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Size is a main driver for hydration traits in cyano-and cephalolichens of boreal rainforest canopies

Sonia MERINEROa,c, Olga HILMOb, Yngvar GAUSLAAa,*aDepartment of Ecology and Natural Resource Management, Norwegian University of Life Sciences, P.O. Box 5003,

NO-1432 �As, NorwaybNorwegian University of Science and Technology, Faculty of Natural Science and Technology, Department

of Biology, NO-7491 Trondheim, NorwaycUniversidad Rey Juan Carlos, Departamento de Biolog�ıa y Geolog�ıa, �Area de Biodiversidad y Conservaci�on,

C/ Tulip�an s/n, E-28933 Madrid, Spain

a r t i c l e i n f o

Article history:

Received 27 June 2013

Revision received 4 November 2013

Accepted 19 December 2013

Available online 18 January 2014

Corresponding editor:

Peter D Crittenden

Keywords:

Allometry

Canopy gradient

Epiphytes

Lichens

Lobaria pulmonaria

Lobaria scrobiculata

Pseudocyphellaria crocata

Photobiont

Specific thallus mass

Water holding capacity

* Corresponding author.E-mail address: yngvar.gauslaa@nmbu.no

1754-5048/$ e see front matter ª 2013 Elsevhttp://dx.doi.org/10.1016/j.funeco.2013.12.001

a b s t r a c t

We measured the water holding capacity per area (WHCA; mg H2O cm�2), and thus the

saturating rainfall (mm), for sympatric cyano- (Lobaria scrobiculata and Pseudocyphellaria

crocata) and cephalolichens (Lobaria pulmonaria) along canopy height gradients in boreal

rainforests, to quantify the importance of specimen size, photobiont type and branch

height as WHCA drivers. Size increased WHCA by a factor of four. Cyanolichens had z1.5

times higher WHCA than cephalolichens. Finally, branch height significantly increased

WHCA for the Lobaria species. Reported responses are consistent with higher optimal

rainfall requirements for reproducing versus juvenile specimens, and for cyanolichens

versus those with green algal photobionts. Increased WHCA with height in the canopy is

consistent with acclimation to stronger evaporative demands. The results highlight the

link between rainfall patterns and maximal sizes realized for a given lichen species and

habitat, and extend our understanding of why the cyanolichen/green algal lichen-ratio

increases in forests with increasing rainfall.

ª 2013 Elsevier Ltd and The British Mycological Society. All rights reserved.

Introduction green algae as the only or major photobiont, respectively (e.g.

Poikilohydric organisms like lichens depend on hydration

events to resume metabolic processes and grow (e.g.

Palmqvist & Sundberg, 2000). While humid air alone can

activate photosynthesis in chloro- and cephalolichens with

(Y. Gauslaa).ier Ltd and The British M

Jonsson Cabrajic et al., 2010; Lid�en et al., 2010), cyanolichens

entirely depend on liquidwater for positive carbon gain (Lange

et al., 1986). These two hydration traits associate with mor-

phological adaptation and/or acclimation: Many lichens,

chlorolichens in particular, are thin and rapidly resume

ycological Society. All rights reserved.

60 S. Merinero et al.

photosynthesis in humid air, whereas thick lichens need a

longer time (Larson & Kershaw, 1976; Larson, 1981; Lange &

Kilian, 1985), or remain inactive (cyanolichens). To compen-

sate for the longer time needed to fill thewater storage of thick

lichens with water from humid air, thick lichens retain water

for longer periods after hydration events. Water holding

capacity (WHCA; expressed as mass of water at saturation per

thallus area) is an often ignored, but important, lichen trait

that equates to mm rainfall needed for saturation. It deter-

mines the duration of hydration periods and influences the

ecological niche (as reviewed by Gauslaa, 2014). Specific thal-

lus mass (STM; dry mass per thallus area) drives the WHCA at

intra- and interspecific levels (Gauslaa & Coxson, 2011). STM is

the inverse equivalent of the frequently used parameter spe-

cific leaf area, SLA, in plant science, connected to the resource

use economy (e.g. Reich et al., 1998; Wright et al., 2004). In

adult lichen life stages, STM increases with size (Dahlman

et al., 2002; Gauslaa et al., 2009; MacDonald & Coxson, 2013).

