Within slash pine clone banks, there were significant effects due to scion chrono- ... of female strobili on chronologically older scion could to a small degree ...
New Forests 15: 243–259, 1998. c 1998 Kluwer Academic Publishers. Printed in the Netherlands.
The effects of scion maturation on growth and reproduction of grafted slash pine S. R. PARKER1, T. L. WHITE2 , G. R. HODGE3 and G. L. POWELL2 1
Champion Int. Corp., Newberry, SC, USA; 2 Department of Forestry, University of Florida, Gainesville, FL, USA; 3 Camcore, N.C. State University, Raleigh, NC, USA
Accepted 4 October 1997
Key words: clone banks, juvenility, pollen, seed orchards, strobili Application. Within slash pine clone banks, there were significant effects due to scion chronological age (years since seed germination). The slightly earlier, and more prolific, production of female strobili on chronologically older scion could to a small degree shorten the breeding cycle and increase early strobilus production. However, this may not significantly reduce the time to operational seed production. Further, the larger, more branched, chronologically younger scions are likely to produce more pollen, and eventually may produce more female strobili. Thus, operationally it might be desirable to have chronologically younger scions in an orchard to help reduce pollen contamination in the early production years of a seed orchard, or to have a mix of older and younger material to balance male and female strobilus production in early years. Abstract. Establishment of the University of Florida Cooperative Forest Genetics Research Program’s clone banks provided an opportunity to look at scion maturation effects on growth and reproduction of many grafted slash pine clones. In 1988 and 1989, clone banks were established in nine locations in the Southeastern United States. Over 460 scion clones varying from 5 to greater than 40 years old from time of seed germination (chronological age) were grafted into the clone banks. Comparisons of diameter growth, height growth, lateral branch number and female and male strobili production were made annually for six years after grafting. Within slash pine clone banks, there were significant effects due to scion chronological age. Chronologically older scions (backward selections) grew less, had fewer branches and produced only a few more female strobili than chronologically younger material (forward selections). Forward selections produced significantly more catkin clusters than backward selections. By year six, there was no significant difference in numbers of female strobili per tree between backward and forward scions, but forward selections produced about 2.5 times as many catkin clusters as the backward selections. Similar effects on growth and reproduction due to chronological age were also found among clones within the forward selections, with older selections growing more slowly and producing fewer catkin clusters. The size and breadth of this study lends strong support to the idea that these patterns of growth will occur for grafted slash pine in any location throughout its native range.
This is Journal Series No. R-05550 of the Institute of Food and Agricultural Sciences,
University of Florida, Gainesville, 32611.
244 Introduction As woody plants age, their development proceeds from the juvenile phase through a transition phase to the mature (adult) phase (Greenwood and Hutchison 1993). The juvenile phase can last from a few days to as long as 30–40 years in some species (Hackett 1985; Hackett et al. 1990), and primarily involves vegetative growth with little or no reproductive growth. Development from a juvenile growth form to a mature growth form is commonly called maturation (Brink 1962; Hackett 1985). There are many synonyms for maturation, such as phase change, ontogeny, cyclophysis, ontogenetic aging, meristem aging (Oleson 1973), and aging (Hackett 1985). For consistency, the term maturation will be used here to refer to the change from the juvenile phase to the mature phase, and chronological age will refer to the time elapsed since the original ortet germinated from seed (Fortanier and Jonkers 1976). The age of a ramet since the time of grafting will be called the ramet age. Scion refers to the clonal material grafted onto the rootstocks and the whole grafted plant is considered a ramet of the ortet. Backward (parental) selections were original selections made in the 1950s which were maintained as ramets in orchards. Forward (offspring) selections