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Lakeside riparian forests support diversity of wood fungi in managed boreal forests Atte Komonen, Mari E. Niemi, and Kaisa Junninen
Abstract: Riparian forests often have a more diverse tree species composition and more woody debris than neighboring upland forests, but little is known about their importance for the conservation of deadwood-dependent species. We studied the forest characteristics and the diversity of wood fungi (poroid Aphyllophorales) in lakeside riparian (flat and sloping topography) and upland boreal forests in eastern Finland. Riparian forests had a higher density of broadleaved trees and broadleaved debris than did upland forests. A total of 48 species of wood fungi were recorded, including eight red-listed or old-growth forest indicator species. Overall, more species and records and greater diversity were observed in the flat riparian sites than in the sloped riparian and upland sites. The mean species richness did not differ significantly among site categories, indicating greater b diversity among the flat riparian sites. Species composition was more similar between the two riparian categories than between the riparian and upland sites. Riparian sites also hosted more fungal species associated with broadleaved trees. The results show that riparian forests support the diversity of wood fungi in managed boreal forests. Diversity of deadwood-dependent organisms can be promoted by leaving wider and completely unharvested riparian buffer zones. Re´sume´ : Les foreˆts riveraines ont une composition en espe`ces arborescentes plus diversifie´e et plus de de´bris ligneux que les meˆmes foreˆts en milieu sec mais on ne connaıˆt pas leur importance pour la conservation des espe`ces qui de´pendent du bois mort. Nous avons e´tudie´ les caracte´ristiques de la foreˆt et la diversite´ des champignons lignicoles (Aphyllophorales poroı¨des) dans les foreˆts riveraines d’un lac (terrain de niveau et en pente) et dans les foreˆts bore´ales correspondantes en milieu sec dans l’est de la Finlande. Les foreˆts riveraines avaient une plus forte densite´ de feuillus et de de´bris d’espe`ces feuillues que les foreˆts en milieu sec. Au total, 48 espe`ces de champignons lignicoles ont e´te´ observe´es, incluant huit espe`ces sur la liste rouge ou indicatrices de vieilles foreˆts. Dans l’ensemble, plus d’espe`ces, une plus grande fre´quence et une plus forte densite´ ont e´te´ observe´es dans les stations riveraines de niveau que dans les stations riveraines en pente ou dans les stations en milieu sec. La richesse en espe`ces moyenne n’e´tait pas significativement diffe´rente entre les cate´gories de stations, indiquant que la diversite´ beˆta e´tait plus grande dans les stations riveraines de niveau. La composition en espe`ces e´tait plus semblable entre les deux cate´gories riveraines qu’entre les stations riveraines et les stations en milieu sec. Les stations riveraines e´taient aussi l’hoˆte de plus d’espe`ces fongiques associe´es aux espe`ces feuillues. Les re´sultats montrent que la diversite´ des champignons lignicoles dans les foreˆts bore´ales ame´nage´es de´pend des foreˆts riveraines. On peut favoriser la diversite´ des organismes qui de´pendent du bois mort en laissant des zones tampons riveraines plus larges et en n’y faisant aucune re´colte. [Traduit par la Re´daction]
Introduction Unharvested buffer zones are generally left adjacent to lakes, streams, and rivers to protect waters from sediment and nutrient flow from adjacent harvested areas (Blinn and Kilgore 2001). Riparian forests have also been found to be important for maintaining a variety of terrestrial taxa in human-modified landscapes (Sabo et al. 2005). Although over 80% of the riparian forest area in Europe and North America has been altered by forest management (Naiman et al. 1993), riparian areas may still hold significant proportion of unmanaged forests in many regions. Thus, riparian forest Received 27 February 2008. Accepted 9 July 2008. Published on the NRC Research Press Web site at cjfr.nrc.ca on 30 September 2008. A. Komonen.1 Department of Ecology, SLU, Box 7044, SE-750 07, Uppsala, Sweden. M.E. Niemi and K. Junninen. Faculty of Forest Sciences, University of Joensuu, Box 111, FI-80101, Joensuu, Finland. 1Corresponding
author (e-mail:
[email protected]).
