Understanding the physiology of juvenile oak growth and development is crucial to developing sound management practices for successful oak regeneration. Although the inherent growth potential of northern red oak is excellent, fast growth is seldom obtained in the field. Under the stresses typical of field conditions, multiple flushing usually occurs only if root systems are large and the seedlings are growing in full or nearly full light. Consequently, rapid shoot growth seldom occurs unless the overstory is destroyed or substantially reduced in density (Johnson 1979, Johnston 1941). Such events can result from fire, windthrow, insect- and disease-related mortality and defoliation, drought, mechanical and chemical release and timber harvesting (Johnson, 1993a).

Stem and leaf growth of northern red oak occurs in episodic flushes with cycles of shoot growth and apparent rest. Shoot growth progresses from a bud stage, to a linear stem growth stage, to a linear leaf growth stage, to a lag stage (apparent rest); then the cycle is repeated (Hanson et al 1986). Leaf development in northern red oak is acropetal and physiological leaf maturation continues past full leaf expansion, unlike that in most temperate tree species with simple leaves (Tomlinson et al 1989, 1991). Root growth in northern red oak seedlings has been found to be both constant (Halle and Martin 1968) and episodic (Vogel 1975), providing a mechanism to control shoot/root ratios. This shoot-root interaction enables the plant to respond to good environmental conditions with rapid flush cycles and height growth while maintaining a balanced shoot/root ratio.

Carbon allocation within plants is a major determinant of growth. The studies available on carbon budgets in northern red oak have established that carbon fixation, carbon distribution(or, carbon allocation within plant) and carbon partitioning (carbon flow among different chemical fractions) are all episodic and closely related to leaf and plant developmental stage (QMI) rather than chronological time.  Leaves of previous flushes are important contributors to the growth of subsequent flushes. Therefore, juvenile northern red oak seedlings growing in the field are dependent upon an adequate light environment to maintain a positive carbon balance and improve survival and early growth{Dickson 2000}.

In general, there is a lack of fundamental knowledge of the physiological processes controlling early growth and development in oaks compared to many tree species. This lack of knowledge is partly attributable to the relatively few studies on carbon fixation and allocation in oak.  However northern red oak has been the focus of a number of studies related to such physiological processes.  (Kramer and Decker 1944, Farmer 1975, Chabot and Lewis 1976, Hinckley et al 1978, Heichel and Turner 1983, Jurik 1986, Dickson et al 1990, Tomlinson and Dickson 1992). Knowledge of how carbon fixation and allocation change in response to changing environmental conditions could help us better understand a plants performance in natural environments and the potential impact of environmental stress on growth. Moreover, understanding carbon budgets of important oak species in more detail could also lead to improved management practices for natural regeneration or nursery production. In northern red oak carbon fixation and allocation are tightly linked with acquisition of other resources, such as nitrogen and water (Dickson and Isebrands 1991).  Moreover carbon fixation, carbon transport from source leaves, and carbon allocation within the plant are closely tied to the episodic or flushing growth habit of northern red oak {Dickson 2000}.

This information about northern red oak, while extremely valuable, should only be extrapolated to other oak species upon careful consideration of the similarities and dissimilarities to northern red oak.

See: Juvenile growth from an ecological perspective.

Growth of northern red oak occurs in episodic flushes with cycles of shoot growth and apparent rest (Borchert 1975, Reich et al 1980, Isebrands et al 1988, Dickson 1994). Shoot growth progresses from a bud stage, to a linear stem growth stage, to a linear leaf growth stage, to a lag stage (apparent rest); then the cycle is repeated (Hanson et al 1986). Within-leaf development in northern red oak is acropetal and physiological leaf maturation continues past full leaf expansion, unlike that in most temperate tree species with simple leaves (Tomlinson et al 1989, 1991). In controlled environments, several episodic flushes may occur, depending upon environmental conditions and culture. In nurseries, northern red oak seedlings usually exhibit two or three flushes in a season in the northern part of the species range and four to five in the southern part (P. Kormanik, personal communication). In the field, seedlings have one to two flushes in the north and two to three in the south, depending upon environmental conditions. The number of leaves within a flush varies with age and size of seedling. The first flush has 3 to 7 leaves, the second 5 to 10, and the third 8 to 15 (Hanson et al 1986). Freely growing coppice shoots can have many leaves and may even approach an indeterminate shoot growth pattern because of the large phototsynate reserves contained in the parent root system (Cobb et al 1985). Additionally, the number of leaves in a flush and the timing of flushing are under genetic control (Farmer 1975) (Isebrands et al., 1994).

