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Colonization by lichens and the development of lichen-dominated communities in the maritime Antarctic
Lichenologiit
27(6): 473-483
(1995)
COLONIZATION BY LICHENS AND THE DEVELOPMENT OF LICHEN-DOMINATED COMMUNITIES IN THE MARITIME ANTARCTIC R. I. LEWIS
SMITH*
Abstract: Three long-term studies of lichen growth and colonization have been undertaken at Signy Island, South Orkney Islands, in the maritime Antarctic. Small individual thalli of several crustose species and uncolonized plots on 12 fresh rock surfaces were photographically monitored at intervals of 3-4 years over a period of up to 20 years. The development of Ochrolechiafi’da colonies on a regenerating moss bank, recently uncovered by a receding glacier, was similarly monitored. The results indicate that many lichens growing in sites enriched by nitrogenous compounds derived from populations of sea birds, have relatively rapid colonization and growth rates. Mean percentage increase in thallus area can be as high as 1532% per annum in some nitrophilous saxicolous species (e.g. Acarosporu nzacrocyclos, Xanchotia elegans and species of Buellia and Caloplaca), but as low as 0+41/o in nitrophobous species (Lecanora physciella, Lmidea sp., Rhizocarpon geographicurn). Unzbilicaria anrarcrica and Usnea anrarccica also yielded data indicating high growth rates, with colonist plants reaching several centimetres after 20 years. Colonization by mixed assemblages of lichens of new rock surfaces can attain 40->90% cover after 20 years in nutrient-enriched sites, and even 20-25% in non-biotically influenced sites. Colonization by or increase in extant 0. frigida on the regenerating moribund moss bank was also quite rapid. It is suggested that the exceptionally large thalli of several lichen species and the locally extensive dense lichen fellfield communities in the maritime Antarctic may be much younger than previously supposed. 0 1995 The British Lichen Society
Introduction Under the prevailing climate, climax vegetation in Antarctica proceeds beyond solely cryptogamic communities only where one or both of the native phanerogams Colobanthus quite& (Kunth) Bar& and Deschampsia antarctica Desv. occur, i.e. in the maritime Antarctic (sensu Smith 1984). In dry, wind-exposed lithic habitats ranging from cliff faces to gravel, lichens predominate. In the milder wetter maritime Antarctic, lichens. develop locally extensive, dense and relatively complex communities occasionally covering several hectares of rocky or stony terrain. Several of these communities are multi-layered with the macrolichens (notably the fruticose genera Bryoria, Himantormia, Ramalina and Usnea, and the umbilicate foliose genus Umbilicari~) forming a canopy over a diverse understorey of filamentous fruticose taxa (Pseudephebe), foliose taxa (Parmelia, Physcia, Rhizoplaca, Xanthoria) and crustose and stipitate taxa (Buellia, Caloplaca, Candelariella, Lecanora, Lecidea, Ochrolechia, Pertusaria, Rhizocarpon, and many more). *British Antarctic Cambridge CB3 0024-2829/95/060473+
Survey, Natural OET, UK. 11 $12.00/O
Environment
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Council, 0
High
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Recent revisions of the Antarctic lichen flora indicate 250-300 species (Caste110 & Nimis 1995 in press) in a land area of c. 14.5 x lo6 km’, of which less than 2% is ice-free. Of these, probably less than 25 species achieve dominance over areas of more than 25 m2. Mature (i.e. climax) communities often possess a high density of large thalli, which are generally assumed to be of great age.‘In moist sheltered rock-face communities near the coast some species reach exceptional dimensions, e.g. Byoria chalybeiformis (Ach.) Brodo & Hawksw. (45 cm in length), Umbilicaria antarctica Frey et Lamb (35 cm diam.), Usnea antarctica Du Rietz (25 cm, but a single record of 67 cm in length, Lindsay 1976), U. aurantiaco-atra (Jacq.) Bory (20 cm). Many crustose thalli may exceed 20 cm diameter, and a thallus diameter of 78 cm was recorded for Placopsis contortuplicata Lamb on a dry shaded cliff face by Smith (1972: 44). Because lichens, particularly in polar and alpine biomes, are traditionally regarded as having very slow ‘metabolic and growth rates, they are consequently considered to exhibit slow community development. As regards the lichen colonization process in Antarctica, almost nothing is known of (a) the time required to become established, or how long it takes a particular substratum to become suitable for colonization, (b) the production, viability, dissemination, longevity or developmental requirements of propagules, both sexual and asexual, (c) the rate of growth of individual species or of the rate of development of the community following the pioneer stage, and (d) the long-term effects of the current trend in increasing summer temperatures and of ultraviolet-B radiation on colonization, growth and survival. There is much speculation about the age of large lichen thalli and of mature lichen communities. The aim of this paper is to present some data from the only long-term monitoring study of lichen colonization and growth, and their development towards the formation of communities, in Antarctica. Study
sites and methods
The study has been undertaken at Signy Island, South Orkney Islands (60”43’S, 45”38’W), in the northern maritime Antarctic. Here, the climate is cold oceanic with a mean summer (DecemberFebruary) air temperature of 0.5 to 1.5”C and mean winter (May-October) temperature of - 8’C to - 12X; extreme temperatures may briefly reach 15°C and - 35°C. Cloud cover is high and precipitation frequent (400 mm rainfall equivalent) with rain often falling in summer. Growth of individual thalli on rock In 1972 T. N. Hooker undertook a detailed investigation of inna- and interseasonal radial growth in ctustose lichens on Signy Island. Between five and 12 small thalli each of 15 species (total >300 thalli) were selected for monitoring at 32 sites, all below 50 m altitude and O-500 m fiorn the coast (see Hooker 1980a). A small spot of paint was placed beside each tballus and re-marked every few years. The thalli, together with a 0.5 mm scale were photographed during dry weather (to ensure the plants were in a dehydrated state), using monochrome fihn and a macro close-up lens. The photographic monitoring has continued every 2-3 years until the present, although many of the thalli coalesced with neighbouring colonies or became eroded through die-back or abrasion and could no longer yield accurate data. For the relatively small number of thalli that were measured in this long-term study, large prints were made and the entire thallus, omitting gaps in the tissue, was carefully delineated in black ink. This method is less accurate than that used by Hooker (Hooker & Brown 1977) to measure radial growth but, because of the large number of thalli to be measured and the substantial growth that occurred over the 20 years, it was
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Development
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considered suitable for a comparative using a Seescan Solitaire image calculated.
lichen communities-Smith
assessment of area growth. analyser and the percentage
475
The area of each was determined increase with time was then
Colonization of fresh rock In 1973 T. N. Hooker established permanent quadrats on freshly prepared rock surfaces, i.e. by overturning large boulders and thoroughly cleaning the uncolonized surface of all debris. Each quadrat, of about 0.5 ma, was painted on the rock and maintained until present. Seventeen sites were chosen in the south-eastern part of the island, 1 O-l 15 m a.s.1. and 50-300 m from the coast, in locations ranging Tom strongly bird-influenced to non-biotically influenced. The quadrats were photographed, with a fme scale, at 2-3 yearly intervals, and the total area of all lichen thalli determined from large prints using the image analysis technique described above. The percentage increase in area with time was then calculated. Colonization of a re-exposed moss bank by Ochrolechia &&da This study was conducted on a small (c. 25 m*), shallow (20-25 cm), gently sloping (c. 5’) Chorirodonrium aciphyllum (Hook. f. et Wils.) Broth. turfon a quartz-mica-schist outcrop at about 85 m a.s.1. on the eastern margin of the receding McLeod Glacier, south of Khyber Pass. The site was not influenced by birds, but was situated about 0.9 km from the nearest penguin colonies at Gourlay Peninsula. When the study was initiated in 1977 by the author, the lower portion was eroded peat still emerging from the ice while the upper part, about 6 m uphill and 1 m vertically above it, remained as healthy live moss. Two radiocarbon dates obtained for the eroded moribund moss surface were 1715 and 1875, indicating that the glacier had expanded over part of the outcrop during the ‘Little Ice Age’. The glacier in this area began thinning in the early 1970s and by 1992 the moss/peat bank was 3 m above the level of the surrounding glacier. There was a gradient from top to bottom commencing with over 80% live moss and about 10% OchroZechiafrz&du (SW.) Lynge at the top, decreasing to 25% moss, 5% lichen and increasing cover of black cyanobacteria, then zones of cyanobacteria, pale green unicellular algae and light grey colonies of crustose lichen in the early stage of development, and finally no visible microbiota on the dead moss and eroded peat. Colour photographs were taken at 3-4 yearly intervals and the total area of 0. frigida determined from large prints using the image analyser method.
