Four Years of Epiphyte Colonization in Douglas-fir Forest Canopies
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1 The Bryologist 103(4), pp Copyright 000 by the American Bryological and Lichenological Society, Inc. Four Years of Epiphyte Colonization in Douglas-fir Forest Canopies STEPHEN C. SILLETT Department of Biological Sciences, Humboldt State University, Arcata, CA 9551, U.S.A. BRUCE MCCUNE, JERILYNN E. PECK, AND THOMAS R. RAMBO Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331, U.S.A. Abstract. In 1995, we installed surface-sterilized, rough-barked and smooth-barked tree branches in clearcuts, young forests, and old growth. Half of the experimental branches were inoculated with propagules of the epiphytic cyanolichen, Lobaria oregana. In 1997, we concluded that L. oregana was associated with old-growth Douglas-fir forests because of dispersal limitation; addition of L. oregana propagules resulted in a marked increase in establishment rates. In 1999, we revisited the experiment to determine whether other epiphytes had colonized the tree branches. We also checked to see if the 1997 results of the experiment persisted. A total of 6 epiphyte genera (nine bryophytes and 17 lichens) had colonized the branches. Lichen colonization was generally fastest in clearcuts. Colonization by alectorioid lichens was rapid in both clearcuts and old growth but slow in young forests. In contrast, bryophyte colonization was relatively rapid in all age classes. Epiphyte colonization was generally more rapid on smooth bark than on rough bark, although Cladonia was more frequent on rough-barked branches. Bryophytes, cyanolichens, and Sphaerophorus globosus were more frequent on inoculated branches than on control branches, implying that the L. oregana propagule mixture used in 1995 was contaminated with other epiphytes. Like L. oregana, these species may also be dispersal-limited. The number of established L. oregana thalli in clearcuts and young stands decreased from 1997 to 1999, but the number of thalli remained relatively stable in old growth. After four years, established L. oregana thalli were larger in clearcuts than in either young stands or old growth. Overall, the fourth-year results of our experiment confirm the importance of dispersal limitation as the cause of old-growth association in L. oregana in western Oregon. The importance of propagule availability to plant community development has been known for many years (Gleason 196). However, it was difficult to believe that dispersal limitations could result in the huge epiphytic differences between old growth and younger forests in the Pacific Northwest. The much higher epiphyte biomass and diversity of old growth has usually been attributed to microclimatic and structural differences between old and young forests (e.g., Franklin et al. 1981; Lesica et al. 1991). In 1995, we began experiments to contrast the relative importance of propagule supply versus habitat in controlling the development of Lobaria oregana (Tuck.) Müll. Arg. populations. We chose this cyanolichen for its massive accumulation and renown as the dominant epiphytic lichen in oldgrowth Douglas-fir forests of western Oregon (McCune 1993; Pike et al. 1975; Sillett 1995). In 1997, we found that L. oregana can establish and grow in a wide range of habitats, including clearcuts and young forests (Sillett et al. 000). Dispersal limitations result in very slow development of L. oregana populations after clearcutting in this region. Are other epiphytes also dispersal-limited? The diversity of reproductive strategies in lichens led us to believe that many, if not most, species would be more successful than L. oregana in long distance dispersal. Sorediate species and those producing abundant ascospores should be able to colonize new substrates more easily than L. oregana with its relatively large, heavy lobules. Experimental branches, which were initially devoid of epiphytes, were placed in a variety of habitats for long-term study. This allowed us to measure natural rates of colonization in these habitats. During re-examination of our experimental branches in 1999, we also checked to see if the 1997 results of the L. oregana dispersal experiment persisted for a longer period of time /00/ $1.05/0
