THE ECOLOGY OF ARCTIC AND ALPINE PLANTS

Biol. Rev. (1968), 43, p p . 481-529

THE ECOLOGY OF ARCTIC AND ALPINE PLANTS

BY W. D. BILLINGS AND H. A. MOONEY Duke University, Durham, North Carolina, and Stanford University,

Stanford, California, U.S.A.

(Received I 5 May I 968)

CONTENTS

I. Introduction . . . . . . . . . . . . 481 484

(I) Present and past distributions of tundras . . . . . . 484 (2) Environmental characteristics . . . . . . . . 485 (3) Vegetational characteristics . . . . . . . . 489

11. Geographic extent and general characteristics of arctic and alpine vegetation

111. Adaptations of plants to arctic and alpine environments . . , . (2) Physiological ecology of the life-cycle in arctic and alpine vascular plants

Seedling establishment . . . . . . . . .

( I ) Life forms and general morphology . . . . . . . Seed dormancy and germination . . . . . . . Chlorophylls and other pigments . . . . . . . Photosynthesis and respiration . . . . . . . . . . . . . Annual cycle of growth . . . . . . . . .

IV. Primary productivity . . . . . . . . . . . Effects of water availability and use

V. Summary . . . . . . . . . . . . . 522 VI. References. . . . . . . . . . . . . 524

I. INTRODUCTION

Among the earth's terrestrial environments, none has less biologically usable heat or has fewer kinds of adapted plants than the tundras and barrens above and beyond the alpine and arctic timberlines. Here, plant phenotypes are environmentally selected by a climatic severity unknown in the mild, moist tropical environments where vascular plants originated and remain in such variety today. Nor does so severe a selection operate in temperate regions where warm summers help to compensate for cold winters by supplying a season of tropical heat to the metabolic activities of plants emerging from dormancy. Only a few kinds of phenotypes have passed this low-temperature screening successfully and have added their gene-enzyme systems to the floras and vegetations of polar and alpine regions. It is the purpose of this review to bring together in brief form the principal facts and theories concerning plant adaptations to these cold environments.

In short space, we cannot improve on the detailed coverage of certain aspects of plant adaptation to arctic or alpine conditions provided by Holm (1922), Schroeter (1926), Sarensen (1941), Pisek (1960), Tikhomirov (1963), Bliss (1962b), Tranquillini (1964), and others. Here, we shall attempt to bring such information up to date and to discuss the problems of physiological adaptation to low-temperature environments.

482 W. D. BILLINGS AND H. A. MOONEY In attacking this problem, it is appropriate to ask ‘What can we learn from studying

arctic and alpine plants that cannot be learned from other kinds of plants?’ Before answering this question, we must define our terms.

We shall define an arctic plant as one growing beyond the arctic timberline or belonging to a species whose main distribution is beyond this timberline. An alpine plant has the same relationships with the alpine timberline. Many arctic or alpine species occur also in meadows or open areas below timberline. Because of this fact and because timberlines are often broken, indistinct, or even lacking, timberline is only a rough boundary between the severity of a tundra environment and the relative protection of a forest or a subalpine meadow.

Timberline is a relatively reliable guide in the Northern Hemisphere but it is much less so in the southern part of the world. For example, in the alpine regions of New Zealand the Nothofagus timberline is at too low an elevation to indicate the real boundary between alpine and subalpine conditions. The situation is carried to an extreme in such places as the western slopes of the Andes in central Chile where there is no montane forest, thus no timberline, and the lower edge of the alpine zone is left solely to the ecologist’s judgement. In the last analysis, what constitutes arctic or alpine conditions always is a matter of judgement. However, the effect of a forest on microclimate rules out the radiation conditions of an open tundra, and thus the timberline boundary has some reality. (See Brockmann-Jerosch (1919) for a more complete discussion of timberline and its climatic relationships.)

In both arctic and alpine situations there are environmental gradients, genetic clines, and vegetational continua which cut across any sort of arbitrary boundary. It is thus impossible to delineate arctic conditions from subarctic, alpine from subalpine, in an absolute manner. Arctic and alpine conditions are primarily a matter of degree. However, such gradients and clines are usually steepest at timberline; thus, timberline provides us with an approximate and reasonably acceptable lower limit to arctic and alpine conditions. Unfortunately, this may not be true for much of the Southern Hemisphere for a variety of environmental and genetic reasons which result in a low timberline or none at all. While we shall be concerned primarily with true arctic and alpine plants in this review, we shall not exclude information derived from subarctic, subalpine, or subantarctic plants if this can be helpful in understanding the adaptive ecology of plants of cold regions.

While some plant species are endemic to the Arctic, and a great many more are endemic to the alpine regions of one mountain range or another, a relatively large group of common tundra species are widespread and occur in both arctic and alpine locations. Such taxa are commonly called ‘ arctic-alpine’ species. They provide important links between the arctic flora and the numerous alpine floras; an understanding of their adaptive mechanisms can provide answers to questions concerning evolution within and migrations between these similar, but different, low-temperature environments. Among the more widespread of these arctic-alpine species are Trisetum spicatum,* Oxyria digyna and Silene acaulis, which are almost cosmopolitan in arctic and alpine regions of the Northern Hemisphere. Trisetum spicatum and a few other

* Nomenclature follows Polunin (1959) in so far as the species are included by him.

The ecology of arctic and alpine plants 483 species of arctic-alpine vascular plants also occur in the mountains of the cold- temperate parts of the Southern Hemisphere. They are, thus, ' bipolar arctic-alpine '. A number of species of lichens and mosses are also bipolar arctic-alpine.

Terrestrial plants of arctic and alpine regions are mainly flowering plants (Angio- sperms), bryophytes, and lichens; ferns are also represented but with fewer species. Almost all the Angiosperms are herbaceous perennials or very low shrubs ; annuals are very rare. The perennial herbs are of four principal life-forms: cushion or polster plants, rosette plants, leafy-stemmed plants, and grass-form plants.

All tundra plants, woody or herbaceous, show rapid shoot growth after melting of the snow-cover in spring or early summer. Such extremely rapid growth, in a matter of a week or two, is one of the unique characteristics of such vegetation. The energy and materials for this fast shoot growth are supplied by carbohydrates and lipids stored in roots, rhizomes, or bulbs. Tundra plants also have the ability to metabolize and to reproduce at low growing-season temperatures which are not far above the freezing mark. Under such conditions, sexual reproduction is often replaced by apomixis, vivipary, or various kinds of vegetative reproduction. All polar and alpine Angio- sperms, except for the few small and delicate annuals, have these characteristics in common. Additionally, many species, especially those of exposed, windy habitats, also can withstand extremely low temperatures and desiccation during the dormant season. In an already severe regional environment, windy ridge crests which are snow-free in winter provide one extreme in local severity, while the late-melting snowbank is the cause of an environmental severity of a quite different sort-the very short growing season. Angiosperms adapted to either extreme are relatively few; some lichens are well-adapted to the wind-swept environments and a few moss species are abundant in some but not all late snowbank sites. Really extreme situations of both types are without any plants.

The uniqueness of polar and alpine plants lies in the fact that they are the only plants adapted to metabolizing, growing, and reproducing at low temperatures. Many other kinds of plants from the forests, grasslands, and cold deserts of the middle latitudes can tolerate and survive extremely low temperatures during the dormant season but require higher temperatures for growth and development than do the plants of arctic and alpine environments. In subarctic or subalpine environments, such higher temperature requirements are met by higher daytime temperatures since subalpine nights are often colder than alpine nights because of cold-air drainage. Similarly, subarctic nights often are colder than those of the Arctic because the sun goes below the horizon for several hours in contrast to the continuous daylight of higher latitudes. Higher daytime temperatures are closely allied with photosynthetic processes and thus it is daytime temperature that marks the real boundary between true arctic or alpine tundra and subarctic or subalpine meadows.

To answer our earlier question: by studying arctic and alpine plants we can hope to learn how this relative handful of species in the world's flora has succeeded not only in surviving low temperatures during dormancy but in manufacturing relativeIy large amounts of food at low temperatures in very short periods of time. We can get additional dividends by applying the question to alpine plants in particular. Alpine

484 W. D. BILLINGS AND H. A. MOONEY plants are subject not only to the rigours of low temperatures day and night but also to the other environmental stresses inherent in high altitudes: low partial pressures of oxygen and carbon dioxide, strong winds, and intense solar radiation including ultraviolet. The answers we get to these questions of low-temperature adaptation of populations and ecosystems will be worth the quest not only scientifically but also from the economic standpoint of food production in cold climates.

11. GEOGRAPHIC EXTENT AND GENERAL CHARACTERISTICS OF ARCTIC AND ALPINE VEGETATION

( I ) Present and past distribution of tundras Because of the moderating influence of the Arctic Ocean, tundra vegetation occurs

as far north as Peary Land on the northern tip of Greenland, reaching its limit with Saxifrage oppositifoliaat KapMorris Jesup in latitude 83" 39' N. (Holmen, 1957). South of this extreme, tundra extends around the seaward edges of the Greenland ice-cap and in a circumpolar band across northern Eurasia. Wherever mountain ranges enter the Arctic from the south, as in Alaska, Scandinavia, and the U.S.S.R., arctic tundras merge almost imperceptibly with alpine tundras and mountain meadows. Farther south, Northern Hemisphere types of alpine tundra and fell-fields exist in many mountain ranges of the middle latitudes and reach almost to the tropics in Nepal and south-western China.

Along the equator, in the high mountains of Africa and South America, are alpine regions very different from those farther north in environments, floras, and vegetation. The small alpine areas of the Southern Hemisphere in the southern Andes, New Zealand, and Australia superficially resemble those of the North in environments and in the life forms of the plants but, except for a few bipolar species, have a flora of quite different derivation. Subantarctic tundra occurs on some of the oceanic islands south of 55' S. and, sparsely, even on the shores of Palmer Peninsula in Antarctica to 64' S.

Good (1964) provides some figures on the approximate area of land covered by arctic or alpine vegetation. By far the largest amount is in the Northern Hemisphere: almost 9.1 million square miles compared to less than 0.5 million square miles in the Southern Hemisphere. In the Northern Hemisphere about 60 yo of this vegetation is north of 60" N. and can be considered as arctic or subarctic. Northern Hemisphere alpine areas are relatively small, isolated, and floristically diverse as compared with the circumboreal belt of arctic tundra. Conversely, in the Southern Hemisphere almost all of the tundra vegetation is alpine, with less than 0.1 yo being south of 60" S. In the Arctic, the land is peripheral to the Arctic Ocean, which moderates the climate and, in summer allows thawing and temperatures high enough for plant growth. In the Antarctic the high continent is central and the ocean peripheral; the result is ice- covered land with little or no chance for plant establishment.

The present distribution of tundra ecosystems with the greater area occurring at high latitudes in a circumpolar zone has been characteristic only of the warm interglacials of the Pleistocene and perhaps also of the later Tertiary. During much of the Pleistocene, tundra climates and biota have migrated back and forth with the cycles of

The ecology of arctic and alpine plants 485 continental and alpine glaciations. While little is known of the distribution of tundra during full-glacial times, continental ice-sheets and alpine glaciers covered much of the tundra’s present range. In North America and Europe, except for the unglaciated parts of Alaska and nunataks in the Scandinavian mountains and in the Canadian Cordillera, arctic plants could survive only south of the ice-front. Alpine plants grew on the lower mountain slopes, in the lowlands, and probably in mountain ranges such as the southern Appalachians, which are completely forest-covered today. In many places there must have been considerable mingling of the arctic and alpine floras. The resultant tundra in middle-latitude North America may have been only a relatively narrow zone between ice and forest. However, because much of Eurasia was both unglaciated and very cold, full-glacial tundra there could have covered a very large area, particularly in Russia and Siberia. An unusual situation existed in north-western Alaska, which was unglaciated and separated at full-glacial from the rest of the North American continent by 2000 miles of ice. Here, a large sample of North American tundra vegetation remained in the Arctic during the height of glaciation and for many thousands of years had better migrational connexions with the Eurasian tundra than with the remnants of the American tundra, which had retreated far to the south. The effects of this isolation are still evident in tundra floras and species structure in western and north-western North America.

( 2 ) Environmental characteristics Arctic and alpine tundra ecosystems may be described briefly as treeless areas beyond

timberline characterized by cool or cold summers and occupied by low herbaceous or shrubby vegetation, often with extensive mats of lichens or mosses, Beyond these generalities, there are many variations due principally to the uneven distribution of snow and meltwater, permafrost, soil parent materials, and topography. Table I is an attempt at a rough quantification of the general environmental characteristics of an arctic tundra station (Barrow, Alaska) and an alpine tundra location (Niwot Ridge, Colorado) compared with those of a cold temperate forest of pine. It should be emphasized that long-term environmental data from tundra locations are rare because of the physical difficulties of operating instruments in such places. While much of the information in Table I is short-term and therefore approximate, there is value in the data and they speak for themselves in telling of the severity of tundra environments.

In regard to summer solar radiation, the daily totals at Barrow, Alaska, are only slightly lower than those at the two montane stations. However, since the arctic photoperiod is continuous, the intensity or rate at Barrow is only about half that in Colorado and Wyoming. The greater altitude of these latter stations also contributes to their higher rates of radiation and also contributes to the higher amounts of U.V.

(Caldwell, 1968). Air and soil temperatures are generally lower in the Arctic but wind-chill on the alpine ridge keeps the summer maximum temperatures low; this is a common phenomenon in the mountains.

Precipitation is much lower at Barrow than in the two middle-latitude stations even though these stations themselves are dry as compared to many mountain regions. Fcr example, Sonnblick at 3106 m. in the Hohe Tauern of Austria has an annual mean

486 W. D. BILLINGS AND H. A. MOONEY Table I . Comparative environmental characteristics of an arctic,

an alpine and a temperate forest ecosystem component

Solar Radiation (I 965)

Highest daily total

Av. July daily total Av. July intensity Quality

(June, July)

Max. photoperiod Temperature (+ I m., "C.) Air

Annual mean January mean July mean Absolute max. Absolute min.

Soil ( - 15 cm., "C.) Annual mean January mean July mean Absolute max. Absolute min.

Precipitation (mm.) Annual mean Highest monthly (wettest month)

Lowest monthly (driest month)

Wind (km/hr.)

Max. water stress in plants (Source F)

Annual mean

Arctic tundra*

Source A

760 langleys

426 langleys 0.30 cal./cm.-* min.-' Low in short wavelengths, particularly short U.V. (2950- 3 1.50 A.1

84 days Source A

- 12-4 - 26.7

3'9 25.6

-48.9 Source D - 6.2 - 14.5

2'5 2'5

- 15 '5 Source A

107 71

0

Source E 19'3

Low (- 4 to - 5 bars)

Metabolic gases (Source G) COa fmg./lJ 0 5 7 Oa (partial pressure 160 in mm.)

Soil frost activity Source D: much, active

Depth of soil thaw Source F: 20-100 cm. depending on site;

Alpine tundra? Temperate forestf

Source B Source A, Laramie,

780 langleys 704 langleys

497 langleys 5 14 langleys 0.56 cal./cm.-* min.-' 0 5 8 cal./cm.-B rnin.-' High in all wavelengths High in all wavelengths particularly short u v.