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conservation and management have received increasing attention (Macdonald et al. 2004; Rodewald and Bakermans 2006). Many abiotic and biotic factors influence riparian forests. A complex array of edaphic influences and natural disturbances contribute to the compositional and structural complexity of plant and animal communities: water and nutrient accumulation maintain high productivity, and disturbances such as flooding, ice scouring, wind, and beaver activity create canopy gaps and woody debris (Naiman and De´camps 1997). As a natural ecotone between terrestrial and aquatic ecosystem, riparian forests are expected to have greater biodiversity than upland forests (Doyle 1990; Suzuki et al. 2002; but see Whitaker and Montevecchi 1997). Managed upland forests, in turn, can be seen as heavily disturbed ecosystems: they are often dominated by a single planted conifer species, have an even-aged structure, and have only small amounts of woody debris. In general, such forests are expected to have a low species richness and a high dominance structure typical of many disturbed ecosystems (Connell 1978; Suzuki et al. 2002).
doi:10.1139/X08-105
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Riparian forests are generally composed of broadleaved tree species (Pabst and Spies 1999; Barker et al. 2002), such as aspen, which in boreal Fennoscandia is a keystone species for biodiversity but has been largely eradicated from managed forests (Latva-Karjanmaa et al. 2007). Multiple disturbances in riparian buffers create woody debris of both coniferous and broadleaved trees (Harper and Macdonald 2001; Wimberly and Spies 2001). As the amount of coarse woody debris has decreased to about one-tenth of its pristine values in Fennoscandia (Siitonen 2001), riparian forests could provide crucial habitats for deadwood-dependent species, which constitute a large proportion of the threatened forest biota (Rassi et al. 2001). However, little is known about the biological diversity of deadwood-dwelling organisms in riparian forests. This information would increase our understanding of how the tree species composition and forest structure of riparian zones translate into diversity patterns of associated species and thus would also have implications for forest planning and management. Polypores (poroid Aphyllophorales) are wood-decaying fungi that mostly colonize weakened and dead trees. One should therefore expect that they are generally favored in riparian forests, where disturbances continuously create woody debris. The greater tree species diversity, particularly the presence of broadleaved trees, in riparian forests should further favor polypore diversity, as about 60% of the 226 species in Finland grow on broadleaved trees (Niemela¨ 2005). Many polypore species have specific microclimatic requirements in terms of water availability, temperature, and gaseous regime (Rayner and Boddy 1988). These factors are likely to differ between riparian and upland forests and thus contribute to differences in polypore species composition as well as abundances of individual species. The specific ecological conditions and continuous moderate disturbances in riparian forests should promote the diversity of species dependent on woody debris. In this paper, we studied the diversity of polyporous fungi in two types of lakeside riparian forests (different topographical positions) and in nearby upland forests in eastern Finland. We hypothesized that the riparian sites have, in comparison with the upland sites, (1) greater diversity of living and dead trees; (2) larger amount of deadwood; (3) greater polypore diversity, i.e., higher species richness and lower dominance in species abundances; and (4) a unique polypore species composition
Materials and methods Study area Our study was conducted in a managed forest landscape in eastern Finland. The study area consists of the landscape ecological plan for state-owned forests in Heina¨vesi (62826’N, 28845’E; Silvennoinen 2000), covering an area of 17 500 ha, of which 16 021 ha is forest land. The area belongs to the southern boreal vegetation zone (Ahti et al. 1968) and is characterized by a large number of small lakes. For the period 1971–2000, the mean annual precipitation was 500–700 mm and the mean annual temperature, 3.1– 4.0 8C (data from Finnish Meteorological Institute). Forests in the region are dominated by young age-classes: 65% are less than 41 years old and only 13% are over 80 years old.