2 66 THE BRYOLOGIST [VOL. 103 METHODS Study area. In summer 1995, we initiated experiments on epiphyte colonization in fifteen forest stands from five areas of the Willamette National Forest in the Cascade Range of western Oregon. One stand of each of three age classes (old growth, young, and clearcut) was selected from each area. The old-growth stands were between 450 and 500 yr of age, had 60 to 85 m tall canopies, and were dominated by Pseudotsuga menziesii (Mirb.) Franco and Tsuga heterophylla (Raf.) Sarg. The young stands were between 30 and 40 yr of age and had 0 to 30 m tall canopies. They originated from 10 to 30 ha clearcuts that were replanted exclusively with P. menziesii, and they had not been thinned since replanting. The clearcut stands (5 to 0 ha) contained scattered shrubs and young trees (mostly P. menziesii) not exceeding 1.5 m in height and 10 yr of age. All stands were within the T. heterophylla Zone (Franklin & Dyrness 1973) between 400 and 800 m elevation and less than 10 m vertical distance from a perennial stream or body of water. Additional information about each stand can be found in Sillett et al. (000). Experimental design. We used sterilized P. menziesii branch segments to serve as substrates for colonization by sown propagules of L. oregana. The segments were one m long and had bark of two types: 1) old, rough-barked branches (4.6 to 10.1 cm diameter) cut from 00-yr-old trees, and ) young, smooth-barked branches (.1 to 5.1 cm diameter) cut from 80-yr-old trees. We removed side branchlets and twigs, and rubbed off macrolichens and bryophytes without damaging the underlying bark. Branches were sterilized by fumigating them with propylene oxide to ensure that any epiphytes observed in the experiment were not regrowth of previously established thalli or propagules. A total of eight rough-barked and eight smooth-barked branches were installed in each forest stand. In the oldgrowth stands, we accessed the crowns of four trees (two dominant P. menziesii, one suppressed P. menziesii, and one codominant T. heterophylla) using standard rope climbing techniques. Excessively leaning trees and trees with dead tops were avoided for the safety of tree climbers. In each tree crown, we installed two pairs of branches by lashing them to living branches with nylon cord. Each pair consisted of a smooth-barked and a rough-barked branch. One pair was used for experimental treatment, and the other served a control. Branches were installed one to two m away from the main trunk at the height of each tree s greatest estimated L. oregana abundance (usually m). In the young stands, we installed branches in the same manner as in the old-growth stands except that all four trees were P. menziesii accessed by ladders and free climbing. Installation height in the young trees ranged from three to nine m, depending on the heights of the lowest living branches. In the clearcuts, we installed branches on racks made from five cm by five cm by.5 m wooden poles. Racks were constructed by lashing crossbars between tripods at a height of 1.5 m above the ground. We lashed branches to the crossbars. Racks were placed in open areas of the clearcuts so that they were not shaded by nearby vegetation. Experimental branches in each tree or rack were inoculated with L. oregana propagules four times over the course of one year: once per season beginning in summer Lichen thalli were collected from standing or freshly fallen trees near the study area, air-dried, placed in a plastic bag, and manually crushed. In addition to freeing natural propagules (i.e., lobules), this treatment mechanically produced artificial propagules (i.e., thallus fragments). All propagules were passed through a two mm mesh screen and then thoroughly mixed. Batches of about 3.8 g of this propagule mixture were then measured out as inoculum. Branches were misted with water prior to inoculation in order to promote adhesion of propagules to bark. Using a spice shaker with 3 mm diameter holes, we then sprinkled a batch of propagules onto the upper surface of each experimental branch so that it was thoroughly covered with propagules (i.e., thousands per dm ). We measured establishment of L. oregana in summer 1997 and again in summer 1999, two and four years after the first inoculation. Branches were first misted with water to help distinguish L. oregana, which appears yellowgreen when wet due to the presence of usnic acid, from other epiphytes. We counted the total number of established L. oregana thalli within a five dm long cylindrat (i.e., cylinder-shaped sample plot) centered on each branch. Numbers of established L. oregana thalli were expressed per dm bark. We estimated bark surface area within each cylindrat by multiplying branch diameter (in dm) by five. In 1999, we also measured the maximum diameter of the largest L. oregana thallus and noted the presence of any naturally colonizing epiphytes on each cylindrat. Additional details about the experimental design can be found in Sillett et al. (000). Data analyses. We used JMP 3. (SAS Institute 1997) to conduct ANOVA. Lobaria