Wyoming

15 hr. Source C

- 3'3 - 12.8

18.3 36.6

Source C - 1'7

8.3

-

13.3

Source C - 20'0

634 203

6

Source C 29.6

Rel. low (- 6 to - 8 bars)

0 3 6 I00

15 hr. Source C

8.3 - 1.7

20.6 37'2

-33.8 Source C

8.3 - - 31-1

Source C - 10'0

533 203

0

Source C 10.3 .

Rel. high but no data (probably -25 bars or higher)

044 I22

Source C: some, active, Source C: none in on small scale; large, growing season fossil stone nets

bedrock; permafrost frost Source H: 30 cm to Source H: no perma-

permafrost universally rare present

Dupontia-Eriophorum alpine vegetation types of Pinus ponderosa tundra with Kobresia meadow

tundra as climatic climax

Vegetation Source D: Carex- Source C: mosaic of Source C: open forest

SOURCES: A, Climatological Data, National Summary, US. Weather Bureau, 1965; B, Clark & Marr (1966); C, Marr (1966); D, Brown & Johnson (1965); E, Watson (1959); F, J. Dennis & T. F. Rochow (1967), personal commun.; G, W. D. Billings; H., Marr (1961).

* Barrow, Alaska (altitude 7 m., latitude 71' 20' N.). t Niwot Ridge, Colorado (altitude, 3749 m.; latitude 40" N.). 1 Bummer's Gulch, Colo. (altitude 2195 m., latitude 40' N.).

The ecology of arctic and alpine plants 487 of 1643 mm., Mt Washington at 1917 m. in the White Mts of New Hampshire receives 1784 mm., and though quantitative data are lacking, there are many alpine locations that receive much more precipitation. Even though Barrow could be considered a 'middle Arctic' station in the sense of Polunin (1951), its precipitation is as typically low as that of a 'high Arctic' station such as Isachsen at 78" 47' N. on Ellef Ringnes Island which has an annual mean of 99 mm. or Eureka at 80" N. on Ellesmere with only 67 mm. per year. As Savile (1964) says of Hazen Camp (81" 49' N., Ellesmere), 'aridity is far more important than temperature as a limiting factor in plant growth [at Hazen] '. If Barrow were hilly rather than flat and poorly drained, aridity would be an important factor in plant growth there. As it is, water from annual soil thaw above permafrost provides abundant soil moisture (Brown & Johnson, 1965).

Low precipitation in the high Arctic often results in such weak soil leaching that salts accumulate on or below the soil surface in amounts such as to restrict all plant growth except that of an occasional Puccinellia. Savile calls such areas 'true desert'. Apparently, Stocker (1963) would agree, but goes even farther in his description of most of the high Arctic as 'cold-desert'. Such deserts are rare in alpine situations but occur on the eastern slopes of the high Andes in Argentina, for example.

Alpine sites are windier than most arctic locations and, of course, have lower concentrations of metabolic gases due to lower atmospheric pressures. Soil frost activity and permafrost are much more important environmental factors in the Arctic than they are in most alpine sites.

In these arctic and alpine environments the plants are small, close to the ground, and often widely separated, with bare soil or rock in between. Compared with the situation in a forest, the modification of the climate by vegetation is minimal and the physical environment is dominant. Radiation and wind have easy access to the soil and rock surfaces and to most of the above-ground plant tissues as well. I n such open windy places, the effects of real microenvironment are pronounced. Even a few centimetres difference in microtopography makes a considerable difference in soil temperature, depth of thaw, wind effects, snow drifting, and resultant protection to twigs, buds, and leaves. Such microtopography may be a small rock, a peat hummock, or polygon rim caused by soil frost action-or it may be a small depression in which snow accumulates. Whatever the microtopographic pattern, the results are an uneven distribution of snow and consequently unevenness in protection from wind-blast, in the distribution of soil moisture, reception of solar radiation, and in soil temperature. As we have shown (1959), some of these microtopographic features change through time and peat hummocks may eventually rise so high as to be wind-blasted in dry winters so that soil frost-thrusting may push through the scars at the tops of the hummocks and the whole bog may be base-levelled into soil polygons.

In an open vegetation of isolated cushion plants, solar radiation reaches the soil in relatively great amounts even in the Arctic. On the other hand, in sedge or grass turf communities, the sod insulates against heat flow with resultant slowing down of soil thawing and freezing. The soil and lower air-temperature situations are thus quite different between an open fell-field and a moist meadow.

Local temperature gradients are controlled by the distribution of soil moisture,

488 W. D. BILLINGS AND H. A. MOONEY which is dependent to a large extent on snowdrift pattern which is the result of interaction between wind and topography (see diagram in Fig. I) , These gradients are sharper in alpine places but the effects are also visible in the Arctic. The drier the summer, the steeper are the local moisture gradients because they relate directly to position of late snowbanks; this is particularly characteristic of the alpine zone of the Sierra Nevada of California. With the possible exception of the effects of certain types

SNOW COVER TOPOGRAPHIC SITE

snow free

upper slope

bed

lee exposure windward exposure

WIND EXPOSURE

Fig. I . Alpine vegetational pattern along topographic and moisture gradients in the Beartooth Mts., Wyoming. Redrawn from Johnson & Billings (1962).

of underlying rocks such as dolomite, limestone, or serpentine, the distribution of soil moisture controls most local environmental and vegetational gradients both in alpine and arctic regions. All of the plants are adapted to low temperatures but some are better adapted to drought and extreme temperatures; these are on the ridges and open fell-fields, where they have less control over their environment but where the sun’s rays hitting dry soils provide warmer microenvironments in a shallow layer close to the ground.

While isolated tundra plants may not have much influence on the local climate, the microclimate within the crown of the plant itself may be considerably different from that in the open air between plants. This ‘phytomicroclimate’ is influenced by leaf size, shape, colour, pubescence, and arrangement and the temperature and heat balance of the plant itself. The hollow stems of wet meadow plants even enclose a phytomicroclimate where temperatures far exceed those in the open (Billings & Godfrey, 1967). The heating effects in plant tissues are most pronounced on bright sunny, cool days, and are almost negligible in cloudy or misty weather; the phenomenon is more

The ecology of arctic and alpine plants 489 prevalent under alpine conditions. Some of the heat energy is convected into the air within the plant canopy and this air, protected from the wind a few centimetres above, becomes heated. The plant is immersed in a warmer microenvironment than might be imagined by an observer subjected to the chilling breeze.

Arctic environmental characteristics are described by Bliss (1956), Serensen (1941) , and in considerable detail and scope in the great compendium on Cape Thompson edited by Wilimovsky & Wolfe (1966). Alpine environmental data are available in Bliss (1956,1966) , Marr (1961) , Hedberg (1964), Turner (1958) , Gates & Janke (1966) , and Mark ( 1 9 6 5 ~ ) .

Since so much of the alpine or arctic landscape is characterized by scattered plants, such plants have only a very local effect on the modification of the microenvironment. The plants themselves are at the mercy of the structure and fluctuations of the physical environment. Also plant-to-plant interactions which result in competition or ‘inter- ference’ are less marked than they are in the forests and meadows of milder climates. In this respect, the vegetations of arctic and alpine areas resemble those of deserts. As with desert plants, tundra and fell-field plants are ill-equipped to utilize the milder environments at the limits of their ranges where better-adapted competitors deny them the needed light and water. Yet even in the most open fell-fields, cushion plants such as Silene acaulis are invaded and eventually out-competed by other tundra species (Griggs, 1956). Except for the work of Griggs and a few others, however, little is known about interactions between plants in arctic or alpine regions.

( 3 ) Vegetational characteristics Beyond saying that arctic and alpine vegetation consists of low perennial herbs and

dwarf shrubs, it is impossible to generalize about its composition and structure. In the Arctic and in the Northern Hemisphere mountains, tundra vegetation is a complex mosaic of communities arrangeable into types or along vegetational gradients. The controlling environmental factors are topographic exposure and distribution of snow and meltwater superimposed upon geological substratum patterns. One of the commonest gradients is that from cushion plants such as Silene acaulis and Saxijraga oppositijolia on exposed ridges and rocks to dry meadows and heaths at midslope, thence across snowbanks to the dense peaty turf of bogs and wet meadows dominated by grasses such as Deschampsia caespitosa and various species of Poa and by the sedges Carex and Eriophorum. But there are innumerable variations on this theme.

Once one leaves the Arctic and comes south into the middle-latitude mountain ranges of the Northern Hemisphere, the floristic variety increases somewhat and the vegetational mosaics and gradients become more complex. Still, however, most alpine vegetation resembles that of the Arctic both floristically and in structure. However, on entering the tropical mountains, the vegetation becomes much more complex floristically and often is marked by the presence of columnar or arborescent life-forms. The tropical alpine environment is under diurnal control rather than annual; there are great differences between day and night heat budgets and temperatures. There is relatively little resemblance to the Arctic here in either environment or vegetation.

Southern Hemisphere alpine vegetation does show the typical arctic-alpine gradients 32 Biol. Rev. 43

490 W. D. BILLINGS AND H. A. MOONEY from ridge to bog but floristically has little resemblance to the vegetation of the North except for a few grasses, sedges, lichens, and mosses held in common. Very dwarf shrubs are abundant.

It is not possible to mention all the valuable papers which have been written on tundra vegetation. Excellent descriptions of typical vegetational patterns, composition, and structure, however, can be found in the following publications.

Arctic. Britton (1957), Bocher (1963), Hanson (1953), Johnson, Viereck, Johnson & Melchior (1966), Larsen (1965), Polunin (1949 Raup (1965).

Eurasian Alpine. Dahl(1956), Gjaerevoll(1956), Jenny-Lips (1948), Braun-Blanquet & Jenny (1926), McVean & Ratcliffe (1962), Braun-Blanquet (1948), Sukachev (1965), and many papers in the series Beitrage zur geobotanischen Landesaufnahme der Schweiz published by the Schweizerischen Naturforschenden Gesellschaft in Bern.

North American Alpine. Bliss (1963), Johnson & Billings (1962), Marr (1961). Tropical Alpine. Hedberg (1964), Troll (1957), Weberbauer (191 I). Southern Hemisphere Alpine. Billings & Mark (1961), Costin (1967), Ward &

Subantarctic. Taylor (1955). Dimitri (1966).

111. ADAPTATIONS OF PLANTS TO ARCTIC AND ALPINE ENVIRONMENTS

(I) Life forms and general morphology The most obvious adaptations to severe tundra or alpine environments are reduc-

tion in plant height and a tendency toward an herbaceous habit. In exposed places, even small trees are blasted by wind and blowing snows so that ‘tree’ growth is possible only as a twisted shrubby ‘Krummholz’ near the ground. Snow collects and packs hard in the dense branches of the Krummholz and thus protects the evergreen leaves against death by desiccation in the dry winter air when the soil is cold or frozen. Snow also insulates the leaves against temperature extremes: low in winter and high in the bright sun of early spring before the soil has thawed.

Exposure to the rigours of winter is not the only factor limiting upward and northern distribution of trees. As Hustich (1948), Daubenmire (1954), and others have pointed out, summer temperature strongly affects cambial growth of that season, and also seed production. Hustich correctly stresses the sensitivity of trees at timberline to the smallest changes in climate-particularly in the temperature of the warmest month. Boysen-Jensen (1932) suggests that timberline occurs where the amount of dry matter produced each summer is consumed entirely in respiration and in the production of new leaves; there is nothing left over for wood. One might say that the use of carbohydrate for the permanent cellulose of aerial wood is an unattainable luxury when compared to the efficient re-use of sugars, starches, and lipids by herbaceous plants and prostrate shrubs in the same cold environment. These digestible substances can be stored underground and used the following season in leaf production and stem elongation. On the other hand, radial growth of trees appears to be dependent mainly upon carbohydrates produced during the growing season in which that growth occurs (Hustich, 1948). If that growing season is cold, enzyme systems leading to sugar and

The ecology of arctic and alpine plants 491 starch seem to have priority over those to cellulose. This could explain the sensitivity of radial growth of trees at timberline to even small year-to-year differences in temperature during the summer. If favourable summer temperature years are few, woody stem volume will increase very slowly; if favourable temperature years never occur, the production of even a dwarfed tree trunk is impossible.

In the same sense, it would seem as if the metabolic expense of producing a whole new crop of leaves each year is exorbitant for a tree under timberline conditions (Bliss, 1966). Moreover, as Strain (1966) found with Populus tremuloides below timberline in the Sierra Nevada of California, there is always the danger of young leaves of deciduous species being severely damaged by late frosts. This may be a common weakness of deciduous species in subalpine or subarctic environments since we have noticed that evergreen species in such places break bud dormancy somewhat later than do the deciduous species. Evergreen trees can afford the apparent waste of these days of uncertain weather early in the growing season since their older leaves are already in photosynthetic operation; deciduous trees must take the chance of producing leaves as early as possible.

Even though evergreen leaves save the expense of producing all new photosynthetic tissue each year, there are some disadvantages. Principal among these is the prevalence of winter-killing of exposed leaves due to desiccation by dry winds at times when soil moisture is cold or frozen, Snow blast also takes its toll. Under these conditions, the Krummholz mat at the base of the tree has advantages over the battered and one- sided ‘flag-form’ crown where leaf life is relatively short. Under the most extreme situations a crown extending above the snow is impossible and only the mat-like Krummholz represents the species.

Timberline in equatorial mountains is rather difficult to define (Troll, 1957). Columnar or sparsely branched small ‘trees’ of genera not usually tree-like are scattered through shrubby or tussocky alpine slopes above the true forest. The leaves and inflorescences of these columnar plants are usually covered with thick coats of woolly hairs; Troll (1958) callsthis life form ‘ Wollkerzengewachse’, woolcandle form. Hedberg (1964) uses the term ‘giant rosette plants’. There has been parallel evolution of these forms on the high East African volcanoes and in the northern Andes. In Africa the principal genera represented by giant rosette plants are Senecio and Lobelia, while in South America the comparable genera are Espeletia, Lupinus, and Puya. Very similar in form is the silver-sword, Argyroxiphium sandwicense, on the high Hawaiian volcanoes. These equatorial alpine environments have no winter and summer seasons but are characterized by strong incoming radiation by day and strong outgoing radiation at night all through the year. The winters of the middle-latitude mountains are unknown here but frost occurs almost every night.

The ecology of these equatorial alpine locations in Africa (‘ afroalpine ’) has been studied by Hedberg (1964). The principal advantages of the columnar giant rosette plants (Senecio and Lobelia) apparently are concerned with the nightly protection of the buds, which are never dormant. The large woolly leaves curve inward at night, covering the growing tip and protecting it against frost. Additionally, Lobelia keniensis contains water in the rosette ; this water according to Hedberg apparently is secreted by

32-2

492 W. D. BILLINGS AND H. A. MOONEY the plant and covers the shoot apex and leaf primordia to the depth of ca. 10 cm. Every night the uppermost water freezes but the lower water never freezes and its heat protects the growing tip of the shoot. In addition to these large ‘night buds’, the sheathing of the stem by the old hairy leaves and the hairy bracts on the inflorescence not only may act as insulation against loss of heat during the night but they also reflect the intense sunlight during the day. While this work of Hedberg’s pertains to only the ‘afroalpine’ rosette plants, it is probably true to a large extent for the South American and Hawaiian giant rosette plants also.

