Communities Adjust their Temperature Optima by Shifting
Producer-to-Consumer Ratio, Shown in Lichens as Models:
II. Experimental Verification
Henry J. Sun1, E. Imre Friedmann2
(1) Desert Research Institute, 755 East Flamingo Rd., Las Vegas, NV 89119–7363, USA
(2) NASA Ames Research Center, Mail Stop 245-3, Moffett Field, CA 94035–1000, USA
Received: 13 July 2004 / Accepted: 18 July 2004 / Online publication: 17 May 2005
predicts that more algae are necessary for the same
number of fungi at higher temperatures. We tested this
prediction in Cladina rangiferina (L.) Nyl., a cosmopolitan lichen with wide ecological distribution from the
Arctic to the tropics.
To put the ecological significance of community
adaptation in perspective, we also investigated the role of
other adaptive mechanisms in the thermal ecology of lichens. Within the same lichen species, (which by definition
contains the same mycobiont species as lichens are named
after their mycobionts), the mycobiont may combine with
different photobiont species in different thermal environments (photobiont substitution). Several investigators [2,
6, 19] reported that many mycobionts have the ability to
combine alternately with two or more photobionts, although the ecological role of these observations is yet to be
explained. Fungi in general tolerate a wider range of temperatures than algae, so in a cosmopolitan lichen such as C.
rangiferina, alternate photobionts may be necessary to
accommodate the extraordinarily wide temperature range
of the mycobiont. We assessed this possibility by isolating
photobionts from Cladina spp. collected from the Arctic,
temperate, and tropical habitats and completing specieslevel, taxonomic identification.
At the organismal level, the photobiont may adapt by
two mechanisms. The first is genetic adaptation. In different thermal regimes, mutation and natural selection
may give rise to different genotypes. This was tested by
determining the degree to which growth temperature
optima of the photobiont (in this case Trebouxia sp.) vary
with habitat temperature. The second mechanism,
operating on a seasonal time scale, is photosynthetic
acclimation. The same genotype grown under different
thermal regimes may exhibit different photosynthetic
temperature optima [3, 4, 18]. We estimated the range of
acclimation in one of the isolated Trebouxia strains in the
laboratory.
Abstract
The community adaptation hypothesis [7] predicts that
lichens, simple communities of microorganisms, can
adapt to a wide range of thermal regimes by regulating
the ratio of primary producers (algae) and consumers
(fungi): Rp/c. To test this hypothesis, we determined
Rp/c values by image analysis of cross sections of herbarium specimens of the lichen Cladina rangiferina,
which is widely distributed between the Arctic and the
tropics. We found that Rp/c for C. rangiferina increases
with summer temperature by more than one order of
magnitude, consistent with the hypothesis. To assess the
ecological significance of community adaptation (Rp/c
regulation), other adaptive mechanisms (e.g., photobiont
substitution, genetic adaptation, and photosynthetic
acclimation in North American Cladina spp.) were
studied. Laboratory investigations with algae and fungi
isolated in culture from live specimens suggested that the
role of these mechanisms is relatively minor and cannot
account for the high degree of lichen adaptability.
Introduction
This study presents experimental verification for the
hypothesis of community adaptation [7], which posits
that lichens can adapt to a range of thermal regimes by
regulating the ratio of primary producers and consumers
(Rp/c). Consequently, each habitat temperature has a
specific Rp/c value determined by the equilibrium between algae (primary producers) and fungi (consumers).
In warmer climates, respiration increases more rapidly
(higher Q10) than photosynthesis. Thus, the hypothesis
Correspondence to: Henry J. Sun; E-mail: [email protected]
528
DOI: 10.1007/s00248-005-3679-x
d
Volume 49, 528–535 (2005)
d
Springer Science+Business Media, Inc. 2005
H.J. SUN
AND
E.I. FRIEDMANN: COMMUNITIES ADJUST
THEIR
OPTIMA, II. EXPERIMENTAL VERIFICATION
The situation with fungal components of
C. rangiferina is more complex. Although the mycobionts
were successfully isolated in culture, they are extremely
slow-growers, and their growth curves could not be
determined reliably. Many (or perhaps all) North American Cladina species, however, contain a fast-growing,
dominant parasymbiont, Pestalotiopsis maculans (Corda)
Nag Raj [24]. To estimate the degree of genetic adaptation
in fungal components, we determined the growth temperature optima of eight strains of P. maculans originating
across the geographic range of our studies.