oregana establishment data were analyzed by a four-way, mixed model ANOVA with one level of nesting. This analysis tested for three fixed effects (i.e., age class, dispersal treatment, and substrate type) one random effect (i.e., stand nested within age class), and seven interactions (see Table in Sillett et al. 000). Changes in the numbers of established L. oregana thalli on inoculated branches between 1997 and 1999 were assessed by a three-way mixed model ANOVA with one level of nesting. This analysis tested for two fixed effects (i.e., age class and substrate), one random effect (i.e., stand nested within age class), and two interactions. Size of the largest established L. oregana thallus per tree was compared by a two-way mixed model nested ANOVA. This analysis tested for one fixed effect (i.e., age class) and one random effect (i.e., stand nested within age class). Nesting was accommodated in these ANOVA by testing main effects against the stand-to-stand variation within an age class rather than against error terms for tree replicates within a stand. Stand-level frequencies (i.e., numbers of branches per stand) of epiphytes on rough- vs. smoothbarked and on inoculated vs. control branches were separately analyzed by two-way ANOVA. These analyses tested for main effects (i.e., age class and either substrate or dispersal) and their interactions with stands as the units of replication. When necessary, we used the Box-Cox transformation (Sokal & Rohlf 1995) to normalize residuals and eliminate heteroscedasticity prior to ANOVA. However, since ANOVA on untransformed and Box-Cox transformed data consistently identified the same main effects and interactions as statistically significant, we present analyses of untransformed data for simplicity. We used single degree of freedom orthogonal contrasts to make multiple comparisons of group means for significant factors by using the standard least squares procedures in JMP 3. (SAS Institute 1997). Experimentwise error rates were controlled in these comparisons by employing the contrasts in a stepwise manner. Results were considered statistically significant if p (type I error) Finally, we used PC-ORD (McCune & Mefford 1999) to generate genus-area curves for colonizing epiphytes on rough- and smooth-barked branches; we were unable to
3 000] SILLETT ET AL.: EPIPHYTE COLONIZATION 663 FIGURE 1. Genus-area curves for epiphytes on smooth-barked and rough-barked experimental branches in Douglasfir forests. Note that the x-axis is on a log scale. identify many of the tiny specimens to species. Since this analysis assumed that all samples within a substrate type had equal areas, we assigned average surface areas for rough-barked (11.5 dm ) and smooth-barked (5.3 dm ) cylindrats to the samples prior to analysis. RESULTS Epiphyte colonization. We identified 6 genera of lichens and bryophytes on the experimental branches in 1999, including five mosses (Antitrichia, Dicranum, Hypnum, Isothecium, and Orthotrichum), four liverworts (Cephaloziella, Frullania, Porella, and Radula), four cyanolichens (Lobaria, Nephroma, Pseudocyphellaria, and Sticta), four alectorioid lichens (Alectoria, Bryoria, Nodobryoria, and Usnea), and nine other green algal lichens (Candelaria, Cetraria, Cladonia, Evernia, Hypogymnia, Parmelia, Platismatia, Ramalina, and Sphaerophorus). Smooth bark accumulated epiphytes more quickly than rough bark; genus richness was higher on smooth bark than on rough bark across all sampled branch surface areas (Fig. 1). Responses of colonizing epiphytes to age class, dispersal treatment, and substrate type were not uniform across epiphyte functional groups or species. Bryophytes were more frequent colonists in old growth and young stands than in clearcuts (Fig. ). The moss Antitrichia curtipendula rapidly colonized several experimental branches by outward growth of well-established mats in the old-growth forest canopy. Alectorioid lichens were much less frequent colonists in young stands than in either clearcuts or old growth (Fig. ). Cladonia species, Sphaerophorus globosus, and other green algal lichens were more frequent colonists in clearcuts than in either young stands or old growth (Fig. ). Bryophytes, cyanolichens, and Sphaerophorus globosus were more frequent colonists of inoculated branches than controls (Fig. 3). Finally, Cladonia species were more frequent colonists of rough bark than smooth bark (Fig. 4). Lobaria oregana establishment. There were 7 times as many thalli (mean 8.08 vs thalli/ dm ) in 1997 (Sillett et al. 000) and 13 times as many thalli (mean 1.7 vs thalli/dm )in 1999 on inoculated branches compared to controls. By 1999, the dispersal treatment was the only sig-
