Ecology, 95(6): 1464-1471 Farber, L., Solhaug, K., Esseen, …umu.diva-portal.org/smash/get/diva2:734415/FULLTEXT0… · · 2014-07-17June 2014 PENDULOUS LICHENS IN BOREAL CANOPIES

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Citation for the original published paper (version of record):

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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Ecology, 95(6), 2014, pp. 1464–1471� 2014 by the Ecological Society of America

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

LEONIE FARBER,1 KNUT ASBJØRN SOLHAUG,1 PER-ANDERS ESSEEN,2 WOLFGANG BILGER,3 AND YNGVAR GAUSLAA1,4

1Department of Ecology and Natural Resource Management, Norwegian University of Life Sciences, P.O. Box 5003,NO-1432 As, Norway

2Department of Ecology and Environmental Science, Umea University, SE-90187 Umea, Sweden3Christian-Albrechts-University, Botanical Institute, Olshausenstr. 40, DE-24098 Kiel, Germany

Abstract. Pendulous lichens dominate canopies of boreal forests, with dark Bryoriaspecies in the upper canopy vs. light Alectoria and Usnea species in lower canopy. Thesegenera offer important ecosystem services such as winter forage for reindeer and caribou. Themechanism behind this niche separation is poorly understood. We tested the hypothesis thatspecies-specific sunscreening fungal pigments protect underlying symbiotic algae differentlyagainst high light, and thus shape the vertical canopy gradient of epiphytes. Three pale specieswith the reflecting pigment usnic acid (Alectoria sarmentosa, Usnea dasypoga, U. longissima)and three with dark, absorbing melanins (Bryoria capillaris, B. fremontii, B. fuscescens) werecompared. We subjected the lichens to desiccation stress with and without light, and assessedtheir performance with chlorophyll fluorescence. Desiccation alone only affected U.longissima. By contrast, light in combination with desiccation caused photoinhibitory damagein all species. Usnic lichens were significantly more susceptible to light during desiccation thanmelanic 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 shiftin type and functioning of sunscreening pigments, from high-light-tolerant Bryoria in theupper to susceptible Alectoria and Usnea in the lower canopy.

Key words: Alectoria sarmentosa; boreal forest; Bryoria spp.; desiccation tolerance; epiphytes;melanin; photoinhibition; sunscreening pigments; Totenasen, Norway; Usnea spp.; usnic acid; Vindeln,Sweden.

INTRODUCTION

Pendulous lichens often envelop canopies in boreal

forests (Esseen et al. 1996). Such epiphytic communities

are dominated by the genera Alectoria, Bryoria, and

Usnea, which play important functional roles. They

provide winter forage for reindeer and caribou (Kinley

et al. 2006, Kivinen et al. 2010) and habitat for canopy-

living invertebrates constituting critical fodder for

overwintering passerine birds (Pettersson et al. 1995).

The biomass of pendulous lichens peaks in old forests

(Esseen et al. 1996, Price and Hochachka 2001), and

conversion of old forests to managed stands with short

rotations (,100 years) has dramatically decreased this

epiphytic component (Dettki and Esseen 1998, 2003).

Several species, such as Usnea longissima, are of concern

for conservation (Rolstad et al. 2013), as well as for

ecosystem and wildlife management (Peck and McCune

1997).

Epiphyte communities often show vertical stratifica-

tion (McCune 1993). Pendulous lichens in boreal forests

form a vertical gradient, with Bryoria in the upper

canopy (Fig. 1a) and Alectoria (Fig. 1b) and/or Usnea

on lower, often defoliated branches (Campbell and

Coxson 2001, Benson and Coxson 2002, Coxson and

Coyle 2003). In Norwegian boreal forests, the biomass

of Bryoria increased by a factor of 1.6 from 2–3 m to 5–6

m above the ground, with a concurrent decline (to 61%)

in Alectoria and Usnea (Gauslaa et al. 2008); their sites

are in the same bioclimatic region as our Norwegian site.

The mechanism behind this niche partitioning is poorly

understood, but various factors are apparently involved.

Goward (1998, 2003) hypothesized that lack of Bryoria

in the lower canopy is due to their susceptibility to

prolonged wetting and preference for well-ventilated

upper canopy. Coxson and Coyle (2003) supported this

hypothesis and predicted higher photosynthetic rates for

Alectoria sarmentosa in the lower canopy where it

occurs, but concluded that growth responses alone did

not explain the niche partitioning in pendulous lichens.

