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Article in press (2007), Journal of Sustainable Forestry [G.P. Berlyn Festschrift Special Issue, Volume 25, Issue 1-2] A review of the theories to explain and alpine treelines around the world†

Andrew D. Richardson1* and Andrew J. Friedland2

ABSTRACT growth is restricted at high and high elevations, and the limits of growth in these environments are dramatically marked by the treeline transition from vertical, erect tree stems to prostrate, stunted shrub forms. However, after four centuries of research, there is still debate over the precise mechanism that causes Arctic and alpine treelines. We review the various theories for treeline, including excessive light, low partial pressure of CO2, snow depth, exposure, reproductive failure, frost drought, and temperature. Some of these theories are very old and are no longer held in high esteem; while they may help to explain treeline physiognomy or local variation in treeline position, they generally fail as global explanations. Temperature- based theories appear to be the most reasonable, since cold temperature is really the only trait that is universally characteristic of treelines around the world. Temperature may limit a variety of physiological processes, such as carbon fixation, cuticular ripening, or new tissue development, and theories invoking these mechanisms are discussed. The vertical growth habit of is unfavorable to growth in this hostile environment: low- profile vegetation enjoys a far more favorable microenvironment for growth. Recent evidence gives strong support for a theory based on “sink limitation”, i.e., that new tissue development is restricted not by carbon availability but by cold treeline temperatures which limit cell division, and that this situation is exacerbated by arborescent growth (above-ground meristems coupled to cold ambient air temperatures) and self-shading (which keeps soil temperatures cold and restricts below-ground activity).

KEYWORDS. Alpine, Arctic, biogeography, climate change, elevation, forest limit, , , montane , sink limitation, sub-alpine, treeline.

1Andrew Richardson is a Research Scientist at the University of , Complex Systems Research Center, Durham NH 03824. 2Andrew Friedland is a Professor and Chair of the Environmental Studies Program, Dartmouth College, 6182 Steele Hall, Hanover NH 03755. *Corresponding author. Mailing address: USDA Forest Service, 271 Mast Road, Durham NH 03824 USA. Tel: 603 868 7654, Fax: 603 862 0188, e-mail: [email protected]

†This is a contribution to the Festschrift in honor of Professor Graeme Berlyn and his long career at the Yale School of Forestry and Environmental Studies. Our choice of topic is a tribute to Graeme’s lifelong interest in Arctic and alpine ecosystems, and his participation in numerous studies of the environment (see Fig. 1). We thank Jim Kellner for helpful comments on the manuscript.

THE CAUSES OF ALPINE AND ARCTIC TREELINES

INTRODUCTION Treelines are phenomena that occur at the transition from forestland to some other type of vegetation, such as between forest and grassland, or at the margins of a or : treelines are therefore a “tension zone” (Griggs, 1934). Causes of treeline can be varied, but include abiotic factors (e.g., temperature, salinity, drought, waterlogging, or soil nutrients), and disturbance, both natural (e.g., fire), and anthropogenic (e.g., timber harvesting, development or agriculture). [FIGURE 1 ABOUT HERE] One of nature’s most dramatic examples of treeline is the border marking the upper limit of forest growth, i.e., the alpine (high elevation) or Arctic (high latitude) treelines that will be the focus of this review paper (Fig. 1). These treelines may be sudden or indistinct (Fig. 2), they may be wavy or straight, and they may advance or recede over time. Here our goal is to review the theories, both historic and current, that explain alpine and Arctic treelines. We will limit our discussion to those treelines that are climate-driven, and ignore anomalies such as the grass balds of the southern Appalachians, for which there are other causes (Mark, 1958). [FIGURE 2 ABOUT HERE] Air cools as it rises and consequently the air temperature decreases at a rate intermediate between 0.50°C/100 m (the saturated adiabatic lapse rate) and 0.98°C/100 m (the dry adiabatic lapse rate). On average, the lapse rate is usually about 0.60°C/100 m increase in elevation (Barry, 1992; Körner, 1999; Richardson et al., 2004). Temperature also generally decreases with increasing latitude. This occurs because at higher latitudes the sun’s radiation is less direct. Richardson et al. (2003a) calculated that mean annual temperature in decreases by 1.15°C per degree increase in latitude, and based on these data, they concluded that a 1°C increase in latitude was roughly comparable to a 192 m increase in elevation. Humbolt’s Law, which dates to 1817, proposes that in terms of temperature, latitude compensates for altitude, and treeline thus occurs at a lower elevation as one moves from equator to Arctic (Salisbury and Ross, 1992). There are, however, differences between alpine and Arctic (Billings, 1973), and there are similar differences between sub-alpine and sub-Arctic. Generally the sub-alpine zone has greater light intensity and more UV, with less annual day length variation but more diurnal temperature variation, than the sub-Arctic. However, both sub-alpine and sub-Arctic frequently have short growing seasons, low temperatures and high (Berlyn, 1993). Low temperature is one of the few factors globally common to both. Many authors differentiate between Arctic and alpine treelines, Arctic treelines being associated with increasing latitude, and alpine treelines being associated with increasing altitude. However, in some of the world’s high-latitude mountain ranges, it is difficult to distinguish between the two. An example of this is the Richardson (Yukon-NWT border, 67°-70°N in Canada), where the forest limit is determined both by high latitude and altitude. In most cases, the distinction between Arctic and alpine is more easily made. The scientific study of treeline has a long history, as according to Troll (1973), it began in the Swiss during the 16th and 17th centuries. Despite four centuries of research, there is not yet a consensus theory to explain Arctic and alpine treelines universally around the world. However, some explanations are more valid than others at a universal level, whereas some theories seem to provide good explanations for local

THE CAUSES OF ALPINE AND ARCTIC TREELINES variation in treeline positions. The purpose of this paper is to assess the arguments both for and against the theories that have been popular in the past and those that are popular now. We will begin by offering some definitions of treeline and describing the physiognomy of different treelines around the world, and then proceed to an assessment of the different theories. In recent years, there has been a renewed interest in treeline research, spurred on by concerns about human-induced climate change and potentially dramatic changes in high-mountain vegetation patterns. A better understanding of the controls over treeline location will enable better predictions to be made about the effects of climate change on these climate-sensitive indicator ecosystems.