4 664 THE BRYOLOGIST [VOL. 103 FIGURE. Frequency of colonizing epiphytes on experimental branches after four years by stand age class. Data are means and standard errors (n 5 stands per age class). Asterisks indicate epiphytes whose frequencies across age classes differed significantly (p 0.05). nificant experimental effect on L. oregana establishment; stand age class and substrate type did not have significant overall effects on the number of L. oregana thalli (Table 1). However, there were less than half as many thalli on rough bark as on smooth bark in clearcuts, and there were almost three times as many thalli on rough bark in old growth as on rough bark in clearcuts (Fig. 5). The change in the number of established thalli from 1997 to 1999 was not uniform across either age classes or substrate types (Table ). The greatest losses of thalli occurred on smooth bark in clearcuts and young stands; old growth changed the least (Fig. 6). The number of L. oregana thalli actually increased on 18% of the experimental branches in old growth. In both clearcuts and young stands, however, the number of thalli always either decreased or remained the same. Finally, L. oregana thalli were largest in clearcuts; maximum thallus diameter was higher in clearcuts ( , mean 1 SE) than in young stands ( ) and old growth ( ) (p 0.01). The largest four-yr-old L. oregana thallus was 18 mm wide. A few older and larger thalli (up to 150 mm wide) had apparently fallen from above and become attached to branches in the old-growth forest canopy. DISCUSSION Colonization dynamics. Lichen colonization was generally most rapid in the exposed environment of clearcuts. Rapid colonization of alectorioid lichens in clearcuts and old growth contrasted sharply with their poor performance in young stands. Establishment of alectorioid lichens in young stands may therefore be difficult, unless the stand is very open. This agrees with our observation that alectorioid lichens are usually sparse in young forests except for occasional stands that have a more open canopy (e.g., rocky sites or otherwise understocked stands). Colonization patterns of Cladonia and Sphaerophorus globosus were qualitatively similar to, but less dramatic than, the pattern of alectorioid lichens. Other green algal lichens (mainly Cetraria, Hypogymnia, Parmelia, and Platismatia) also colonized clearcuts more rapidly than young forests. Canopy closure may thus form a bottleneck in community dynamics of epiphytic lichens, just as it does with vascular plants. A paucity of herbaceous plants and lichens in the undergrowth of dense, young Douglas-fir plantations is commonly observed. Subsequent breakup and opening of the
5 000] SILLETT ET AL.: EPIPHYTE COLONIZATION 665 FIGURE 3. Frequency of colonizing epiphytes on experimental branches after four years by dispersal treatment. Data are means and standard errors (n 15 stands). Asterisks indicate epiphytes whose frequencies across treatments differed significantly (p 0.05). canopy during forest stand development once again allows successful establishment of epiphytic lichens in exposed overstory habitats. In contrast to lichens, bryophyte colonization was most rapid in old growth, although bryophytes were frequent colonists in all age classes, including young stands. Rapid bryophyte colonization in old growth is largely attributable to the moss Antitrichia curtipendula, which was much more frequent on experimental branches in old growth (3.9%) than in either young forests (5.0%) or clearcuts (1.4%). This species is the dominant epiphytic bryophyte in old-growth Douglas-fir forest canopies within the study area (Sillett 1995). Faster bryophyte colonization in young stands than in clearcuts is largely attributable to the moss Isothecium myosuroides, which was much more frequent on experimental branches in young stands (57.5%) and old growth (31.6%) than in clearcuts (5.6%). This shade tolerant species dominates the lower canopy and understory of Douglas-fir forests within the study area (Sillett & Rambo 000). Overall, the sheltered lower canopy of dense young forests is much more suitable for bryophytes than lichens. Aside from stand age effects on epiphyte colonization, two other results warrant discussion. First, not all epiphytes were as indifferent to substrate type as L. oregana. Cladonia species colonized rough bark much more rapidly than smooth bark. Squamules of these lichens thrive inside deep bark fissures, which are lacking on smooth bark. This underscores the danger of extrapolating experimental results for L. oregana to other epiphytes. Overall, however, epiphytes colonized smooth bark just as quickly as rough bark, implying that few