Next Article in Journal
Seasonal Phenotypic Variation in the Aeolian Wall Lizard, Podarcis raffonei, of the Capo Grosso (Vulcano) Population
Previous Article in Journal
Exploring the Genetic Structure and Phylogeographic Patterns of the Copepod Genus Eurytemora in Europe
Previous Article in Special Issue
Genetic Variation among Rare Florida Endemic Hymenocallis henryae Populations and the Implication for Conservation and Management
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Diversity
Volume 16
Issue 8
10.3390/d16080484
diversity-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Diversity Begets Diversity: Structural Heterogeneity Determines Fine-Scale Epiphyte Community Structure in a Temperate Rainforest

by
Kaela M. Hamilton
and
Carrie L. Woods
*
Biology Department, University of Puget Sound, Tacoma, WA 98416, USA
*
Author to whom correspondence should be addressed.
Diversity 2024, 16(8), 484; https://doi.org/10.3390/d16080484
Submission received: 25 June 2024 / Revised: 4 August 2024 / Accepted: 7 August 2024 / Published: 9 August 2024
(This article belongs to the Special Issue Plant Diversity Hotspots in the 2020s)
Browse Figures
Versions Notes

Abstract

:
A foundational concept in ecology is the positive relationship between habitat heterogeneity and species diversity. Epiphytes demonstrate microhabitat specialization to particular areas within a tree; thus, epiphyte communities are potentially influenced by the structural heterogeneity of host trees. We evaluated the relationship between structural features of Acer macrophyllum and epiphyte distributions and abundance in a temperate rainforest in Washington, USA. Epiphytes and structural features of three Acer macrophyllum trees were systematically surveyed using the point-intercept method from the base to the crown and on three branches for each tree. Rarefied species richness increased with structural richness. Species richness along the trunk differed significantly among types of structural features (i.e., broken branches, burls, holes, rivets, branches, and trunks); broken branches had the highest species richness and branches had the lowest, followed by trunks. Rarefied species richness increased with height and peaked at 12 m, but the relationship between structural diversity and height was not significant. The species that occurred on branches were different to those that occurred on trunks, and species composition varied significantly among trunk features. The high structural diversity in northern temperate rainforest trees influenced the fine-scale distribution of nonvascular epiphytes and may explain their coexistence in tree crowns.

1. Introduction

The habitat heterogeneity hypothesis posits that environmental complexity can promote species diversity and coexistence by offering a greater diversity of niches and reducing competitive exclusion [1,2,3,4]. Structural complexity, defined as the variation in the physical three-dimensional structure of an ecosystem, has been found to influence patterns of diversity in coral reefs [5,6], marine rocky shores [7], temperate forests [8], and canopy systems [9,10], among others. The variety of microhabitats that are generated by fine-scale structurally heterogeneous environments allow for specialization and, as a result, more diverse communities. Many studies have found that key structural components contribute disproportionately to diversity, such as particular coral species [6], large trees in human-modified landscapes [9,10,11], soil in tropical canopy trees [12,13], and rocks and crevices in intertidal zones [7]. Identifying these important keystone structures can be crucial for maintaining biodiversity and informing conservation efforts.
Large, old trees are critical components and keystone ecological structures of many ecosystems worldwide [9,14,15]. Their complex three-dimensional structures create a variety of microhabitats that influence the diversity and distribution of both fauna [2,16,17] and flora [12,15,18,19,20,21]. Epiphytes, structurally dependent non-parasitic plants, are distributed non-randomly within tree crowns due to their associations with microhabitats [1,2,3] created by gradients in light, relative humidity, substrate types, and structural features among different areas of the tree [12,18,20,22,23,24]. Bark traits and tree architecture have been found to influence epiphyte communities [25,26,27,28], and tree size is known to be a predictor of epiphyte species richness [12,29,30,31]. However, the specific structural features of host trees that determine these preferences require further investigation [32].
Although much of the research focusing on epiphytic microhabitat associations has occurred in tropical rainforests (e.g., [12,20,33]), epiphyte distributions in temperate rainforests can also be influenced by tree factors [18,21,22,34,35,36]. In coastal temperate rainforests in New Zealand, distinct epiphyte communities were found among different areas of host trees, including trunks, inner branches, and outer branches [36,37]. Epiphyte distributions in Acer macrophyllum trees in Pacific Northwest northern temperate rainforests were found to be non-random across broad-scale Johansson zones, with distinct epiphyte communities on trunks and branches [18]. In Nothofagus temperate rainforests in the Chilean Andes, fine-scale epiphyte community composition varied with tree height, with some species restricted to trunks or branches [21]. These patterns have been hypothesized to be due to either physiological or morphological adaptations of epiphytes to variations in microclimate, particularly sunlight and water availability differences from the upper to lower parts of trees [21,37]. However, other studies have found structural features, such as the number and size of branches, to be more important than microclimate in determining epiphyte distributions [18,38].
Explorations of fine-scale distribution patterns, including the contribution of structural features to epiphyte community patterns and how these structural features vary within trees, are needed to fully understand the relationship between host structural heterogeneity and epiphyte communities. They may also determine the key attributes of host trees for maintaining epiphyte biodiversity and inform forestry and conservation initiatives. The objective of this study was to evaluate the relationship between epiphyte community structure and host tree structural heterogeneity at a very fine scale in a northern temperate rainforest, where the epiphyte community was made up primarily of bryophytes. We surveyed epiphyte communities every meter from the base to as far up each of three trees as was logistically feasible, as well as every meter along at least three branches in each tree. We noted any structural features with each survey, including branches, broken branches, burls, holes, and rivets. We tested the hypothesis that epiphyte species richness and composition would be impacted by variations in host tree structural and spatial heterogeneity. We predicted that epiphyte species richness would increase with higher structural diversity and that epiphyte species would be specialized to unique microhabitats generated by host tree structures.