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About half of the forest land is dominated by Picea abies (L.) Karst. and belongs to the Myrtillus forest site type according to Cajander (1926). Study site selection The study forests were selected based on the forestry data in the landscape ecological plan and on updated information obtained from the Finnish Forest and Park Service. Because the edge influence varies according to soil type, topography, canopy cover, and forest age (Harper et al. 2005), study sites were selected based on the following criteria: sprucedominated, mineral soil forests along lakes (1–10 ha in size); Myrtillus or Oxalis–Maianthemum type; and over 70 years old. Spruce-dominated forests were selected for the study because they host species-rich assemblages of wood fungi, particularly if there is a mixture of broadleaved trees (Penttila¨ et al. 2004; Sippola et al. 2005; Junninen and Kouki 2006), as can be expected for the riparian forests. Thirty-two riparian forest sites fulfilled the above criteria and were verified in the field. Of these, 20 were selected for the study, as the other stands were too small or were bordered by recent cuttings. As the riparian sites differed in their topography, we divided them in two categories: flat topography (slope less than 58; n = 10) and sloping topography (slope 58–258; n = 10). The riparian sites faced different compass directions, though none faced north. As control forests, we selected 10 upland sites belonging to the same forest type and age-class as the riparian sites. These were selected as close as possible to the flat riparian forests (150 m to 1 km) to minimize the potential impact of regional heterogeneity on species composition. All stands included in the study were 6.30, pmc < 0.039). The mean difference in the density of total broadleaved woody debris was 2.86 ± 1.26 ha–1 for FR versus UP sites and 3.22 ± 1.26 ha–1 for SR versus UP sites. There were significant differences among the three categories in the mean density of the different types of broadleaved debris, but not in the density of conifer debris (Table 2). There were also significant differences in the me#
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Table 1. Summary of the ANOVA comparing the density of living trees per 0.01 ha among flat riparian sites, sloped riparian sites, and upland sites.
Conifers Picea Pinus Broadleaveda Betulaa Populusa,b Alnusa Salixa,b Sorbusa,b
MS 10.46 2.27 3.26 1.48 0.83 0.15 0.64 0.01 0.05
F[2,27] 1.84 0.42 2.44 29.21 18.96 2.43 14.79 2.62 4.17
p 0.178 0.663 0.106c 0.0001c 0.0001c 0.107 0.0001c 0.091 0.026c
Note: See Fig. 1 for pairwise comparisons. a
Log10+ 1 transformation was used. Homogeneity of variances was not achieved using transformation. c Significant differences in the median density, using Kruskal–Wallis test. b
Fig. 1. Mean density per 0.01 ha of living trees in the flat riparian sites, sloped riparian sites, and upland sites (n = 10 in each). Error bars are SEs. Pairwise differences between the upland (control) and riparian sites were tested using Dunnett’s t test. Asterisks indicate significant differences at the 0.05 level. See Table 1 for the summary of the ANOVA.
Table 2. Summary of the ANOVA comparing the density of woody debris (diameter ‡5 cm) per 0.01 ha among flat riparian sites, sloped riparian sites, and upland sites.
Overall Standing Downed Conifers Standing Downed Picea Pinus Broadleaved Standinga Downed Betula Populus Alnusa,b Salix Sorbusa,b
MS 31.10 7.41 8.53 0.24 0.03 0.29 0.63 0.10 34.46 6.71 11.04 2.59 1.34 12.11 0.21 0.76
F[2,27] 3.93 3.39 2.50 0.32 0.17 0.81 1.13 1.44 5.65 4.09 4.36 2.82 2.24 7.17 0.68 4.84
p 0.032c 0.049c 0.100c 0.730 0.840 0.460 0.339 0.255 0.009c 0.028c 0.023c 0.077c 0.126 0.003c 0.516 0.016c
Note: Taxon-level comparisons include both standing and downed trees. See Fig. 2 for pairwise comparisons. a
Log10+ 1 transformation was used. Homogeneity of variances was not achieved using transformation. c Significant differences in the median density, using Kruskal–Wallis test. b
woody debris, 1% (5) of Alnus woody debris, and 2% (1) of Salix woody debris had diameters ‡ 20 cm. Coarse woody debris of broadleaved trees was predominantly found in riparian sites. Overall, most of the woody debris was of decay stages 1–2, i.e., consisted of recently dead trees. In the FR, SR, and UP sites, 22%, 10%, and 25% of the total number of conifer woody debris, and 36%, 35%, and 39% of the broadleaved woody debris were at advanced decay stages 3–5.