However, the size-dependency ofWHCA from early juvenile to

late reproductive stages is not known. Because small juvenile

thalli are likely particularly influenced by their ability to retain

moisture, they may represent a more critical stage in the

lichen life cycle than buffered mature thalli (Gauslaa &

Solhaug, 1998).

Epiphytic lichens representing a threatened biodiversity

component show strong vertical gradients in tree canopies

(McCune, 1993; McCune et al., 1997; Gauslaa, 1997; Coxson &

Coyle, 2003; Gauslaa et al., 2008; Rambo, 2010; Marmor et al.,

2013). However, regulating factors for such gradients are

insufficiently known. We will search for vertical gradients in

STM and WHCA for the cephalolichen Lobaria pulmonaria and

for the cyanolichens Pseudocyphellaria crocata and Lobaria

scrobiculata in boreal Picea abies-dominated rainforests in

Norway recognized as hot spot areas for epiphyte diversity

(Holien & Tønsberg, 1996; Rolstad et al., 2001). The canopy

height gradient is complex because spruce drains the water

away from the inner and lower canopy (see Stoutjesdijk &

Barkman, 1987; Goward, 2003). Availability of liquid water

may thus decline with increasing distance from tree tops,

whereas air humidity tends to be highest in sheltered lower

canopy, at least during the day (Geiger, 1950). Wind and light

often increase with height, leading to increasing evaporative

demands. In such canopy gradients, WHCA of cyanolichens

Table 1 e Summary statistics of habitat characteristics in the s

Parameter Lobaria pulmonaria

No of thalli 223

No of trees 7

No of branches 8

Height range, m 2e9

Mean height of thalli, m 4.8 � 0.1

Height of trees, m 29.1 � 0.2

Tree circumference, cm 118 � 1

Tree age, yr 129 � 2

Branch length, cm 301 � 2

Branch circumference, cm 12.3 � 0.2

Mean values � SE are given.

that depends on liquidwatermay respond differently than the

WHCA of lichens with green algae capable also of using humid

air.

By focusing on STM and WHCA, we add information to a

recent trend in quantifying lichen traits (e.g. Asplund &

Wardle, 2013; Lang et al. 2009). We will quantify these two

traits across size classes for each of three sympatric study

species sampled on branches from different height levels in

Picea abies-dominated old rainforests. Our aim is to test the

following hypotheses: (1) Thallus size drives WHCA in a sim-

ilar way across size classes e consistent with the view that

reproduction per se does not have major effects on hydration

requirements. (2) WHCA is shaped by STM in species-specific

ways e consistent with species-specific water storage traits;

and/or (3) The photobiont influences the size-dependency of

WHCA in lichens e consistent with a trade-off between rapid

and frequent uptake of humidity in thin green algal lichens

versus more water conserving strategies in cyanolichens that

depend on liquid water. (4) WHCA increases with height in the

canopy e consistent with acclimation tuning these traits to

ambient hydration sources. Finally, we discuss howmeasured

traits influence the ecology of our species.

Material and methods

Site

We studied lichens on Picea abies in old ravine forests in Foss,

Nord-Trøndelag, Norway (64�47’80000N, 12�00’07900E, 50e100 m

a.s.l.). The stand age, estimated from cores of 27 trees, was 120

yr (Table 1). The site, classified as boreal rainforest (DellaSala

et al., 2011), is located in the markedly oceanic section of the

southern boreal vegetation zone with 240 rainy days a year

(Moen, 1999). Mean annual precipitation is 1 375 mm, varying

from 59 mm (May) to 154 mm (Oct.). Rainfall was frequent;

128 d of 214 d in total were rainy for Mar.eSep. averaged for

2010e2012, but gentle (52 d � 1 mm; 106 d � 10 mm d�1).

Rainfall data were obtained from the Norwegian Meteoro-

logical Institute, eklima.met.no., Overhalla.