Materials and Methods
Determination of Rp/c.
Forty-four herbarium specimens of C. rangiferina (L.) Nyl. [synonymous with
Cladonia rangiferina (L.) Web.] were obtained from the
United States National Herbarium, Smithsonian Institution, Washington, DC. (see list in Table 1). The
C. rangiferina thallus is tubular and has two concentric
tissue layers—the porous, photobiont-containing medulla and the dense, all-fungus stereome (Figs. 1, 2). Rp/c
values of thalli were determined under the microscope
using cross sections. Thallus portions were embedded in
SpurrÕs resin (to prevent loss of unconnected tissue
portions during sectioning) and sectioned on an ultramicrotome. Sections were about 0.1 lm thick, less than
the diameter of algal cells, thereby ensuring correct cell
counts. Fungi were quantified by surface area measurements of the medulla and stereome corrected for algae
and airspaces. A study of twenty-three sections showed
that, on average, fungi covered 39% of the medulla.
Rp/c in each cross section was calculated in arbitrary
units as follows:
Rp=c ¼
Np
ðAs þ 0:39Am Þ
where Np is the number of algal cells, As is the surface
area of the stereome, and Am is the surface area of the
medulla.
Because Rp/c varies along the thallus, it was necessary
to ensure that comparable portions were sampled from
different herbarium specimens. A detailed study of four
specimens showed that Rp/c was relatively constant in the
lower half of the thallus from about the fifth internode
down, irrespective of thallus height (Fig. 3). Therefore, we
took our samples from this part of the thallus. For each
specimen, five thalli were sampled. From each thallus, 10
sections were analyzed. Their average was taken as Rp/c of
C. rangiferina at the given geographic locality.
Identification and Determination of Growth TemperaWe isolated photobionts
ture Optima of Photobionts.
from two C. rangiferina, two C. subtenuis, two C. mitis,
529
and one C. macroceras collected from North America
following the aseptic technique [1]. All isolates (listed in
Table 2) were identified by Prof. Thomas Friedl of the
University of Bayreuth (Germany) to the species level on
the basis of morphological characteristics.
Partial growth curves were determined using a temperature gradient table as described previously [17]. For
each algal isolate, seven (BoldÕs Basal Medium BBM)
plates were spread-inoculated and mounted on the
temperature table with thermally conductive paste to be
incubated at temperatures ranging from 19.0C to 31.5C
(±0.1C). This temperature range encompassed both Topt
and Tmax of the seven isolates. Continuous illumination
was provided at 40 lmol m)2 s)1 PAR (photosynthetically active radiation) photon flux. Upon appearance of
confluent growth, incubation was terminated. Growth
was then enumerated under the microscope with a
hemacytometer and expressed as percent increase of
inoculum.
Determination of Optimal Growth Temperatures of
As it is notoriously difficult to
Fungi (Parasymbionts).
determine the growth temperatures of mycelium-forming
fungi, we calculated optimal temperatures of P. maculans
from measured Tmax values. To determine Tmax, Malt
Yeast Extract (MYE) plates were inoculated by streaking a
straight line of conidia across the center of each plate. The
plates were incubated at 25C for 5 h until conidia started
to germinate and then on a temperature table at various
temperatures ranging from 25C to 35C. The plates were
arranged so that the inoculated streaks formed a nearly
continuous line in the direction of the temperature gradient. By the 3rd or 4th day of incubation, the point between growth and no growth became distinct along the
inoculated line. The temperature of this point, Tmax, was
measured using a thin thermocouple. We estimated values
of Topt by subtracting 5C from Tmax. We derived the 5C
difference between Topt and Tmax from comparing complete growth curves of four selected strains (Fig. 4). To
determine these curves, MYE plates were inoculated with
conidia (using a needle) to create four small growth
points on each plate. After incubation at 25C until
conidia started to germinate, the plates were distributed in
incubators at 0, 5, 10, 15, 20, 22, 25, 27, 29, 31, 33, and
35C. We calculated growth rate as daily increase in colony surface area. This indirect method yielded more
accurate measurements of optimal growth temperatures
for microscopic fungi than any other method described in
the literature.
