Notes on Phenology (last updated in 2000)

INTRODUCTION
Phenology, as broadly defined as the periodicity of biological phenomena in relation to climate, is a crucial aspect of any effort towards predicting seasonal patterns of carbon exchange between terrestrial ecosystems and the atmosphere. Studies on vegetation phenology have a long history (e.g. Linnaeus 1751) and typically concentrate on seasonal changes of canopy development, that is, on the timing of the onset of leaf growth and the onset of leaf senescence (e.g. Lieth 1974). While the presence or absence of a photosynthetically active canopy clearly has dramatic effects on plant carbon exchange (White et al. 1997), a complete understanding of vegetation-atmosphere carbon fluxes must include the seasonal activity of non-photosynthetic tissues such as stems and roots which contribute to carbon losses through respiration. Further, different plants respond differently to similar conditions so it is important to consider the phenological characteristics of different growth forms (e.g. woody and herbaceous) and habits (e.g. evergreen and deciduous).

PHENOLOGY OF PHOTOSYNTHESIS
Other factors besides the timing of onset and senescence of photosynthesis can affect photosynthetic carbon exchange during a growing season. Not only are leaves not created equal but during their lifetime, photosynthetic capacity can vary with temperature (e.g. Badger et al. 1982), availability of light, CO2, and water (e.g. Sims et al. 1998), and with age (Mooney et al. 1981, Reich et al. 1995). Thus, phenology should be considered in relation to physiological status as well as onset and senescence. However, the length of the growing season, and hence the timing of onset and senescence, are clearly important (Goulden et al. 1997, 1998, Ham and Knapp 1998).

Since leaf development will not be of benefit to a plant unless the environment is favorable for photosynthesis, the onset and senescence of photosynthesis should correlate with the onset and senescence of canopy development. However, White et al. (1997) argue that onset and of photosynthesis lags initial leaf expansion (and offset precedes total leaf fall in deciduous trees). The principle biophysical controls on canopy development are temperature of the soil and air, precipitation and soil moisture, and solar radiation and daylength. Generally, the onset or senescence of photosynthesis is controlled by whichever factor tends to be most limiting to root or leaf functioning in a given environment.


Optimally, onset is precisely determined by the time when conditions are favorable for photosynthesis. Similarly, the optimal timing and rate of senescence is determined by the rate at which photosynthesis decreases and the time when net photosynthesis is no longer positive (Kikuzawa 1995). Thus, the onset of photosynthesis is often predicted by taking into account the photosynthetic response to light, temperature, soil moisture, humidity, etc. and determining the time when photosynthesis exceeds leaf respiration (e.g. Aber and Federer 1992, Ludeke et al. 1994). This approach is similarly used to predict photosynthesis during senescence. While the latter approach seems reasonable, a plant cannot suddenly begin photosynthesis the instant conditions are favorable. Rather, a suite of physiological changes must be instigated in response to various environmental cues to produce new (deciduous or annual plants) or activate existing foliage (evergreens). Evergreens have a clear advantage in this regard because they can quickly reactivate needles for photosynthesis (Walter 1985). Photosynthetic activity in many evergreen plants persists in winter during periods near or above 0C (Saeki and Nomoto 1958, Bourdeau 1959). Thus, onset of photosynthesis may deviate from the optimal date, particularly in annuals and deciduous plants.


Global Trends
Based on global scale correlations between NDVI, air temperature, and precipitation, Schultz and Halpert (1993) found that onset and offset of photosynthetic activity is influenced by temperature in cold regions, by both precipitation and temperature in temperate regions, and by precipitation in regions where the amplitude of the annual temperature cycle is small. These regional scale observations are consistent with the correlation between plant functional type (e.g. woody/herbaceous, evergreen/deciduous, etc.) and climate (e.g Holdridge 1947). Plants generally exist where they are most competitive for resources (Walter 1993), thus it is no surprise that cold-adapted species are found where it gets cold and drought adapted species are found where it gets dry, etc. These large-scale patterns also mask species-specific or functional-specific responses to climate which become evident (and important) when climate deviates from its norm or when species are displaced from the climate to which they are adapted. Such responses can be elucidated by examining the correlation between NDVI and temperature and precipitation anomalies, as done by Schutz and Halpert (1993) over a 7-year time period.