2. Materials and Methods

2.1. Study Area

Our study was conducted in the Hoh Rainforest just outside the entrance to the Olympic National Park in the Hoh River valley, Washington, USA (47°52′15″ N, 123°55′52″ W; Figure 1). The site is a flood plain along the Hoh River dominated by large bigleaf maples (Acer macrophyllum) with scattered Sitka spruce (Picea sitchensis) in the overstory and vine maple (Acer circinatum) and western sword fern (Polystichum munitum) in the understory. The climate is mild and wet, with temperatures fluctuating between −7 and 21 °C (average temperature: 10 °C) and the average precipitation fluctuating between 320 and 344 cm [39,40]. Within this temperate rainforest, Acer macrophyllum trees support more epiphyte biomass than any other tree in the Pacific Northwest, and the biomass of epiphytes can be four times that of their host tree’s foliage [41]. Therefore, Acer macrophyllum was selected as the focal host species for this study.

2.2. Study Design and Data Collection

Three large (>95 cm dbh) Acer macrophyllum trees were selected from a grove of approximately 20 maple trees. The three trees in this study were chosen based on previous findings of non-random distributions of epiphytes within trees across broad Johansson zones [18], the feasibility of establishing two clear climbing lines to allow access to all areas of the trunks, the absence of any dramatic lean or fork in the trunks, and clear access to at least three live branches.
To examine the effect of fine-scale structural and spatial characteristics of Acer macrophyllum on epiphyte community structure, the three trees were systematically surveyed every meter up the trunk until it was not feasible to climb any higher (12–17 m) and every meter along three branches for three meters (0 m, 1 m, and 2 m). The trees were climbed using single-rope climbing techniques [42]. The point-intercept method was used to measure the percent cover of epiphytes by identifying the epiphyte species and substrate type (i.e., bark or detritus) under each of 100 random dots on a 22 × 28 cm acetate sheet. The acetate sheets were connected using CommandTM strips (3M, Maplewood, MN, USA) and wrapped around the entire circumference of the trunk and branches at every meter. We conducted a total of 576 surveys of epiphyte communities in the three Acer macrophyllum trees across two summer field seasons.
Substrate features were noted at each height on the trunk under the corresponding acetate sheets and included broken branches, burls, holes, and rivets (i.e., cavities or ruts running vertically up the trunk). At every meter surveyed on the trunk, canopy openness and bryophyte depth were recorded at each cardinal direction and averaged to obtain a measure of canopy openness and depth at each meter. Canopy openness and bryophyte depth were found to vary in these trees across broad Johansson zones [18], so we measured them as confounding variables. On the branches, canopy openness and bryophyte depth were recorded on the tops, bottoms, and both sides (facing outwards from the trunk) for each meter surveyed. Canopy cover was measured with a spherical densiometer (Forestry Suppliers, Jackson, MS, USA), and bryophyte depth was measured using calipers or a 5 m tape. The diameter at breast height (dbh) was measured for each tree surveyed and at each meter along the branches. Because previous research on these trees found no significant differences in microclimate (i.e., temperature, relative humidity, and vapor pressure deficit) across Johansson zones [18] or fine-scale distances (every 0.5 m; Woods, unpublished data), we did not include microclimatic variables in our study.

2.3. Statistical Analyses

We measured rarefied species richness as the total number of species found in each 1 m survey while accounting for the total area surveyed, and we measured structural richness as the number of structural features (i.e., broken branches, burls, holes, rivets, and branches) found at each 1 m survey. To evaluate the relationship between rarefied species richness and structural richness on the trunk, we used linear regression. A one-way ANOVA analysis was used to evaluate how rarefied species richness varied among structural features and was followed by Tukey HSD tests for pairwise comparisons across structures. We used two-way ANOVAs to determine if the way that structure affected richness depended on individual trees or heights in trees. Non-linear regressions were conducted to evaluate the relationship between structural richness and height and between rarefied species richness and height. For the analysis of structural richness and height, both variables were square-root-transformed to meet the normality assumptions of the model.
Non-metric multi-dimensional scaling (NMDS) ordination was used to evaluate variation in species composition among structural and spatial features (i.e., trunks, broken branches, burls, holes, and rivets, as well as the tops, sides, and bottoms of branches). We used the Morista–Horn index with 1000 iterations using the vegan package in R [43]. We tested whether the NMDS was significantly different from random using the Monte Carlo test with 1000 iterations. To be considered statistically different from random, the stress level of the Monte Carlo test had to be larger than the NMDS stress level [44]. We examined whether bryophyte depth, canopy openness, and height in tree correlated with variations in species composition using the envfit() function in the vegan package with 1000 iterations [43]. The direction of vectors represents their maximum correlation with the ordination axes and their length represents the strength of the correlation. We used the adonis function in the vegan package and the pairwiseAdonis package in github to test for significant differences in species composition among structures and branch zones with 1000 permutations [43,45]. Statistical analyses were performed using R v. 4.0.2 or R v. 4.2.0 in RStudio [46].

3. Results

Overall, we found a total of 22 species, which were mostly bryophytes, including 16 mosses and 3 liverworts. In addition, we also found one lichen and two vascular plant species (one lycophyte and one fern) (Table 1). Bryophyte species showed specialization to structures on the trunks and to zones on the branches. While most bryophyte species were found on the trunk, the mosses Antitrichia curtipendula, Hylocomium splendens, and Rhytidiadelphus loreus had a higher average percent cover on trunk structures than on the trunk, and the liverwort Scapania bolanderi was only found on burls. In contrast, the mosses Claopodium crispifolium, Hypnum subimponens, and Metaneckera menziesii and the lichen Lepraria spp. had the greatest percent covers on trunks. Polypodium glycerrhiza, the only epiphytic fern, was found exclusively on trunks, although by June and July in the Hoh Rainforest, this species has lost its leaves and its rhizome is buried under moss mats, so this is likely an underestimate. Among branch zones, bryophyte species also showed specialization. The mosses Antitrichia curtipendula, Dicranum fuscenscens, Kindbergia oregana, Kindbergia praelonga, Neckera douglasii, and Rhytidiadelphus triquestrus were restricted to the sides of branches, and this pattern was also observed for Lepraria spp. Except for the moss Kindbergia oregana, these species were also abundant on trunks, which suggests a preference for vertical structures.

