyanolichens (gray) across the eight plots for the same tree species included in above graph (i.e., only species with some cyanolichens present were included).

greater percentage of trees had fruticose lichens on them (plot 3 tree size: Fig. 4a, c). Size was a significant predictor for the most important tree species hosting fruticose lichens, but not for tree species where fruticose lichen occurrence was infrequent (tree size 3 tree species: Fig. 4b, d). The tree species useful in predicting presence of fruticose species varied by plot. The three species significant for higher fruticose occurrence across plots were Picea rubens, Abies balsamea and Acer rubrum (plot 3 tree species: Fig. 4d). Other descriptive variables that were not included in the final models because of lack of significance were tree position in the canopy, health of the tree (dead, healthy, unhealthy) and whether the tree was growing into a canopy gap (Table 2). Plots D1 and D3 had highest percent of trees in

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canopy gaps (both 20%) while plots D2 and 67 were lowest (5.6 and 7%, respectively). The percent of dead trees was fairly even across the plots (average 6 1SD: 17.2% 6 3.9) with the highest percentage dead at plot 66 (25.4%). The conifer-dominated plots had a more even canopy structure than the deciduous-dominated plots with 40% of the trees dominant or co-dominant at conifer plots compared to around 25% in these two classes at deciduous plots (Table 2). Tree-level patterns. Tree-level epiphyte species richness was higher for maple trees than spruce (maples in conifer stands: 15.4 6 3.2; maples in deciduous forest: 15.3 6 2.4; spruce in conifer stands: 11.2 6 2.5) and this difference could be explained by higher bryophyte diversity on maples relative to spruce. On average, bryophytes accounted for 46% of epiphyte species richness on maples compared to only 8% on spruce. Diversity of epiphytes (including bryophytes and lichens) on maples did not differ by tree composition within the stand. The NMS ordination positioning the 32 climbed maple trees based on their epiphyte species assemblages identified a strong pattern in tree-level composition with separation of trees by canopy dominance (Fig. 5; 16.14886 5 final stress for 2dimensional solution; 0.00007 5 final instability). The axes explained a total of 83.2% of the variation in the data (Fig. 5). Tree height (r 5 0.658, p , 0.001) and circumference (r 5 0.586, p , 0.001) were significantly correlated to ordination Axis 1, and no measured tree characters were correlated to the second axis (Fig. 5). Axis 2 may represent a light gradient based on knowledge of environmental preferences of the species correlated to this axis (data not shown). Epiphytes that can be interpreted as significant indicators of deciduous-dominated stands at both the plot and tree scales were three mosses, Anomodon attenuatus, Neckera pennata and Orthotrichum sordidum; two liverworts, Metzgeria furcata and Porella platyphylla; and five macrolichens, Lobaria quercizans, Melanelia subaurifera, Phaeophyscia rubropulchra, Punctelia rudecta and Pyxine sorediata (Tables 4, 5). Although only lichens on maple boles were included in this analysis, there were three macrolichens that resolved as significant indicators of conifer-dominated forests at both the plot and tree-

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Figure 4. Fruticose lichen species occurrence at six study plots in ACAD. A. Boxplot of tree size by plot showing the difference for trees with (gray) and without (white) fruticose lichen species. B. Boxplots of tree size by tree species showing differences for trees with (gray) and without (white) fruticose lichen species. C. Bar graph of the number of trees with (gray) and without (white) fruticose lichen species by plot. D. Cumulative percent bar graph showing relative importance of tree species for fruticose lichen occurrence by plot. Tree species are abbreviated by the first two letters of their genus and species.

Figure 5. Ordination of individual trees by macrolichen species composition with spruce-dominated plots shown by filled symbols and hardwood-dominated plots shown by open symbols. Tree height and circumference were significantly, positively correlated to Axis 1. The percent variation explained is given in parentheses beside each axis label. There is clear separation between the epiphyte floras of maple trees depending on tree composition in the stand.

level: Hypogymnia physodes, Imshaugia aleurites and Platismatia glauca (Tables 4, 5). Species richness (r 5 0.251, p . 0.05) was not related to overall patterns in the epiphyte data. Several tree variables were correlated with one another (average values given in Table 6). Tree height and DBH were positively correlated (r 5 0.742, p , 0.001). Tree-level species richness of macrolichens was positively correlated to DBH (r 5 0.423, p 5 0.02), number of canopy lichen species (r 5 0.781, p , 0.001), number of fruticose species (r 5 0.396, p 5 0.03) and sum of abundance scores from the lower bole survey (r 5 0.594, p , 0.001). The number of canopy lichen species was positively correlated to tree height (r 5 0.489, p 5 0.004), the number of fruticose species (r 5 0.544, p 5 0.002) and tree DBH (r 5 0.443, p 5 0.01). The number of species detected in the circumference sample was positively correlated to the sum of abundance scores from the lower bole survey (r 5 0.585, p , 0.001).