Quercus morphological index

Knowledge of the seedling developmental stages and leaf maturation patterns is essential for studies of the carbon budget for northern red oak. Without careful attention to the exact stage of development, investigators can easily confound and misinterpret carbon fixation and allocation patterns (Dickson 1989, 1991). A Quercus morphological index (QMI) was developed to avoid these problems (Hanson et al 1986, Dickson 1994). The QMI is based on simple leaf and stem growth measurements of northern red oak seedlings. Four distinct stages have been defined for each flushing episode-bud swell (Bd), linear stem elongation (SL), linear leaf elongation (LL), and lag (Lg).

Quercus Morphological Index

1. To ensure uniformity of morphological stages of development in parallel studies of the same seed source at different locations,
2. To compare seed sources from year to year,
3. To determine shifts in plant development due to different treatments or environments, and
4. To relate the morphological stages of seedling development to specific biochemical, physiological, and anatomical events and processes.

Carbon fixation and allocation patterns in northern red oak are episodic and closely related to leaf and plant developmental stage (for this discussion, carbon fixation is defined as the carbon exchange rate (CER; ?mol CO₂ m^-2s^-1), or net photosynthetic rate). Unlike most temperate trees, northern red oak has an acropetal pattern of within-leaf differentiation, and physiological leaf maturation continues past full expansion. Leaves of previous flushes are important contributors to the growth of subsequent flushes. Juvenile northern red oak seedlings growing in the field are dependent upon an adequate light environment to maintain a positive carbon balance and improve survival and early growth. Carbon fixation and allocation in northern red oak in field environments are similar to those in a controlled environment.

In one study on changing carbon budgets in response to simulated insect defoliation of 9- to 11-year-old northern red oak saplings, Heichel and Turner (1983) found defoliation significantly decreased carbon fixed from 69 g CO₂ d^-1 in control trees to 24 g CO₂ d^-1 in 75 percent defoliated trees. Even after the defoliated trees had produced new leaves, carbon fixation increased only to 38 g CO₂ d^-1, much less than in undefoliated trees. Sixty percent of the increase in daily carbon fixation was attributed to new foliage, and the remainder was attributed to an increase in carbon assimilation rate of the remaining old leaves (Isebrands et al., 1994).

In another study on northern red oak seedlings at selected stages of growth (QMIs), Hanson et al (1987a) examined the influence of light on carbon budgets. They estimated daily carbon gain of a three-flush northern red oak seedling growing in open conditions to be 1.7 g CO₂ d^-1. Maximum CO2 fixation occurred in full sunlight (1900 ?mol m^-2s^-1), and fixation did not decrease appreciably until there was more than 50 percent shade (500 ?mol m^-2s^-1). In heavy shade (less than 200 ?mol m^-2s^-1), daily carbon gain was always negative. This budget analysis suggested that small northern red oak seedlings growing under a full forest canopy or under dense vegetation do not receive sufficient light for photosynthesis to offset respiratory losses. Thus, mortality is likely. The silvicultural implications of these results are significant- larger seedlings are desirable to decrease competition, and an adequate light environment for the seedlings must be maintained through overstory manipulation and understory control (Isebrands et al., 1994).

Carbon Exchange Rate

CER as a function of QMI

Carbon fixation in northern red oak trees varies widely with stage of leaf development, tree age, and environmental conditions. In northern red oak seedlings growing under optimal conditions in controlled environments, light-saturated CER increased during leaf development (Hanson et al 1988a) and continued beyond full leaf expansion before declining (Hanson et al 1988a, Tomlinson et al 1991). In first-flush leaves, CER increased from the 1-SL stage to the 2-LL stage, decreased during 2-Lg, then increased again during the third flush. The CER of second-flush leaves followed this same pattern, increasing from 2-SL to 3-SL before decreasing during 3-Lg. The maximum CER recorded under controlled environment conditions (i.e., 400 ?mol photosynthetic photon flux density) was between 7 and 8 ?mol m^-2s^-1 (Hanson et al 1988b) (Isebrands et al., 1994).