Recently, phosphorus availability (McCune and Cald-

well 2009) and exogenous carbohydrates (Campbell et

al. 2013) have been introduced as factors influencing the

realized niches for foliose canopy lichens.

Field evidence suggests that the bright pigment usnic

acid (Alectoria and Usnea) vs. dark melanins (Bryoria)

shape the vertical gradient. Alectoria and Bryoria

Manuscript received 16 December 2013; revised 19 February2014; accepted 26 February 2014. Corresponding Editor: F. C.Meinzer.

4 Corresponding author.E-mail: [email protected]

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containing contrasting pigments are taxonomically more

related to each other than to the genera (Alectoria andUsnea) containing usnic acid (Thell and Moberg 2011).

Both melanins (e.g., Gauslaa and Solhaug 2001) andusnic acid (McEvoy et al. 2007) screen light, and thus

protect underlying photobionts. However, these pig-ments function differently: melanins absorb light,whereas usnic acid reflects excess light (Solhaug and

Gauslaa 2012). We do not know which screeningmechanism is most efficient. Light-screening has not

yet been directly measured in pendulous lichens. If thesepigments play a functional role for vertical epiphyte

distribution, we hypothesize that melanin is the mostefficient screening compound. This needs to be tested,

because lichen compounds may have multiple functions(Molnar and Farkas 2010).

The upper canopy experiences stronger solar radiationand desiccation than low branches (Parker 1997, Coxson

and Coyle 2003). Because light is strongest in clear anddry weather, high light stress is confounded with

desiccation stress. Both high light (Gauslaa and Solhaug1996) and desiccation (Green et al. 1991) can adversely

affect forest lichens. Here, we experimentally separatedthe effects of desiccation from those caused by high light

by exposing six pendulous lichens to four drying regimeswith and without light, using chlorophyll fluorescence toquantify damage and the recovery of the photosynthetic

apparatus. We tested the following hypotheses: (1)lichens with melanins (Bryoria) are more tolerant to

high light than Alectoria and Usnea with usnic acid; and(2) Bryoria species are more tolerant of desiccation than

Alectoria and Usnea.

MATERIAL AND METHODS

Lichen material and study area

Among our species (Fig. 1c), Alectoria sarmentosa

(Ach.) Ach., Usnea dasypoga (Ach.) Nyl., and U.longissima Ach. contained usnic acid, whereas Bryoria

capillaris (Ach.) Brodo and D. Hawksw., B. fuscescens(Gyeln.) Brodo and D. Hawksw., and B. fremontii(Tuck.) Brodo and D. Hawksw. contained melanins.

Lichens were collected August–October 2012 in oldforests from Picea abies branches in the boreal sites

Vindeln (northern Sweden) and Totenasen (southeasternNorway). Sampling was done 2–4 m above ground

because we wanted to study species-specific rather thanenvironmental effects, and the lower canopy is the only

vertical zone where all species may co-occur.Vindeln had 600 mm annual precipitation (;65% as

rain; snow from November–April); mean annual temper-ature was 28C,�118C in January and 148C in July (Raab

and Vedin 1995). Collections were done at 175–200 mabove sea level; B. fuscescens, B. fremontii (6481304700 N,

1984605700 E), and A. sarmentosa (6481402300 N, 1984704600

E) were from mesic, semi-open stands with Picea abies

and Pinus sylvestris. Bryoria capillaris was collected in amesic, open P. sylvestris and P. abies stand (6481305800 N,

19849 03700 E), whereas U. dasypoga (6481401300 N,

1984702900 E) was from a moist-wet, closed-canopy P.

abies stand near a small stream.

In Totenasen (6083501500 N, 1180200400 E; 720 m a.s.l.),

all lichens were collected from the same branches. The

open, old P. abies forest was moist (1000 mm annual

precipitation; 180–190 d/yr had .0.1 mm, and snow

lasting 175–199 d; Moen 1999), located in upper parts of

a steep, northeast-facing slope. Mean annual tempera-

ture was 0–28C, ranging from �88C in January to 148C

in July.