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Table 5. Indicator species for conifer- and hardwood-dominated sites based on single-tree surveys for macrolichens and bryophytes on maple trees at eight study sites in Acadia National Park, Maine. Indicator values are derived from the relative frequency and abundance of species in each forest type (calculated using Indicator Species Analysis in PC-ORD). P-values indicate significantly higher indicator value than randomized data. Only species with p-values of # 0.051 are shown here. Melanelia spp. includes M. exasperatula, M. fuliginosa and M. halei. Conifer matrix indicators Species

Hardwood matrix indicators

Indicator value

p

Species

78.5 65.6 50 31.2 41.6 100

0.001 0.001 0.002 0.043 0.014 0.001

Indicator value

p

38.3 29.8 35.9 81.2 18.7 41.4 62.5 50 25

0.003 0.006 0.003 0.001 0.031 0.014 0.001 0.024 0.012

18.7 72.5 25 18.7 30 18.7 73 18.7 80.6

0.022 0.001 0.008 0.029 0.007 0.042 0.001 0.04 0.001

Macrolichens Cladonia squamosa Hypogymnia physodes Imshaugia aleurites Parmeliopsis capitata Platismatia glauca unidentified crustose spp.

Flavoparmelia caperata Lobaria quercizans Melanelia spp. Melanelia subaurifera Parmelia fertilis Parmelia sulcata Phaeophyscia rubropulchra Punctelia rudecta Pyxine sorediata Bryophytes Anomodon attenuatus Frullania eboracensis Hypnum pallescens Metzgeria furcata Neckera pennata Orthotrichum sordidum Platygyrium repens Porella platyphylla Ulota crispa

Comparison to Bear Brook and Maine FIA data. This comparison includes only two-hour timed survey macrolichen data, including our data from ACAD. The final NMS solution described a threedimensional ordination explaining 85.7% of the

variation in the data sets (Fig. 6). Axis 1 was significantly correlated to plot elevation (r 5 0.498, p , 0.001) and latitude (r 5 0.592, p , 0.001) (Fig. 6). Axis 2 was significantly correlated to the percent of hardwoods in the plot (r 5 0.834, p ,

Table 6. Maple (Acer spp.) tree variables summarized by site (N 5 4) in terms of mean and standard deviation (in parentheses). Tree height and DBH were the only significant differences between sites and only tree height had significant post-hoc subsets indicated by superscript letters beside the mean values. The tree-level data are used in the ordination shown in Fig. 5.

Site D1 D2 D3 D4 66 67 160 162

Tree height (m) 18.50b 20.48b 18.38b 19.00b 14.05a 18.88b 14.15a 14.03a

(1.12) (3.27) (0.74) (1.82) (2.50) (1.47) (0.93) (0.62)

DBH (cm) 39.49 (3.33) 42.28 (6.26) 38.12 (4.91) 42.68 (11.08) 32.52 (2.27) 36.62 (4.00) 30.57 (5.84) 28.66 (7.38)

Species only in Species in Sum of canopy Fruticose species circum-sample Total species abundance scores 6.50 9.50 8.75 9.25 6.25 7.00 4.75 8.50

(2.38) (2.65) (2.36) (5.38) (0.96) (3.65) (3.10) (4.04)

1.75 1.25 2.25 2.25 0.75 1.00 2.50 2.00

(0.50) (0.96) (0.50) (1.71) (0.96) (1.41) (2.08) (0.82)

7.00 6.00 7.25 6.00 9.50 5.75 8.00 6.25

(2.16) (2.16) (1.50) (2.16) (1.73) (1.71) (2.58) (1.71)

21.75 (1.50) 24.5 (3.70) 24.25 (3.77) 24.50 (7.05) 24.25 (3.59) 22.00 (7.35) 19.00 (2.45) 22.25 (6.95)

43.75 (2.87) 42.50 (2.89) 44.00 (10.23) 46.25 (6.18) 49.25 (9.91) 40.00 (9.35) 44.25 (7.41) 38.50 (10.47)

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Figure 6. Ordination of 62 plots in Maine surveyed using the FIA two-hour timed survey macrolichen protocol with plots coded into five groupings (see legend). The top ordination shows the solution for axes 1 and 2, and the bottom ordination shows axes 1 and 3. The percent variation explained is given in parentheses beside each axis label.

0.001). Axis 3 was significantly correlated to longitude (r 5 0.597, p , 0.001). At the plot-level across Maine, percent of hardwoods in the stand was the most significant variable relating to macrolichen species composition. On average, macrolichen species richness on Bear Brook and the Maine FIA plots was considerably lower than on our plots (20.4 6 5.8 species; range 6– 34; compare with Table 1). Fifteen species found in 12 ACAD plots were absent from other plots in Maine surveyed with the FIA two-hour timed search (50 plots): Cladonia coniocraea, C. cenotea, C. pleurota, Dendriscocaulon intricatulum, Everniastrum catawbiense, Heterodermia obscurata, Hypotrachyna afrorevoluta, Melanelia fuliginosa, M. halei, Normandina pulchella, Parmotrema crinitum, P.