Results Growth
of individual
thalli
A detailed account of radial growth in the lichen thalli after 5 years was reported by Hooker (1980a), using a precise photographic technique (Hooker & Brown 1977; Hooker 1980b). In the present study the percentage increase in growth of selected thalli after up to 18 years is given in Table 1. It is immediately clear that several nitrophilous species (e.g. Acarospora macrocyclos, Buellia species, Caloplaca species, Xanthoria elegans), growing in areas subjected to aerosol deposition of nitrogenous compounds from nearby penguin rookeries or other seabirds, have considerably higher growth rates than more nitrophobous species (e.g. Lecanora physciella, Lecidea sp., Rhizocalpon geographicum) growing in areas not subjected to such biotic influence. After many years several of the monitored thalli had merged with or were inhibited by neighbouring thalli, some of which had become established after the experiment commenced. Some of the thalli began to lose material by erosion as they aged, while a very few appeared to be grazed by mites. Photographs taken in different years of one thallus of Caloplaca millegrana always had the common mite Alaskozetes antarcticus Michael visible in the
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476 TABLE
1. Mean
dnnual
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LICHENOLOGIST
percenrage
increase in thallus
area ajier up to 18 years*
Number
Species
I
Acarospora macrocyclos Vain. Buellia lacemarginara Darb. Caloplaca cirrochrooides (Vain.) Zahlbr. Caloplaca millegrana (Mull. Arg.) Zahlbr. Lecanora physciella (Darb.) Hertel or Lecidea Rhizocarpon geographicum (L.) DC. Xanrhoria elegant (Link) Th. Fr. or Caloplaca lucens (Nyl.) Zahlbr. Umbilicank antarctica Frey et Lamb *Due *NM
Originally marked
sp.
of thalli Measured
10 22 34 31 28 63
5 8 6 6 6 10
51 NW
8 3
Mean annual % increase (+SD) 18 32 17 14 4 0.4
(3.0) (3.2) (4.5) (4.2) (1.5) (0.2)
21 (2.6) 39 (4.6)
to coalescence, final measurements for some thalli were made after less than 18 years. Not marked, but adjacent to marked crustose thalli and present in photographs.
successively increasing gaps within the thallus. In several species, especially of Buellia, it is possible to follow the development of apothecia, although the production of spores was not investigated. Colonization of fi-esh rock Of the 17 initial sites, 12 yielded results (Fig. 1). Four sites (3, 4, 5, 7) were adjacent to penguin rookeries and were continuously affected by trampling and guano deposition so that no colonization was possible. One site (15), on a massive boulder on the ice-cored lateral moraine flanking Orwell Glacier, was displaced after about 10 years by melting and ended upside-down at the foot of the moraine. Of the remaining sites, all showed extensive colonization by numerous lichens. Surprisingly, moss colonization was almost negligible. The maximum cover afforded by all colonizing lichens at each site after 20 years is given in Table 2. While direct biotic influence inhibited colonization, in general, there was significantly greater lichen development on those rocks moderately influenced by aerosol deposition of ornithogenic nitrogenous compounds than on rocks only slightly or not affected by birds. Thus, at Site 6 (Fig. lA), which was on a high outcrop within a penguin (Pygoscelis spp.) colony and occasionally affected directly by the passage of birds, visible colonization did not commence until after about 10 years, and achieved only 4% lichen cover after 20 years (mainly Caloplaca cf. millegrana and an unidentified grey crustose species). However, where direct bird influence was not severe, colonization by numerous omithocoprophilic species was rapid. Sites 13, 2 and 1 (Fig. 1A) lay progressively downwind of the large concentration of penguin colonies on Gourlay Peninsula, from which they derived considerable aerosol nutrient deposition. They were also frequently used as perches by brown skuas (Catharacta liinnbergii Matthews). There was a decline in the rate of lichen colonization along this gradient, the effect being least at Site 1. Lichens were fnst visible after 7 years (up to 3% cover at Site 13) and by 20 years had reached 94% at Site 13, 54% at Site 2 and 42% at
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604020
-
0 100 (B)
$i $ 0 @
6040-
100 (Cl 80 -
!ii 0g e
60
Site
11
40 20
t 1980
1983
1986
1989
1991
1993
Year FIG.
lA-C.
Colonization
of fresh rock surfaces 20 years. See Table
by lichens on Signy 2 for site details.
Site 1 (mainly, in order of abundance, Acarospora aspidophora and species of Buellia and Caloplaca).
Island
over
macrocyclos,
a period
of
Rhizoplaca
Site 10 (Fig. 1B) was in a sheltered gully close to several Wilson’s petrel nests and to colonies of cliff-breeding snow petrels
(Oceanites oceanicus Kti)
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THE TABLE
Site number
2 6 8 9 10 11 12 13 14 16 17
2. Percentage
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coral lichen cover at 12 sites after 20 years Distance from shore (ml
Location Lenton Point Lenton Point Pageant Point Observation Bluff Observation Bluff Factory Cove Observation Bluff Observation Bluff Tilbrook Hill Orwell Moraine Pageant Point Orwell Moraine
LICHENOLOGIST
(east) (west) (central) (central)
75 100 75 200 100 50 200 200 300 300 75 75
Altitude 6-4 15 10 30 100 115 10 90 90 50 15 30 10
(year
0~0%
Biotic influence*
cover) Total lichen cover after 20 years (%)
M M St N N Sl N N Sl SI M-St SI
*St=strong; M=moderate; Sl=slight; N=negligible. *Reached 69% cover by 1989 but severely damaged by fur seals in later years. Sites 2, 3, 4, 7 (Pantomime Point) were destroyed by penguins; Site 15 (Orwell destroyed by a landslip.
42 54 4 46 21 89 51 40 94 23
21* 23
Moraine)
was
(Pagodroma nivea Forster) and cape petrels (Daption capense L.). About 2% lichen cover was recorded after 7 years and this had increased to 89% after 20 years (predominantly A. macrocyclos, species of Buellia and several unidentified grey and brown microlichens). Most lowland areas of Signy Island are experiencing severe impact from an annual summer influx of immature bull fur seals from sub-Antarctic South Georgia (Smith 1988; 1996). Since the mid-1970s large tracts of coastal vegetation have been either completely destroyed or damaged to some extent. Lichen communities are particularly vulnerable and this was demonstrated at Site 16 (Fig. 1B). The study plot was on the top of a rock ‘island’ in a large penguin colony, but not readily accessible to the birds. Lichen cover followed the same trend as Sites 10 and 13 until around 1989. Between 1989 and 1991 the site was invaded by fur seals and lichen cover declined sharply, due mainly to the removal of the dominant species, the foliose Turgidosculum complicatulum (Nyl.) Kohlmeyer et Kohlmeyer [syn: Mastodia tesselata (Hook. f. et Harv.) Hook f. et Harv.], the lichenized form of the very abundant green alga Prasiola ctipa (Lightf.) Meneghini. The remaining cover was afforded almost entirely by crustose taxa (Acarospora macrocyclos and species of Buellia and Caloplaca). Sites 14 and 17 (Fig. 1B) were on wind-exposed moraine below Orwell Glacier and served as occasional perches for Antarctic terns (Sterna vittata Gmelin), but received little nutrient input from the birds. Colonization was considerably slower than at Sites 1, 2 and 13. Both had very similar rates of colonization with up to 3% cover after 7 years and each achieving 23% cover after 20 years. Here the principal species were, in order of abundance, A. macrocyclos, R. aspidophora, B. latemarginata, B. anisomera, ?Lecidea sp., C. millegrana and Usnea antarctica.
