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Colonization of old-forest lichens in a young and an old boreal Picea abies forest: an experimental approach
Biological Conservation 102 (2001) 251–259 www.elsevier.com/locate/biocon
Colonization of old-forest lichens in a young and an old boreal Picea abies forest: an experimental approach Olga Hilmoa,*, Sigurd M. Sa˚stadb a
Department of Botany, Faculty of Chemistry and Biology, Norwegian University of Science and Technology, N-7491 Trondheim, Norway b Department of Natural History, Norwegian University of Science and Technology, N-7491 Trondheim, Norway Received 17 October 2000; received in revised form 26 January 2001; accepted 3 April 2001
Abstract Understanding the factors limiting the distribution of a species is crucial for designing conservation strategies. We evaluated whether the scarcity of old-forest lichens in young forests was due to unfavourable environmental conditions for colonization in young stands or to dispersal limitations. Vegetative diaspores of Lobaria scrobiculata, Platismatia glauca and Platismatia norvegica were sown on 240 spruce twigs transplanted to a young and an old stand of spruce. Our results demonstrate that the old-forest species established and grew as rapidly in the young as in the old forest. Higher light levels in the young, compared with the old forest, did not reduce diaspore development. Moreover, greater numbers of juvenile thalli of Platismatia were found on control twigs (unsown) in the old forest, compared with the young forest, suggesting higher propagule density and more efficient dispersal in the old stand. Our results indicate that life-history characteristics, which include dispersal characters, are important for explaining the species scarcity in younger stands. Minimizing the distance between regeneration units and potential sources of propagules is probably important for maintaining lichen biodiversity in managed forest ecosystems. # 2001 Elsevier Science Ltd. All rights reserved. Keywords: Conservation; Diaspores; Dispersal; Establishment
1. Introduction Commercial large-scale forestry affects biodiversity at various spatial and temporal scales (Franklin, 1993; Esseen et al., 1997). Habitat loss, habitat alteration and fragmentation of previously continuous forests has reduced species diversity in forest ecosystems (e.g. Harris, 1984; Saunders et al., 1991; Angelstam, 1992). Due to forest fragmentation, several species have elevated risks of local extinction (Nilsson and Ericson, 1997). Epiphytic lichens are considered to be particularly sensitive to forestry (e.g. Lesica et al., 1991; Esseen et al., 1997), and many such species are mainly confined to old forests stands in the boreal region (Tibell, 1992; McCune, 1993; Holien, 1996, 1997; Kuusinen and Siitonen, 1998). The lichen biomass in managed second growth stands is lower than in old-growth forests (Hyva¨rinen et al., 1992; McCune, 1993; Esseen et al., 1996; Dettki and Esseen, 1998). * Corresponding author. Fax: +47 73596100. E-mail address: [email protected] (O. Hilmo).
The survival of lichen populations is influenced by life-history characteristics such as production and dispersal of diaspores and the species ability to establish and develop under different environmental conditions. The scarcity of old forest lichens in younger forest stands could be due to inefficient dispersal of lichen propagules (Esseen et al., 1996; Sillett and McCune 1998) or it could be that unfavourable microclimatic conditions in the younger stands preclude establishment. Species confined to old, natural forests are considered to be sensitive to alteration in environmental conditions (Rose, 1992). Juvenile stages of epiphytic lichens have been shown to be sensitive to environmental influences as the rate of development differs between locations with relatively similar microclimate (Ott, 1987). Further, the microtopography of the bark significantly influences the establishment and survival of diaspores (Armstrong, 1990). Scheidegger (1995a) found that low reproduction potential limited the distribution of Lobaria pulmonaria. Understanding the factors influencing the size of a population is of great importance when designing conservation strategies aimed to
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maintain species diversity in forest ecosystems. Identification of critical life cycle stages determining population or metapopulation dynamics is crucial for designing recovery measures in conservation biology (Schemske et al., 1994). However, earlier studies of lichens in boreal forests have paid little attention to the initial phase of the life cycle. The aim of this study was to compare success of establishment and rate of development of lichen diaspores in a young, planted stand of Picea abies (L.) Karst. and an old Picea abies forest where the studied species occur naturally. Our experiment included Lobaria scrobiculata (Scop.) DC and Platismatia norvegica (Lynge) W. Culb. & C. Culb., both mainly distributed in old humid forests (Gauslaa, 1995; Holien and Tønsberg, 1996; Thor and Arvidsson, 1999) and defined as oldforest lichens in the present study. We also included Platismatia glauca (L.) W. Culb. & C. Culb. which is a common species in forests of different successional stages. By doing a field experiment we wished to assess whether old-forest species can establish in younger stands, or whether establishment is precluded for example, by sensitivity to environmental factors or because the twig bark of young stands is unsuitable for diaspore attachment. If successful establishment of the diaspores in the younger stand is found, this would indicate that dispersal or diaspore production is limiting for the species distribution. It is of vital interest to discriminate between these alternative models of explanations when assessing various methods in forestry, aimed to maintaining biodiversity in managed forest ecosystem.
Degel., Lobaria scrobiculata, Parmeliella parvula P. M. Jørg. and Platismatia norvegica on branches indicates a humid climate (Ahlner 1948; Jørgensen 1978). The common macrolichens colonizing the twigs are C. hultenii, H. physodes, H. tubulosa, Parmelia sulcata T. Tayl. and Platismatia glauca. P. glauca is the most dominant epiphytic foliose species in the old stand. A summary of stand temperature, humidity, radiation and bark pH is given in Table 1. The bark pH was measured according to Gauslaa and Holien (1998). 2.2. Lichen material The reproductive strategies of the three investigated species is mainly vegetative by production of symbiotic propagules. Apothecia (sexual reproductive structures) are very rarely observed (Purvis et al., 1992). Lobaria scrobiculata reproduces by soredia and Platismatia norvegica by formation of isidia, which sometimes become granular-sorediate. The regenerative structures of P. glauca are highly variable from simple-coralloid isidia to granular soredia (Purvis et al., 1992). 2.3. Experimental design Twigs of Picea abies (240 twigs, 10 mm in diameter) were sampled in the study area and cut to 10-cm in length. Lichen fragments and diaspores were removed from the twigs and the ends of the twigs were waxed. The twigs were not sterilized. Within three separate areas, each 1 cm2 in size, we made four parallel depressions to increase the roughness of the bark. Mature thalli of the three species were collected in the investigation
2. Material and methods 2.1. Study area The field experiment was performed in an old spruce forest (10.5 ha) and in an adjacent younger planted stand (1.1 ha) bordering the north side of the old forest. The study area is situated at 185 m a.s.l. in Melhus, SørTrøndelag, central Norway (63 080 N, 10 060 E). Picea abies dominates the area, where forestry has created a mosaic of contrasting successional stages. The younger forest consisted mainly of 5–7 m tall spruce trees about 30 years old. The epiphytic lichens represent a pioneer community (Hilmo, 1994) dominated by crustose species and Hypogymnia physodes (L.) Nyl. Other colonists in the young stand are Hypogymnia tubulosa (Schaer.) Hav. and Cetraria chlorophylla (Willd.) Vain. A few juvenile thalli of Platismatia glauca were observed on some of the branches. The old spruce forest has naturally regenerated and is multilayered. Some selective felling and windfall in the past has formed gaps in the canopy. The tallest trees are about 20 m high and 120 years old. The occurrence of Cavernularia hultenii
Table 1 Mean air temperature ( C), relative air humidity (%), photon flux density (mmol m2 s1) and total number of hours 5150 mmol m2 s1 in July and January, measured 2 m above ground among north-facing branches, in the young and old forest Young forest
Old forest
Air temperature
July January
12.8 5.4
12.2 4.8
Air humidity
July January
82.3 82.0
82.9 81.4
Photon flux density
July January
121.1 4.1
Number of hours 5150 mmol m2 s1
July
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January Bark pH
(814.0) (44.7)
0 4.1 (3.8–4.4)
14.9 0.6
(268.8) (7.1)
5 0 4.3 (3.9–4.5)
The radiation sensor (LI-190SZ Quantum Sensor) and the probe measuring humidity and temperature (HMP35AC, LI-COR) recorded at intervals of 10 min and the hourly mean was stored. Maximum values of photon flux density are given in parenthesis. Bark pH (median, minimum and maximum) are given for 25 twigs at each stand.