perlatum, P. reticulatum, Ramalina intermedia and Usnea ceratina. Conversely, 24 species occurred on the Bear Brook and Maine FIA plots that were not found in our ACAD plots; however, because we sampled a much smaller number of plots this was to be anticipated. Only ten of these 24 species are not on the full ACAD list (Sullivan 1996): Candelaria fibrosa, Leptogium burnetiae, L. milligranum, L. saturninum, Flavoparmelia baltimorensis (mainly a saxicolous species), Phaeophyscia ciliata, Melanelia olivetorum, Ramalina thrausta, Tuckermanella fendleri and Xanthoria hasseana. Of the eight macrolichens, which were significant indicators of tree composition at the treeand plot-levels, five of these species remained significant indicators of tree composition across the Maine plots. For hardwood-dominated plots these were Phaeophyscia rubropulchra, Punctelia rudecta and Pyxine sorediata (Table 7). For coniferdominated forests Imshaugia aleurites and Platismatia glauca remained significant indicators (Table 7). On average 15 6 10% of the total macrolichen flora was added outside of the two-hour timed survey and many of the added species occurred above reachable height or below the specified bole search area (Appendix A). Canopy surveys added an average of 6.3 6 4.3% of total species on the plots. Typical canopy species missed in the two-hour ground surveys included Usnea spp., Ramalina spp., Parmelia fertilis and Hypogymnia tubulosa. However, whole tree surveys are not a replacement for full plot inventory as only an average of 58% of the plot flora was captured in the whole-tree surveys of four maple trees on each plot (data not shown). For the eight spruce-dominated plots, which were surveyed by two-hour survey in both 2005 and 2006, an average of 1.1 (6 1.2) of the plot-level rarest species were not found again in 2006 and we suspect that collection of voucher specimens in 2005 (required by FIA protocol) led to the short-term local extirpation of these species from the plots (data for lost species given in Appendix A).

DISCUSSION This study provides a significant expansion of the knowledge of epiphytes in Acadia National Park


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Table 7. Indicator species for conifer- and hardwood-dominated sites based on FIA plot-level surveys for macrolichens at 62 sites across Maine (including our 12 ACAD sites). Indicator values are derived from the relative frequency and abundance of species in each forest type. P-values indicate significantly higher indicator value than randomized data. Only species with p-values of # 0.051 are shown here. Conifer forest indicators Species Ahtiana aurescens Bryoria furcellata Bryoria nadvornikiana Bryoria trichodes Cladonia chlorophaea group Cladonia macilenta var. bacillaris Cladonia ochrochlora Evernia mesomorpha Hypogymnia krogiae Hypotrachyna revoluta Imshaugia aleurites Menegazzia terebrata Platismatia glauca Platismatia tuckermanii Ramalina dilacerata Tuckermanopsis orbata Usnea filipendula Usnea fulvoreagens

Hardwood forest indicators

Indicator value

p

15.6 55.3 37.7 15.6 53.3 22.4 34 59.3 35.6 20.1 41.5 20.2 54.3 50.2 25.6 55.1 37.2 15.6

0.049 0.001 0.001 0.053 0.001 0.021 0.029 0.001 0.027 0.039 0.017 0.067 0.001 0.016 0.026 0.005 0.008 0.055

and provides evidence for the general importance of mixed stands and large trees for maintaining epiphyte diversity. The importance for lichen diversity of hardwood trees in conifer forests has been found in several previous studies (Boudreault et al. 2000; Lo¨bel et al. 2006; Neitlich & McCune 1997). The retention of large trees has also been recommended from studies of lichen epiphytes in Quebec (Boudreault et al. 2000) and northern New York (Root et al. 2007b). The protected forests of ACAD provide a critical reference for forest managers who seek to conserve forest integrity in Maine. Forest composition significantly affected the epiphyte flora on maple trees, that is, the lichens ‘‘see’’ the forest and not just the tree on which they are growing. The pattern we found was probably influenced by differences between deciduous and evergreen canopies in terms of: 1) throughfall and stemflow inputs (Goward & Arsenault 2000; Weathers et al. 2006; Weibull 2003); 2) incoming light levels and spectra of light, especially in winter

Species Anaptychia palmulata Cetrelia olivetorum Cladonia pyxine Collema subflaccidum Melanelia fuliginosa Melanelia halei Melanelia olivetorum Myelochroa aurulenta Myelochroa galbina Parmelia fertilis Parmelia sulcata Phaeophyscia pusilloides Phaeophyscia rubropulchra Physconia detersa Physcia stellaris Punctelia rudecta Pyxine sorediata Ramalina americana

Indicator value

p

36.8 26.7 16.7 43.7 27.4 39.2 43.4 24.6 40.9 18.7 55.8 32.2 80.3 58.6 67.5 53.6 40.1 31

0.002 0.053 0.022 0.004 0.008 0.002 0.001 0.011 0.027 0.026 0.012 0.008 0.001 0.001 0.001 0.016 0.003 0.038

(Federer & Tanner 1966; Loppi & Frati 2004); and 3) fog capture and rates of evaporation. In hardwood stands at ACAD, we noted possible drip zone effects (sensu Goward & Arsenault 2000) in the occurrence of Melanelia spp. and Ulota crispa on conifers only. In addition, the only records of cyanolichens on conifers in this study were Parmeliella triptophylla and Pannaria pezizioides on the base of Thuja occidentalis in a deciduous stand (plot D4). Condition of the forest should be considered in a study of epiphytes. In ACAD, American beech trees disfigured by the beech bark scale disease complex offered an unusual microhabitat in some stands. We found abundant Phaeophyscia rubropulchra, a common species, but also Anaptychia palmulata and Normandina pulchella especially on large deformed beech trees with their pocked boles. The latter two lichens are thought to be associated with old-growth forest at least in eastern North America (Selva 1994). In other parts of the boreal forest, wounded hardwood trees also can have areas of enrichment with higher bark pH conducive to colonization by

