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Farber, L., Solhaug, K., Esseen, P., Bilger, W., Gauslaa, Y. (2014) Sunscreening fungal pigments influence the vertical gradient of pendulous lichens in boreal forest canopies. Ecology, 95(6): 1464-1471 http://dx.doi.org/10.1890/13-2319.1

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Sunscreening fungal pigments inﬂuence the vertical gradient of pendulous lichens in boreal forest canopies

1 1 2 3 1,4 LEONIE FA¨ RBER, KNUT ASBJØRN SOLHAUG, PER-ANDERS ESSEEN, WOLFGANG BILGER, AND YNGVAR GAUSLAA 1Department of Ecology and Natural Resource Management, Norwegian University of Life Sciences, P.O. Box 5003, NO-1432 A˚s, Norway 2Department of Ecology and Environmental Science, Umea˚ University, SE-90187 Umea˚, Sweden 3Christian-Albrechts-University, Botanical Institute, Olshausenstr. 40, DE-24098 Kiel, Germany

Abstract. Pendulous lichens dominate canopies of boreal forests, with dark Bryoria species in the upper canopy vs. light Alectoria and Usnea species in lower canopy. These genera offer important ecosystem services such as winter forage for reindeer and caribou. The mechanism behind this niche separation is poorly understood. We tested the hypothesis that species-specific sunscreening fungal pigments protect underlying symbiotic algae differently against high light, and thus shape the vertical canopy gradient of epiphytes. Three pale species with the reflecting pigment usnic acid (Alectoria sarmentosa, Usnea dasypoga, U. longissima) and three with dark, absorbing melanins (Bryoria capillaris, B. fremontii, B. fuscescens) were compared. We subjected the lichens to desiccation stress with and without light, and assessed their performance with chlorophyll fluorescence. Desiccation alone only affected U. longissima. By contrast, light in combination with desiccation caused photoinhibitory damage in all species. Usnic lichens were significantly more susceptible to light during desiccation than melanic ones. Thus, melanin is a more efficient light-screening pigment than usnic acid. Thereby, the vertical gradient of pendulous lichens in forest canopies is consistent with a shift in type and functioning of sunscreening pigments, from high-light-tolerant Bryoria in the upper to susceptible Alectoria and Usnea in the lower canopy. Key words: Alectoria sarmentosa; boreal forest; Bryoria spp.; desiccation tolerance; epiphytes; melanin; photoinhibition; sunscreening pigments; Totena˚sen, Norway; Usnea spp.; usnic acid; Vindeln, Sweden. eports