Lichens were stored air-dry at �208C (recommended

by Honegger 2003). Six months later, two samples were

taken from each specimen, resulting in n ¼ 48 samples

per species and site; n ¼ 432 samples in total. Each

sample was selected species-wise for a given desiccation/

light treatment according to random numbers. Separate

thalli were randomly taken for chlorophyll measure-

ments (Appendix A).

Preconditioning of lichens and measurement

of chlorophyll fluorescence parameters

Lichens were sprayed with deionized water and kept

moist at 148C in low light (20 lmol�m�2�s�1) for 24 h to

reduce occasional photoinhibition from the field. Then

they were kept 15 min in darkness before maximal

quantum yield (Fv/Fm) of photosystem II (PSII),

FIG. 1. The vertical canopy gradient with (a) melanicBryoria species in the upper canopy and (b) usnic lichens in thelower canopy (e.g., Alectoria sarmentosa) represents a strikingboreal phenomenon, not only in Scandinavia where this studywas done, but also in inland north-central British Columbia(a, b, upper Slim Creek valley; photo credit: Y. Gauslaa). (c)Sampled lichen species in this study from left to right: Alectoriasarmentosa, Usnea dasypoga, U. longissima, Bryoria capillaris,B. fremontii, B. fuscescens (photo credit: K. A. Solhaug).

June 2014 1465PENDULOUS LICHENS IN BOREAL CANOPIESR

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maximal (Fm), and minimal fluorescence (F0), where

variable fluorescence Fv is the difference between Fm and

F0 (Maxwell and Johnson 2000), were measured by a

portable fluorometer (PAM-2000; Heinz Walz GmbH,

Effeltrich, Germany), with the fiber optics 1 cm away

from the sample using the 608 distance clip (Model

2010A; Heinz Walz GmbH). Each sample was arranged

to fully cover the measuring area and the measuring

light was set at intensity ;0.05 lmol�m�2�s�1; the

saturation pulse had the maximal intensity, and

duration of 0.6 s. The lichens were then air-dried at

228C.

Light and desiccation treatment

The experiment, modified after Gauslaa et al. (2012),

was repeated three times. Two samples of each species3

site combination were included in each replication (n¼ 6

samples per treatment). During treatment, air-dry

lichens lay on a net, 5 mm below the lid of a clear,

sealed plastic box (103 83 4 cm). Each box had 25 mL

of saturated salt solutions or silica gel to obtain 75%,

55%, and 33% relative humidity using NaCl, Mn(NO)3,

and MgCl2, respectively (Greenspan 1977), and 0%

(silica gel).

Eight boxes, two for each humidity, were placed for 7

d at 148C under a high-intensity (400 lmol�m�2�s�1)LED light-diodes panel (SL3500; Photon Systems

Instruments, Brno, Czech Republic). Boxes were rotated

daily to ensure similar light doses for all treatments.

Temperatures of lichens, salt solutions, and air inside

boxes were measured with a thermocouple data logger

(model TC-08; Pico Technology, St Neots, Cambridge-

shire, UK). Lichens reached 228C, salt solutions reached

198C, and air temperature inside the boxes was 228C.

Another set of eight boxes (as previously described) were

kept in darkness for 7 d at 228C to eliminate temperature

differences between light and dark treatments. Thereaf-

ter, lichens were hydrated with deionized water and were

kept moist for 24 h. We measured Fv/Fm, Fm, and F0 as

described for the preconditioning, but the kinetics

during recovery were recorded after 15 minutes of dark

adaptation at 30 min, 2 h, 6 h, and 24 h in low light.

Statistical analyses

We analyzed data from the two sites separately.

General linear models (GLM with Tukey’s HSD post

hoc test) were used to test if initial Fv/Fm, Fm, and F0

varied by species. Fm and F0 were square-root-trans-

formed. We analyzed species performance after the

experiment by expressing Fv/Fm as percentage of initial

Fv/Fm values to remove the initial between-species

variability. We ran a full GLM model with humidity,

light treatment, and species as fixed factors. The

temporal response during the recovery was analyzed in

separate GLMs for 0.5 h and 24 h, because variances

decreased over time following the increase in Fv/Fm.

Heteroscedasticity and non-normality were checked by

examining residuals. No transformation was needed for

Fv/Fm. Analyses were done in IBM SPSS version 21

(IBM 2012).