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area and in adjacent mature forests. Diaspores were brushed off the thalli and stored at 5 C for up to 2 days before sowing. Diaspores of the three species were sown separately within the three areas on each twig. The marked area was completely covered by diaspores (100% cover). The twigs were carefully sprayed with water before and after sowing. Twenty twigs were mounted with plastic coated wires on each of 12 frames made of polyvinylchloride (Fig. 1). Ten twigs were from the young stand (young forest substratum) and 10 were from the old natural forest (old forest substratum). Four twigs on each frame were controls without sown diaspores. These twigs were added to assess the establishment of naturally dispersed diaspores in the two habitats. The twigs were also used to compare the amount of juvenile thalli developed from naturally dispersed diaspores on young and old forest substrata. The frames were placed on the most north-facing branch 2 m above ground on randomly selected trees within an area of 3050 m. Six frames were located in the young forest and six frames in the old forest. The experiment started in July 1995 and ended in July 1999.
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Fig. 1. Units used for experiment of establishment and development of lichen diaspores. 10 twigs, from each habitat, with sown diaspores fastened to a specially constructed frame.
2.4. Harvest of twigs Twigs with sown diaspores were harvested monthly from August 1995 until November 1995, and then every second month until October 1996. At each harvest one twig was taken randomly from each frame. Three twigs of young forest substratum and three twigs of old forest substratum were removed from each habitat at each harvest. Additional harvests were made in April, July and November 1997 and in June 1998. The two last twigs of each substratum type were harvested in June 1999.
Fig. 2. Diaspores of Platismatia norvegica attached to the substratum (arrow) by outgrowing hyphae. Scale=100 mm.
2.5. Analyses of establishment success and rate of development Establishment was defined as when the diaspores were attached to the substratum by outgrowing hyphae (Fig. 2). To determine establishment, diaspores on harvested twigs were examined in a scanning microscope (Jeol, JMS-25s; Hilmo and Ott, unpublished). The degree of establishment was estimated from the percentage cover of diaspores within each sown area during a 1 year period from November 1995 to October 1996. The cover of diaspores was measured with a stereomicroscope. The measurements started after the diaspores were attached to the substratum by outgrowing hyphae (November 1995), but ended before the diaspores started to elongate and develop further (October 1996; Fig. 2). The rate of development of sown diaspores was estimated as: (1) percentage cover of flattened lobules (Fig. 3) of the established diaspores, and (2) as size (mm) of the 10 largest lobules within each sown area.
Fig. 3. Flattened lobules of Platismatia norvegica 4 years after transplantation. Scale=100 mm.
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The size represented the largest diameter (mm) of each lobule. These measurements were performed with a stereomicroscope on the 24 twigs sampled at the end of the experiment in June 1999.
yijkln ¼ þ Spi þ Hj þ Sk þ lðjÞ þ SpHij þ SpSik
2.6. Light measurements
where yijkln is the response of the nth sowing unit on the lth frame on the kth substratum, from the jth habitat, belonging to the ith species, and is the mean of the response. The frame random effect () is nested within habitat (H) and is used as an error term when testing for differences between habitat. Species (Sp), substratum (S) and frames () were tested against the residual error. Species, habitat and substratum were considered fixed effects. All interactions among the fixed effects were included in the model. Cover of diaspores was ln-transformed and the percentage cover of flattened lobules was arcsin transformed to achieve homogenous variation among samples. Lobaria scrobiculata was omitted from the statistical treatment of cover of flattened lobules and size of lobules, because very few diaspores had reached this stage of development. ANOVA was carried out using the general linear modelling option in SPSS, version 8.0 for windows (SPSS, Inc. 1997).
Photosynthetically active radiation (mmol photons m2 s1) was measured at five points within each of the 12 frames. These measurements were made on cloudy days and included simultaneous measurements of radiation at a reference point in an adjacent open field (radiationref) and radiation measurements within the frames (radiationframe). Radiation was measured three times during 2 days, at 9 a.m., 12 p.m. and 3 p.m. in July. The radiation at each point within the frames was expressed as a radiation index calculated by the formula: (radiationframe /radiation ref) 100%. 2.7. Statistical treatment of data Cover of diaspores of the three lichen species was analysed using analysis of variance (ANOVA) according to the model:
þ HSjk þ SpHSijk þ ijkln
ð2Þ
yijklmn ¼ þ Spi þ Hj þ Sk þ lðjÞ þ mðlÞ þ SpHij 3. Results þ SpSik þ HSjk þ SpHSijk þ ijklmn
ð1Þ 3.1. Success of establishment
where yijklmn is the response of the nth sowing unit on the mth twig on the lth frame on the kth substratum, from the jth habitat, belonging to the ith species, and is the mean of the response. The twig random effect (b), is nested within frame () and used as an error term when testing for differences between substratum (S) and frames. The frame random effect is nested within habitat (H) and is used as an error term when testing for differences between habitat. Species (Sp) were tested against the residual error term. Species, habitat and substratum were all considered fixed effects. All interactions among the fixed effects were included in the model. The twig within frame effect may be potentially ascribed not only to natural variation among twigs, but also by the fact that twigs were harvested at intervals of about 2 months over a 1 year period. The date of harvest is not considered in the analysis as linear regression revealed no significant relationship between time of sampling and cover of diaspores on 72 twigs sampled during the period November 1995 to October 1996 (P=0.342). The analyzed time interval starts when the diaspores were attached to the twigs by outgrowing hyphae and ended before the diaspores showed sign of expansion. Percentage cover of flattened lobules and mean size of the largest thalli were analysed using ANOVA according to the model:
The loss of sown diaspores was high during the first weeks before the diaspores attached to the substratum by outgrowing hyphae. Subsequent to attachment the loss was negligible. The mean untransformed cover of diaspores was 4.8% within the investigated sown areas. In spite of high initial loss of diaspores, none of the sampled twigs during the experiment was totally lacking diaspores. Cover of diaspores differed significantly between the two substrata (Table 2; Fig. 4). Although the mean cover of diaspores was slightly higher on twigs located in the old forest, compared with the young forest (5.2 and 4.4%, respectively) this difference was not significant (Table 2). Cover of diaspores also differed significantly between the species (Table 2), with Platismatia norvegica having the highest and Lobaria scrobiculata the lowest cover of diaspores (Fig. 4). Analysis of variance revealed much variation in cover of diaspores among frames within the localities (Table 2). The mean cover of diaspores of all three species on the 12 frames varied between 2.6 and 9.5%. Cover of diaspores also varied considerably among twigs within frames (Table 2). Linear regression showed a significant positive relationship between cover of diaspores and light exposure of the frames for each of the species located in the old forest (Fig. 5). A negative
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relationship between light and cover of diaspores is indicated in the young forest. This relationship, however, is not significant because of the relatively high cover of diaspores found on twigs situated on a frame with extreme light values (Fig. 5). 3.2. Rate of development Four years after sowing the diaspores, flattened lobules (Fig. 3) of the Platismatia species were observed within all the sown areas. A significantly higher percentage cover of flattened lobules was found in P. norvegica (62.9%), compared with P. glauca (34.6%; Table 3). However, no interactions were found between species and habitat or species and substratum (Table 3). The mean size of the 10 largest juvenile lobules was 0.5 mm for P. norvegica and 0.4 mm for P. glauca, but the differences observed between analysed species, habitat or substratum regarding this variable were not Table 2 ANOVA of cover of diaspores of Lobaria scrobiculata, Platismatia glauca and Platismatia norvegica (‘Species’) in a young and old forest (‘Habitat’) sown on substratum from young and old forest (‘Substratum’) Source of variation
d.f.