Above and beyond timberline outside of the tropics, the vegetation is dominated by herbaceous plants and low or prostrate shrubs. Again, the same advantages in a cold environment pertain to the herbaceous life forms-but to a considerably lesser extent over low shrubs than over trees. The more severe the environment, the more likely the shrubs are to be prostrate or restricted to snow accumulation areas. The amount of new wood necessary each year is very small because the support function is not needed in prostrate shrubs. As a result, such shrubs are almost as well adapted to severe conditions as herbs, and some species occur almost to the limit of plant growth in the Arctic; Salix arctica and Cassiope tetragona both extend north of latitude 83Q in northern Greenland (Holmen, 1957). In such places, some shrub species are likely to reflect site conditions by their form, each species being very selective of habitat. Cassiope tetragona (non-prostrate) is of this type and is restricted to snow-covered areas with soils rich in humus. On the other hand, Salix arctica is prostrate, which allows it to grow in wind-swept places free of snow in the winter; but it also occurs in many other sites including those covered with as much as 4-5 m. of snow (Holmen,

The same type of dwarf shrub adaptation has arisen independently in the subantarctic alpine flora of New Zealand, and is related there (as in the north) to increasing severity of the environment. For example, A. F. Mark (personal comm.) has found that species of dwarf shrubs (‘suffrutescent ’) increase in floristic percentage at the expense of species of ordinary shrubs (‘woody’) and of herbaceous species with increase in elevation from ‘lower alpine’ to ‘high alpine’ (as defined by Wardle, 1964). These data appear in Table 2.

One of the advantages of a prostrate shrub or suffrutescent plant in a severe environment is that of permanence; its yearly maintenance can be low and its reproduction need occur only at long intervals. Raup (1965) found a number of shrubs of Salix arctica in north-east Greenland to be more than 60 years old, some were older than IOO years, and one was about 236 years old. Almost all of them showed great irregu- larities of growth through time and also the ability to remain alive and grow using only one side of the stem. The long-lived prostrate shrub form apparently provides a certain amount of flexibility in meeting temporal exigencies in the environment, and in this respect may be the equal of the well-adapted herbaceous perennial. This is particularly true if the shrub is evergreen, for the same advantages exist in evergreen tundra shrubs that exist in evergreen trees at timberline: it is not necessary to spend food reserves on a wholly new photosynthetic apparatus each year. Hadley & Bliss (1964) found that evergreen tundra shrubs on Mt Washington had lower respiratory

1957).

The ecology of arctic and alpine plants 493 and photosynthetic rates than the deciduous shrub Vaccinium uliginosum or various herbaceous species. Pisek & Knapp (1959) also found that alpine evergreen shrubs and timberline evergreen trees have lower respiratory rates than deciduous ones in the same environments. The evergreens can operate at these lower rates since they do not have to produce a wholly new photosynthetic apparatus each year. Hadley & Bliss (1964) also suggest that the older leaves may act as winter food storage organs since lipids and proteins are mobilized and translocated from old to new leaves during the growing season.

Table 2. Percentages of shrubs, dwarf shrubs, and herbs in the alpine Jlora of New Zealand

(Data from A. F. Mark. Alpine zones after Wardle (1964).)

Species occurring in

Species both ‘ lower Species confined to alpine’ and confined to All ‘alpine’

‘lower alpine’ ‘high alpine’ ‘high alpine’ species

Total no. of species. . . 358 161 79 598 % ‘woody’ (ordinary shrubs) 21’2 7‘5 6.3 15.6 yo ‘ suffrutescent’ (dwarf shrubs) 13.1 37-9 392 23.2 % ‘herbaceous’ 65.6 54’7 547 61.2

As well adapted as some shrub species are, the greater number of higher plant species beyond timberline are herbaceous. Almost all of these herbs are perennials with large underground root or stem storage systems; few are biennial, and fewer still are annual. Of the ninety-six species of higher plants in the flora of Peary Land, North Greenland (Holmen, 1957), only one, Koenigia islandica, is an annual. Similarly, even in an alpine flora, that of the Beartooth Plateau (Johnson & Billings, 1962), only three species are annual out of a vascular flora of 191 species. Apparently, in most arctic or alpine locations, annual species constitute only 1-2 yo of the flora. However, alpine floras in relatively dry regions tend to have somewhat higher percentages of annuals. For example, in Howell’s (1951) alpine flora of 108 taxa in the southern Sierra Nevada of California, six are annual. Went (1953) suggests that at least forty species of annuals occur at elevations of greater than 3000 m. in the southern Sierra. Perusal of his table I indicates that perhaps twenty-seven of these species occur as high as timberline at 3300 m. or even higher. There is no doubt that the annual life form is more common in the Sierran alpine zone than in that of most other mountain ranges. This could be partially due to the warm dry microenvironments during the summer in this great mountain range which emerges above a Mediterranean-type climate. Additionally, most of the Sierran annual species are not arctic-alpine but are in genera common in the nearby deserts and may represent upward migration and evolution from desert to dry alpine conditions.

The typical herbaceous plant of arctic and alpine environments is an herbaceous perennial with a relatively large root and/or rhizome system. These perennials are of three main types : graminoid, leafy dicot, and cushion dicot. A few ferns and lily-like plants also occur.

494 W. D. BILLINGS AND H. A. MOONEY In a typical alpine situation, dicots generally have a deep primary root system with

shoots proliferating near the soil surface (Rauh, 1940; Daubenmire, 1941). A few species have rhizomes or bulbs which are utilized in food storage and a few reproduce vegetatively by horizontal rhizomes or even roots. Most alpine dicots in western North America reproduce by seeds rather than by rhizomes. As shown in Fig. 2, western American Oxyriu digynu plants (south of the Canadian Rockies) lack rhizomes while

Fig. 2. Typict.. plants of Oxyriu digynu grown in the same environment from different seed sources and showing the extensive root system (from Mooney & Billings, 1961). A, Beartooth Mts, Wyoming, seed source; non-rhizomatous. B, Sagavanirktok River, Alaska, seed source ; rhizomatous.

those in the rest of its arctic-alpine circumboreal range have reproductive rhizomes (Mooney & Billings, 1961). At the risk of over-generalizing, it appears that spreading rhizomes may be more typical of arctic perennials than of alpine ones. Whether characterized by rhizomes or not, the underground portions of most arctic or alpine perennial dicots have much greater dry weight than the shoots (2-6 times greater) and act as carbohydrate storage organs (Mooney & Billings, 1960; Scott & Billings, 1964; Aleksandrova, 1958). This also seems to hold true for alpine herbfields in New Zealand, but less so for alpine cushion plant communities there (Bliss & Mark, 1965). The New Zealand alpine cushion plants are essentially dwarf evergreen shrubs-and like Bliss’s Mt Washington alpine shrubs, most of the storage is in the form of lipids in the leaves rather than in roots. In Celmisiu viscosu the leaves contain from I 5 yo to 20% lipids (Bliss & Mark)-and burn easily. Apparently, grasses and sedges have smaller root:shoot ratios than do dicots (Scott & Billings, 1964); the reasons for this are not

The ecology of arctic and alpine plants 495 known. Rhizomes and stolons are more frequent in these graminoid plants than in dicots, particularly in the Arctic.

In addition to the large food storage capacity, the herbaceous perennial, whether dicot or monocot, has another adaptation which makes the most of a short cold growing season: the pre-formed shoot and flower bud. This has been illustrated for almost all of the plants of north-east Greenland by Ssrensen (1941). Hodgson (1966) reports it for Alaskan grasses also but it is absent in most temperate zone grasses. We, also, have found it to be almost universal in alpine plants as well. The flower-bud primordia are often initiated early in the growing season of the year before flowering and are usually well developed by the time the perennating bud is formed late in the summer and winter dormancy comes on. In some species, the first indication of floral primordia is two seasons ahead of flowering (Ssrensen). The advantages are obvious: shoot elongation and flowering can and do occur very quickly after snow-release and temperature increase. As a corollary, flowering is thus also dependent upon environmental conditions during floral initiation in the year preceding actual flowering. Most of these flower buds overwinter quite close to the soil surface and in snow-free areas are subjected to intense cold. In Braya humilis, the fruiting inflorescence itself regularly overwinters and completes development the following summer in spite of growing in exposed sites almost without snow and subject to bitter cold (Ssrensen, 1941).

Mark (1965 b) has found pre-formed flower buds in the narrow-leaved snow tussock, Chionochloa rigida, in New Zealand. Apparently, pre-formed flower buds are quite common in New Zealand alpine plants (Mark, personal comm.), which indicates parallel evolution of this adaptation in both Northern and Southern Hemispheres.

The disadvantages of the annual life form in a cold short growing season lie principally in the necessity to complete the whole life-cycle from germination to seed production. This demands an ability to germinate and carry on metabolism at high rates at low temperatures. In fact, although data do not seem to be available, it might be postulated that annual plants in an arctic or alpine environment should have higher photosynthesis and respiration rates than perennial plants from the same locations at the same temperatures. Annual plants do better under desert conditions because even though the growing season is as short there as that in the tundra, temperatures are much higher and growth and reproduction consequently more rapid. Whether in the desert with its short period of water availability or in the alpine zone with its short period of growing temperatures, annuals are of necessity small and delicate. Only in non-stress locations (such as the moist subtropics and tropics) is it possible to afford the metabolic luxury of a large annual plant. Koenigiu islundica, certainly one of the most widespread of arctic-alpine annuals, and often the only annual species present in a tundra region, is extremely small in size in both vegetative and reproductive organs. Dahl (1963) believes that Koenigia is confined to wet sites because of the necessity of keeping the plants' temperatures below the lethal limit of 45" C. by evaporation. This seems quite reasonable and undoubtedly is important in allowing the species to exist in geographic areas otherwise too warm for it. However, a wet environment might have other advantages for an annual in an environment with cold nights: the thermal stability of the surrounding water might allow warmer night temperatures near the

496 W. D. BILLINGS AND H. A. MOONEY plants, thus keeping respiration and growth rates relatively high for longer periods of time. This could be an advantage to an annual plant faced with a short growing season at low temperatures. One might expect to find the few typical widespread arctic-alpine annuals in those microenvironments with the longest periods of stable, moderate temperatures. This might not be true of most of the Sierran alpine annuals, which being desert-derived are mostly in the warmer and dryer sites such as sandy, south-facing slopes.

The small stature of arctic and alpine perennials is essentially genetic (Turesson, 193 I ; Clausen, Keck & Heisey, 1940, 1948; Mooney & Billings, 1961; Lona, 1963; Landolt, I 967) but phenotypic plasticity often allows considerable morphological adjustment. On the other hand, extreme dwarfism, without much phenotypic plasticity, is inherent in certain populations of widely distributed tundra species (Oxyria digyna, Polygonium viviparum). These dwarf plants show up in cultivations in growth chambers and in phenotypic form in herbarium collections. In the Arctic, they are principally from the ‘high Arctic’ in such places as Ellesmere Island and Thule, Greenland. We have designated these as ‘arctic dwarfs’. Similar genetic ‘alpine dwarfs’ occur on many high exposed mountains. For example, on Medicine Bow Peak, Wyoming, near the summit at 3650 m. there is a population of dwarf Oxyria, and similar populations of Trisetum spicatum (Clebsch, 1960) and Thlaspi alpestre (Rochow, 1967). Plants from these populations are much smaller than plants of the same species 300-400 m. lower on the mountain when grown side by side in controlled conditions. Since the site near the summit was above the Pleistocene glaciers that buried the east face of the peak, and is somewhat isolated at the top of a 300 m. cliff, there is the possibility that these populations of dwarf plants represent descendants of populations that survived full glacial conditions on the nunatak summit of the peak.

The most severe alpine or arctic environments are of two general types: ( I ) late- lying snowbank areas where the growing season is extremely short, and (2) windswept, dry ridges. Both of these microenvironments become more severe toward the ‘high Arctic’ and the ‘high alpine’. Plants are absent in the most severe situations in either late-lying snowbanks or exposed ridges. However, at the limits of plant growth in both cases, plants tend to be cryptogams-for the most part mosses in the snowbeds and crustose lichens and sometimes mosses on the windswept, rocky barrens of the hilltops. In the latest-lying snowbeds of the Scandinavian mountains, for example, Gjaerevoll (1956) reports that vascular plants are almost lacking and the sites are dominated by various moss communities. Similar situations exist throughout the Arctic and particularly in alpine regions, although mosses are relatively unimportant in alpine snowbeds in the western American mountains where the transition from grasses and sedges to bare ground and rock under late-lying snow is a sharp one (Billings & Bliss, 1959). The ‘high Arctic’, north of 77O is so dry and cold (Savile, 1961, 1964; Holmen, 1957) that snowbed vegetation is considerably restricted in size and also in flora. In places, snowbed vegetation may even be absent in the sense that it occurs farther south in moister climates. Where snowdrifts do occur in the high Arctic, much of the water probably sublimes into the dry summer air; some of the meltwater may seep rapidly into the porous, rocky soil to emerge lower down slope

The ecology of arctic and alpine plants 497 as the main source of water for other communities in this dry, barren land (Savile,

Windswept ridges provide the most severe environments in terms of temperature, drought stress, and wind abrasion. Beyond the limits of any vascular plants, crustose and sometimes fruticose lichens will be found. In the high Arctic, hilltops and ridges are virtually unvegetated except for such lichens and the grey moss Rhacomitrium lanuginosum, with an occasional plant of Saxifraga oppositifolia (Savile, 1961). Polunin (1951) says that such barrens are ‘desolate in the extreme’ and that ‘most areas have scarcely a plant to be seen’. Similar, but smaller, areas occur on high alpine ridges but the terrain is usually so varied that the term ‘barrens’ is scarcely appropriate except perhaps on the high Tibetan Plateau and in some of the high mountain ranges of the Eurasian and American deserts (the White Mountains of California, for example).

Comparable domination of moist areas by moss carpets and dry, rock areas by crustose and fruticose lichens characterizes the maritime Antarctic (Longton, 1967). Mosses become much less important in continental Antarctica and the only plants in the most severe environments are crustose lichens (Greene et al. 1967).

At the limits of vascular plants in snowbeds, there is apt to be a variety of life forms : graminoid, small herb, cushion plants, prostrate shrubs such as Salix arctica and S. herbacea. On windswept ridges, however, small-leaved dwarf rosette, moss-like, or cushion plants with occasional grass tussocks represent vascular plants at their limit of tolerance. In the Arctic, such plants are Saxifraga oppositifolia, Papaver radicatum, Erysimum pallasii, Saxifraga tricuspidata, S . caespitosa, Cerastium arcticum, Luzula confusa, Poa abbreviata, Hierochloe alpina, and others (Savile, 1961, 1964; Polunin, 1951 ; Holmen, 1957). Plants of these species not only can withstand the winter cold and wind without a snow cover but also tolerate the drought of summer in the most severe environment the Arctic has to offer.

