Вы находитесь на странице: 1из 18

Ecological Relationships of Desert Fog Zone Lichens

Author(s): Philip W. Rundel


Reviewed work(s):
Source: The Bryologist, Vol. 81, No. 2 (Summer, 1978), pp. 277-293
Published by: American Bryological and Lichenological Society
Stable URL: http://www.jstor.org/stable/3242189 .
Accessed: 11/07/2012 03:21
Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .
http://www.jstor.org/page/info/about/policies/terms.jsp

.
JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of
content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms
of scholarship. For more information about JSTOR, please contact support@jstor.org.

American Bryological and Lichenological Society is collaborating with JSTOR to digitize, preserve and extend
access to The Bryologist.

http://www.jstor.org

The Bryologist 81(2), 1978, pp. 277-293


Copyright @ 1978 by the American Bryological and Lichenological Society, Inc.

Ecological Relationships of Desert Fog Zone Lichens"l3


PHILIP W. RUNDEL2

Abstract. Patterns of environmental conditions prevailing in coastal desert


fog zones provide habitats extremelyfavorable for lichen growth. Phylogenetically related groups of lichens occur in geographically isolated desert fog
zones, but endemism at both the species and genus levels is relatively high.
The ecological importance of lichens in these regions is related to morphological and physiological adaptations to water uptake in both a liquid and vapor
form. Much of this moisture is unavailable to vascular plants, allowing a large
biomass of lichens to occur in areas with little or no vascular plant cover. The
relative importance of fruticose lichens in such habitats, in comparison to
crustose and foliose forms, is determined largely by the physical form of atmospheric moisture.
Coastal deserts share many environmental features common to all deserts. Rainfall
is low and vegetation is commonly sparse or lacking. At the same time, coastal deserts
have certain distinctive characteristics not shared by inland deserts. Temperature
differences between night and day are moderated by the proximity of the sea. More
important for lichens, however, is the typical occurrence of high atmospheric humidity, fog and/or dew along the coast.
Extensive coastal deserts occur in three areas of the world: the Peruvian and Chilean Atacama deserts, the coastal Sonoran Desert in Baja California and the Namib
Desert in southwestern Africa. Each of these areas shares the same origin of climatic
development in the movements of sub-tropical high pressure centers resulting in the
transport and upwelling of cold currents adjacent to their coasts. Details of the general
climatology of these regions has been described in many publications (e.g. Meigs,
1966; Rumney, 1968). Each of these coastal fog deserts is characterized by lichen
floras rich in both diversity and biomass. This review describes the ecological and
floristic relationships of lichens in these coastal fog deserts with particular emphasis
on the coastal Atacama and Baja California regions.
Coastal Atacama Desert.-The
Atacama desert along the coasts of Peru and northern Chile, perhaps the driest region in the world in terms of measurable precipitation,
extends from the region north of Trujillo near the Ecuadorian border of Peru (50OS)
south to La Serena (30OS) in Chile, a total distance of more than 3500 km. Along this
belt is a narrow strip of coastal desert whose biological characteristics are profoundly
influenced by frequent maritime fogs. The cold northward flowing Humboldt current
1 This researchwas supportedby NSF grantsGB-40509 and DEB-75-19848. I thankProfessors
Otto L. Lange, Ludger Kappen and Thomas H. Nash for helpful discussion.
2
Department of Ecology and Evolutionary Biology, University of California, Irvine, CA
92717.
3 Part of symposium on "The Role of Lichens in Ecosystems," Second International Mycological Congress. Tampa, Florida, U.S.A. Aug. 27-Sept. 3, 1977.

0007-2745/78/277-293$1.95/0

278

THE BRYOLOGIST

[Volume

81

1000

800

no vegetation

600woody
plants
400

growth
ofopen
perennials

0o

cryptograms

S200-

i~n

no vegetation

vegetation-

FIGURE1. Diagrammaticview of vegetation zonation in the coastal lomas of Southern Peru.


Redrawn from Ellenberg (1959).

and associated areas of extensive upwelling of deep ocean waters off the Atacama
Coast produce a mild, uniform climate in the coastal zone and such stable air mass
conditions that precipitation is rare or even absent. In the coastal Chilean Atacama,
mean annual precipitation ranges from a high of 26 mm at Caldera to an incredible
0.6 mm at Arica over a 44 year record. In central Peru precipitation increases slightly,
reaching 41 mm yr-1 at Lima. Available climatological data for the Atacama desert has
been detailed by Hajek and di Castri (1975) and di Castri and Hajek (1976). Less data
are known for coastal Peru, but available records are summarized by Meigs (1966). A
summary of climatic data for selected coastal stations is shown in Table 1.
Although precipitation is slight, water input from moisture condensation from
coastal fogs allows local development of rich biological communities. Thick low fogs,
termed the garua in Peru and the camanchaca in Chile, form along the coast almost
daily during the winter season from June to October. Although the elevational limits
of the garua and camanchaca vary somewhat with latitude and local topography, fog
is typically present in a well-defined band extending from 300-800 m (Rundel &
Mahu, 1976). Where the coastal topography is low and relatively flat, the effects of
the fog are dissipated over broad areas with little resultant biological influence. Where
steep coastal mountains are present, however, fog condensation is concentrated in a
narrow belt where moisture input allows the development of relatively lush fog zone
vegetation. Conditions for condensation of fog moisture are particularly favorable
along the Atacama coast (Ellenberg, 1959). The temperature of the Humboldt Current
is warmer than that of similar currents off the coasts of Baja California and Namibia,
producing high water vapor contents and consequently high aerosol liquid water content of air masses with subsequent cooling. Also important is the constant light southwest winds, blowing onshore at velocities up to 4 m/s. This wind is important in
providing a continuing source of new aerosol water for condensation against the steep
coastal mountains.
Vegetation development in the coastal lomas of Peru has been described by many
(e.g. Troll, 1932; Weberbauer, 1945; Ellenberg, 1959; Koepcke, 1961; Walter, 1971).
A diagrammatic representation of a typical coastal fog zone is shown in Figure 1. The
coastal plain below the fog zone is barren of vegetation, except for scattered stands
of unrooted terrestrial Tillandsia (Bromeliaceae) which occurs on windblown sand

1978]

279

RUNDEL: DESERT FOG ZONE LICHENS

TABLE1. Climatic data for coastal stations in the AtacamaDesert of Peru and Chile, Sonoran
Desert on the Pacific Coast of Baja Californiaand Nanib Desert of Angola, Namibia and South
Africa. Data from Meigs (1966), di Castri and Hajek (1976) and Hastings and Humphrey (1969).
Mean

Mean

Mean

Mean Annual Annual Annual


Eleva- Annual Max.
Min. Precipi- Years
Latitude
tion
Temp. Temp. Temp. tation of Prec.
(mm) Records
(m)
(0C)
(OSor ON)
(0C)
(0C)
Atacama-Peru
Lambayegue
Chiclayo

Trujillo
Lima

Mollendo
Atacama-Chile
Arica
Iquique
Los Condores
Cerro Moreno
Taltal
Chafiaral
Caldera
La Serena

Sonoran-BajaCalifornia
Isla Todos Santos
San Telmo
El Socorro
El Rosario
Vizcaino

Bahia Tortugas
Punta Abreojos
San Juanico

Bahia Magdalena
La Aguja

Todos Santos
Namib
Luanda
Lobito
Mogamedes
Walvis Bay
Port Nolloth
Klaver

6037'

22.2

6041'

22.9
15.2

8
3-4

19

21.1

27.9

2-4

49

18.9

23.9

16.1

45.7

26

17058'

17.8

19.4

16.1

22.1

13

18028'
20015'
23029'
25025'
26020'
27003'

29
515
518
119
39
9
28

18.7
17.9
15.5
17.0
17.4
16.4
16.1

22.2
21.2
19.0
20.1
22.0
19.3
19.7

15.1
14.1
10.2
13.3
14.5
12.2
12.9

0.6
2.1
0.0
2.2
25.1
1.7
25.8

44
49
7
7
21
7
49

29054'

32

14.8

18.9

11.2

127.4

91

8005'
12000'

20012'

31048'

22

255.6

30058'
30020'
30004'
27059'
27042'

100
10
15
10

16.3
16.9
20.9
18.8

172.1
137.7
95.0
79.8

17
11
14
10

26044'

5
15

20.3
21.6

95.8
76.8

11
12

26016'

12

21.1

64.1

24038'

12

21.4

73.7

31

23059'

10

22.4

49.9

23026'

18

22.0

169.6

30

8050'
12013'
15010'
29010'

60
1
3
7
7

24.4
24.4
21.1
17.2
13.9

27.2
27.2
25.0
22.2
18.3

21.7
21.1
16.7
11.7
9.4

322.6
353.1
53.3
22.9
58.4

59
19
21
20
64

31043'

42

19.4

26.7

12.2

22053'

dunes. The lower margin of the fog zone is characterized by cryptogamic communities
of Nostoc and Teloschistes on stable sand surfaces and crustose lichens on rock substrates. Higher up, scattered stands of herbaceous plants and low woody vegetation
merge into a true fog forest of evergreen trees 5-8 m in height at the center of the fog
zone. Epiphytic mosses and lichens are abundant. As the density of the fog zone
decreases at 700 m, open stands of vegetation give way to scattered cacti and tillandsias and, finally, to barren land free of plants. Ellenberg (1959) found that vascular
plant development over the fog moisture gradient was related to the depth of penetration of soil moisture. Virtually no data are available on lichen zonation, however.
Vegetation zonation in the coastal fog belt of northern Chile at Paposo has been
described in detail by Rundel and Mahu (1976), and broadly by Reiche (1911) while

THE BRYOLOGIST

280

[Volume

81

-1000

NO
VEGETATION

.. ..

. ..

....

..

...:.

..

..

CO PIAPOA

..

-800

....

.................
:EULYCHNIA:?.. F-600

..COPIAPOA
..

EUPHORBIA.EULYCHNIA
/

H:::::::::::::
A::::::

EUL

YCH

IA-

PU

-200
SOPEN

COASTAL PLAIN-COPIAPOA

o-10
FIGURE2. Diagrammaticview of vegetation zonation in the coastal fog zone at Paposo,
AtacamaProvince, Chile. From Rundel and Mahu (1976).

the flora of this zone has been treated by Johnston (1929). Here the coastal plain
below the fog belt supports scattered stands of small globular cacti grading to a distinct
belt of terrestrial Puya (Bromeliaceae) at the lower margin of the fog zone (Figure 2).
Within the central fog zone, woody vegetation becomes dominant in forming dense
stands 2-3 m in height with 60% ground cover. At higher elevations in the upper fog
zone, open slopes with increasingly scattered cacti replace woody vegetation (Rundel
& Mahu, 1976), with the area above 1000 m virtually free of any vegetation. While
the development of woody vegetation is not as luxuriant as in the lomas of Peru, the
diversity and biomass of lichen epiphytes are greater. Detailed studies of the lichen
flora of the coastal Chilean zone have been made at Cerro Moreno near Antofagasta
(Follmann, 1960, 1967c), at Paposo (Rundel, unpublished data) and at the desertsclerophyll transition zone of Coquimbo and Aconcagua Provinces (Follmann, 1960;
Follmann & Redon, 1972; Redon, 1972).
Coastal Sonoran Desert of Baja California.-The
coastal Sonoran Desert extends
from El Rosario south along the Baja California peninsula. Coastal fogs and high
humidity, extending as much as 50 km inland, are characteristic of this desert area as
well as semi-arid sclerophyll and thorn forest vegetation transitions on the northwestern coast and southern end of the peninsula. The general vegetation characteristics and vascular plant flora of this desert region were described in detail by Shreve
and Wiggins (1964). Extensive climatological data for Baja California have also been
published (Hastings, 1964; Hastings & Humphrey, 1969). Data for coastal stations are
summarized in Table 1.
Unlike the South American coastal desert region, no distinctive fog zone forms
along the coast of Baja California. While fogs are common along the coast, they lack
the temporal and structural regularity of the garua/camanchaca. Winter fogs are particularly common, occurring down to sea level, and moist marine air close to moisture
saturation blows strongly onshore throughout the year. Contrasting with the gentle

1978]

RUNDEL:

DESERT

FOG ZONE LICHENS

281

but steady onshore winds characteristic of the Coastal Atacama, strong irregular winds
blow off of the Pacific Ocean in Baja California, stunting vascular plant vegetation
along the coast and frequently continuing only slightly abated up to 20 km or more
inland. Steep topographic features are rare along the Baja California coast, allowing
maritime influences to reach well across the peninsula in both the central Vizcaino
Region and the Magdalena Plain (Shreve & Wiggins, 1964). Moisture condensation
from humid air masses and irregular fogs allow the development of a moderately
diverse epiphytic lichen community (Nash et al., 1977) and a locally dense growth of
Tillandsia recurvata on a variety of shrubs and succulents.
Although true coastal fog belts do not form along the coast of Baja California,
distinctive vegetation zones dominated by lichens develop where steep cliffs on moderate slopes are topographically developed along the immediate coast (Rundel et al.,
1972). Vascular plant vegetation is commonly restricted severely in these habitats by
soil aridity, wind desiccation and salt spray. Local conditions are optimal, however,
for luxuriant growth of epiphytic, saxicolous and terricolous lichens, and lichen biomass may rival or even surpass that of vascular plants in these coastal areas. Although
published studies of the floristics and ecology of lichens in this coastal zone are few
(Rundel et al., 1972; Nash et al., 1977; Dodge, 1936), the lichen flora is relatively well
known.
Namib Desert.-The
Namib Desert stretches along the southwest coast of Africa,
km
2800
from
Luanda (8?45'S) in Angola to St. Helena Bay (32?45?S) in
extending
South Africa (Meigs, 1966). Like the deserts of Baja California and the coast of Peru
and Chile, the coastal Namib is characterized by cool, moist sea fogs, resulting from
the cold Benguela Current. Observations at Luderitz Bay showed 285 days during the
year with fog or dew (Meigs, 1966). Even when there is no fog, relative humidities
remain at 100 percent during most of the day. Surface condensation of this water is
the major source of moisture for an extensive lichen flora, as well as for several unusual
succulent plants (Walter, 1971; Giess, 1962; Bornman et al., 1973). Annual precipitation is commonly in the range of only 20-50 mm along the coast. Although several
general discussions of the environment and vegetation of the Namib Desert are available (Cannon, 1924; Logan, 1960; Walter, 1936, 1971), detailed descriptions of the
flora are scarce (Giess, 1962, 1968). Vascular plant adaptations have been discussed
by Schulze and Schulze (1976) and Schulze et al. (1976). The lichen flora of this area
has not been described.
Level, gravelly desert plains of the outer Namib support only rare individuals of
vascular plants, but the windward sides of even small pebbles have well-developed
lichen growth. This growth, dominated by Caloplaca, occurs both as upright subfoliose morphotypes which take advantage of direct fog interception and small crustose
growths at soil level which utilize runoff from fog condensation on the rock above. A
variety of strange specialized lichen growth forms from the southern Namib were
described by Vogel (1955). Farther inland, dense colonies of Teloschistes form a distinct stabilizing element on low sand dunes, comparable to the zone of T. peruensis
in southern Peru. The windward slopes of quartzite and marble ridges in nearby areas
provides vertical faces where fog condensation may become concentrated. A variety
of both stem and leaf succulent plants dominate these slopes, together with a rich
saxicolous lichen flora (L. Kappen, pers. comm.).
FLORISTIC

COMPARISONS

Despite the wide geographic separation of the three major regions of desert fog
zones, considerable floristic similarities exist among the lichen floras of these areas.

282

THE BRYOLOGIST

[Volume

81

TABLE2. Occurrence of species of Roccellaceae in the coastal fog deserts of BajaCalifornia


and Chile. Data from Rundel et al. (1972), Follmann (1967c), Follmann & Redon (1972) and
Rundel (unpublished data).
Baja California
Crustose
Dirina catalinariae Hasse

Chile
Dirina chilensis (Nyl.) Follm.
D. limitata Nyl.
D. lutosa Zahlbr.
Dirinastrum chilense (Dodge) Follm.
Lobodirina cerebriformis (Mont.) Follm.
L. mahuiana Follm.

Fruticose-Foliose
Darbishirella gracillima (Kremph.)Zahlbr.
Dendrographa leucophaea (Tuck.) Darb.

Reinkella parishii Hasse


Roccella babingtonii Mont.
R. fimbriata Darb.
R. sp.

Dolichocarpus chilensis Sant.


Ingaderia pulcherrima Darb.
Pentagenella fragillima Darb.
Reinkella lirellina Darb.
Roccella babingtonii Mont.
R. cervicornis Follm.
R. gayana Mont.
R. minima Sant.
R. portentosa (Mont.) Darb.
Roccellaria mollis (Hampe) Zahlbr.
Roccellina condensata Darb.
R. luteola Follm.

Schizopelte californica Th.Fr.


However, unlike dry desert floras of terricolous and saxicolous lichens, where individual species frequently have worldwide distribution patterns (Weber, 1962), the
floristic similarity of desert fog zones is primarily evident at the family and genus
levels.
All three desert fog zone regions are dominated by species of Roccellaceae on
coastal rocks, where aerosol moisture input is high. The diversity of species is variable
between regions, however. At Cerro Moreno near Antofagasta in northern Chile, 19
species of Roccellaceae in 12 genera are present (Table 2). At a comparable site in
Baja California, only seven species in five genera are present, although the total biomass of Roccellaceae is greater (Rundel, unpublished data). Despite the differences
in diversity between species in the Roccellaceae between Baja California and Chile,
the relative occurrence of species on different substrate types is remarkably similar.
In Baja California, 33% of the species typically occur on vascular plant substrates,
while the remaining 67% are on rock. In Chile, 37% are on vascular plants, 58% on
rock and 5% on soil.
Genera of the Roccellaceae, hypothetically very old taxa, are today commonly
geographically isolated. Coastal desert fog zones where these endemic genera are
concentrated, however, are geologically recently formed. Recent isolation of genotypes does not appear to be an important consideration in speciation, and therefore
diversity, in either Chile or California/Baja California. The majority of species have
a wide latitude of occurrence in coastal habitats. A notable exception to this pattern

1978]

RUNDEL: DESERT FOG ZONE LICHENS

283

TABLE 3. Occurrence of species of Ramalinaceae in the coastal fog deserts of Baja California and Chile. Data from Rundel et al. (1972), Follmann (1967c), Follmann and Redon
(1972), Redon (1972) and Rundel (unpublished data).

Baja California

Chile

Cenozosia inanis Mont.


Niebla cephalota (Tuck.) Rund. & Bowl.
Niebla cephalota (Tuck.) Rund. & Bowl.
N. ceruchis (Ach.) Rund. & Bowl.
N. ceruchis (Ach.) Rund. & Bowl.
N. flaccescens (Nyl.) Rund. & Bowl.
N. homalea (Ach.) Rund. & Bowl.
N. josecuervoi (Rund. & Bowl.) Rund. & Bowl. N. tigrina (Follm.) Rund. & Bowl.
N. pulchribarbara (Rund. & Bowl.)
N. sp. nov.
Rund. & Bowl.
N. robusta (Tuck.) Rund. & Bowl.
N. sp. nov.
N. sp. nov.
N. sp. nov.
Ramalina chilensis Bert.
Ramalina bajacalifornica Bowl. & Rund.
R. complanata (Sw.) Ach.
R. duriaei (DeNot.) Jatta
R. denticulata (Eschw.) Nyl.
R. dusenii Magn. nom. nudum
R. duriaei (DeNot.) Jatta
R. ecklonii (Spreng.) Mey. & Flot.
R. farinacea (L.) Ach.
R. peruviana Ach.
R. leptocarpha Tuck.
R. sulcatula Nyl.
R. menziesii Tayl.
R. terebrata Hook. & Tayl.
R. moranii Rund. & Bowl.
R. sp.
R. subleptocarpha Rund. & Bowl.
R. wigginsii Rund. & Bowl.
R. sp. nov.
Trichoramalinacrinita (Tuck.) Rund. & Bowl.

is Hubbsia, restricted to a single rock outcrop on Guadeloupe Island, an oceanic island


off the coast of Baja California (Weber, 1965). Only two species of Roccellaceae, both
Roccella, are shared between Baja California and Chile (Table 2). One of these, R.
babingtonii, is a sorediate species whose wide distribution is in all three desert fog
regions. This is consistent with the hypothesis of relatively great dispersability and
establishment of sorediate forms (Bowler & Rundel, 1975). Three genera, Roccella,
Reinkella and Dirina, occur in both regions, while eight genera are endemic to Chile
and three to California-Baja California. A single endemic genus of Roccellaceae, Combea, is known from the Namib Desert. Numerous species of Roccella are present,
however.
A second important family of desert fog zone lichens is the Ramalinaceae. As in
the Roccellaceae, however, few species are shared between regions. Only Ramalina
duriae occurs in all three regions. Two species of Niebla are shared between Baja
California and Chile, and a single species of Ramalina is present in both Chile and
the Namib. This is a very small species similarity in view of the high diversity of
Ramalinaceae in all three regions.
Opposite to the situation in the Roccellaceae, the diversity of Ramalinaceae is
greater in Baja California than in Chile (Table 3). Three genera and 20 species of
Ramalinaceae are characteristic in this zone of Baja California, including Trichoramalina which is absent from Chile. Three genera and 12 species are present in Chile,
including the endemic Cenozosia. For Baja California, 62% of these species are corticolous, with the remaining 38% on saxicolous or terricolous substrates. This latter
group, including the majority of taxa of Niebla, are extremely prominent and locally

284

THE BRYOLOGIST

[Volume

81

produce large biomasses in the immediate coastal zone where aerosol moisture is
high. Away from the coast, corticolous Ramalina is dominant. In Chile, saxicolous and
terricolous habitats for Ramalinaceae are relatively unimportant although 28% of the
species are typically on such substrates. Large biomasses of saxicolous taxa are totally
absent. Numerous taxa of Ramalinaceae are present in the Namib Desert, but the
majority of species of Ramalina are endemic and remain undescribed. Trichoramalina
melanothrix, with a related species in Baja California, is an unusual endemic (Rundel
& Bowler, 1974).
A third family which forms important elements of desert fog zone lichens is the
Teloschistaceae, most notably the genus Teloschistes. Four species of this genus are
present in the fog deserts of both Baja California and Chile-T. exilis, T. flavicans, T.
chrysophthalmus and T. villosus. The latter is typically restricted to the immediate
coast, while the others occur well inland. As previously described, the endemic T.
peruensis is extremely important ecologically on sand dunes at the lower margin of
the fog zone in Peru (Thomson & Iltis, 1968). The Namib Desert and adjacent parts
of South Africa are likewise characterized by many ecologically important species of
Teloschistes. The unique fruticose Xanthoria flammea is also restricted to this region.
Many other floristic elements are important in all of the desert fog zone regions.
Species of Parmelia with upright growth-forms occur in each region and may dominate
the flora locally as with P. hottentota and similar species on rocky slopes in the Namib.
Chile and Baja California are alike in the frequent occurrence of ciliate species of

Heterodermia.
TRENTEPOHLIA SYMBIOSES

An unusually large percentage of the lichen floras of coastal fog zones of Baja
California and Chile are composed of species with Trentepohlia as an algal symbiont.
Trentepohlioid algae are the symbionts in such ecologically important fog zone genera

as Roccella, Dendrographa, Darbishirella, Dolichocarpus, Hubbsia, Pentagenella, Ingaderia, Reinkella, Dirina, Schizopelte, Opegrapha and Coenogonium, as well as in
a variety of less dominant crustose genera in the Pyrenulaceae, Arthoniaceae, Opegraphaceae and Graphidaceae. Although not well investigated, lichens with trentepohlioid symbionts are also ecologically important in the coastal Namib (L. Kappen,
pers. comm.). Within the macrolichen flora, only Ramalina, Niebla, Usnea and Heterodermia, all with Trebouxia, rival the ecological dominance of the genera with
trentepohlioid symbionts.
There is considerable controversy in the lichenological literature concerning the
biological basis for the establishment of symbioses between spores of lichenized fungi
and Trebouxia. Since Trebouxia is not commonly observed free-living in nature, the
source of the necessary algal cells is unclear, and yet sexual reproduction clearly takes
place with fertile lichen species (Bowler & Rundel, 1975). With Trentepohlia, however, the potential source of symbionts for lichenization can be easily seen in the
field. Free-living colonies of Trentepohlia are common on both rock and plant surfaces
in both the Baja Californian and Chilean coastal deserts.
Little is known of the physiology and ecology of Trentepohlia. The characteristic
orange-red color results from 8-carotene dissolved in fat deposits (Geitler, 1923).
This pigment hypothetically relates to the resistance of Trentepohlia to high light
intensities. In shaded localities the pigment may be almost completely lacking
(Fritsch, 1948). With full pigmentation, Trentepohlia is extremely resistant to high
insolation, much more so than typical green and blue-green algae. Nevertheless, many

1978]

285

RUNDEL:DESERTFOG ZONELICHENS

TABLE4. Relative growth-formdistribution of warm desert lichen floras.


Lichen Growth-Form(%)

Interior Desert
Algerian SaharaDesert
(Faurel et al., 1953)
Negev Desert, Israel
(Galun, 1970)
Sonoran Desert
Rock Valley, California
(Nash et al., 1977)
Silverbell, Arizona
(Nash et al., 1977)
MaricopaCo., Arizona
(Nash, 1975)
Chihuahuan Desert
Jornada,New Mexico
(Nash et al., 1977)
Coastal Fog Desert
Baja California, Mexico
(Rundel & Nash, unpublished data)
Cerro Moreno, Atacama
Prov., Chile
(Follmann, 1967b)

Number of
Species

Fruticose

Foliose

Crustose &
squamulose

114

98

44

93

17

12

88

21

19

81

78

28

72

48

40

60

67

54

13

33

146

25

14

60

lichens with Trentepohlia appear to be very tolerant of low light levels, notably spe-

cies of Opegrapha, Coenogonium, Graphis, Lecanactis and Lepraria. Although there


has been little study of the temperature tolerances of lichens with Trentepohlia symbionts, there is some speculation that many of these species may be sensitive to cold
temperatures (Kappen, 1973). The geographic distribution of macrolichens with Trentepohlia is consistent with this hypothesis.
Plants of Trentepohlia can withstand long periods of desiccation (Howland, 1929),
an important adaptation for survival in the variable fog conditions of coastal deserts.
The availability of colonies of Trentepohlia for lichenization is increased by its reproductive characteristics. It commonly reproduces vegetatively by wind-blown fragments, although it may also reproduce sexually with swarmers in wet conditions
(Fritsch, 1948). Cultural experiments utilizing several crustose genera of lichens have
shown that lichenization occurs within three to six weeks of the time after Trentepohlia and mycobiont cultures of symbionts were placed together (Herisset, 1946;
Ahmadjian, 1973).
MORPHOLOGICAL
ADAPTATIONS
Morphological adaptations to specific environmental stresses are to be expected
in lichens as well as in vascular plants. Such adaptations to hot, dry desert environments include: 1. increased cortical thickness under conditions of high light intensity
(Vogel, 1955; Galun, 1963; Follmann, 1965; Poelt & Wirth, 1968); 2. increased pruinosity or other superficial layers to protect against high light intensity (Schulz, 1931;
Galun, 1963; Poelt & Wirth, 1968; but see also Weber, 1962); and 3. increased relative
dominance of crustose growth form (Galun, 1970). Under environmental conditions

286

THE BRYOLOGIST

[Volume

81

in desert fog zones, however, the structure and morphological characteristics of lichen
floras differ greatly. The most significant environmental factors appear to be moderate
temperatures, high atmospheric moisture content, strong winds and variable solar
insolation. Natural selection should be expected, therefore, to favor adaptations for
optimizing water uptake, reducing desiccation rates and minimizing mechanical damage due to wind.
Contrary to the situation in hot, dry deserts, fruticose lichen growth forms dominate
in coastal fog deserts (Table 4). Crustose lichens in fact, comprise only a small percentage of the total lichen coverage in many areas of unusually high fog frequency in
both Baja California and Chile. It appears, therefore, that the fruticose growth form
may have selective value for optimizing moisture uptake, provided fogs are frequent
and temperatures moderate.
Morphological adaptations to maximize water uptake have been demonstrated in
fog zone lichens. The size and structure of reticulations in Ramalina menziesii Tuck.
(= R. reticulata Kremph.) are related to frequency of fog and relative levels of atmospheric humidity (Rundel, 1974). Morphological variation related to fog occurrence in
Ramalina usnea is present in tropical areas (Rundel, 1978).
Desert lichens may have capabilities of accumulating water rapidly, but only slowly, losing it through desiccation (Zukal, 1896; Galun, 1963; Follmann, 1965). Blum
(1965, 1973), however, rejected the significance of xeromorphic adaptations for protection against evaporation. Experimental studies with arctic and subarctic lichens
have clearly established that morphological characteristics may profoundly affect thallus water relations (Larson & Kershaw, 1976). Thallus surface to volume ratio, branch
shape and degree of clumping of branches all influence the evaporative resistance,
producing significant intraspecific and interspecific population variability. These same
morphological characteristics are clearly important in habitat selection by coastal fog
zone lichen taxa.
Saxicolous and terricolous substrates in coastal fog zones characterized by aerosol
liquid moisture input are dominated by thallus morphologies which expose large areas
of branch surface perpendicularly to the direct moisture-laden winds. This thallus
surface area may be exposed as flattened branches (Niebla josecuervoi) or dense
clumps of terete branches (Niebla "ceruchoides," Teloschistes spp.). Crustose growthforms of lichens on horizontal surfaces are poorly adapted for moisture uptake from
aerosol sources. Fruticose growth forms typically dominate, but some crustose forms
are ecologically successful on such surfaces by utilizing morphological adaptations to
increase thallus surface areas exposed to moist winds. Many taxa in groups typically
crustose become virtually fruticose, forming a clumped to caespitose growth form.
This morphological development can be best seen in Caloplaca coralloides and Lecanora phyganitis in the California-Baja California coastal flora. Raised verrucae in
coastal taxa of Thelomma may represent a similar adaptation.
On corticolous substrates, where moisture condensation on foliage and branches
produces considerable available water, the thallus growth form is less critical. Characteristically, however, thalli are most abundant well inside shrubs rather than on
small branches on the outer surface. On cacti in northern Chile, downward pointing
spines act as major condensation foci and epiphytic lichens are concentrated near the
spine tip rather than on the aereoles. Pendulous or tufted lichens near the spine tips
are ideally suited to maximize water uptake (Figure 3).
In inland areas of fog zones where major moisture input is in a water vapor form,
vertical orientation of thallus branches is less important and foliose and crustose

1978]

RUNDEL:

DESERT

FOG ZONE LICHENS

IsUs
ng3~-

i-':?-:
p~nga
~~:~ ..........s
er
aa:i ..........

.......
7.......
..
hL

FIGURE3.

Lichen diversity on spines of Eulychnia iquiquensis at Paposo.

287

288

THE BRYOLOGIST

[Volume

81

growth forms increase in importance. Total biomass of lichens in such areas is relatively low, however (Kappen et al., 1975; Nash et al., 1977).
Many individual morphological characteristics of lichen thalli may also be important in water relations. Cilia frequently occur in taxa of desert fog zone lichens (e.g.
Heterodermia, Parmelia, Trichoramalina, Tornabenia). Although definitive experiments have not been completed, such cilia would be expected to have adaptive value
in straining aerosol water droplets out of humid air. Pseudocyphellae and related
white striations (maculae), present in many taxa, may also relate to water uptake.
These structures are positively correlated with populations of the Ramalina usnea
complex from foggy microenvironments (Rundel, 1978).
Thick cortices are characteristic of many desert fog zone lichens (Rundel & Bowler,
1974). It is doubtful if this adaptation is primarily a response to high light intensities
as in lichens from hot, dry deserts. More likely, cortical thickness is largely influenced
by potential mechanical damage and desiccation by wind. Morphological adaptations
to sand blasting in Antarctica include the formation of a cortex with thick-walled
hyphae closely appressed (Dodge, 1965). Such cortical structure is characteristic of
the Ramalinaceae in coastal deserts (Rundel, unpublished data).
PHYSIOLOGICAL

ADAPTATIONS

Field studies of photosynthesis and water relations of desert lichens subject to


high humidities or fog condensation are limited to experiments in Israel. Measurements of CO2 exchange of lichens in natural habitats in the Negev Desert have demonstrated that Niebla maciformis (= Ramalina maciformis), Teloschistes lacunosus
and six species of Caloplaca, Diploschistes, Xanthoria and Squamaria are able to
photosynthesize using only water from dew condensation or water vapor uptake
(Lange, 1969; Lange et al., 1970a,b, 1975). Similar adaptations to water vapor uptake
have also been shown for several Antarctic lichens (Gannutz, 1970; Lange & Kappen,
1972). ForNiebla maciformis, average dew condensation is sufficient for approximately
three hours of positive net photosynthesis following sunrise (Lange et al., 1970a). With a
frequency of dew condensation of 198 nights per year, the annual increase in lichen
biomass is 5-10% (Lange et al., 1975). Similar calculations have been made for Caloplaca aurantia in the same habitat (Lange & Evenari, 1971).
Although field physiological data is not available for lichens in true coastal fog
deserts, a considerable amount of data has been compiled on laboratory experiments
with a group of Baja California species (Rundel & Lange, unpublished data). These
studies reveal both similarities and differences from patterns observed in the Negev
Desert.
Unlike other desert lichens, desert fog zone taxa frequently experience thallus
moisture saturation lasting for several days. While Niebla maciformis, rarely saturated
in the Negev, exhibits no decline in rate of photosynthetic assimilation with increasing
moisture content (Lange et al., 1975), a pattern of rapid drop in assimilation rate is
characteristic of typical fog zone taxa. Niebla maciformis has no decline in assimilation
at 10 or 20'C while the sand form of Niebla homalea has a sharp decline at both
temperatures. The saxicolous form of N. homalea, zoned higher and further from the
ocean along the coast of Baja California, has no decline in assimilation at 100 but a
sharp decline at 20'C. The observed gradient in water relations response is contrary
to what might be expected since the greatest pattern of decline in assimilation with
approaching saturation is associated with the greatest frequency of saturation conditions from fogs. The gradient can be explained hypothetically, however, by patterns

289

RUNDEL: DESERT FOG ZONE LICHENS

1978]

DENDROGRAPHALEUCOPHAEA

0.3-

0.1---------

0
CO2 FIXATION
(mg CO2gd-wt.:
h -I)
-0.I

-----

---------

45000
lux
-0.3

9000

lux

-0.5
1900 lux

dark
5

10

T5

20
Temperature (C)

25

30

FIGURE 4. Photosynthetic response to temperature and light intensity in saturatedthalli of


Dendrographa leucophaea Tuck. Darb. Points are mean values for four thalli.

of cortical thickness. Thick cortices, an important adaptation in lichens subject to


frequent high winds (Ahmadjian, 1970; Rundel, unpublished data), swell tightly when
saturated with moisture, restricting gas exchange to the algal layer. Cortices are thickest in the exposed sand populations of Niebla homalea, intermediate in the less exposed rock form of this species and relatively thin in N. maciformis.
Patterns of photosynthetic response at thallus saturation are shown for Dendrographa leucophaea in Figure 4. At light intensities above 9000 lux (350 E m-2 s-1)
maximal CO2 assimilation occurs at a relatively cool 10'C. This maximal rate is approximately 30% of the maximal value at optimal thallus water content. Other fog
desert lichens in Baja California have saturation values 30-50% of optimal water content levels (Rundel & Lange, unpublished data; Nash et al., 1977). Above 23?C, no
net positive CO2 assimilation occurs.
Physiological tolerances to high salinities are important adaptations in coastal lichens subject to salt spray or windborne aerosol salts. Follmann (1967a) described
heavy salt encrustations on coastal lichens in central Chile and speculated that hydrophilic salt crusts may improve the water relations of these lichens by forming a favorable water potential gradient for uptake of moisture. Although published data by
Follmann (1967a; 1967b) are difficult to interpret because of unrealistic time axes, the
phenomenon he describes appears to be true.

290

[Volume 81

THE BRYOLOGIST

80-

Dendrographo leucophaea - salt crust

70

60
Nieblo

homalea - salt crust

50
Thallus

Moisture
Content
(%drywt.)

leucophoeo

ContueDendrogropho
4Nieblo

40

homaleo

30

20

10

10

14

18
Time

22
(hours)

26

30

34

38

42

FIGURE5. Water uptake by salt-encrusted and non-encrusted thalli of Dendrographa leucophaea Tuck. Darb. and Niebla homatea Ach. Rund. & Bowl. Points are mean value for four
thalli.
Comparative data for moisture uptake of air dry thalli previously saturated with
salt water and with deionized water are shown in Figure 5 for two species of lichens
from Baja California. In Niebla homalea (sand form) saturation at 100% relative humidity is reached at a water content of 40% of dry weight in thalli without a salt crust.

1978]

RUNDEL: DESERT FOG ZONE LICHENS

291

When a crust is present, saturation moisture content is nearly 60%. In Dendrographa


leucophaea salt crusts increase the saturation moisture content from 45% to 75%.
Experiments investigating the physiological tolerance of lichens to high osmotic
potential have shown that coastal lichens are favorably adapted to maintaining high
rates of photosynthesis under considerable osmotic stress (Rundel & Lange, unpublished data). The maximal photosynthetic rate of Dendrographa leucophaea over a
drying curve at 20'C and 45,000 lux (1900 pE m-2 s-1) is unaffected by saturation in
sea water or 2 M NaCl (-98 bars) even with original saturation of 4 M NaCl (-252
bars), photosynthesis rates are 30% of maximal values of thalli treated with deionized
water. Reduced levels of maximal photosynthesis rates occur in drying curves for sea
water saturated thalli of Niebla homalea and N. josecuervoi and amount to 50-90% of
normal values. Although the physiological tolerance of coastal zone lichens is highly
adapted, lichens in general appear to have a genetic pre-adaptation of osmotic stress
tolerance. Even Ramalina fraxinea and Lobaria pulmonaria, characteristic of environments free of salt encrustations, have positive rates of photosynthetic assimilation
at osmotic potentials in excess of -370 bars (Rundel & Lange, unpublished data).
LITERATURE CITED
AHMADJIAN,V. 1970. Adaptations of Antarctic terrestrial plants. In: M. W. Holgate (ed.), Antarctic Ecology. Vol. 2. New York.
. 1973. Resynthesis of lichens. In: V. Ahmadjian and M. E. Hale (eds.), The Lichens.
New York.
BLUM, O. B. 1965. Rate of water reserve consumption in fruticose and foliate lichens of mesoand xerotic habitats. Ukr. Bot. Zh. 22: 26-34.
. 1973. Water relations. In: V. Ahmadjian and M. E. Hale (eds.), The Lichens. New York.
BORNMAN, C. H., C. E. J. BOTHA & L. J. NASH. 1973. Welwitschia mirabilis: Observations on
movement of water and assimilates under f6hn and fog conditions. Madoqua, Ser. II, 2: 2531.
BOWLER,P. A. & P. W. RUNDEL. 1975. Reproductive strategies in lichens. Bot. Jour. Linn. Soc.,
London. 70: 325-340.
CANNON, W. A. 1924. General and physiological features of the vegetation of the more arid
portions of southern Africa, with notes on the climatic and environment. Carnegie Inst. Wash.

Publ. 354.

DI CASTRI, F. & E. HAJEK. 1976. Bioclimatologia

de Chile. Univ. Catolica de Santiago.


DODGE, C. W. 1936. Lichens of the G. Allan Hancock Expedition of 1934, collected by Wm. R.
Taylor. Hancock Pacific Expeditions 3: 33-46.
. 1965. Lichens. Monogr. Biol. 15: 194-200.
H. 1959. Oiber den Wasserhaushalt tropischer Nebeloasen an der Kiistenwiiste
ELLENBERG,
Perus. Ber. Geobot. Forsch. Inst. Riibel 1958: 47-74.
FAUREL, L., P. OZENDA & G. SCHOTTER. 1953. Les lichens du Sahara algerien. Res. Counc.
Isr. Spec. Publ. 2: 310-317.
FOLLMANN,G. 1960. Ein dornbewohnende Flechtengesellschaft der zentralchilenischen Sukkulenten formationen mit kennzeichnender Chrysothrix noli-tangere Mont. Ber. Deut. Bot.
Ges. 73: 449-462.
1965. Fersterflechten in der Atacamawiiste. Naturwissenschaften 52: 434-435.
. 1967a. Zur Bedeutung der Salzbestliubung fiir den Wasserhaushalt von Kiistenflechten.
Ber. Deut. Bot. Ges. 80: 206-208.
1967b. F6rdern Salzkrusten die Wasseraufnahme von kiistenflechten? Umschau Wiss.
Tech. 13: 420.
. 1967c. Die Flechtenflora der nordchilenischen Nebeloase Cerro Moreno. Nova Hedwigia 14: 215-281.
& J. REDON. 1972. Ergaenzungen zur Flechtenflora der nordchilenischen Nebeloasen
Fray Jorge und Talinay. Willdenowia 6: 431-459.
FRITSCH, F. E. 1948. The structure and reproduction of the algae. Vol. I. Cambridge Univ.
Press.
GALUN, M. 1963. Autecological and synecological observations on lichens of the Negev, Israel.
Isr. Jour. Bot. 12: 179-187.

292

THE BRYOLOGIST

[Volume 81

. 1970. The Lichens of Israel. Israel Acad. Sci. Hum., Jerusalem. 116 p.
GANNUTZ,T. P. 1970. Photosynthesis and respiration of plants in the Antarctic peninsula area.
Antarctic Jour. 5: 49-51.
GEITLER, L. 1923. Studien iiber das Hamatochrom und die Chromatophoren von Trentepohlia.
Osterr. Bot. Zeitschr. 73: 76-83.
GIESS, W. 1962. Some notes on the vegetation of the Namib Desert. Cimbebasia, Windhoek,
No. 2.
-. 1968. A short report on the vegetation of the Namib coastal area from Swakopmund to
Cape Frio. Dinteria 1: 13-29.
HAJEK,E. & F. DI CASTRI. 1975. Bioclimatograffa de Chile. Univ. Catolica de Santiago.
HASTINGS, J. R. 1964. Climatological data for Baja California. Tech. Rep. on Meteorology and
Climatology of Arid Regions. No. 14. Univ. Ariz. Inst. Atm. Physics.
& R. R. HUMPHREY. 1969. Climatological data and statistics for Baja California. No. 18.
Univ. Ariz. Inst. Atm. Physics.
HiRISSET, A. 1946. Demonstration expierimental du r8le du Trentepohlia umbrina (Kg.) Born.
dans la synthese des Graphidees corticoles. C. R. Acad. Sci. 222: 100-102.
HOWLAND, L. J. 1929. Periodic observations of Trentepohlia aurea Martinus. Ann. Bot. 43: 173202.
JOHNSTON,I. M. 1929. Papers on the Flora of Northern Chile. Contr. Gray Herb. 85: 1-171.
KAPPEN, L. 1973. Response to extreme environment. In: V. Ahmadjian and M. E. Hale (eds.),
The Lichens. New York.
, O. L. LANGE, E.-D. SCHULZE,M. EVENARI& U. BUSCHBOM. 1975. Primary production
of lower plants (lichens) in the desert and its physiological basis. In: P. J. Cooper (ed.),
Photosynthesis and Productivity in Different Environments. London.
KOEPCKE,H. W. 1961. Synokologische Studien an der Westseite der peruanischen Anden.
Bonn. Geogr. Abh. No. 29.
LANGE, O. L. 1969. Experimentell-bkologische
Untersuchungen an Flechten der Negev-Wiiste.
I. CO2-Gaswechsel von Ramalina maciformis (Del.) Bory unter kontrollierten Bedingungen
im Laboratorium. Flora 158: 324-359.
& M. EVENARI. 1971. Experimentell-6kologische
Untersuchungen an Flechten der Negev-Wiiste. IV. Wachstumsmessungen an Caloplaca aurantia (Pers.) Hellb. Flora 160: 100104.
& L. KAPPEN. 1972. Photosynthesis of lichens from Antarctica. Antarctic Research Series
(G. A. Llano, ed.). 20: 83-95.
- , E.-D. SCHULZE, L. KAPPEN, U. BUSCHBOM& M. EVENARI. 1975. Adaptations of desert
lichens to drought and extreme temperatures. In: N. F. Hadley (ed.), Environmental Physiology of Desert Organisms. Stroudsberg, Penn.
- , E.-D. SCHULZE& W. KOCH. 1970a. Experimentell-6kologische
Untersuchungen an Flechten der Negev-Wiiste. II. CO2 Gaswechsel und Wasserhaushalt von Ramalina maciformis
(Del.) Bory am natiirlichen Standort wahrend der sommerlichen Trockenperiode. Flora 159:
38-62.
Untersuchugen an
, E.-D. SCHULZE & W. KOCH. 1970b. Experimentelle-6kologische
Flechten der Negev-Wiiste. III. C02-Gaswechsel und Wasserhaushalt von Krusten- und Blattflechten an Naturlichen Standort Wahrend der sommerlichen Trockenperiode. Flora (Jena)
159: 525-538.
LARSON, D. W. & K. A. KERSHAW. 1976. Studies on lichen-dominated systems. XVIII. Morphological control of evaporation in lichens. Canad. Jour. Bot. 54: 2061-2073.
LOGAN, R. F. 1960. The Central Namib Desert, Southwest Africa. Nat. Acad. Sci. Nat. Res.
Council Publ. 758.
MEIGS, P. 1966. Geography of Coastal Deserts. Arid zone research No. 28. UNESCO, Paris.
NASH, T. H., III. 1975. Lichens of Maricopa County, Arizona. Jour. Ariz. Acad. Sci. 10: 119-125.
, G. T. NEBEKER,T. MOSER & T. REEVES. 1977. Lichen vegetational gradients in Baja
California in relation to coastal fog. Unpublished manuscript.
, S. L. WHITE & J. E. MARSH. 1977. Lichen and moss distribution and biomass in hot
desert ecosystems. THE BRYOLOGIST80: 470-479.
POELT, J. & V. WIRTH. 1968. Flechten aus dem nordbstlichen Afghanistan, gesammelt von H.
Roemer im Rahmen der Deutschen Wakhan--Expedition
1964. Mitt. Bot. Staatssammlung
Miinchen. 7: 219-261.
REDON, J. 1972. Liquenes de la regi6n de Cachagua y Zapallar, Provincia de Aconcagua, Chile.
Annal. Mus. Hist. Nat., Valparaiso 5: 105-115.

1978]

RUNDEL: DESERT FOG ZONE LICHENS

293

in das Kiistengebiet der Atacama (Chile). Bot. Jahr. 45:


340-353.
RUMNEY,G. R. 1968. Climatology and the World's Climates. New York.
RUNDEL, P. W. 1974. Water relations and morphological variation in Ramalina menziesii Tayl.
THE BRYOLOGIST77: 23-32.
. 1978. Evolutionary relationships in the Ramalina usnea complex. Lichenologist (in
press).
& P. A. BOWLER. 1974. The lichen genus Trichoramalina. THE BRYOLOGIST77: 188194.
-, & T. W. MULROY. 1972. A fog-induced lichen community from northwestern
Baja California with two new species of Desmazieria. THE BRYOLOGIST75: 501-508.
& M. MAHU. 1976. Community structure and diversity in a coastal fog desert in northern
Chile. Flora 165: 493-505.
SCHULZ, K. 1931. Die Flechtenvegetation der Mark Brandenburg. Feddes Repert. Beih. 67: 1192.
E.-D. & I. SCHULZE. 1976. Distribution and control of photosynthetic pathways in
SCHULZE,
plants growing in the Namib Desert, with special regard to Welwitschia mirabilis Hook/fil.
Madaqua 9: 5-13.
, H. ZIEGLER& W. STRICHLER.1976. Environmental control of crassulacean acid metabolism in Welwitschia mirabilis Hook. fil. in its range of natural distribution in the Namib
Desert. Oecologia 24: 323-334.
SHREVE, F. & I. L. WIGGINS. 1964. Vegetation and Flora of the Sonoran Desert. Stanford Univ.
Press.
THOMSON,J. W. & H. H. ILTIS. 1968. A fog-induced lichen community in the coastal desert of
southern Peru. THE BRYOLOGIST71: 31-34.
TROLL, C. 1932. Die tropischen Andenlander. Hdb. Geogr. Wissen. Bd. Siidamerika, 309-462.
VOGEL, S. 1955. Niedere "Fensterpflanzen" in der siidafrikanischen Wiiste. Eine 5kologische
Schilderung. Beitr. Biol. Pflanz. 31: 45-135.
WALTER, H. 1936. Die Okologischen Verhilltnisse in der Namib-Nebelwiiste
(Siidwestafrika).
Jahrb. Wiss. Bot. 84: 58-222.
. 1971. Ecology of Tropical and Subtropical Vegetation. 539 p. Edinburgh.
WEBER, W. A. 1962. Environmental modification and the taxonomy of the crustose lichens.
Svensk Bot. Tidskr. 56: 293-333.
. 1965. Hubbsia, a new genus of Roccellaceae (Lichenized Fungi) from Mexico. Svensk
Bot. Tidskr. 59: 59-64.
A. 1945. El mundo vegetal de los Andes Peruanos (Estudio fitogeografico). MinWEBERBAUER,
ist. de Agric., Lima.
ZUKAL, H. 1896. Morphologische und biologische Untersuchungen fiber Flechten. III. Abh.
Sitzungsber. Kaiserl. Akad. Wiss. Wien, Math-Natur. K1. Abt. 1 105: 197-264.
REICHE, K. 1911. Ein Friihlingsausflug