were offspring of backward selections and were generally selected from progeny tests. The effects of maturation on trees are of both economic and scientific interest. Important economic aspects such as seed production, wood quality, rooting ability and length of breeding cycle are strongly affected by the maturity of the material being manipulated (Meier-Dinkel and Kleinschmidt 1990; Thorpe and Harry 1990). A great deal of research examining maturation has been conducted in horticultural crops especially Citrus, Prunus and Pyrus species (Visser 1964, 1965; Zimmerman 1972; Hackett 1985; Oliveira and Browning 1993; Snowball et al. 1994); however, less has been done with conifers, and almost none with slash pine, Pinus elliottii Engelm. var elliottii (Franklin 1969; Hood and Libby 1978; Greenwood and Nussbaum 1981; Greenwood 1981, 1984; Bolstad and Libby 1982; Greenwood et al. 1989; Burris et al. 1991). As conifer tree improvement moves into advanced generations it has become common to have mixtures of backward and forward selections in orchards and clone banks. Which precipitates the need to obtain more information on the effects of scion maturation on the growth and flowering of grafted conifers. The University of Florida Cooperative Forest Genetics Research Program (CFGRP) established nine clone banks in four states (Alabama, Florida, Georgia and Mississippi) containing 463 clones with variable chronological ages. These clone banks provided the opportunity to determine if the maturity
245 of scions grafted in the clone banks had a significant effect on growth and reproduction. Specific objectives were: 1. To determine effects of scion chronological age on early growth and form of ramets using 10 different variables in two distinct age groups of scion clones: backward selections (chronologically old material) and forward selections (chronologically younger material). 2. To examine the persistence of scion chronological age effects for six years after grafting. 3. To quantify effects of scion chronological age on precocity (early reproduction) and fecundity (amount of reproduction).
Materials and methods Plant material From 1988 to 1989 clone banks for the second-generation breeding population were established by the CFGRP. Over the next three years they were augmented with the final selections, and necessary regrafts were made. Of the 14 clone banks initially established, nine were used in this study. The other five were dropped due to poor grafting success or because the scion were graft onto unknown rootstock. The nine clone banks, located in Alabama, Florida, Georgia and Mississippi (Table 1), contained over 3600 ramets. These trees represented 463 different clones with chronological ages from 5 to 30 years (at the time of grafting) among the forward selections, and greater than 40 years (at the time of grafting) for the backward selections. The forward selections had a mean age of 9. About 30% of all clones had a chronological age of 6 to 10 years old. The clone banks are planted on a 4.6 by 9.2 meters (15 by 30 feet) spacing with from 5 to 12 blocks (1 block is 0.25 hectares or 0.62 acres), and 40 to 120 scion clones per clone bank (Table 1). Each block contains 10 to 20 different clones grafted onto the 8 to 10 rootstock families. Typically, half the blocks in each clone bank were planted in 1988 and half in 1989; however, two clone banks contain grafts from a single year only. Data collection and analysis Measurements made each winter or spring from 1988 until 1995 included: total height, height to graft union, scion and rootstock diameter (just above and below the graft union), number of lateral branches, and numbers of female strobili and male catkin clusters (spring 1993–1995).
246 Table 1. Number of blocks, ramets (trees), forward (offspring) selections and backward (parental) selections contained in nine clone banks. Number of scion clones Number Number Forward Backward Total of blocks of ramets selections selections
Test number
Location by county and state
700 702 703 704 705 706 707 708 712
Wayne, Georgia 10 Gilchrist, Florida 12 Decatur, Georgia 6 Nassau, Florida 8 Putnam, Florida 7 Lafayette, Florida 10 Hamilton, Florida 5 Doole, Georgia 8 George, Mississippi 5
410 702 337 399 391 564 268 357 240
71
3668
Grand totala
31 61 32 33 37 32 7 42 23
47 59 29 38 31 70 42 22 17
78 120 61 71 68 102 49 64 40
a Totals for the number of different clones are not given since many scion clones are present in more than one clone bank.