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No part of Signy Island is more than about 1.5 km from the coast and, since there are many very large bird colonies and large aggregations of seals around the coast, the island receives a substantial input of nutrients (especially nitrogenous compounds) in aerosol form. Consequently, surfaces not directly affected by birds may receive indirect nutrient input from this source. The highest sites (8, 9, 11 and 12, see Fig. lC), on Observation Bluff, received virtually no direct influence from birds yet had high colonization rates. Visible colonists began to appear after 7 years and increased in cover after 20 years to around 40-50% (Sites 8, 11, 12), although Site 9 (on the exposed summit) reached only half this value. The nutrient enrichment was implied by the prominence of several nitrophilous lichens (A. macrocyclos, Caloplaca sp., R. aspidophora), but the predominant lichen was an as yet unidentified black crustose taxon. There were also numerous thalli of Usnea antarctica and occasional thalli of Umbilicaria antarctica, both of which tolerate relatively high nitrogen concentrations on rock faces close to bird colonies. In most of the monitored plots several lichen thalli reached quite substantial dimensions after 20 years, although the time taken to achieve these does not take into account the time required for the substratum to become suitable for colonization or for propagules to become lodged in favourable microhabitats. Some of the largest thalli measured included Buellia Zutemarginata (24 mm), Caloplaca millegrana (18 x 16 mm), Umbilicaria antarctica (24 x 18 mm), and Usnea antarctica (60 mm x 34 mm high). Colonization of a re-exposed moss bank by Ochrolechiafrigida Over the 16-year period of investigation the living moss and, more particularly, the cyanobacterial crust and eroded peat became progressively more heavily encrusted by thalli of Ochrokchiu frigida (Table 3). Similarly, there was a steady increase in the amount of regenerating moss. At the top of the bank, which had not been covered by ice, the lichen increased only slightly, whereas in the adjacent quadrat (2) there was a substantial increase as the lichen colonized the living moss and cyanobacterial crust, reducing these from 40 and 53% cover, respectively, to 18 and 40%. Below this the site had been covered by ice, each quadrat representing ‘zones’ of decreasing age of exposure, each being about 3 years ‘older’ than the quadrat downhill from it. Thus quadrat 3 had been exposed for about 10 years longer than quadrat 6. Quadrats 3 and 4 had almost complete cover of cyanobacteria in 1977 and this crust became abundantly colonized by Ochrolechiu. The two lowermost quadrats were colonized slowly. Quadrat 5 commenced with a grey algal-and ‘protolichen’ crust, which yielded about 12% distinctive Ochrolechiu cover after 16 years. Quadrat 6 commenced with a predominantly algal film; 16 years later this had been transformed into extensive cover of the grey algal/protolichen crust together with numerous thalli of Ochrolechia. It is not clear if the protolichen crust is an early stage of this species. Discussion Several recent physiological investigations of lichens in this region have shown that many species have very low temperature and solar u-radiance optima for
480
THE TABLE
3. Increase
Distance from top of site (m)
1
2 3 4 5 6
I
in percentage
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LICHENOLOGIST cover of Ochrolechia
fiigida
on a re-exposed
moss bank
1977
1981
1985
1989
1993
Increase over 16 years
11 7 3 1 1 0
12 12 4 2 2 1
14 20 8 4 3 2
16 28 16 8 5 6
18 39 26 15 12 17
7 32 23 14 11 17
photosynthesis (Kappen & Redon 1987; Kappen et al. 1986, 1987, 1988, 1990). However, so far no attempt has been made to relate carbon fixation and dry weight production to increase in thallus size. Similarly, virtually nothing is known about the process of lichen colonization because, as pointed out by Kappen (1993: 440) ‘We do not know the kinds and numbers of lichen propagules that arrive on barren ground in Antarctica or how long it takes a lichen vegetation to become established’. The present study covers the longest period of monitoring lichen growth and colonization within the Antarctic. However, Sancho & Valladares (1993) have undertaken a detailed investigation of lichen colonization of a moraine system approximately 34 years after it became exposed by a receding glacier on Livingston Island, South Shetland Islands. The results of the present study have been derived horn three separate investigations, although it is appreciated that in two of these there was no replication of monitored plots. Nonetheless, they revealed that in the maritime Antarctic many lichens have a relatively rapid rate of development, particularly in biotically influenced habitats close to the coast. Consequently, some coastal lichen-dominated communities have been shown to develop rather quickly, reaching the climax stage, i.e. maximal cover with minimal change in species composition, within about 30 years. This has been confirmed by Usnea antarctica colonizing accumulations of pebbles in abandoned giant petrel (Macronectes gzganteus Gmelin) nests after a period of only about 10 years, and becoming dense lichen-dominated fellfield after a further 20 years (Smith 1990). Lindsay (1978) suggested that the process from initial colonization of a fresh substratum to a climax Andreaea-Usnea fellfield community probably takes 200 years or more, while in more extreme environments it could take much longer. However, more montane or nitrophobous lichens have very slow rates of colonization and growth (as evidenced particularly by Rhizocapon geographicurn). None of this category of lichens had colonized the fresh rock surfaces after 20 years. It is postulated that such species probably take from many decades to several centuries to develop a climax community. Lindsay (1973) calculated that R. geographicurn on Signy Island had a radial growth rate of 0.08 mm year- ‘, while Hooker (1977, 1980a) obtained half that rate. However, Sancho & Valladares (1993), using a lichenometric technique based on the largest thalli found on known-age rock surfaces, estimated the annual radial growth rate of this species to be 0.34 mm year - ‘. In the present study
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the mean radial growth of R. geographicum was 0.025 mm year- ‘, which, Sancho & Valladares (1993) imply, may have been inhibited by competition from neighbouring lichens. A lo-cm-diam. thallus, which is not uncommon but usually has an irregular outline and may therefore include daughter thalli, could in theory be 2000 years old. Conversely, however, some of the nitrophilous species monitored in this study (e.g. Acarospora macrocyclos, Buellia spp., Xanthoria elegans), with radial growth rates of up to 1.0-l -2 mm reach this size after only 40-50 years. Similarly, year - ’ could, potentially, some of the thalli of Umbilicaria antarctica and Usnea antarctica, developed from colonizing propagules, reached dimensions of several cm after 20 years. In all these examples, nothing is known of the length of time it takes the substratum to become suitably weathered for the propagule to become trapped and commence development. It is assumed that, from the few examples monitored in this study, most Antarctic macrolichens become established from vegetative propagules (e.g. soredia, isidia, thallus fragments), which already possess both symbionts, whereas many microlichens may rely on spores. This assumption is based on the fact that few macrolichens reproduce sexually while a large proportion of the crustose forms do. In their investigation of lichen colonization of recent moraines on Livingston Island, Sancho & Valladares (1993: 23 1) comment that ‘it is remarkable that all crustose lichens studied [14 taxa] lacked asexual propagules while possessing abundant apothecia . . . Sexual reproduction, thus, seems to be clearly involved in the primary colonization of the Antarctic moraines . . .’ Various authors have commented on the reproductive biology of colonizing saxicolous lichens, stating that, in stressful habitats, they are predominantly sexually reproducing species (e.g. Topham 1977; Fahselt et al. 1989), although new niches are commonly exploited rapidly by vegetatively reproducing species (Bowler & Rundel 1975; Awasthi 1983; Ott 1987). This study has shown that lichen colonization and growth in the maritime Antarctic environment can proceed relatively rapidly, at least in the favourable conditions experienced near sea-level and in habitats influenced by seabirds. However, in inland and upland sites in the maritime Antarctic, and virtually all situations in continental Antarctica, growth and development are exceedingly slow and metabolic rates low. This is in keeping with lichen establishment in the high Arctic, where Fahselt et al. (1988) found that the onset of colonization on bare rock surfaces took about 80 years. In the maritime Antarctic colonization of recently exposed moraine debris is very much quicker (e.g. Hooker 1977; Birkenmajer 1980; Sancho & Valladares 1993). Evidence from the present study of colonization of fresh rock surfaces suggests that (a) the substratum is very quickly rendered suitable for spore (or asexual propagule) entrapment, (b) hyphal foraging from the germinating spore for the appropriate algal symbiont (usually Trebouxia) is both rapid and successful, or (c) the alga may already be an integral component of the spore at the time of its release from the ascus, although genera exhibiting this phenomenon are believed to be scarce in the Antarctic. Colonization and community development in the coastal lowlands of the maritime Antarctic appear to be relatively rapid processes, and it seems probable that many large thalli may, in fact, be relatively young, at least for crustose taxa. Once a community has reached the