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sensitive lichen species such as Lobaria pulmonaria and associates (Gauslaa 1995). Changes in the composition of lichens along the vertical gradient of a tree can provide important ecological information regarding some lichen species, especially those that are canopy specialists. In our study, Parmelia fertilis, Punctelia perreticulata and Usnea strigosa were added to specific plot lists exclusively from tree-climbing surveys. In addition, Usnea subscabrosa and U. subfloridana were found at some plots only during tree-climbing surveys. In general, upper bole surveys added about 6% of total species richness on the plots and a more complete assessment of fruticose species was obtained by including tree-climbing surveys. We recommend inclusion of climbing surveys when the main aim of a study is to document the diversity and abundance of fruticose lichens. Bennett and Wetmore (2005) listed the lichen flora of ACAD as 91–99% known. This high percentage of known species was largely due to the work of Sullivan (1996). However, this study emphasizes that even in well-surveyed conservation holdings many important new discoveries may await. We added six lichens to Sullivan’s (1996) list from on-plot surveys and several additional species including the rare macrolichens: Degelia plumbea and Usnea flammea from off-plot survey work (specimens cited by Clerc & May 2007; Hinds & Hinds 2007). In addition, our collections of Hypotrachyna afrorevoluta were fundamental in establishing the presence of this species in North America (Hinds & Hinds 2007; Knudsen & Lendemer 2006). ACAD plots had a more diverse macrolichen flora than plots from elsewhere in Maine. Although this is partially an artifact of differences in collection intensity, ACAD is rich in macrolichens including 63% of the species listed by Selva (1994) as indicators of old-growth, seven of the species listed as decreasing in New England, seven of the species listed as ‘‘R1,’’ the rarest in New England with an additional 22 species also listed as ‘‘rare and declining in New England’’ (Hinds & Hinds 2007). Several contributing factors to high diversity of lichens at ACAD include proximity to the coast, high topographic diversity, and land use practices within the Park, which minimize tree harvest.

Current knowledge of macrolichen diversity at ACAD fails to reveal whether species that are most sensitive to air pollution were lost prior to recent documentation. In particular, the paucity of Leptogium, Collema, Protopannaria and Nephroma species in this study and the inability to locate known declining species such as Anzia colpodes, Fuscopannaria spp., Pannaria spp. and Sticta spp. may be cause for concern (Hinds & Hinds 2007). The bryophyte flora of ACAD is less well documented than the lichen flora. However, the occurrence of Frullania bolanderi on our plots was notable for its infrequency in the literature. Miller and Miller (1998) suggested that F. bolanderi is an indicator of old-growth forests in the Northeast and reported collections of this tiny liverwort from red maple trees in coastal Maine locations. In addition, Zygodon viridissimus var. rupestris, which was fairly frequent on our plots, is considered uncommon in much of the Northeast. This study also includes three of the four bryophyte species suggested to have higher frequency and cover in old-growth versus second-growth forests in Massachusetts (CooperEllis 1998; Anomodon attenuatus, Frullania eboracensis and Leskeella nervosa). Other bryophyte species on our plots that are regionally uncommon and may be considered as indicators of mature hardwood or mixed-wood forests include: Anacamptodon splachnoides, Anomodon rugellii, Drummondia prorepens, Haplohymenium triste, Homalia trichomanoides, Leucodon andrewsianus, Neckera pennata, Platydictya subtile and Ulota coarctata. The Forest Indicator Analysis (FIA) and former Forest Health Monitoring (FHM) programs of the United States Forest Service have contributed valuable epiphytic lichen data for North America (McCune 2000). Data from FIA plots have provided much needed regional and large scale perspectives on forest macrolichens (e.g., McCune 2000; McCune et al. 1997b; Will-Wolf et al. 2006). The data have also provided important information on the general distribution and occurrence of macrolichens in the Northeast (Hinds & Hinds 2007). The FIA lichen protocol has been shown to be repeatable for general patterns in lichen species composition, but not in species richness of the plots


(McCune et al. 1997a). Non-experts captured approximately 65% of lichen species found by lichen experts and almost all FIA lichen data are collected in the field by trained non-experts (McCune et al. 1997a). In this study, we noted that a two-hour timed survey such as that used on FIA plots missed an average of 15% of the lichen species even when the plot was surveyed by relative lichen ‘‘experts.’’ In our case, the time constraint probably contributed to the low repeatability of lichen species richness on the plots as some plots had over 500 trees that needed to be searched and lichen cover was fairly high (Table 2; Appendix A). In addition, many cyanolichens occurred mostly below the 0.5 m height limit on tree boles, suggesting that the methodology reduces likelihood of recording an important and sensitive component in the epiphyte flora at least in eastern forests. Given the increasing recognition of the peril of cyanolichens in most northern forests (Gauslaa 1995; Hinds & Hinds 2007; Richardson & Cameron 2004) and their usefulness in assessing stand quality (Campbell & Fredeen 2004; Whitman & Hagan 2007), we suggest that some form of cyanolichenspecific searching and abundance estimation be added to the FIA protocol. For instance, the FIA lichen protocol could be expanded to include more comprehensive estimates of the abundance for the more common and easily recognizable cyanolichens: Lobaria pulmonaria and jelly lichens (i.e., Collema and Leptogium spp.) (Campbell & Fredeen 2004; Edman et al. 2008; Root et al. 2007b; Whitman & Hagan 2007). This would necessitate expanding downward the area of the bole to be surveyed and the lower limit might consist of the ground. Although influence of the moisture and nutrients from the soil and leaf litter are probably great, it appears that ignoring this zone cannot be justified given the importance of cyanolichens that often occur only at the base of trees in eastern forests. In this multi-scale study of epiphytes we have demonstrated the importance of tree size and tree species to epiphyte species diversity, and by extension, to biodiversity in forests of Maine. Epiphytes are important indicators for forest managers not only because of their inherent sensitivities, but also because they are important