DEFINITION OF TREELINE Different definitions of tree, forest, timber, and line complicate things somewhat. For example, although most authors agree that trees are erect, woody stems, Troll (1973) insists on a minimum height of 5 m, whereas Körner (1998) specifies 3 m, and Wardle (1974) settles for 2 m. These authors therefore distinguish between “trees” and the prostate, stunted “Krummholz” (from the German for “elfin wood”) found at the extreme limits of growth. Körner defined timberline to be the limit of closed forest, but noted that this transition is rarely abrupt: with increasing elevation or latitude, tree size generally decreases gradually while at the same time the canopy opens up. Wardle (1965) defined timberline to be the upper limit of tall, erect timber-sized trees. Treeline marks the highest patches of forest across slopes of similar according to Körner (1998), but in Daubenmire’s (1954) nomenclature, the forest line is the upper edge of continuous forest and is the elevation of the highest “tree”, whether Krummholz or not. We acknowledge that these terms all have somewhat different connotations. For the purpose of this paper, however, we wish to keep a broad view of treeline, for the delineation of any line or limit is inherently subjective. It is important to focus on the phenomenon of interest (rather than semantics), namely the vegetation change, be it gradual or sudden, from tall trees to prostrate shrubs that occurs at high elevations and high latitudes. We follow Wardle’s (1974) definitions, but will use the term treeline rather than Wardle’s tree limit. Thus: treeline is the extreme limit of trees and tall shrubs (more than 2 m in height). Trees growing closely together make a forest and therefore define the forest limit. In some places, forest limit and treeline are the same (e.g., most Nothofagus in ). In other systems, there may be a zone of parkland between forest limit and treeline, or the trees between the forest limit and treeline might be stunted and deformed Krummholz: in this case, treeline is the point where Krummholz with flagged stems changes to prostrate Krummholz. We consider vegetation immediately below the treeline to be sub-alpine (or, as the case may be, sub-Arctic) whereas vegetation above the treeline is alpine (or Arctic).

GENERAL PATTERNS OF TREELINE Treeline elevations range from near sea level, as in and Alaska, up to 4,700 m in Tibet and 5,000 m in the of and (Troll, 1973). Treeline elevation generally increases as one moves from the poles to the equator, but there is a wide variation in treeline elevation at a given latitude. Aspect, prevailing winds, soil quality, and the height of surrounding mountains are thought to cause local variation

THE CAUSES OF ALPINE AND ARCTIC TREELINES in treeline (Daubenmire, 1954). Human use, grazing, and fire are all disturbances which can also have indirect effects on treeline elevations (Wardle, 1974). At night, cold air drainage onto floors may create what is known as an “inverted treeline”. In the humid tropics, treeline is generally higher in valleys or gullies rather than on ridges, but the reverse is often true in the temperate zone (Troll, 1973). There is more variability in treeline elevations in the than the southern hemisphere. This may be due to the prevalence of interior or continental mountains in the northern hemisphere, which are more or less absent in the southern hemisphere (Körner, 1999). This difference is significant because of the large mountain mass effect, “Massenerhebungseffekt”, whereby the adiabatic lapse rate is generally lower on large mountains (or in the middle of a mountain range) than small mountains (or at the edges of a mountain range). Treeline thus occurs at higher elevations in the middle of a range compared to the edges, due to less moisture, more sun, and less exposure—all of which contribute to warmer temperatures (Daubenmire, 1943; Barry, 1992; Körner, 1999). Coastal mountain ranges similarly have lower treelines than inland ranges. For example, treeline in the Cascade Range (Pacific Northwest) or White Mountains (New England) occurs at about 1500 m, compared to 3000 m in the (). Nevertheless, within a mountain range there is a fairly consistent latitude- elevation relationship for treeline between 35° and 70°N latitude, as demonstrated by Daubenmire (1954). The y-axis (elevation) intercept changes somewhat among mountain ranges, but the slope is relatively constant: the elevation of treeline decreases by approximately 110 m for each 1° increase in latitude. Below 35°N, the relationship flattens. The relationship is a bit different in the southern hemisphere, but the slope appears similar. Using a larger data set, Körner (1999) reports that from 45°N to 70°N, the ratio is 45 m for every 1° latitude. From 30°N to 50°N, the slope is almost three times as great: 130 m for every 1° latitude. In the northern Appalachians, the alpine treeline decreases from 1480 m at 44°N to 550 m at 55°N. This corresponds to an 83 m decrease in treeline elevation for every 1° increase in latitude (Cogbill and White, 1991). Due to the fact that treeline can vary significantly both among mountains in the same range and even at different points on the same mountain, it seems unlikely that any single treeline theory can be applied to the entire world’s Arctic and alpine treelines, regardless of latitude or continent. Rather, we should perhaps look for a general theory that predicts the approximate treeline location, and then consider what factors might be responsible for local or smaller scale variation (Körner and Paulsen, 2004). Assessment of treeline theories is complex because treeline position can change over time with climatic change. It is important to ask whether present treelines indicate current climatic conditions, or past climatic conditions? Trees are long-lived and fairly resilient to environmental change, whereas germinating seeds and seedlings may die during even relatively short spells of unfavorable weather (Slatyer and Noble, 1992; note that the age structure at treeline tends to be “top heavy”, see Stevens and Fox, 1991), so the answer is more likely past climatic conditions (Körner, 1998). For example, when treeline is advancing, changes in treeline will lag behind changes in climate because seedlings must not only become established (out competing existing vegetation), but then survive long enough, and grow large enough, to be identified as treeline individuals. Furthermore, when treeline recedes, existing trees have to die, which may also take time.