Measurement of Photosynthesis.
We used midlog phase culture of T. irregularis [strain (624)C.mit.NC]
raised on MYE agar under continuous illumination at 20
lmol m)2 s)1 PAR photon flux. Prior to experiments,
cells were collected and suspended in liquid BBM at
Colville River, Umiat, Alaska, USA
Disko, Godhavn, W. Greenland
Canoe Lake, Richardson Mountain,
Northwest Territories, Canada
Paxson, Alaska, USA
Coppermine, MacKenzie District, Canada
Mount McKinley Natl. Park, Alaska, USA
Eagle Summit Tundras, Alaska, USA
Hálfdán Pass, Bildudalur, Iceland
PP. Haukipudas, Kello, Isoniemi, Finland
Cassiar, British Columbia, Canada
Summit Pass, British Columbia, Canada
Great Slave Lake, Northwest
Territories, Canada
Ennadai Lake, Keewatin District,
Northwest Territories, Canada
Uusimaa, Finland
Bow River Watershed, Alberta, Canada
Herbert Glacier Trail, Juneau, Alaska, USA
Iskwasum Lake, Manitoba, Canada
Nanaimo, British Columbia, Canada
Clark Fork, Bonner Co., Idaho, USA
Voyageurs Natl. Park, St. Louis Co.,
Minnesota, USA
Paradise, Chippewa Co., Michigan, USA
Indian Pass, Essex Co., New York, USA
Lake Placid Trail, Hamilton Co., New York, USA
Essex Co., New York, USA
Clear Lake, Lane Co., Oregon, USA
La Porte, Sullivan Co., Pennsylvania, USA
Little Stony Creek, Giles Co., Virginia, USA
Stone Valley Experimental Forest,
Huntingdon Co., Pennsylvania, USA
Hocking Co., Ohio, USA
Fall Creek Falls State Park, Van Buren Co.,
Tennessee, USA
Cedar of Lebanon State Park, Wilson Co.,
Tennessee, USA
De Soto State Park, De Kalb Co., Alabama, USA
Ouachita Natl. Forest, Montgomery Co., Arkansas, USA
Cedar Grove, Walker Co., Georgia, USA
Forty Acre Rock, Lancaster Co., South Carolina, USA
Walnut Grove, Walton Co., Georgia, USA
Wadley, Randolph Co., Alabama, USA
30, J. W. Thomson and S. Shushan
162, P. Gelting
15703, J. W. Thomson and J. A. Larson
4630009, D. Demaree
43394, D. Demaree
30629, M. E. Hale
20, W. T. Batson and J. C. Cogffey
30613, M. E. Hale
1300, H. A. McCullough
335
299
222
173
244
213
3430¢N
3430¢N
3443¢N
3430¢N
3345¢N
3307¢N
8537¢W
9340¢W
9340¢W
8040¢W
8350¢W
8534¢W
3612¢N 8617¢W
3930¢N 8230¢W
3539¢N 8520¢W
2.1
1.1
2.7
0.6
1.2
1.4
0.7
0.4
2.3
6.3
9.9
17.2
10.6
7.2
5.6
25.6d
26.2e
26.3d
26.3d
26.2d
26.1d
(Continued)
2.9
2.9
5.4
1.7
3.5
0.9
10.0 ± 2.9
26.6d
±
±
±
±
±
±
19.2 ± 5.2
3.9 ± 2.2
3.0
2.2
0.9
2.2
1.1
0.9
4.7
± 2.8
± 2.3
±1.8
± 2.6
± 1.2
± 2.9
± 2.1
± 3.1
±
±
±
±
±
±
±
22.0d
25.6d
7.6
6.4
3.1
7.9
5.0
8.3
12.7
12.2
10.7
11.3
16.8
4.5
12.9
7.7
12.0
b
b
b
±
±
±
±
±
±
±
±
±
4.7 ± 1.6
4.1
2.4
5.5