The following nine variables were analyzed at each age: rootstock diameter, scion diameter, scion height (total height minus height to graft union), number of lateral branches, lateral branches per unit of scion height, ratio of scion diameter to rootstock diameter, ratio of scion height to scion diameter, number of female strobili per tree and number of male catkin clusters per tree. Also, three incremental variables were calculated and analyzed: annual scion diameter growth, annual rootstock diameter growth and annual scion height growth. Of the 12 variables 10 are measures of growth and two are measures of reproduction. In years 1 through 3 production of female strobili was insufficient to test for differences in production between backward and forward selections. Also, several clone banks had been pruned for operational reasons in years 5 and 6, therefore analyses of number of lateral branches and lateral branches per unit of scion height could not be performed beyond year 4. The analyses of scion age effects were conducted in two stages. First, analyses of variance (ANOVA) were used to examine the difference between backward and forward selections. Second, regression analyses were used to examine chronological age effects from 5 to 30 years, employing only data from the forward selections.
247 Comparison of backward and forward selections For the ANOVA, a unit of observation was a mean of a group (backward selections or forward selections) within a year of grafting (1988 or 1989) within a location (9 clone banks). For example, the mean of all forward selections grafted in 1988 in test number 700 (Table 1) was considered to be one observation. Forward selections frequently were located in different blocks within the same grafting year (i.e., not randomized within blocks); the only replication was due to the different grafting years and the nine clone bank locations. By combining the individual tree data into means by group for a given year of grafting and location, there were 32 possible observations in each of 6 different measurement years. For some dependent variables, there were less than 32 observations since some variables were not measured every year in each clone bank. The linear model for the analysis comparing backward and forward selections was:
xijk = li + yj + lyij + gk + lgik + ygjk + lygijk
(1)
where [xijk ] = response value of k th age group within j th year grafted within ith location, li = random effect of ith location (i = 1, : : : 9), yj = random effect of j th year grafted (j = 1988 or 1989), lyij = random effect of interaction of ith location and j th year, gk = fixed effect of k th age group (k = backward or forward selection), lgik = random effect of interaction of ith location and kth group, ygjk = random effect of interaction of j th year and kth group, lygijk = random effect of interaction of ijkth location-year-group (residual error). The three-way interaction (also considered the residual error term in this model) had a maximum of 8 degrees of freedom, but in practice there were fewer actual degrees of freedom due to missing data. Thus, there was little power for testing differences associated with other effects. As a result, the chance of a type II error was high, and any inferences drawn were inconclusive. Satterthwaite’s approximate F-tests were used to determine the appropriate F-tests for this mixed model (Milliken and Johnson 1984) using the TEST option of the RANDOM statement in the SASCircledR GLM procedure (SAS Institute 1989). Also, since the year of grafting effect was treated as a temporal replication factor in this experiment, the two two-way interactions containing years
248 (lyij and ygjk ) were sometimes pooled with the three-way interaction to increase the power of the error term. However, prior to pooling, the statistical significance of each of the three two-way interactions was tested to determine whether pooling would reduce the significance of the F-tests in the ANOVA (Bozivich et. al. 1956; Bancroft 1968). Model terms were not pooled unless the F-test was nonsignificant at the = 0.25 level. There were 60 ANOVAs (12 traits across years) in which interactions were examined for possible pooling with error. For the year of grafting group interaction (ygjk ), out of the 60 tests of significance only 35% were significant at the = 0.25 level, with no consistency by trait or measurement year. All were combined with the error term with only a marginal expected increase in the likelihood of a type I error (Bozivich et. al. 1956). For the location year of grafting interaction (lyij ), 60% of the F-tests were significant at the = 0.25 level, so this interaction was not pooled with the error. This interaction was probably significant due to the large differences among clone bank locations, therefore it was important to separate this interaction from the error term. For the location group interaction (lgik ), about 30% of the F-tests were significant at the = 0.25 level, and there was no consistent pattern by trait or measurement year. To minimize the chance of a type I error, the location group interaction was pooled only when the F-tests were non-significant at the = 0.25 level (in 13 out of 60 ANOVAs). Pooling led to the use of a reduced model in which the residual error consisted of the pooled lygijk and ygjk interactions for 47 F-tests, and to the use of the pooled lygijk , ygjk and lgik interactions for the remaining 13 F-tests. Analysis of maturation effects within forward selections Individual tree measurements were used to determine if significant differences, due to chronological age, could be found within the forward selections. The linear model considered chronological age a continuous, independent variable for regressions, while location year-grafted and block effects were in the model as class or dummy variables:
xijk = li + yj + lyij + b(ly)ijk + 1 a + 2 a2 + where xijk = response to scion age within k th block of j th li = yj = lyij = b(ly)ijk = 1 a =
(2) year of
ith
location, effect of ith location (i = 1, : : : 9), effect of j th year (1988 or 1989), random effect of interaction of ith location and j th year, effect of k th block within the ith location and j th year, linear effect of scion age,
249
2 a2
= quadratic effect of scion age, = random error.