We randomly collected 37 entire intact branches from 23

trees, as a subset of a larger lichen population study (Hilmo

et al., 2013). Trees had to be alive, >50 cm in circumference

ampling site

Lobaria scrobiculata Pseudocyphellaria crocata

567 388

23 11

36 14

2e14 2e10

7.1 � 0.2 3.4 � 0.1

26.2 � 0.1 26.8 � 0.1

104 � 1 106 � 1

106 � 1 89 � 1

285 � 3 311 � 2

9.3 � 0.1 9.2 � 0.1

Specific thallus mass, mg DM cm-2

02987654 10

Wat

er h

oldi

ng c

apac

ity, m

g H

2O c

m-2

5

6

7

89

20

30

40

10

Lobaria pulmonaria

Lobaria pulmonaria

Lobaria scrobiculata

Lobaria scrobiculata

Pseudocyphellaria crocata

Pseudocyphellaria crocata

Fig 1 e The relationship between specific thallus mass

(STM) and water holding capacity (WHCA) in Lobaria

pulmonaria, L. scrobiculata and Pseudocyphellaria crocata

sampled on branches of Picea abies in boreal rainforests.

Regression equations: Lobaria scrobiculata:

log(WHCA) [ 0.312 D 0.956 log(STM); r2adj [ 0.878;

p < 0.001. Lobaria pulmonaria: log(WHCA) [ 0.192 D 0.105

log(STM); r2adj [ 0.842; p< 0.001. Pseudocyphellaria crocata:

log(WHCA) [ 0.248 D 0.993 log(STM); r2adj [ 0.852;

p < 0.001.

Size drives hydration traits in canopy lichens 61

at breast height, and the tree top should not be broken. We

established a canopy height gradient from 2 to 14 m above the

ground, comprising >2 branches per m height level (tree and

branch variables; see Table 1). Sampled branches were dried

at room temperature and stored 13 months at �20 �C before

sampling of lichens.

Lichen material

Studied lichens were L. pulmonaria with green algal primary

photobiont with Nostoc in internal cephalodia, versus L. scro-

biculata and P. crocatawith Nostoc only. Lobaria scrobiculatawas

the most abundant species, followed by P. crocata, and then L.

pulmonaria (Hilmo et al., 2013). We randomly gathered a

numerically representative sample of healthy and intact thalli

of each species, including the smallest and largest on every

branch to widen the size distribution (Table 1; 1 178 thalli in

total). Each thallus was stored after debris had been removed.

Functional traits

Lichens were hydrated by repeated sprayings with deionized

water until full saturation. Photographs were taken of fully

hydrated thalli placed on awhite light transilluminator (Model

TW-43 White light, UVP, Upland, CA 91786 USA) and flattened

below a piece of glass (Nikon D300 camera; Nikon AF-S Micro

Nikkor 105 mm lens). Area (A) was recorded by analyzing

photographs in ImageJ 1,46f version (Wayne Rasband,

National Institutes of Health, USA). Shortly after taking the

photographs, thalli were again fully moistened, and then

gently blottedwith filter paper to remove excess surfacewater

before wet mass (WM) was measured. After 2 hr of air-drying

at room temperature, thalli were oven-dried for 24 hr at 70 �Cand reweighed to obtain dry mass (DM). Mass was measured

to the nearest 10 mg, or 0.1 mg, depending on thallus size.

Based on A and DM values, specific thallus mass (STM), was

calculated as STM ¼ DM/A. The water holding capacity

(WHCA) was calculated as WHCA ¼ (WM�DM)/A. The percent

water at saturation was calculated as % water ¼ [(WM�DM)

*100]/DM. Lichen mass per area at full hydration is thus

STM þ WHCA.

Statistical analyses

Distributions of studied variables were not normal. Therefore,

KruskaleWallis and Dunn’s methods were used to test dif-

ferences among species. For simple and multiple regressions,

all variables were log-transformed to improve normality and

linearity. Multiple regressions were done in SigmaPlot 11.0

Table 2 e Mean values ± SE for thallus size (minimum e maxicapacity (WHCA) and percentage water at saturation for sampl

n Size (mm2) STM (mg

Lobaria pulmonaria 223 853 � 140a (3.2e12 450) 8.6 �Lobaria scrobiculata 567 468 � 49a (2.3e16 630) 9.7 �Pseudocyphellaria crocata 388 242 � 20a (2.4e3 126) 7.3 �

Among species, means sharing the same letter are not statistically differen

(Systat Software Inc., San Jose, CA); other analyses were done

inMinitab 16 (Minitab Inc., State College, PA).We analyzed the

effect of canopy height onWHCA by using best subsetmultiple

regression analyses for each species separately. In order not to

use strongly correlated independent variables, we used the

mass of water (WMeDM) at saturation (dependent variable)

instead of WHCA, and the independent variables used were

thallus area and branch height. However, for comparison, we

also ran the best subset regressionmodels for species-specific

WHCA by adding STM.