THE CAUSES OF ALPINE AND ARCTIC TREELINES

Treeline position and climate are therefore not likely to be in perfect equilibrium. The timescale of this mismatch is not entirely clear, but it is more likely in the years-to- decades range, rather than centuries. These observations are significant because only if a treeline is stable and truly representative of current conditions can valid experimental tests of treeline hypotheses actually be carried out (Beaman, 1962; Stevens and Fox, 1991). It is also important to note that the variability in climate from year to year may mask climate-treeline relationships unless the data record is long enough. As pointed out by Griggs (1934), the treeline is a “mobile migration front” rather than a “static climatic boundary”. In Kodiak, AK, treeline is very sudden (Griggs, 1934), with no crippled or deformed trees, no Krummholz, and no dead trees at the margin between Sitka spruce forest and alder grassland. Cone production is abundant, and there is significant reproduction beyond treeline. Griggs deduced that the forest border at Kodiak is actually advancing, and that it has advanced at a rate of about 15 m/yr for at least the last few centuries. Fonda and Bliss (1969) describe alpine invasion by in the Olympic Mountains, WA. Forest reversion to has been noted in the central Yukon Territory (Cwynar and Spear, 1991). Climatic warming has been associated with the advance of the treeline in the Range, BC (Brink, 1959). In parts of Scotland, the treeline is at 600 m, but stumps dated to 5,000-9,000 years ago have been found in the peat at 800 m. Similarly, there is evidence from that the treeline has dropped by 200 m over the last 8,600 years (Grace, 1989). Changes in treeline position appear strongly correlated with changes in temperature. Using historical data, a 1°C change in annual temperature was shown to translate to a 100 m change in treeline elevation (Grace, 1989). Various temperature-based theories about treeline will be discussed in greater detail below.

TRENDS IN ABIOTIC FACTORS WITH REGARD TO ELEVATION AND LATITUDE It may be dangerous to make broad generalizations, but in an attempt to characterize high-elevation and high-latitude treelines, we offer Tables 1 and 2, which highlight some of the important differences between low and high elevation and low and high latitude. Note that auto-correlation among climatic variables may make it difficult to determine the precise mechanism responsible for treeline (Körner 1998). It is therefore important to remember that correlation does not necessitate causation. [TABLE 1 ABOUT HERE] [TABLE 2 ABOUT HERE] The tremendous diurnal variation in temperature at high elevations in the tropics is worth special mention: this has been described as causing summer every day and winter every night because there is a diurnal pattern of freeze-thaw not commonly found in temperate high-elevation areas. Rather, in the temperate zone, such temperature extremes are observed only across seasons (Smith and Young, 1987). More detailed data can be found in Körner (1999) and Barry (1992). Bliss (1956) compares the of Arctic and plants, including valuable data on radiation, temperature, wind and precipitation. What becomes apparent from these tables is that the sub-Arctic and sub-alpine are in many ways dissimilar. Is it reasonable to expect a single explanation to apply for both high-elevation and high-latitude treelines?

THE CAUSES OF ALPINE AND ARCTIC TREELINES

DIFFERENCES IN TREELINE PHYSIOGNOMY Treelines occur from 70°N to 55°S, across virtually every climatic zone and a wide range of plant families, e.g., Fagaceae, Ericaceae, Pinaceae, Podocarpaceae, and Rosaceae. Evergreenness appears to confer certain advantages at high elevations, since evergreen Pinaceae species such as spruce (Picea), fir (Abies) and sometimes pine (Pinus) form most alpine treelines. Other , such as hemlock (Tsuga), (Juniperus), and cypress (Chamaecyparis), have local representation at treeline in some parts of the world. Evergreen species can photosynthesize year-round whenever conditions are favorable; deciduous trees can only photosynthesize following spring flush and before are dropped in the autumn (or wet/dry season, depending on the local pattern). Furthermore, many conifers have highly xeromorphic leaves that are very resistant to the desiccation that is common at high elevations and high latitudes. However, deciduousness may also have some advantages in extreme environments, such as reduced water loss during times of low potential photosynthetic activity, or reduced trapping of snow, which could minimize broken branches. Indeed, the deciduous larch (Larix gmelini), a , is known to form the Arctic treeline in , at 72°30’N. Some birch (Betula) species form the treeline in Japan, Scotland, Russia, and parts of Scandinavia, and other angiosperms, such as alder (Alnus), beech (Fagus), mountain ash (Sorbus), poplar (Populus) are also found at treeline in other parts of the world. The physiognomy of treeline varies among regions around the world. In temperate regions, there is generally a progression from closed forests of large timber (broadleaf species at the base of a mountain, conifers higher up), to smaller and more widely-spaced trees (the Kampfzone), to shrubby, deformed and often prostrate Krummholz, to treeless alpine vegetation (Berlyn, 1993). However, this pattern is by no means universal. For example, in the Rocky Mountains of Alberta, tall Picea and Abies define the forest limit, and although somewhat stunted trees of these two species continue to the treeline, there is generally no evidence of flagging or deformation (Wardle, 1965). On the other hand, in Colorado, similar species form the irregular but clearly-defined forest limit and less- clearly-defined treeline, but beyond the treeline there are often many flagged, prostrate, and deformed Krummholz thickets (Griggs, 1946; Wardle, 1965). Griggs (1946) observed many seedlings above treeline: he suggests they germinated from seeds blown up from low elevations, since the highest elevation trees seldom produce cones or viable seed. At high elevation in the northern Appalachians, dwarfing of balsam fir begins as much as 600 m below treeline (Griggs, 1946). This is in contrast to the pattern in the northern Rockies, where tall, large-diameter trees are found right up to treeline (Griggs, 1938). In the Appalachians, Griggs reported that flagging occurs when an individual stem is higher than surrounding stems. However, the vertical growth habit is maintained and stem density remains extremely high all the way to treeline. Above treeline, islands of Krummholz scrub continue to within 300-600 m of the summit of Mt. Washington (1916 m above sea level), although some individual stems survive in sheltered locations within 25 m of the summit. In the southern hemisphere, the pattern is usually quite different. First, most treeline species are broadleaf evergreens from many different families. There is much more diversity in species mixture than in the northern hemisphere. A variety of mountain beech (Nothofagus) and eucalypt () species form treeline in different parts of New Zealand and Australia, where treeline tends to be very abrupt and clearly-defined,