3.1. Effect of Structure

Rarefied species richness increased as the number of structural features increased (linear regression, F1,35 = 7.66, p = 0.009; Figure 2). Further, rarefied species richness significantly varied among types of structures (one-way ANOVA, F5,447 = 22.43, p < 0.001; Figure 2). Mean (±SE) rarefied species richness was highest on broken branches (4.32 ± 0.28) and lowest on branches (2.28 ± 0.08), followed by trunks (3.03 ± 0.09; Figure 2). Rarefied species richness on holes, burls, and rivets was also higher than on bare trunks (Figure 2). Rarefied species richness on trunks was 28.25% higher than richness on branches (p < 0.001), but 25.36% lower than on burls (p < 0.001) and 35.10% lower than on broken branches (p = 0.006). In addition, rarefied species richness on branches was 44.90% lower than on rivets (p = 0.014), 52.67% lower than on burls (p < 0.001), and 61.82% lower than on broken branches (p < 0.001). All other pairwise comparisons among structures were not statistically different from each other. The way that structure affected richness did not depend on the tree (two-way ANOVA, F5, = 0.54, p = 0.74) and it did not depend on height (two-way ANOVA, F4 = 2.21, p = 0.071), indicating that the patterns of species richness and structure were consistent across trees and heights.

3.2. Effect of Height

Average rarefied species richness showed a non-linear relationship with height in the trees and reached a maximum at 12 m (non-linear regression, F1,149 = 4.89, p = 0.029; Figure 3). Average structural richness demonstrated a similar trend with height, but the effect was not significant (non-linear regression, F2,36 = 0.44, p = 0.648; Figure 3).
Species varied in their percent covers along the trunks with height in the trees (Figure 4). Metaneckera menziesii and Isothecium myosuroides were found in almost equal abundance across all heights on the trunk (Figure 4). Leucolepis acanthaneuron occurred on the lower parts of the trunk, while Porella navicularis, Selaginella oregana, Rhytidiadelphus loreus, and Hypnum subimponens occurred higher up the trunk (Figure 4).

3.3. Species Distributions

Our NMDS was significantly different from random (stress = 0.16, Monte Carlo stress = 0.26; Figure 5). There were significant differences in species composition among trunk structures and branch zones (Adonis, R2 = 0.43, F7,253 = 26.93, p < 0.001), which were supported by the lack of overlap in species composition between all trunk structures and branches and the pairwise comparisons that showed that the trunks and trunk structures were all significantly different from the branches (pairwiseAdonis, p < 0.001). Among the trunk structures, the composition on the trunk was significantly different from that on burls (pairwiseAdonis, R2 = 0.04, F1,136 = 6.02, p < 0.001) and broken branches (pairwiseAdonis, R2 = 0.03, F1,113 = 3.82, p = 0.005), and the composition on rivets was significantly different from that on broken branches (pairwiseAdonis, R2 = 0.24, F1,10 = 2.88, p = 0.027; Figure 5). While there was some overlap in species composition among trunk structures, species composition could vary in another dimension, which could explain the significant differences. All branch zones were significantly different from each other (pairwiseAdonis, p < 0.001). Species composition was significantly related to bryophyte depth (MD; r2 = 0.28, p < 0.001) and height (r2 = 0.37, p < 0.001), both of which were highest on branches. Species composition did not significantly relate to canopy openness (CO, r2 = 0.02, p = 0.06).