Similar rosette, moss-like, or cushion plants and dwarf graminoids characterize the windswept rocks of high alpine locations. However, high on the rocky peaks or gipfels there are also miniature ‘snowbeds’ in the crevices of the rocks; these shelter and supply water to plants of a softer nature such as Ranunculus which depend upon meltwater to a greater extent than do the cushion plants. In many cases, these softer plants reach higher elevations than do the moss-like or cushion plants on the more exposed sites. Such ‘snow-cranny’ plants extend well up into the zone of permanent snow where their only plant associates are crustose lichens and a few moss tufts. Reisigl & Pitschmann (1958) have compiled data for the Austrian and Swiss Alps on the highest elevation reached by alpine vascular plants. Cushion or moss-like plants such as Minuartia sedioides (3825 m. on the Monte Rosa), Saxifraga moschata (4000 m. on the Finsteraarhorn), Draba $adzinensis (41 50 m. on the Rimpfischgrat), and Androsace alpina (4200m. on the Matterhorn) go well up onto the snowy peaks. Saxifraga oppositifolia, the outlier of vascular plants in the windswept Arctic, goes only to 3540 m. on the Triftjoch, also windswept. But equally high are the relatively soft ‘snow-cranny’ plants Linaria alpina (4150 m. on the Rimpfischgrat), Poa alpina (41 50 m. on the Rimpfischhorn) and Ranunculus glacialis, which reaches the highest level of any vascular plant in the Alps at 4270 m. on the Finsteraarhorn. A parallel

1961, 1964).

498 W. D. BILLINGS AND H. A. MOONEY situation exists at the other end of the world in New Zealand, where Ranunculus grahami exists in snow-crannies well above the permanent snow line as high as 2900 m. on Malte Brun (Fisher, 1965); this is about the altitudinal equal of any vascular plant in New Zealand. Fisher believes that this species with its soft foliage overwinters in the dormant form (as do R. glacialis and Oxyria digyna in the Northern Hemisphere) and that overwintering by evergreen rosettes could not easily endure the frequent avalanches and compacted ice covers of the high-altitude winters.

Webster (1961) lists the highest elevations known to be reached by vascular plants. Since the lowest elevation on the list is 5500 m., all of the locations are, of course, in the Himalayas, Karakorams, or Andes. The highest vascular plants listed are Lagotis glauca, Potentilla saundersiana, Arenaria sp., and Pedicularis sp. photographed by Oleg Polunin at 5945 m. on Mohala Bhanjyang, Nepal. Since Webster’s report, Swan (1967) has found Stellaria decumbens as high as 6136m. on Makalu in the Himalayas. This apparently was not flowering, and yet, not far below, at 6100 m., Parrya lanuginosa, Pegaeophyton scapgorum, and Gentiana urnula were in bloom as early as 27 May. While the Stellaria and Parrya, at least, are small-leaved cushion or moss-form plants, Lagotis glauca and perhaps some of the others have relatively large leaves and are of the same life-form as Ranunculus glacialis. The Lagotis, Potentilla, Arenaria and Pedicularis at 5945 m. on Mohala Bhanjyang were on a gravelly fell-field. The plants on Makulu were confined to what Swan calls the ‘rock-base niche’, where small snowdrifts are captured and provide meltwater as a result of thermal re-radiation from the rocks. The ‘ rock-base niche’ is the ecological equivalent of our ‘snow-cranny ’. This protected and water-supplying microenvironment allows vascular plants to reach their altitudinal limits in the cold, windy, and dry environments of the high peaks where most snow sublimes or blows away; thus, lack of liquid water is the principal limiting factor.

As in the polar lands, lichens and, to a lesser extent, mosses occur beyond the limits of vascular plants on most high mountains. This is true particularly of crustose lichens on the rocks in the mountains of Europe and North America, at least. Mattick (1950) states that lichens exist as high as 6200 m. in the Himalayas. According to Swan (1967)’ however, lichens are scarce or lacking at these high elevations where vascular plants occur above 6100 m. He ascribes this to the lack of surface water from snowmelt. Snow-blast could also be a factor, as Rudolph (1967) notes in Antarctica. At elevations in the Himalayas below 5750 m., subsurface liquid water from snowmelt allows the development of little ‘oases’ of vascular plants in the scree. Here, there are lichens tangled in with the small herbaceous plants. The relative aridity due to low temperatures and snow sublimation thus confining plants to portions of scree slopes with underground meltwater sources or to rock-base niches is strongly reminiscent of Savile’s (1961) observations in the high Arctic on Ellef Ringnes Island.

Apparently, lichens can withstand environments with lower ‘ growing ’ season temperatures than can vascular plants, if there is a supply of surface liquid water at some time during the year. If there is not such a surface supply, rooted vascular plants may actually do quite as well if not better than lichens. The former situation prevails in places such as the relatively moist west coast of the Antarctic Peninsula, where the

The ecology of arctic and alpine plants 499 richness of the lichen vegetation is unequalled in most other parts of the world (Rudolph, in Greene et aZ. 1967), but the vascular vegetation is depauperate and consists of only two species. Of the cu. 350 species of lichens known from Antarctica, ca. IOO have been found only on the west coast of the Antarctic Peninsula. The east coast of the peninsula, being drier and colder, has only ca. 20 yo as many lichen species as the whole peninsula. The lichen flora and vegetation of the rest of the continent is relatively depauperate, a fact related to cold and aridity. The same decrease in luxuri- ance in lichen vegetation may be seen in a transect from the relatively moist low Arctic to the arid high Arctic. And, of course, we have the situation of 'frozen aridity' presented by Swan for the high Himalayas.

So, provided there is an occasional supply of water, the lichen life form seems more efficient and better fitted to extremely cold summer situations than are most vascular plants. Why is this? There appear to be several advantages to the lichen life-form in a cold environment. First, the highest daytime temperatures are close to the rock- or soil-air interface where the lichens exist. This can produce meltwater and allows photosynthesis in the lichens to operate efficiently. The very low night temperatures at the same interface do not damage lichens. Furthermore, Lange (1965) has found optimum photosynthetic temperatures for several species of alpine and antarctic lichens to be around 5" C. All of these lichens had positive net photosynthesis in light even at several degrees below 0" C. (as low as - 10' C. in Parmelia coreyi from Victoria Land, Antarctica, and StereocauZon atpinurn from the Otztaler Alps). Presumably, most of the water in the thallus was frozen at these temperatures (Scholander, Flagg, Hock & Irving, 1953). Some CO, uptake occurred at temperatures as low as -24" C. in lichens from a lowland dry site in Europe, so there appears to be little correlation of site with the ability of a lichen to take up CO, in the light at low temperatures. The lowland European lichens may well be more active in the winter than they are in the dry summer, while the reverse is probably true of the polar and alpine lichens.

Another possible advantage of lichens over vascular plants in a cold or dry environment is the ability to absorb water rather quickly into the photosynthetic system. If temporary liquid water is available, it can move almost directly into the algal cells which are at a favourable temperature for photosynthesis, thus circumventing the need to enter a conducting system (with its resistances) by way of soil and roots. I t would not be surprising to find some high-altitude vascular plants with similar rapid absorption by leaves. The lack of roots in lichens and mosses has another advantage: Hedberg (1964) reports both kinds of plants riding in loose balls or plates on the tops of active solifluction areas on Mt Kenya.

Lastly, lichens are long-lived perennials-up to I 300 years for Rhixocarpon geo- graphicum in the Alps and 4500 years in West Greenland (Beschel, 1961). As such, there is no need to produce new biomass each year. Near the limits of plant growth this is a real advantage, since favourable years for growth may be far fewer than un- favourable ones. Lichen growth may be thought of as being 'opportunistic', thus taking advantage of temporary environmental events to an extent not possible in most vascular plants. The reverse is also true: lichens can remain dormant for long periods of time at low temperatures, and when thawed resume normal physiological activity.

500 W. D. BILLINGS AND H. A. MOONEY Lange (1966) measured the photosynthesis rates of Cladonia alcicornis at various temperatures then froze the thalli at -15' C. for periods of time to up I I O weeks; photosynthesis rates were normal after thawing.

( 2 ) Physiological ecology of the life-cycle in arctic and alpine vascular plants The ability of a vascular plant to survive and reproduce in arctic or alpine environ-

ments is based on the physiology of the whole plant in its natural milieu. Bliss (1962b) has provided an excellent summary of this adaptational ecology of arctic and alpine plants. Also, Larsen (1964) has reviewed the roles of physiology and environment in the distribution of arctic plants, while Tranquillini (1964) has done somewhat the same thing for plants at high altitudes. Here, we shall summarize and evaluate the current state of knowledge concerning the physiological ecology of both arctic and alpine plants. As we have done with Oxyria digyna (Mooney & Billings, 1961), the basis of the presentation will be the life-cycle, starting with the seed.

Seed dormancy and germination The weather during some growing seasons in the Arctic or in the high mountains

is so cold that flowering and fruiting are seriously hampered and little or no viable seed is produced. However, in other seasons, some plants may have abundant seed crops. Because of the shortness of the summer season, such seeds usually ripen not long before the return of winter conditions. Indeed, they may not ripen at all during the year of flowering but, as in Braya humilis in north-east Greenland, the developing fruits may become dormant, go through the winter, and ripen the following summer (Serensen, 1941).

Because of the early onset of winter, one might anticipate finding almost universal seed dormancy as a protective mechanism, but such is not the case. Given a suitable environment in the laboratory, fresh seeds of most alpine and tundra plants germinate rather easily (Soyrinki, 1938, 1939; S~rensen, 1941; Bliss, 1958; Bonde, 1965a, b ; Sayers & Ward, 1966). Seeds of some species, however, do show dormancymechanisms of one kind or another (Pelton, 1956; Amen, 1965; Rochow, 1967). I n understanding the extent and role of seed dormancy in alpine species, we are aided by Amen's recent review of the subject (1966). Of sixty-two alpine species listed by Amen (based on the individual works of Amen, Bliss, Bonde and Pelton), only about 40% showed dormancy at time of harvest. Carex, Trifolium, and Salix are the principal genera having dormant seeds. Most dormancy is caused by seed-coat inhibition (Carex, Luxula, Thlaspi, Trifolium) and can be overcome by scarification. A few species, such as Erythronium grandiforum, require a chilling period of ca. 4' C., while Cerastium beeringianum and Saxifraga rhomboidea go through after-ripening phases at higher temperatures. Amen's review indicates that seed dormancy is more common among dominant and abundant species; he suggests that such dormancy may contribute to their success.

There is some indication of ecotypic variation in dormancy or degrees of dormancy. In Oxyria digyna, germination is better in light than in dark (Mooney & Billings, 1961) ; this indicates that some seeds in a population have a light requirement for germination

The ecology of arctic and alpine plants 501

while others do not. This light requirement trait in Oxyria is more frequent in American alpine populations (72-97 yo of viable seeds being light-requiring) than in arctic ones (20-64 % of viable seeds being light-requiring).

Intrinsic seed dormancy, then, apparently is not common among arctic or alpine species. Even such dormancy as does exist is easily overcome by scarification, chilling, light, or simply elapsed time. We can conclude that dormancy in nature is principally under the control of the tundra environment and its low winter temperatures. Seed usually matures too late in the season to meet the right combination of temperature and moisture for germination.

Optimum germination temperatures, as measured by speed and completeness of germination, are surprisingly high for most tundra species (20-30" C.) ; such temperatures are comparable to those at which seeds of most temperate and tropical species germinate. In our work with Oxyria (1961) the optimum temperature was 20" C. There was still germination at 10' and 30°, but none at 3" C. Strangely, the southern- most alpine populations showed better germination at 10" C. than did those from the Arctic, while the arctic populations did better at 30" C. than did most of the alpine collections. R. H. Wagner (personal comm.) tested some of our Oxyria seed collections on a temperature gradient bar germinator and found curves similar to ours for alpine populations from the Donjek Mountains, Yukon, and Niwot Ridge, Colorado. How- ever, an arctic population from Pitmegea River, Alaska, showed IOO % germination at 10-12' C. and no germination at 8-10" C., a sharp cut-off indeed.

Amen (1966) states that there is no evidence to suggest that any alpine seeds can germinate at temperatures below 10" C. He, of course, is referring to constant temperatures; Wagner's data are also from constant temperatures. Sayers & Ward (1966) also got no germination of any alpine seeds at a constant 5" C. This seems surprising since the seeds of several cereal grasses and weeds are reported to germinate at temperatures as low as 3-5" C. (Mayer & Poljakoff-Mayber, 1963). Also, Juhren, Hiesey & Went (1953) found that seeds of several species of Poa, Agropyron, and Bromus from western North America will germinate fairly well at a constant temperature of 3-5" C.

The only evidence which we have found of germination in a tundra species at a constant temperature of 5" C. is that reported by Holtom & Greene (1967) for Deschampsia antarctica, one of the two antarctic angiosperm species. The other, Colobanthus crassifolius, had no germination at 5" C. However, seeds of both species germinated well if exposed to temperatures which fluctuated between 5' and 18" C. This result confirms what apparently is a typical reaction to temperature in germination of tundra seeds. For example, we (1961) tested seeds of four populations of Oxyria at temperatures which cycled once every 24 hr. between 13" and 2" C. (mean 7.5' C.), thus approximating summer temperatures on the Alaskan arctic coastal plain. Germination (as high as 65 %) took place in all populations. Vickery (1967) got similar results ; germination occurred in all eleven populations tested in two western American species of Mimulus at temperatures alternating between 9" and 4" C.

Field temperatures in arctic and alpine sites are not constant. The germination that occurs there is thermally opportunistic, mostly at temperatures lower than the laboratory optimum, and over a much longer period of time. For example, S~lrensen (1941)

W. D. BILLINGS AND H. A. MOONEY found that germination in several species at Eskimonaes in north-east Greenland could take place in early June even though the surface soil and seeds were frozen for many hours each day. Apparently, arctic or alpine seeds germinate better at low alternating temperatures than they do at low constant temperatures; but more research is needed.

When does germination occur in the field? The best answers to this question may be found in the observations of Soyrinki (1938, 1939) and Ssrensen (1941). With their observations and the available laboratory temperature data as guides, germination appears to take place a week or so after snowmelt in the early summer after soil surface temperatures get up to IOO or 15' C. in the daytime, and before the soil dries out. Most germination in late summer is impeded by lack of soil moisture in the upland tundras and most (but not all) of the species there produce non-dormant seed. Late soil moisture is available in most wet meadows; many (but not all) of the principal species in such places have seed dormancy mechanisms (Amen, 1966): Carex, Luxula, Erythronium, Saxifraga rhomboidea, Deschampsia caespitosa, Polygonum bistortoides. However, some plants in such wet places do produce seed that germinates the same year. Bliss (1958) found that seeds of Salixplanifolia var. monica in the Rocky Moun- tains ripen in July and germinate immediately in the wet habitat. On the other hand, seeds of Salix brachycarpa do not ripen until August, when its site has become rather dry; these seeds overwinter in viable form and germinate early the next summer.

We can conclude that almost all seed germination in alpine locations, at least, takes place in early summer after snowmelt during the year following seed production. Most species lack a seed dormancy mechanism and the elapsed year (or more) between seed production and germination is environmentally imposed. There are a few species, however, which do have an intrinsic seed dormancy mechanism of one kind or another; the commonest type is caused by a hard and impermeable seed coat. Many but not all of these species with seed dormancy are dominant and abundant in moist or wet alpine meadows.