INTRODUCTION form a vertical gradient, with Bryoria in the upper Pendulous lichens often envelop canopies in boreal canopy (Fig. 1a) and Alectoria (Fig. 1b) and/or Usnea R forests (Esseen et al. 1996). Such epiphytic communities on lower, often defoliated branches (Campbell and are dominated by the genera Alectoria, Bryoria, and Coxson 2001, Benson and Coxson 2002, Coxson and Usnea, which play important functional roles. They Coyle 2003). In Norwegian boreal forests, the biomass provide winter forage for reindeer and caribou (Kinley of Bryoria increased by a factor of 1.6 from 2–3 m to 5–6 et al. 2006, Kivinen et al. 2010) and habitat for canopy- m above the ground, with a concurrent decline (to 61%) living invertebrates constituting critical fodder for in Alectoria and Usnea (Gauslaa et al. 2008); their sites overwintering passerine birds (Pettersson et al. 1995). are in the same bioclimatic region as our Norwegian site. The biomass of pendulous lichens peaks in old forests The mechanism behind this niche partitioning is poorly (Esseen et al. 1996, Price and Hochachka 2001), and understood, but various factors are apparently involved. conversion of old forests to managed stands with short Goward (1998, 2003) hypothesized that lack of Bryoria rotations (,100 years) has dramatically decreased this in the lower canopy is due to their susceptibility to epiphytic component (Dettki and Esseen 1998, 2003). prolonged wetting and preference for well-ventilated Several species, such as Usnea longissima, are of concern upper canopy. Coxson and Coyle (2003) supported this for conservation (Rolstad et al. 2013), as well as for hypothesis and predicted higher photosynthetic rates for ecosystem and wildlife management (Peck and McCune Alectoria sarmentosa in the lower canopy where it 1997). occurs, but concluded that growth responses alone did not explain the niche partitioning in pendulous lichens. Epiphyte communities often show vertical stratification (McCune 1993). Pendulous lichens in boreal forests Recently, phosphorus availability (McCune and Cald- well 2009) and exogenous carbohydrates (Campbell et al. 2013) have been introduced as factors influencing the Manuscript received 16 December 2013; revised 19 February realized niches for foliose canopy lichens. 2014; accepted 26 February 2014. Corresponding Editor: F. C. Field evidence suggests that the bright pigment usnic Meinzer. 4 Corresponding author. acid (Alectoria and Usnea) vs. dark melanins (Bryoria) E-mail: [email protected] shape the vertical gradient. Alectoria and Bryoria 1464 June 2014 PENDULOUS LICHENS IN BOREAL CANOPIES 1465 containing contrasting pigments are taxonomically more related to each other than to the genera (Alectoria and Usnea) containing usnic acid (Thell and Moberg 2011). Both melanins (e.g., Gauslaa and Solhaug 2001) and usnic acid (McEvoy et al. 2007) screen light, and thus protect underlying photobionts. However, these pigments function differently: melanins absorb light, whereas usnic acid reflects excess light (Solhaug and Gauslaa 2012). We do not know which screening mechanism is most efficient. Light-screening has not yet been directly measured in pendulous lichens. If these pigments play a functional role for vertical epiphyte distribution, we hypothesize that melanin is the most efficient screening compound. This needs to be tested, because lichen compounds may have multiple functions (Molna´ r and Farkas 2010). The upper canopy experiences stronger solar radiation and desiccation than low branches (Parker 1997, Coxson and Coyle 2003). Because light is strongest in clear and dry weather, high light stress is confounded with desiccation stress. Both high light (Gauslaa and Solhaug 1996) and desiccation (Green et al. 1991) can adversely affect forest lichens. Here, we experimentally separated the effects of desiccation from those caused by high light FIG. 1. The vertical canopy gradient with (a) melanic R by exposing six pendulous lichens to four drying regimes Bryoria species in the upper canopy and (b) usnic lichens in the with and without light, using chlorophyll fluorescence to lower canopy (e.g., Alectoria sarmentosa) represents a striking boreal phenomenon, not only in Scandinavia where this study quantify damage and the recovery of the photosynthetic was done, but also in inland north-central British Columbia eports apparatus. We tested the following hypotheses: (1) (a, b, upper Slim Creek valley; photo credit: Y. Gauslaa). (c) lichens with melanins (Bryoria) are more tolerant to Sampled lichen species in this study from left to right: Alectoria high light than Alectoria and Usnea with usnic acid; and sarmentosa, Usnea dasypoga, U. longissima, Bryoria capillaris, B. fremontii, B. fuscescens (photo credit: K. A. Solhaug). (2) Bryoria species are more tolerant of desiccation than Alectoria and Usnea. 1984702900 E) was from a moist-wet, closed-canopy P. MATERIAL AND METHODS abies stand near a small stream. 0 00 0 00 Lichen material and study area In Totena˚sen (60835 15 N, 11802 04 E; 720 m a.s.l.), all lichens were collected from the same branches. The Among our species (Fig. 1c), Alectoria sarmentosa open, old P. abies forest was moist (1000 mm annual (Ach.) Ach., Usnea dasypoga (Ach.) Nyl., and U. precipitation; 180–190 d/yr had .0.1 mm, and snow longissima Ach. contained usnic acid, whereas Bryoria lasting 175–199 d; Moen 1999), located in upper parts of capillaris (Ach.) Brodo and D. Hawksw., B. fuscescens a steep, northeast-facing slope. Mean annual tempera- (Gyeln.) Brodo and D. Hawksw., and B. fremontii ture was 0–28C, ranging from 88C in January to 148C (Tuck.) Brodo and D. Hawksw. contained melanins. Lichens were collected August–October 2012 in old in July. forests from Picea abies branches in the boreal sites Lichens were stored air-dry at 208C (recommended Vindeln (northern Sweden) and Totena˚sen (southeastern by Honegger 2003). Six months later, two samples were Norway). Sampling was done 2–4 m above ground taken from each specimen, resulting in n ¼ 48 samples because we wanted to study species-specific rather than per species and site; n ¼ 432 samples in total. Each environmental effects, and the lower canopy is the only sample was selected species-wise for a given desiccation/ vertical zone where all species may co-occur. light treatment according to random numbers. Separate Vindeln had 600 mm annual precipitation (;65% as thalli were randomly taken for chlorophyll measure- rain; snow from November–April); mean annual temper- ments (Appendix A). ature was 28C, 118C in January and 148C in July (Raab Preconditioning of lichens and measurement and Vedin 1995). Collections were done at 175–200 m of chlorophyll fluorescence parameters above sea level; B. fuscescens, B. fremontii (6481304700 N, 1984605700 E), and A. sarmentosa (6481402300 N, 1984704600 Lichens were sprayed with deionized water and kept E) were from mesic, semi-open stands with Picea abies moist at 148C in low light (20 lmolm2s1) for 24 h to and Pinus sylvestris. Bryoria capillaris was collected in a reduce occasional photoinhibition from the field. Then mesic, open P. sylvestris and P. abies stand (6481305800 N, they were kept 15 min in darkness before maximal 0 00 0 00 19849 37 E), whereas U. dasypoga (64814 13 N, quantum yield (Fv/Fm) of photosystem II (PSII), 1466 LEONIE FA¨ RBER ET AL. Ecology, Vol. 95, No. 6