First-flush leaves of northern red oak seedlings do not attain maximum CER until the plant reaches the leaf linear stage of the second flush (2-LL), well after the first-flush leaves have stopped expanding (see both figures above). This pattern distinguishes northern red oak (and perhaps other oaks) from most temperate trees with simple leaves in which CER usually peaks at or near full leaf expansion. The continued increase in CER beyond full leaf expansion in oak is a result of the continuing development of photosynthetic pigment and enzyme systems rather than leaf anatomical differentiation (Isebrands et al 1988, Tomlinson et al 1991) (Isebrands et al., 1994).  This observation implies that survival and growth of oak seedlings and seedling sprouts is closely tied to the light regime at the forest floor.  Moreover both overstory and understory densities need to be considered when evaluating the adequacy of light reaching the forest floor needed to take advantage the unique carbon exchange rate characteristics of the oaks  .As an example, reduced light levels beneath evergreen understory shrubs in Southern Appalachian hardwood forests limits carbon fixation and suppresses growth of first year oak seedlings {Beier 2005}.

Dark respiration in northern red oak seedlings grown in controlled environments is highest (most negative) during leaf expansion (i.e., SL and LL) and decreases to the lowest (most negative) rate at 100 percent leaf expansion (i.e., Lg). It is stable thereafter through subsequent flushes, averaging -0.5 to -1.5 ?mol m^-2s^-1 (Hanson et al 1987b, 1988a). Other investigators have confirmed these respiration rates in the field (Heichel and Turner 1983. Jurik 1986) (Isebrands et al, 1994).

Carbon fixation rates in northern red oak leaves under field conditions are more variable than in controlled environments; however, the number of reports on this subject is limited. In a drought experiment in which field-grown saplings were transplanted into the greenhouse, Hinckley et al (1978) found that northern red oak exhibited rather low CER with an upper asymptote of 5.7 ?mol m^-2s^-1. CER peaked at 26?C, but dropped dramatically when temperatures approached 40?C. Drought significantly decreased CER to about 1.5 ?mol m^-2s^-1, but rates recovered soon after rewatering. In addition, Heichel and Turner (1983) studied CER of northern red oak saplings in the field before and after simulated insect defoliation. CERs were between 5 and 8 ?mol m^-2s^-1, depending on light conditions. Maximum CER occurred in July and August and then decreased in September and October. CER increased in leaves remaining after defoliation, partially compensating for the adverse effects of defoliation. In a study of CER in mature overstory northern red oaks, Jurik (1986) found that CER varied with light conditions, season, and year. CER of leaves in the top of the canopy reached 14 ?mol m^-2s^-1 during one season, while CER in the understory leaves was only 6.7 ?mol m^-2s^-1. Hanson and others (1987a) concluded from these field studies that leaves of mature northern red oak maintain a rather high level of CER through much of the growing season unless they are subjected to stress such as drought or defoliation (Hanson et al. 1987a) (Isebrands et al., 1994).

In general, there have been few studies of carbon budgets in northern red oak. The paucity of studies is likely due to the lack of fundamental information on carbon fixation and allocation in the species in general and the difficulty in obtaining some of the measurements, such as root respiration, necessary for calculating carbon budgets. More research is needed, and that research should be scaled up from the seedling level to larger trees and from tree crowns to forest canopies. This effort should include studies of carbon allocation during flowering and acorn production (Isebrands et al., 1994).

Changes in Carbon 14 Fixation

The variability seen in the developmental stages of northern red oak seedlings in nursery beds and in the field presents major practical management problems because of the way carbon is allocated with the seedlings.  Ideally, any silvicultural manipulation of northern red oak seedlings should take place at a uniform developmental stage. For example, undercutting of seedlings in the nursery should be done during the lag stage when photosynthate is being allocated to root systems and is available for new root growth. However, the variable rate of development among seedlings makes it difficult for managers to prescribe standard silvicultural practices designed to improve survival and early growth of northern red oak seedlings. That task would be less difficult if flushing variability could be decreased through genetic selection or unproved nursery practices. (Isebrands et al., 1994)

Carbon Exchange Rate

There has been little, if any, work on carbon allocation in mature northern red oak trees, although some possible guidelines are provided by McLaughlin et al (1979, 1980), who studied seasonal changes of photosynthate and chemical reactions in leaves and branches of mature Quercus alba trees. They found that canopy growth and maintenance imposed a significant drain on photosynthate throughout the growing season. However, because there are physiological differences between species, similar studies in northern red oak are necessary. (Isebrands et al., 1994)