Since tundra environments may not be suitable for germination every year, we would like to know how long such seeds may remain viable. Even under good germination conditions, there is often considerable intrapopulational variation in how long it takes a seed to germinate. In one sample of snow tussock (Chionochloa rigida) seed from the New Zealand mountains, Mark (1965b) found (at 21' C. in the dark) that after 50 days only 31.57~ had germinated, 40% had germinated at 109 days, and the last germination did not take place until 1450 days, almost 4 years after the start, at which time 94% of the seed had germinated and the experiment was terminated. Such intermittent intrapopulational germination over a long period of time could have survival value for a tundra population near the limits of growth.

If it took almost four years for some of Mark's snow tussock seed to germinate in the laboratory at 21' C. with moisture, these same seeds might have retained viability in the cold field environments for many years before the right combination of conditions allowed germination. In our laboratory at Duke University we have over 1000 collections of arctic and alpine seeds stored dry at -18" C. Most of these seeds retain their viability indefinitely in this frozen condition; our oldest collections are now 15 years old.

The ecology of arctic and alpine plants 503 A possible answer to how long arctic seeds may remain viable is provided by the

recent paper of Porsild, Harington & Mulligan (1967) on the germination of seeds of Lupinus arcticus recovered from permanently frozen burrows of the collared lemming (estimated age 10,000 years B.P.) in unglaciated central Yukon. The seeds may have survived at least 10,oooyears of freezing and 12 years of dry, normal temperatures after they were collected and before they were given to the National Museum of Canada. Six of the seeds germinated within 48 hr. on wet filter paper (presumably at room temperature) ; the seedlings were transferred to pots, and at least one has subsequently flowered. This may not be too surprising when one recalls that Scholander et aE. (1953) found a steep drop in respiratory rate in living arctic plants when frozen, so that the respiratory Ql0 at -5' C. was between 20 and 50, where it levelled off with further drop in temperature. As Scholander and his co-workers suggested at that time, if the survival time of an isolated organism depends upon the rate at which its energy stores are used up, an organism capable of surviving 'a modest 10 days' at oo C. would last for 1000 years at -23" C. with a Qlo of 50, and for I,OOO,OOO years at -42" C. These are conservative estimates when one considers that the Lupinus arcticus seeds were capable of surviving 12 years of ordinary temperatures after recovery and before being put in moist conditions suitable for germination. It would not be surprising if viable lichens (see Lange, 1966) and seeds could be recovered from permafrost cores far older than 10,ooo years.

We can conclude that if seeds of certain arctic and alpine plants remain frozen in soil or perhaps glacial ice, their period of viability may be very long. Certainly, such viability could span time periods as long as full glacials and, in the right places, even interglacials. Thus, delayed germination could act in lieu of refugia. It might allow the re-establishment of a species in situ tens of thousands of years later after the retreat of the ice and permafrost. This could help to explain some apparently rapid 're- invasions ' and some puzzling species distributions in the Arctic.

Seedling establishment Even less is known of seedling establishment in tundras than is known about

germination requirements. Considerable information is provided by Soyrinki (I 938, 1939). Wager (1938) has also made observations on seedling establishment in the Arctic.

Since most seed germination in the tundra occurs in early summer, the seedling has only a few weeks to develop a root system and to produce enough carbohydrates to allow survival through the following winter. There are several reasons why years may pass between episodes of successful seedling establishment of a species in a given tundra location. First, the temperature must be warm enough for germination to take place. Secondly, this must occur early enough in the summer to allow time for good growth before the return of temperatures constantly below freezing, and in some years these come unusually early. In regard to this point, Bliss (1958) notes that seedling reproduction is more common in those species growing on deeply thawed soils in the Arctic. Thirdly, the seedlings must not be exposed to drought in the latter half of the summer before the root system has penetrated to a reliable water supply.

504 W. D. BILLINGS AND H. A. MOONEY The more severe the tundra (high Arctic, high alpine), the fewer are the years in which all of these conditions are met and in which, therefore, there is a good chance for seedling survival.

Perhaps it should not be surprising that germination temperature requirements are fairly high. If temperature thresholds were lower, germination could be triggered in a season too cold for adequate photosynthetic and respiratory rates in the seedling- or too late in a moist season in which the seeds were produced. Establishment would thus be hampered by too little root and leaf growth to prevent death by drought, frost-heaving, or inadequate carbohydrate storage.

Seedling growth is very slow under natural conditions and at the end of the first season the seedling is still very tiny in most species. Wager (1938), at Kangerdlugssuak (68" 30' N.) in East Greenland, found that Oxyria seedlings at the end of their first summer had two cotyledons and two leaves of 2.5 mm. diameter. Comparably small seedlings were typical of other species. In Saxifraga oppositifolia, growth was so slow that the true leaves did not develop until the second year.

We have grown thousands of Oxyria seedlings during our research activities and have watched seedling development in a qualitative way. At temperatures averaging 20" C. seeds of all populations (arctic and alpine) germinate readily and the cotyledons appear above ground in 3-5 days. Shoot growth then becomes rather slow but root growth goes on rather rapidly with the development of a tap root several centimetres long within a week or two, By the end of a month, two or three leaves have appeared; at this time, shoot growth is resumed at a fairly rapid pace. In nature, this resumption of shoot growth does not occur in most Oxyria populations until the second year. The first field growing season is devoted primarily to root-system establishment. This is important to survival since the surface soil may become very dry in late summer in many alpine locations and even in the Arctic. There is an interaction also between frost-lifting of seedlings with too-shallow root systems during the ensuing winter and subsequent greater susceptibility to drought-killing in the second summer (Mark,

Such lifting by needle-ice action or frost-thrusting is a real danger. It has been shown by Hedberg (1964) for the high African mountain plants, where seedlings starting in open soil are rapidly eliminated by frost-lifting which occurs diurnally on most nights of the year. In spite of root competition, seedlings of many afro-alpine species stand a better chance of survival in closed vegetation rather than in open soil. The result is a patchiness in vegetation in the upper parts of the alpine zones of Mt Kenya and Kilimanjaro.

While there are advantages from the standpoint of light and moisture for a seedling starting in the open, there are also advantages in a needle-ice or solifluction area for seedlings to have the protection of well-anchored mature plants. This may be at least a partial explanation for the observations of Griggs (1956) in the fell-fields of the Rocky Mountains that seedlings of many alpine plants are more common and survive better in the cushions of Silene acaulis and similar plants than they do in the open. Such cushion plants with their deep tap-root systems are the pioneers in bare gravels subject to frost action and other disturbances.

19653).

The ecology of arctic and alpine plants 505 Reproduction by seedlings appears to be most common and most important in the

drier alpine sites than in any other arctic or alpine environmental type. However, seedling establishment every year is necessary only in the few alpine annuals such as Koenigia. Even here, it is probable that the seeds may remain viable in the ground for several years. With the abundant and slow-growing perennials, seedling establishment need only occur now and then for the population to be maintained. In the Arctic and in wet and moist meadows of alpine locations, vegetative reproduction by rhizomes or runners is more common by far than reproduction by seeds.

Chlorophylls and other pigments Standing crops of chlorophyll in tundra vegetation have been measured by Bliss

(1966) for alpine communities on Mt Washington (1917 m.) in New Hampshire and by Tieszen & Johnson (1967) for arctic communities on the northern coastal plain of Alaska. The combined chlorophyll a + b contents for seven community-types on Mt Washington ranged from 0.18 td 0.90 g./m.2; in four arctic types the range was 0.32-0.77g./m.~. On a land-area basis, chlorophyll content is roughly the same in these two relatively moist tundra regions. Furthermore, they are equivalent to chlorophyll contents in temperate herbaceous communities of Minnesota as reported by Bray (1962). Comparable land-surface chlorophyll data do not seem to be available for the drier and higher mountains of western North America.

On the basis of individual plants within single species, Henrici (1918) in Switzerland found that on a fresh-weight basis lowland forms (250-450 m.) had over twice as much chlorophyll as alpine forms (1700-2450 m.) of the same species. Her results are on a relative basis only, with Urtica dioica being used as a standard. Seybold & Egle (1940), however, found that, on a leaf-area basis, alpine plants in general had just as much chlorophyll as lowland plants. They did confirm Henrici’s results that some alpine plants have less chlorophyll than Urtica on a fresh-weight basis-but so did some lowland plants.

There are no data available for chlorophyll content in alpine plants of western North America as compared to lowland plants of the same species in the same latitudinal region. However, chlorophyll determinations on leaves of Oxyria dkyna collected and preserved in the field showed lower values for plants at 3292 m. in Wyoming than for plants at I 158 m. in Alaska on both fresh-weight (0.387 mg./gfw. u. 0.636) and leaf-area (0.674 mg./dm.2 v. 0.867) bases (Mooney & Billings, 1961). We also determined chlorophyll contents on plants of eight populations of Oxyvia (four for the arctic, four from alpine North America) grown from seed under controlled conditions in two simulated environments : arctic and alpine. Under simulated arctic conditions, plants from high-altitude alpine populations had less chlorophyll than did those from the low-altitude arctic populations. The rate of decrease with source altitude was about the same for both bases: fresh-weight or leaf-area. Under simulated alpine conditions, there was slightly less chlorophyll in the high-altitude populations than they had in the arctic chamber. However, the low-altitude arctic populations, when grown under alpine conditions, had more than twice as much chlorophyll as they showed under arctic conditions. This was true on both a fresh-weight basis and a leaf-

33 Biol. Rev. 43

506 W. D. BILLINGS AND H. A. MOONEY area basis. These data indicate that within this single arctic-alpine species, there is less chlorophyll in plants of alpine populations than in plants of arctic populations, and that this difference has both genetic and environmental bases.

The striking increase in chlorophyll content in the arctic populations under alpine conditions can possibly be explained by the 8 hr. of darkness out of every 24 which provided a respite from photo-oxidation. This respite had little efFect on the alpine populations, which were from locations where such a respite is part of the natural environment. Clebsch (1960) also found that chlorophyll content on a fresh-weight basis increased dramatically when an arctic population of Trisetum spicatum was grown under simulated alpine conditions. The genetic potential for higher chlorophyll contents in arctic races was also noted by Mooney & Johnson (1965) using alpine and arctic populations of Thalictrum alpinum in a growth chamber programmed for simulated arctic conditions ; chlorophyll contents of the arctic populations were about 25 yo higher than that of an alpine population.

Since solar radiation intensities are much higher in alpine environments than in lowland or arctic situations, one would expect more photo-oxidation of chlorophyll at high altitudes. In addition to the genetically determined lower chlorophyll contents of alpine Oxyrias as compared to arctic ones, the lower field values obtained in alpine Oxyrias may be due to daily photo-oxidation. Montfort (I950), for example, found that plants of most (but not all) lowland species showed much chlorophyll destruction in the bright light of high altitudes, and that even some alpine plants showed evidence of chlorophyll damage.

McWilliam & Naylor (1967) have shown that there is, indeed, an interaction between temperature, light and genetic system in chlorophyll content at low temperatures and in bright light. Corn (Zea mays) develops almost no chlorophyll at 16" C. and 4500 f.c., but at 28" C. chlorophyll accumulates normally. On the other hand, wheat accumulates chlorophyll in a normal manner at both temperatures. They found that the lack of chlorophyll at 16" C. in corn was not due to a block in the pigment syn- thesizing mechanism but rather to the photodestruction of chlorophyll prior to its stabilization in the membrane structure of the chloroplast lamellae. This prolongation of the photosensitive stage in chlorophyll synthesis in corn at low temperatures does not occur in wheat, which is better adapted to low temperatures. The analogy to alpine plants o. lowland plants is obvious.

Shakhov et ul. (1965) suggest that some of the chlorophyll damage at high altitudes may be due to ultra-violet radiation. They irradiated arctic and alpine plants in the field with additional U.V. and detected changes in chloroplast structure and pigment content. They also found that, in the light, there was some recovery from such U.V.

damage by photoreactivation. In this regard, the alpine U.V. climate and its effects on plants and their pigments

has recently been investigated by CaldwelI (1968). Almost all U.V. damage to higher plants in nature is the result of u.v.-B (2800-3150 A). While direct beam solar u.v.-B increases with altitude, sky u.v.-B decreases; the result is only a modest rate of increase in global u.v.-B with elevation. On a cloudless summer day in Colorado, Caldwell found that integrated u.v.-B irradiance at 4350 m. was only cu. 26 yo greater than at

The ecology of arctic and alpine plants 507 147om. Leaves of alpine plants (including Oxyria digyna) in a simulated alpine environment in the laboratory were subjected to precisely defined u.v.-B irradiation (1-4 x 1015 quanta cm.-2 sec.-l at 2967 ,& for 40 min.) without the presence of longer wavelengths. Chlorophyll breakdown and tissue destruction occurred in some of these plants. Photoreactivation of such damage took place when leaves were exposed to longer wavelengths (2.0 x 1o16 quanta cm.-2 sec.-l at 4358 A for 4-5 hr.) immediately after doses of u.v.-B irradiation. In the field, natural filtration of u.v.-B by epidermal pigments (mainly flavonoid compounds) in alpine plants combined with photoreactivation are the most likely adaptations to the u.v.-B climate.

In regard to chlorophyll content in tundra plants, we come to the following tentative conclusions: (I) chlorophyll content per unit land area is probably not very different between arctic and alpine communities occupying the same position on the soil moisture gradient; (2) within a single species, there is less chlorophyll in alpine forms than in arctic forms whether on a leaf-area or fresh-weight basis; this difference is both genetically and environmentally controlled; (3) the evidence is less clear for lowland TJ. alpine forms in the same latitude but alpine forms apparently have less chlorophyll; (4) u.v.-B irradiation and perhaps other short wavelengths break down chloroplasts but longer wavelengths in the alpine environment simultaneously allow photoreactivation of this damage; ( 5 ) some species of plants apparently have too slow a rate of protochloro- phyllide synthesis to keep ahead of photo-oxidation of chlorophyll in bright light at low temperatures; (4) the lower chlorophyll content of alpine forms causes greater reflectance and may be involved in the heat balance of the leaf.

The bright light and low temperatures which result in low chlorophyll contents also allow a build-up of anthocyanins in the leaf and young stem. This can be seen in the high mountains, particularly early in the season just after snowmelt and again near the end of the season just before the leaves die back. The same effect may be observed in growth chambers by lowering the temperature while light intensity remains the same.

In Oxyria, plants of some populations appear to produce much more anthocyanin than do plants of other populations. In North American Oxyrias, plants of alpine populations have more than those of arctic populations, but there seems to be no consistent correlation with elevation of source. Some alpine populations are anthocyanin-producers, others produce very little. Among European Oxyrias, even some arctic ones from Lappland have anthocyanin in fair quantity.

Bjorkman & Holmgren (1958) found a good correlation of autumn anthocyanin content with source altitude in Solidago virgaurea plants growing in a uniform garden in Uppsala. Alpine and subalpine ecotypes from 870 to 1350 m. source elevations had 4-5 times as much anthocyanin in their leaves as did plants from two sea-level ecotypes. Apparently there is a strong hereditary tendency to produce anthocyanins in alpine populations of both Oxyria and Solidago as compared to lowland populations.