MS
F
P
Species Habitat Substratum SpeciesHabitat SpeciesSubstratum HabitatSubstratum SpeciesHabitatSubstratum Frame (Habitat) Twig (Frame) Residual
2 1 1 2 2 1 2 10 58 136
8.173 1.248 5.865 0.085 0.462 0.249 0.050 2.167 0.497 0.367
22.293 0.576 11.802 0.230 1.259 0.500 0.137 4.359 1.356
0.000 0.465 0.001 0.794 0.287 0.482 0.872 0.000 0.077
Fig. 4. Cover of diaspores of Lobaria scrobiculata, Platismatia glauca and P. norvegica on bark substratum from the young forest (&) and bark substratum from the old forest (&). Error bars are one Standard Error.
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significant (Table 4). Observations of Lobaria scrobiculata with scanning microscopy, revealed diaspores in different stages of development on six twigs from the young forest and five twigs from the old forest. However, well-developed juvenile lobules were observed on only two twigs, one from each of the habitats. The ontogeny of the investigated species is thoroughly discussed in Hilmo and Ott (unpublished). Cover of flattened lobules (Table 3) and mean size of the 10 largest thalli (Table 4) of Platismatia varied widely among frames within the localities. The mean percentage cover of flattened lobules (of the established diaspores) on the 12 frames varied between 20.0 and 78.8. The mean size of the 10 largest juvenile thalli within each of the frames varied between 0.3 and 0.7 mm. Table 3 ANOVA of percentage cover of flattened lobules of Platismatia glauca and Platismatia norvegica (‘Species) in young and old forest (‘Habitat’), and on substratum from young and old forest (‘Substratum’) Source of variation
d.f.
MS
F
P
Species Habitat Substratum SpeciesHabitat SpeciesSubstratum HabitatSubstratum SpeciesHabitatSubstratum Frame (Habitat) Residual
1 1 1 1 1 1 1 10 30
1.405 0.014 0.013 0.013 0.002 0.010 0.164 0.320 0.030
46.822 0.044 0.418 0.420 0.080 0.319 5.466 10.661
0.000 0.837 0.523 0.522 0.779 0.576 0.026 0.000
The dependent variable was arcsin transformated to achieve homogenous varians.
Fig. 5. Relationship between cover of diaspores of Lobaria scrobiculata (^), Platismatia glauca (*) and P. norvegica (&) and light exposure of each frame situated in the young (open symbols) and old forest (filled symbols). Separate linear regression of the three species in the old forest are shown: Platismatia norvegica (solid line; r2=0.80*), Platismatia glauca (dotted line; r2=0.66*) and Lobaria scrobiculata (dashed line; r2=0.73*). *P<0.05.
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4. Discussion
Fig. 6. Pigmented cortex of juvenile lobes of Platismatia glauca located in the young forest. Scale=1 mm. Table 4 ANOVA of mean size of the 10 largest juvenile thalli of Platismatia glauca and Platismatia norvegica (‘Species’) in a young and old forest (‘Habitat’), and on young and old forest substratum (‘Substratum’) Source of variation
df
MS
F
P
Species Habitat Substratum SpeciesHabitat SpeciesSubstratum HabitatSubstratum SpeciesHabitatSubstratum Frame (Habitat) Residual
1 1 1 1 1 1 1 10 30
0.0517 0.0069 0.0005 0.0095 0.0230 0.0038 0.0252 0.0711 0.0173
2.995 0.097 0.027 0.550 1.331 0.218 1.461 4.122
0.094 0.762 0.870 0.464 0.258 0.644 0.236 0.001
A dark pigmented cortex was characteristic for the juvenile thalli of Platismatia located in the young forest (Fig. 6). This pigmentation was not found in the old natural forest. Examination of the control twigs (48 twigs) at the end of the experiment revealed a significantly higher number of marked areas (1 cm2) with juvenile lobules of Platismatia in the old natural forest (29%), compared to the young forest (10%; P=0.006, w2test). No significant differences were found between the two substratum types, as 46% of the twigs with observed small lobules were young forest substratum and 54% of the twigs were old forest substratum (P=0.593, w2test). Lobules of Hypogymnia were observed within the marked areas on 8 and 9% of the control twigs from the young and old forest, respectively. However, only a few lobules were established within the marked areas for both Platismatia and Hypogymnia and the cover of the lobules did not exceed 1% of the marked areas. With exception of two observation of Cetraria chlorophylla and one observation of Bryoria no other species was observed on the control twigs.
The absence of any species in a habitat can be explained by several biotic or abiotic factors including production and dispersal of propagules, attachment of propagules to the substratum, substratum quality, substratum availability and microclimatic conditions (Armstrong, 1988). The distribution of several lichens confined to old forests, e.g. species in the Lobaria community, has been explained by the particular microenvironment created by the structure of old forests (Lesica et al., 1991; Kuusinen, 1996). Our results, however, demonstrate that the environmental conditions in young forests are not necessarily unfavourable for establishment and development of diaspores of old-forest species such as Lobaria scrobiculata and Platismatia norvegica. The success of establishment and rate of development of the diaspores are as high in the young forest as in the old forest. This is in accordance with recent results of Sillett et al. (2000) who emphasized that particular substrata and microenvironments found only in old growth forest are not essential for the distribution of Lobaria oregana. 4.1. Dispersal limitations This investigation indicates that diaspore production and dispersal ability are probably important in determining the distributional patterns of some old-forest species. The absence of Lobaria scrobiculata on the control twigs in both spruce stands and very few lobules of Platismatia on the control twigs in the young forest, even if the experimental frames were located only about 50 m from the forest edge, support the hypothesis of low dispersal ability. Little attention has been paid to the effectiveness of different diaspores to disperse. However, Dettki et al. (2000), who investigated the occurrence of lichen thalli in young forests at increasing distances (10, 50 and 100 m) from the old-growth forest, found that the number of thalli displayed a pronounced decrease with increasing distances from the source of propagules. Our result is also supported by Sillett et al. (2000) who found that establishment and growth of diaspores of Lobaria oregana sown on branches of Douglas-fir grew as rapidly in young as in old forests. The development of L. oregana populations was limited by poor dispersal and establishment. Low dispersal ability is also postulated by Sillett and Goslin (1999) who found that the biomass of lichen species, associated with old-growth forests, were highest near remnant trees in younger forest stands. In general, the production of vegetative diaspores is considered advantageous for rapid colonization (Bowler and Rundel, 1975; Bailey, 1976; Jahns, 1988). However, studies of lichen dispersal have shown that soredia from several species are mostly deposited within a short distance of their source (Tapper, 1976;
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Armstrong, 1987, 1994; Stevenson, 1988). According to Jahns (1984, 1988) heavy isidia serves primarily for growth and regeneration at the site, not for dispersal of the species. 4.2. Substratum quality The higher cover of diaspores on young compared with the old forest substratum shows that the bark properties in the young forest stand were favourable for diaspore attachment. The higher cover of diaspores on twigs sampled in the young forest could be due to a slightly more sticky bark of these twigs (probably due to a higher content of resin), compared with the twigs collected in the old forest. A higher bark pH on twigs from the old forest, compared with twigs from the young forest (Table 1) seems not to have affected diaspore development of Lobaria scrobiculata in our experiment. The availability of naked bark is higher on mature trees in the old forest compared with younger trees in the plantation. On young trees the needles cover almost the whole branch, from branch tip to branch base, whereas only the branch tip is covered by needles of mature trees. If the cover of needles negatively influences the establishment or development of diaspores, the amount of suitable sites to colonize are more scarce in the young compared with the old forest. Since the experimental twigs had no needles this factor is not taken into consideration. It is unlikely that the lack of needles on the experimental twigs could explain the relatively low success of establishment and development of the sown diaspores of L. scrobiculata. Field observations of L. scrobiculata in the investigation area shows that juvenile thalli mainly are distributed on the outermost part of the branches on needle-free twigs as well as on needle-bearing twigs. According to Hilmo (1994) the cover of Platismatia norvegica is highest on spruce branches with a low cover of needles. The high loss of diaspores observed, indicates that rapid development of anchoring hyphae is crucial for successful establishment at a new site. The period before the hyphae anchors the deposited diaspores to the substratum is thus a critical phase in the life cycle. This is supported by Scheidegger (1995b) who claimed that immobilization of diaspores on the substratum seems to be a major limiting factor in the reproductive process. 4.3. Microclimatic conditions A number of environmental factors are considered important for lichens; for example light conditions (Gauslaa and Solhaug, 1996; Palmqvist and Sundberg, 2000), water accessibility (Lange et al., 1986; Nash, 1996), bark pH (Gauslaa and Holien, 1998) and bark stability of growing trees (Hesselman, 1937). The air humidity was high throughout the year, both in the