Figure 1. NDVI versus temperature (top) and precipitation (bottom) anomalies. High correlation (dark area) is representative of the degree of importance to the onset and offset of photosynthesis. Taken from Schultz and Halpert (1993).
 
Correlations between NDVI and climate anomalies (Figure 1) suggest a slightly different pattern than that suggested by standard correlations. As expected, extreme northern regions, where it gets very cold (e.g. Siberia), appear to be controlled by temperature but temperate regions (e.g. Great Plains) appear more limited by precipitation. Also, areas of the tropics (e.g. Amazon basin) appear more influenced by temperature than precipitation. (The variation in temperature in the Amazon may have been greater than that by precipitation, which may have always been above the level favorable for growth.) Overall, these regional scale observations are broadly consistent with those at the ecosystem and individual plant level.

Temperature
Onset among many plants has been attributed to temperature-related triggers, as exemplified by the widespread use and success of numerous growing-degree day (GDD) or thermal summation models of tree phenology (Reaumur 1735, Hickin and Vittum 1976, Thomson and Moncrieff 1981, Valentine 1983, Cannel and Smith 1986, Murray et al. 1989, Hari and Hakkinen 1991, Hunter and Lechowicz 1992, Caprio 1993, Hanninen et al. 1993, Kramer 1994). Canopy onset and senescence in autumn-deciduous trees and shrubs are partially under temperature control. Further, bud-burst is often triggered after a winter period or “rest break” consisting of a sequence of changes in the balance between growth promoters and growth inhibitors in the bud (Hanninen 1995). The exact nature of these changes remains unclear but this chilling requirement is clearly important (Smith and Kefford 1964, Perry 1971, Hanover 1980, Dennis 1987). For example, the spruce Picea sitchensis requires 140 days with a temperature of less than 5C, followed by a spring period of warmer weather (Cannell and Smith, 1986).
 
Soil temperature appears to be more important than air temperature. Growth regulators, such as cytokinins, produced by fine roots and required for leaf expansion, cannot be produced until the soil thaws (White et al. 1997). Soil temperature plays a critical role in both the onset and senescence of photosynthesis in evergreen conifers (Walter and Breckle 1991). Before spring thaw, canopy conductance in a spruce-fir forest was severely restricted (Hollinger et al. 1999) which apparently limited water flow into the trees and ultimately, photosynthesis (Teskey et al. 1984, Day et al. 1989). Further, conifer photosynthesis is typically reduced following nights with subfreezing soil temperatures  (Delucia and Smith 1987, Hallgren et al. 1990). Many species show strong relationships between root temperature and soil water absorption (Kramer 1983), such that increased root resistance as a result of subfreezing temperatures may be a general cause of senescence of stomatal conductance and photosynthesis. The biochemistry of photosynthesis can apparently tolerate temperatures below
0 degC (Larcher 1994) and the functional range of a species will vary strongly with the local growing season temperature (Woodward and Smith 1994). It thus appears that conductance, and hence soil temperatures, rather than foliar biochemistry, per se, is more important to the onset and senescence of photosynthesis under natural field conditions. However, the biochemistry of the C4 pathway is inhibited at temperatures well above freezing (Berry and Bjorkman 1980) such that the phenology of photosynthesis in C4 plants is likely more sensitive to air than soil temperature (under well-watered conditions).

Deciduous trees typically begin photosynthesis after leaves are developed, well after the soil has thawed (e.g. Goulden et al. 1996). The results of White et al. (1997) indicate that photosynthetic activity of deciduous broadleaf forests from various latitudes (35-46
degN) in North America ceases when soil temperatures fall below 2 degC or when both soil temperatures are below 11.15 degC and daylength is less than 655 minutes. Grasslands in relatively wet, cool areas are primarily limited by temperature (Ram et al. 1988). White et al. (1997) also found that onset of grasslands was strongly controlled by temperature, whereas photosynthetic offset appeared dependent on both cold weather and drought.