TABLE 1. Initial values of chlorophyll ﬂuorescence parameters (arbitrary units for Fm and F0, means 6 SE) measured in hydrated specimens of six pendulous lichens with usnic acid or melanins as cortical sunscreening pigments collected from Sweden and Norway.

Usnic acid Fluorescence parameter Alectoria sarmentosa Usnea dasypoga Usnea longissima

Maximal quantum yield, Fv/Fm Sweden 0.716ab 6 0.002 0.704bc 6 0.003 Norway 0.706a 6 0.004 0.692a 6 0.004 0.693a 6 0.004

Maximal ﬂuorescence, Fm Sweden 0.818a 6 0.029 0.879a 6 0.037 Norway 0.660a 6 0.025 0.593ab 6 0.024 0.557b 6 0.021

Minimal fluorescence, F0 Sweden 0.231a 6 0.008 0.259a 6 0.010 Norway 0.193a 6 0.007 0.181ab 6 0.006 0.168b 6 0.005 Notes: Sample size is n ¼ 48 replicates per species 3 site combination. Values for P and adjusted r2 are from GLMs testing effects of species on fluorescence parameters within each site. Superscripts with different letters within a row denote species that are significantly different (at P , 0.05; Tukey post hoc test). Boldface indicates significant at P , 0.05. Ellipses indicate that no data were available.