Results

STM was a main driver of WHCA in each of the three species

(Fig 1; r2adj ¼ 0.842�0.878). The more biomass the lichen

invested per thallus area, the higher was its WHCA,

mum is given), specific thallus mass (STM), water holdinged thalli of studied species

DM cm�2) WHCA (mg H2O cm�2) % Water at saturation

0.2b 12.7 � 0.3a 146 � 1a

0.1c 18.0 � 0.2b 187 � 1c

0.1a 12.8 � 0.2a 176 � 1b

t from each other (all pairwisemultiple procedures: Dunn’s; p< 0.05).

62 S. Merinero et al.

particularly in cyanolichens. Across the entire STM range, L.

pulmonaria had the lowest and L. scrobiculata the highest

WHCA. L. scrobiculata had a WHCA/STM-ratio of 1.86 versus

1.75 in P. crocata, and 1.48 in L. pulmonaria as computed from

overall means (Table 2).

STM as well as WHCA highly significantly increased with

thallus size in all species (Fig 2). P. crocata had the lowest STM

(7.3 � 0.1 mg DM cm�2), followed by L. pulmonaria

(8.6� 0.2mgDMcm�2) and L. scrobiculata (9.7� 0.1mgDMcm�2;

Table 2). The WHCA in P. crocata (12.8 � 0.2 mg H2O cm�2)

matched the WHCA in L. pulmonaria (12.7 � 0.3 mg H2O cm�2)

despite itssignificantly lowerSTM.Thesetwospecieshad lower

WHCA than L. scrobiculata (18.0� 0.2mg H2O cm�2; Fig 2D). The

slope of all regression lines (Fig 2AeC) were similar in the

logelog plot, summarized in Fig 2D, implying that the increase

in WHCA with size in plots with linear scales would have been

significantly steeper in the two cyanolichens than in the

cephalolichen. The two cyanolichens had significantly higher

percentwater at saturation than the cephalolichen, andamong

the cyanolichens, L. scrobiculata containedmostwater (Table 2).

WHCA directly translates to the minimum mm rainfall

needed to saturate a lichen specimen with water

(10 mg H2O cm�2 ¼ 0.1 mm rain). The minimum rainfall nee-

ded for full photosynthetic activation depended on size, but

Thallus

1 10 100 1000 10000

STM

, mg

DM

cm

-2 a

nd W

HC

, mg

H2O

cm

-2

3

456789

15

20

30

4050

10

Lobaria scrobiculata

456789

20

30

4050

10

Lobaria pulmonaria

A

B

Fig 2 e The thallus size (area) dependency of specific thallus ma

scrobiculata, (B) L. pulmonaria and (C) Pseudocyphellaria crocata s

Regression lines for all species (see AeC) with corresponding 95

scrobiculata: log(WHCA) [ 0.954 D 0.138 log(area); r2adj [ 0.693; p

p < 0.001. L. pulmonaria: log(WHCA) [ 0.759 D 0.153 log(area); r

r2adj [ 0.763; p < 0.001. P. crocata: log(WHCA) [ 0.75 D 0.167 l

log(area); r2adj [ 0.583; p < 0.001. Closed symbols: STM; open

was in the range of 0.05e0.4 mm for studied thalli (Fig 3).

Relatively large (100 cm2) thalli needed 3.6 times (L. scrobicu-

lata) to 4.7 times (P. crocata) higher rainfall for activation than

small ones (1 mm2). At all the low intensity rainfall levels

shown in Fig 3, approximately 10 times larger thalli were fully

hydrated for L. pulmonaria than for L. scrobiculata. For example,

0.2 mm rain only saturates L. scrobiculata up to a size of

3.3 cm2, but fully hydrates 10 times larger L. pulmonaria

(35 cm2) and six times larger P. crocata (20 cm2; see Fig 3).