Precipitation and Soil Moisture
Soil moisture is important where temperature and photoperiod are not limiting. Senescence of desert shrub grasslands is largely controlled by precipitation and drought (Burk 1982, Kemp 1983, Sharifi et al. 1988). In drier tropical ecosystems, moisture often functions as the primary controller of canopy development and leaf senescence (Long 1990, Miranda et al. 1997, Hanan et al. 1998). Drought limits plant water uptake which, in turn, restricts stomatal conductance and, ultimately, photosynthesis. Water stress also causes biochemical limitations to photosynthesis (Sharkey and Seeman 1989) and, depending on the severity and duration, can induce senescence (Russell et al. 1989).

Solar Radiation and Daylength
In woody plants, senescence appears to be induced by photoperiod (Vegis 1964, Nooden and Weber 1978). The critical daylength apparently varies with latitude (Vaartaja 1960, 1961, Allen and McGregor 1962, Heide 1974, Hanninen et al. 1990, Oleksyn et al. 1992) such that northern plants become dormant while days are relatively long while southern plants continue growth well into short daylengths. This suggests that temperature is also important. Senescence in trees can be prolonged by warm temperatures and curtailed by cold temperatures (Heide 1974, Koski and Selkainaho 1982, Smit-Spinks et al. 1985). Photoperiod appears important only within a certain temperature range. Extremely low temperatures will induce senescence, while at warm temperatures, growth will continue regardless of photoperiod (White et al. 1997). In contrast to most woody plants, photoperiod does not appear to be a strong determinant of onset or senescence in grasslands. However, with a few exceptions (e.g. Sharifi et al. 1998), phenology is generally observed under natural conditions. Water is likely to become limiting before photoperiod such that even if the plants were sensitive to daylength, it will not be observed. Photoperiod has long been known to induce flowering (and subsequently senescence) in herbaceous crops (Garner and Allard 1920)


Figure 2. Representation of herbaceous (shallow, fibrous root system) and woody (deeper, coarse root system) plants. Taken from Walter (1985).


Woody Versus Herbaceous Plants
Onset of photosynthesis by plants at northern latitudes and temperate zones is generally induced by temperature in both herbaceous and woody plants. Offset, on the other hand, is controlled by temperature in herbaceous plants and by both temperature and photoperiod in woody plants (White et al. 1997). In the tropics, where temperatures are rarely limiting to photosynthesis to either herbaceous or woody plants (based on review by Larcher 1994), offset in both plant types is largely influenced by precipitation (Reich 1995, Miranda et al. 1997, Hanan et al. 1998).
 
Woody and herbaceous plants differ in both their above- and belowground structure. Aboveground, woody plants have the advantage of persistent support structures from which to display leaves above herbaceous plants. In temperate deciduous forests, understory herbaceous plants generally develop leaves before canopy trees, thereby ensuring they have access to light before canopy closure (Yoshie and Yoshida 1987, Walter 1985). Thus, at similar temperatures, herbaceous plants may exhibit onset of photosynthesis before woody plants. Further, herbaceous plants employ a “crash and burn” strategy in that they photosynthesize very strongly as soon as conditions are favorable and as water becomes scarce or temperatures drop, photosynthesis continues until the leaves, usually the entire aerial shoot system, dies (Walter 1985). Woody plants tend to take a more leisurely, conservative approach. Photosynthesis is relatively slow to start as compared to herbaceous plants. Further, woody plants generally have coarse roots which extend far into the soil in every direction, providing access to both a large volume of soil and water at great depths. They are thus less susceptible to short term drought in the upper soil layers where herbaceous roots are found. However, at the fist indication of drought or cold (i.e. decreased daylength), photosynthesis in woody plants is radically reduced and preparations are made for dormancy (Walter 1985). Thus, senescence of photosynthesis in herbaceous plants may often occur later than in woody plants.

Evergreen Versus Deciduous Plants
All else being equal, onset of photosynthesis will occur earlier for extratropical evergreen plants than deciduous plants because less time is required for evergreen plants to activate their leaves after winter dormancy (Walter 1985). Goulden et al. (1998) found that photosynthetic activity at a temperate deciduous forest (Harvard Forest) began about one month after the onset of photosynthesis at a boreal evergreen forest 13 farther north. The growing season of  evergreen vegetation can thus be longer than that of a deciduous vegetation under similar conditions (Hollinger 1992). Accordingly, Hollinger et al. (1990) found that, despite being 3 north, the growing season length at an evergreen spruce-fir forest exceeded that of Harvard Forest. Similarly, Bubier et al. (1998) found the growing season length of evergreen shrubs in a rich fen was longer than that of nearby deciduous shrubs.