RESULTS

Initial fluorescence parameters

Initial fluorescence parameters showed similar pat-

terns in Sweden and Norway (Table 1). In Sweden, Fv/

Fm differed by species. The highest Fv/Fm (0.728)

occurred in the darkly melanic B. fremontii and B.

fuscescens. The lowest values (�0.694) were observed in

the pale B. capillaris (Sweden) and the usnic lichens U.

dasypoga and U. longissima (Norway). Maximal (Fm)

and minimal fluorescence (F0) were strongly coupled

across (r2adj ¼ 0.970; n ¼ 432) and within (r2

adj ¼ 0.854–

0.966; P , 0.001; n ¼ 48) all species 3 locality

combinations. The species-specific differences were

much stronger for Fm and F0 than for Fv/Fm (Table 1).

At both sites, Fm was four times higher in A. sarmentosa

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

Fluorescence parameter

Usnic acid

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 n¼48 replicates per species3 site combination. Values for P and adjusted r2 are from GLMs testing effectsof species on fluorescence parameters within each site. Superscripts with different letters within a row denote species that aresignificantly different (at P , 0.05; Tukey post hoc test). Boldface indicates significant at P , 0.05. Ellipses indicate that no datawere available.

LEONIE FARBER ET AL.1466 Ecology, Vol. 95, No. 6R

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and U. dasypoga than in the melanic B. fremontii and B.

fuscescens, with U. longissima and B. capillaris in

between.

Desiccation and light experiment

As a percentage of initial values, Fv/Fm differedstrongly between light and dark treatments and between

species (Fig. 2, Table 2). Desiccation in the absence oflight (7 d), even at 0% relative humidity, had minor

effects on Fv/Fm (Appendix B). In some Bryoria species,

mean Fv/Fm at the end of the dark treatment exceededinitial values after 24 h of recovery at low light

(Appendix C). However, in U. longissima the dark

treatment caused substantially delayed recovery of Fv/Fm (Fig. 2b). After 24 h of hydration, full recovery still

had not taken place (94.1% 6 1.2%; mean 6 1 SE).

Unlike the other species, U. longissima was thussusceptible to desiccation.

Light during desiccation caused significant and lasting

Fv/Fm depression (Fig. 2, Table 2). The light3 humidityinteraction was highly significant for the Swedish

samples, implying that the hardest desiccation aggra-vated the decline of Fv/Fm in light-treated specimens.

Lichens exposed to light recovered more slowly than

those kept dark (Fig. 2). Melanic and usnic speciesdiffered in post hoc tests after 30 minutes of recovery;

confidence intervals did not overlap up to 6 h in any site.

The melanic species were less photoinhibited than thosewith usnic acid. Usnea longissima was more light

susceptible than the other species (Appendix C), withmuch delayed and incomplete recovery subsequent to

hydration, followed by A. sarmentosa and U. dasypoga.

Among usnic lichens, U. dasypoga was fairly similar tothe most susceptible weakly melanic species, B. capil-

laris. The pale B. capillaris showed an initially deeper

depression than the two dark Bryoria spp. (Fig. 2c),although the mean after 24 h of recovery did not differ

much (Appendix C).

The intra- and interspecific variation in fluorescenceparameters is shown in Fig. 3, where Fv/Fm after 30

minutes of recovery was plotted against initial F0 for

samples subjected to light (Fig. 3a) and dark treatment

(Fig. 3b). The light treatment during drying increased

the variation in Fv/Fm in all species apart from U.

longissima, which exhibited strong variation also afterdesiccation in darkness. For lichens treated with light,

there was a stronger decrease of Fv/Fm with increasing

F0 than for those in darkness (Fig. 3). This discrepancywas stronger in a similar plot (not shown) with Fv/Fm

and Fm: for light, r2adj ¼ 0.211, P , 0.001; for darkness,

r2adj ¼ 0.015, P ¼ 0.039 (n¼ 216).