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indicators of the condition of forest food webs. Epiphyte diversity and abundance have repeatedly been shown to be important predictors of invertebrate diversity (Gunnarsson et al. 2004; Root et al. 2007a; Stubbs 1989; Wagner et al. 2007). Our results reı¨nforce the need to retain large trees on the landscape for the sake of biota and forest values other than timber. These data support a point made by Edman et al. (2008) that retention of large trees is crucial, but this practice alone would not be sufficient to maintain epiphyte diversity in the forests of Maine. Many of the epiphytes appear to depend upon the forest and not just the tree on which they are growing. Comprehensive epiphyte baseline surveys such as the one we report from ACAD can serve as a reference against which the ‘‘integrity’’ of more disturbed stands can be assessed. This study serves as an important baseline for detecting future changes in the epiphyte flora of ACAD and further highlights the importance of mixed stands of advanced age to epiphyte conservation in northern forests of eastern North America.

ACKNOWLEDGMENTS This work was funded by a National Park Research Fellowship to NLC and by Acadia Partners for Science and Research grant sponsored by L.L. Bean to NLC and ACD. Thank you to: Howard Prescott for crucial assistance with tree-climbing and plot surveys in 2006; Jim Hinds, Stephen Clayden, James Lendemer and Philippe Clerc for aiding with difficult macrolichen determinations; David Manski and Bill Gawley for facilitating plot selection and research permits that made the use of Acadia National Park resources possible; Gregory McGee for the loan of his Big Shot; Ian Halm for recommending the purchase of mechanical ascenders; and Susan Will-Wolf, Sarah Jovans, Marian Glenn and Bill Buck for providing reviewer comments to improve the manuscript.

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Hale, M. E. 1952. Vertical distribution of cryptogams in a virgin forest in Wisconsin. Ecology 33: 398–406. ———. 1965. Vertical distribution of cryptogams in a red maple swamp in Connecticut. The Bryologist 68: 193–197. Hinds, J. W. & P. L. Hinds. 2007. Macrolichens of New England. Memoirs of the New York Botanical Garden 96: i–xx, 1–584. Knudsen, K. & J. C. Lendemer. 2006. Changes and additions to the North American lichen mycota —V. Mycotaxon 95: 309–313. Lo¨bel, S., T. Sna¨ll & H. Rydin. 2006. Species richness patterns and metapopulation processes—evidence from epiphytic communities in boreo-nemoral forests. Ecography 29: 169–182. Loppi, S. & L. Frati. 2004. Influence of tree substrate on diversity of epiphytic lichens: comparison between Tilia platyphyllos and Quercus ilex (central Italy). The Bryologist 107: 340–344. McCune, B. 2000. Lichen communities as indicators of forest health. The Bryologist 103: 353–356. ———, J. P. Dey, J. E. Peck, D. Cassell, K. Heiman, S. WillWolf & P. N. Neitlich. 1997a. Repeatability of community data: species richness versus gradient scores in large-scale lichen studies. The Bryologist 100: 40–46. ———, ———, ———, K. Heiman & S. Will-Wolf. 1997b. Regional gradients in lichen communities of the southeast United States. The Bryologist 100: 145–158. ——— & M. J. Mefford. 1999. PC-ORD User’s Guide. MjM software design, Gleneden Beach, OR. Miller, N. G. & A. D. Miller. 1998. Occurrence of the leafy liverwort, Frullania bolanderi, in old-growth forests of northeastern North America. Journal of the Torrey Botanical Society 125: 109–116. Neitlich, P. N. & B. McCune. 1997. Hotspots of epiphytic lichen diversity in two young managed forests. Conservation Biology 11: 172–182. Oksanen, J. 1988. Impact of habitat, substrate and microplot classes on the epiphyte vegetation: interpretation using exploratory and canonical correspondence analysis. Annales Botanici Fennici 25: 59–71. Otnyukova, T. 2007. Epiphytic lichen growth abnormalities and element concentrations as early indicators of forest decline. Environmental Pollution 146: 359–365. Palmer, M. W. 1986. Pattern in corticolous bryophyte communities of the North Carolina Piedmont: do mosses see the forest or the trees? The Bryologist 89: 59–65. Poikolainen, J., M. Kuusinen, K. Mikkola & M. Lindgren. 1998. Mapping of the epiphytic lichens on conifers in Finland in the years 1985–86 and 1995. Chemosphere 36: 1073–1078. Richardson, D. H. S. & R. P. Cameron. 2004. Cyanolichens: their response to pollution and possible management strategies for their conservation in northeastern North America. Northeastern Naturalist 11: 1–22.