3.5
3.7
5.2
3.5
1.1
4.6
16.2d
19.0d
18.8d
22.8d
15.0e
22.1d
21.2d
23.4d
16.7h
15.7a,
13.8e
17.4a,
16.4a,
18.2e
19.2e
b
b
b
b
b
b
7.3 ± 1.5
7.3 ± 1.3
6.6 ± 1.6
Rp/c ± SD
THEIR
165
210
213
8502¢W
7401¢W
7425¢W
7345¢W
12405¢W
7629¢W
8104¢W
7649¢W
2517¢E
11430¢W
13436¢W
10046¢W
12402¢W
11610¢W
9250¢W
12.7a,
12.9e
9.2a,
12.6e
14.1e
10.1h
15.4h
12.8a,
13.1a,
12.7a,
5.5
8.0c
12.6a,
e
Tsummer (C)
E.I. FRIEDMANN: COMMUNITIES ADJUST
37142, M. E. Hale
13319, M. E. Hale
37131, M. E. Hale
4638¢N
4408¢N
4358¢N
4322¢N
4401¢N
4125¢N
3756¢N
4038¢N
6022¢N
5050¢N
5834¢N
5437¢N
4909¢N
4812¢N
4830¢N
6042¢N 10143¢W
6302¢N 14529¢W
6745¢N 11338¢W
6343¢N14858¢W
6529¢N 14529¢W
6540¢N 2337¢W
6510¢N 2520¢E
5915¢N 12945¢W
5830¢N 12445¢W
6243¢N 10635¢W
6925¢N 15210¢W
6915¢N53 32¢W
6812¢N 13554¢W
Geographic coordinate
AND
270
671
549
305
85
599
1219
196
65
1707
61
285
884
650
361
325
1082
4
638
265
183
0
1200
1372
164
61
18
9
Alt. (m)
H.J. SUN
34444, M. E. Hale
13945, F. J. Hermann
14556, F. J. Hermann
437, I. M. Brodo
L-567, L. H. Pike
17116, M. E. Hale
11368, W. L. Culberson
5710009, R. W. Becking
10612, M. J. Lai
21928, C. D. Bird and D. Gill
150, R. Hale
636102, J. Looman
V. I./551, A. E. Szczawinski
48119, M. E. Hale
31161, C. W. Wetmore
11810, J. W. Thomson et al.
L21, H. B. Hanson
12392, J. W. Thomson and J. A. Larson
3986, A. Nelson and R. A. Nelson
18215, J. W. Thomson and T. Ahti
9197, H. Kristinsson
T. Ulvinen
684/7, A. F. Szczawinski
179/1, A. E. Szczawinski
10962, J. W. Thomson and J. A. Larson
Geographic locality
Table 1. Relationship between algae-to-fungi ratio (Rp/c) and summer temperature (Tsummer) in Cladina rangiferina
Herbarium no. and collectors
530
OPTIMA, II. EXPERIMENTAL VERIFICATION
Las Vigas, Estado de Veracruz, Mexico
La Vega, Domincan Republic
Santa Catarina Lachatao, Estado de Oaxaca, Mexico
Commissairs, Haiti
Estado Trujillo, Venezuela
Estado de Merida, Venezuela
Cundinamarca, Columbia
20932, M. E. Hale Jr and C. F. Culberson
18999, W. L. Culberson
H. H. Iltis
1331B, L. R. Holdridge
13146, M. L. Figueiras
44389, M. L. Figueiras
10, A. M. Cleef
2140
2160
2050
1600
3250
2950
2900
Alt. (m)
1940¢N 9715¢W
1917¢N 9735¢W
1715¢N 9627¢W
1900¢N 7230¢W
922¢N 7026¢W
830¢ N 7100¢W
500¢N 7400¢W
Geographic coordinate
17.3
26.7g,
19.2g,
27.2g,
15.2i
7.2i
15.1i
j
j
j
g, j
Tsummer (C)
8.3
6.4
10.1
8.8
7.2
6.2
8.1
±
±
±
±
±
±
±
2.8
0.9
3.8
2.3
3.0
2.8
2.2
Rp/c ± SD
AND
Sources for TJuly data:
a
Atmospheric Environment Service, Climatic Atlas of Canada: A Series Maps Portraying CanadaÕs Climate, 1984 Ottawa.