THE CAUSES OF ALPINE AND ARCTIC TREELINES and there is no Krummholz (Wardle, 1965). On the other hand, at high elevation in the humid tropics there is often a very sudden treeline without Krummholz, rather just a rapid transition to Páramo grasslands (high Andes) or Afro-alpine (east and central Africa) vegetation (Troll, 1973). In South America, high-elevation vegetation and may include “megaphytes”, or large arborescent herbs, such as Espeletia, which may or may not be considered trees. Similar ambiguous examples, sometimes involving tree ferns (e.g., Cyathea) are common in the mountains of both Africa and (Wardle, 1974). These differences in treeline physiognomy around the world are significant because they once again bring into question the existence of a single treeline-determining factor that can be considered universal across both alpine and Arctic treelines.

THEORIES TO EXPLAIN TREELINE We will now review and critique the major theories advanced to explain the location of treeline. Quite a few of these are more than half a century old and they are not currently held in high esteem. Nevertheless, presenting them here provides historical context and information upon which the newer theories are based. As will be seen, few theories actually enable direct prediction of treeline location. Most theories fail to account for differences in seasonality between temperate and tropical treelines. Other theories fail to account for the sudden shift, by a single species, from vertical to prostrate growth form that is found at most treelines.

Excessive light On clear days, radiation intensity at high elevations can be severe in some mountain ranges, and one early theory for treeline suggested that treeline marked the point at which light intensity became too high for trees to withstand (reviewed by Daubenmire, 1954). Unfortunately, this theory doesn’t explain the presence of treelines in foggy coastal mountains, like the and Coast Ranges of the Pacific Northwest. In the White Mountains of New Hampshire, incoming solar radiation differs little between low and high-elevation, despite frequent clouds at high elevation, and yet the treeline is as low as anywhere in the coterminous United States (Richardson et al., 2004). Nor does the theory give any explanation for why alpine shrubs and herbs can tolerate the high light intensity, but trees cannot.

Low CO2 partial pressure Because the barometric pressure decreases with increasing elevation, the partial pressure of CO2 is lower at high elevations. Treeline has been attributed to the effects of reduced CO2 on photosynthetic rates (reviewed by Daubenmire, 1954). However, Gale (1972) argued on theoretical grounds that the depressed partial pressure of CO2 may have little effect on the availability of CO2 for photosynthesis in plants, because the diffusivity of CO2 increases at roughly the same rate as the partial pressure decreases; this has been further debated by others (Cooper, 1986; Gale, 1986; Lamarche et al., 1986; Terashima et al., 1995). In any case, it cannot explain the decrease in treeline elevation that occurs with increasing latitude, since changes in barometric pressure with elevation are more or less independent of latitude.

THE CAUSES OF ALPINE AND ARCTIC TREELINES

Snow depth Snow depth may modify treeline elevations to some degree since snowpack that lingers to mid-summer can significantly shorten the already-short growing season at high elevations and high latitudes. For example, in parts of the Selkirk Mountains, BC, snow accumulates in depressions and remains there through the end of the summer: this prevents establishment of seedlings in hollows, while nearby snow-free ridges at the same elevation often have mature stands of timber (Daubenmire, 1954). Fonda and Bliss (1969) similarly attribute local depression of treeline in the Olympic Mountains, WA, to late snowmelt. But this theory cannot explain why snow-free ridges at high elevations don’t have trees, nor why some tropical mountains with little or no annual snowfall still have treelines. Variation in snow pack probably is a highly significant factor in local treeline variation in some parts of the world.

Wind Wind appears to play a role in many northern hemisphere treelines, since flagging and desiccation of high-elevation trees are common (Griggs, 1938; Lindsay, 1971; Hadley and Smith, 1983) and may cause breakage or buckling of exposed branches and even trunks. Strong prevailing winds may cause eccentric stems to develop (in the direction of wind loading), and may, in extreme cases, result in the formation of reaction wood (G.P. Berlyn, pers. comm.). In many instances, only sheltered individuals can survive at highest elevations, and treeline is often higher on leeward slopes. Wind is thought to be a major factor determining treeline in the northern Appalachians, since summer treeline temperatures are considerably warmer than have been reported at other treeline sites around the world, and Krummholz showing evidence of wind damage is abundant (Cogbill and White, 1991). Based on studies with Picea and Abies, Hadley and Smith (1983) concluded that winter snow might protect prostrate Krummholz mats from desiccation by high winds. They showed that exposed shoots suffered from wind abrasion that resulted in low cuticular resistance. However, since wind abrasion does not appear to be a factor near the equator or in the southern hemisphere (Daubenmire, 1954), it seems clear that while wind may cause local variation in treelines, it is not the driving force behind Arctic and alpine treelines in general. Furthermore, Marchand (1996) has argued that winter wind will actually decrease transpiration, and others have found little evidence for a wind effect (Baig and Tranquillini, 1980; Sowell et al., 1982). With the above arguments in mind, however, wind seems to be a convincing explanation for some of the variation in physiognomy seen in the world’s treelines.