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young and old forest. In spite of markedly higher light levels in the young compared to the old forest (Table 1), there were no significant differences in success of establishment or rate of development between the two stands. This is in contrast to the results of Ott (1987) who found different rates of diaspore development between localities even when environmental differences were small. The lichens investigated by Ott developed most rapidly at locations where they occur naturally. Ott (1987) used different species and different forest environments than us, which could account for some of the different results between the two studies. The increase in cover of established diaspores with light exposure in the old forest indicates that low light may limit hyphal growth and hence attachment to the substratum. This is supported by Ahmadjian (1993) who found vacuolated, irregularly shaped hyphae in dark culture of the mycobiont. Since radiation in a forest can be highly spatially variable (Gauslaa and Solhaug, 2000), some of the old forest frames could well have been located in positions with radiation at, or around, the compensation point for photosynthesis. Gauslaa and Solhaug (1996) also found that Lobaria species were susceptible to high photon flux densities as photoinhibition was measured. Our study may indicate a unimodal response to light in all three species but the evidence for this is weak and requires that the one extremely exposed frame is omitted from the analysis. Brownish pigmentation of the juvenile cortex of Platismatia species situated in the young forest might support the hypothesis of a protective function of melanin pigmentation (Rikkinen, 1995). Although we did not find differences between the young and the old forest, which could be ascribed to environmental differences, a gradient from favourable to unfavourable microsites probably exists within both habitats due to variation in microclimatic conditions and also biotic factors such as herbivore activity. This may have caused the relatively high within-site variation in establishment and growth of the lichens. 4.4. Consequences for forest management Understanding the factors that limit the size of the lichen populations in managed forests is important for developing strategies to maintain biodiversity. Our field experiment indicate that the scarcity of old-forest lichens in younger stands are due to low dispersal ability of propagules, rather than environmental factors or bark properties. Our study supports the findings of Sillett et al. (2000), and these two studies are as far as we know, the only studies comparing establishment and development of lichen diaspores in young and old forests. Thus, it may be difficult to generalize on basis of the results and the study should be replicated under varying macroclimatic conditions. However, the results
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so far indicate that dispersal limitations is one important factor explaining the absence of old-forest species from the younger stand. Therefore, one strategy to promote lichen abundance in younger stands and to conserve old-forest associated lichens in managed forests could be to minimize the distance between regeneration units and potential sources of propagules. Retention of old trees in regeneration cohorts is one appropriate conservation method to increase the amount of diaspores in younger forest stands. Peck and McCune (1997) predicted that a group of remnant trees in regeneration cohorts provide canopy habitat that maintains the environment necessary for the establishment and growth of Lobaria oregana and alectorioid lichens. The importance of long ecological continuity for many epiphytic lichens is supported by a slow rate of development after attachment to the substratum.
Acknowledgements This work was founded by the Norwegian Research Council and Norwegian University of Science and Technology, Department of Botany. The authors are grateful to Yngvar Gauslaa, Ha˚kan Hytteborn and Sieglinde Ott for their valuable comments on the manuscript. We also wish to thank Line Bretten and Sigrid Lindmo for assisting in sampling of lichens and brushing of diaspores and Kjell Evjen, Asbjørn Fjellvika˚s and Ka˚re Sommervold for technical assistance. References Ahlner, S., 1948. Utbredningstyper bland nordiska barrtra¨dslavar. Acta Phytogeographica Suecica 22, 1–157. Ahmadjian, V., 1993. The Lichen Symbiosis. John Wiley, New York. Angelstam, P., 1992. Conservation of communities — the importance of edges, surroundings and landscape mosaic structure. In: Hansson, L. (Ed.), Ecological Principles of Nature Conservation. Elsevier, London, pp. 9–70. Armstrong, R., 1987. Dispersal in a population of the lichen Hypogymnia physodes. Environmental and Experimental Botany 27, 357–363. Armstrong, R., 1988. Substrate colonization, growth, and competition. In: Galun, M. (Ed.), CRC Handbook of Lichenology, Vol. II. CRC Press, Boca Raton, Florida, pp. 3–16. Armstrong, R., 1990. Dispersal, establishment and survival of soredia and fragments of the lichen Hypogymnia physodes. New Phytologist 114, 239–245. Armstrong, R., 1994. Dispersal of soredia from individual soralia of the lichen Hypogymnia physodes (L) Nyl in a simple wind-tunnel. Environmental and Experimental Botany 34, 39–45. Bailey, R., 1976. Ecological aspects of dispersal and establishment in lichens. In: Brown, D.H., Hawksworth, D.L., Bailey, R.H. (Eds.), Lichenology: progress and problems. Academic Press, London, pp. 215–247. Bowler, P.A., Rundel, P.W., 1975. Reproductive strategies in lichens. Botanical Journal of the Linnean Society 70, 325–340. Dettki, H., Esseen, P.-A., 1998. Epiphytic macrolichens in managed and natural forest landscapes: a comparison at two spatial scales. Ecography 21, 613–624.
Dettki, H., Klintberg, P., Esseen, P.-A., 2000. Are epiphytic lichens in young forests limited by local dispersal? Ecoscience 7, 317–325. Esseen, P.-A., Ehnstro¨m, B., Ericson, L., Sjo¨berg, K., 1997. Boreal forests. Ecological Bulletins 46, 16–47. Esseen, P.-A., Renhorn, K.-E., Petterson, R.B., 1996. Epiphytic lichen biomass in managed and old-growth boreal forests: effect of branch quality. Ecological Applications 6, 228–238. Franklin, J.F., 1993. Preserving biodiversity: species, ecosystems or landscapes? Ecological Applications 3, 202–205. Gauslaa, Y., 1995. The Lobarion, an epiphytic community of ancient forests threatened by acid rain. Lichenologist 27, 59–76. Gauslaa, Y., Holien, H., 1998. Acidity of boreal Picea abies-canopy lichens and their substratum, modified by local soils and airborne acidic depositions. Flora 193, 249–257. Gauslaa, Y., Solhaug, K.A., 1996. Differences in the susceptibility to light stress between epiphytic lichens of ancient and young boreal forests stands. Functional Ecology 10, 344–354. Gauslaa, Y., Solhaug, K.A., 2000. High-light-intensity damage to the foliose lichen Lobaria pulmonaria within a natural forest: the applicability of chlorophyll fluorescence methods. Lichenologist 32, 271–289. Harris, L.D., 1984. The fragmented forest: island biogeography theory and the preservation of biotic diversity. University of Chicago Press, Chicago. Hesselman, H., 1937. Om humusta¨ckets beroende av besta˚ndets a˚lder och sammansa¨ttning i den nordiska granskogen av bla˚ba¨rsrik Vaccinium-typ och dess inverkan pa˚ skogens fo¨ryngring och tillva¨xt. Meddelanden fra˚n statens skogfo¨rso¨ksanstalt 30, 530–716. Hilmo, O., 1994. Distribution and succession of epiphytic lichens on Picea abies branches in a boreal forest, Central Norway. Lichenologist 26, 149–169. Holien, H., 1996. Influence of site and stand factors on the distribution of crustose lichens of the Caliciales in a suboceanic forest area in Central Norway. Lichenologist 28, 315–330. Holien, H., 1997. The lichen flora on Picea abies in a suboceanic spruce forest area in Central Norway with emphasis on the relationship to site and stand parameters. Nordic Journal of Botany 17, 55–76. Holien, H., Tønsberg, T., 1996. Boreal regnskog i Norge-habitatet for trøndelags-elementets lavarter. Blyttia 54, 157–177. Hyva¨rinen, M., Halonen, P., Kauppi, M., 1992. Influence of stand age and structure on the epiphytic lichen vegetation in the middle-boreal forests of Finland. Lichenologist 24, 165–180. Jahns, H.M., 1984. Morphology, reproduction and water relations — a system of morphogenetic interactions in Parmelia saxatilis. Beihefte Nova Hedwigia 79, 715–737. Jahns, H.M., 1988. The lichen thallus. In: Galun, M. (Ed.), CRC Handbook of Lichenology, Vol. I. CRC Press, Boca Raton, Florida, pp. 95–143. Jørgensen, P-M., 1978. The lichen family Pannariaceae in Europe. Opera Botanica 45, 1–124. Kuusinen, M., 1996. Cyanobacterial macrolichens on Populus tremula as indicators of forest continuity in Finland. Biological Conservation 75, 43–49. Kuusinen, M., Siitonen, J., 1998. Epiphytic lichen diversity in oldgrowth and managed Picea abies stands in southern Finland. Journal of Vegetation Science 9, 283–292. Lange, O.L., Kilian, E., Ziegler, H., 1986. Water vapour uptake and photosynthesis of lichens: performance differences in species with green and blue-green algae as phycobionts. Oecologia 71, 104–110. Lesica, P., McCune, B., Cooper, S.V., Hong, W.S., 1991. Differences in lichen and bryophyte communities between old-growth and managed second-growth forests in Swan Valley, Montana. Canadian Journal of Botany 69, 1745–1755. McCune, B., 1993. Gradients in epiphyte biomass in three Pseudotsuga-Tsuga forests of different ages in western Oregon and Washington. Bryologist 96, 405–411.