Transport of 14C-Photosynthate

Direction of Translocation

Northern Red Oak Grown
in a Controlled Enviornment

Time to acheive given QMI

Distribution of current photosynthate from first-flush leaves of northern red oak seedlings grown in controlled environments is directly related to plant developmental stage, or QMI (Dickson and Isebrands 1987, Isebrands and Dickson 1987, Dickson et al 1990). C₁₄ fixation and translocation patterns mirror CER patterns, while the quantity of ₁₄C retained in the source leaf is inversely related to that transported from the leaf (Dickson 1991, p. 65). ₁₄C transport from a first-flush source leaf increases from about 20 percent at 1-Lg to more than 70 percent at 2-SL, decreases during 2-Lg, then increases during the third flush. About 90 percent of the translocated photosynthate is transported upward to the developing stem and leaves during the second flush and about 90 to 95 percent is transported downward to the lower stem and roots during Lg periods. First-flush leaves also contribute photosynthate to developing third-flush leaves and stem, allocating about 50 percent of the translocated ₁₄C upward. These patterns all indicate that source leaf metabolism is strongly controlled by sink demand in northern red oak seedlings (Isebrands et al., 1994).

The transport pattern of ₁₄C from second-flush leaves is similar to that found for first-flush leaves, primarily upward during the third flush and downward during 3-Lg (Tomlinson and Dickson 1989). Of the photosynthate transported from a median second-flush leaf, about 60 percent is transported upward to developing leaves and stem during 3-LL, but only about 10 percent is transported upward during 3-Lg and 3-Bd stages. Moreover, during active shoot growth, basal second-flush leaves translocate more ₁₄C-photosynthate to the lower stem and roots than apical leaves, while apical leaves transport more to the developing shoot. However, these leaf positional differences are not present in lag plants because essentially all transport is downward to the lower stem and roots. Thus, leaf position within a flush influences distribution only during active shoot growth (Tomlinson and Dickson 1989) (Isebrands et al., 1994).

When ₁₄C transport patterns from first-flush leaves of northern red oak seedlings grown in controlled-environment growth chambers are compared to those from seedlings grown in the greenhouse and field, the patterns are similar if the plants were presented ₁₄C at the same developmental stage. Tomlinson and Dickson (1992) examined carbon allocation in potted plants (year 1) in the growth chamber and greenhouse as well as in a typical nursery bed. When first-flush leaves are labeled with ₁₄C -CO₂ at different developmental stages, the percent of ₁₄C exported during 48 hours from the first-flush leaves to developing second-flush shoots and roots are similar for all environments (see figure at right, part A). During development of the second flush, approximately 90 percent of ₁₄C exported from the first-flush leaves was transported to the developing shoot (see figure at right, part B). But, in the absence of active shoot growth, nearly all the ₁₄C exported was found in the roots (see figure at right, part C). Allocation within the plant is controlled by the changing sink strength of the developing leaves as defined by the developmental stage within the flush cycle. Differences in transport patterns in different environments are related to timing of each developmental stage (QMI) of the seedling. Days after emergence (DAE) required to reach a specific QMI stage is 5 to 10 days longer in field-grown seedlings than in seedlings grown in a controlled environment. Thus, carbon allocation patterns in northern red oak seedlings are related to plant developmental stages rather than some chronological time such as DAE (Isebrands et al., 1994).

Partitioning of 14C
as a function of time

Changes in partitioning of 14C

Carbon partitioning among chemical fractions in leaves of northern red oak seedlings changes over time and with stage of plant development. This result indicates that both stem and taproot accumulate reserves during the lag period when more assimilate is available than needed for growth. This might help explain high root shoot ratios often observed in seedling sprouts and thus the ability of oaks to persist for long periods of time in the understory.

When first-flush leaves at 1-Lg at 1-Lg (see Quercus Morphological Index, QMI) are fed ₁₄C -CO2, the percentage of ₁₄C in sugar decreases with time after treatment as sugar is metabolized or translocated from the leaf. In contrast, the percentage of ₁₄C in the residue (i.e., structural carbohydrate) fraction increases with time, indicating continuing vascular development. The percentage of ₁₄C in starch increases during the light period (i.e., the first 12 hours), then decreases during the subsequent dark period. Starch storage in leaves during 1-Lg is primarily associated with the diurnal cycle of carbon storage. The starch accumulated during the light period is degraded in the dark to maintain sugar transport out of the leaf. The percentage of ₁₄C found in protein increases during the first 6 hours after treatment, then remains constant (Isebrands et al., 1994).