Significance was tested both with and without the quadratic term for age, and a prediction equation was generated for all measured variables in all measurement years. In order to compare the results to the first analysis, the prediction equation was used to estimate the means at 5- and 15-year-old scion age values. Chronological ages of 5 and 15 years were chosen since they encompassed the majority of forward selections in the data sets. Results and discussion For most dependent variables (across all 6 years), there was a statistically significant difference at the = 0.05 level between forward and backward selections. This difference was most evident when using the reduced model in which the year of grafting age-group (lyij ) and location age-group (lgik ) interactions were pooled with the error. Also, the effect due to scion chronological age in the regression analysis of forward selections was significant at the = 0.05 level for most variables across all 6 years. Maturation effects on growth and branching Scion diameter In all except the first measurement year, the difference between scion diameters of backward and forward selections was significant at the = 0.01 level (Figure 1a). In addition, the effect due to chronological age within forward selections was significant at the = 0.01 level for ramet ages 3, 4 and 6 and significant at the = 0.10 level for ramet age 5. (Figure 1a). Therefore, differences due to scion chronological age existed both between backward and forward selections and within the forward selections. Annual scion diameter growth was consistently larger for forward selections than for backward selections in all years, though in year 6 it was only significant at the = 0.08 level (Figure 1b). Forward selections grew 3–6 millimeters more in diameter per year than backward selections in every year. Scion height Forward selections were significantly taller, at the = 0.01 level, than the backward selections in all six years (Figure 2a). Additionally, in all but year six the annual growth increments for forward selections significantly exceeded those for backward selections (Figure 2b). Also, the effect due to scion chronological age, within the forward selections, was significant at the = 0.01 level in all six years.
250
Figure 1. Scion diameter growth of backward selections and forward selections for 6 years after grafting: (a) total diameter; (b) annual diameter growth. The values in parentheses are the levels at which the comparisons between backward and forward selections were significant. The 5 and 15 years lines in figure a) are the results from the prediction equations. The regression of scion diameter on scion chronological age within forward selections was significant (at = 0.01) in years 3, 4 and 6 for Figure a.
251
Figure 2. Scion height growth of backward selections and forward selections over 6 years; (a) total scion height; (b) annual scion height growth. The values in parentheses are the levels at which the comparisons between backward and forward selections are significant. The 5 and 15 year lines in figure a) are the results from the prediction equations. The regression of scion height on scion chronological age within forward selections was significant (at = 0.01) in all years for Figure a.