Root, H. T., G. G. McGee & R. A. Norton. 2007a. Arboreal mite communities on epiphytic lichens of the Adirondack Mountains of New York. Northeastern Naturalist 14: 425–438. ———, ——— & R. D. Nyland. 2007b. Effects of two silvicultural regimes with large tree retention on epiphytic macrolichen communities in Adirondack northern hardwoods, New York, USA. Canadian Journal of Forest Research 37: 1854–1866. Schuster, R. 1966–1992. The Hepaticae and Anthocerotae of North America. Volumes I–VI. Columbia University Press, New York (vol. I–IV); Field Museum of Natural History, Chicago (vols. V, VI). Selva, S. B. 1994. Lichen diversity and stand continuity in the northern hardwoods and spruce-fir forests of northern New England and western New Brunswick. The Bryologist 97: 424–429. Sillett, S. C. & P. N. Neitlich. 1996. Emerging themes in epiphyte research in westside forests with special reference to cyanolichens. Northwest Science 70: 54–60. Stubbs, C. 1989. Patterns of distribution and abundance of corticolous lichens and their invertebrate associates on Quercus rubra in Maine. The Bryologist 92: 453–460. Studlar, S. M. 1982. Host specificity of epiphytic bryophytes near Mountain Lake, Virginia. The Bryologist 85: 37–50. Sullivan, T. J. 1996. Lichens of Acadia National Park. Ph.D. Thesis, University of Minnesota, St. Paul, MN. USDA. 1999. USDA Forest Service, National Forest Health Monitoring Program. Research Triangle Park, N.C.

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ms. received March 27, 2008; accepted December 16, 2008.

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Appendix A. Epiphytic macrolichens and bryophytes at 12 study sites in Acadia National Park, Maine, compiled from a combination of: 1) two-hour timed surveys in 34.7 m-radius sites with abundance values given according to the FIA protocol, 2) complete tree tallies and 3) climbing of four maple trees per site (at 8 sites in boldface). Abundance ratings are: 1 5 1–4 individuals, 2 5 5–10 individuals, 3 5 more than 10 individuals, but on less than half the tree boles and 4 5 on half or more of the boles. An ‘‘a’’ beside the abundance code means that the species was added to site list outside of the two-hour time limit. A ‘‘c’’ means that the species was recorded from the plot only above 2 m height on the climbed trees. An asterisk ‘‘*’’ applies to the eight spruce-dominated sites (sites without ‘‘D’’ in name), in which species with an asterisk after their abundance rating were found in 2005 but not seen during comprehensive re-surveys in 2006. Note that site totals given here differ from those in Table 1 because Table 1 was limited to species captured during the two-hour timed survey. Nomenclature follows: Hinds and Hinds (2007) for macrolichens; Crosby et al. (1999) for mosses; and Schuster (1966–1992) for liverworts.

LICHENS Ahtiana aurescens Allocetraria oakesiana Anaptychia palmulata Bryoria furcellata Bryoria nadvornikiana Bryoria trichodes Candelaria concolor Cetrelia chicitae Cetrelia olivetorum Cladonia caespiticia Cladonia cenotea Cladonia chlorophaea group Cladonia coniocraea Cladonia macilenta/ bacillaris Cladonia ochrochlora Cladonia pleurota Cladonia squamosa Collema subflaccidum Dendriscocaulon intricatulum Evernia mesomorpha Everniastrum catawbiense Flavoparmelia caperata Heterodermia obscurata Hypocenomyce friesii Hypocenomyce scalaris Hypogymnia krogiae Hypogymnia physodes Hypogymnia tubulosa Hypotrachyna afrorevoluta Hypotrachyna revoluta Imshaugia aleurites Leptogium cyanescens Lobaria pulmonaria Lobaria quercizans Lobaria scrobiculata Melanelia exasperatula Melanelia fuliginosa Melanelia halei Melanelia subaurifera Menegazzia terebrata Myelochroa aurelenta

D1

D2

D3

D4

11

18

66

67

160

162

284

285

0 2 1 0 0 0 1 1 2 3 0 3 1 2 1 1 2 1 0 1 0 4 0 0 0 1 3 1 2 1 1 3 1 1 0 1 1 3 4 0 0

0 1 1 0 0 0 0 1 1 1 0 0 1 0 0 0 2 3 0 1 0 1 0 0 1 0 1 1 1 1 0 3 2 3 0 2 0 1 4 0 0

0 4 1 0 0 0 1 0 1a 0 0 3 3 0 0 0 3 1 0 0 0 4 0 0 0 1 3 a, c 3 0 1 3 2 3 0 0 1 4 4 0 1

0 1 0 0 0 0 0 2 0 0 0 1 a, c 1 0 0 1 1 0 1 0 4 1 1 1 1 1 1 1 1 0 2 3 3 0 0 1 0 4 1 0

0 3 0 3 3 0 0 1a 0 0 1a 4 1a 1 2 0 4 0 0 3 3 1a 0 0 0 4 4 3 0 0 4 0 0 0 0 0 0 0 1* 0 0

1* 2 0 2 2 0 0 1a 1a 0 1a 3 1a 3 1 0 3 0 0 3 2 1 0 0 0 3 4 3 0 0 4 0 0 0 0 0 0 0 0 1a 0

0 2 0 3 0 0 0 2 2 0 0 3 3 0 3 0 3 0 0 1 1a 3 2 0 1a 3 4 3 3 1a 4 1 3 1 0 0 0 2 2 0 0