b
Meteorological Branch of Canada, Atlas of Climatic Maps: Series 1-10, 1967-1970, Ottawa.
c
Orvig S (ed), Climates of the Polar Regions, World Survey of Climatology, Vol. 14, 1970, Amsterdam.
d
United States National Oceanic and Atmospheric Administration, Climates of the States: Vol. 1, the Eastern States, 1974, Port Washington, NY.
e
United States National Oceanic and Atmospheric Administration, Climates of the States: Vol. 2, the Western States, 1974, Port Washington, NY.
f
United States National Oceanic and Atmospheric Administration: Monthly Climatic Data for the World, 1991, Asheville, NC.
g
Universidad Nacional de Mexico, Atlas Nacional de Mexico, 1990, Mexico.
h
World Meteorological Organization, Climatic Atlas of Europe, 1970, Geneva.
i
World Meteorological Organization, Climatic Atlas of South America, 1975, Geneva.
j
World Meteorological Organization, Climatic Atlas of North and Central America, 1979, Geneva.
Geographic locality
Herbarium no. and collectors
Table 1. Continued
H.J. SUN
E.I. FRIEDMANN: COMMUNITIES ADJUST
THEIR
OPTIMA, II. EXPERIMENTAL VERIFICATION
531
Figure 1. Typical thallus morphology of Cladina rangiferina. Scale
bar 5 mm.
about 106 cells ml)1. This suspension was loaded into a 5
ml Plexiglas chamber with temperature controlled by a
surrounding water jacket and monitored by a built-in
thermocouple. After 30 minute equilibration, NaHCO3
was added to reach 50 lmol. A projector lamp was then
switched on to provide illumination at 300 lmol m-2 s)1
PAR photon flux. Both conditions were determined to be
sufficient to saturate photosynthesis. Partial O2 pressure
in the suspension was measured with a YSI 5331 oxygen
electrode (Yellow Springs Instrument Co., Yellow
Springs, OH 45387). The electrode was calibrated in
atmosphere-equilibrated water and anoxic water containing excess (Na)2S2O4. A magnetic stirrer bar ensured
rapid mixing in the chamber. The rate of photosynthetic
oxygen evolution was normalized to the content of
chlorophyll a, which was extracted in dimethyl sulfoxide
in the dark at 65C for 40 min and quantified spectrophotometrically [21].
Figure 2. Partial transverse thin-section of the tubular thallus of C.
rangiferina, showing the photobiont (P)-containing medulla (M),
the stereome (S), and the central cavity (C). Scale bar 100 lm.
532
H.J. SUN
AND
E.I. FRIEDMANN: COMMUNITIES ADJUST
THEIR
OPTIMA, II. EXPERIMENTAL VERIFICATION
Figure 3. Distribution of algae-to-fungi ratio (Rp/c) along C. rangiferina thallus. Rp/c in all specimens decreases
sharply but stabilizes at around the fifth internode, providing the basis for sampling of the fifth internode to
study geographic trend of Rp/c. Specimens: New York
state (No. 13945); West Greenland (No. 162); British
Columbia (No. 684/7); Alabama (No. 4630009).
Summer Temperature (Tsummer).
The thermal operating environment of a lichen can only be determined
accurately from a continuous, year-round record of light,
temperature, and water activity in the immediate vicinity
of the thallus [12]. Summer temperature—the mean air
temperature of the warmest month, July for the northern
hemisphere or February for the southern hemisphere—has been shown, however, to be a fairly good
predictor of photosynthetic optima of lichens [15, 16].
We therefore used summer temperature values at the
nearest meteorology stations as approximations of habitat temperatures (sources listed in Table 1).
Results
Rp/c in C. rangiferina.
Across the geographic range of
our study, Rp/c values varied by more than one order of
magnitude and in general increased from the Arctic to
the tropics (Table 1). The correlation between Rp/c and
Tsummer, the July mean air temperature at the nearest
meteorological station, was significant: r2 = 0.24, P <
0.001 (Fig. 5).
Photobiont Substitution.
Photobionts were isolated in culture from seven live specimens including two
C. rangiferina, two C. subtenuis, two C. mitis, and one
C. macroceras. All isolates were identified based on
morphological characteristics as Trebouxia irregularis
Hildreth et Ahmadjian (Table 2).