maximal (Fm), and minimal fluorescence (F0), where kept moist for 24 h. We measured Fv/Fm, Fm, and F0 as variable fluorescence Fv is the difference between Fm and described for the preconditioning, but the kinetics F0 (Maxwell and Johnson 2000), were measured by a during recovery were recorded after 15 minutes of dark portable fluorometer (PAM-2000; Heinz Walz GmbH, adaptation at 30 min, 2 h, 6 h, and 24 h in low light. Effeltrich, Germany), with the fiber optics 1 cm away Statistical analyses from the sample using the 608 distance clip (Model 2010A; Heinz Walz GmbH). Each sample was arranged We analyzed data from the two sites separately. to fully cover the measuring area and the measuring General linear models (GLM with Tukey’s HSD post 2 1 light was set at intensity ;0.05 lmolm s ;the hoc test) were used to test if initial Fv/Fm, Fm, and F0 saturation pulse had the maximal intensity, and varied by species. Fm and F0 were square-root-trans- duration of 0.6 s. The lichens were then air-dried at formed. We analyzed species performance after the

eports 228C. experiment by expressing Fv/Fm as percentage of initial Fv/Fm values to remove the initial between-species Light and desiccation treatment variability. We ran a full GLM model with humidity,

R The experiment, modified after Gauslaa et al. (2012), light treatment, and species as fixed factors. The was repeated three times. Two samples of each species 3 temporal response during the recovery was analyzed in site combination were included in each replication (n ¼ 6 separate GLMs for 0.5 h and 24 h, because variances samples per treatment). During treatment, air-dry decreased over time following the increase in Fv/Fm. lichens lay on a net, 5 mm below the lid of a clear, Heteroscedasticity and non-normality were checked by sealed plastic box (10 3 8 3 4 cm). Each box had 25 mL examining residuals. No transformation was needed for of saturated salt solutions or silica gel to obtain 75%, Fv/Fm. Analyses were done in IBM SPSS version 21 (IBM 2012). 55%, and 33% relative humidity using NaCl, Mn(NO)3, and MgCl2, respectively (Greenspan 1977), and 0% RESULTS (silica gel). Eight boxes, two for each humidity, were placed for 7 Initial fluorescence parameters dat148C under a high-intensity (400 lmolm2s1) Initial fluorescence parameters showed similar pat-

LED light-diodes panel (SL3500; Photon Systems terns in Sweden and Norway (Table 1). In Sweden, Fv/ Instruments, Brno, Czech Republic). Boxes were rotated Fm differed by species. The highest Fv/Fm (0.728) daily to ensure similar light doses for all treatments. occurred in the darkly melanic B. fremontii and B. Temperatures of lichens, salt solutions, and air inside fuscescens. The lowest values (0.694) were observed in boxes were measured with a thermocouple data logger the pale B. capillaris (Sweden) and the usnic lichens U.

(model TC-08; Pico Technology, St Neots, Cambridge- dasypoga and U. longissima (Norway). Maximal (Fm) shire, UK). Lichens reached 228C, salt solutions reached and minimal ﬂuorescence (F0) were strongly coupled 2 2 198C, and air temperature inside the boxes was 228C. across (radj ¼ 0.970; n ¼ 432) and within (radj ¼ 0.854– Another set of eight boxes (as previously described) were 0.966; P , 0.001; n ¼ 48) all species 3 locality kept in darkness for 7 d at 228C to eliminate temperature combinations. The species-speciﬁc differences were

differences between light and dark treatments. Thereaf- much stronger for Fm and F0 than for Fv/Fm (Table 1). ter, lichens were hydrated with deionized water and were At both sites, Fm was four times higher in A. sarmentosa June 2014 PENDULOUS LICHENS IN BOREAL CANOPIES 1467

TABLE 1. Extended.