DISCUSSION

Although earlier studies on vertical niche partitioning

in pendulous lichens have focused on growth and

macroclimatic limitations (Goward 1998, 2003, Camp-bell and Coxson 2001, Coxson and Coyle 2003), this

study emphasizes the role of cortical pigments. By

screening excessive light for underlying photobionts,fungal pigments improve lichen functioning in well-lit

habitats (Solhaug and Gauslaa 2012). Foliose usnic

lichens are abundant in sun-exposed habitats at alllatitudes (e.g., Elix 1994, Hauck et al. 2007), whereas

melanic lichens grow in sunny habitats at high latitudesor altitudes (e.g., Brodo and Hawksworth 1977, Es-

slinger 1977, Hauck et al. 2007). Thus, both usnic acid

and melanins may form efficient sunscreens. However,dark Bryoria species were more tolerant to light in the

desiccated state than were similar life-forms with usnic

acid (Fig. 2), consistent with higher screening bymelanins. Recorded photoinhibition in usnic lichens,

evidenced as depressed Fv/Fm, may explain why they are

replaced by melanic species with increasing branchheight. In a northern Sweden site, biomass of dark

Bryoria had a higher canopy openness threshold than

that of A. sarmentosa (P.-A. Esseen, unpublished data),showing that similar replacement processes along

gradients from sun to shade occur on vertical as wellas on horizontal forest scales. Shifts between melanic

and pale lichens in coniferous canopies are probably

driven by height- and/or canopy-openness-dependentvariation in solar radiation, consistent with reported

physical and physiological limitations of pendulous

lichens (Coxson and Coyle 2003).

TABLE 1. Extended.

Melanins

P r2adjBryoria capillaris Bryoria fremontii Bryoria fuscescens

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


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FIG. 2. Recovery of photosynthetic performance (measured as percentage of initial values of maximal quantum yield, Fv/Fm,) inlichens with melanins (solid symbols) and usnic acid (open symbols) as sunscreening pigments after seven days’ treatment (a, b) indarkness and (c, d) in high light (400 lmol�m�2�s�1) 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% confidenceintervals; 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 fromtwo sites (Sweden and Norway), two light treatments, and four humidity treatments measured after 0.5 h and 24 h duringrecovery.

Factor

Sweden Norway

df

0.5 h (r2adj¼ 0.808) 24 h (r2

adj¼ 0.281)

df

0.5 h (r2adj¼ 0.751) 24 h (r2

adj¼ 0.417)

F P F P F P F P

Species, S 4 33.3 ,0.001 3.7 0.007 3 94.1 ,0.001 27.8 ,0.001Light, L 1 824.8 ,0.001 63.2 ,0.001 1 285.1 ,0.001 39.2 ,0.001Humidity, H 3 2.2 0.093 2.9 0.036 3 2.3 0.083 0.8 0.498S 3 L 4 8.0 ,0.001 1.8 0.129 3 5.2 0.002 7.7 ,0.001S 3 H 12 1.5 0.118 0.8 0.674 9 0.6 0.791 0.9 0.522L 3 H 3 6.3 ,0.001 5.2 0.002 3 1.2 0.313 2.5 0.060S 3 L 3 H 12 0.9 0.593 1.1 0.334 9 0.8 0.630 0.4 0.935Total 240 192

Notes: The light treatments were 0 vs. 400 lmol�m�2�s�1; the humidity treatments were 0%, 33%, 55%, and 75% relativehumidity. Recovery was at 20 lmol�m�2�s�1 in the hydrated state. Boldface indicates significance at P , 0.05.


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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, differ-

ences 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

height effects on growth in transplanted adult A.

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

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

species U. longissima strengthens the relationship,

particularly in light (from r2adj ¼ 0.160; n ¼ 216 to r2

adj ¼0.271; n ¼ 192), probably because it is susceptible to

desiccation (Fig. 2b). We believe that its high suscepti-

bility to desiccation as well as to light may contribute to

its rareness and decline throughout Europe (Rolstad et

al. 2013) and its restriction to humid coastal forests in

North America. Otherwise, our data do not support the

hypothesis that desiccation tolerance plays a role for the

vertical stratification between usnic and melanic lichens.

Melanins and usnic acid are induced and regulated by

UV-B (Solhaug et al. 2003, McEvoy et al. 2006),

meaning that these pigments in general occur in higher

contents in lichens of sun-exposed places as a result of

acclimation to high light (Gauslaa and Solhaug 2001,

McEvoy et al. 2007). At the same time, there is also a

genetic control of the melanin synthesis, because some

Bryoria species are pale, whereas others are dark (Brodo

and Hawksworth 1977). Strong contrasts in color occur

between B. capillaris and B. fuscescens, even when they

grow on the same branch.