The species distribution along the height gradient differed

between the species (Table 1). L. pulmonaria (2e10 m) and P.

crocata (2e9 m) grew in a narrower canopy height range

(<10 m) than L. scrobiculata, (2e14 m; Table 1). In the best

subset multiple regression analysis (Table 3), increasing can-

opy height was highly significantly associated with larger

water storage for both Lobaria species. However, in P. crocata

with most thalli found on the lower branches, water storage

slightly, but significantly ( p ¼ 0.026) decreased with increas-

ing canopy height. Adding STM to the species-specific model

given in Table 3 (data not shown), branch height became

slightly more significant; size and STM both gave highly sig-

nificantly positive contributions to the WHCA. These models

should be treated with some caution due to intercorrelation

between size and STM (VIF ¼ 2.4e4.4).

area, mm2

Pseudocyphellaria crocata

1 10 100 1000 10000

WHC L.pulm

WHC L. scob

WHC P. croc

STM L. pulm

STM L. scrob

STM P. croc

C

D

ss (STM) and water holding capacity (WHCA) in (A) Lobaria

ampled on branches of Picea abies in boreal rainforests. (D)

% confidence intervals are given. Regression equations: L.

< 0.001, log(STM) [ 0.688 D 0.136 log(area); r2adj [ 0.701;2adj [ 0.769; p < 0.001, log(STM) [ 0.643 D 0.131 log(area);

og(area); r2adj [ 0.630; p < 0.001, log(STM) [ 0.543 D 0.15

symbols: WHCA.

0.0 0.1 0.2 0.3 0.4 0.5

# ra

iny

days

(<0.

6 m

m d

ay-1

) Mar

ch -

Sept

embe

r

0

5

10

15

20

Low rainfall intensities, mm day-1

Max

imum

thal

lus

area

(cm

2 ) rea

chin

g sa

tura

tion

10

10

10

10

10

10

10

10

10Lobaria pulmonaria

Lobaria scrobiculata

Pseudocyphellaria crocata

Rainfall intensity, mm dayAc

cum

ulat

ed %

Rainy days (128 days)Total rain (771 mm)

Fig 3 e The frequency (left y-axis) of low rainfall events

(<0.6 mm dL1) given as vertical bars, during Mar.eSep.

(averaged across 2010e2012). The maximum thallus sizes

(right y-axis) of Lobaria pulmonaria (open circles), L.

scrobiculata (filled triangles), and Pseudocyphellaria crocata

(open triangles) that can become fully hydrated at these

rainfall events, based on regressions in Fig 2. The inset

shows the accumulated percentage of number of rainy

days (filled circles) as well as accumulated total rainfall

(open circles) given in 1 mm rainfall increments (x-axis)

during Mar.eSep.. Rainfall data are from the Norwegian

Meteorological Institute, eklima.met.no, Overhalla.

Size drives hydration traits in canopy lichens 63

Percent water at saturation did not significantly relate to

size (data not shown). There were weak, but highly significant

positive regressions between percent water at saturation and

WHCA ( p < 0.001) for all three species. WHCA accounted for a

very minor part of the variation in percent water at saturation

for the two cyanolichens (r2adj ¼ 0.033 for L. scrobiculata and

r2adj ¼ 0.096 for P. crocata). For the cephalolichen, the rela-

tionship was somewhat stronger (r2adj ¼ 0.286). WHCA and

percent water at saturation were not strongly coupled

parameters (Table 2).

Table 3 e Best subset multiple regression models for the massscrobiculata and Pseudocyphellaria crocata sampled on branches

Variable Coef. � std. error

Lobaria pulmonaria (r2adj ¼ 0.995; p < 0.001; n ¼ 223)

Constant 0.998 � 0.0197

Log(thallus size) 1.156 � 0.0056

Log(branch height) 0.104 � 0.0293

Lobaria scrobiculata (r2adj ¼ 0.986; p < 0.001; n ¼ 567)

Constant 1.260 � 0.0096

Log(thallus size) 1.031 � 0.0053

Log(branch height) 0.0536 � 0.0120

Pseudocyphellaria crocata (r2adj ¼ 0.988; p < 0.001; n ¼ 388)

Constant 1.100 � 0.0081

Log(thallus size) 1.168 � 0.0065

Log(branch height) �0.035 � 0.0016

VIF: Variation Inflation Factor.