What are the functions of anthocyanins in the leaves of alpine plants? First, it is possible that anthocyanins act as a ‘sink’ for excess sugars during cool, bright weather or under conditions of poor nitrogen or phosphorus nutrition. Secondly, they may act as absorbers of ultraviolet radiation in the epidermis or mesophyll (Cappelletti, 1929- 30). Also, Biebl (1942) found that destruction of epidermal cells in onion bulbs by

33-2

508 W. D. BILLINGS AND H. A. MOONEY u.v.-B was in inverse proportion to their anthocyanin content. Caldwell (1968) provides additional evidence with Sedum rosea, an alpine species, where green epidermis transmitted almost 3 times as much U.V. as did epidermis with much anthocyanin. He also found that red leaves of Oxyria digyna and Geum rossii from the Rocky Mountains were consistently less susceptible to tissue destruction by irradiation of 2967 r f than were green leaves of the same species. Red leaves of both species had reduced U.V. transmission. Colourless flavonoids in the epidermis also reduced U.V.

transmission in some species. From these results, it seems clear that an epidermis rich in anthocyanin makes a good U.V. filter.

A third possible function of anthocyanin in alpine leaves and young stems may be the absorption of energy at other wavelengths with resultant increase in leaf temperature. We do not have any evidence for this but suggest it as a possibility.

Photosynthesis and respiration The key to successful adaptation to tundra or alpine environments is the develop-

ment and operation of a metabolic system which can capture, store, and utilize energy at low temperatures and in a short period of time. The short, cold tundra ‘growing season’ is at the opposite end of an environmental gradient from the moist, warm, year- long environment of a tropical rainforest. In between lie the seasonal warm summer- cold winter conditions of temperate forests, meadows, and most crop land. An understanding of the workings of the photosynthetic-respiratory systems of tundra plants will be aided if we ask how such systems compare with their temperate and tropical counterparts in regard to seasonality, temperature effects, light effects, and the availability of metabolic gases and water. Fortunately, we have the reviews of Pisek (1960), Bliss (1962 b), Tranquillini (1964)) and Larsen (1964) which can heIp us with the answer.

Seasonality of carbon metabolism. As Gessner (1960) has pointed out, it is not the high temperatures nor high light intensities which are the reasons for high productivity in tropical rainforests but the uniformly good photosynthetic conditions throughout the year which are responsible. Thus, in true tropical rainforest, photosynthesis has little or no seasonality. Away from this ideal extreme, all other kinds of vegetation show some degree of annual cycle in photosynthesis with extreme seasonality being shown by plants of deserts and tundras.

The photosynthetic seasons of arctic and alpine tundras are fully as short as those of desert vegetation but somewhat more regular, The principal limiting factor is low temperature, and of course, in all but the windy ridge habitat, the duration of snow cover. The snow-free period decreases with elevation (see fig. 3, Pisek, 1960; also Winkler & Moser, 1967) and towards the centres of snowbeds so that, at last, any snow-free period is so short that there is no photosynthetic season. In alpine regions, thus, the growing season of photosynthetic activity ranges from 3 or 4 months where the snow melts early in June to none at all. For most alpine plants, the season ranges from 6 to 10 weeks (Bliss, 1956; Billings & Bliss, 1959; Holway & Ward, 1963) with low temperatures and snowmelt governing the start of the season; relative soil drought, return of low temperatures, shortened photoperiod, and perhaps carbohydrate accumulation govern the end of the period. In years of unusually great snow accumulation,

The ecology of arctic and alpine plants 509 the plants may not be uncovered at all or for only a few days of activity before the new snow and low temperatures of September return (Billings & Bliss, 1959; Moser, 1967).

Photosynthetic activity in alpine plants occurs throughout most of the snow-free period when temperatures during the daylight hours are near or above 0" C., but photosynthesis is not uniform throughout the season. Net photosynthesis of shoots is relatively low early in the season because of high respiratory rates associated with rapid growth immediately after snowmelt (Hadley & Bliss, 1964; Bliss, 1966). How- ever, some of the respiratory carbon dioxide may be recycled by photosynthesis inside the hollow young stems of rapidly growing plants around snowbanks (Billings & Godfrey, 1967), thus making up, in part, the photosynthetic deficit during early growth. As the microenvironment warms up, photosynthesis increases as long as water is available, According to Glagolev & Filipov (1965), maximum photosynthesis is reached during the flowering stage.

In the Arctic, perhaps because of the longer photoperiod, plants may start growing somewhat earlier than in most alpine situations. Initiation of growth can be as early as late April or early May in Saxifraga oppositifolia on dry sites in northern Norway and as early as late May even at 73" 30' N. at Myggbukta in north-east Greenland (Serrensen, 1941). At the latter location, flowering of Saxifraga occurs before the mean daily temperature reaches 0" C. Zubkof (1935) also noted that Saxifraga oppositifolia was the first plant to show signs of life in the spring on Novaya Zemlya at 76" 14' N. Growth started before daily mean temperatures became positive, so that the metabolic period of Saxifraga at this high Arctic location was 107 days while the duration of positive mean daily temperatures was only 78 days. Other dry site plants, notably many Cruciferae, often start growth early in the Arctic according to Serrensen. Soil drought usually puts an end to the vegetative season of these plants before low temperatures become effective.

A common phenomenon both in arctic and alpine locations is the speeding up or telescoping of phenological events in plants released from snow-cover relatively late in the summer. Plants released from snow by early or mid-June will take much longer to reach maturity and have a longer photosynthetic season than those of the same species released in mid-July. This has been commented upon by Serrensen (1941) for the Arctic and by Billings & Bliss (1959) and Rochow (1964) for alpine situations. While these later plants grow faster in shorter time than plants released earlier, they are smaller and produce less dry matter.

Effect of temperature on photosynthesis and respiration. Temperatures of air and soil decrease, in a general way, with increasing latitude and altitude so that arctic and alpine plants not only must survive low temperatures but spend much of their growing seasons in such temperatures. What are the relationships between temperature and metabolic rates in such plants?

In evaluating such temperature effects, one must attempt to separate those inherent in the genotype and those brought about by environment, since both sources of variation are present in the phenotype. There appears to be some degree of genotypic control over rates of net photosynthesis. Mooney, Wright & Strain (1964) found that plants of alpine and subalpine species in the White Mountains of California reached

5 1 0 W. D. BILLINGS AND H. A. MOONEY maximum photosynthesis at lower temperatures than did plants from lower elevations when all were grown under uniform greenhouse conditions. The same kind of situation occurs between arctic and alpine populations of both Oxyria digyna and Thalictrurn alpinurn (Mooney & Billings, 1961 ; Mooney & Johnson, 1965) with arctic populations having optima at lower temperatures than do alpine populations grown in the same environment.

r +3 i -c n

'0 6 0

E? 2 -3

-6

-9

-12

50 60 70 80 90 100 110

(OF.)

Fig. 3. Effect of temperature on rates of net photosynthesis and dark respiration of plants from an arctic and an alpine population of Oxyriu digyna grown at low temperatures (4-10" C.) and at high temperatures (21-32' C.). The effect of environmental history is greater than the ecotypic effect of the two widely separated populations. Arctic population seed source: Breiddalur, Iceland ; alpine population : Niwot Ridge, Colorado (from Billings & Godfrey, 1968).

Even though the genotypic effect is marked, the effect of environmental regime is greater. Plants grown under low temperatures not only show optimum photosynthesis shifted toward lower temperatures (Fig. 3) but the upper limit of positive net photosynthesis occurs at a decidedly lower temperature than that in plants acclimated to higher temperatures (Mooney & West, 1964; Billings & Godfrey, 1968).


The absolute temperature minimum for photosynthesis is also lower for alpine plants than in plants of lowlands or warmer climates. Pisek, Larcher & Unterholzner (1967) found that, in summer, Ranunculus glacialis and Oxyria digyna can carry on photosynthesis at temperatures as low as -6" C. while Mediterranean broad-leaved evergreens such as Citrus and Laurus had no net photosynthesis below - I" C. Some lichens can photosynthesize at temperatures as low as -24' C. but there appears to be only a slight relationship of this ability with the coldness of their natural environments

There is evidence that dark respiration rate at all temperatures is higher in alpine and arctic plants than in lowland or middle-latitude plants. This effect is both genetically and environmentally controlled. We (Mooney & Billings, 1961) found that an Oxyria population from the Arctic had higher respiration rates than did one from an alpine location in Colorado when grown under the same controlled environment. Clebsch (1960) found the same thing in arctic and alpine populations of Trisetum spicatum. However, Billings & Godfrey ( I 968) found relatively small genetic differences in respiration rates among seventeen latitudinal populations of Oxyria grown in uniform environments. On the other hand, there were great increases in these rates when the plants were grown at lower temperatures. Genetic differences in respiration rates within this species, then, appear to be far less important than the effects of environmental temperature (see Fig. 3). Furthermore, these environmental effects are reversible within a matter of days or even hours in a new environment.

Bjorkman & Holmgren (1961) found that leaves of an alpine ecotype of Solidago virgaurea had higher rates of respiration at the same temperatures than did leaves of a coastal ecotype when grown under the same conditions. Mooney (1963) found the same effect in alpine and lowland races of Polygonum bistortoides. At least a partial explanation of these genetic and environmental effects on respiration rate in alpine plants is provided by Klikoff (1966), who found that the oxidative rates of mitochondria in four altitudinal populations of Sitanion hystrix (grown under uniform conditions) showed a direct relationship at 20° C., with source elevation.

Eflects of light on photosynthesis. Photosynthetic adjustment to light in tundra plants is also both genetically and environmentally controlled. Mooney & Billings (1961) found that arctic Oxyrias reached photosynthetic light saturation at lower light intensities than did alpine populations. Clebsch (1960) had similar results in Trisetum spicatum. Bjorkman & Holmgren (1963), however, did not find this latitudinal effect in Solidago virgaurea from 55" 55' N. and 69" 35' N. This may have been because the latitudinal span was not as great as in the Oxyria and Trisetum populations and possibly because both Solidago populations were from relatively low elevations in contrast to the high source elevations of the alpine Oxyrias and Trisetums. They did find, however, a great effect of light intensity acclimation in these two populations. Plants grown at low light intensities (3 x 104 erg. cm.3. sec.-l) reached saturation at much lower intensities than those grown at high intensities (15 x 104 erg.cm.-Z.sec.-l) with the result that maximum net photosynthesis rates that could be attained were almost twice as high at 30 x 104 erg. cm.-2. sec.3 in the plants grown in bright light.

Temperature-light interactions. In nature, temperature and light interact with still

(Lange, 1965).

5 12 W. D. BILLINGS AND H. A. MOONEY other factors (and environmental history) to produce the daily photosynthetic curve. Relatively few measurements of photosynthesis of arctic and alpine plants have been made under field conditions. Cartellieri (1940) using a conductometric method, obtained maximum net photosynthesis rates of 9-13'5 mg. CO, . dm-, (two surfaces). hr-l with plants of several species in the Tirolean Alps. These compare quite well with our figures of 4.15-13.4 mg. CO,. dm-2 (two surfaces). hr-l (average = 9-32) using whole plants of four alpine species in an infrared gas analyser system in the Rocky Mountains (Billings, Clebsch & Mooney, 1966). Moser (1965) has measured photosynthesis in Ranunculus glacialis, Geum reptans and Oxyria digyna with a gas analyser at 3190 m. on the Hoher Nebelkogel in the Tirol but his results have not yet been published.

In the Arctic on Jan Mayen Island (71" N.) and Cornwallis Island (75O N.), Warren Wilson (1960), using the detached leaf method, found that for several species (including Oxyria digyna), the net assimilation rate was between 0-5 and 0.8 g . drn-,. week-l. This is about half the value obtained using the same method for plants in temperate regions. Warren Wilson ascribes this depression in rate to low temperatures, since mean July solar radiation at Resolute on Cornwallis Island is 5 10 langleys/day, almost twice the daily rate at London. Since the detached-leaf method ignores respiratory losses in the rest of the plant, Warren Wilson (1960, 1966) cautions against comparing such rates with gas analyser results and coming to an erroneous conclusion that arctic plants in the field have high photosynthetic rates.

Bjorkman & Holmgren (1963) found in Solidago ztirgaurea that the optimal temperature of photosynthesis increases with light intensity. Conversely, increased temperature results in a higher light-saturation level. Scott & Billings (1964) also found in several species of alpine plants from Wyoming that more light was needed for compensation and saturation with increasing temperature. Warren Wilson (1966) suggests that the lower light saturations of arctic plants at low temperatures may be due to accumulation of assimilates.

Carbon dioxide and oxygen ejfects. There is some evidence that alpine plants may be able to carry on photosynthesis at lower carbon dioxide concentrations than lowland or arctic forms. Using a closed infrared analyser system, Billings, Clebsch & Mooney (1961) found that with Oxyria plants of equal age and from a uniform environment, a subalpine population from Montana was more efficient at all carbon dioxide levels than an arctic sea-level population. The subalpine population also had positive net photosynthesis at carbon dioxide concentrations as low as 0.1 mg./l., which approxi- mates the carbon dioxide tension at an altitude of 12,200 m.; the arctic sea-level plants could not do this. Mooney, Strain & West (1966) found no apparent photosynthetic acclimation to differences in carbon dioxide tensions in plants of four species after being grown at two widely different elevations: 1250 m. and 3094 m.

While almost no work has been done on the effects of oxygen concentrations on field metabolic rates of alpine plants, rapidly decreasing oxygen concentrations with increasing altitude would lead one to suspect a pronounced effect on dark respiration rates, at least. On the other hand, normal oxygen concentrations (21 %) inhibit photosynthesis in vascular plants (Bjorkman, 1967); the photosynthetic rate increases at light saturation as oxygen concentration is decreased to zero. There may be some

The ecology of arctic and a&im plants 513 enhancement of photosynthesis at high altitudes due to low oxygen concentrations, but controlled field data are lacking.

Synthesis of information on metabolism. It is obvious that metabolism of arctic and alpine plants is controlled both by genetic variation and by past and present environments of the phenotype. The actual diurnal and seasonal course of photosynthesis and respiration is the resultant of complex interactions between these controls. With the information available at present, the effect of immediate past and present environment on the metabolism of an individual arctic or alpine plant seems to outweigh intraspecific genetic differences. These plants seem to have ample phenotypic plasticity in metabolism, particularly in regard to temperature. A large part of their ability to operate in cold environments is probably due to such an ability to acclimate their metabolism to low air temperatures. Ability to absorb solar radiation and thus raise leaf and stem temperatures may be helpful also in acclimation. More information is badly needed on the metabolic plasticity of the phenotypes of different ecotypes of alpine and arctic species. To do this, gas-exchange methods need to be standardized, environmental preconditioning controlled, and genetic stocks recognized.

Effects of water availability and use High mountains are rather efficient producers of precipitation, and as a result, most

alpine areas outside the trade-wind tropics are moist and covered with snow through most of the year. However, some mountainous areas, notably those in western North America, are subjected to summer drought of varying degrees of intensity. Much of the Arctic, because of low temperatures and cloud, is relatively moist, but the lowlands of the high Arctic are dry, even desert-like, because of low precipitation. In view of the occurrence of drought in certain arctic and alpine locations, we may ask what effect drought stress has on the plants.