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climax stage (i.e. where maximum cover has been attained) it may persist indefinitely until influenced by a catastrophic event (e.g. long-term burial by ice, erosion, expansion of seal or sea bird populations (see Smith 1988, 1990), human impact, etc.). Once this stage has been reached, and as long as conditions remain stable, there is no evidence that the community composition changes. Most Antarctic habitat types support a specific assemblage of species (bryophytes, lichens, algae and various combinations of these depending on habitat conditions) of which only one or two usually become dominant. Once dominance is achieved after a short succession of primary and secondary colonists, it remains static unless there is a major environmental impact-and then the lichen component is generally reduced or totally removed (Smith 1972; Lindsay 1978). Ecological changes in bryophyte and phanerogam communities in the maritime Antarctic have recently been detected as a direct response to increasing summer temperatures (Smith 1993, 1994), but it is not yet known if lichen metabolic and growth rates or reproductive success are also responding positively. If they do then this may lead to more rapid colonization and growth, and greater species diversity in some communities. However, conversely, the increasing ultraviolet-B radiation resulting from the annually increasing area of ozone depletion over the maritime (and continental) Antarctic may have an inhibitory effect on growth and metabolism (or stimulate an increased production of photoprotectant pigments), while viable propagule production may decline and lead to reduced establishment and species diversity. I am especially grateful to Dr T. N. Hooker, who established the lichen growth and saxicolous lichen colonization studies in 19721973. I am indebted to the many field research assistants at Signy Island who maintained the study sites and took the photographs used in this long-term project; they were J. E. Bell, R. W. V. Anthony, S. Hutchinson, K. J. Richard, A. D. Hemmings, G. D. Cohen, D. J. Wright, H. E. MacAhster, M. G. Smithers and M. 0. Chambers. My thanks also to M. R. Worland who prepared the graphs, and to Dr D. D. Wynn-Williams who instructed me in the use of his image analyser.
REFERENCES Awasthi, D. D. (1983) Reproduction in lichens. Photontorphologv 33: 26-30. Birkenmajer, K. (1980) Lichenometric dating of glacier retreat at Admiralty Bay, King George Island (South Shetland Islands, West Antarctica). Bulletin de l’Acadt%nie Polonuke des Sciences, Sir. Sciences de la Terre 17: 77-85. Bowler, P. A. & Rundel, P. W. (1975) Reproductive strategies in lichens. BotanicalJournal ofche Linnean Society 70: 325-340. Castello, M. & Nimis, P. L. (1995) A critical revision of Antarctic lichens described by C. W. Dodge. Bibliotheca Lichenologiia 57: 71-92. Castello, M. & Nimis, P. L. (in press) Biodiversity of Antarctic lichens. In Antarctic Communities. Species, Scrucrure and Survival (B. Battaglia, G. di Prisco & D. W. H. Walton, eds). Cambridge: Cambridge University Press. Fahselt, D., Maycock, P. F. & Svboda, J. (1988) Initial establishment of saxicolous lichens following recent glacial recession in Sverdrup Pass, Ellesmere Island, Canada. Lichenologist 20: 253-268. Fahselt, D., Maycock, P. & Wong, P. Y. (1989) Reproductive modes of lichens in stressful environments in central Ellesmere Island, Canadian high Arctic. Lichenologist 21: 343-353. Hooker, T. N. (1977) The growth and physiology of Anrarcric lichens. Ph.D. Thesis, University of Bristol.
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Hooker, T. N. (1980a) Factors affecting the growth of Antarctic crustose lichens. British Antarctic Suwey Bulletin 50: 1-19. Hooker, T. N. (19806) Lobe growth and marginal zonation in crustose lichens. Lichenologisr 12: 313-323. Hooker, T. N. & Brown, D. H. (1977) A photographic method for accurately measuring growth of crustose and foliose saxicolous lichens. Lichenologist 9: 65-75. Kappen, L. (1993) Lichens in the Antarctic region. In Anrurcric Microbiology (E. I. Friedmann, ed.): 433-490. New York: Wiley-Liss. Kappen, L. & Redon, J. (1987) Photosynthesis and water relations of three maritime Antarctic lichen species. Flora 179: 215-229. Kappen, L., Bolter, M. & Kuhn, A. (1986) Field measurements of net photosynthesis of lichens in the Antarctic. Polar Biology 5: 255-258. Kappen, L., Bolter, M. & Kuhn, A. (1987) Photosynthetic activity of lichens in natural habitats in the maritime Antarctic. Bibliotheca Lichenologica 2.5: 297-3 12. Kappen, L., Meyer, M. & Bolter, M. (1988) Photosynthetic production of the lichen Ramalinu cerebrum Hook. f. et Tayl., in the maritime Antarctic. Folutforschung 58: 181-188. Kappen, L., Schroeter, B. & Sancho, L. G. (1990). Carbon-dioxide exchange of Antarctic crustose lichens in situ measured with a CO,/H,O porometer. Oecologiu 82: 311-316. Lindsay, D. C. (1973) Estimates of lichen growth in the maritime Antarctic. Arctic and Alpine Research 5: 341-346. Lindsay, D. C. (1976) An abnormal form of Usnea unrurcnca Du Rietz. British Anrurccic Survey Bulletin 44: 102-103. Lindsay, D. C. (1978) The role of lichens in Antarctic ecosystems. Byologist 81: 268-276. Ott, S. (1987) Reproductive strategies in lichens. Bibliotheca Lichenologicu 25: 81-93. Sancho, L. G. & Valladares, F. (1993) Lichen colonization of recent moraines on Livingston Island (South Shetland I., Antarctica). Polar Biology 13: 227-233. Smith, R. I. Lewis (1972) Vegetation of the South Orkney Islands with particular reference to Signy Island. British Antarctic Survey Scienttfc Repons 68: 1-124. Smith, R. I. Lewis (1984) Terrestrial plant biology of the sub-Antarctic and Antarctic. In Anrurczic Ecology (R. M. Laws, ed.): 1: 61-162. London: Academic Press. Smith, R. I. Lewis (1988) Destruction of Antarctic terrestrial ecosystems by a rapidly increasing fur seal population. Biological Consewanon 45: 55-72. Smith, R. I. Lewis (1990) Signy Island as a paradigm of biological and environmental change in Antarctic terrestrial ecosystems. In Antarctic Ecosystems. Ecological Change and Consewazion (K. R. Kerry & G. Hempel, eds): 32-50. Berlin: Springer-Verlag. Smith, R. I. Lewis (1993) The role of bryophyte propagule banks in primary succession: Case-study of an Antarctic fellfield soil. In Primuy Succession on Lund 0. Miles & D. W. H. Walton, eds): 55-78. Oxford: Blackwell Scientific Publications. Smith, R. I. Lewis (1994) Vascular plants as bioindicators of regional warming in Antarctica. Oecologiu 99: 322-328. Smith, R. I. Lewis (1996) Impact of an increasing fur seal population on Antarctic plant communities: resiliance and recovery. In Anrarcric Communities-Species, Srrucrure und Suwivul (B. Battaglia, G. di Ptisco & D. W. H. Walton, eds) Cambridge: Cambridge University Press: in press. Topham, P. B. (1977) Colonization, growth, succession and competition. In Lichen Ecology (M. R. D. Seaward, ed.): 31-68. New York: Academic Press. Accepted for publication
24 May
1995
27(6): 473-483
(1995)
COLONIZATION BY LICHENS AND THE DEVELOPMENT OF LICHEN-DOMINATED COMMUNITIES IN THE MARITIME ANTARCTIC R. I. LEWIS
SMITH*