4. Discussion

The positive effect of structural complexity on species richness and diversity is well documented across ecosystems [5,6,12,47]. Our results on epiphytes in a northern temperate rainforest, which were mostly composed of bryophytes, support this trend in the literature, as species richness increased with increasing structural richness. It has been long established in the literature that epiphytes are found in different microhabitats within trees [12,19,48]. Here, we provide evidence that fine-scale structural heterogeneity created by particular structures within a tree explains non-random patterns of epiphyte community structure and species distributions.
We found support for the prediction that epiphytes would be specialized to unique structural features of the trees. Broadly, we found distinct epiphyte communities on the trunks and branches, consistent with previous findings from other studies in temperate rainforests [18,21,37]. The epiphyte species on the trunks were primarily bryophytes but also included the lichen Lepraria spp. and a fern. On the trunks, richness varied significantly with the presence of structural features. Rarefied species richness on branches and bare trunks was surprisingly low compared to all other trunk structures, and, further, richness varied among types of structural features. The mosses Metaneckera menziesii and Isothecium myosuroides dominated the trunks and were quite rare on trunk structures, which suggests a preference for vertical substrates. These findings are consistent with those of other studies which found that M. menziesii and I. myosuroides were abundant on trunk surfaces [22,49]. Broken branches and burls were covered with epiphytes and had the greatest numbers of species on them, including some species that were specialized to these structures. These results are supported by other studies in the Pacific Northwest and elsewhere that found the highest covers of epiphytes on the oldest structures closest to the trunk [12,34,50]. The bryophytes Antitrichia curtipendula, Rhytidiadelphus loreus, and Scapania bolanderi were most abundant on burls, and Hylocomium splendens was most abundant on broken branches. A. curtipendula and R. loreus are large mosses that form bushy mats on horizontal surfaces, whereas S. bolanderi is a small liverwort that forms tufts or turfs and often occurs on the sides of trees or logs and on tree trunks [49,51,52]. Thus, burls may offer a variety of microhabitats that support large mat-forming bryophyte species on the top and small, turf-forming species on the sides and bottom. H. splendens is a large feather moss that is very abundant on old, decaying logs and on the forest floor in this forest [39,51]. Thus, it may be able to colonize the horizontal surfaces that broken branches offer. The specialization of species to structures along the trunk supports structural richness as a driver of species richness.
Fine-scale partitioning of tree crowns was evident on branches, as species composition varied across the tops, sides, and bottoms of branches. Branches were dominated by particular bryophyte species, as well as one vascular plant species. The mosses Claopodium crispifolium, Hypnum subimponens, and Leucolepis acanthaneuron were restricted to the tops of branches, while seven species were restricted to the sides of branches. The most abundant species on the tops of branches were the mosses Rytidiadelphus loreus and L. acanthaneuron, while the most abundant on the sides were R. loreus and Metaneckera menziesii, which supports the notion that M. menziesii is a vertical specialist. R. loreus forms large bushy mats on large branches close to the trunk, which suggests that it requires a large surface area and might be a competitive dominant on old branches. The bottoms of the branches were dominated by Selaginella oregana and Isothecium myosuroides. S. oregana is a pendulous lycophyte that requires canopy soil to root into. Canopy soil forms on burls, broken branches, along the trunk, and on large branches [37,41]. S. oregana was found on all these structures, suggesting canopy soil presence as a requirement for S. oregana establishment. I. myosuroides has dimorphic phyllids that form both tufts close to the bark and pendulous, stringy tails that hang below branches. Pendant bryophytes and vascular epipihytes have been found hanging below branches in other systems [12,37]. Thus, S. oregana and I. myosuroides hang in large mats below branches, which explains their dominance on the bottoms of branches as well as the greater bryophyte depth in this zone.
Rarefied epiphyte species richness increased with height but was highest at intermediate–upper trunk zones. A concentration of epiphytes at intermediate heights in a tree is a common trend across systems [19,34,53,54] and could be due to various factors. Some researchers have suggested that this relationship is due to gradients in abiotic factors, such as humidity and light, with height in the tree [12,19,21,22,37], while others found structural features to be more important [18,38]. We found support for the prediction that epiphyte species richness is correlated with structural richness because structural richness also peaked at intermediate heights on the trunk. Microclimate was found not to vary with broad-scale zones or correlate with epiphyte communities in our system [18]. Acer macrophyllum trees are much shorter than the dominant conifers that surround them, such as Picea sitchensis (Sitka spruce) and Pseudotsuga menziesii (Douglas fir), and they are therefore considered part of the understory. We found support for this in the lack of a significant relationship of canopy cover with species composition in the NMDS. As a result, there is likely less of a gradient in microclimate and light than in other temperate rainforests where trees are much taller [21,37]. The positive relationships between structural richness and height and between structural richness and epiphyte richness in our study suggest that structural heterogeneity is more important than height in influencing the vertical distribution of epiphytes in these northern temperate rainforest trees.
The unique structures within a tree likely create microhabitats to which epiphyte species can become specialized. Thus, trees with more structural complexity should, in theory, support a greater diversity of epiphytes. While strict host specificity is uncommon in epiphytes [32,33,55,56], network analyses of epiphytes and host trees reveal that epiphyte–host relationships are not completely random [32,57,58,59,60]. Epiphyte colonization patterns are known to be impacted by bark traits [26,27,32,61,62] and tree architecture [28]. Epiphyte richness and diversity also increase with tree size due to increased time for colonization and increased heterogeneity in old tree crowns (e.g., [10,29,61]). Microhabitat partitioning of trees by epiphytes may also be favored under more constant environmental conditions [63], such as those found in our study system and others [37,38]. This study builds on this research by highlighting the importance of structurally diverse trees in the maintenance of epiphyte diversity. Given our finding of the contribution of particular structural components of large, old-growth trees to epiphyte richness, our study provides further support for the protection of large, old trees with complex architectures [9,14,28].

Author Contributions

C.L.W. conceived the research idea; K.M.H. and C.L.W. collected the data; K.M.H. and C.L.W. performed the statistical analyses; K.M.H., with contributions from C.L.W., wrote the paper; both authors discussed the results and commented on the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

Funding was provided by the M.J. Murdock Charitable Trust (reference number: 2015293:MNL:2/25/2016), the University of Puget Sound Summer Research Grants for undergraduate students in the Sciences and Math to K.M.H., and the University of Puget Sound Biology department.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The original contributions presented in the study are included in the article, further inquiries can be directed to the corresponding author.