Reproduction Reproduction rates at treeline are often quite low: seed development, dispersal, germination, and seedling establishment are all limited by cold (although dispersal is enhanced by wind). It has been hypothesized that reproductive failure or recruitment limitation may be a defining characteristic of high-elevation and high-latitude treelines (see Stevens and Fox, 1991, and discussion by Körner, 1998). However, there is little evidence to support this hypothesis (Tranquillini, 1979; Körner, 1998). Although Wardle’s experiments (1965, 1971) showed that young seedlings can be especially susceptible to the stresses experienced at treeline (see also Johnson et al., 2004), seedlings and even dwarfed trees are often found above the treeline (Griggs, 1946): the

THE CAUSES OF ALPINE AND ARCTIC TREELINES question is, why do they not develop into forest (Körner, 1998)? The reason for this is probably that there is a climatic constraint imposed by getting out of the warm boundary layer found near ground level (Körner, 1998; Smith et al., 2003); the prostate growth form of Krummholz may be an adaptive response to remain within this boundary layer.

Winter Desiccation: Frosttrocknis Frost drought, or Frosttrocknis, occurs during late winter when the soil is frozen but skies are clear and solar radiation is high: as exposed foliage warms in direct sun, a strong vapor pressure deficit is created, evapotranspiration from the is high, and desiccation occurs. Frost drought is accepted as a major cause of shoot dieback at timberline in the European (Daubenmire, 1954) and Japanese (Sakai, 1970) Alps. Although this may play a role in determining treeline in these ranges, it is not thought to be a universal phenomenon (Marchand and Chabot, 1978; Kincaid and Lyons, 1981; Körner, 1998). For example, in a study of three conifers in the elevations just below treeline in New England, Vostral et al. (2002) did not find evidence of winter desiccation stress in any of the species. Furthermore, winter frost drought does not occur in aseasonal tropical mountain ranges. Interestingly, frost drought is not likely to happen in the coldest part of the year, which may be why minimum temperature does not seem correlated with treeline position. Unfortunately, testing any sort of winter damage hypothesis is difficult because the damage is only obvious considerably after it has occurred. Often it is difficult to differentiate between desiccation and frost damage (Perkins et al., 1991). However, there is some evidence that frozen soil is not the real cause of frost drought, although for many years it was assumed that frozen soil was the cause. Investigating the problem in New England, Marchand (1996) studied winter water relations in and Abies balsamea. Marchand demonstrated that even when it was impossible for water replenishment to occur (due to a severed stem or frozen soil), foliar desiccation did not occur until late spring. Under normal conditions, there is enough water stored in the tree’s stem to survive moderate cuticular transpiration throughout the winter. Therefore, frozen soil alone is not the cause of winter drought: elevated needle temperatures resulting in dramatically increased cuticular transpiration must occur, and then the water reserves in the stem must be exhausted. Similarly, Sowell et al. (1996) have shown that stem water can recharge needles throughout the winter. It is clear that while some winter damage may contribute to local fine-tuning of the treeline, frost drought due to frozen soil is not itself the determinant of treeline positions around the world.

Temperature There is considerable evidence for a direct link between temperature and treeline. For example: 1) south-facing slopes have a higher treeline than north-facing slopes (in the Northern hemisphere); 2) treeline is higher in the Rockies (clear, warm summers) than New England (cloudy, cool summers); and 3) treeline decreases in elevation with increasing latitude. Indeed, one of the oldest explanations for treeline is that it is determined solely by temperature. A good correlation between treeline position and the 10°C mean July isotherm was demonstrated in early work (Daubenmire, 1954; but see more recent analyses by Körner, 1998 and Virtanen et al., 2004). Certainly, both Arctic and alpine treelines have cold, inhospitable climates, with mean growing season air and

THE CAUSES OF ALPINE AND ARCTIC TREELINES soil temperatures consistently falling in the 5–8°C range (Körner, 1999; Körner and Paulsen, 2004). However, neither growing season length, which ranges from 92 days in the Sierra of , to year-round (or close to it) in the tropics, nor accumulated heat sums, nor temperature extremes, correlates globally with treeline location (Körner and Paulsen, 2004). Interestingly, although air temperature heat sums (daily means above 10 °C) differ between Arctic (temperature sum of 600–700°C) and alpine (200–300°C) timberlines, it has been observed that leaf temperature heat sums are similar (800°C) at both high-latitude and high-elevation timberlines (Davitaja and Melnik 1962, cited in Tranquillini 1979). To the best of our knowledge, this analysis has not been repeated by other researchers in other treeline ecosystems, but it could potentially provide the foundation for a theory that simultaneously explains both high-elevation and high- latitude treeline positions. Thus, it is not entirely clear what the temperature-based mechanism might be: does temperature limit photosynthesis, reproduction, growth or some other physiological process? When are temperatures most limiting? Are mean temperatures, extreme temperatures, air temperatures, soil temperatures, or perhaps even leaf temperatures, critical? We will now compare a number of temperature-based theories for treeline. It is interesting to note that, by very nature of their vertical growth habit, trees expose themselves to a microenvironment that is unfavorable for growth. The degree to which shoot meristems are coupled with the ambient environment depends on radiation, wind speed, and vegetation height. Boundary layer effects mean that increased radiation and reduced wind speed dramatically increase the meristem temperatures of low profile vegetation (e.g., Krummholz, as well as alpine cushion plants) relative to air temperature, and this can be a significant advantage in cold environments (Grace, 1989). For tall trees, meristems are more tightly coupled to the ambient air temperature, which is a disadvantage when temperatures are below the photosynthetic temperature optimum. Closely spaced trees also shade and insulate their own soil; soil temperature under a forest stand at treeline is generally close to the mean annual air temperature (Grace, 1989; Körner, 1998). By comparison, the open spacing of Krummholz islands permits much more soil warming to occur (Körner and Paulsen, 2004). These factors combine to make the prostrate growth form far more suitable than a vertical, arborescent form for survival at high elevations and high latitudes.