Abstract: Three long-term studies of lichen growth and colonization have been undertaken at Signy Island, South Orkney Islands, in the maritime Antarctic. Small individual thalli of several crustose species and uncolonized plots on 12 fresh rock surfaces were photographically monitored at intervals of 3-4 years over a period of up to 20 years. The development of Ochrolechiafi’da colonies on a regenerating moss bank, recently uncovered by a receding glacier, was similarly monitored. The results indicate that many lichens growing in sites enriched by nitrogenous compounds derived from populations of sea birds, have relatively rapid colonization and growth rates. Mean percentage increase in thallus area can be as high as 1532% per annum in some nitrophilous saxicolous species (e.g. Acarosporu nzacrocyclos, Xanchotia elegans and species of Buellia and Caloplaca), but as low as 0+41/o in nitrophobous species (Lecanora physciella, Lmidea sp., Rhizocarpon geographicurn). Unzbilicaria anrarcrica and Usnea anrarccica also yielded data indicating high growth rates, with colonist plants reaching several centimetres after 20 years. Colonization by mixed assemblages of lichens of new rock surfaces can attain 40->90% cover after 20 years in nutrient-enriched sites, and even 20-25% in non-biotically influenced sites. Colonization by or increase in extant 0. frigida on the regenerating moribund moss bank was also quite rapid. It is suggested that the exceptionally large thalli of several lichen species and the locally extensive dense lichen fellfield communities in the maritime Antarctic may be much younger than previously supposed. 0 1995 The British Lichen Society
Introduction Under the prevailing climate, climax vegetation in Antarctica proceeds beyond solely cryptogamic communities only where one or both of the native phanerogams Colobanthus quite& (Kunth) Bar& and Deschampsia antarctica Desv. occur, i.e. in the maritime Antarctic (sensu Smith 1984). In dry, wind-exposed lithic habitats ranging from cliff faces to gravel, lichens predominate. In the milder wetter maritime Antarctic, lichens. develop locally extensive, dense and relatively complex communities occasionally covering several hectares of rocky or stony terrain. Several of these communities are multi-layered with the macrolichens (notably the fruticose genera Bryoria, Himantormia, Ramalina and Usnea, and the umbilicate foliose genus Umbilicari~) forming a canopy over a diverse understorey of filamentous fruticose taxa (Pseudephebe), foliose taxa (Parmelia, Physcia, Rhizoplaca, Xanthoria) and crustose and stipitate taxa (Buellia, Caloplaca, Candelariella, Lecanora, Lecidea, Ochrolechia, Pertusaria, Rhizocarpon, and many more). *British Antarctic Cambridge CB3 0024-2829/95/060473+
Survey, Natural OET, UK. 11 $12.00/O
Environment
Research
Council, 0
High
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Cross, British
Madingley
Road,
Lichen
Society
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Recent revisions of the Antarctic lichen flora indicate 250-300 species (Caste110 & Nimis 1995 in press) in a land area of c. 14.5 x lo6 km’, of which less than 2% is ice-free. Of these, probably less than 25 species achieve dominance over areas of more than 25 m2. Mature (i.e. climax) communities often possess a high density of large thalli, which are generally assumed to be of great age.‘In moist sheltered rock-face communities near the coast some species reach exceptional dimensions, e.g. Byoria chalybeiformis (Ach.) Brodo & Hawksw. (45 cm in length), Umbilicaria antarctica Frey et Lamb (35 cm diam.), Usnea antarctica Du Rietz (25 cm, but a single record of 67 cm in length, Lindsay 1976), U. aurantiaco-atra (Jacq.) Bory (20 cm). Many crustose thalli may exceed 20 cm diameter, and a thallus diameter of 78 cm was recorded for Placopsis contortuplicata Lamb on a dry shaded cliff face by Smith (1972: 44). Because lichens, particularly in polar and alpine biomes, are traditionally regarded as having very slow ‘metabolic and growth rates, they are consequently considered to exhibit slow community development. As regards the lichen colonization process in Antarctica, almost nothing is known of (a) the time required to become established, or how long it takes a particular substratum to become suitable for colonization, (b) the production, viability, dissemination, longevity or developmental requirements of propagules, both sexual and asexual, (c) the rate of growth of individual species or of the rate of development of the community following the pioneer stage, and (d) the long-term effects of the current trend in increasing summer temperatures and of ultraviolet-B radiation on colonization, growth and survival. There is much speculation about the age of large lichen thalli and of mature lichen communities. The aim of this paper is to present some data from the only long-term monitoring study of lichen colonization and growth, and their development towards the formation of communities, in Antarctica. Study
sites and methods
The study has been undertaken at Signy Island, South Orkney Islands (60”43’S, 45”38’W), in the northern maritime Antarctic. Here, the climate is cold oceanic with a mean summer (DecemberFebruary) air temperature of 0.5 to 1.5”C and mean winter (May-October) temperature of - 8’C to - 12X; extreme temperatures may briefly reach 15°C and - 35°C. Cloud cover is high and precipitation frequent (400 mm rainfall equivalent) with rain often falling in summer. Growth of individual thalli on rock In 1972 T. N. Hooker undertook a detailed investigation of inna- and interseasonal radial growth in ctustose lichens on Signy Island. Between five and 12 small thalli each of 15 species (total >300 thalli) were selected for monitoring at 32 sites, all below 50 m altitude and O-500 m fiorn the coast (see Hooker 1980a). A small spot of paint was placed beside each tballus and re-marked every few years. The thalli, together with a 0.5 mm scale were photographed during dry weather (to ensure the plants were in a dehydrated state), using monochrome fihn and a macro close-up lens. The photographic monitoring has continued every 2-3 years until the present, although many of the thalli coalesced with neighbouring colonies or became eroded through die-back or abrasion and could no longer yield accurate data. For the relatively small number of thalli that were measured in this long-term study, large prints were made and the entire thallus, omitting gaps in the tissue, was carefully delineated in black ink. This method is less accurate than that used by Hooker (Hooker & Brown 1977) to measure radial growth but, because of the large number of thalli to be measured and the substantial growth that occurred over the 20 years, it was
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Development
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considered suitable for a comparative using a Seescan Solitaire image calculated.
lichen communities-Smith
assessment of area growth. analyser and the percentage
475
The area of each was determined increase with time was then
Colonization of fresh rock In 1973 T. N. Hooker established permanent quadrats on freshly prepared rock surfaces, i.e. by overturning large boulders and thoroughly cleaning the uncolonized surface of all debris. Each quadrat, of about 0.5 ma, was painted on the rock and maintained until present. Seventeen sites were chosen in the south-eastern part of the island, 1 O-l 15 m a.s.1. and 50-300 m from the coast, in locations ranging Tom strongly bird-influenced to non-biotically influenced. The quadrats were photographed, with a fme scale, at 2-3 yearly intervals, and the total area of all lichen thalli determined from large prints using the image analysis technique described above. The percentage increase in area with time was then calculated. Colonization of a re-exposed moss bank by Ochrolechia &&da This study was conducted on a small (c. 25 m*), shallow (20-25 cm), gently sloping (c. 5’) Chorirodonrium aciphyllum (Hook. f. et Wils.) Broth. turfon a quartz-mica-schist outcrop at about 85 m a.s.1. on the eastern margin of the receding McLeod Glacier, south of Khyber Pass. The site was not influenced by birds, but was situated about 0.9 km from the nearest penguin colonies at Gourlay Peninsula. When the study was initiated in 1977 by the author, the lower portion was eroded peat still emerging from the ice while the upper part, about 6 m uphill and 1 m vertically above it, remained as healthy live moss. Two radiocarbon dates obtained for the eroded moribund moss surface were 1715 and 1875, indicating that the glacier had expanded over part of the outcrop during the ‘Little Ice Age’. The glacier in this area began thinning in the early 1970s and by 1992 the moss/peat bank was 3 m above the level of the surrounding glacier. There was a gradient from top to bottom commencing with over 80% live moss and about 10% OchroZechiafrz&du (SW.) Lynge at the top, decreasing to 25% moss, 5% lichen and increasing cover of black cyanobacteria, then zones of cyanobacteria, pale green unicellular algae and light grey colonies of crustose lichen in the early stage of development, and finally no visible microbiota on the dead moss and eroded peat. Colour photographs were taken at 3-4 yearly intervals and the total area of 0. frigida determined from large prints using the image analyser method.