Acknowledgments

We are grateful to Anna Marchand and Sean Grealish for help with data collection in the field and to the Hoh River Trust and the Nature Conservancy for access to our field site and for allowing us to climb the trees. We thank the Olympic Natural Resources Center in Forks, Washington, for logistics.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Hutchinson, G.E. Homage to Santa Rosalina or Why Are There So Many Kinds of Animals? Am. Nat. 1959, 93, 145–159. [Google Scholar] [CrossRef]
  2. MacArthur, R.H.; MacArthur, J.W. On Bird Species Diversity. Ecology 1961, 42, 594–598. [Google Scholar] [CrossRef]
  3. Rosenzweig, M.L. Species Diversity in Space and Time; Cambridge University Press: Cambridge, UK, 1995. [Google Scholar]
  4. Stein, A.; Gerstner, K.; Kreft, H. Environmental Heterogeneity as a Universal Driver of Species Richness across Taxa, Biomes and Spatial Scales. Ecol. Lett. 2014, 17, 866–880. [Google Scholar] [CrossRef] [PubMed]
  5. Graham, N.A.J.; Nash, K.L. The Importance of Structural Complexity in Coral Reef Ecosystems. Coral Reefs 2013, 32, 315–326. [Google Scholar] [CrossRef]
  6. Messmer, V.; Jones, G.P.; Munday, P.L.; Holbrook, S.J.; Schmitt, R.J.; Brooks, A.J. Habitat Biodiversity as a Determinant of Fish Community Structure on Coral Reefs. Ecology 2011, 92, 2285–2298. [Google Scholar] [CrossRef] [PubMed]
  7. Firth, L.B.; Crowe, T.P. Competition and Habitat Suitability: Small-Scale Segregation Underpins Large-Scale Coexistence of Key Species on Temperate Rocky Shores. Oecologia 2010, 162, 163–174. [Google Scholar] [CrossRef] [PubMed]
  8. Franklin, J.F.; Van Pelt, R. Spatial Aspects of Structural Complexity in Old-Growth Forests. J. For. 2004, 102, 22–28. [Google Scholar] [CrossRef]
  9. Stagoll, K.; Lindenmayer, D.B.; Knight, E.; Fischer, J.; Manning, A.D. Large Trees Are Keystone Structures in Urban Parks. Conserv. Lett. 2012, 5, 115–122. [Google Scholar] [CrossRef]
  10. Yamaura, Y.; Unno, A.; Royle, J.A. Sharing Land via Keystone Structure: Retaining Naturally Regenerated Trees May Efficiently Benefit Birds in Plantations. Ecol. Appl. 2023, 33, e2802. [Google Scholar] [CrossRef]
  11. Manning, A.D.; Fischer, J.; Lindenmayer, D.B. Scattered Trees Are Keystone Structures—Implications for Conservation. Biol. Conserv. 2006, 132, 311–321. [Google Scholar] [CrossRef]
  12. Woods, C.L.; Cardelús, C.L.; DeWalt, S.J. Microhabitat Associations of Vascular Epiphytes in a Wet Tropical Forest Canopy. J. Ecol. 2015, 103, 421–430. [Google Scholar] [CrossRef]
  13. Victoriano-Romero, E.; Valencia-Díaz, S.; García-Franco, J.G.; Mehltreter, K.; Toledo-Hernández, V.H.; Flores-Palacios, A. Interactions between Epiphytes during Canopy Soil Formation: An Experiment in a Lower Montane Cloud Forest of Southeast Mexico. Plant Biol. 2023, 25, 468–477. [Google Scholar] [CrossRef] [PubMed]
  14. Lindenmayer, D.B.; Laurance, W.F.; Franklin, J.F.; Likens, G.E.; Banks, S.C.; Blanchard, W.; Gibbons, P.; Ikin, K.; Blair, D.; McBurney, L.; et al. New Policies for Old Trees: Averting a Global Crisis in a Keystone Ecological Structure. Conserv. Lett. 2014, 7, 61–69. [Google Scholar] [CrossRef]
  15. Azuma, W.A.; Komada, N.; Ogawa, Y.; Ishii, H.; Nakanishi, A.; Noguchi, Y.; Kanzaki, M. One Large Tree Crown Can Be Defined as a Local Hotspot for Plant Species Diversity in a Forest Ecosystem: A Case Study in Temperate Old-Growth Forest. Plant Ecol. 2022, 223, 99–112. [Google Scholar] [CrossRef]
  16. Emmons, L.H. Ecology and Resource Partitioning among Nine Species of African Rain Forest Squirrels. Ecol. Monogr. 1980, 50, 31–54. [Google Scholar] [CrossRef]
  17. Sushma, H.S.; Singh, M. Resource Partitioning and Interspecific Interactions among Sympatric Rain Forest Arboreal Mammals of the Western Ghats, India. Behav. Ecol. 2006, 17, 479–490. [Google Scholar] [CrossRef]
  18. Woods, C.L.; Nevins, L.M.; Didier, E.J. Structural Heterogeneity of Trees Influences Epiphyte Distributions in a Northern Temperate Rainforest. J. Veg. Sci. 2019, 30, 1134–1142. [Google Scholar] [CrossRef]
  19. Johansson, D. Ecology of Vascular Epiphytes in West African Rain Forest. Acta Phytogeogr. Suec. 1974, 59, 1–136. [Google Scholar]
  20. Hietz, P.; Hietz-Seifert, U. Structure and Ecology of Epiphyte Communities of a Cloud Forest in Central Veracruz, Mexico. J. Veg. Sci. 1995, 6, 719–728. [Google Scholar] [CrossRef]
  21. Mellado-Mansilla, D.; León, C.A.; Ortega-Solís, G.; Godoy-Güinao, J.; Moreno, R.; Díaz, I.A. Vertical Patterns of Epiphytic Bryophyte Diversity in a Montane Nothofagus Forest in the Chilean Andes. N. Z. J. Bot. 2017, 55, 514–529. [Google Scholar] [CrossRef]
  22. Kenkel, N.C.; Bradfield, G.E. Epiphytic Vegetation on Acer macrophyllum: A Multivariate Study of Species-Habitat Relationships. Vegetatio 1986, 68, 43–53. [Google Scholar] [CrossRef]
  23. Bartels, S.F.; Chen, H.Y.H. Mechanisms Regulating Epiphytic Plant Diversity. Crit. Rev. Plant Sci. 2012, 31, 391–400. [Google Scholar] [CrossRef]
  24. Zimmerman, J.K.; Olmsted, I.C. Host Tree Utilization by Vascular Epiphytes in a Seasonally Inundated Forest (Tintal) in Mexico. Biotropica 1992, 24, 402. [Google Scholar] [CrossRef]
  25. Elias, J.P.C.; Mortara, S.R.; Nunes-Freitas, A.F.; Van den Berg, E.; Ramos, F.N. Host Tree Traits in Pasture Areas Affect Forest and Pasture Specialist Epiphyte Species Differently. Am. J. Bot. 2021, 108, 598–606. [Google Scholar] [CrossRef] [PubMed]