Despite their similar induction mechanism, melanins

and usnic acid screen light differently. Pigments

influence temperature, as shown in two hair-like mat-

forming terricolous lichens with contrasting color. The

reflecting A. ochroleuca (usnic acid) was much less

heated than neighboring melanic Bryocaulon divergens

(Gauslaa 1984). Darkly melanic lichens absorb visible

and near-infrared light efficiently, whereas usnic lichens

reflect much of the energy in both wavelength ranges

(Gauslaa 1984). Thus, dark Bryoria species are heated

and can melt the snow in tree canopies during winter

and thus cause hydration and activation of photosyn-

thesis (Coxson and Coyle 2003). Some melanic lichens

are susceptible to heating by excess light (Gauslaa and

Solhaug 1999). This may explain why some large

melanic lichen genera such as Bryoria (Brodo and

Hawksworth 1977) and Melanelia (Esslinger 1977) are

restricted to cool-cold climates.

We treated lichens with light during desiccation, when

repair mechanisms are inactive. Because long-lasting

high light occurs in clear weather, our conclusions may

not hold in rain forests. At a Scandinavian scale, there is

a gradient from continental eastern parts to western

oceanic sites (Gauslaa 2014), along which Usnea moves

upward in the canopy (Y. Gauslaa, personal observa-

tions). Even U. longissima enters upper canopies of oaks

in western rain forests (see photo in Gauslaa et al. 1992).

In wet coastal sites, Bryoria species do not always occur

(Bruteig 1993), presumably because of their susceptibil-

FIG. 3. Relationship between maximal quantum yield (Fv/Fm, expressed as percentage of initial values) after 30 minutes ofrecovery subsequent to hydration, vs. initial F0 values in allmeasured specimens of the three pendulous lichens with usnicacid (open symbols) and the three with melanins (solid symbols)that had been exposed to 7 days of (a) light and (b) darkness inthe desiccated state. Linear regression was much stronger aftertreatment in light (r2

adj ¼ 0.160, P , 0.001, n ¼ 216) than afterdark treatment (r2

adj ¼ 0.053, P , 0.001, n ¼ 216).


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ity to excess wetting (Goward 1998). Consistent with

Scandinavian patterns, Alectoria (Benson and Coxson

2002) and Usnea (Antoine and McCune 2004) occurred

high up in the canopies of wet forests of northern British

Columbia and Washington, respectively.

In conclusion, melanin in Bryoria is a more efficient

sunscreen than usnic acid in Alectoria and Usnea. Our

experimental evidence provides a new functional mech-

anism for the vertical gradient of pendulous lichens in

boreal forests, and may explain at least parts of the clear

change from melanic Bryoria dominating the upper

canopy to light-colored Alectoria/Usnea with usnic acid

in the lower canopy (Fig. 1). The results suggest that the

low tolerance to high light of Alectoria and Usnea

contributes to their absence in the upper canopy.

ACKNOWLEDGMENTS

The study was funded by a PROMOS scholarship to L.Farber from Deutscher Akademischer Austauschdienst totravel from Christian-Albrechts-University to the NorwegianUniversity of Life Sciences, and by Formas (Sweden) through agrant to P.-A. Esseen (230-2011-1559). We thank Annie Aasenfor measuring chlorophylls and Johan Olofsson for help withstatistics.

LITERATURE CITED

Antoine, M. E., and B. McCune. 2004. Contrasting fundamen-tal and realized ecological niches with epiphytic lichentransplants in an old-growth Pseudotsuga forest. Bryologist107:163–173.

Benson, S., and D. S. Coxson. 2002. Lichen colonization andgap structure in wet-temperate rainforests of northerninterior British Columbia. Bryologist 105:673–692.

Brodo, I. M., and D. L. Hawksworth. 1977. Alectoria and alliedgenera in North America. Opera Botanica 42:1–164.

Bruteig, I. E. 1993. Large-scale survey of the distribution andecology of common epiphytic lichens on Pinus sylvestris inNorway. Annales Botanici Fennici 30:161–179.

Campbell, J., P. Bengtson, A. L. Fredeen, D. S. Coxson, andC. E. Prescott. 2013. Does exogenous carbon extend therealized niche of canopy lichens? Evidence from sub-borealforests in British Columbia. Ecology 94:1186–1195.