Results Growth
of individual
thalli
A detailed account of radial growth in the lichen thalli after 5 years was reported by Hooker (1980a), using a precise photographic technique (Hooker & Brown 1977; Hooker 1980b). In the present study the percentage increase in growth of selected thalli after up to 18 years is given in Table 1. It is immediately clear that several nitrophilous species (e.g. Acarospora macrocyclos, Buellia species, Caloplaca species, Xanthoria elegans), growing in areas subjected to aerosol deposition of nitrogenous compounds from nearby penguin rookeries or other seabirds, have considerably higher growth rates than more nitrophobous species (e.g. Lecanora physciella, Lecidea sp., Rhizocalpon geographicum) growing in areas not subjected to such biotic influence. After many years several of the monitored thalli had merged with or were inhibited by neighbouring thalli, some of which had become established after the experiment commenced. Some of the thalli began to lose material by erosion as they aged, while a very few appeared to be grazed by mites. Photographs taken in different years of one thallus of Caloplaca millegrana always had the common mite Alaskozetes antarcticus Michael visible in the
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476 TABLE
1. Mean
dnnual
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LICHENOLOGIST
percenrage
increase in thallus
area ajier up to 18 years*
Number
Species
I
Acarospora macrocyclos Vain. Buellia lacemarginara Darb. Caloplaca cirrochrooides (Vain.) Zahlbr. Caloplaca millegrana (Mull. Arg.) Zahlbr. Lecanora physciella (Darb.) Hertel or Lecidea Rhizocarpon geographicum (L.) DC. Xanrhoria elegant (Link) Th. Fr. or Caloplaca lucens (Nyl.) Zahlbr. Umbilicank antarctica Frey et Lamb *Due *NM
Originally marked
sp.
of thalli Measured
10 22 34 31 28 63
5 8 6 6 6 10
51 NW
8 3
Mean annual % increase (+SD) 18 32 17 14 4 0.4
(3.0) (3.2) (4.5) (4.2) (1.5) (0.2)
21 (2.6) 39 (4.6)
to coalescence, final measurements for some thalli were made after less than 18 years. Not marked, but adjacent to marked crustose thalli and present in photographs.
successively increasing gaps within the thallus. In several species, especially of Buellia, it is possible to follow the development of apothecia, although the production of spores was not investigated. Colonization of fi-esh rock Of the 17 initial sites, 12 yielded results (Fig. 1). Four sites (3, 4, 5, 7) were adjacent to penguin rookeries and were continuously affected by trampling and guano deposition so that no colonization was possible. One site (15), on a massive boulder on the ice-cored lateral moraine flanking Orwell Glacier, was displaced after about 10 years by melting and ended upside-down at the foot of the moraine. Of the remaining sites, all showed extensive colonization by numerous lichens. Surprisingly, moss colonization was almost negligible. The maximum cover afforded by all colonizing lichens at each site after 20 years is given in Table 2. While direct biotic influence inhibited colonization, in general, there was significantly greater lichen development on those rocks moderately influenced by aerosol deposition of ornithogenic nitrogenous compounds than on rocks only slightly or not affected by birds. Thus, at Site 6 (Fig. lA), which was on a high outcrop within a penguin (Pygoscelis spp.) colony and occasionally affected directly by the passage of birds, visible colonization did not commence until after about 10 years, and achieved only 4% lichen cover after 20 years (mainly Caloplaca cf. millegrana and an unidentified grey crustose species). However, where direct bird influence was not severe, colonization by numerous omithocoprophilic species was rapid. Sites 13, 2 and 1 (Fig. 1A) lay progressively downwind of the large concentration of penguin colonies on Gourlay Peninsula, from which they derived considerable aerosol nutrient deposition. They were also frequently used as perches by brown skuas (Catharacta liinnbergii Matthews). There was a decline in the rate of lichen colonization along this gradient, the effect being least at Site 1. Lichens were fnst visible after 7 years (up to 3% cover at Site 13) and by 20 years had reached 94% at Site 13, 54% at Site 2 and 42% at
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604020
-
0 100 (B)
$i $ 0 @
6040-
100 (Cl 80 -
!ii 0g e
60
Site
11
40 20
t 1980
1983
1986
1989
1991
1993
Year FIG.
lA-C.
Colonization
of fresh rock surfaces 20 years. See Table
by lichens on Signy 2 for site details.
Site 1 (mainly, in order of abundance, Acarospora aspidophora and species of Buellia and Caloplaca).
Island
over
macrocyclos,
a period
of
Rhizoplaca
Site 10 (Fig. 1B) was in a sheltered gully close to several Wilson’s petrel nests and to colonies of cliff-breeding snow petrels
(Oceanites oceanicus Kti)
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THE TABLE
Site number
2 6 8 9 10 11 12 13 14 16 17
2. Percentage
Vol. 27
coral lichen cover at 12 sites after 20 years Distance from shore (ml
Location Lenton Point Lenton Point Pageant Point Observation Bluff Observation Bluff Factory Cove Observation Bluff Observation Bluff Tilbrook Hill Orwell Moraine Pageant Point Orwell Moraine
LICHENOLOGIST
(east) (west) (central) (central)
75 100 75 200 100 50 200 200 300 300 75 75
Altitude 6-4 15 10 30 100 115 10 90 90 50 15 30 10
(year
0~0%
Biotic influence*
cover) Total lichen cover after 20 years (%)
M M St N N Sl N N Sl SI M-St SI
*St=strong; M=moderate; Sl=slight; N=negligible. *Reached 69% cover by 1989 but severely damaged by fur seals in later years. Sites 2, 3, 4, 7 (Pantomime Point) were destroyed by penguins; Site 15 (Orwell destroyed by a landslip.
42 54 4 46 21 89 51 40 94 23
21* 23
Moraine)
was
(Pagodroma nivea Forster) and cape petrels (Daption capense L.). About 2% lichen cover was recorded after 7 years and this had increased to 89% after 20 years (predominantly A. macrocyclos, species of Buellia and several unidentified grey and brown microlichens). Most lowland areas of Signy Island are experiencing severe impact from an annual summer influx of immature bull fur seals from sub-Antarctic South Georgia (Smith 1988; 1996). Since the mid-1970s large tracts of coastal vegetation have been either completely destroyed or damaged to some extent. Lichen communities are particularly vulnerable and this was demonstrated at Site 16 (Fig. 1B). The study plot was on the top of a rock ‘island’ in a large penguin colony, but not readily accessible to the birds. Lichen cover followed the same trend as Sites 10 and 13 until around 1989. Between 1989 and 1991 the site was invaded by fur seals and lichen cover declined sharply, due mainly to the removal of the dominant species, the foliose Turgidosculum complicatulum (Nyl.) Kohlmeyer et Kohlmeyer [syn: Mastodia tesselata (Hook. f. et Harv.) Hook f. et Harv.], the lichenized form of the very abundant green alga Prasiola ctipa (Lightf.) Meneghini. The remaining cover was afforded almost entirely by crustose taxa (Acarospora macrocyclos and species of Buellia and Caloplaca). Sites 14 and 17 (Fig. 1B) were on wind-exposed moraine below Orwell Glacier and served as occasional perches for Antarctic terns (Sterna vittata Gmelin), but received little nutrient input from the birds. Colonization was considerably slower than at Sites 1, 2 and 13. Both had very similar rates of colonization with up to 3% cover after 7 years and each achieving 23% cover after 20 years. Here the principal species were, in order of abundance, A. macrocyclos, R. aspidophora, B. latemarginata, B. anisomera, ?Lecidea sp., C. millegrana and Usnea antarctica.