  26. Callaway, R.M.; Reinhart, K.O.; Moore, G.W.; Moore, D.J.; Pennings, S.C. Epiphyte Host Preferences and Host Traits: Mechanisms for Species-Specific Interactions. Oecologia 2002, 132, 221–230. [Google Scholar] [CrossRef] [PubMed]
  27. Wyse, S.V.; Burns, B.R. Short Communication: Do Host Bark Traits Influence Trunk Epiphyte Communities? N. Z. J. Ecol. 2011, 35, 296–301. [Google Scholar]
  28. Izuddin, M.; Webb, E.L. The Influence of Tree Architecture, Forest Remnants, and Dispersal Syndrome on Roadside Epiphyte Diversity in a Highly Urbanized Tropical Environment. Biodivers. Conserv. 2015, 24, 2063–2077. [Google Scholar] [CrossRef]
  29. Zotz, G.; Vollrath, B. The Epiphyte Vegetation of the Palm Socratea exorrhiza-Correlations with Tree Size, Tree Age and Bryophyte Cover. J. Trop. Ecol. 2003, 19, 81–90. [Google Scholar] [CrossRef]
  30. Adhikari, Y.P.; Hoffmann, S.; Kunwar, R.M.; Bobrowski, M.; Jentsch, A.; Beierkuhnlein, C. Vascular Epiphyte Diversity and Host Tree Architecture in Two Forest Management Types in the Himalaya. Glob. Ecol. Conserv. 2021, 27, e01544. [Google Scholar] [CrossRef]
  31. Zhao, M.; Geekiyanage, N.; Xu, J.; Khin, M.M.; Nurdiana, D.R.; Paudel, E.; Harrison, R.D. Structure of the Epiphyte Community in a Tropical Montane Forest in SW China. PLoS ONE 2015, 10, e0122210. [Google Scholar] [CrossRef]
  32. Wagner, K.; Mendieta-Leiva, G.; Zotz, G. Host Specificity in Vascular Epiphytes: A Review of Methodology, Empirical Evidence and Potential Mechanisms. AoB Plants 2015, 7, plu092. [Google Scholar] [CrossRef] [PubMed]
  33. Spicer, M.E.; Woods, C.L. A Case for Studying Biotic Interactions in Epiphyte Ecology and Evolution. Perspect. Plant Ecol. Evol. Syst. 2022, 54, 125658. [Google Scholar] [CrossRef]
  34. Lyons, B.; Nadkarni, N.M.; North, M.P. Spatial Distribution and Succession of Epiphytes on Tsuga heterophylla (Western Hemlock) in an Old-Growth Douglas-Fir Forest. Can. J. Bot. 2000, 78, 957–968. [Google Scholar]
  35. Király, I.; Nascimbene, J.; Tinya, F.; Ódor, P. Factors Influencing Epiphytic Bryophyte and Lichen Species Richness at Different Spatial Scales in Managed Temperate Forests. Biodivers. Conserv. 2013, 22, 209–223. [Google Scholar] [CrossRef]
  36. Dickinson, K.J.M.; Mark, A.F.; Dawkins, B. Ecology of Lianoid/Epiphytic Communities in Coastal Podocarp Rain Forest, Haast Ecological District, New Zealand. J. Biogeogr. 1993, 20, 687. [Google Scholar] [CrossRef]
  37. Hofstede, R.G.M.; Dickinson, K.J.M.; Mark, A.F. Distribution, Abundance and Biomass of Epiphyte-Lianoid Communities in a New Zealand Lowland Nothofagus-Podocarp Temperate Rain Forest: Tropical Comparisons. J. Biogeogr. 2002, 28, 1033–1049. [Google Scholar] [CrossRef]
  38. Clement, J.P.; Shaw, D.C. Crown Structure and the Distribution of Epiphyte Functional Group Biomass in Old-Growth Pseudotsuga menziesii Trees. Ecoscience 1999, 6, 243–254. [Google Scholar] [CrossRef]
  39. Harmon, M.E.; Franklin, J.F. Tree Seedlings on Logs in Picea-Tsuga Forests of Oregon and Washington. Ecology 1989, 70, 48–59. [Google Scholar] [CrossRef]
  40. East, A.E.; Jenkins, K.J.; Happe, P.J.; Bountry, J.A.; Beechie, T.J.; Mastin, M.C.; Sankey, J.B.; Randle, T.J. Channel-Planform Evolution in Four Rivers of Olympic National Park, Washington, USA: The Roles of Physical Drivers and Trophic Cascades. Earth Surf. Process. Landf. 2017, 42, 1011–1032. [Google Scholar] [CrossRef]
  41. Nadkarni, N.M. Biomass and Mineral Capital of Epiphytes in an Acer macrophyllum Community of a Temperate Moist Coniferous Forest, Olympic Peninsula, Washington State. Can. J. Bot. 1984, 62, 2223–2228. [Google Scholar] [CrossRef]
  42. Perry, D.R. A Method of Access into the Crowns of Emergent and Canopy Trees. Biotropica 1978, 10, 155–157. [Google Scholar] [CrossRef]
  43. Oksanen, J.; Simpson, G.B.; Blanchet, F.G.; Kindt, R.; Legendre, P.; Wagner, H.; Barbour, M.; Bedward, M.; Bolker, B.; Borcard, D.; et al. Vegan, Community Ecology PackageR Package version 2.6-7. 2024. Available online: https://github.com/vegandevs/vegan (accessed on 20 July 2024).
  44. McCune, B.; Grace, J.B. Analysis of Ecological Communities; MjM Software Design: Gleneden Beach, OR, USA, 2002; ISBN 0972129006. [Google Scholar]
  45. Martinez Arbizu, P. pairwiseAdonis, Version 0.4.1; Pairwise Multilevel Comparison Using Adonis; R Package. 2020. Available online: https://github.com/pmartinezarbizu/pairwiseAdonis (accessed on 20 July 2024).
  46. R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2022. [Google Scholar]
  47. Schneider, K.N.; Winemiller, K.O. Structural Complexity of Woody Debris Patches Influences Fish and Macroinvertebrate Species Richness in a Temperate Floodplain-River System. Hydrobiologia 2008, 610, 235–244. [Google Scholar] [CrossRef]
  48. Freiberg, M. Spatial Distribution of Vascular Epiphytes on Three Emergent Canopy Trees in French Guiana. Biotropica 1996, 28, 345–355. [Google Scholar] [CrossRef]
  49. Hoffman, G.R.; Kazmierski, R.G. An Ecologic Study of Epiphytic Bryophytes and Lichens on Pseudotsuga menziesii on the Olympic Peninsula, Washington I. A Description of the Vegetation. Bryologist 1969, 72, 149–169. [Google Scholar] [CrossRef]
  50. Ingram, S.W.; Nadkarni, N.M. Composition and Distribution of Epiphytic Organic Matter in a Neotropical Cloud Forest, Costa Rica. Biotropica 1993, 25, 370. [Google Scholar] [CrossRef]