C3 Versus C4 Pathways
Plants with the C3 photosynthetic pathway can tolerate low temperatures whereas C4 plants cannot (Pearcy and Eherlinger 1984, Woodward and Smith 1994). They are absent from areas with a mean summer minimum temperature below 8C (Long 1983, Henderson 1994) but tend to out-compete C3 plants at high temperatures (>30C). As a result, the onset of photosynthesis in C4 plants will lag that in C3 plants in temperate zones where early growing season temperatures are low. Further, the onset of senescence in C4 plants will begin sooner than in C3 plants as temperatures drop.

PHENOLOGY OF RESPIRATION
The onset and senescence of respiration generally parallels that of photosynthesis (Baldocchi et al. 1997, Goulden et al. 1997, Hollinger et al. 1999).  In a mesic deciduous forest, Baldocchi et al. (1997), found that both autotrophic respiration (leaves, stems and roots) and photosynthesis exhibited similar trends over the growing season. Often, however, the timing of respiration lags photosynthesis (Hanan et al. 1998). Such lags may reflect stress at the respiring tissue or the need for carbohydrate replenishment prior to growth (Goulden et al. 1997).

Temperature, moisture, and the presence or absence of leaf area and standing biomass are among the factors that affect the onset of plant respiration (Ryan et al. 1994, Amthor 1994, Sprugel et al. 1995). Rates of respiration, like all chemical reactions, increase (exponentially) with temperature. Water stress reduces photosynthesis, growth, and total plant respiration (Bradford and Hsiao 1982). Further, respiration is regulated by the amount of respiratory machinery (enzymes and transporters) and the amount of respiratory substrate (carbohydrates) (Amthor 1994). Thus, environmental conditions influence respiration, in part, through their effect on photosynthesis and carbon partitioning.


Leaves
The most immediate temporal interactions between respiration and photosynthesis occur in leaves (Amthor 1994). Respiration in a mature leaf at night can be positively related to the previous daytime net photosynthesis (Ludwig et al. 1975) as can shoot and whole-plant respiration (Amthor 1993). Thus, the phenology of foliage respiration will generally track the phenology of photosynthesis. Furthermore, a large component of respiration is associated with the production of new tissue (i.e. at bud break). Thus, deciduous plants, unlike evergreens, will experience respiration costs associated with the construction of new leaves in the spring.
 
Stems
The onset and senescence of stem respiration is largely determined by the rate of wood production and the amount of respiring sapwood at the time favorable for respiration (Sprugel et al. 1995). Wood production begins and ends, for the most part, in sync with photosynthesis. The temperature at which stem respiration will begin and cease varies from plant to plant, and can vary depending on the temperature to which a plant is adapted or acclimated (Korner and Larcher 1988).
 
Roots
The phenology of root respiration can, in part, be understood by the phenology of root growth. Roots generally grow whenever soil temperature and moisture is favorable (Stevens 1931, Cossmann 1939) and energy is available (Ford and Deans 1977). They often exhibit a distinct early spring and late summer bimodal growth peak (Resa 1877, Stevens 1931, Cossmann 1939). It is thus common for root growth to appear out of phase with shoot growth (Wilcox 1962, Leshem 1965). However, root growth is a continuous process and does not cease during stem radial growth or elongation (Ford and Deans 1977). The periodic behavior of root growth results from a reduction in growth during stem thickening, when less assimilate is available (Deans and Ford 1986). Roots in close proximity to stems rely on current photosynthate or on imported reserves while distal roots use starch reserves in root bark (Luxmoore et al. 1995). Asynchrony between shoot and root growth allows the same reserves to serve different parts of a plant during a growing season (Chapin 1980). These patterns apply to both coarse and fine roots.
 
The linkage between root and shoot growth and metabolism dictates a linkage between the phenology of photosynthesis and root respiration. Root respiration supports growth and maintenance in roots and active uptake of nutrients from the soil solution (Amthor 1994). In herbaceous plants, a change in photosynthesis in response to light levels results in a concomitant change in root respiration within a few hours (Hansen 1977). Also, Szaniawski and Adams (1974) found root respiration rates were highest for Tsuga canandensis seedlings when the shoots were photosynthesizing.