dian densities of Betula, Alnus, and Sorbus debris among the categories (K–W c2 > 7.23, pmc < 0.022), and the difference remained significant for the mean densities of Alnus and Sorbus (Table 2, Fig. 2b). In the FR, SR, and UP sites, 74%, 73%, and 27% of the total number of woody debris items (diameter ‡5 cm) were broadleaved trees. Overall, however, the majority of the broadleaved woody debris had small diameters — only 10% (29 items) of Betula woody debris, 11% (18) of Populus
Species diversity Altogether, 395 records of 48 polypore species were made (see Appendix A). Of the recorded species, 24 occur primarily on broadleaved trees, 20 on coniferous trees, and four species can be considered generalists. Five red-listed and five old-growth forest indicator species (not mutually exclusive) were represented by a total of 26 records. The total number of species was significantly larger in the FR sites than in the other two categories, which, in turn, did not differ from each other (Fig. 3a). However, when the cumulative number of species was rarefied to a common number of records (nupland = 80), the differences disappeared (Fig. 3b). The overall diversity of the polypore assemblage in the FR sites, in particular, was greater than that in the upland sites (Fig. 4). Neither the mean nor the median standardized number of species or records differed among the FR, SR, and UP sites (ANOVA F[2,27] < 1.31, p > 0.28, records were log10 + 1 transformed; K–W c2 < 3.99, pmc > 0.12, df = 2; Fig. 5). Overall, species composition was more similar between #
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Fig. 2. Mean density per 0.01 ha of woody debris by type (A) and by genus (B) in the flat riparian sites, sloped riparian sites, and upland sites (n = 10 in each). Error bars are SEs. Pairwise differences between the upland (control) and riparian sites were tested using Dunnett’s t test. Asterisks indicate significant differences at the 0.05 level. See Table 2 for the summary of the ANOVA.
Fig. 3. The sample-based (A) and record-based (B) rarefaction curves for the number of polypore species in the flat riparian sites, sloped riparian sites, and upland sites. Broken lines indicate 95% confidence intervals.
the two riparian assemblages than between the riparian and upland assemblages (Table 3), but variation in species composition within the categories was great (Fig. 6). The number of species associated with broadleaved trees was larger in the riparian sites than in the upland sites, but the difference was not statistically significant (Fisher’s Exact c2 = 1.95, p = 0.40). Of the species that occurred only in riparian sites (n = 11), 82% are associated with broadleaved trees. Twenty-four species were recorded only from the riparian sites. Thirteen species were unique to the FR sites, and six species were unique to the UP sites; no species were recorded only from SR sites. The total abundance of the shared species, i.e., species that two categories have in common (n = 17), in FR sites
was almost twice that in UP sites (139 vs. 70 records). Also, the abundance of the shared species (n = 13) was 30% larger in the SR than in the UP sites (82 vs. 63 records). There was no correlation between any of the woody debris types and the density of species or records within the study categories. Red-listed or indicator species were recorded from all categories (Appendix A).
Discussion Forest characteristics Lakeside riparian forests had a higher density of living and dead trees than upland forests, mainly because of the presence of broadleaved trees. Our results thereby support #
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Komonen et al. Fig. 4. Rank-abundance plots for flat riparian sites, sloped riparian sites, and upland sites. Diversity indices are Simpson (1/D) and Brillouin (HB), and heterogeneity indices are Berger–Parker (BP) and Simpson’s evenness (E1/D). The indices were calculated for the pooled data and thus no measure of variation is included.
2655 Table 3. Similarity of the polypore assemblages between flat riparian sites (FR), sloped riparian sites (SR), and upland sites (UP).
FR–SR FR–UP SR–UP
Shared species 24 17 13
So¨rensen incidence 0.74 0.52 0.54
So¨rensen abundance 0.58 0.46 0.43
Fig. 6. Similarity of polypore assemblages among flat riparian sites, sloped riparian sites, and upland sites, based on the detrended correspondence analysis ordination.
Fig. 5. The standardized median number of polypore species and records per 0.1 ha in the flat riparian sites, sloped riparian sites, and upland sites (n = 10 in each). Boxes indicate the 25th and 75th percentiles and whiskers the 10th and 90th percentiles. The values above the whiskers are the total number of species or records in each category.
debris in the studied riparian sites. Yet, the observed difference in the mean density of broadleaved woody debris per 0.01 ha between the riparian and upland sites corresponds to about 300 items per hectare, which is a biologically significant difference. Lakeside riparian forests thus contribute to landscape heterogeneity in managed boreal forests.