  51. Woods, C.L.; Maleta, K.; Ortmann, K. Plant–Plant Interactions Change during Succession on Nurse Logs in a Northern Temperate Rainforest. Ecol. Evol. 2021, 11, 9631–9641. [Google Scholar] [CrossRef]
  52. Fukasawa, Y.; Ando, Y. Species Effects of Bryophyte Colonies on Tree Seedling Regeneration on Coarse Woody Debris. Ecol. Res. 2018, 33, 191–197. [Google Scholar] [CrossRef]
  53. Zotz, G.; Schultz, S. The Vascular Epiphytes of a Lowland Forest in Panama—Species Composition and Spatial Structure. Plant Ecol. 2008, 195, 131–141. [Google Scholar] [CrossRef]
  54. Wang, X.; Long, W.; Schamp, B.S.; Yang, X.; Kang, Y.; Xie, Z.; Xiong, M. Vascular Epiphyte Diversity Differs with Host Crown Zone and Diameter, but Not Orientation in a Tropical Cloud Forest. PLoS ONE 2016, 11, e0158548. [Google Scholar] [CrossRef]
  55. Cardelús, C.L. Vascular Epiphyte Communities in the Inner-Crown of Hyeronima alchorneoides and Lecythis ampla at La Selva Biological Station, Costa Rica. Biotropica 2007, 39, 171–176. [Google Scholar] [CrossRef]
  56. Naranjo, C.; Iriondo, J.M.; Riofrio, M.L.; Lara-Romero, C. Evaluating the Structure of Commensalistic Epiphyte–Phorophyte Networks: A Comparative Perspective of Biotic Interactions. AoB Plants 2019, 11, plz011. [Google Scholar] [CrossRef] [PubMed]
  57. Burns, K.C. Meta-Community Structure of Vascular Epiphytes in a Temperate Rainforest. Botany 2008, 86, 1252–1259. [Google Scholar] [CrossRef]
  58. Taylor, A.; Burns, K. Epiphyte Community Development throughout Tree Ontogeny: An Island Ontogeny Framework. J. Veg. Sci. 2015, 26, 902–910. [Google Scholar] [CrossRef]
  59. Burns, K.C.; Zotz, G. A Hierarchical Framework for Investigating Epiphyte Assemblages: Networks, Meta-Communities, and Scale. Ecology 2010, 91, 377–385. [Google Scholar] [CrossRef] [PubMed]
  60. Laube, S.; Zotz, G. Neither Host-Specific nor Random: Vascular Epiphytes on Three Tree Species in a Panamanian Lowland Forest. Ann. Bot. 2006, 97, 1103–1114. [Google Scholar] [CrossRef] [PubMed]
  61. Shao, Y.; Wang, S.; Li, Y.; Chen, Y.; Zhao, H.; Wang, J.; Liu, F.; Yuan, Z. Importance of Bark Physicochemical Properties in an Epiphytic Bryophyte Community within a Temperate Deciduous Broadleaf Forest. Diversity 2023, 15, 688. [Google Scholar] [CrossRef]
  62. Tatsumi, S.; Ohgue, T.; Azuma, W.A.; Nishizawa, K. Bark Traits Affect Epiphytic Bryophyte Community Assembly in a Temperate Forest. Plant Ecol. 2023, 224, 1089–1095. [Google Scholar] [CrossRef]
  63. Gentry, A.H.; Dodson, C.H. Diversity and Biogeography of Neotropical Vascular Epiphytes. Ann. Mo. Bot. Gard. 1987, 74, 205–233. [Google Scholar] [CrossRef]
Diversity 16 00484 g001
Figure 1. Location of the Acer macrophyllum grove examined in this study. The star in the inset shows the location of the field site along the Hoh river.
Figure 1. Location of the Acer macrophyllum grove examined in this study. The star in the inset shows the location of the field site along the Hoh river.
Diversity 16 00484 g001
Diversity 16 00484 g002
Figure 2. There was a positive effect of structure on rarefied species richness of epiphytes in Acer macrophyllum. (a) An increase in structural richness on the trunk led to a corresponding increase in rarefied species richness of epiphytes (p = 0.009). (b) Average (±SE) rarefied species richness of epiphytes also varied among structural features (p = 0.001) and was lowest on branches and bare trunks. Bars with different letters are significantly different from each other according to a Tukey’s HSD test (p < 0.05).
Figure 2. There was a positive effect of structure on rarefied species richness of epiphytes in Acer macrophyllum. (a) An increase in structural richness on the trunk led to a corresponding increase in rarefied species richness of epiphytes (p = 0.009). (b) Average (±SE) rarefied species richness of epiphytes also varied among structural features (p = 0.001) and was lowest on branches and bare trunks. Bars with different letters are significantly different from each other according to a Tukey’s HSD test (p < 0.05).
Diversity 16 00484 g002
Diversity 16 00484 g003
Figure 3. Mean rarefied species richness (a) and structural richness (b) of epiphytes with height in Acer macrophyllum (n = 3). (a) Points represent average (±SE) rarefied epiphyte species richness with height (p = 0.014). (b) Points represent average (±SE) structural richness with height (p = 0.648).
Figure 3. Mean rarefied species richness (a) and structural richness (b) of epiphytes with height in Acer macrophyllum (n = 3). (a) Points represent average (±SE) rarefied epiphyte species richness with height (p = 0.014). (b) Points represent average (±SE) structural richness with height (p = 0.648).
Diversity 16 00484 g003
Diversity 16 00484 g004
Figure 4. Average percent cover of epiphyte species found on trunks and all trunk structures with height zones in three Acer macrophyllum trees in the Hoh Rainforest. Species found on branches were not included. See Table 1 for species codes.
Figure 4. Average percent cover of epiphyte species found on trunks and all trunk structures with height zones in three Acer macrophyllum trees in the Hoh Rainforest. Species found on branches were not included. See Table 1 for species codes.
Diversity 16 00484 g004
Diversity 16 00484 g005