genera require deep bark fissures for successful establishment. Second, bryophytes, cyanolichens, and Sphaerophorus globosus colonized branches inoculated with L. oregana propagules more rapidly than they colonized control branches. Propagules of these epiphytes must have been present in the experimental propagule mixture. Like L. oregana, but perhaps to a lesser extent, these epiphytes are dispersal-limited; the addition of propagules resulted in increased rates of establishment on branches. The importance of dispersal limitations. There are three potential causes of old-growth associations among epiphytes: 1) species may demand particular microenvironments created by the structure of old forests, ) colonization may be slow because of a shortage of suitable substrates in young forests, and 3) colonization may be limited by slow rates
6 666 THE BRYOLOGIST [VOL. 103 FIGURE 4. Frequency of colonizing epiphytes on experimental branches after four years by substrate type. Data are means and standard errors (n 15 stands). Asterisks indicate epiphytes whose frequencies across substrates differed significantly (p 0.05). of dispersal (Sillett & Neitlich 1996). The fourthyear results of our experiment confirm the importance of dispersal limitation as a cause of oldgrowth association in L. oregana in western Oregon (Sillett et al. 000). In fact, the significance of differences among stand age classes and substrate types evident in 1997 disappeared, leaving the experimental sowing of propagules as the only significant effect. The longer period of observation afforded some further insights. The natural colonization rate of L. oregana, even in old-growth forests where it is abundant, is surprisingly low. Control branches in the old-growth forest canopy were sparsely colonized by L. oregana, even after four years. In young stands with sparse to moderate natural populations of L. oregana (Sillett & McCune 1998), colonization of control branches by L. oregana was near zero. These results underscore the weak dispersal and establishment abilities of L. oregana and TABLE 1. Four-way ANOVA summary for 1999 results of Lobaria oregana dispersal experiment. The dependent variable is the number of established L. oregana thalli per dm bark. Source of variation df MS F P Age class Stand (age) Dispersal treatment Substrate type Dispersal substrate Age dispersal Age substrate Age dispersal substrate Dispersal stand (age) Substrate stand (age) Dispersal substrate stand (age) Residual
7 000] SILLETT ET AL.: EPIPHYTE COLONIZATION 667 FIGURE 5. Number of Lobaria oregana thalli on experimental branches after four years by stand age class, dispersal treatment, and substrate type. Data are means and standard errors (n 5 stands per age class). the importance of retaining Lobaria-bearing trees during logging operations in western Oregon (Peck & McCune 1997; Sillett & Goslin 1999; Sillett et al. 000). We emphasize that our finding of dispersal limitations in L. oregana in western Oregon should only be extrapolated to other regions and to other epiphytes with great caution. Since the ecology of an epiphytic lichen is not necessarily uniform throughout its entire geographic range (Goward 1995), our results may not apply to L. oregana in TABLE. Three-way ANOVA summary for Lobaria oregana dispersal experiment. The dependent variable is the change in the number of established L. oregana thalli on inoculated branch segments between 1997 and Source of variation df MS F P Age class Stand (age) Substrate type Age substrate Substrate stand (age) Residual other portions of its range (e.g., the hypermaritime forests of British Columbia). And even within western Oregon, some old-growth associated lichens have a completely different reproductive strategy than L. oregana, which reproduces almost exclusively by lobules (Rhoades 1983). For example, calicioid lichens, which invest heavily in ascospore production, appear to be substrate-limited rather than dispersal-limited. We assume that ascospores of calicioid lichens are effectively dispersed to new substrates by animal vectors (Tibell 1994). On the other hand, some epiphytic lichens in the Pacific Northwest (e.g., Pseudocyphellaria rainierensis) appear to have dispersal limitations even stronger than those of L. oregana (Sillett & Goward 1998). In other regions of the world, we are also likely to find such dispersal-limited lichens. For example, a number of the Lobaria species in temperate east Asia reproduce by lobules, and Usnea longissima and U. diffracta in far-east Russia reproduce primarily by fragmentation (McCune pers. obs.). Such lichens may also be associated with oldgrowth forests due to dispersal limitations.