Soil temperature and moisture have the greatest influence on the seasonality of root growth (Leshem 1965) and by extension, respiration. Observations suggest that root respiration is generally inhibited by drought conditions (Baldocchi and Meyers 1991, Hanan et al. 1998). Soil temperatures lag behind air temperatures, thus root respiration will likely lag aboveground respiration. Further, root senescence will likely lag shoot senescence. Overall, the onset and senescence of root respiration is expected to lag that of photosynthesis while soil temperature and moisture will act to prolong or shorten the belowground growing season.


REFERENCES
Aber,JD; Federer,CA (1992): A generalized, lumped-parameter model of photosynthesis, evapotranspiration and net primary production in temperate and boreal forest ecosystems. Oecologia 92, 463-474.

Aber,JD; Reich,PB; Goulden,ML (1996): Extrapolating leaf CO2 exchange to the canopy: A generalized model of forest photosynthesis validated by eddy correlation. Oecologia 106, 257-265.

Amthor,JS (1993): Plant respiratory responses to the environment and their effects on the carbon balance. In: Plant-environment interactions. (Ed: Wilkinson,RE) Marcel Dekker, New York, .
 
Amthor,JS (1994): Higher plant respiration and its relationships to photosynthesis. In: Ecological Studies: Ecophysiology of Photosynthesis. Vol. 100. (Eds: Schultze,E-D; Caldwell,MM) Springer-Verlag, Berlin, 71-101.

Badger,MR; Mjorkman,O; Armond,PA (1982): An analysis of photosynthetic response and adaptation to temperature in higher plants: Temperature acclimation in the desert evergreen Nerium oleander L. Plant, Cell, and Environment 5, 85-99.

Baldocchi,DD; Vogel,CA; Hall,B (1997): Seasonal variation of carbon dioxide exchange rates above and below a boreal jack pine forest. Agricultural and Forest Meteorology 83, 147-170.

Berry,JA; Bjorkman,O (1980): Photosynthetic response and adaptation to temperature in higher plants. Ann. Rev. Plant Physiol. 31, 491-543.

Bourdeau,PF (1959): Seasonal variations of the photosynthetic efficiency of evergreen conifers. Ecology 40, 63-67.

Bradford,KJ; Hsiao (1982): Physiological responses to moderate water stress. In: Physiological plant ecology. II. Water relations and carbon assimilation. Encyclopedia of plant physiology. New series. Vol. 12. (Eds: Lange,OL; Nobel,PS; Osmond,CB; Ziegler,H) Springer-Verlag, Berlin, 263-324.

Bubier,JL; Crill,PM; Moore,TR; Savage,K; Varner,RK (1998): Seasonal patterns and controls on net ecosystem CO2 exchange in a boreal peatland complex. Global Biogeochem. Cycles, .

Burk,JH (1982): Phenology, germination, and survival of desert ephemerals in deep canyon, Riverside county, California. Madrono 29, 154-163.

Cannell,MJR; Smith,RI (1986): Climatic warming, spring budburst and frost damage on trees. J. Appl. Ecol. 23, 177-191.

Caprio,JM (1993): Flowering dates, potential evapotranspiration and water use efficiency of Syringa vulgaris L. at different elevations in the western United States of America. Agricultural and Forest Meteorology 63, 55-71.

Cossmann,KF (1939): Citrus roots: their anatomy, osmotic pressure and periodicity of growth. Palest. J. bot. Rehovt. 3, 1-103.

Deans,JD; Ford,ED (1986): Seasonal patterns of radial root growth and starch dynamics in plantation-grown Sitka spruce trees of different ages. Tree Physiology 1, 241-251.

Delucia,EH; Smith,WK (1987): Air and soil temperature limitations on photosynthesis in Englemann spruce during summer. Can. J. For. Res. 17, 527-533.

Dennis,FG Jr (1987): Two methods of studying rest: temperature alternation and genetic analysis. Hort. Sci. 22, 820-824.

de Reaumur,RAF (1735): Obersvations du thermometre, faites a Paris pendant l'annee 1735, compares avec celles qui ont ete faites sous la ligne, a l'Isle de France, a Alger et en quelqes-unes de nos isles de l'Amerique. Mem. Acad. des Sci., Paris 1735 1735, 545.