Melanins 2 Bryoria capillaris Bryoria fremontii Bryoria fuscescens P radj

0.694c 6 0.004 0.728a 6 0.003 0.728a 6 0.003 ,0.001 0.241 0.701a 6 0.006 0.111 0.016

0.570b 6 0.028 0.246c 6 0.012 0.201c 6 0.009 ,0.001 0.783 0.163c 6 0.010 ,0.001 0.740

0.172b 6 0.008 0.067c 6 0.003 0.054c 6 0.003 ,0.001 0.813 0.049c 6 0.003 ,0.001 0.772 and U. dasypoga than in the melanic B. fremontii and B. (Fig. 3b). The light treatment during drying increased fuscescens,withU. longissima and B. capillaris in the variation in Fv/Fm in all species apart from U. between. longissima, which exhibited strong variation also after desiccation in darkness. For lichens treated with light, Desiccation and light experiment there was a stronger decrease of Fv/Fm with increasing As a percentage of initial values, Fv/Fm differed F0 than for those in darkness (Fig. 3). This discrepancy strongly between light and dark treatments and between was stronger in a similar plot (not shown) with Fv/Fm 2 species (Fig. 2, Table 2). Desiccation in the absence of and Fm: for light, radj ¼ 0.211, P , 0.001; for darkness, R 2 light (7 d), even at 0% relative humidity, had minor radj ¼ 0.015, P ¼ 0.039 (n ¼ 216). effects on Fv/Fm (Appendix B). In some Bryoria species,

DISCUSSION eports mean Fv/Fm at the end of the dark treatment exceeded initial values after 24 h of recovery at low light Although earlier studies on vertical niche partitioning (Appendix C). However, in U. longissima the dark in pendulous lichens have focused on growth and treatment caused substantially delayed recovery of Fv/ macroclimatic limitations (Goward 1998, 2003, Camp- Fm (Fig. 2b). After 24 h of hydration, full recovery still bell and Coxson 2001, Coxson and Coyle 2003), this had not taken place (94.1% 6 1.2%; mean 6 1SE). study emphasizes the role of cortical pigments. By Unlike the other species, U. longissima was thus screening excessive light for underlying photobionts, susceptible to desiccation. fungal pigments improve lichen functioning in well-lit Light during desiccation caused significant and lasting habitats (Solhaug and Gauslaa 2012). Foliose usnic Fv/Fm depression (Fig. 2, Table 2). The light 3 humidity lichens are abundant in sun-exposed habitats at all interaction was highly significant for the Swedish latitudes (e.g., Elix 1994, Hauck et al. 2007), whereas samples, implying that the hardest desiccation aggra- melanic lichens grow in sunny habitats at high latitudes vated the decline of Fv/Fm in light-treated specimens. or altitudes (e.g., Brodo and Hawksworth 1977, Es- Lichens exposed to light recovered more slowly than slinger 1977, Hauck et al. 2007). Thus, both usnic acid those kept dark (Fig. 2). Melanic and usnic species and melanins may form efficient sunscreens. However, differed in post hoc tests after 30 minutes of recovery; dark Bryoria species were more tolerant to light in the confidence intervals did not overlap up to 6 h in any site. desiccated state than were similar life-forms with usnic The melanic species were less photoinhibited than those acid (Fig. 2), consistent with higher screening by with usnic acid. Usnea longissima was more light melanins. Recorded photoinhibition in usnic lichens, susceptible than the other species (Appendix C), with evidenced as depressed Fv/Fm, may explain why they are much delayed and incomplete recovery subsequent to replaced by melanic species with increasing branch hydration, followed by A. sarmentosa and U. dasypoga. height. In a northern Sweden site, biomass of dark Among usnic lichens, U. dasypoga was fairly similar to Bryoria had a higher canopy openness threshold than the most susceptible weakly melanic species, B. capil- that of A. sarmentosa (P.-A. Esseen, unpublished data), laris. The pale B. capillaris showed an initially deeper showing that similar replacement processes along depression than the two dark Bryoria spp. (Fig. 2c), gradients from sun to shade occur on vertical as well although the mean after 24 h of recovery did not differ as on horizontal forest scales. Shifts between melanic much (Appendix C). and pale lichens in coniferous canopies are probably The intra- and interspecific variation in fluorescence driven by height- and/or canopy-openness-dependent parameters is shown in Fig. 3, where Fv/Fm after 30 variation in solar radiation, consistent with reported minutes of recovery was plotted against initial F0 for physical and physiological limitations of pendulous samples subjected to light (Fig. 3a) and dark treatment lichens (Coxson and Coyle 2003). 1468 LEONIE FA¨ RBER ET AL. Ecology, Vol. 95, No. 6 eports R