Genetic Adaptation.
Growth temperature optima
of the seven photobiont T. irregularis isolates varied from
19C to 26C, a difference of only 7C while Tsummer
values varied from 12.6C to 27.4C, a more substantive
difference of 14.8C (Table 2, Fig. 6). In general,
photobiont isolates from warmer, southern localities had
higher growth temperature optima and higher maximal
growth rates than those from colder, northern localities.
The correlation between photobiont optima and Tsummer
was significant: r2 = 0.74, P < 0.005.
Growth temperature optima of eight isolates of the
dominant parasymbiont P. maculans varied from 26C to
28C, a difference of only 2C while the range of Tsummer
values was 8.2C (Table 3). There was no significant
correlation between fungal optima and Tsummer values.
Table 2. Relationship between optimum growth temperature (Topt) and summer temperature (Tsummer) in the photobiont Trebouxia
irregularis
Photobiont strain
Lichen
Geographic locality
Geographic coordinate
Alt. (m)
Topt (C)
Tsummer (C)
(626)
(625)
(621)
(623)
(624)
(622)
(619)
C.
C.
C.
C.
C.
C.
C.
Valdez, Alaska, USA
Valdez, Alaska, USA
Toronto, Ont., Canada
Rhode Island, USA
Franklin Co., NC, USA
Tallahassee, FL, USA
Santa Catarina Lachatao,
Oaxaca, Mexico
6100¢N
6118¢N
4345¢N
4131¢N
3543¢N
3019¢N
1715¢N
300
300
200
30
600
20
2050
19.0
19.0
21.0
21.0
23.0
26.0
21.0
12.6
13.0
21.2
21.3
18.0
27.4
19.2
a
C.
C.
C.
C.
C.
C.
C.
mac.AA
mit.AA
rang. TNTC
subt.RI
mit.NC
subt.TL
rang. OA
macroceras
mitis
rangiferina
subtenuis
mitis
subtenuis
rangiferina
See the end of Table 1 for climatological sources.
14600¢W
14600¢W
7940¢W
7118¢W
8323¢W
8425¢W
9627¢W
(e)a
(e)
(a, b)
(d)
(d)
(d)
(g, j)
H.J. SUN
AND
E.I. FRIEDMANN: COMMUNITIES ADJUST
THEIR
OPTIMA, II. EXPERIMENTAL VERIFICATION
Figure 4. Growth temperature curves of parasymbiontic fungi
(Pestalotiopsis maculans) isolated from North American lichens.
Photosynthetic Acclimation.
When grown at 7C,
T. irregularis [strain (624)C.mit.NC] showed a photosynthetic optimum at 33C under our experimental
conditions (Fig. 7). When cultured at 22C, it exhibited a
slightly higher photosynthetic optimum at 37C. Acclimation also resulted in a decrease in the maximal photosynthetic rate, from 2.9 to 1.1 lmol O2 lg chl a)1 h)1.
These changes are consistent with those reported for
photosynthetic acclimation in cyanobacteria, plants, and
algae [3, 4, 18, 22].
Discussion
This study
confirms the prediction of the community adaptation
hypothesis that the ratio of producers and consumers in a
lichen association changes with the thermal environment
[7]. Two experimental facts stand out, the first of which is
the unexpectedly large, about one order of magnitude, Rp/c
range occurring within a single lichen ‘‘species.’’ The
second is the relatively high correlation between Rp/c in
Community Adaptation in C. rangiferina.
Figure 5. Algae-to-fungi ratio (Rp/c) in C. rangiferina as a function
of habitat temperature (Tsummer). Each Rp/c datum is an average
based on fifty sections sampled from five thalli. See Table 1 for
detailed geographic and herbarium information.
533
Figure 6. Growth temperature curves of photobionts (Trebouxia
irregularis) isolated from North American Cladina ssp. (1) Tallahassee, (2) N. Carolina, (3) Rhode Island, (4) Oaxaca, (5) Toronto,
(6) Alaska, (7) Alaska.