Partitioning patterns in the stem and roots after ₁₄C labeling of mature leaves are similar to those found in leaves (Dickson et al 1990). In both stem and root tissue, the percentage of ₁₄C in sugars decreases and that in structural carbohydrates (residue) increases with time. In stems, ₁₄C in starch increases for 12 hours in the light, decreases during the dark period, then increases for the remaining period. This pattern indicates that stems have both diurnal and long-term starch storage pools. In roots, the percentage of ₁₄C in starch increases for 12 to 24 hours, then remains constant, indicating long-term storage. Taproots contain about three times as much ₁₄C starch as lateral roots do (data not shown). The ₁₄C content in protein of stem and root tissues increases during the first 12 hours, then remains constant for the rest of the chase period. Lateral roots contain almost twice as much ₁₄C protein as the taproot does (data not shown) (Isebrands et al., 1994).

Changes in 14C Fixation

Like carbon fixation, carbon partitioning patterns in northern red oak are episodic and related to leaf growth and subsequent plant development (Dickson 1986, 1991; Dickson and Tomlinson 1988). The partitioning of recently fixed ₁₄C among different chemical fractions first-flush source leaves changes dramatically when leaves are exposed to ₁₄C -CO₂ and analyzed at different QMI stages. These changes reflect both maturation processes with the leaf and metabolic changes in carbon flow due to changing sink demands in the seedling. For example, almost 50 percent of the ₁₄C recovered in first flush source leaves at 1-Lg is found in residue. Although ₁₄C partitioning into residue decreases during each subsequent QMI stage through 2-Lg, more than 15 percent ₁₄C is still incorporated into residue at 2-Lg and later QMI stages, indicating continued vascular development well after full leaf expansion. The percentage of ₁₄C incorporated into protein increases from 1-Lg to 2-Bd, decreases to 2-Lg, then increases again at the beginning of the third flush. This pattern of protein synthesis indicates that physiological development continues well after full leaf expansion and shows a response (similar to that observed for CER) to increased sink demand during flushing episodes, perhaps indicating cyclic synthesis of Rubisco (Isebrands et al., 1994).

Carbon Exchange Rate

Transport of 14C-Photosynthate

The percentage of ₁₄C recovered in both sugar and starch also changes with QMI. The ₁₄C remaining in the sugar fraction after 48 hours increases almost linearly from 1-Lg to 3-Lg, although there may be a slight cycle from 1- to 2-Lg and from 2- to 3-Lg. This sugar is probably a storage pool that increases with leaf age and does not respond to sink demand as do CER and translocation. ₁₄C incorporation into starch in first-flush source leaves at 1-Lg is primarily into the diurnal storage pool because less than 10 percent of ₁₄C is present in starch after 48 hours. In contrast, the percentage of 14C found starch increases from 1-Lg to 2-Lg, then decreases to 3-SL, then increases again. This partitioning pattern indicates that, in addition to diurnal storage, there is a long-term starch storage pool in northern red oak leaves that changes in size over development. 14C incorporated into this starch storage pool may also reflect both the increasing physiological maturity of the source leaf ( 1-Lg to 2-Lg) and changing sink demand for assimilate (after 2-Lg) (Isebrands et al., 1994).

The incorporation of ₁₄C into residue, starch, and sugars of both stem and taproot is also cyclic and varies with QMI. Although more total ₁₄C is recovered in each of these fractions during 2-Lg and 3-Bd when most transport is downward from source leaves, the percentage of ₁₄C decreases in residue and increases in sugar and starch (data not shown).  (Isebrands et al., 1994).

Factors influencing episodic growth in oaks

Northern red oak is a good example of a hardwood with episodic flushing growth habit (or semi-determinate growth, see Defining growth habits). Endogenous mechanisms control the rhythmic growth of episodic flushing of oak and other species of trees grown under constant environmental conditions or under fluctuating environmental conditions still conducive to growth. At the end of a growth flush, leaf expansion stops and a dormant (resting) bud is initiated. This bud is initiated and held in a dormant state by endogenous control mechanisms (Greathouse et al 1971, Mialoundama et al 1984). The dormant state is apparently induced by a biochemical signal originating in some other part of the plant and could be termed paradormancy (Lang et al 1987). The various states of dormancy and related terminology have been extensively discussed in the past and will not be repeated here (Romberger 1963, Levins 1969, Perry 1971, Champagnat 1983, Lang et al 1987) (Dickson, 1994).