FIG. 2. Recovery of photosynthetic performance (measured as percentage of initial values of maximal quantum yield, Fv/Fm,) in lichens with melanins (solid symbols) and usnic acid (open symbols) as sunscreening pigments after seven days’ treatment (a, b) in darkness and (c, d) in high light (400 lmolm2s1) in Sweden and Norway. Data were pooled over four humidity levels (0%,35%, 55%, and 75%; n ¼ 24 replicates for each species 3 light treatment 3 site combination). Values are means with 95% conﬁdence intervals; different letters in the keys indicate species that are signiﬁcantly different (P , 0.05) after 0.5 h and 24 h.

TABLE 2. Summary of GLMs for maximal quantum yield (Fv/Fm, percentage of initial values) for pendulous lichen species from two sites (Sweden and Norway), two light treatments, and four humidity treatments measured after 0.5 h and 24 h during recovery.

Sweden Norway 2 2 2 2 0.5 h (radj¼ 0.808) 24 h (radj¼ 0.281) 0.5 h (radj¼ 0.751) 24 h (radj¼ 0.417) Factor df FPFPdf FPFP Species, S 4 33.3 ,0.001 3.7 0.007 3 94.1 ,0.001 27.8 ,0.001 Light, L 1 824.8 ,0.001 63.2 ,0.001 1 285.1 ,0.001 39.2 ,0.001 Humidity, H 3 2.2 0.093 2.9 0.036 3 2.3 0.083 0.8 0.498 S 3 L 4 8.0 ,0.001 1.8 0.129 3 5.2 0.002 7.7 ,0.001 S 3 H 12 1.5 0.118 0.8 0.674 9 0.6 0.791 0.9 0.522 L 3 H 3 6.3 ,0.001 5.2 0.002 3 1.2 0.313 2.5 0.060 S 3 L 3 H 12 0.9 0.593 1.1 0.334 9 0.8 0.630 0.4 0.935 Total 240 192 Notes: The light treatments were 0 vs. 400 lmolm2s1; the humidity treatments were 0%,33%,55%, and 75% relative humidity. Recovery was at 20 lmolm2s1 in the hydrated state. Boldface indicates signiﬁcance at P , 0.05. June 2014 PENDULOUS LICHENS IN BOREAL CANOPIES 1469

Initial F0 and Fm in usnic species were much higher than in melanic ones (Table 1). Because we used the same measuring light for recording fluorescence, differences in F0 and Fm should reflect differences in screening efficiency and/or chlorophylls. However, F0 and Fm cannot be explained by chlorophylls because the concentrations were as high or higher in melanic than in usnic species (Appendix A). The low F0 and Fm in the dark Bryoria species are thus consistent with high screening. The pale B. capillaris (Fig.1c),with intermediate F0 and Fm, has higher cortical transmit- tance than the dark Bryoria, whereas A. sarmentosa and U. dasypoga have the weakest cortical screening (Table 1). Low screening in A. sarmentosa is consistent with higher modeled C fixation (Coxson and Coyle 2003) and higher growth rates of usnic compared to melanic species in the shaded lower canopy (Renhorn and Esseen 1995) in our Swedish collection site. Lack of heighteffectsongrowthintransplantedadultA. sarmentosa and B. fuscescens (Stevenson and Coxson 2003) suggests that impacts of photoinhibition on fitness may be a long-term effect or may operate more on juvenile stages.