Figure 5. Non-metric multidimensional scaling ordination (NMDS) of epiphyte species composition by structural features of trunks (i.e., trunks (black squares), burls (gray diamonds), broken branches (white triangles), holes (white squares), and rivets (white diamonds)) and branches (i.e., tops (black circles), sides (gray circles), and bottoms (white circles)). The Marista–Horn similarity index was used on abundance data. Ellipses show the covariance matrix centered on the mean of each structure; overlapping ellipses indicate similar species composition. Two-dimensional stress = 0.16, Monte Carlo stress with 1000 iterations = 0.26. Species codes are shown in red (see Table 1 for species codes). Environmental variables are shown as blue vectors. Bryophyte depth (MD, r2 = 0.28, p < 0.001) and height (r2 = 0.37, p < 0.001) explained a significant proportion of the variation in species composition, but canopy openness (CO, r2 = 0.02, p = 0.06) did not.
Figure 5. Non-metric multidimensional scaling ordination (NMDS) of epiphyte species composition by structural features of trunks (i.e., trunks (black squares), burls (gray diamonds), broken branches (white triangles), holes (white squares), and rivets (white diamonds)) and branches (i.e., tops (black circles), sides (gray circles), and bottoms (white circles)). The Marista–Horn similarity index was used on abundance data. Ellipses show the covariance matrix centered on the mean of each structure; overlapping ellipses indicate similar species composition. Two-dimensional stress = 0.16, Monte Carlo stress with 1000 iterations = 0.26. Species codes are shown in red (see Table 1 for species codes). Environmental variables are shown as blue vectors. Bryophyte depth (MD, r2 = 0.28, p < 0.001) and height (r2 = 0.37, p < 0.001) explained a significant proportion of the variation in species composition, but canopy openness (CO, r2 = 0.02, p = 0.06) did not.
Diversity 16 00484 g005
Table 1. Average percent cover of epiphyte species found on trunk structures and branch zones of Acer macrophyllum. For each epiphyte species, average percent cover represents the total count of a species on each trunk structure or branch zone divided by the total count of the species across all trunk structures or branch zones, averaged across the three trees surveyed.
Table 1. Average percent cover of epiphyte species found on trunk structures and branch zones of Acer macrophyllum. For each epiphyte species, average percent cover represents the total count of a species on each trunk structure or branch zone divided by the total count of the species across all trunk structures or branch zones, averaged across the three trees surveyed.
Average % Cover on Trunk Structures Average % Cover on Branches
SpeciesCodeFamilyLife FormBroken BranchBurlHoleRivetTrunk TopBottomSide
Antitrichia curtipendulaAntCurLeucodontaceaeMoss0.0025.450.000.007.88 0.000.0033.33
Apometzgeria pubescensApoPubHaplomitriaceaeLiverwort3.860.000.880.0028.60 0.000.000.00
Claopodium crispifoliumClaCriLeskeaceaeMoss0.007.650.770.7690.83 30.8822.7315.28
Dicranum fuscescensDicFusDicranaceaeMoss8.330.000.000.0058.33 0.000.0081.22
Homalothecium fulgesensHomFulBrachytheciaceaeMoss0.008.330.000.0025.00 0.000.000.00
Hylocomium slpendensHylSlpHylocomiaceaeMoss27.8313.041.380.0024.42 0.000.000.00
Hypnum subimponensHypSubHypnaceaeMoss3.277.740.000.0088.99 31.250.0018.75
Isothecium myosuroidesIsoMyoLembophyllaceaeMoss1.585.351.632.4688.90 18.7531.5445.40
Kindbergia oreganaKinOreBrachytheciaceaeMoss0.000.000.000.000.00 0.000.0033.33
Kindbergia praelongaKinPraBrachytheciaceaeMoss33.330.000.000.0033.33 0.000.0020.98
Lepraria spp.LepStereocaulaceaeLichen1.243.250.240.0095.27 0.000.0033.33
Leucolepis acanthroneuraLeuAcaMniaceaeMoss10.0614.321.381.1273.12 44.950.0010.61
Metaneckera menziesiiMetMenNeckeraceaeMoss0.053.400.281.4794.80 11.2925.7559.76
Mnium spinulosumMniSpiMniaceaeMoss0.000.000.000.0033.33 0.000.000.00
Neckera douglasiiNecDouNeckeraceaeMoss0.009.960.000.0056.71 0.000.0080.98
Plagiomnium venustrumPlaVenMniaceaeMoss0.0020.990.000.0045.68 33.330.000.00
Polypodium glycyrrhizaPolGlyPteridaceaeFern0.000.000.000.0066.67 0.000.000.00
Porella navicularisPorNavPorellaceaeLiverwort5.4616.812.470.1375.13 30.7311.0839.29
Rhytidiadelphus loreusRhyLorHylocomiaceaeMoss10.9652.390.000.0036.65 45.834.8056.26
Rhytidiadelphus triquetrusRhyTriHylocomiaceaeMoss0.000.000.000.0033.33 0.000.0012.01
Selaginella oreganaSelOreSelaginellaceaeLycophyte3.6817.461.470.7276.66 13.3342.4831.25
Scapania bolanderiScaBolScapaniaceaeLiverwort0.0033.330.000.000.00 0.000.000.00
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Hamilton, K.M.; Woods, C.L. Diversity Begets Diversity: Structural Heterogeneity Determines Fine-Scale Epiphyte Community Structure in a Temperate Rainforest. Diversity 2024, 16, 484. https://doi.org/10.3390/d16080484

AMA Style

Hamilton KM, Woods CL. Diversity Begets Diversity: Structural Heterogeneity Determines Fine-Scale Epiphyte Community Structure in a Temperate Rainforest. Diversity. 2024; 16(8):484. https://doi.org/10.3390/d16080484

Chicago/Turabian Style

Hamilton, Kaela M., and Carrie L. Woods. 2024. "Diversity Begets Diversity: Structural Heterogeneity Determines Fine-Scale Epiphyte Community Structure in a Temperate Rainforest" Diversity 16, no. 8: 484. https://doi.org/10.3390/d16080484

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop