Ecological Relationships of Desert Fog Zone LichensAuthor(s): Philip W. RundelReviewed work(s):Source: The Bryologist, Vol. 81, No. 2 (Summer, 1978), pp. 277-293Published by: American Bryological and Lichenological SocietyStable URL: http://www.jstor.org/stable/3242189 .Accessed: 11/07/2012 03:21

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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 extremely favorable for lichen growth. Phylogenet- ically 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 morpholog- ical 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 at- mospheric 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 humid- ity, fog and/or dew along the coast.

Extensive coastal deserts occur in three areas of the world: the Peruvian and Chi- lean 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 north- ern 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 research was supported by NSF grants GB-40509 and DEB-75-19848. I thank Professors 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 Myco- logical 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

600woody

•• •plants

no vegetation

400 r open growth 0o of perennials

S200- cryptograms

no vegetation i~n vegetation-

FIGURE 1. Diagrammatic view 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 con- tent of air masses with subsequent cooling. Also important is the constant light south- west 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] RUNDEL: DESERT FOG ZONE LICHENS 279

TABLE 1. Climatic data for coastal stations in the Atacama Desert of Peru and Chile, Sonoran Desert on the Pacific Coast of Baja California and 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. (OS or ON) (m) (0C) (0C) (0C) (mm) Records

Atacama-Peru Lambayegue 6037' 5 22.2 22.9 8 Chiclayo 6041' 15.2 3-4 Trujillo 8005' 19 21.1 27.9 2-4 Lima 12000' 49 18.9 23.9 16.1 45.7 26 Mollendo 17058' 7 17.8 19.4 16.1 22.1 13

Atacama-Chile Arica 18028' 29 18.7 22.2 15.1 0.6 44 Iquique 20012' 515 17.9 21.2 14.1 2.1 49 Los Condores 20015' 518 15.5 19.0 10.2 0.0 7 Cerro Moreno 23029' 119 17.0 20.1 13.3 2.2 7 Taltal 25025' 39 17.4 22.0 14.5 25.1 21 Chafiaral 26020' 9 16.4 19.3 12.2 1.7 7 Caldera 27003' 28 16.1 19.7 12.9 25.8 49 La Serena 29054' 32 14.8 18.9 11.2 127.4 91

Sonoran-Baja California Isla Todos Santos 31048' 22 255.6 7 San Telmo 30058' 100 16.3 172.1 17 El Socorro 30020' 10 16.9 137.7 11 El Rosario 30004' 15 20.9 95.0 14 Vizcaino 27059' 10 18.8 79.8 10 Bahia Tortugas 27042' 5 20.3 95.8 11 Punta Abreojos 26044' 15 21.6 76.8 12 San Juanico 26016' 12 21.1 64.1 8 Bahia Magdalena 24038' 12 21.4 73.7 31 La Aguja 23059' 10 22.4 49.9 5 Todos Santos 23026' 18 22.0 169.6 30

Namib Luanda 8050' 60 24.4 27.2 21.7 322.6 59 Lobito 12013' 1 24.4 27.2 21.1 353.1 19 Mogamedes 15010' 3 21.1 25.0 16.7 53.3 21 Walvis Bay 22053' 7 17.2 22.2 11.7 22.9 20 Port Nolloth 29010' 7 13.9 18.3 9.4 58.4 64 Klaver 31043' 42 19.4 26.7 12.2

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 sub- strates. 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 tillands- ias 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 pene- tration 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

280 THE BRYOLOGIST [Volume 81

-1000 NO

0 VEGETATION

.. . .. .. .... .. .. .. .. ...:. CO PIAPOA -800

.... ................. :EULYCHNIA- . .COPIAPOA

:?.. .. . F-600

EUPHORBIA-

-

/

.EULYCHNIA

H::::::::::::: - A:::::: EUL YCH IA- PU A

-200

SOPEN COASTAL PLAIN-COPIAPOA

o-10 FIGURE 2. Diagrammatic view of vegetation zonation in the coastal fog zone at Paposo,

Atacama Province, 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 desert- sclerophyll 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 north- western coast and southern end of the peninsula. The general vegetation character- istics 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 par- ticularly 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 mod- erate 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 bio- mass 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, extending 2800 km from Luanda (8?45'S) in Angola to St. Helena Bay (32?45?S) in 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 precipi- tation 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 avail- able (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 subfo- liose 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 dis- tinct 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

TABLE 2. Occurrence of species of Roccellaceae in the coastal fog deserts of Baja California and Chile. Data from Rundel et al. (1972), Follmann (1967c), Follmann & Redon (1972) and Rundel (unpublished data).

Baja California Chile

Crustose Dirina catalinariae Hasse 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.

Dolichocarpus chilensis Sant.

Ingaderia pulcherrima Darb.

Pentagenella fragillima Darb. Reinkella parishii Hasse Reinkella lirellina Darb. Roccella babingtonii Mont. Roccella babingtonii Mont. R. fimbriata Darb. R. cervicornis Follm. R. sp. 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 indi- vidual 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 bio- mass 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 geno- types 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 Cali- fornia 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. homalea (Ach.) Rund. & Bowl. N. flaccescens (Nyl.) 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 bajacalifornica Bowl. & Rund. Ramalina chilensis Bert. 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. Trichoramalina crinita (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, Com- bea, 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 Trichora- malina 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 cor- ticolous, 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, In- gaderia, Reinkella, Dirina, Schizopelte, Opegrapha and Coenogonium, as well as in a variety of less dominant crustose genera in the Pyrenulaceae, Arthoniaceae, Ope- graphaceae and Graphidaceae. Although not well investigated, lichens with trente- pohlioid symbionts are also ecologically important in the coastal Namib (L. Kappen, pers. comm.). Within the macrolichen flora, only Ramalina, Niebla, Usnea and Het- erodermia, 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, how- ever, 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] RUNDEL: DESERT FOG ZONE LICHENS 285

TABLE 4. Relative growth-form distribution of warm desert lichen floras.

Lichen Growth-Form (%)

Number of Crustose & Species Fruticose Foliose squamulose

Interior Desert Algerian Sahara Desert 114 0 2 98

(Faurel et al., 1953) Negev Desert, Israel 44 5 2 93

(Galun, 1970) Sonoran Desert

Rock Valley, California 17 0 12 88 (Nash et al., 1977)

Silverbell, Arizona 21 0 19 81 (Nash et al., 1977)

Maricopa Co., Arizona 78 0 28 72 (Nash, 1975)

Chihuahuan Desert Jornada, New Mexico 48 0 40 60

(Nash et al., 1977) Coastal Fog Desert

Baja California, Mexico 67 54 13 33 (Rundel & Nash, unpublished data)

Cerro Moreno, Atacama 146 25 14 60 Prov., Chile

(Follmann, 1967b)

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 sym- bionts, there is some speculation that many of these species may be sensitive to cold temperatures (Kappen, 1973). The geographic distribution of macrolichens with Tren- tepohlia 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 re- productive characteristics. It commonly reproduces vegetatively by wind-blown frag- ments, 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 Trente- pohlia 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 environ- ments include: 1. increased cortical thickness under conditions of high light intensity (Vogel, 1955; Galun, 1963; Follmann, 1965; Poelt & Wirth, 1968); 2. increased prui- nosity 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 dam- age 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 per- centage 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 atmos- pheric 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 slow-

ly, losing it through desiccation (Zukal, 1896; Galun, 1963; Follmann, 1965). Blum (1965, 1973), however, rejected the significance of xeromorphic adaptations for pro- tection against evaporation. Experimental studies with arctic and subarctic lichens have clearly established that morphological characteristics may profoundly affect thal- lus 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 growth- forms 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 Lec- anora 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. Char- acteristically, 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 287

IsUs ng3~-

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

....... 7 .. ..... ..

hL

FIGURE 3. Lichen diversity on spines of Eulychnia iquiquensis at Paposo.

288 THE BRYOLOGIST [Volume 81

growth forms increase in importance. Total biomass of lichens in such areas is rela- tively low, however (Kappen et al., 1975; Nash et al., 1977).

Many individual morphological characteristics of lichen thalli may also be impor- tant in water relations. Cilia frequently occur in taxa of desert fog zone lichens (e.g. Heterodermia, Parmelia, Trichoramalina, Tornabenia). Although definitive experi- ments 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. Measure- ments of CO2 exchange of lichens in natural habitats in the Negev Desert have dem- onstrated 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 Cal- oplaca 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 condi- tions from fogs. The gradient can be explained hypothetically, however, by patterns

1978] RUNDEL: DESERT FOG ZONE LICHENS 289

0.3- DENDROGRAPHA LEU C OPHAEA

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 25 30 Temperature (C)

FIGURE 4. Photosynthetic response to temperature and light intensity in saturated thalli 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 thick- est in the exposed sand populations of Niebla homalea, intermediate in the less ex- posed rock form of this species and relatively thin in N. maciformis.

Patterns of photosynthetic response at thallus saturation are shown for Dendro-

grapha 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 ap- proximately 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 con- tent 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 li- chens subject to salt spray or windborne aerosol salts. Follmann (1967a) described heavy salt encrustations on coastal lichens in central Chile and speculated that hydro- philic salt crusts may improve the water relations of these lichens by forming a fa- vorable 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 THE BRYOLOGIST [Volume 81

80- Dendrographo leucophaea - salt crust

70

60

Nieblo homalea - salt crust

50

Thallus Moisture

ContueDendrogropho leucophoeo

Content (% dry wt.)

4Nieblo homaleo 40

30

20

10

2 6 10 14 18 22 26 30 34 38 42 Time (hours)

FIGURE 5. Water uptake by salt-encrusted and non-encrusted thalli of Dendrographa leu- cophaea 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 hu- midity 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, unpub- lished 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 envi- ronments 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.), Ant- arctic 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 meso- and 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: 25- 31.

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.

ELLENBERG, H. 1959. Oiber den Wasserhaushalt tropischer Nebeloasen an der Kiistenwiiste 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 Suk- kulenten 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 Hed-

wigia 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: 173-

202. 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 Ne- gev-Wiiste. IV. Wachstumsmessungen an Caloplaca aurantia (Pers.) Hellb. Flora 160: 100- 104.

- & 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 Physi- ology of Desert Organisms. Stroudsberg, Penn. - , E.-D. SCHULZE & W. KOCH. 1970a. Experimentell-6kologische Untersuchungen an Fle- chten der Negev-Wiiste. II. CO2 Gaswechsel und Wasserhaushalt von Ramalina maciformis (Del.) Bory am natiirlichen Standort wahrend der sommerlichen Trockenperiode. Flora 159: 38-62.

, E.-D. SCHULZE & W. KOCH. 1970b. Experimentelle-6kologische Untersuchugen an Flechten der Negev-Wiiste. III. C02-Gaswechsel und Wasserhaushalt von Krusten- und Blatt- flechten 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. Mor- phological 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 BRYOLOGIST 80: 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

REICHE, K. 1911. Ein Friihlingsausflug 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 BRYOLOGIST 77: 23-32. . 1978. Evolutionary relationships in the Ramalina usnea complex. Lichenologist (in

press). & P. A. BOWLER. 1974. The lichen genus Trichoramalina. THE BRYOLOGIST 77: 188-

194. - , - & T. W. MULROY. 1972. A fog-induced lichen community from northwestern

Baja California with two new species of Desmazieria. THE BRYOLOGIST 75: 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: 1- 192.

SCHULZE, E.-D. & I. SCHULZE. 1976. Distribution and control of photosynthetic pathways in 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 metab- olism 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 BRYOLOGIST 71: 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.

WEBERBAUER, A. 1945. El mundo vegetal de los Andes Peruanos (Estudio fitogeografico). Min- 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.