Ford,ED; Deans,JD (1977): Growth of a sitka spruce plantation:Spatial distribution and seasonal fluctuations of lengths, weights and carbohydrate concentrations of fine roots. Plant and Soil 47, 463-485.

Frolking,S (1997): Sensitivity of spruce/moss boreal forest net ecosystem productivity to seasonal anomalies in weather. J. Geophys. Res. 102(D24), 29,053-29,064.

Garner,WW; Allard,HA (1920): Effect of the relative length of day and night and other factors of the environment on growth and reproduction in plants. J. Agr. Res. 18, 553-607.

Goulden,ML; Daube,BC; Fan,S-M; Sutton,DJ; Bazza,A; Munger,JW; Wofsy,SC (1997): Physiological responses of a black spruce forest to weather. J. Geophys. Res. 102 (D24), 28,987-28,996.

Goulden,ML; Munger,JW; Fan,S-M; Daube,BC; Wofsy,SC (1996): Exchange of carbon dioxide by a deciduous forest: Response to interannual climate variability. Science 271, 1576-1578.

Goulden,ML; Wofsy,SC; Harden,JW; Trumbore,SE; Crill,PM; Gower,ST; Fries,T; Daube,BC; Fan,S-M; Sutton,DJ; Bazzaz,A; Munger,JW (1998): Sensitivity of boreal forest carbon balance to soil thaw. Science 279, 214-217.

Grace,J; Lloyd,J; McIntyre,J; Miranda,A; Meir,P; Miranda,H; Moncrieff,J; Massherder,J; Wright,I; Gash,J (1995): Fluxes of carbon dioxide and water vapour over an undisturbed tropical forest in south-west Amazonia. Global Change Biology 1, 1-12.

Hallgren,J; Lundmark,-ET; Strand,M (1990): Photosynthesis of Scots pine in the field after night frosts during summer. Plant Physiology and Biochemistry 28, 437-445.

Ham,JM; Knapp,AK (1998): Fluxes of CO2, water vapor, and energy from a prairie ecosystem during the seasonal transition from carbon sink to carbon source. Agricultural and Forest Meteorology 89, 1-14.
 
Hanan,NP; Kabat,P; Dolman,AJ; Elbers,JA (1998): Photosynthesis and carbon balance of a Sahelian fallow savanna. Global Change Biology 4, 523-538.

Hanninen,H (1995): Effects of climatic change on trees from cool and temperate regions: An ecophysiological approach to modelling of bud burst phenology. Canadian Journal of Botany 73, 183-199.

Hanninen,H; Hakkienen,R; Hari,P; Koski,V (1990): Timing of growth cessation in relation to climatic adaptation of northern woody plants. Tree Physiology 6, 29-39.

Hanninen,H; Kellomaki,S; Laitinen,K; Pajari,B; Repo,T (1993): Effect of increased winter temperature on the onset of height growth of Scots pine: A field test of a phenological model. Silva Fenn 27, 251-257.

Hanover,JW (1980): Control of tree growth. BioScience 30, 756-762.

Hari,P; Hakkinen,R (1991): The utilization of old phenological time series of budburst to compare models describing annual cycles of plants. Tree Physiology 8, 281-287.

Heide,OM (1974): Growth and dormancy in Norway Spruce ecotypes (Picea abies), I, Interatction of photoperiod and temperature. Physiol. Plant 30, 1-12.

Hickin,RP; Vittum,MT (1976): The importance of soil and air temperature in spring phenoclimatic modeling. Int. J. Biometeorol. 20, 200-206.

Holdridge,LR (1947): Determination of world plant formations from simple climatic data. Science 105, 367-368.

Hollinger,DY (1992): Leaf and simulated whole-canopy photosynthesis in two co-occuring tree species. Ecology 73, 1-14.

Hollinger,DY; Goltz,SM; Davidson,EA; Lee,JT; Tu,K; Valentine,HT (, in press): Seasonal patterns and environmental control of carbon dioxide and water vapor exchange in an ectonal boreal forest. Global Change Biology, .

Hunter,AH; Lechowicz,MJ (1992): Predicting the timing of budburst in temperate trees. J. Appl. Ecol. 29, 597-604.