C. rangiferina and the mean July air temperature in North
and Central America (Table 1, Fig. 5). The large data
scatter is evidently due to the fact that while Rp/c values
were determined with relatively high accuracy, Tsummer
values at the nearest meteorological station were, out of
necessity, crude approximations of the lichen thermal
environment. The latter is controlled by nanoclimate (i.e.,
climate in the millimeter range of the lichen thallus), not
by mesoclimate, the climate of a small geographic area [8].
In other words, lichens that grow under the same general
climate may experience very different microenvironments
due to shade, albedo, moisture content of the soil, and
other factors. Conversely, the actual, operating thermal
environments for lichens in different mesoclimate regimes
may be quite similar: for example, a shaded tropical
microenvironment versus an arctic habitat warmed under
direct, full sun [12]. Thus, the actual correlation between
Rp/c and nanoclimate may well be higher than that shown
in Fig. 5.
Scattered observations exist in the literature that
photobiont-to-mycobiont ratios in lichens vary with
environmental conditions. These observations can now be
interpreted as examples of community adaptation. For
instance, C. uncialis thalli in southern Finland have a
thicker algal layer than do those from the colder Arctic
Kevo [11]. Aspicilia desertorum and Dictyonema glabratum
thalli contained more photobiont cells in direct sunlight
than in shade [13, 14]. In C. subtenuis, C. rangiferina, and
C. sylvatica algal abundance depends on the relative position of the thallus within a tuft—thalli in the periphery
contain more algae than do those in the center; thalli facing
west and south contain more algae than those facing east
and north [20]. The photobiont-to-mycobiont ratio in
Cetraria nivalis increases with decreasing geographic latitude (increasing habitat temperature) between Ny Ålesund, Svalbard (7855¢N), and Mount Glungezer (4713¢N)
in Austria [23].
The community adaptation hypothesis also predicts
that, at least in fast-growing lichens, Rp/c will change
534
H.J. SUN
AND
E.I. FRIEDMANN: COMMUNITIES ADJUST
THEIR
OPTIMA, II. EXPERIMENTAL VERIFICATION
Table 3. Relationship between optimum growth temperature (Topt) and summer temperature (Tsummer) in the dominant secondary
fungus Pestalotiopsis maculans
Strain
Lichen
Locality
Geographic coordinate
Topt (C)b
Tsummer (C)
761
Cladina. rangiferina (L.) Wigg.
1715¢N 9627¢W
26
19.2 (g, j)a
762
763
764
766
769
770
771
C. subtenuis (Abbayes) Mattick
Parmotrema perforatum (Jacq.) Massal.
Usnea strigosa (Ach.) Eaton
C. mitis Sandst.
C. subtenuis
C. rangiferina (L.) Wigg.
C. subtenuis
Santa Catarina Lachatao,
Estado de Oaxaca, Mexico
Tallahassee, FL, USA
Tallahassee, FL, USA
Tallahassee, FL, USA
Lizard Lick, NC, USA
SoldierÕs Delight, MD, USA
GambrillÕs State Park, MD, USA
Mattapoisett, MA, USA
3019¢N
3019¢N
3019¢N
3549¢N
3925¢N
3929¢N
4139¢N
26.5
27
28
27
27
28
28
27.4
27.4
27.4
25.3
26.4
26.4
23.4
8425¢W
8425¢W
8425¢W
7823¢W
7650¢W
7729¢W
7049¢W
(d)
(d)
(d)
(f)
(f)
(f)
(f)
a
See the end of Table 1 for climatological sources.
Determined as Tmax ) 5C (see ‘‘Methods’’).
b
seasonally. Indeed, Rp/c appears to fluctuate seasonally
in Cladonia subtenuis, C. rangiferina, C. sylvatica,
Hypogymnia physodes, and Parmelia caperata [5, 10, 20].
We suggest that community adaptation (Rp/c regulation) directly contributes to the cosmopolitan distribution
of C. rangiferina. Most other lichens have a more limited,
or even a narrow range of thermal distribution. The direct
reason for this narrow distribution is not immediately
evident but probably can be attributed to other factors that
limit a lichen to a certain ecological niche.
Organismal Adaptation in Cladina.