O. Hilmo, S.M. Sa˚stad / Biological Conservation 102 (2001) 251–259 Nash, T.H., 1996. Photosynthesis, respiration, productivity and growth. In: Nash, III T.H. (Ed.), Lichen Biology. Cambridge University Press, Cambridge, pp. 88–121. Nilsson, S.G., Ericson, L., 1997. Conservation of plant and animal populations in theory and practice. Ecological Bulletins 46, 117–139. Ott, S., 1987. Differences in the developmental rates of lichens. Annales Botanici Fennici 24, 385–393. Palmqvist, K., Sundberg, B., 2000. Light use efficiency of dry matter gain in five macrolichens: relative impact of microclimate conditions and species-specific traits. Plant, Cell and Environment 23, 1–14. Peck, J.E., McCune, B., 1997. Remnant trees and canopy lichens communities in western oregon: a retrospective approach. Ecological Application 7, 1181–1187. Purvis, O.W., Coppins, B.J., Hawksworth, D.L., James, P.W., Moore, D.M., 1992. The Lichen flora of Great Britain and Ireland. The British Lichen Society, London. Rikkinen, J., 1995. What’s behind the pretty colours? A study on the photobiology of lichens. Bryobrothera 4, 1–239. Rose, F., 1992. Temperate forest management: its effects on bryophyte and lichen floras and habitats. In: Bates, J.W, Farmer, A.M. (Eds.), Bryophytes and lichens in a changing environment. Claredon Press, Oxford, pp. 211–233. Saunders, D.A., Hobbs, R.J., Margules, C.R., 1991. Biological consequences of ecosystem fragmentation. A review. Conservation Biology 5, 18–32. Scheidegger, C., 1995a. Early development of transplanted isidioid sorestia of Lobaria pulmonaria in an endangered population. Lichenologist 27, 361–374.
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Scheidegger, C., 1995b. Transplantation of symbiotic propagules and thallus fragments: methods for the conservation of threatened epiphytic lichen populations. Mitteilungen der Eidgeno¨ssischen Forschungsanstalt fu¨r Wald, Schnee und Landschaft 70, 41–62. Schemske, D.W., Husband, B.C., Ruckelhaus, M.H., Goodwillie, C., Parker, I.M., Bishop, J.G., 1994. Evaluating approaches to the conservation of rare and endangered plants. Ecology 75, 584–606. Sillett, S.C., Goslin, M.N., 1999. Distribution of epiphytic macrolichens in relation to remnant trees in a multiple-age Douglas-fir forest. Canadian Journal of Forest Research 29, 1204–1215. Sillett, S.C., McCune, B., 1998. Survival and growth of cyanolichen transplants in Douglas-fir forest canopies. Bryologist 101, 20–31. Sillett, S.C., McCune, B., Peck, J.E., Rambo, T.R., Ruchty, A., 2000. Dispersal limitations of epiphytic lichens result in species dependent on old-growth forests. Ecological Applications 10, 789–799. SPSS Inc. 1997. SPSS Advanced Statistics 75. SPSS Inc., Chicago. Stevenson, S.K., 1988. Dispersal and colonization of arboreal forage lichens in young forests. British Columbia Ministry of Environment and British Columbia Ministry of Forest, IWIFR (Integrated Wildlife Intensive Forestry Research) 38. Victoria, British Columbia, Canada. Tapper, R., 1976. Dispersal and changes in the local distributions of Evernia prunastri and Ramalina farinacea. New Phytologist 77, 725– 734. Thor, G., Arvidsson, L., 1999. Ro¨dlistade lavar i Sverige — Artfakta. [Swedish Red Data Book of Lichens]. ArtDatabanken, SLU, Uppsala. Tibell, L., 1992. Crustose lichens as indicators of forests continuity in boreal coniferous forests. Nordic Journal of Botany 12, 427–450.
Colonization of old-forest lichens in a young and an old boreal Picea abies forest: an experimental approach Olga Hilmoa,*, Sigurd M. Sa˚stadb a
Department of Botany, Faculty of Chemistry and Biology, Norwegian University of Science and Technology, N-7491 Trondheim, Norway b Department of Natural History, Norwegian University of Science and Technology, N-7491 Trondheim, Norway Received 17 October 2000; received in revised form 26 January 2001; accepted 3 April 2001
Abstract Understanding the factors limiting the distribution of a species is crucial for designing conservation strategies. We evaluated whether the scarcity of old-forest lichens in young forests was due to unfavourable environmental conditions for colonization in young stands or to dispersal limitations. Vegetative diaspores of Lobaria scrobiculata, Platismatia glauca and Platismatia norvegica were sown on 240 spruce twigs transplanted to a young and an old stand of spruce. Our results demonstrate that the old-forest species established and grew as rapidly in the young as in the old forest. Higher light levels in the young, compared with the old forest, did not reduce diaspore development. Moreover, greater numbers of juvenile thalli of Platismatia were found on control twigs (unsown) in the old forest, compared with the young forest, suggesting higher propagule density and more efficient dispersal in the old stand. Our results indicate that life-history characteristics, which include dispersal characters, are important for explaining the species scarcity in younger stands. Minimizing the distance between regeneration units and potential sources of propagules is probably important for maintaining lichen biodiversity in managed forest ecosystems. # 2001 Elsevier Science Ltd. All rights reserved. Keywords: Conservation; Diaspores; Dispersal; Establishment
1. Introduction Commercial large-scale forestry affects biodiversity at various spatial and temporal scales (Franklin, 1993; Esseen et al., 1997). Habitat loss, habitat alteration and fragmentation of previously continuous forests has reduced species diversity in forest ecosystems (e.g. Harris, 1984; Saunders et al., 1991; Angelstam, 1992). Due to forest fragmentation, several species have elevated risks of local extinction (Nilsson and Ericson, 1997). Epiphytic lichens are considered to be particularly sensitive to forestry (e.g. Lesica et al., 1991; Esseen et al., 1997), and many such species are mainly confined to old forests stands in the boreal region (Tibell, 1992; McCune, 1993; Holien, 1996, 1997; Kuusinen and Siitonen, 1998). The lichen biomass in managed second growth stands is lower than in old-growth forests (Hyva¨rinen et al., 1992; McCune, 1993; Esseen et al., 1996; Dettki and Esseen, 1998). * Corresponding author. Fax: +47 73596100. E-mail address: [email protected] (O. Hilmo).