the general patterns of broadleaved tree dominance and greater tree species diversity in riparian forests (Pabst and Spies 1999; Barker et al. 2002; Suzuki et al. 2002). In riparian sites, most of the living trees and, consequently, woody debris had small diameters (£20 cm). Apparently, mesic site characteristics, self-thinning due to high tree density, and continuous small-scale disturbances promote fine woody debris in riparian forests (Pabst and Spies 1999; Sakai et al. 1999; Martin and Grotefendt 2007). As well, selective logging of larger trees has reduced the amount of coarse woody
Species diversity Overall, riparian sites harbored a larger number of polypore species and records, and had greater diversity, than upland sites. These results are in accordance with the general ecological understanding that greatest species richness and lowest dominance are often found in sites that continuously face multiple but moderate disturbances (Connell 1978; Suzuki et al. 2002). The observed differences in overall species richness likely result from a larger number and greater diversity of woody debris, and consequently a larger number of polypore records (Penttila¨ et al. 2004; Sippola et al. 2005; Junninen and Kouki 2006). Previous studies have found contradictory results concerning the importance of lakeside riparian forests for maintaining terrestrial biodiversity (Macdonald et al. 2006), but most of these studies have concerned organisms other than those directly dependent on particular disturbance-related characteristics. There were also significant differences between the flat and sloped riparian sites. The flat riparian sites had almost twice as many polypore species than the sloped riparian sites, whereas in terms of polypore records and diversity statistics, the values obtained for the sloped sites are between those of the flat riparian and upland sites. The density of #
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woody debris in sloped sites was similar to that in flat sites and much greater than that in upland sites, but there were no differences in the overall amount of coarse woody debris among the site categories. Flat riparian sites had more Populus debris and associated polypores (five species) than sloped sites. In flat sites, there was also a greater number of polypores species associated with conifers (nine species), although no significant differences in conifer debris were observed between flat and sloped riparian sites. The greater number of stumps in the sloped sites indicates that human interference had been more intense in these sites than in flat sites. The biodiversity patterns observed in this study likely result from slight differences among sites in woody debris characteristics and past human influence, coupled with stochastic factors due to small sample size. There were no significant differences in the mean or median number of species or records per site. On the one hand, this finding results from large variation within study categories, and consequent low power in statistical tests. Species richness varied considerable among the riparian sites, which comprised both very species rich and species poor sites, whereas the upland sites were more consistently species poor. On the other hand, greater total species richness in the flat riparian sites, coupled with similar mean richness among all site categories, indicates greater b diversity in flat riparian sites than in sloped riparian and upland sites. Species composition and red-listed species The species composition of riparian sites differed from that of upland sites. This difference is largely due to the occurrence of species associated with broadleaved trees in the riparian sites. Similarly, the higher polypore richness in oldgrowth forests compared with managed forests is generally due to species associated with broadleaved debris, particularly with large aspens (Penttila¨ et al. 2004; Sippola et al. 2005). Furthermore, the abundances of many species were higher in the riparian than in the upland sites, suggesting that riparian forests may be important for maintaining populations of many polypore species and may act as source areas in the midst of the managed forest landscapes. Our results are in general agreement with the understanding that riparian forests often harbor biotic assemblages that are different from those of adjacent upland forests (Sabo et al. 2005). Red-listed or indicator species (eight species, 17% of recorded species) were found in all forest categories; however, most of these species were associated with the flat riparian sites. Given the small area sampled and the long history of slash-and-burn cultivation and modern forestry in the region (Silvennoinen 2000), this figure is relatively high and in line with the observations from herb-rich forests (Sippola et al. 2005; Junninen and Kouki 2006). Even in forest reserves the number of red-listed species is often small when the number of woody debris items (diameter >10 cm) is less than 200 ha–1 (Penttila¨ et al. 2004), which was the situation in this study (max. 171 ha–1). Although fine woody debris has been recently identified as an important substrate for many polypore species (Norde´n et al. 2004), most threatened polypore species occur predominantly on coarse woody debris, which was infrequent in this study.
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Management implications The importance of riparian zones for maintaining polypore diversity in managed forests depends on their habitat quality (e.g., amount of woody debris), total area, and landscape context. Although the amount of woody debris in the studied riparian forests was small compared with that in most reserves (Penttila¨ et al. 2004), it was about twice the amount in upland forests. Furthermore, most of the upland landscape in our study region consists of young successional stages (65%