0 3 1 3 1a 0 0 1 1 0 0 2 1 0 0 0 1 0 1 2 1 3 3 0 0 1 4 3 2 0 4 3 3 2 1 0 0 1 2 0 0

0 3 0 3 2 0 0 0 0 1a 0 3 3 3 0 0 0 0 0 3 2 3 0 0 0 3 4 3 a, c 3 3 3 2 0 0 0 0 0 a, c 0 0

0 2 0 3 1a 1 0 2 1 1a 1a 3 0 3 2 0 3a 0 0 2 1 3 1a 0 0 3 4 2 1a 1 3 3 3 3 1 0 0 1 1a 1a 0

0 1 0 1 1 1 0 1 2 0 1a 3 1a 2 0 1 3 0 0 3 1 3 0 0 0 3 4 3 2 2 4 0 0 0 0 0 0 1 2 0 0

0 1 0 2 1 0 0 1* 0 1 0 2 1 2 1a 0 3 0 0 3 1 2 0 0 0 3 4 3 3 1 4 0 0 0 0 0 0 1* 1* 0 0


485

Appendix A. Continued.

LICHENS Myelochroa galbina Nephroma parile Normandina pulchella Parmelia fertilis Parmelia saxatilis Parmelia squarrosa Parmelia sulcata Parmeliella triptophylla Parmeliopsis capitata Parmeliopsis hyperopta Parmotrema crinitum Parmotrema perlatum Parmotrema reticulatum Peltigera spp. Phaeophyscia pusilloides Phaeophyscia rubropulchra Physcia aipolia Physcia millegrana Physconia detersa Physconia leucoleiptes Platismatia glauca Platismatia tuckermanii Pseudevernia cladonia Pseudevernia consocians Protopannaria pezizoides Punctelia perreticulata Punctelia rudecta Pyxine sorediata Ramalina americana Ramalina intermedia Tuckermanopsis americana Tuckermanopsis orbata Usnea ceratina Usnea cornuta Usnea filipendula Usnea fulvoreagens Usnea glabrescens Usnea hirta Usnea mutabilis Usnea rubicunda Usnea strigosa Usnea subfloridana Usnea subscabrosa Vulpicida pinastri Macrolichen totals: BRYOPHYTES Amblystegium serpens Amblystegium serpens var. juratzkanum

D1

D2

D3

D4

11

18

66

67

160

162

284

285

0 0 0 a, c 1 4 4 1 2 0 2 1 0 0 0 4 1 0 3 1 1 0 0 0 0 1 4 3 0 1 1 0 0 0 1 0 0 0 0 0 0 a, c 0 0 48

1 0 1 0 0 1 1 0 2 0 2 1 0 0 1 4 0 0 1 0 0 0 0 0 0 0 4 3 0 1 0 0 0 1 1 0 0 0 0 0 0 0 0 0 36

1 0 1 a, c 0 4 3 0 3 0 3 0 0 0 0 4 0 0 1 0 1 1 0 0 0 0 4 2 0 0 0 0 0 0 0 0 0 0 0 0 a, c a, c 0 0 36

0 0 0 1 0 4 4 1 1 0 3 1 1 1 0 1 1 0 1 0 1 1 0 0 1 0 4 1 0 0 0 0 0 0 0 0 0 0 0 0 a, c a, c 0 0 42

0 0 0 0 4a 3 2 0 3 0 0 0 0 0 0 0 0 0 0 0 4 3 0 0 0 0 2 0 0 0 1 1 0 1a 4 1 0 0 0 1 0 2 1 0 33

0 0 0 0 4 3 1 0 3 1 0 0 0 0 0 0 0 0 0 0 3 3 1a 0 0 0 1 0 0 0 0 1 1a 0 1 0 0 1a 0 0 0 3 0 0 34

0 1 0 0 2 4 0 0 3 0 3 2 0 0 0 1 1 0 0 0 4 2 2a 0 0 0 3 1 0 0 0 1 0 0 1a 0 0 0 0 1a 0 2 0 0 41

1 1a 1a a, c 0 4 1 0 2 0 1 1 0 0 0 0 0 1 1 0 4 2 0 a,c 0 0 3 1 0 1 0 1 0 0 1 0 0 0 1a 0 a, c 1 0 0 47

2* 1a 0 0 2a 4 3 1 2 0 0 0 0 1a 0 1a 0 0 0 0 3 3 0 0 1a a, c 3 0 1a 1a 2 2 1a 0 3 1a 0 0 0 1a a, c 3 1a 0 44

0 0 0 a, c 1 4 3 0 3 0 0 0 0 0 0 0 0 0 1 0 3 3 0 0 0 a, c 3 0 1 1a 3 1 1a 0 2 1 3 0 0 0 0 2 a, c 1* 50

0 0 0 0 4a 3 2 0 3 1 0 0 0 0 0 1* 0 0 0 0 4 3 0 0 0 0 3 0 0 1a 2 0 0 0 1a 0 1 1a 0 0 0 2 0 3 39

0 0 0 0 4 2 2 0 4 1 0 0 0 0 0 1* 1* 0 0 0 3 3 0 0 0 0 3 0 0 0 1 1 0 0 1 0 0 1 0 0 0 3 0 1 37