The survival of lichen populations is influenced by life-history characteristics such as production and dispersal of diaspores and the species ability to establish and develop under different environmental conditions. The scarcity of old forest lichens in younger forest stands could be due to inefficient dispersal of lichen propagules (Esseen et al., 1996; Sillett and McCune 1998) or it could be that unfavourable microclimatic conditions in the younger stands preclude establishment. Species confined to old, natural forests are considered to be sensitive to alteration in environmental conditions (Rose, 1992). Juvenile stages of epiphytic lichens have been shown to be sensitive to environmental influences as the rate of development differs between locations with relatively similar microclimate (Ott, 1987). Further, the microtopography of the bark significantly influences the establishment and survival of diaspores (Armstrong, 1990). Scheidegger (1995a) found that low reproduction potential limited the distribution of Lobaria pulmonaria. Understanding the factors influencing the size of a population is of great importance when designing conservation strategies aimed to
0006-3207/01/$ - see front matter # 2001 Elsevier Science Ltd. All rights reserved. PII: S0006-3207(01)00100-8
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maintain species diversity in forest ecosystems. Identification of critical life cycle stages determining population or metapopulation dynamics is crucial for designing recovery measures in conservation biology (Schemske et al., 1994). However, earlier studies of lichens in boreal forests have paid little attention to the initial phase of the life cycle. The aim of this study was to compare success of establishment and rate of development of lichen diaspores in a young, planted stand of Picea abies (L.) Karst. and an old Picea abies forest where the studied species occur naturally. Our experiment included Lobaria scrobiculata (Scop.) DC and Platismatia norvegica (Lynge) W. Culb. & C. Culb., both mainly distributed in old humid forests (Gauslaa, 1995; Holien and Tønsberg, 1996; Thor and Arvidsson, 1999) and defined as oldforest lichens in the present study. We also included Platismatia glauca (L.) W. Culb. & C. Culb. which is a common species in forests of different successional stages. By doing a field experiment we wished to assess whether old-forest species can establish in younger stands, or whether establishment is precluded for example, by sensitivity to environmental factors or because the twig bark of young stands is unsuitable for diaspore attachment. If successful establishment of the diaspores in the younger stand is found, this would indicate that dispersal or diaspore production is limiting for the species distribution. It is of vital interest to discriminate between these alternative models of explanations when assessing various methods in forestry, aimed to maintaining biodiversity in managed forest ecosystem.
Degel., Lobaria scrobiculata, Parmeliella parvula P. M. Jørg. and Platismatia norvegica on branches indicates a humid climate (Ahlner 1948; Jørgensen 1978). The common macrolichens colonizing the twigs are C. hultenii, H. physodes, H. tubulosa, Parmelia sulcata T. Tayl. and Platismatia glauca. P. glauca is the most dominant epiphytic foliose species in the old stand. A summary of stand temperature, humidity, radiation and bark pH is given in Table 1. The bark pH was measured according to Gauslaa and Holien (1998). 2.2. Lichen material The reproductive strategies of the three investigated species is mainly vegetative by production of symbiotic propagules. Apothecia (sexual reproductive structures) are very rarely observed (Purvis et al., 1992). Lobaria scrobiculata reproduces by soredia and Platismatia norvegica by formation of isidia, which sometimes become granular-sorediate. The regenerative structures of P. glauca are highly variable from simple-coralloid isidia to granular soredia (Purvis et al., 1992). 2.3. Experimental design Twigs of Picea abies (240 twigs, 10 mm in diameter) were sampled in the study area and cut to 10-cm in length. Lichen fragments and diaspores were removed from the twigs and the ends of the twigs were waxed. The twigs were not sterilized. Within three separate areas, each 1 cm2 in size, we made four parallel depressions to increase the roughness of the bark. Mature thalli of the three species were collected in the investigation
2. Material and methods 2.1. Study area The field experiment was performed in an old spruce forest (10.5 ha) and in an adjacent younger planted stand (1.1 ha) bordering the north side of the old forest. The study area is situated at 185 m a.s.l. in Melhus, SørTrøndelag, central Norway (63 080 N, 10 060 E). Picea abies dominates the area, where forestry has created a mosaic of contrasting successional stages. The younger forest consisted mainly of 5–7 m tall spruce trees about 30 years old. The epiphytic lichens represent a pioneer community (Hilmo, 1994) dominated by crustose species and Hypogymnia physodes (L.) Nyl. Other colonists in the young stand are Hypogymnia tubulosa (Schaer.) Hav. and Cetraria chlorophylla (Willd.) Vain. A few juvenile thalli of Platismatia glauca were observed on some of the branches. The old spruce forest has naturally regenerated and is multilayered. Some selective felling and windfall in the past has formed gaps in the canopy. The tallest trees are about 20 m high and 120 years old. The occurrence of Cavernularia hultenii
Table 1 Mean air temperature ( C), relative air humidity (%), photon flux density (mmol m2 s1) and total number of hours 5150 mmol m2 s1 in July and January, measured 2 m above ground among north-facing branches, in the young and old forest Young forest
Old forest
Air temperature
July January
12.8 5.4
12.2 4.8
Air humidity
July January
82.3 82.0
82.9 81.4
Photon flux density
July January
121.1 4.1
Number of hours 5150 mmol m2 s1
July
252
January Bark pH
(814.0) (44.7)
0 4.1 (3.8–4.4)
14.9 0.6
(268.8) (7.1)
5 0 4.3 (3.9–4.5)
The radiation sensor (LI-190SZ Quantum Sensor) and the probe measuring humidity and temperature (HMP35AC, LI-COR) recorded at intervals of 10 min and the hourly mean was stored. Maximum values of photon flux density are given in parenthesis. Bark pH (median, minimum and maximum) are given for 25 twigs at each stand.
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area and in adjacent mature forests. Diaspores were brushed off the thalli and stored at 5 C for up to 2 days before sowing. Diaspores of the three species were sown separately within the three areas on each twig. The marked area was completely covered by diaspores (100% cover). The twigs were carefully sprayed with water before and after sowing. Twenty twigs were mounted with plastic coated wires on each of 12 frames made of polyvinylchloride (Fig. 1). Ten twigs were from the young stand (young forest substratum) and 10 were from the old natural forest (old forest substratum). Four twigs on each frame were controls without sown diaspores. These twigs were added to assess the establishment of naturally dispersed diaspores in the two habitats. The twigs were also used to compare the amount of juvenile thalli developed from naturally dispersed diaspores on young and old forest substrata. The frames were placed on the most north-facing branch 2 m above ground on randomly selected trees within an area of 3050 m. Six frames were located in the young forest and six frames in the old forest. The experiment started in July 1995 and ended in July 1999.
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Fig. 1. Units used for experiment of establishment and development of lichen diaspores. 10 twigs, from each habitat, with sown diaspores fastened to a specially constructed frame.
2.4. Harvest of twigs Twigs with sown diaspores were harvested monthly from August 1995 until November 1995, and then every second month until October 1996. At each harvest one twig was taken randomly from each frame. Three twigs of young forest substratum and three twigs of old forest substratum were removed from each habitat at each harvest. Additional harvests were made in April, July and November 1997 and in June 1998. The two last twigs of each substratum type were harvested in June 1999.
Fig. 2. Diaspores of Platismatia norvegica attached to the substratum (arrow) by outgrowing hyphae. Scale=100 mm.
2.5. Analyses of establishment success and rate of development Establishment was defined as when the diaspores were attached to the substratum by outgrowing hyphae (Fig. 2). To determine establishment, diaspores on harvested twigs were examined in a scanning microscope (Jeol, JMS-25s; Hilmo and Ott, unpublished). The degree of establishment was estimated from the percentage cover of diaspores within each sown area during a 1 year period from November 1995 to October 1996. The cover of diaspores was measured with a stereomicroscope. The measurements started after the diaspores were attached to the substratum by outgrowing hyphae (November 1995), but ended before the diaspores started to elongate and develop further (October 1996; Fig. 2). The rate of development of sown diaspores was estimated as: (1) percentage cover of flattened lobules (Fig. 3) of the established diaspores, and (2) as size (mm) of the 10 largest lobules within each sown area.
Fig. 3. Flattened lobules of Platismatia norvegica 4 years after transplantation. Scale=100 mm.