Temperature: Carbon Balance With increasing elevation, lower temperatures result in lower maximal rates of photosynthesis and a shortened growing season. As reviewed by Grace (1989), high- elevation trees photosynthesize at a 30-50% lower rate than low-elevation trees, and low temperatures decrease the quantum yield of photosystem II because turnover of the protein electron acceptor Qb is restricted in cold environments, which results in photoinhibition (see also Richardson and Berlyn, 2002). The carbon balance theory suggests that treeline occurs at the point where carbon fixation by photosynthesis, frequently restricted to a short growing season, is offset by respiratory losses and the production of foliage, with no carbon left over for wood production (Stevens and Fox, 1991). For example, large reductions in growth increment of Nothofagus have been observed across an elevational difference of ≈300 m and a temperature difference of only a few °C (Wardle, 1985).

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It is thought to be more difficult for large trees to have a positive carbon balance at high elevation than it is for small trees, which may explain why tree size decreases with increasing elevation, as well as the transition from vertical “tree” to prostrate Krummholz. Trees are a relatively inefficient growth form in that production of woody stems and roots both require large amounts of carbon. The ratio of photosynthetic tissue to total biomass decreases with increasing tree size (Daubenmire, 1954; Stevens and Fox, 1991) and respiration of this non-photosynthesizing tissue may impose a significant carbon burden. On the other hand, prostrate Krummholz and other shrubs can survive at higher elevations because of a more favorable near ground level and more efficient carbon allocation patterns (Daubenmire, 1954; Stevens and Fox, 1991; Smith et al., 2003). The carbon balance theory neglects a number of important facts. First, moisture status is generally favorable to photosynthesis during the growing season at high elevations—often more favorable than it is at lower elevations (Körner, 1998). Trees at high elevation may have lower maximal rates of photosynthesis, but when integrated over the growing season, total carbon fixation may actually be quite high. Second, satisfactory growth has been shown to occur in Nothofagus seedlings at 300 m above local treeline, which suggests that carbon fixation at treeline is not inadequate (Wardle, 1971), although carbon budgets for mature trees could be quite different. In fact, of the total carbon production of at treeline in Austria, only one-third was required for respiration and biomass production (see reference in Wardle, 1974). Third, most tropical high-elevation ecosystems are marked by little or no seasonality, and thus while carbon balance may be a factor when the growing season is short, it is probably not the deciding factor in tropical mountain ranges with a year-round growing season.

Temperature: Cuticle ripening theory Wardle (1965, 1968, 1971) resurrected decades-old hypothesis, advanced by Michaelis (1934a, b; cited by Wardle, 1965, and Tranquillini, 1979) in Ökologische Studien an der alpinen Baumgrenze (“Ecological studies of the alpine timberline”). This is another temperature-based explanation for treelines; it also combines elements of the frost drought theory. Wardle suggested that at high elevations, newly formed tissue might be unable to “ripen” due to the short growing season. According to Wardle, ripening has several components, including anatomical (cuticle development and lignification) and physiological (ability to withstand low temperatures and desiccation) aspects. Inadequately ripened shoots cannot withstand winter desiccation, and Frosttrocknis results. Since low-lying Krummholz vegetation is often protectively covered by snow during late winter when frost drought is liable to be most severe, only those shoots which stick up above the snow are likely to be killed off (Wardle, 1974). Only the prostrate form can thus survive above a certain elevation. Wardle published a series of papers which provided evidence in support of the ripening hypothesis: his 1965 comparison of timberlines in New Zealand and ; his 1968 study of Picea in Colorado; and his 1971 study of Nothofagus in New Zealand. In the first paper, he related death of high-elevation seedlings to desiccation and the failure of some shoots to develop fully. In the second paper, he hypothesized that winter desiccation of needles is influenced by events in preceding seasons, and that this resulted in inadequate hardening against winter. In the third paper, Wardle demonstrated

THE CAUSES OF ALPINE AND ARCTIC TREELINES that growing season length was well correlated with the degree of tissue maturation and with elevation. Bud flush occurred later at higher elevations, and so the time available for ripening thus decreased. Wardle concluded that the short growing season caused incomplete development of the cuticle, epicuticular wax and lignin. Foliar mortality resulted from excessive desiccation due to unripe cuticles. Many other authors have provided evidence that cuticle thickness at treeline is impaired, and that these trees may be prone to high levels of cuticular transpiration (Platter, 1976; Baig and Tranquillini 1976, 1980; Delucia and Berlyn, 1984; Hansen-Bristow, 1985; Berlyn et al., 1993). The strength of the cuticle ripening hypothesis is that it offers a decent mechanism for the sudden change from erect tree to prostrate Krummholz: during the summer, elevated crown tissue is in a less favorable microclimate, so it is unable to ripen. In the winter, any foliage not close to ground level does not get covered in snow, and is subject to desiccation. However, like many other treeline hypotheses, the cuticle ripening theory fails to be a universal explanation because tropical mountains don’t have seasonality that would interfere with cuticular ripening. Even where winter is a factor, cuticles may still ripen properly at treeline. Grace (1990) demonstrated that in the mountains of Scotland, there was no evidence of poor cuticle development on high elevation Pinus sylvestris, as cuticle mass per unit of leaf surface area was not related to elevation (however, it is worth noting that most other authors have looked at cuticle thickness, which could be easier to measure accurately). Although high-elevation needles transpired more than low-elevation needles, Grace attributed this to stomatal dysfunction resulting from mechanical damage from blowing ice. Needles that were visibly damaged had especially high rates of transpiration. Other studies have shown that winter desiccation is not universal. The tissue ripening theory requires that lethal desiccation through the cuticle occur. As described above, it has been clearly shown that the cause of winter drought is not frozen soil; there is also considerable evidence that winter drought does not occur everywhere, and that even where it does occur, the cause may not be poorly developed cuticles (Hadley and Smith, 1986; Perkins et al., 1991).