Kemp,PR (1983): Phenological patterns of Chihuahuan desert plants in relationship to the timing of water availability. Jornal of Ecology 71, 427-436.

Kikuzawa,K (1995): The basis for variation in leaf longevity of plants. Vegetatio 121, 89-100.

Korner,Ch; Larcher,W (1988): Plant life in cold climates. In: Plants and Temperature. Vol. 42. (Eds: Long,SP; Woodward,FI) The Company of Biologists Limited, Cambridge, 25-57.

Koski,V; Selkainaho,J (1982): Experiments on the joint effect of heat sum and photoperiod on seedlings of Betula pendula. Commun. Inst. For. Fennaiae 105, 1-34.

Kramer,K (1994): Selecting a model to predict the onset of growth of Fagus sylvatica. J. Appl. Ecol. 31, 172-181.

Kramer,PJ (1983): Water Relations of Plants. Academic Press, New York. 489 pages.

Larcher,W (1994): Photosynthesis as a tool for indicating temperature stress events. In: Ecophysiology of photosynthesis. (Eds: Schulze,E-D; Caldwell,MM) Springer-Verlag, Berlin, 261-277.

Leshem,B (1965): The annual activity of intermediary roots of the aleppo pine. For. Sci. 11(3), 291-298.

Lieth,H (Ed.) (1974): Ecological Studies, Analalysis and Synthesis:Phenology and Seasonality Modeling. 1st ed. Vol. 8. Springer-Verlag, New York. 444 pages.

Linnaeus,C (1751): Philosophia Botanica. Kiesewetter, Stockholm.

Long,SP (1983): C4 photosynthesis at low temperatures. Plant, Cell, and Environment 6, 345-363.

Long,SP (1990): Primary production in grasslands and coniferous forests in relation to climate change: an overview of the information abailable for modelling change in this process. Ecol. Appl.,

Ludeke,MKB et al. (1994): The Frankfurt biosphere model. A global process oriented model for the seasonal and longterm CO2 exchange between terrestrial ecosystems and the atmosphere. Climate Research 4, 143-166.

Ludwig,LJ; Charles-Edwards,DA; Withers,AC (1975): Tomato leaf photosynthesis and respiration in various light and carbon dioxide environments. In: Environmental and biological control of photosynthesi. (Ed: Marcell,R) Junk, The Hague, 29-36.

Miranda,AC; Miranda,HS; Lloyd,J; Grace,J; Francey,RJ; McIntyre,JA; Meir,P; Riggan,P; Lockwood,R; Brass,J (1997): Fluxes of carbon, water and energy over Brazilian cerrado: An analysis using eddy covariance and stable isotopes. Plant, Cell, and Environment 20, 315-328.

Mooney,HA; Field,C; Gulmon,SL; Bazzaz,FA (1981): Photosynthetic capacity in relation to leaf position in desert versus old-field annuals. Oecologia 50, 109-112.

Murray,MB; Cannel,MJR; Smith,RI (1989): Date of budburst of fifteen tree species in Britain following climatic warming. J. Appl. Ecol. 26, 693-700.

Nooden,lD; Weber,JA (1978): Environmentaland hormonal control of domancy release in terminal buds of plants. In: Dormancy and Development Arrest. (Ed: Cluuter,ME) Academic, San Diego, CA, 222-268.
 
Oleksyn,J; Tjoelker,MG; Reich,PB (1992): Growth and biomass partitioning of populations of European Pinus sylvestris L. Under simulated 50E and 60EN day lengths: Evidence for photoperiodic ecotypes. New Phytol. 120, 561-574.

Pearcy,RW; Ehleringer,J (1984): Comparative ecophysiology of C3 and C4 plants. Plant, Cell, and Environment 7, 1-13.

Perry,TO (1971): Dormancy of trees in winter. Science 171, 29-36.

Ram,J; Singh,SP; Singh,JS (1988): Community level phenology of grassland above treeline in central Himalaya, India. Arctic and Alpine Research 20, 325-332.

Resa,F (1877): Uber die Periode der Wutzelbildung. Carthaus, Bonn.

Russell,G; Jarvis,PG; Monteith,JL (1989): Absorption of radiation by canopies and stand growth. In: Plant canopies: Their growth, form, and function. (Eds: Russell,G; Marshall,B; Jarvis,PG) Cambridge University Press, Cambridge, 21-39.