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The size represented the largest diameter (mm) of each lobule. These measurements were performed with a stereomicroscope on the 24 twigs sampled at the end of the experiment in June 1999.
yijkln ¼ þ Spi þ Hj þ Sk þ lðjÞ þ SpHij þ SpSik
2.6. Light measurements
where yijkln is the response of the nth sowing unit on the lth frame on the kth substratum, from the jth habitat, belonging to the ith species, and is the mean of the response. The frame random effect () is nested within habitat (H) and is used as an error term when testing for differences between habitat. Species (Sp), substratum (S) and frames () were tested against the residual error. Species, habitat and substratum were considered fixed effects. All interactions among the fixed effects were included in the model. Cover of diaspores was ln-transformed and the percentage cover of flattened lobules was arcsin transformed to achieve homogenous variation among samples. Lobaria scrobiculata was omitted from the statistical treatment of cover of flattened lobules and size of lobules, because very few diaspores had reached this stage of development. ANOVA was carried out using the general linear modelling option in SPSS, version 8.0 for windows (SPSS, Inc. 1997).
Photosynthetically active radiation (mmol photons m2 s1) was measured at five points within each of the 12 frames. These measurements were made on cloudy days and included simultaneous measurements of radiation at a reference point in an adjacent open field (radiationref) and radiation measurements within the frames (radiationframe). Radiation was measured three times during 2 days, at 9 a.m., 12 p.m. and 3 p.m. in July. The radiation at each point within the frames was expressed as a radiation index calculated by the formula: (radiationframe /radiation ref) 100%. 2.7. Statistical treatment of data Cover of diaspores of the three lichen species was analysed using analysis of variance (ANOVA) according to the model:
þ HSjk þ SpHSijk þ ijkln
ð2Þ
yijklmn ¼ þ Spi þ Hj þ Sk þ lðjÞ þ mðlÞ þ SpHij 3. Results þ SpSik þ HSjk þ SpHSijk þ ijklmn
ð1Þ 3.1. Success of establishment
where yijklmn is the response of the nth sowing unit on the mth twig on the lth frame on the kth substratum, from the jth habitat, belonging to the ith species, and is the mean of the response. The twig random effect (b), is nested within frame () and used as an error term when testing for differences between substratum (S) and frames. The frame random effect is nested within habitat (H) and is used as an error term when testing for differences between habitat. Species (Sp) were tested against the residual error term. Species, habitat and substratum were all considered fixed effects. All interactions among the fixed effects were included in the model. The twig within frame effect may be potentially ascribed not only to natural variation among twigs, but also by the fact that twigs were harvested at intervals of about 2 months over a 1 year period. The date of harvest is not considered in the analysis as linear regression revealed no significant relationship between time of sampling and cover of diaspores on 72 twigs sampled during the period November 1995 to October 1996 (P=0.342). The analyzed time interval starts when the diaspores were attached to the twigs by outgrowing hyphae and ended before the diaspores showed sign of expansion. Percentage cover of flattened lobules and mean size of the largest thalli were analysed using ANOVA according to the model:
The loss of sown diaspores was high during the first weeks before the diaspores attached to the substratum by outgrowing hyphae. Subsequent to attachment the loss was negligible. The mean untransformed cover of diaspores was 4.8% within the investigated sown areas. In spite of high initial loss of diaspores, none of the sampled twigs during the experiment was totally lacking diaspores. Cover of diaspores differed significantly between the two substrata (Table 2; Fig. 4). Although the mean cover of diaspores was slightly higher on twigs located in the old forest, compared with the young forest (5.2 and 4.4%, respectively) this difference was not significant (Table 2). Cover of diaspores also differed significantly between the species (Table 2), with Platismatia norvegica having the highest and Lobaria scrobiculata the lowest cover of diaspores (Fig. 4). Analysis of variance revealed much variation in cover of diaspores among frames within the localities (Table 2). The mean cover of diaspores of all three species on the 12 frames varied between 2.6 and 9.5%. Cover of diaspores also varied considerably among twigs within frames (Table 2). Linear regression showed a significant positive relationship between cover of diaspores and light exposure of the frames for each of the species located in the old forest (Fig. 5). A negative
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relationship between light and cover of diaspores is indicated in the young forest. This relationship, however, is not significant because of the relatively high cover of diaspores found on twigs situated on a frame with extreme light values (Fig. 5). 3.2. Rate of development Four years after sowing the diaspores, flattened lobules (Fig. 3) of the Platismatia species were observed within all the sown areas. A significantly higher percentage cover of flattened lobules was found in P. norvegica (62.9%), compared with P. glauca (34.6%; Table 3). However, no interactions were found between species and habitat or species and substratum (Table 3). The mean size of the 10 largest juvenile lobules was 0.5 mm for P. norvegica and 0.4 mm for P. glauca, but the differences observed between analysed species, habitat or substratum regarding this variable were not Table 2 ANOVA of cover of diaspores of Lobaria scrobiculata, Platismatia glauca and Platismatia norvegica (‘Species’) in a young and old forest (‘Habitat’) sown on substratum from young and old forest (‘Substratum’) Source of variation
d.f.
MS
F
P
Species Habitat Substratum SpeciesHabitat SpeciesSubstratum HabitatSubstratum SpeciesHabitatSubstratum Frame (Habitat) Twig (Frame) Residual
2 1 1 2 2 1 2 10 58 136
8.173 1.248 5.865 0.085 0.462 0.249 0.050 2.167 0.497 0.367
22.293 0.576 11.802 0.230 1.259 0.500 0.137 4.359 1.356
0.000 0.465 0.001 0.794 0.287 0.482 0.872 0.000 0.077
Fig. 4. Cover of diaspores of Lobaria scrobiculata, Platismatia glauca and P. norvegica on bark substratum from the young forest (&) and bark substratum from the old forest (&). Error bars are one Standard Error.
255
significant (Table 4). Observations of Lobaria scrobiculata with scanning microscopy, revealed diaspores in different stages of development on six twigs from the young forest and five twigs from the old forest. However, well-developed juvenile lobules were observed on only two twigs, one from each of the habitats. The ontogeny of the investigated species is thoroughly discussed in Hilmo and Ott (unpublished). Cover of flattened lobules (Table 3) and mean size of the 10 largest thalli (Table 4) of Platismatia varied widely among frames within the localities. The mean percentage cover of flattened lobules (of the established diaspores) on the 12 frames varied between 20.0 and 78.8. The mean size of the 10 largest juvenile thalli within each of the frames varied between 0.3 and 0.7 mm. Table 3 ANOVA of percentage cover of flattened lobules of Platismatia glauca and Platismatia norvegica (‘Species) in young and old forest (‘Habitat’), and on substratum from young and old forest (‘Substratum’) Source of variation
d.f.
MS
F
P
Species Habitat Substratum SpeciesHabitat SpeciesSubstratum HabitatSubstratum SpeciesHabitatSubstratum Frame (Habitat) Residual
1 1 1 1 1 1 1 10 30
1.405 0.014 0.013 0.013 0.002 0.010 0.164 0.320 0.030
46.822 0.044 0.418 0.420 0.080 0.319 5.466 10.661
0.000 0.837 0.523 0.522 0.779 0.576 0.026 0.000
The dependent variable was arcsin transformated to achieve homogenous varians.
Fig. 5. Relationship between cover of diaspores of Lobaria scrobiculata (^), Platismatia glauca (*) and P. norvegica (&) and light exposure of each frame situated in the young (open symbols) and old forest (filled symbols). Separate linear regression of the three species in the old forest are shown: Platismatia norvegica (solid line; r2=0.80*), Platismatia glauca (dotted line; r2=0.66*) and Lobaria scrobiculata (dashed line; r2=0.73*). *P<0.05.