Discussion

Size dependency

Large lichen specimens storemorewater per thallus area than

small ones (Gauslaa & Solhaug, 1998; Fos et al., 1999). Never-

theless, our study is the first to show that WHCA, and thus the

mm rain needed to fill the lichen water storage, also increase

with size at similar rates throughout all life stage classes from

juvenile to old ages (Fig 2).Within themain growing season for

lichens in our study area (Larsson&Gauslaa, 2011), asmany as

2/3 of the 128 rainy days had �0.6 mm rain (Fig 3; inset). The

other source of liquid water, dewfall, is often <0.2 mm

(Richards, 2002; Jacobs et al., 2002, 2006; Hao et al., 2012), but

may occasionally extend to 0.3e0.5 mm (Garratt & Segal, 1988;

Xiao et al., 2013). Because the variation inWHCA in our species

equates to a range of 0.04e0.40 mm rain corresponding to

common rainfall intensities in the study area (see Fig 2), many

low rainfall events influence hydration and growth in a

strongly size-dependent way.

Small thalli with green algae are opportunistic as they do

not depend only onmajor rainfalls, which is also the situation

for thin lichen thalli (Larson & Kershaw, 1976; Larson, 1981;

Lange & Kilian, 1985). For example, the thin Lecanora muralis

depends more on dew than on rain for its annual carbon gain

(Lange, 2002, 2003b, a). With increasing size, lichens should

become more dependent on lasting rain, and benefit more

from canopy drainage water flushing the lichens, particularly

because overlying branches trap the first rain in a tree canopy.

Drainagewater probably allows the lichenswe studied to form

much larger thalli on trunks of deciduous trees than on spruce

branches. Growth rate (Armstrong & Bradwell, 2011) and

mature size (Jackson et al., 2006) of a given lichen species vary

substantially between its habitats. Variation in water avail-

ability likely influences habitat-specific mature sizes of a

given lichen species.

Size influences lichen growth, survival and reproduction

(Armstrong & Bradwell, 2011; Larsson & Gauslaa, 2011; Hilmo

et al., 2013). As large specimens stay moist and active for

longer periods than small ones, they should grow faster or

of water, log(WM L DM), in Lobaria pulmonaria, L.of Picea abies in boreal rainforests

t P VIF

50.68 <0.001 0.000

208.21 <0.001 1.023

3.54 <0.001 1.023

130.92 <0.001 0.000

194.93 <0.001 1.033

4.468 <0.001 1.033

136.65 <0.001 0.000

180.10 <0.001 1.003

�2.23 0.026 1.003

64 S. Merinero et al.

reproduce more. Significant increases in chlorophyll content

per thallus area with increasing size in L. pulmonaria (Asplund

& Gauslaa, 2007) may also imply higher growth potential with

increasing size. However, large and/or thick thalli require

more water, and their high biomass per area necessarily

implies higher maintenance costs than for small ones, as is

the case for leaves of most plants (e.g. Milla & Reich, 2007).

Investments in carbon-based secondary compounds increase

with size (Asplund & Gauslaa, 2007). Also reproductive effort

increases with size, and reproduction reduces growth rates

(Gauslaa, 2006). In general, growth rates declinewith size even

in juvenile stages (Larsson & Gauslaa, 2011), and likely reflect

more rapidly increasing costs than benefits. Also in plants,

growth is reduced with increasing specific leaf mass, or with

decreasing specific leaf area using plant biology terms (e.g.

Poorter & Remkes, 1990). Thereby, increasing size, and thus

higher WHCA and chlorophyll contents, may just be the way

growing lichens maintain the status quo.