Campbell, J., and D. S. Coxson. 2001. Canopy microclimateand arboreal lichen loading in subalpine spruce–fir forest.Canadian Journal of Botany 79:537–555.

Coxson, D. S., and M. Coyle. 2003. Niche partitioning andphotosynthetic response of alectorioid lichens from subalpinespruce–fir forest in north-central British Columbia, Canada:the role of canopy microclimate gradients. Lichenologist 35:157–175.

Dettki, H., and P.-A. Esseen. 1998. Epiphytic macrolichens inmanaged and natural forest landscapes: a comparison at twospatial scales. Ecography 21:613–624.

Dettki, H., and P.-A. Esseen. 2003. Modelling long-term effectsof forest management on epiphytic lichens in northernSweden. Forest Ecology and Management 175:223–238.

Elix, J. A. 1994. Xanthoparmelia. Pages 201–308 in C.Grgurinovic, editor. Flora of Australia. Volume 55. Austra-lian Biological Resources Study, Department of Environ-ment and Heritage, Canberra, ACT, Australia.

Esseen, P.-A., K. E. Renhorn, and R. B. Pettersson. 1996.Epiphytic lichen biomass in managed and old-growth borealforests: effect of branch quality. Ecological Applications 6:228–238.

Esslinger, T. L. 1977. A chemosystematic revision of the brownParmeliae. Journal of the Hattori Botanical Laboratory 42:1–211.

Gauslaa, Y. 1984. Heat resistance and energy budget indifferent Scandinavian plants. Holarctic Ecology 7:1–78.

Gauslaa, Y. 2014. Rain, dew, and humid air as drivers ofmorphology, function and spatial distribution in epiphyticlichens. Lichenologist 46:1–16.

Gauslaa, Y., G. Anonby, G. Gaarder, and T. Tønsberg. 1992.Usnea longissima, a rare ancient forest lichen in westernNorway. Blyttia 50:105–114. [In Norwegian with Englishsummary.]

Gauslaa, Y., D. S. Coxson, and K. A. Solhaug. 2012. Theparadox of higher light tolerance during desiccation in rareold forest cyanolichens than in more widespread co-occurringchloro- and cephalolichens. New Phytologist 195:812–822.

Gauslaa, Y., M. Lie, and M. Ohlson. 2008. Epiphytic lichenbiomass in a boreal Norway spruce forest. Lichenologist 40:257–266.

Gauslaa, Y., and K. A. Solhaug. 1996. Differences in thesusceptibility to light stress between epiphytic lichens ofancient and young boreal forest stands. Functional Ecology10:344–354.

Gauslaa, Y., and K. A. Solhaug. 1999. High-light damage inair-dry thalli of the old forest lichen Lobaria pulmonaria—interactions of irradiance, exposure duration and hightemperature. Journal of Experimental Botany 50:697–705.

Gauslaa, Y., and K. A. Solhaug. 2001. Fungal melanins as asun screen for symbiotic green algae in the lichen Lobariapulmonaria. Oecologia 126:462–471.

Goward, T. 1998. Observations on the ecology of the lichengenus Bryoria in high elevation conifer forests. CanadianField Naturalist 112:496–501.

Goward, T. 2003. On the vertical zonation of hair lichens(Bryoria) in the canopies of high-elevation old-growth coniferforests. Canadian Field Naturalist 117:39–43.

Green, T. G. A., E. Kilian, and O. L. Lange. 1991.Pseudocypellaria dissimilis: a desiccation-sensitive, highlyshade-adapted lichen from New Zealand. Oecologia 85:498–503.

Greenspan, L. 1977. Humidity fixed points of binary saturatedaqueous solutions. Journal of Research of the NationalBureau of Standards Section A, Physics and Chemistry 81:89–96.

Hauck, M., C. Dulamsuren, and M. Muhlenberg. 2007. Lichendiversity on steppe slopes in the northern Mongolianmountain taiga and its dependence on microclimate. Flora202:530–546.

Honegger, R. 2003. The impact of different long-term storageconditions on the viability of lichen-forming ascomycetes andtheir green algal photobiont, Trebouxia spp. Plant Biology 5:324–330.

IBM. 2012. IBM SPSS version 21. IBM Software Group,Chicago, Illinois, USA.

Kinley, T. A., T. Goward, B. N. McLellan, and R. Serrouya.2006. The influence of variable snowpacks on habitat use bymountain caribou. Rangifer Special Issue 17:93–102.