Episodic Shoot Growth Pattern

The development of the resting bud is much different from the development of a winter dormant bud. The resting bud in red oak is much smaller than the winter bud and covered with stipules that do not expand to form bud scales. When the next flush expands, the basal 1 to 5 internodes elongate very little, and have stipules present but no leaves (Hanson et al 1986). It is yet unclear why these basal leaves do not develop. Perhaps these leaf primordia (last formed on the current flush or first formed on the next flush?) that receive the rest signal abort as was found for cottonwood (Populus deltoides) (Goffinet and Larson 1981). The exact timing of primordia initiation in respect to the flush cycle requires further careful study. Barnola et al. (1986) reported that primordia initiation was continuous over the entire flush cycle, indicating an increased rate of initiation during the flush (Dickson, 1994).

Although several hypotheses have been presented, the endogenous control mechanisms that regulate leaf and internode expansion and primordia initiation are unknown. Different hormones, water stress, carbohydrate concentrations and interactions between these factors have all been implicated. Some researchers believe that water stress, initiated in the shoot by a decreasing rate of root growth (Borchert 1975, 1978, 1991) or by competition between leaves and the developing apex for available water (Halle and Martin 1968, McIntyre 1987), induces bud rest and episodic growth. Others have implicated abscisic acid (ABA) or the interactions of ABA and water stress (Orchard et al 1980, 1981; Abo-Hamed et al 1981, 1983). Still others believe that varying concentrations of cytokinins are important in slowing leaf development or initiating bud break (Wareing 1980, Orchard et al 1981, Carmi and Van Staden 1983). The best scenario seems to be that during a flush, photosynthate movement to roots decreases, root growth decreases, water stress and ABA concentrations increase, cytokinin concentrations and/or translocation decrease, primordia development decreases, leaf growth decreases, and buds set (Orchard et al 1981, Alatou et al 1989). Because it is very difficult to separate the effects of each of these factors and their interactions, the mechanism of endogenous control of episodic flushing is far from clear (Wareing 1980, Little and Wareing 1981, Zeevaart and Creelman 1988). What is clear is that a functional equilibrium between shoots and roots (in relative growth rates, nutrient uptake, carbohydrate allocation, hormone production and transport, and water movement) must be maintained if the episodic growth cycles are maintained (Dickson, 1994).

Growth potential of northern red oak

The growth potential of northern red oak is excellent, although seldom obtained under field conditions. Under the stresses typical of field conditions, multiple flushing usually occurs only if root systems are large and the reproduction is growing in full or nearly full light. Consequently, rapid shoot growth seldom occurs under field conditions unless the overstory is destroyed or substantially reduced in density (Johnson 1979, Johnston 1941). Such events can result from fire, windthrow, insect- and disease-related mortality and defoliation, drought, and timber harvesting (Johnson, 1993a).

In growth room or controlled conditions with adequate water and fertilization, northern red oak seedlings will continue to flush until the roots become restricted by the pots (pot-bound). Under controlled environment growing conditions at Rhinelander, Wisconsin, Hanson and others observed three-flush seedlings 80 cm tall within 60 days after emergence from the potting mix (see figure above). Six-flush seedlings up to 2 m tall could be produced in the growth rooms before the seedlings became pot-bound and stopped episodic flushing. During a growth flush, internode elongation begins first and is largely completed before the leaves begin to expand (Hanson et al 1986).

Individual Internode and
Leaf Growth Patterns

A typical pattern of stem, internode, and leaf development in red oak is shown by measurements taken during expansion of the second flush. Both internodes and leaves, when measured acropetally, increase then decrease progressively in size during flush development. The last internodes and the last leaf of a flush are often much smaller than previous stem units (leaf-node-internode) indicating growth inhibition during the last phase of the flush. The growth patterns seen here (see figure at right) most likely result from endogenous control mechanisms because environmental conditions did not change during the flush (Dickson, 1994).