Species-specific differences

In addition to strong size-dependencies of STM and WHCA,

there were significant differences between sympatric lichen

species (Fig 2). L. scrobiculata needs much higher hydration

levels to become photosynthetically active than the thinner

L. pulmonaria with rapid water uptake/loss (MacKenzie &

Campbell, 2001), but the former species has longer periods

of carbon fixation (M�aguas et al., 1997). Across a range of

adult heteromerous lichen species (Gauslaa & Coxson, 2011),

WHCA in cyanolichens was approximately two times higher

than the STM (close to our values for L. scrobiculata and P.

crocata; Table 2); in cephalolichens WHCAs were 1.5 times

higher than STMs (as in our L. pulmonaria; Table 2); in chlor-

olichens (not studied by us), WHCAs equal the STMs. Thus,

photobionts shape STM-WHCA relationships. Also in a wider

range of species, it was shown that cyanolichens store sig-

nificantly more water than cephalolichens (Beckett, 1995).

Cyanobacteria as such store much more water than green

algae (Gauslaa et al., 2010; Gauslaa & Coxson, 2011), pre-

sumably because their gelatinous sheaths take up much

water (Honegger et al., 1996). However, other structures can

also influence the water storage (Larson, 1981; Palmer &

Friedmann, 1990; Green & Lange, 1991; Valladares et al.,

1998).

Low STM, as in many chloro- and cephalolichens, allows

rapid and frequent hydration (Larson & Kershaw, 1976;

Larson, 1981). Thereby, they do not need the high resistance

reported in cyanolichens to survive dry periodswith high light

(Gauslaa et al., 2012). The strong dominance of L. scrobiculata in

studied forests, as well as a general cyanolichen dominance in

rainforests (Marini et al., 2011), is consistent with the view

that rain rather than dew is their important source of water.

At the same time, the higher water requirements of L. scrobi-

culata than of the two more opportunistic species (Fig 3) may

explain its consistently lower growth rates in the studied

region (Larsson & Gauslaa, 2011). In fact, the cyanolichen L.

scrobiculata needs 2.5 times greater hydration level than L.

pulmonaria to become photosynthetically active (MacKenzie &

Campbell, 2001).

Habitat-specific differences

In addition to size- and species-specific differences, there is

still some environmental regulation of STM andWHCA. After 3

months transplantation to shaded young stands darker than

source stands, STM in L. pulmonaria decreased, whereas it

increased in clear-cuts (Gauslaa et al., 2006). Across all sizes, L.

pulmonaria had higher STM when growing on the light-

demanding Alnus incana than on nearby shade-tolerant Abies

lasiocarpa (MacDonald & Coxson, 2013). Likewise, STM in

Lobaria species increased in sunny dry seasons and decreased

in wet seasons (Larsson et al., 2012). Thus, STM increases with

increasing light and/or evaporative demands. Here, WHCA

and STM in L. pulmonaria and L. scrobiculata increased with

height in the canopy. High WHCA may improve lichen func-

tioning in dry upper canopies, and we see this as acclimation

to increased light and/or evaporative demands (Hilmo, 2002;

Gaio-Oliveira et al., 2004; Gauslaa & Goward, 2012). However,

P. crocata did not respond in this way, whichmay contribute to

its rarity in upper canopies (Hilmo et al., 2013), as well as

explain its absence outside Atlantic forests in Europe (Holien

& Tønsberg, 1996). The low WHCA of this and other thin cya-

nolichen members of Pseudocyphellaria, like Pseudocyphellaria

anomala (Gauslaa & Coxson, 2011) and Pseudocyphellaria dis-

similis (Snelgar & Green, 1981), probably constrains their eco-

logical niche to very humid sites (Green & Lange, 1991),

whereas the Lobaria species benefitting from humid air (L.

pulmonaria) or from large water storage (L. scrobiculata) have

wider ecological amplitudes.

In conclusion, WHCA strongly increases with increasing

size, consistent with partly different ecological niches for

small and large specimens. Secondly, species respond differ-

ently, consistentwith photobiont-specificwater storage traits.

Finally, the two Lobaria species acclimate by increasing WHCA

with increasing height in canopy gradients, consistent with

acclimation to increasing evaporative demands.

Acknowledgments

This research was supported by Norwegian Research Council

and The Norwegian Forest Owners’ Federation, and by an FPU

grant awarded by the Spanish Education Ministry to S. Mer-

inero. We thank H�akon Holien and Torstein Myhre for sam-

pling branches, and the local forest owner and forest

authorities for permissions.

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