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4. Discussion
Fig. 6. Pigmented cortex of juvenile lobes of Platismatia glauca located in the young forest. Scale=1 mm. Table 4 ANOVA of mean size of the 10 largest juvenile thalli of Platismatia glauca and Platismatia norvegica (‘Species’) in a young and old forest (‘Habitat’), and on young and old forest substratum (‘Substratum’) Source of variation
df
MS
F
P
Species Habitat Substratum SpeciesHabitat SpeciesSubstratum HabitatSubstratum SpeciesHabitatSubstratum Frame (Habitat) Residual
1 1 1 1 1 1 1 10 30
0.0517 0.0069 0.0005 0.0095 0.0230 0.0038 0.0252 0.0711 0.0173
2.995 0.097 0.027 0.550 1.331 0.218 1.461 4.122
0.094 0.762 0.870 0.464 0.258 0.644 0.236 0.001
A dark pigmented cortex was characteristic for the juvenile thalli of Platismatia located in the young forest (Fig. 6). This pigmentation was not found in the old natural forest. Examination of the control twigs (48 twigs) at the end of the experiment revealed a significantly higher number of marked areas (1 cm2) with juvenile lobules of Platismatia in the old natural forest (29%), compared to the young forest (10%; P=0.006, w2test). No significant differences were found between the two substratum types, as 46% of the twigs with observed small lobules were young forest substratum and 54% of the twigs were old forest substratum (P=0.593, w2test). Lobules of Hypogymnia were observed within the marked areas on 8 and 9% of the control twigs from the young and old forest, respectively. However, only a few lobules were established within the marked areas for both Platismatia and Hypogymnia and the cover of the lobules did not exceed 1% of the marked areas. With exception of two observation of Cetraria chlorophylla and one observation of Bryoria no other species was observed on the control twigs.
The absence of any species in a habitat can be explained by several biotic or abiotic factors including production and dispersal of propagules, attachment of propagules to the substratum, substratum quality, substratum availability and microclimatic conditions (Armstrong, 1988). The distribution of several lichens confined to old forests, e.g. species in the Lobaria community, has been explained by the particular microenvironment created by the structure of old forests (Lesica et al., 1991; Kuusinen, 1996). Our results, however, demonstrate that the environmental conditions in young forests are not necessarily unfavourable for establishment and development of diaspores of old-forest species such as Lobaria scrobiculata and Platismatia norvegica. The success of establishment and rate of development of the diaspores are as high in the young forest as in the old forest. This is in accordance with recent results of Sillett et al. (2000) who emphasized that particular substrata and microenvironments found only in old growth forest are not essential for the distribution of Lobaria oregana. 4.1. Dispersal limitations This investigation indicates that diaspore production and dispersal ability are probably important in determining the distributional patterns of some old-forest species. The absence of Lobaria scrobiculata on the control twigs in both spruce stands and very few lobules of Platismatia on the control twigs in the young forest, even if the experimental frames were located only about 50 m from the forest edge, support the hypothesis of low dispersal ability. Little attention has been paid to the effectiveness of different diaspores to disperse. However, Dettki et al. (2000), who investigated the occurrence of lichen thalli in young forests at increasing distances (10, 50 and 100 m) from the old-growth forest, found that the number of thalli displayed a pronounced decrease with increasing distances from the source of propagules. Our result is also supported by Sillett et al. (2000) who found that establishment and growth of diaspores of Lobaria oregana sown on branches of Douglas-fir grew as rapidly in young as in old forests. The development of L. oregana populations was limited by poor dispersal and establishment. Low dispersal ability is also postulated by Sillett and Goslin (1999) who found that the biomass of lichen species, associated with old-growth forests, were highest near remnant trees in younger forest stands. In general, the production of vegetative diaspores is considered advantageous for rapid colonization (Bowler and Rundel, 1975; Bailey, 1976; Jahns, 1988). However, studies of lichen dispersal have shown that soredia from several species are mostly deposited within a short distance of their source (Tapper, 1976;
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Armstrong, 1987, 1994; Stevenson, 1988). According to Jahns (1984, 1988) heavy isidia serves primarily for growth and regeneration at the site, not for dispersal of the species. 4.2. Substratum quality The higher cover of diaspores on young compared with the old forest substratum shows that the bark properties in the young forest stand were favourable for diaspore attachment. The higher cover of diaspores on twigs sampled in the young forest could be due to a slightly more sticky bark of these twigs (probably due to a higher content of resin), compared with the twigs collected in the old forest. A higher bark pH on twigs from the old forest, compared with twigs from the young forest (Table 1) seems not to have affected diaspore development of Lobaria scrobiculata in our experiment. The availability of naked bark is higher on mature trees in the old forest compared with younger trees in the plantation. On young trees the needles cover almost the whole branch, from branch tip to branch base, whereas only the branch tip is covered by needles of mature trees. If the cover of needles negatively influences the establishment or development of diaspores, the amount of suitable sites to colonize are more scarce in the young compared with the old forest. Since the experimental twigs had no needles this factor is not taken into consideration. It is unlikely that the lack of needles on the experimental twigs could explain the relatively low success of establishment and development of the sown diaspores of L. scrobiculata. Field observations of L. scrobiculata in the investigation area shows that juvenile thalli mainly are distributed on the outermost part of the branches on needle-free twigs as well as on needle-bearing twigs. According to Hilmo (1994) the cover of Platismatia norvegica is highest on spruce branches with a low cover of needles. The high loss of diaspores observed, indicates that rapid development of anchoring hyphae is crucial for successful establishment at a new site. The period before the hyphae anchors the deposited diaspores to the substratum is thus a critical phase in the life cycle. This is supported by Scheidegger (1995b) who claimed that immobilization of diaspores on the substratum seems to be a major limiting factor in the reproductive process. 4.3. Microclimatic conditions A number of environmental factors are considered important for lichens; for example light conditions (Gauslaa and Solhaug, 1996; Palmqvist and Sundberg, 2000), water accessibility (Lange et al., 1986; Nash, 1996), bark pH (Gauslaa and Holien, 1998) and bark stability of growing trees (Hesselman, 1937). The air humidity was high throughout the year, both in the
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young and old forest. In spite of markedly higher light levels in the young compared to the old forest (Table 1), there were no significant differences in success of establishment or rate of development between the two stands. This is in contrast to the results of Ott (1987) who found different rates of diaspore development between localities even when environmental differences were small. The lichens investigated by Ott developed most rapidly at locations where they occur naturally. Ott (1987) used different species and different forest environments than us, which could account for some of the different results between the two studies. The increase in cover of established diaspores with light exposure in the old forest indicates that low light may limit hyphal growth and hence attachment to the substratum. This is supported by Ahmadjian (1993) who found vacuolated, irregularly shaped hyphae in dark culture of the mycobiont. Since radiation in a forest can be highly spatially variable (Gauslaa and Solhaug, 2000), some of the old forest frames could well have been located in positions with radiation at, or around, the compensation point for photosynthesis. Gauslaa and Solhaug (1996) also found that Lobaria species were susceptible to high photon flux densities as photoinhibition was measured. Our study may indicate a unimodal response to light in all three species but the evidence for this is weak and requires that the one extremely exposed frame is omitted from the analysis. Brownish pigmentation of the juvenile cortex of Platismatia species situated in the young forest might support the hypothesis of a protective function of melanin pigmentation (Rikkinen, 1995). Although we did not find differences between the young and the old forest, which could be ascribed to environmental differences, a gradient from favourable to unfavourable microsites probably exists within both habitats due to variation in microclimatic conditions and also biotic factors such as herbivore activity. This may have caused the relatively high within-site variation in establishment and growth of the lichens. 4.4. Consequences for forest management Understanding the factors that limit the size of the lichen populations in managed forests is important for developing strategies to maintain biodiversity. Our field experiment indicate that the scarcity of old-forest lichens in younger stands are due to low dispersal ability of propagules, rather than environmental factors or bark properties. Our study supports the findings of Sillett et al. (2000), and these two studies are as far as we know, the only studies comparing establishment and development of lichen diaspores in young and old forests. Thus, it may be difficult to generalize on basis of the results and the study should be replicated under varying macroclimatic conditions. However, the results
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so far indicate that dispersal limitations is one important factor explaining the absence of old-forest species from the younger stand. Therefore, one strategy to promote lichen abundance in younger stands and to conserve old-forest associated lichens in managed forests could be to minimize the distance between regeneration units and potential sources of propagules. Retention of old trees in regeneration cohorts is one appropriate conservation method to increase the amount of diaspores in younger forest stands. Peck and McCune (1997) predicted that a group of remnant trees in regeneration cohorts provide canopy habitat that maintains the environment necessary for the establishment and growth of Lobaria oregana and alectorioid lichens. The importance of long ecological continuity for many epiphytic lichens is supported by a slow rate of development after attachment to the substratum.
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