Temperature: Tranquillini integration Tranquillini basically extended Wardle’s work. Tranquillini (1979) asserted there are three possible causes of timberlines: an unfavorable carbon balance, an arrested phenological cycle, and inadequate plant resistance to climatic stress. Through a chain of cause and effect, the short growing season results in immature plant tissues, particularly the cuticle. Trees then enter winter with reduced resistance to transpiration. Finally, excessive water loss occurs during late winter as a result of both accelerated cuticular water loss and frozen soil. Although it proposes a slightly more complex mechanism, the Tranquillini theory fails for the same reasons as both the Wardle theory and the traditional frost drought theory. However, it is hard to dispute that in some parts of the world there appears to be a striking relationship between increasing altitude/latitude and decreasing cuticle thickness/resistance. Although this may not actually be the cause of timberlines, it should definitely be a key factor to look at in order to understand how plants in such extreme habitats function in relation to their environment.

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Temperature: Impaired sink theory The most recent comprehensive treeline theory centers on growth limitation. Körner (1998, 1999) proposed that cell division and differentiation into functional tissue is shut off at temperatures below a certain threshold, which is thought to be between 3°C and 10°C, probably in the 5.5°C–7.5°C range. Körner (1998, 1999) hypothesized that even though there is enough carbon being fixed at treeline, temperatures are too low for carbon sinks like growth and renewal, since cellular development is impaired. Cold nights for canopies coupled to the ambient atmosphere may mean that shoot expansion cannot occur at night. Trees shade and insulate their own root zone (Körner and Paulsen, 2004) and cold soils probably impair root growth. The resulting reduced meristem activity, both aboveground and belowground, means that inhibited sinks rather than sources are the limiting factor for growth of tree-like forms at high elevations. There is evidence for this sort of threshold temperature in the root and shoot growth of Pinus cembra. A literature survey suggests that freezing is not involved with this threshold. Rather, it appears that cell doubling time rises asymptotically at ≈1–2°C (Körner, 1999). Furthermore, because photosynthesis at these temperatures is only reduced by ≈70% relative to the temperature optimum, it is clearly possible for sink limitation to occur at temperatures sufficient for an adequate carbon supply. This theory is supported by work reported by Tranquillini (1979) which showed that growth rates were reduced by as much as four-fold with only small (< 300 m) increases in elevation: this is much greater than any change we would expect in incident radiation or a temperature-related photosynthesis effect. Furthermore, Körner (1998) noted that ring widths frequently are doubled during a growing season that is only modestly warmer (2-3°C) at treeline, and growth of seedlings has been shown to be dramatically reduced at low temperatures. Radial growth has also been shown to be linearly correlated with temperature above a minimum temperature of ≈7– 8°C (Grace, 1989). And Grace et al. (2002) found zero growth of Pinus sylvestris at 5°C, despite the fact that photosynthetic rates at that temperature were still ≈30% of the rate at 20°C. As suggested by other temperature-based theories, trees may, by the very nature of their growth form, render themselves unsuitable for growth at treeline. Although Körner’s theory relies on the existence of a very sudden threshold temperature at which cellular growth is reduced to zero, it can be imagined how, because of differences in microenvironment, tall trees could fall on one side (the wrong side) of this threshold, whereas low-lying, prostate vegetation, in a more favorable microclimate, is not subject to temperature limitations. The main advantage of this theory is that it would appear to apply universally from the equator to high latitudes.

RECENT FIELD STUDIES In recent years, a number of novel experiments have been conducted with the hopes of determining which (if any) of the above theories for treeline is correct. Research has focused on the carbon limitation and impaired sink hypotheses. Körner (2003) proposed that tissue concentrations of non-structural carbohydrates (NSC) offer insight into the balance between carbon supply and demand, i.e., between photosynthetic production and the requirements for growth. A recent study found that Pinus cembra at the highest elevations in the Alps accumulated more NSCs than those at lower elevations