A distinction should be made between drought stress during the summer growing season and drought stress produced by frozen soils and dry winds of winter. Tran- quillini ( I 964) indicates that plants in European alpine communities seldom are subjected to drought during the summer. However, during the winter, in exposed, snowless sites at timberline and above, evergreen shrubs and small pioneer trees are subjected to rigorous drought stress. On sunny days, such plants lose a great deal of water by cuticular transpiration in spite of closed stomates. This water cannot be replaced because of the frozen soil, and water stress becomes more severe as the winter goes on. The leaves lose much of their water and the osmotic value rises to over 40 atmospheres (Tranquillini, 1963, 1964; Larcher, 1963). Shrubs covered with snow, however, actually gain water by absorption so that the osmotic value drops during the winter. But if such plants (for example, Rhododendron ferrugineum) are denuded of snow in late winter, they lose water rapidly and may be killed since their drought resistance is low. On the other hand, certain dwarf or prostrate shrubs such as Loise- leuria procumbens, characteristic of open, snowless, windswept places, have low transpiration rates all year and tolerate the winter drought very well. According to Larcher, Loiseleuria can also take up surface meltwater late in the winter by shallow, adventitious roots when most of the soil is frozen.

514 W. D. BILLINGS AND H. A. MOONEY Winter drought stress also prevails in the mountains of western North America,

with the same general patterning into snow-protected and snow-free environments. Lindsay (1967) measured leaf-water potential in Picea engelmannii at timberline (3300 m.) in the Medicine Bow Mountains of Wyoming and also in the closed forest 250 m. lower in elevation. In the windswept, relatively snow-free timberline location, leaf-water potential stayed near or below -30 bars from September to early June, and only during midsummer did it rise to near -15 bars. With the drought of late summer, leaf-water potential decreased to its low winter values. In the forest location, leaf-water potential was higher throughout the year. Because of the deep snow cover in the forest, soil moisture was relatively more available throughout the winter; here, leaf-water potential did not go much below -20 bars, and this at the same time that water potential at timberline was -34 bars. Abies Zusiocarpa showed similar results.

The dry ridge-late snowbank environmental gradient is much sharper and extreme in the mountains of western North America than it is in most of Europe. This is due, partially, to the more regular incidence of late summer drought and the gradient is particularly pronounced in the Sierra Nevada of California. Here, the sandy granitic slopes and ridges are xeric environments in the long summer drought but the meadows below snowbanks are usually green and moist throughout the summer (Klikoff, 1965 a). We (Mooney, Billings & Hillier, 1965) have found that in the Sierra Nevada specific transpiration rates of alpine plants are closely related to the water supply of the habitat. Plants from moist sites have higher transpiration rates and little control over transpiration as compared with the more efficient water use of dry-site plants. Thus, water availability in the dry Sierran summer has much to do with the sharp vegetational patterning characteristic of the high Sierra.

Water stress which develops in these plants along the dry meadow-wet meadow gradient during the summer greatly affects photosynthesis Iates and thus productivity. Klikoff (1965 b) found that photosynthesis in Calamugrostis breweri (in the uniform environment of a growth chamber) decreased to almost zero at water potentials below - 10 bars but photosynthesis of Carex exserta, characteristic of dry meadows, was operating at almost maximum values at - 10 bars and at 25 % of maximum at water potentials as low as -20 bars.

It is clear that in both alpine and high arctic areas, windswept ridges and windward slopes are the principal stress environments, and that these are particularly severe in winter. The cushion plant, prostrate evergreen shrub, and dry tussock life forms are adapted as much to this winter drought stress as to that of summer. The summer drought on such dry sites comes earlier than in the moist meadows both in alpine and arctic regions. S~rensen (1941) has pointed out that summer drought may stop growth in such plants in north-east Greenland while temperatures are still favourable for growth. Billings & Bliss (1959) noticed the same effect in the alpine vegetation of Wyoming. Such cessation of growth due to late summer drought may be involved in the hardening preceding onset of dormancy. For example, Holway & Ward (1965) have noted that, in Geum turbinatum, time of dormancy onset is closely related to soil moisture with dormancy coming earlier in dry years.

The ecology qf arctic and alpine plants 515

Annual cycle of growth Breaking of dormancy. Dormancy may be broken in arctic and alpine plants as early

as April or May, or as late as August or September. The keys to time of starting of new growth are the melting of the snow-cover or, on snow-free areas, the increase of soil and lower air temperatures to about oo C. As Ssrensen (1941) has pointed out, dormancy may be broken and growth started in many arctic plants before the mean temperature of the day arises to oo C. ; the plants make use of even the few hours of positive temperatures around noon. Liquid water is another requirement for early growth; some growth may take place even under the old snow providing water is available on the soil surface or in the upper soil. A relatively long photoperiod appears to be important in breaking the dormancy of perennating buds in some species (Oxyriu digyna), but without positive temperatures there is no photoperiodic effect (Billings, Godfrey & Hillier, 1965).

Growth. Once dormancy is broken, growth of shoots is very fast. In spite of the low temperatures, it is here that the perennial nature of the tundra herbaceous plant is of decided advantage. The carbohydrates stored in roots and rhizomes are rapidly translocated to the young shoots and leaves (Mooney & Billings, 1960). In the bright light and low temperatures after snowmelt, these are not only incorporated into new tissue but a considerable amount into anthocyanins, so that the young vigorous shoots are often dark red. Such anthocyanins are effective in absorption of solar u.v., thus preventing damage to tissues (Caldwell, 1968).

Another common attribute of some fast-growing herbaceous stems of plants is the lack of pith in many species. The resultant hollow stem is efficient in the saving of materials, the rapidity of its growth, and the advantage of internal photosynthesis with recycling of carbon (Billings & Godfrey, 1967). Such stems can grow several centimetres in height in a day and the high respiration rate of this early-season growth provides an additional supply of carbon dioxide which is utilized within the hollow stem, where temperatures in sunlight may be as much as zoo C. above that of ambient air. These early phases of shoot growth are thus somewhat independent of temperature in the outside environment. After leaf expansion and development of a large supply of chlorophyll, however, further growth is rather closely tied to temperature until late in the season, when drought, photoperiod, and carbohydrate accumulation become involved.

Growth in the cold spells of arctic and alpine regions is fraught with several problems in mineral nutrition. Nitrogen is often limiting in the cold soils of the Arctic (Russell, 1 9 4 0 ~ ; Dadykin, 1952) probably due to the low rates of bacterial activity and also the relative lack of availability of certain other nutrients. Nitrogen build-up in pioneer arctic and subarctic ecosystems is aided by bacterial nodules on legumes and particularly on plants of Dryus (Lawrence, Schoenike, Quispel & Bond, 1967). Nitrogen apparently is not so often a limiting factor in many alpine environments, although Bliss (1966) found that dry-matter production on Mt Washington could be increased significantly only by adding large amounts of nitrogen fertilizer. Cold soils also appear to inhibit growth by suppressing the absorption of phosphorus (Korovin, Sycheva & Bystrova, 1963).

W. D. BILLINGS AND H. A. MOONEY Carbohydrate and lipid storage and use. The general course of the carbohydrate cycle

has been described by Russell (194ob) for arctic plants and by Mooney & Billings (1960) for alpine plants. Carbohydrates are stored in large amounts in roots and rhizomes at the end of the growing season. During the winter, because of low temperatures and dormancy, there is little use of these underground reserves. With the breaking of dormancy in early summer, the stored carbohydrates are utilized in the rapid early growth of the shoot and are depleted to a large degree. During this time, growth is SO

rapid that respiration far exceeds photosynthesis and food is used up faster than it can be made (Hadley & Bliss, 1964). This situation is maintained until shoot growth is 75-90y0 completed. Then, the respiration rate drops, shoot growth slows down, and replenishment of carbohydrate reserves commences. By the onset of dormancy, underground carbohydrate reserves are back to the highest level of the year.

The carbohydrate cycle is modified and changed during periods or whole growing seasons of cold, cloudy weather. Fonda & Bliss (1966) on Mt Washington found that an early August cold period during 1963 reduced shoot carbohydrates in Carex bigelowii from 22% to 13 yo and rhizome carbohydrates from 22% to 17’5%. How- ever, the warmer, sunny days later in the month allowed replacement of the utilized reserves. If there had been no more sunny weather, it is obvious that the plants would have entered winter with less than optimum supplies. Local differences in microsite also modify the carbohydrate cycle. Rochow (1964) found that root and shoot sugar contents in Caltha leptosepala were highest in those plants released from snow-cover late in June. Plants released in the middle of July had lower sugar levels and were unable to increase these levels because of the short growing season remaining. There appears, also, to be some tendency for carbohydrate content to decrease with increasing elevation, as we (Mooney & Billings, 1965) found in roots of Calyptridium umbellatum in California.

The principal reserve foods in alpine and arctic plants are starches, sugars, and lipids. In herbaceous plants these are mostly stored in roots, rhizomes, corms and bulbs, since few leaves remain during the winter. However, in low evergreen shrubs such as Diapensia lapponica and Ledum groenlandicum, Hadley & Bliss (1964) found that old stems and old leaves provided the principal storage reservoir for lipids and also for some carbohydrates. A similar situation occurs in the small evergreen alpine shrubs of New Zealand, where Bliss & Mark (unpublished) found 15-20% lipid content in the leaves of Celmisia viscosa.

There appears to be a close relationship between sugar content and cold resistance, although other factors such as environmental history are very important. Eagles (1967), for instance, found that a Norwegian population of Dactylis glomerata had significantly higher concentrations of soluble carbohydrates (fructosans) at lower temperatures than did a population from Portugal at the same temperatures; fructosan content in sheaths was rapidly reduced by rising temperatures. Sugar content (as opposed to starch) is often high at snowmelt and again just as dormancy sets in (Mooney & Billings, 1960). Parker (1963), in his recent review on cold resistance in woody plants, cites the almost universal correlation of increase in sugars with winter-hardening ; raffinose appears to be very important in this regard. Zavadskaya, Fel’dman & Kamentreva, (1964),

The ecology of arctic and alpine plants 517 working with Dactylis glomerata, Leucanthemum vulgare, Campanula persicifolia and Gagea lutea, say it may be concluded that in the species studied, high cold resistance goes hand in hand with accumulation of raffinose '.

Flowering. Since almost all alpine and arctic perennials have pre-formed flower buds (S~rensen, 1941 and others), the flowering in a particular season depends to a great extent on environmental conditions during the previous one or two summers. The production of flowers from these buds depends upon the completion of the initial stage of leaf and stem growth after snowmelt, upon temperature, and in some cases (particularly in arctic species or ecotypes) upon the interaction between temperature and photoperiod.

In Oxyria digynu, we (1961) found that no populations flowered under a 12 hr. photoperiod, populations from around 40' latitude flowered at 15 hr., but that arctic populations would flower only in very long photoperiods or in continuous light. Alpine populations flowered also under continuous light. Billings et al. (1965), working with seventeen Oxyriu populations under four photoperiodic regimes in the laboratory, found the same thing with more precision. The higher the latitude of origin, the greater the number of hours of continuous light or the longer the photoperiod needed for flowering. This is true not only for the elongation and flowering of the pre-formed bud but for the production of the pre-formed flowering primordia themselves. Both phenomena are tied to carbohydrate availability and neither flowering nor flower primordia initiation take place until the carbohydrate level is sufficient for normal survival. At short photoperiods, arctic populations of Oxyria seem to have difficulty in meeting this carbohydrate requirement; this may be partially responsible for the lack of initiation or aborting of inflorescences in such ecotypes when grown under relatively short photoperiods (Billings et al. 1965).

The photoperiodic effect in Oxyria is also tied to temperature; flowering occurs more rapidly at higher temperatures than at low temperatures under the same photoperiod. Each latitudinal population of Oxyria has its own combination of temperature and photoperiod ; alpine populations are better adapted to shorter photoperiods and higher temperatures and arctic populations better fitted to long photoperiods at lower temperatures. Mark (1965 b) found that flowering in snow tussock (Chionochloa rigida) in New Zealand depends upon the right combinations of long photoperiod and mild temperature minima. Since these relatively high minima do not occur every year, flowering in this grass tends to be irregular.

It has been suggested (S~rensen, 1941; Went, 1964) that some species of arctic or alpine plants may have a chilling requirement. Clebsch (1960) found this requirement in Trisetum spicatum, while Billings et al. (1965) found that although chilling was not a requirement in Oxyria, it did greatly speed up flowering in that species. Chilling requirements seem to be particularly important in bulbous plants such as Erythronium grandiflorum (Caldwell, 1967).

Pollination. Both arctic and alpine plants face pollination problems caused by low temperatures which confine insect activities to a few weeks, and even then mainly to the sunny daylight hours (Mani, 1962). The principal agents, of course, are insects, birds, and wind. Schroeter (1926) cites some data of Raddes from the high mountain

5 18 W. D. BILLINGS AND H. A. MOONEY flora of the Caucasus which shows that 89% of the species are insect-pollinated and I I % are wind-pollinated. Schroeter’s comparable figures from the Arctic (after Aurivillius) show that 32-38 yo are wind-pollinated. A few species are pollinated by humming-birds in some alpine regions (California: H. G. Baker, personal comm.) but these are completely lacking from the Arctic.

The principal kinds of pollinating insects in alpine locations are short-tongued bees, bumblebees, flies, butterflies, and moths. Bumblebees are more common above timberline in the Northern Hemisphere mountains than any other kinds of bees. In many places, they are the only bees present; they fly only during the daylight hours when air temperature is above about 10’ C. (Mani, 1962; L. W. Macior, personal comm.). Flies can and do work at lower temperatures and in dimmer light. As one ascends above 4000 m. in the Himalaya, bee-pollinated flowers disappear completely from the biota and one finds in their place a dominance of brightly coloured flowers pollinated by Lepidoptera and Diptera (Mani, 1962). Muller (1881) found a similar situation in the Alps.

Long-tubed flowers in Northern Hemisphere alpine areas are usually bumblebee- pollinated while small, flat flowers are mostly ‘fly flowers’ (L. W. Macior, personal comm.). While some species of bumblebees (e.g. Bombusfrigidus) are common in parts of the Arctic, Mosquin & Martin (1967) found that on Melville Island ( 7 5 O N.), bumblebees visited only scented flowers of Astragalus alpinus, Petasites frigidus, and perhaps Parrya arctica. They did not visit Pedicularis arctica, P. sudetica or Oxytropis arctica, which were unscented, or any of thirty-six other species with scentless flowers. Mosquin and Martin consider that Diptera are more important flower visitors in the Arctic than bees.

One of the striking differences between the alpine flowers of New Zealand and those of the Northern Hemisphere high mountains is the absence of bright-coloured flowers in alpine New Zealand and the prevalence of small, flat, white or yellow flowers. Heine (1937) explains this, at least in part, by pointing out that there were no long- tongued bees native to New Zealand, so that most insect pollination in the alpine zone there is by small insects, flies, and short-tongued bees.