The significant negative relationship between Fv/Fm R after light treatment and initial F0 (Fig. 3a) supports the use of F0 values as indicators of cortical screening efficiency for pendulous lichens. Removing the outlying eports species U. longissima strengthens the relationship, 2 2 particularly in light (from radj ¼ 0.160; n ¼ 216 to radj ¼ 0.271; n ¼ 192), probably because it is susceptible to FIG. 3. Relationship between maximal quantum yield (Fv/ desiccation (Fig. 2b). We believe that its high suscepti- Fm, expressed as percentage of initial values) after 30 minutes of bility to desiccation as well as to light may contribute to recovery subsequent to hydration, vs. initial F0 values in all measured specimens of the three pendulous lichens with usnic its rareness and decline throughout Europe (Rolstad et acid (open symbols) and the three with melanins (solid symbols) al. 2013) and its restriction to humid coastal forests in that had been exposed to 7 days of (a) light and (b) darkness in North America. Otherwise, our data do not support the the desiccated state. Linear regression was much stronger after treatment in light ( 2 0.160, P , 0.001, n 216) than after hypothesis that desiccation tolerance plays a role for the radj ¼ ¼ dark treatment (r2 ¼ 0.053, P , 0.001, n ¼ 216). vertical stratification between usnic and melanic lichens. adj Melanins and usnic acid are induced and regulated by UV-B (Solhaug et al. 2003, McEvoy et al. 2006), and can melt the snow in tree canopies during winter meaning that these pigments in general occur in higher and thus cause hydration and activation of photosyn- contents in lichens of sun-exposed places as a result of thesis (Coxson and Coyle 2003). Some melanic lichens acclimation to high light (Gauslaa and Solhaug 2001, are susceptible to heating by excess light (Gauslaa and McEvoy et al. 2007). At the same time, there is also a Solhaug 1999). This may explain why some large genetic control of the melanin synthesis, because some melanic lichen genera such as Bryoria (Brodo and Bryoria species are pale, whereas others are dark (Brodo and Hawksworth 1977). Strong contrasts in color occur Hawksworth 1977) and Melanelia (Esslinger 1977) are between B. capillaris and B. fuscescens, even when they restricted to cool-cold climates. grow on the same branch. We treated lichens with light during desiccation, when Despite their similar induction mechanism, melanins repair mechanisms are inactive. Because long-lasting and usnic acid screen light differently. Pigments high light occurs in clear weather, our conclusions may influence temperature, as shown in two hair-like mat- not hold in rain forests. At a Scandinavian scale, there is forming terricolous lichens with contrasting color. The a gradient from continental eastern parts to western reflecting A. ochroleuca (usnic acid) was much less oceanic sites (Gauslaa 2014), along which Usnea moves heated than neighboring melanic Bryocaulon divergens upward in the canopy (Y. Gauslaa, personal observa- (Gauslaa 1984). Darkly melanic lichens absorb visible tions). Even U. longissima enters upper canopies of oaks and near-infrared light efficiently, whereas usnic lichens in western rain forests (see photo in Gauslaa et al. 1992). reflect much of the energy in both wavelength ranges In wet coastal sites, Bryoria species do not always occur (Gauslaa 1984). Thus, dark Bryoria species are heated (Bruteig 1993), presumably because of their susceptibil- 1470 LEONIE FA¨ RBER ET AL. Ecology, Vol. 95, No. 6