Ryan,MG; Linder,S; Vose,JM; Hubbard,RM (1994): Dark respiration of pines. Ecol. Bull. 43, 50-63.

Saeki,T; Nomoto,N (1958): On the seasonal change of photosynthetic activity of some deciduous and evergreen broadleaf trees. Botanical Magazine, Tokyo 71 (841-842), 235-241.

Schultz,PA; Halpert,MS (1993): Global correlation of temperature, NDVI and precipitaion. Adv. Space Res. 13, 277-280.

Sharifi,MR; Meinzer,FC; Nilsen,ET; Rundel,PW; Virginia,RA; Jarrell,WM; Herman,DJ; Clark,PC (1988): Effect of manipulation of water and nitrogen supplies on the quantitative phenology of Larrea tridentata (creosote bush) in the Sonoran Desert of California. American Journal of Botany 75, 1163-1174.

Sharkey,TD; Seemann,JR (1989): Mild water stress effects on carbon-reduction-cycle intermediates, ribulose biphosphate carboxylase activity, and spatial homogeneity of photosynthesis in intact leaves. Plant Physiol. 89, 1060-1065.

Sims,DA; Seemann,JR; Luo,Y (1998): The significance of differences in the mechanisms of photosynthetic acclimation to light, nitrogen and CO2 for return on investment in leaves. Functional Ecology 12, 185-194.

Smith,H; Kefford,NP (1964): The chemical regulation of the dormancy phases of bud development. American Journal of Botany 51, 1002-1012.

Smit-Spinks,B; Swanson,BT; Markhart III,AH (1985): The effect of photoperiod and thermoperiod on cold acclimation and growth of Pinus sylvestris. Can. J. For. Res. 15, 453-460.

Sprugel,DG; Ryan,MR; Brooks,JR; Vogt,KA; Martin,TA (1995): Respiration from the organ to the stand. In: Resource Physiology of Conifers. (Eds: Smith,W; Hinckley,T) Academic Press, New York, 255-299.

Stevens,CL (1931): Root growth of white pine (Pinus strobus L.). Bull. Yale Univ. School Forestry 32, .

Teskey,RO; Hinckley,TM; Grier,CC (1984): Temperature-induced change in the water relations of Abies amabilis. Plant Physiol. 74, 77-80.

Thomson,AJ; Moncrieff,SM (1981): Prediction of budbust in Douglas-fir by degree-day accumulation. Can. J. For. Res. 12, 448-452.

Vaartaja,O (1960): Ecotypic variation of photoperiodic response in trees, especially in two Populus species. For. Sci. 6, 200-206.

Vaartaja,O (1961): Demonstration of photoperiodic ecotypes in Liriodendron and Quercus. Canadian Journal of Botany 35, 649-654.

Valentine,HT (1983): Budbreak and leaf growth functions for modeling, herbivory in some gypsy moth hosts. For. Sci. 29, 607-617.

Vegis,A (1964): Dormancy in Higher Plants. Ann. Rev. Plant Physiol. 5, 185-222.

Walter,H (Ed.) (1985): Vegetation of the earth and ecological systems of the geo-biosphere. 3rd ed. Springer-Verlag, Berlin. 318 pages.

Way,JB; Zimmermann,R; Rignot,E; McDonald,K; Oren,R (1997): Winter and spring thaw as observed with imaging radar at BOREAS. J. Geophys. Res. 102(D24), 29,673-29,684.

White,MA; Thornton,PE; Running,SW (1997): A continental phenology model for monitoring vegetation responses to interannual climatic variability. Global Biogeochem. Cycles 11, No 2, 217-234.

Wilcox,H (1962): Growth studies of the root of incense cedar, Libocedrus decurrens. II. Morphological features of the root system and growth behavior. American Journal of Botany 49, 237-245.

Woodward,FI; Smith,TM (1994a): Global photosynthesis and stomatal conductance: Modelling the controls by soil and climate. Adv. Bot. Res. 20, 1-41.

Yoshie,F; Yoshida,S (1987): Seasonal changes in photosynthetic characteristics of Anemone raddeana, a spring-active geophyte, in the temperate region of Japan. Oecologia 72, 202-206.