1

0

0

0

0

0

0

0

2

0

0

0

0

1

0

0

0

0

0

0

0

0

0

0

486

THE BRYOLOGIST

112(3): 2009


Anacamptodon splachnoides Anomodon attenuatus Anomodon rugellii Brachythecium populeum Brachythecium rutabulum Brachythecium salebrosum Brachythecium velutinum Callicladium haldanianum Campylium chrysophyllum Campylium hispidulum Cololejeunea biddlecomiae Dicranum flagellare Dicranum fuscescens Dicranum montanum Dicranum scoparium Dicranum viride Drummondia prorepens Entodon cladorrhizans Eurhynchium pulchellum Fissidens dubius Frullania bolanderi Frullania eboracensis Frullania tamarisci var. asagrayana Haplohymenium triste Hedwigia ciliata Herzogiella striatella Homalia trichomanoides Hypnum cupressiforme Hypnum cupressiforme var. filiforme Hypnum curvifolium Hypnum imponens Hypnum pallescens Jamesoniella autumnalis Leskeella nervosa Leucodon andrewsianus Lophocolea heterophylla Metzgeria furcata Neckera pennata Orthotrichum pusillum Orthotrichum sordidum Orthotrichum speciosum Paraleucobryum longifolium Plagiothecium laetum Platydictya subtile Platygyrium repens Pleurozium schreberi Porella platyphylla Pseudotaxiphyllum elegans Pterigynandrum filiforme Ptilidium ciliare

D1

D2

D3

D4

11

18

66

67

160

162

284

285

1 1 0 0 0 1 0 1 0 0 0 0 1 3 1 2 1 0 0 0 0 4 1 0 0 0 0 0 1 0 1 3 0 4 0 0 1 3 0 4 2 1 0 1 4 0 3 0 1 0

0 4 1 1 1 1 0 0 0 1 0 0 0 0 0 2 0 0 0 0 0 4 1 2 0 0 0 1 1 0 0 1 0 3 4 0 3 4 2 4 2 0 0 1 3 0 4 0 3 0

0 1 0 0 0 1 0 0 0 0 0 2 0 2 0 2 0 1 0 0 1 4 2 0 0 0 0 0 0 0 0 2 0 4 1 0 1 2 0 4 3 1 0 0 4 0 3 0 3 0

0 2 0 0 0 0 0 0 2 0 0 0 1 2 0 1 0 0 0 1 0 4 2 1 1 0 0 1 2 1 1 1 0 0 3 0 1 4 1 2 0 0 0 0 2 0 2 0 2 0

0 0 0 0 0 0 0 0 0 0 0 1 0 4 0 0 0 0 0 0 0 1 3 0 0 0 0 0 0 0 1 1 0 0 0 0 0 0 0 0 0 0 0 0 2 0 0 0 0 0

0 0 0 0 0 0 0 0 0 0 0 0 0 3 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0 0 0 1 0 4 1 3 0 0 0 0 0 4 4 0 0 0 1 1 3 0 1 4 1 0 0 0 1 1 0 0 0 0 0 1 4 0 1 0 0 0

1 0 0 0 0 1 0 0 0 1 0 2 0 4 0 4 0 0 0 0 0 4 4 0 0 0 0 0 2 0 1 4 0 0 0 0 1 2 0 1 0 0 0 0 4 0 1 0 1 0

0 0 0 0 0 1 1 0 0 0 0 2 0 3 2 3 0 0 1 0 0 3 4 0 0 0 0 3 3 0 0 3 0 0 0 1 0 2 0 1 0 0 0 0 3 0 0 2 0 0

0 0 0 0 0 0 0 0 0 0 0 1 0 0 1 2 0 0 0 0 1 4 3 0 0 0 0 1 2 0 0 3 0 0 0 0 0 1 0 1 0 0 0 0 3 0 0 0 0 0

1 0 0 0 0 0 0 2 0 1 1 0 0 4 0 4 0 0 0 0 0 4 1 0 0 1 0 1 0 0 0 4 0 0 0 0 0 0 0 1 0 0 1 2 4 1 0 0 0 1

0 0 0 0 0 0 0 2 0 0 0 0 0 4 0 0 0 0 0 0 0 3 3 0 0 0 0 0 0 0 0 4 0 0 0 0 0 0 0 0 0 1 0 0 1 0 0 0 0 1


487


Ptilidium pulcherrimum Pylaisia intricata Pylaisia selwynii Radula complanata Rauellia scita Sanionia uncinata Thuidium delicatulum Ulota coarctata Ulota crispa Zygodon viridissimus var. rupestris Bryophyte totals: Epiphyte totals:

D1

D2

D3

D4

11

18

66

67

160

162

284

285

1 3 1 4 1 0 2 1 4 1 34 82

0 3 0 0 0 0 2 2 3 1 30 66

0 2 1 4 0 1 1 2 4 0 27 63

1 4 0 4 0 0 1 2 4 1 30 72

4 0 0 0 0 1 0 0 2 0 10 43

3 0 0 0 0 0 0 0 0 0 4 38

4 2 0 3 0 1 0 0 3 3 23 64

4 3 0 4 0 1 1 2 4 3 25 72

3 0 0 3 0 1 1 4 4 0 24 68

3 0 0 3 0 1 1 3 4 0 18 68

4 2 0 2 0 2 0 2 4 0 23 62

4 0 0 0 0 0 0 0 4 0 10 47