ity to excess wetting (Goward 1998). Consistent with Gauslaa, Y. 1984. Heat resistance and energy budget in Scandinavian patterns, Alectoria (Benson and Coxson different Scandinavian plants. Holarctic Ecology 7:1–78. 2002) and Usnea (Antoine and McCune 2004) occurred Gauslaa, Y. 2014. Rain, dew, and humid air as drivers of morphology, function and spatial distribution in epiphytic high up in the canopies of wet forests of northern British lichens. Lichenologist 46:1–16. Columbia and Washington, respectively. Gauslaa, Y., G. Anonby, G. Gaarder, and T. Tønsberg. 1992. In conclusion, melanin in Bryoria is a more efﬁcient Usnea longissima, a rare ancient forest lichen in western sunscreen than usnic acid in Alectoria and Usnea. Our Norway. Blyttia 50:105–114. [In Norwegian with English summary.] experimental evidence provides a new functional mech- Gauslaa, Y., D. S. Coxson, and K. A. Solhaug. 2012. The anism for the vertical gradient of pendulous lichens in paradox of higher light tolerance during desiccation in rare boreal forests, and may explain at least parts of the clear old forest cyanolichens than in more widespread co-occurring change from melanic Bryoria dominating the upper chloro- and cephalolichens. New Phytologist 195:812–822. canopy to light-colored Alectoria/Usnea with usnic acid Gauslaa, Y., M. Lie, and M. Ohlson. 2008. Epiphytic lichen biomass in a boreal Norway spruce forest. Lichenologist 40: in the lower canopy (Fig. 1). The results suggest that the 257–266. low tolerance to high light of Alectoria and Usnea Gauslaa, Y., and K. A. Solhaug. 1996. Differences in the contributes to their absence in the upper canopy. susceptibility to light stress between epiphytic lichens of ancient and young boreal forest stands. Functional Ecology ACKNOWLEDGMENTS 10:344–354. The study was funded by a PROMOS scholarship to L. Gauslaa, Y., and K. A. Solhaug. 1999. High-light damage in Fa¨ rber from Deutscher Akademischer Austauschdienst to air-dry thalli of the old forest lichen Lobaria pulmonaria— travel from Christian-Albrechts-University to the Norwegian interactions of irradiance, exposure duration and high University of Life Sciences, and by Formas (Sweden) through a temperature. Journal of Experimental Botany 50:697–705. grant to P.-A. Esseen (230-2011-1559). We thank Annie Aasen Gauslaa, Y., and K. A. Solhaug. 2001. Fungal melanins as a for measuring chlorophylls and Johan Olofsson for help with sun screen for symbiotic green algae in the lichen Lobaria statistics. pulmonaria. Oecologia 126:462–471. Goward, T. 1998. Observations on the ecology of the lichen LITERATURE CITED genus Bryoria in high elevation conifer forests. Canadian Antoine, M. E., and B. McCune. 2004. Contrasting fundamen- Field Naturalist 112:496–501. tal and realized ecological niches with epiphytic lichen Goward, T. 2003. On the vertical zonation of hair lichens transplants in an old-growth Pseudotsuga forest. Bryologist (Bryoria) in the canopies of high-elevation old-growth conifer 107:163–173. forests. Canadian Field Naturalist 117:39–43. Benson, S., and D. S. Coxson. 2002. Lichen colonization and Green, T. G. A., E. Kilian, and O. L. Lange. 1991. gap structure in wet-temperate rainforests of northern Pseudocypellaria dissimilis: a desiccation-sensitive, highly interior British Columbia. Bryologist 105:673–692. shade-adapted lichen from New Zealand. Oecologia 85: Brodo, I. M., and D. L. Hawksworth. 1977. Alectoria and allied 498–503. eports genera in North America. Opera Botanica 42:1–164. Greenspan, L. 1977. Humidity ﬁxed points of binary saturated Bruteig, I. E. 1993. Large-scale survey of the distribution and aqueous solutions. Journal of Research of the National ecology of common epiphytic lichens on Pinus sylvestris in Bureau of Standards Section A, Physics and Chemistry 81: 89–96.

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SUPPLEMENTAL MATERIAL

Appendix A R Chlorophyll contents in pendulous lichens, including chlorophyll methods (Ecological Archives E095-129-A1).

Appendix B eports

Recovery of maximal quantum yield, Fv/Fm, percentage of initial values, after desiccation treatments (Ecological Archives E095-129-A2).

Appendix C

Chlorophyll ﬂuorescence parameters (Fv/Fm, F0, and Fm) for all species and treatments (Ecological Archives E095-129-A3).