Heterostyly and dioeciousness, while present in alpine locations of the middle- latitudes, are less important in the Arctic, with heterostyly being rare or not known there (Mosquin, 1966). In the most severe environments, self-pollination, apomixis, or vivipary are often the rule and cross-pollination is relatively rare.

Seedproduction. Seed production may or may not follow pollination depending upon whether the weather remains favourable or not. At higher latitudes and altitudes, years when any seed are produced become fewer, and even in relatively good years the amount of viable seed may be low. Holway & Ward (1965), for example, noted that several species of plants ( Trijolium parryi, Artemisia spithamea, Campanula rotundifolia) bloomed abundantly in the alpine regions of Colorado but failed to set seed. They examined several hundred pods of the Trifolium and found only twenty-eight seeds. Bliss (1956) noted that seed production decreases with an increase in severity of microenvironments in the same general region so that late snowbankpopulations, for example, of a given species may have poor seed-set while seed may be produced in abundance

The ecology of arctic and alpine plants 519 by plants of the same species in more favourable sites nearby. There is a tendency for seed weight to decrease with altitude in some species (Mark, 1965b).

Many arctic and alpine plants, however, do produce seeds rather regularly and in apparent abundance. Such seed, depending upon the species, ripens from mid- July to September. It is usually soon dispersed, often by wind or by falling from the follicle or capsule. In general, seed ripening is too late in most species for germination in that growing season. In fact, Porsild (1951) points out that fruits of some arctic species do not mature and dehisce until after snow arrives in the autumn and are dispersed with the drifting snow of winter.

Vegetative reproduction. As sexual seed production decreases and becomes unreliable in the most severe environments, vegetative reproduction seems to increase. Apomixis is particularly prevalent in tundra environments (Love, 1959). So, also, is the production of bulbils, as in Polygonum viviparum and a number of grasses. Grass bulbils frequently develop into young plants in the inflorescence ('vivipary ') ; these young plants may even flower (Trisetum spicatum growing in controlled conditions, Clebsch, 1960). In nature, the little plants fall to the ground while vegetative, and may become established. Such vivipary has often been deemed a taxonomic character (e.g. in Poa alpigenu var. colpodea), but Clebsch found in several populations of normally non- viviparous Trisetum spicatum that vivipary could be induced by manipulating the experimental environment.

The principal means of vegetative reproduction in both arctic and alpine plants is by rhizomes. Layering is also important in some species, particularly in cushion plants and prostrate shrubs. Intraspecific variation in rhizome production is sometimes coupled to environmental conditions. For example, we (1961) found that in North America, arctic forms of Oxyria digyna have rhizomes and often reproduce by them into clonal colonies. Western American Oxyrias south of about 60" latitude do not have rhizomes and thus reproduce by seed. Rhizome production in Oxyria is geneticdly controlled (Fig. 2).

Onset of dormancy. Under natural conditions, tundra plants beyond the seedling stage are seldom killed by the onset of winter weather. Some plants, such as Bruya humilis in north-east Greenland, may be caught by such weather in flowering or fruiting condition without any damage and resume growth and fruiting the following year (Serrensen, 1941). Normally, however, there is a period of shortening dayIength, lowering temperatures, and often increasing drought which tend to 'harden' the plant and induce a dormancy which prepares it for the oncoming winter. We (1961) found in all the American populations of Oxyria digyna with which we worked that a photoperiod of 12 hr. even at high temperatures induced the formation of a perennating bud which carried the shoot primordia through experimentally maintained winter (freezing) conditions. In further work, Billings et al. (1965) found that there was some tendency for arctic and subarctic Oxyrias to initiate perennating buds at photoperiods as long as 15 hr. and to have well-developed buds by the time the photoperiod had been dropped to 13 hr. Alpine populations from both America and Europe, however, did not form perennating buds until the photoperiod was down to 12 hr., at which day- length the bud was formed rather quickly.

5 2 0 W. D. BILLINGS AND H. A. MOONEY A somewhat similar photoperiodic effect on hardening itself was observed by Biebl

(1967) during some experiments in which he artificially shortened the summer photoperiod (early July) of some plants on Disko Island (West Greenland) to 8 hr. After 10 days of this treatment, plants of Salix glauca ssp. callicarpaea, Betula nana, Vacci- nium uliginosum and Empetrum hemaphroditum had increased resistance to heat. Additionally, the leaves of Betula nana showed an autumnal red colouring and were significantly more resistant to a 24 hr. freezing treatment. A clue to such a photoperiodic effect may be found in the work of Irving & Lanphear (1967). They showed that cold hardiness could be induced in Acer negundo, Viburnum plicatum tomentosum and Weigela jlorida by subjecting these woody plants of the temperate zone to short days followed by low temperatures. The same hardening could be brought about in long days by manually removing the leaves. These observations suggest the presence of a hardiness inhibitor which originates in leaves exposed to long days.

Shortened photoperiod and low temperatures are not the only factors involved in the onset of dormancy in alpine plants, and perhaps in some arctic plants also. Both Bliss (1956) and Billings & Bliss (1959) noted that cessation of growth and onset of dormancy in August in the Rocky Mountain alpine zone was determined by factors other than low temperature. In the 1959 paper it was hypothesized that soil drought limited growth and hastened dormancy. Holway &Ward (1965) found just this kind of response in Geum turbinatum in noting that the time of dormancy up until mid- September was controlled by the year-to-year variation in soil moisture. It seems obvious that in a wet year some other factors must eventually control dormancy in this species after mid-September ; most likely shortened photoperiod and low temperatures provide the stimulus for such a late move into dormancy.

IV. PRIMARY PRODUCTIVITY

Estimates of primary productivity and yield in alpine and arctic vegetation have been assembled by Bliss (1962~). Since then, Scott & Billings (1964) and Bliss (1966) have published more detailed analyses of field standing crops and productivities in two widely separated alpine regions. All values in this section are in grams dry weight unless otherwise specified.

One of the characteristic attributes of arctic and alpine tundras is the great proportion of standing crop which lies underground. Aleksandrova (1958) found as much as 810 g./m.2 of roots and rhizomes in an arctic tundra turf community. We found (1960) 1060 g./m.2 beneath a community of Geum turbinatum in the alpine tundra of Wyoming. In a similar mesic site, Scott & Billings (1964) measured a maximum underground standing crop of over 1100 g./m.2 while at the same time the above- ground crop was about 250 g./m.2; over 80 % of the biomass was underground. Xeric sites in the same vicinity had maximum underground biomass of less than 400 g./m.2 with above-ground crops of about 200 g./m.2. From these figures the relationship of the moisture gradient to standing crop in a cold climate is obvious; the effect on the underground crop seems to be greater than on the crop of shoots. The data presented above are maximum values for their sites; average values are somewhat lower. Never-


theless, even larger underground standing crops have been measured in alpine areas; Bliss (1966) found 3634 g.lm.2 in a sedge meadow on Mt Washington and Bliss & Mark (1965) measured living root biomass of 2120 g./m.2 under an alpine Celmisiu-Poa herbfield in New Zealand. The smallest standing crops, as might be expected, are in the most severe environments : colder, dryer, or those in the latest-melting snowbank areas.

Productivity may be based on an entire year, on the growing season, or on a single day. Since tundra is not productive at all for 70-907~ of the year, annual figures are low compared to most other terrestrial communities. Bliss (1962~) says that annual shoot productivities of tundra ecosystems are within the range 40-128 g.. m.-2. year-l but may be as low as 3 g.. m.-2. year-l in the high Arctic. Since these are for above- ground material only, they should be multiplied by a factor of about 3 for total productivity. Such figures would indicate that tundras on an annual basis are less productive than any other terrestrial ecosystems except those of extreme deserts (Rodin & Bazilovich, 1964).

While annual productivities of tundras are quite low, daily productivities during the short, cold growing seasons of 30-75 days are much more comparable to productivities in other parts of the world. In fact, they usually exceed comparable rates from deserts, grasslands, and on better sites even may be greater than those of culti- vated crops (Scott & Billings, 1964). In terms of average shoot production alone during the growing season, alpine communities range from about 0.5 to 5-0 g.. m.-2. day-l (Bliss, 1966), but if root productivity is included the rate may be as high as I I g., m.-2. day-l on moist sites (Scott & Billings, 1964). Arctic productivity is generally somewhat less than that in the better alpine sites although, except for those of Aleksandrova (1958), arctic data are rare. New Zealand alpine productivity is also lower than that of Northern Hemisphere sites on a daily basis because of low daytime temperatures. However, since the New Zealand alpine growing season is 2-3 times longer, the annual productivity is about the same (L. C. Bliss, personal comm.).

Up to the present time, almost all tundra productivity has been presented in terms of dry weight. Better productivity estimates could be made by utilizing caloric values. Bliss (1962~) found that caloric values for alpine shrubs and herbs are significantly higher than for many tropical and temperate plants. This could indicate that tundra productivities are even higher relative to those in milder regions than the dry weight figures imply. Highest caloric values are in the evergreen prostrate shrubs, reflecting their higher lipid contents.

A very practical question may be asked: 'How can productivity be increased in tundra ecosystems? ' The most obvious answer would be to increase the factors which are limiting: temperature, soil nutrients, or water. We (Billings et ul. 1965) have some controlled experimental evidence with Oxyriu digynu shoot yield to indicate that productivity, in this species at least, is environmentally controlled in the field and can be increased a great deal by increasing the temperature in which the plants are growing. Under continuous light in a cold temperature regime (daily cycle 4-10' C.) for 48 days, an alpine Oxyriu population from Niwot Ridge, Colorado, had an average shoot productivity of 4.40 g.. m.-2. day-l, while one from Thule, Greenland, in the

34 Biol. Rev. 43

W. D. BILLINGS AND H. A. MOONEY same regime had 1-66 g.. m.-2. day-l. These are quite comparable to field figures for a similar growing season. Under a warm regime (16-27" C.), however, the rate for the Niwot population rose to 21.20 g.. m.-2. day-l while that from Thule was 5-58 g.. m.-2. day-l, both far above field figures for their respective regions. Even neglecting the relatively ideal growing conditions, the genetic potential for higher productivity appears to be present even in the dwarf Thule population from the high Arctic. Because of root carbohydrate depletion, the daily rates were decreasing at the high temperature at the end of the experiment. However, they were increasing at that time under the low-temperature regime so that the Niwot population was producing shoot dry weight at the rate of 6.28 g.. m.?. day-l. At an intermediate temperature regime (7-18" C.), the rate for Niwot was holding steady at ca. 16 g. .m.-2. day-l, a very high rate by field standards, and with carbohydrates apparently being maintained. The high Arctic population, however, could hold its own only at the low temperatures.

The addition of certain mineral nutrients will increase productivity in certain locations. Bliss (1966) found under the cold field conditions of M t Washington that addition of large amounts of nitrogen fertilizer would increase productivity. Similar experiments in other alpine regions have often showed no increase in productivity, however. Additions of phosphorus might also increase productivity in some tundra locations.

Since drought stress is a common phenomenon in some western American alpine environments, the addition of irrigation water would probably increase productivity in such places. However, because of the postulated role of drought in the onset of dormancy, the effect of late irrigation on survival should be studied before its value can be estimated.

The real problem in increasing tundra productivity is that most of the biomass increase is underground and not available for harvest by domestic animals or by any other means. Moreover, if one is to assume that most wild tundras are in a steady state over a long period of years, any method which tends to deplete these underground reserves is self-defeating since they are necessary to the survival of the producing plants themselves.

V. SUMMARY

' How are plants adapted to the low temperatures and other stresses of arctic and alpine environments?' At present it is not possible to answer this question completely. Much work remains to be done, particularly on low-temperature metabolism, frost resistance, and the environmental cues and requirements for flowering, dormancy, regrowth, and germination. However, in brief, we can say that plants are adapted to these severe environments by employing combinations of the following general characteristics :

I . Life form: perennial herb, prostrate shrub, or lichen. Perennial herbs have greatest part of biomass underground.

2. Seed dormancy : generally controlled by environment ; seeds can remain dormant for long periods of time at low temperatures since they require temperatures well above freezing for germination.

The ecology of arctic and alpine plants 523 3. Seedling establishment: rare and very slow; it is often several years before a

seedling is safely established. 4. Chlorophyll content: in both alpine and arctic ecosystems not greatly different

on a land-area basis from that in temperate herbaceous communities. Within a single species there is more chlorophyll in leaves of arctic populations than in those of alpine populations.

5. Photosynthesis and respiration: (u) These are at high rates for only a few weeks when temperatures and light are

favourable. ( 6 ) Optimum photosynthesis rates are at lower temperatures than for ordinary

plants; rates are both genetically and environmentally controlled with phenotypic plasticity very marked.

(c) Dark respiration is higher at all temperatures than for ordinary plants; rate is both genetically and environmentally controlled, with phenotypic plasticity very pronounced, i.e. low-temperature environment increases the rate at all temperatures.

( d ) Alpine plants have higher light-saturation values in photosynthesis than do arctic or lowland plants ; light saturation closely tied to temperature.

( e ) There is some evidence that alpine plants can carry on photosynthesis at lower carbon dioxide concentrations than can other plants.

(f) Annual productivity is low, but daily productivity during growing season can be as high as that of most temperate herbaceous vegetation. Productivity can be increased by temperature, nutrients, or water.

6 . Drought resistance: most drought stress in winter in exposed sites is due to frozen soils and dry winds. It is met by decreased water potentials, higher concentrations of soluble carbohydrates, and closed stomates. Little drought resistance in snowbank plants. Alpine plants adapted to summer drought stress can carry on photosynthesis at low water potentials; alpine or arctic plants of moist sites cannot do this.

7. Breaking of dormancy: controlled by mean temperatures near or above oo C., and in some cases by photoperiod also.

8. Growth: very rapid even at low positive temperatures. Respiration greatly exceeds photosynthesis in early re-growth of perennials. Internal photosynthesis may occur in hollow stems of larger plants during early growth. Nitrogen and phosphorus often limiting in cold soil.

9. Food storage: characteristic of all alpine and arctic plants except annuals. Carbohydrates mostly stored underground in herbaceous perennials. Lipids in old leaves and stems of prostrate evergreen shrubs. Depleted in early growth, and usually restored after flowering.

I 0. Winter survival : survival and frost resistance are excellent after hardening. Cold resistance closely tied to content of soluble carbohydrates, particularly raffinose.

I I. Flowering: flower buds are pre-formed the year before. Complete development and anthesis dependent upon temperature of the flowering year and also, in some cases, upon photoperiod.

12. Pollination: mostly insect-pollinated in alpine regions and even in Arctic, but to a lesser extent. Wind-pollination increasingly more important with increasing

34-2

524 W. D. BILLINGS AND H. A. MOONEY latitude. Diptera more important than bees in the Arctic and in the highest mountains.

13. Seed production: opportunistic, and dependent upon temperature during flowering period and latter half of growing season. 14. Vegetative reproduction : by rhizomes, bulbils, or layering. More common and

important in Arctic than in alpine areas. 15. Onset of dormancy: triggered by photoperiod, low temperatures, and drought.

Dormant plant extremely resistant to low temperatures.

This review is an outgrowth of research supported by National Science Foundation Grants GB-1219 and G-5501, for which we are appreciative.

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THE ECOLOGY OF ARCTIC AND ALPINE PLANTS