Kivinen, S., J. Moen, A. Berg, and A. Eriksson. 2010. Effects ofmodern forest management on winter grazing resources forreindeer in Sweden. Ambio 39:269–278.

Maxwell, K., and G. N. Johnson. 2000. Chlorophyll fluores-cence—a practical guide. Journal of Experimental Botany 51:659–668.

McCune, B. 1993. Gradients in epiphyte biomass in threePseudotsuga–Tsuga forests of different ages in westernOregon and Washington. Bryologist 96:405–411.

McCune, B., and B. A. Caldwell. 2009. A single phosphorustreatment doubles growth of cyanobacterial lichen trans-plants. Ecology 90:567–570.

McEvoy, M., L. Nybakken, K. A. Solhaug, and Y. Gauslaa.2006. UV triggers the synthesis of the widely distributedsecondary compound usnic acid. Mycological Progress 5:221–229.


epor

ts

McEvoy, M., K. A. Solhaug, and Y. Gauslaa. 2007. Solarradiation screening in usnic acid-containing cortices of thelichen Nephroma arcticum. Symbiosis 43:143–150.

Moen, A. 1999. National Atlas of Norway: Vegetation.Norwegian Mapping Authority, Hønefoss, Norway.

Molnar, K., and E. Farkas. 2010. Current results on biologicalactivities of lichen secondary metabolites: a review. Zeit-schrift fur Naturforschung C 65:157–173.

Parker, G. G. 1997. Canopy structure and light environment ofan old-growth Douglas-fir western hemlock forest. North-west Science 71:261–270.

Peck, J. L. E., and B. McCune. 1997. Remnant trees andcanopy lichen communities in western Oregon: a retrospec-tive approach. Ecological Applications 7:1181–1187.

Pettersson, R. B., J. P. Ball, K. E. Renhorn, P.-A. Esseen, andK. Sjoberg. 1995. Invertebrate communities in boreal forestcanopies as influenced by forestry and lichens with implica-tions for passerine birds. Biological Conservation 74:57–63.

Price, K., and G. Hochachka. 2001. Epiphytic lichen abun-dance: effects of stand age and composition in coastal BritishColumbia. Ecological Applications 11:904–913.

Raab, B., and H. Vedin. 1995. Climate, lakes and rivers.National Atlas of Sweden 14:1–176. SNA Publishing, Stock-holm, Sweden.

Renhorn, K.-E., and P.-A. Esseen. 1995. Biomass growth in fivealectorioid lichen epiphytes. Mitteilungen Eidgenossische

Forschungsanstalt fur Wald, Schnee und Landschaft 70:133–140.

Rolstad, J., S. Ekman, H. L. Andersen, and E. Rolstad. 2013.Genetic variation and reproductive mode in two epiphytic

lichens of conservation concern: a transatlantic study of

Evernia divaricata and Usnea longissima. Botany 91:69–81.

Solhaug, K. A., and Y. Gauslaa. 2012. Secondary lichen

compounds as protection against excess solar radiation andherbivores. Progress in Botany 73:283–304.

Solhaug, K. A., Y. Gauslaa, L. Nybakken, and W. Bilger. 2003.UV-induction of sun-screening pigments in lichens. New

Phytologist 158:91–100.

Stevenson, S. K., and D. S. Coxson. 2003. Litterfall, growth,

and turnover of arboreal lichens after partial cutting in anEngelmann spruce–subalpine fir forest in north-central

British Columbia. Canadian Journal of Forestry Research

33:2306–2320.

Thell, A., and R. Moberg. 2011. Nordic Lichen Flora Volume

4. Parmeliaceae. Museum of Evolution, Uppsala University,Uppsala, Sweden.

SUPPLEMENTAL MATERIAL

Appendix A

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

Appendix B

Recovery of maximal quantum yield, Fv/Fm, percentage of initial values, after desiccation treatments (Ecological ArchivesE095-129-A2).

Appendix C

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


eports

http://www.esapubs.org/archive/ecol/E095/129/




Ecology, 95(6): 1464-1471 Farber, L., Solhaug, K., Esseen, …umu.diva-portal.org/smash/get/diva2:734415/FULLTEXT0… · · 2014-07-17June 2014 PENDULOUS LICHENS IN BOREAL CANOPIES

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