8 668 THE BRYOLOGIST [VOL. 103 FIGURE 6. Reductions in the number of Lobaria oregana thalli on inoculated branches from 1997 to 1999 by age class and substrate. Data are means and standard errors (n 5 stands per age class). Means with different letters differed significantly (p 0.05). ACKNOWLEDGMENTS We thank Jim Spickler of Eco-Ascension Research for assistance with tree climbing. André Arsenault and Leif Tibell provided constructive comments on the draft manuscript. This work was supported by National Science Foundation grant DEB to Bruce McCune. Sillett was supported by Global Forest during this research (GF ). LITERATURE CITED FRANKLIN, J. F.& C. T. DYRNESS Natural vegetation of Oregon and Washington. U.S. Forest Service General Technical Report PNW-GTR-8., K. CROMACK, W.C.DENISON, A.MCKEE, C.MA- SER, J. SEDELL & G. JUDAY Ecological characteristics of old-growth Douglas-fir forests. U.S. Forest Service General Technical Report PNW-GTR-118. GLEASON, H. A The individualistic concept of the plant association. Bulletin of the Torrey Botanical Club 53: 1 0. GOWARD, T Nephroma occultum and the maintenance of lichen diversity in British Columbia. Mitteilungen der Eidgenössischen Forschungsanstalt für Wald, Schnee und Landschaft 70: LESICA, P., B. MCCUNE, S. COOPER & W. S. HONG Differences in lichen and bryophyte communities between old-growth and managed second-growth forests in Swan Valley, Montana. Canadian Journal of Botany 69: MCCUNE, B Gradients in epiphyte biomass in three Pseudotsuga-Tsuga forests of different ages in western Oregon and Washington. THE BRYOLOGIST 96: & M. J. MEFFORD PC-ORD. Multivariate analysis of ecological data, Version 4. MjM Software Design, Gleneden Beach, OR. PECK, J. E.& B. MCCUNE Remnant trees and canopy lichen communities in western Oregon: a retrospective approach. Ecological Applications 7: PIKE, L. H., W. C. DENISON, D.M.TRACY, M.A.SHER- WOOD & F. M. RHOADES Floristic survey of epiphytic lichens and bryophytes growing on old-growth conifers in western Oregon. THE BRYOLOGIST 78: RHOADES, F. M Distribution of thalli in a population of the epiphytic lichen Lobaria oregana and a model of population dynamics and production. THE BRYOL- OGIST 86: SAS INSTITUTE JMP 3.. Cary, NC. SILLETT, S. C Branch epiphyte assemblages in the forest interior and on the clearcut edge of a 700-yearold forest canopy in western Oregon. THE BRYOLOGIST 98: & M. N. GOSLIN Distribution of epiphytic lichens in relation to remnant trees in a multiple-age
9 000] SILLETT ET AL.: EPIPHYTE COLONIZATION 669 Douglas-fir forest. Canadian Journal of Forest Research 9: & T. GOWARD Ecology and conservation of Pseudocyphellaria rainierensis, a Pacific Northwest endemic lichen, pp In M. G. Glenn, R. C. Harris, R. Dirig & M. S. Cole (eds.), Lichenographia Thomsoniana. Mycotaxon Ltd., Ithaca, NY. & B. MCCUNE Survival and growth of cyanolichen transplants in Douglas-fir forest canopies. THE BRYOLOGIST 101: 0 31.,, J. E. PECK, T.R.RAMBO &A.RUCHTY Dispersal limitations of epiphytic lichens result in species dependent on old-growth forests. Ecological Applications 10: & P. N. NEITLICH. Emerging themes in epiphyte research in westside forests with special reference to the cyanolichens. Northwest Science 70 Special Issue: & T. R. RAMBO Vertical distribution of dominant epiphytes in Douglas-fir forests of the central Oregon Cascades. Northwest Science 74: SOKAL, R. R.& F. J. ROHLF Biometry, 3rd ed. W. H. Freeman & Company, NY. TIBELL, L. B Distribution patterns and dispersal strategies of Caliciales. Botanical Journal of the Linnean Society 116: ms. submitted Jan. 1, 000; accepted July 4, 000.
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