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No part of Signy Island is more than about 1.5 km from the coast and, since there are many very large bird colonies and large aggregations of seals around the coast, the island receives a substantial input of nutrients (especially nitrogenous compounds) in aerosol form. Consequently, surfaces not directly affected by birds may receive indirect nutrient input from this source. The highest sites (8, 9, 11 and 12, see Fig. lC), on Observation Bluff, received virtually no direct influence from birds yet had high colonization rates. Visible colonists began to appear after 7 years and increased in cover after 20 years to around 40-50% (Sites 8, 11, 12), although Site 9 (on the exposed summit) reached only half this value. The nutrient enrichment was implied by the prominence of several nitrophilous lichens (A. macrocyclos, Caloplaca sp., R. aspidophora), but the predominant lichen was an as yet unidentified black crustose taxon. There were also numerous thalli of Usnea antarctica and occasional thalli of Umbilicaria antarctica, both of which tolerate relatively high nitrogen concentrations on rock faces close to bird colonies. In most of the monitored plots several lichen thalli reached quite substantial dimensions after 20 years, although the time taken to achieve these does not take into account the time required for the substratum to become suitable for colonization or for propagules to become lodged in favourable microhabitats. Some of the largest thalli measured included Buellia Zutemarginata (24 mm), Caloplaca millegrana (18 x 16 mm), Umbilicaria antarctica (24 x 18 mm), and Usnea antarctica (60 mm x 34 mm high). Colonization of a re-exposed moss bank by Ochrolechiafrigida Over the 16-year period of investigation the living moss and, more particularly, the cyanobacterial crust and eroded peat became progressively more heavily encrusted by thalli of Ochrokchiu frigida (Table 3). Similarly, there was a steady increase in the amount of regenerating moss. At the top of the bank, which had not been covered by ice, the lichen increased only slightly, whereas in the adjacent quadrat (2) there was a substantial increase as the lichen colonized the living moss and cyanobacterial crust, reducing these from 40 and 53% cover, respectively, to 18 and 40%. Below this the site had been covered by ice, each quadrat representing ‘zones’ of decreasing age of exposure, each being about 3 years ‘older’ than the quadrat downhill from it. Thus quadrat 3 had been exposed for about 10 years longer than quadrat 6. Quadrats 3 and 4 had almost complete cover of cyanobacteria in 1977 and this crust became abundantly colonized by Ochrolechiu. The two lowermost quadrats were colonized slowly. Quadrat 5 commenced with a grey algal-and ‘protolichen’ crust, which yielded about 12% distinctive Ochrolechiu cover after 16 years. Quadrat 6 commenced with a predominantly algal film; 16 years later this had been transformed into extensive cover of the grey algal/protolichen crust together with numerous thalli of Ochrolechia. It is not clear if the protolichen crust is an early stage of this species. Discussion Several recent physiological investigations of lichens in this region have shown that many species have very low temperature and solar u-radiance optima for
480
THE TABLE
3. Increase
Distance from top of site (m)
1
2 3 4 5 6
I
in percentage
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LICHENOLOGIST cover of Ochrolechia
fiigida
on a re-exposed
moss bank
1977
1981
1985
1989
1993
Increase over 16 years
11 7 3 1 1 0
12 12 4 2 2 1
14 20 8 4 3 2
16 28 16 8 5 6
18 39 26 15 12 17
7 32 23 14 11 17
photosynthesis (Kappen & Redon 1987; Kappen et al. 1986, 1987, 1988, 1990). However, so far no attempt has been made to relate carbon fixation and dry weight production to increase in thallus size. Similarly, virtually nothing is known about the process of lichen colonization because, as pointed out by Kappen (1993: 440) ‘We do not know the kinds and numbers of lichen propagules that arrive on barren ground in Antarctica or how long it takes a lichen vegetation to become established’. The present study covers the longest period of monitoring lichen growth and colonization within the Antarctic. However, Sancho & Valladares (1993) have undertaken a detailed investigation of lichen colonization of a moraine system approximately 34 years after it became exposed by a receding glacier on Livingston Island, South Shetland Islands. The results of the present study have been derived horn three separate investigations, although it is appreciated that in two of these there was no replication of monitored plots. Nonetheless, they revealed that in the maritime Antarctic many lichens have a relatively rapid rate of development, particularly in biotically influenced habitats close to the coast. Consequently, some coastal lichen-dominated communities have been shown to develop rather quickly, reaching the climax stage, i.e. maximal cover with minimal change in species composition, within about 30 years. This has been confirmed by Usnea antarctica colonizing accumulations of pebbles in abandoned giant petrel (Macronectes gzganteus Gmelin) nests after a period of only about 10 years, and becoming dense lichen-dominated fellfield after a further 20 years (Smith 1990). Lindsay (1978) suggested that the process from initial colonization of a fresh substratum to a climax Andreaea-Usnea fellfield community probably takes 200 years or more, while in more extreme environments it could take much longer. However, more montane or nitrophobous lichens have very slow rates of colonization and growth (as evidenced particularly by Rhizocapon geographicurn). None of this category of lichens had colonized the fresh rock surfaces after 20 years. It is postulated that such species probably take from many decades to several centuries to develop a climax community. Lindsay (1973) calculated that R. geographicurn on Signy Island had a radial growth rate of 0.08 mm year- ‘, while Hooker (1977, 1980a) obtained half that rate. However, Sancho & Valladares (1993), using a lichenometric technique based on the largest thalli found on known-age rock surfaces, estimated the annual radial growth rate of this species to be 0.34 mm year - ‘. In the present study
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the mean radial growth of R. geographicum was 0.025 mm year- ‘, which, Sancho & Valladares (1993) imply, may have been inhibited by competition from neighbouring lichens. A lo-cm-diam. thallus, which is not uncommon but usually has an irregular outline and may therefore include daughter thalli, could in theory be 2000 years old. Conversely, however, some of the nitrophilous species monitored in this study (e.g. Acarospora macrocyclos, Buellia spp., Xanthoria elegans), with radial growth rates of up to 1.0-l -2 mm reach this size after only 40-50 years. Similarly, year - ’ could, potentially, some of the thalli of Umbilicaria antarctica and Usnea antarctica, developed from colonizing propagules, reached dimensions of several cm after 20 years. In all these examples, nothing is known of the length of time it takes the substratum to become suitably weathered for the propagule to become trapped and commence development. It is assumed that, from the few examples monitored in this study, most Antarctic macrolichens become established from vegetative propagules (e.g. soredia, isidia, thallus fragments), which already possess both symbionts, whereas many microlichens may rely on spores. This assumption is based on the fact that few macrolichens reproduce sexually while a large proportion of the crustose forms do. In their investigation of lichen colonization of recent moraines on Livingston Island, Sancho & Valladares (1993: 23 1) comment that ‘it is remarkable that all crustose lichens studied [14 taxa] lacked asexual propagules while possessing abundant apothecia . . . Sexual reproduction, thus, seems to be clearly involved in the primary colonization of the Antarctic moraines . . .’ Various authors have commented on the reproductive biology of colonizing saxicolous lichens, stating that, in stressful habitats, they are predominantly sexually reproducing species (e.g. Topham 1977; Fahselt et al. 1989), although new niches are commonly exploited rapidly by vegetatively reproducing species (Bowler & Rundel 1975; Awasthi 1983; Ott 1987). This study has shown that lichen colonization and growth in the maritime Antarctic environment can proceed relatively rapidly, at least in the favourable conditions experienced near sea-level and in habitats influenced by seabirds. However, in inland and upland sites in the maritime Antarctic, and virtually all situations in continental Antarctica, growth and development are exceedingly slow and metabolic rates low. This is in keeping with lichen establishment in the high Arctic, where Fahselt et al. (1988) found that the onset of colonization on bare rock surfaces took about 80 years. In the maritime Antarctic colonization of recently exposed moraine debris is very much quicker (e.g. Hooker 1977; Birkenmajer 1980; Sancho & Valladares 1993). Evidence from the present study of colonization of fresh rock surfaces suggests that (a) the substratum is very quickly rendered suitable for spore (or asexual propagule) entrapment, (b) hyphal foraging from the germinating spore for the appropriate algal symbiont (usually Trebouxia) is both rapid and successful, or (c) the alga may already be an integral component of the spore at the time of its release from the ascus, although genera exhibiting this phenomenon are believed to be scarce in the Antarctic. Colonization and community development in the coastal lowlands of the maritime Antarctic appear to be relatively rapid processes, and it seems probable that many large thalli may, in fact, be relatively young, at least for crustose taxa. Once a community has reached the
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climax stage (i.e. where maximum cover has been attained) it may persist indefinitely until influenced by a catastrophic event (e.g. long-term burial by ice, erosion, expansion of seal or sea bird populations (see Smith 1988, 1990), human impact, etc.). Once this stage has been reached, and as long as conditions remain stable, there is no evidence that the community composition changes. Most Antarctic habitat types support a specific assemblage of species (bryophytes, lichens, algae and various combinations of these depending on habitat conditions) of which only one or two usually become dominant. Once dominance is achieved after a short succession of primary and secondary colonists, it remains static unless there is a major environmental impact-and then the lichen component is generally reduced or totally removed (Smith 1972; Lindsay 1978). Ecological changes in bryophyte and phanerogam communities in the maritime Antarctic have recently been detected as a direct response to increasing summer temperatures (Smith 1993, 1994), but it is not yet known if lichen metabolic and growth rates or reproductive success are also responding positively. If they do then this may lead to more rapid colonization and growth, and greater species diversity in some communities. However, conversely, the increasing ultraviolet-B radiation resulting from the annually increasing area of ozone depletion over the maritime (and continental) Antarctic may have an inhibitory effect on growth and metabolism (or stimulate an increased production of photoprotectant pigments), while viable propagule production may decline and lead to reduced establishment and species diversity. I am especially grateful to Dr T. N. Hooker, who established the lichen growth and saxicolous lichen colonization studies in 19721973. I am indebted to the many field research assistants at Signy Island who maintained the study sites and took the photographs used in this long-term project; they were J. E. Bell, R. W. V. Anthony, S. Hutchinson, K. J. Richard, A. D. Hemmings, G. D. Cohen, D. J. Wright, H. E. MacAhster, M. G. Smithers and M. 0. Chambers. My thanks also to M. R. Worland who prepared the graphs, and to Dr D. D. Wynn-Williams who instructed me in the use of his image analyser.
REFERENCES Awasthi, D. D. (1983) Reproduction in lichens. Photontorphologv 33: 26-30. Birkenmajer, K. (1980) Lichenometric dating of glacier retreat at Admiralty Bay, King George Island (South Shetland Islands, West Antarctica). Bulletin de l’Acadt%nie Polonuke des Sciences, Sir. Sciences de la Terre 17: 77-85. Bowler, P. A. & Rundel, P. W. (1975) Reproductive strategies in lichens. BotanicalJournal ofche Linnean Society 70: 325-340. Castello, M. & Nimis, P. L. (1995) A critical revision of Antarctic lichens described by C. W. Dodge. Bibliotheca Lichenologiia 57: 71-92. Castello, M. & Nimis, P. L. (in press) Biodiversity of Antarctic lichens. In Antarctic Communities. Species, Scrucrure and Survival (B. Battaglia, G. di Prisco & D. W. H. Walton, eds). Cambridge: Cambridge University Press. Fahselt, D., Maycock, P. F. & Svboda, J. (1988) Initial establishment of saxicolous lichens following recent glacial recession in Sverdrup Pass, Ellesmere Island, Canada. Lichenologist 20: 253-268. Fahselt, D., Maycock, P. & Wong, P. Y. (1989) Reproductive modes of lichens in stressful environments in central Ellesmere Island, Canadian high Arctic. Lichenologist 21: 343-353. Hooker, T. N. (1977) The growth and physiology of Anrarcric lichens. Ph.D. Thesis, University of Bristol.
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Hooker, T. N. (1980a) Factors affecting the growth of Antarctic crustose lichens. British Antarctic Suwey Bulletin 50: 1-19. Hooker, T. N. (19806) Lobe growth and marginal zonation in crustose lichens. Lichenologisr 12: 313-323. Hooker, T. N. & Brown, D. H. (1977) A photographic method for accurately measuring growth of crustose and foliose saxicolous lichens. Lichenologist 9: 65-75. Kappen, L. (1993) Lichens in the Antarctic region. In Anrurcric Microbiology (E. I. Friedmann, ed.): 433-490. New York: Wiley-Liss. Kappen, L. & Redon, J. (1987) Photosynthesis and water relations of three maritime Antarctic lichen species. Flora 179: 215-229. Kappen, L., Bolter, M. & Kuhn, A. (1986) Field measurements of net photosynthesis of lichens in the Antarctic. Polar Biology 5: 255-258. Kappen, L., Bolter, M. & Kuhn, A. (1987) Photosynthetic activity of lichens in natural habitats in the maritime Antarctic. Bibliotheca Lichenologica 2.5: 297-3 12. Kappen, L., Meyer, M. & Bolter, M. (1988) Photosynthetic production of the lichen Ramalinu cerebrum Hook. f. et Tayl., in the maritime Antarctic. Folutforschung 58: 181-188. Kappen, L., Schroeter, B. & Sancho, L. G. (1990). Carbon-dioxide exchange of Antarctic crustose lichens in situ measured with a CO,/H,O porometer. Oecologiu 82: 311-316. Lindsay, D. C. (1973) Estimates of lichen growth in the maritime Antarctic. Arctic and Alpine Research 5: 341-346. Lindsay, D. C. (1976) An abnormal form of Usnea unrurcnca Du Rietz. British Anrurccic Survey Bulletin 44: 102-103. Lindsay, D. C. (1978) The role of lichens in Antarctic ecosystems. Byologist 81: 268-276. Ott, S. (1987) Reproductive strategies in lichens. Bibliotheca Lichenologicu 25: 81-93. Sancho, L. G. & Valladares, F. (1993) Lichen colonization of recent moraines on Livingston Island (South Shetland I., Antarctica). Polar Biology 13: 227-233. Smith, R. I. Lewis (1972) Vegetation of the South Orkney Islands with particular reference to Signy Island. British Antarctic Survey Scienttfc Repons 68: 1-124. Smith, R. I. Lewis (1984) Terrestrial plant biology of the sub-Antarctic and Antarctic. In Anrurczic Ecology (R. M. Laws, ed.): 1: 61-162. London: Academic Press. Smith, R. I. Lewis (1988) Destruction of Antarctic terrestrial ecosystems by a rapidly increasing fur seal population. Biological Consewanon 45: 55-72. Smith, R. I. Lewis (1990) Signy Island as a paradigm of biological and environmental change in Antarctic terrestrial ecosystems. In Antarctic Ecosystems. Ecological Change and Consewazion (K. R. Kerry & G. Hempel, eds): 32-50. Berlin: Springer-Verlag. Smith, R. I. Lewis (1993) The role of bryophyte propagule banks in primary succession: Case-study of an Antarctic fellfield soil. In Primuy Succession on Lund 0. Miles & D. W. H. Walton, eds): 55-78. Oxford: Blackwell Scientific Publications. Smith, R. I. Lewis (1994) Vascular plants as bioindicators of regional warming in Antarctica. Oecologiu 99: 322-328. Smith, R. I. Lewis (1996) Impact of an increasing fur seal population on Antarctic plant communities: resiliance and recovery. In Anrarcric Communities-Species, Srrucrure und Suwivul (B. Battaglia, G. di Ptisco & D. W. H. Walton, eds) Cambridge: Cambridge University Press: in press. Topham, P. B. (1977) Colonization, growth, succession and competition. In Lichen Ecology (M. R. D. Seaward, ed.): 31-68. New York: Academic Press. Accepted for publication
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1995