Most studies on episodic growth were conducted in controlled environments with small seedlings. Environmental stress, however, may severely modify these endogenous growth patterns (Gaertner 1964, Lavender 1980). In field situations, where multiple stresses are often present, oak seedlings commonly make only one spring flush of growth (Reich et al 1980). Light, moisture, temperature, and nitrogen stresses may affect episodic flushing. The response of different species probably differs widely with any particular stress, and the response to multiple stresses may differ from that obtained with a single stress if other factors are near optimum. Dickson (1994) found that Northern red oak, when grown in controlled environments with adequate nutrients and water, will continue to flush until it becomes pot-bound. Low light intensity (300 ?E m^-2s^-1, about 20 percent full sun) or short days (8 hours of light) have little effect on this endogenous growth rhythm. When plants were grown in a growth room, in a glasshouse, or outside with adequate water and nutrients, flushing was again continuous, but the flushing interval increased in the higher stress situations. For example, the interval for one lag to two lag increased from 17 to 30 to 36 days for the growth room, greenhouse, and outside plants, respectively (Dickson, 1994).

Different tree species have different seasonal patterns of shoot growth. Such patterns have long attracted research interest, and this research has been extensively reviewed (Romberger 1963, Kozlowski 1964, Rudolph 1964, Borchert 1991). Shoot growth patterns can be broadly classified as determinate, semi-determinate, or indeterminate. These classifications are not clear-cut and involve considerable overlap. In all three classifications, the first flush of growth involves expansion of pre-formed stem units (primordia-node-internode) contained in the overwintering bud.

Shoot Growth Patterns

Trees with determinate growth habit exhibit only a single growth flush in the spring, which involves the elongation and maturation of these pre-formed stem units in the bud. This growth habit implies the formation of a true terminal bud.  This form of growth results in relatively straight twigs, as with the maples, walnut, yellow-poplar and willow.  

Trees with indeterminate growth habit produce individual leaves at regular intervals during the growing season. Indeterminate growth is a pattern of bud development associated with continual twig elongation and bud formation until twig growth is stopped by short days or frost. The portion of the twig beyond the last lateral bud then dies.  The last-formed lateral bud then acts as a terminal bud when growth begins during the next growing season.  Examples include elms, birches and black locust.  The end bud produced by indeterminate species is referred to as a pseudoterminal bud.  However, both determinate and indeterminate plants exhibit rhythmic growth cycles during shoot expansion that are not obvious without frequent measurements of shoot growth  (Borchert 1978, Drew 1982; Dickson, 1994).

Trees with semi-determinate growth habit exhibit recurrent, cyclic, or episodic flushes of growth during the growing season.  Somewhere between fixed and free growth species are the recurrently flushing species, such as loblolly pine, longleaf pine, and northern red oak.  These species may grow continually during the growing season providing conditions are favorable.  When conditions are bad, recurrent flushing species may produce a temporary, or resting bud.  While conditions are poor, primordia are stacked under the resting bud.  When conditions are once again favorable, this resting bud flushes.  A resting bud may become an overwintering bud, failing to elongate in response to declining daylength.  Recurrent flushers may produce several flushes during the growing season, usually with the first flush being the longest.  Overall, these waves of growth produce elongation for a longer period than purely fixed growth.

In plants with true or "classical" episodic flushing growth habit, shoot growth is controlled by endogenous factors (Borchert 1975, 1991). Under suitable environmental conditions, a true growth flush involves expansion of the resting bud, expansion and maturation of new stem and leaves, formation of a new resting bud, and a rest period in which no new leaf or stem elongation takes place. These episodic growth flushes will continue as long as environmental conditions are favorable. Episodic growth is common in many tropical trees (Halle and Martin 1968, Greathouse et al 1971, Borchert 1978, Maillard et al 1989), in some conifers (Rudolph 1964, Kremer and Larson 1983, Hendry and Gholz 1986, Von Wuhlisch and Muhs 1987, OReilly and Owens 1989), and in some northern hardwoods (Borchert 1975, Reich et al 1980, Hanson et al 1986). Northern red oak is a good example of a hardwood with episodic flushing growth habit (Dickson, 1994).

There is no question that relative shoot and root growth is closely controlled by metabolic interactions between the shoot and roots. This functional equilibrium has been recognized for a long time and has been extensively studied (Lyr and Hoffmann 1967; Brouwer 1983; Lambers 1983; Schulze 1983); it can be viewed simply as changes in carbon allocation (de Wit and Penning de Vries 1983) or as a much more complex system of carbon, mineral nutrients, and hormonal interactions (Carmi 1986, Zhang and Davies 1989; Dickson, 1994).