In order to
assess the significance of community adaptation, we also
estimated the role of other mechanisms in temperature
adaptation of lichens. At the community level, no evidence suggests that the mycobionts of Cladina in North
America combine with alternate photobionts. In fact, all
seven specimens belonging to four Cladina species and
originating from Arctic, temperate, and tropical localities
contained the same photobiont species, T. irregularis
(Table 2, Fig. 6). The isolates exhibited a significant
amount of genotypic variation, however. From the Arctic
to the tropics, the growth temperature optima of the
isolates increased from 19C to 26C, a range of 7C. At
the same time, however, habitat Tsummer increased twice
as much, from 12.6C to 27.4C, which is presumably the
range of community adaptation by the lichens. Similarly,
the dominant parasymbiont, P. maculans, exhibited a
genotypic variation of 2C, an insignificant range compared to habitat Tsummer, which varied from 19.2C to
27.4C (Table 3).
As expected, our physiological studies also indicated
that Trebouxia photobionts are capable of photosynthetic
acclimation. The adaptive range of acclimation appears
to be limited, however. Photosynthetic optima of cells
grown at two very different temperatures, 7C and 22C,
differ by only 5C (Fig. 7).
We conclude that in the thermal adaptation of
Cladina in North and Central America, the combined
role of mechanisms functioning at the organismal level is
minor in comparison to community adaptation.
Worldwide Trends in Community and Organismal
Figure 8 summarizes available data on
Adaptation.
photosynthetic temperature optima of lichens and growth
temperature optima of isolated bionts on a worldwide
scale. This plot builds primarily upon data on thallose
lichens compiled by Lechowicz [15, 16], but also includes
more recently determined temperature optima of Antarctic cryptoendolithic lichens [9], the growth temperature optima of algae and fungi isolated from them [17],
and the results of the present study on bionts isolated
from North American lichens (Tables 2, 3). As few measurements of nanoclimate conditions exist, Tsummer values
are used as approximations of habitat temperatures.
As expected, Topt of lichens, photobionts, and fungal
components all showed significant correlation with
Tsummer (the lichen-Tsummer correlation reflects community adaptation; the photobiont and fungus correlations
with Tsummer reflect organismal adaptation):
In lichens:
Topt ¼ 0:51 Tsummer þ 9:15
r2 ¼ 0:27; P < 0:01
In algae :
Topt ¼ 0:25 Tsummer þ 16:74
r2 ¼ 0:82; P < 0:01
In fungi :
Topt ¼ 0:18 Tsummer þ 22:58
r2 ¼ 0:69; P < 0:01
Figure 7. Acclimation by photobiont T. irregularis to 7C and
22C, resulting in a 5C shift of photosynthetic optimum.
H.J. SUN
AND
E.I. FRIEDMANN: COMMUNITIES ADJUST
THEIR
OPTIMA, II. EXPERIMENTAL VERIFICATION
Figure 8. Temperature optima of lichens (open circle), photobionts (filled circle), and fungal components (filled square) originating from polar, temperate, and tropical regions. Summer
temperature represents the monthly mean of July for the northern
hemisphere or February for the southern hemisphere. Data are
from [9, 15–17], R. Ocampo-Friedmann, personsal communications, and the present study.
The amplitude of community adaptation far exceeds that
of organismal adaptation, however. Compared with Topt
of bionts, Topt of lichens (1) vary at a higher, closer-tounity rate with Tsummer; (2) scatter more widely around
the correlation, presumably due to microenvironments;
and (3) have a much wider, about 33C, total range on a
worldwide scale. We conclude that lichens, as a rule, are
better adapted to their thermal environment than their
bionts.
Acknowledgments
This work was supported by NSF grant DPP 83-1410, and
NASA grant NSG 7337 to EIF and by NASA RTOP 34450-30-01 to HJS. Drs. Ludger Kappen, Martin Lechowicz,
and Donald Strong read an early version of the manuscript and provided valuable comments. We are grateful
to the late Dr. Mason Hale and Dr. Paula DePriest for
access to the National Herbarium. Dr. Thomas Friedl
kindly identified the photobionts. We thank Roger
Kreidberg for critical editing, Annette Risley for assistance in preparation of graphics, and Dr. John Krug, Mr.
Dana Fiore, and Dr. Mary Allen for supplying specimens.
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