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(Hoch et al., 2002), and a larger study with data from Pinus spp. at sub-tropical (Mexico) and sub-Arctic (Sweden) latitudes gave additional support for this pattern (Hoch and Körner, 2003). From lowland tropics to temperate treeline, there appears to be a generally inverse relationship between growing season temperature and NSC concentrations (Körner, 2003). Thus, from these results it could be concluded that the supply of carbon does not limit growth at treeline. Rather, sink inhibition (i.e., tissue formation) limits growth. Interestingly, however, Körner (2003) found that in a variety of different ecosystems (including three high-elevation treeline forests, as well as a temperate lowland forest and a semi-deciduous tropical forest), NSC concentrations tended to be high throughout the year, even during periods of low growth. Thus, it appears that growth of forest trees around the world, and not just at treeline, may be sink-limited, rather than carbon-limited. (Slow rates of phloem transport have been implicated as a cause of slow growth in some Pinus caribaea individuals; see Anoruo and Berlyn, 1993. Since phloem transport would be inhibited by cold temperatures, this problem could be exacerbated at treeline.) Results of a recent high-elevation free-air CO2 enrichment (FACE) study, led to the opposite conclusion (Hättenschwiler et al., 2002). Because growth of both Larix decidua and Pinus uncinata was stimulated by FACE treatment in the first year, the authors concluded that tree growth at high elevations must be limited by carbon availability. Not discussed by Hättenschwiler et al. was the fact that the FACE treatment also lead to increased foliar accumulation of NSCs, evidence that would tend to support the sink limitation hypothesis. However, Körner (2003) argues that foliar NSC concentrations may not reliably indicate source-sink relationships in CO2 enrichment studies. Rather, inference must be based on stem tissue NSC concentrations. Handa et al. (2005) reported on years two and three of the FACE experiment described by Hättenschwiler et al. (2002). Although L. decidua shoot growth was stimulated by enrichment in all three years, for P. uncinata, there was no enrichment effect in years two or three. This suggests that L. decidua may be carbon limited at treeline, whereas P. uncinata generally is not; however, a defoliation experiment conducted during the second year of enrichment indicated that carbon limitation might periodically occur in response to extreme disturbances at treeline. It is possible that these somewhat conflicting results relate to the fact that the present treeline location is indicative of past climatic conditions.

CLIMATE CHANGE AND TREELINE Responses to climate change are expected to be largest at climate-driven ecotones (see Noble, 1993, for a review and critique). There is considerable interest in the effects of climate change on treeline location: there are clear implications for both changes in forest structure below the treeline, and biodiversity of alpine ecosystems above the treeline (Grace et al., 2002). Analysis of growth ring width along an elevational gradient near treeline in the Swiss and Austrian Alps indicates a strong relationship between increasing elevation and decreasing ring width for the period 1800-1940 (Paulsen et al., 2000). However, since 1940, Paulsen et al. found no such trend; the authors suggest that with the past century and a half of warming, minimum temperature requirements for growth are now consistently met all the way up to the treeline. Based on historic relationships between

THE CAUSES OF ALPINE AND ARCTIC TREELINES treeline location and temperature, it is generally expected that the present warming trend will cause an upslope migration of the treeline. For this to occur, however, new seedlings must become established above the present treeline location. Smith et al. (2003) identified four forms of microsite facilitation (inanimate, interspecific, intraspecific and structural) that promote establishment, carbon gain and, ultimately, enhanced growth and survival, of seedlings at treeline (see also Stevens and Fox, 1991). The results of Hättenschwiler et al. (2002) would seem to indicate that rising atmospheric CO2 may be as important as recent temperature increases for the health and productivity of trees at the highest elevations, and Handa et al.’s (2005) results indicate that the capacity of alpine trees to respond to CO2 increases is very species-specific. Differential effects of enrichment could lead to changes in the competitive balance among species, and might ultimately cause changes in the species composition of treeline forests (see also Richardson et al., 2003b). However, trends in NSC concentrations reported by Hoch et al. (2002) and Körner (2003) appear to indicate that trees at high elevations already take up more CO2 than they can effectively use for growth. Based on Körner’s (1998) impaired sink hypothesis, rapid increases in tree growth are predicted in response to climatic warming, as the capacity for tissue development at low temperatures is very sensitive to temperature increases.

SUMMARY & CONCLUSIONS In this review, we have described general patterns of treelines around the world, and compared the physiognomy of treelines in a variety of different high-elevation and high-latitude ecosystems. The variability across different environments suggests that perhaps there is no single theory that can explain the position of treelines from the equator to the Arctic. Many of the older theories to explain treeline, such as excessive light, low carbon dioxide partial pressure, snow depth, desiccation, wind and reproductive failure, may help to explain specific treeline visual patterns, but they fail to provide a globally relevant explanation for treeline itself. That being said, perhaps the most convincing proposal is Körner’s impaired sink hypothesis, which not only relates treeline to microclimatic differences between trees and prostrate vegetation, but also provides a mechanism that, at least in theory, should be effective globally from tropics to Arctic. Furthermore, the recent work demonstrating that trees at the highest elevations accumulate more non-structural carbohydrates than those at lower elevations gives strong empirical support for this theory. Treelines have fascinated biologists for centuries, and even if the impaired sink hypothesis does emerge as the consensus theory to explain treelines around the world, it is certain that forests at the limits of growth will continue to provide exciting research opportunities in the future.

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Table 1: Differences between low and high latitude.

At a given altitude, lower latitude is associated with… Low latitude High latitude Mean temperature High Low Total ecosystem energy High Low Seasonal temperature amplitude Low High Diurnal temperature amplitude High Low Growing season length Long Short Solar angle & peak radiation High Low Cloudiness High Low

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Table 2: Differences between low and high elevation

At a given latitude, lower elevation is associated with… Low elevation High elevation Mean temperature High Low Diurnal variation in temperature Low High Growing season length Long Short Precipitation Low High Wind Low High Soil quality High Low Total ecosystem energy High Low Radiation intensity when clear Low High UV intensity Low High Partial pressure of CO2 High Low

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Figure 1. Professor Graeme Berlyn and the second author, near treeline on Mt. Moosilauke in the White Mountains of New Hampshire, summer 2001.

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Figure 2. View of the summit ridge on Mt. Mansfield, in the Green Mountains of Vermont, illustrating a somewhat indistinct treeline transition from forest to patchy Krummholz. Note also the rocky, shallow soils which are typical of high elevation.