In trees with episodic shoot growth, both constant (Halle and Martin 1968) and episodic (Vogel 1975) root growth has been found. In research with northern red oak seedlings, root growth rates appear constant as long as the cotyledons are attached. Apparently nutrients from the cotyledons can maintain root growth during episodic growth of the shoot (Hanson 1986). Similar continuous root growth has been found in other oak species, eg. pedunculate oak (Q. robur) (Lavarenne 1968, Belgrand et al 1987). In addition, in older seedlings and in seedlings with detached cotyledons, root growth is also episodic and out of phase with the shoot. Similar results in white, blackjack (Q. marilandica), and black (Q. velutina) oaks have been presented for both seedlings and older trees by others (Hoffmann 1967; Reich et al 1980; Nour and Riedacker 1984; Dickson, 1994).

It is difficult to understand how roots growing at a constant rate can induce episodic growth in shoots. Borchert (1991) has proposed that the increasing leaf area produced during a flush increases water stress in the shoot, which initiates the lag phase in shoot growth. Removing whole or parts of new leaves to maintain a smaller leaf area will often increase flushing rate or initiate continuous shoot growth, thus substantiating this hypothesis (Halle and Martin 1968, Borchert 1975, Vogel 1975, Hilton et al 1987). The differential translocation of nutrients and hormones, however, cannot be ruled out. During a flush when the growth of new leaves takes place, almost no photosynthate from mature leaves is translocated to the root system (Dickson 1989, Isebrands et at 1994). During the lag phase when new leaves are fully expanded, more than 90 percent of current photosynthate is translocated to the root system. This current photosynthate may be important in cycling nutrients and hormones from roots to shoots and in initiating bud break and a new episodic flush of growth. This cycling of carbohydrates to roots and of nutrients (particularly nitrogen) and hormones (e.g., cytokinins) back to shoots would be even more important when both shoots and roots have episodic and out of phase growth patterns (Sleigh et al 1984; Dickson and Isebrands 1991; Dickson, 1994).

Dicksons (1994) hypothesis is useful in summarizing the root-shoot interactions in oaks. He states that episodic growth is the result of genetic factors that provide a mechanism to control shoot/root ratios. This mechanism enables the plant to respond to good environmental conditions with rapid flush cycles and height growth while maintaining a balanced shoot/root ratio. Under adverse conditions, flushing or top growth stops and photosynthate is allocated to root growth and storage, a conservative feature that gives the plant the ability to survive severe environmental stress such as light, moisture, temprature, and nitrogen and to grow on sites with less favorable environments (Dickson, 1994).

See: Shoot Dieback

Oak reproduction survives dieback by resprouting from dominant buds near the root collar. Shoot dieback is common in all oaks growing under a forest canopy, but is especially prevalent in xeric environments like droughty uplands.  Thus dieback and resprouting are important processes in the life of oak reproduction because they facilitate the development of large root-shoot ratios and root mass, which in turn effect rapid shoot growth after the overstory is harvested destroyed by natural forces (Johnson 1979; Sander 1971).  However, xerophytic oaks may require two or more decades in the understory before they develop the root mass necessary for competitive shoot growth after overstory removal (Merz and Boyce 1956; Sander 1971, 1979; Sander and Clark 1971; Isebrands and Dickson, 1994).

Dieback may extend partially or all the way to the root collar. At the root collar there is a concentration of dominant buds capable of producing new sprouts. These are released from dormancy by the death of the terminal buds. Although the physiological mechanisms causing shoot dieback in oak reproduction are poorly understood, several factors can be involved including water stress, insects, pathogens, and fire (Kramer and Kozlowski 1979; Linit et al. 1986; Olson and Boyce 1971; Robbins and Croghan 1984; Johnson, 1993a).

Whatever its cause, recurrent shoot dieback of oak reproduction appears to be important in the adaptive strategy of oaks, especially among the more xeromorphic species. Seedlings of those species have inherently slow shoot growth, and attaining a competitive rate of growth depends on the development of a large root:shoot ratio and large root mass. Potential shoot growth of oak reproduction (stems less than 2 inches d.b.h.) increases as root mass increases. This relation is reflected in the positive correlation between the basal diameter of reproduction (a correlate of root mass) and the annual shoot growth of oak reproduction after overstory removal (Sander 1971). Shoot growth of sprouts originating from the stumps of cut overstory trees also increases with increasing stump diameter (Johnson 1979). However, growth peaks at some diameter, usually at about 6 to 8 inches depending on species, and then declines. All living oaks from seedlings to mature trees thus have some potential to contribute to the regenerative capacity of a stand (Johnson, 1993a).