252 Scion branching Backward selections had significantly fewer lateral branches per ramet ( = 0.05) in years 1 through 4 (Figure 3a). In all 4 years, the effect due to chronological age within forward selections was significant at the = 0.01 level, and the 15-year-old scion had fewer branches than the 5-year-old scion. Thus, the trend that chronologically older scions have fewer branches was present both between backward and forward selections and within the forward selections. In years 1 through 4 there was a significant difference between the backward and forward selections (at = 0.05) for number of branches per unit height (Figure 3b). This difference per unit height and the greater height of forward selections (Figure 2a) provided two bases for the difference in branch number. In all four years, the effect due to chronological age within forward selections was significant at the = 0.01 level, and the 15-year-old scion had fewer branches per unit height than the 5-year-old scion. Thus, chronologically older scions had fewer branches per unit height in both comparisons. The differences within forward selections were as great as the differences between backward and forward selections. Scion diameter to rootstock diameter ratio The ratio of scion diameter to rootstock diameter changed over time. A significant difference in year 1 was probably due to a difference in the size of scion when collected. In year 1 backward selections had a mean ratio of 0.788 and forward selections had a mean ratio of 0.753. Backward selections were probably larger at first because they were collected from widely spaced, intensively managed orchard trees, while the smaller forward selections were collected from denser, less intensively managed progeny tests. In year 2, the scion to rootstock diameter ratio was similar between age groups (backwards were equal to 0.742 and forwards were equal to 0.750) due to greater diameter growth of forward selections. In year 3, the forward selections had a significantly higher scion to rootstock diameter ratio, again probably due to greater growth of forward scion. Backward selections had a ratio of 0.753 and forward selections were 0.773. After the third year, the ratio seemed to stabilize with the forward selections remaining significantly larger than the backward selections. This may reflect the time it takes for complete healing of the graft union. Analysis of the effect of chronological age within forward selections followed almost the same trend as the comparison between backward and forward selections, and was significant at the = 0.01 level in years 1, 4, 5 and 6 of growth.
253
Figure 3. Lateral branch production by backward selections and forward selections over 4 years: (a) total branch number; (b) branch number per unit height. The values in parentheses are the levels at which the comparisons between backward and forward selections are significant. The 5 and 15 year lines are the results from the prediction equations. The regression of branch production on scion chronological age within forward selections was significant (at = 0.01) all in four years for Figure a and b.
254 Scion height to scion diameter ratio The scion height to scion diameter ratio was only significant in the first 2 years of measurement, with backward selections being stockier than the forward selections (i.e., lower height to diameter ratio than the forward selections). The first 2 years values were most likely a result of a significant difference in scion shape at time of scion collection, since the stockier backward selections were collected from intensively managed orchard trees, while the smaller forward selections were collected less intensively managed progeny tests. The lack of significance of the scion height to diameter ratio would indicate that, although the backward selections were growing slower than the forward selections, their stem forms were similar. Maturation effects on reproduction Female strobili production Production of female strobili was insufficient to test for differences in years 1 through 3. In year 4, the difference in female strobili production between backward and forward selections was only significant at the = 0.14 level (Figure 4a). During year 5 the backward selections produced significantly more female strobili at the = 0.05 level than the forward selections; however, in year 6 the difference was non-significant (Figure 4a). There was a greater number of strobili present on backwards selections despite them being smaller in diameter, shorter and having fewer branches. However, the absolute difference was only about 3 female strobili per ramet. There was a significant effect of scion chronological age within forward selections on female strobili production from year 4 through year 6. Differences between the 5- and 15-year-old scions were as great or greater than the differences between backward and forward selections in years 4 and 6 (Figure 4a). This may be due to the older forward selections effectively behaving like the backward selections in terms of female strobili production. Catkin production Forward selections produced significantly more catkin clusters per tree than backward selections in years 5 and 6 (Figure 4b). This could be because most forward selections, though chronologically younger than the backward selections, were close to reproductive maturity. Of the forward selections 72% were 6 to 10 years old. Thus, the forward selections could have already been fully mature, and may have produced more catkin clusters than the backward selections due to their larger size and more branched growth. The effect of scion chronological age on catkin production within forward selections was only significant in year 4 at the = 0.01 level, but there were so few catkin clusters present that the results might not have been representative
255
Figure 4. Female and male strobili production by backward selections and forward selections over 6 years: (a) number of female strobili produced per ramet; (b) number of male catkin clusters per ramet. The values in parentheses are the levels at which the comparisons between backward and forward selections are significant. The 5 and 15 year lines are the results from the prediction equations. The regression of strobili production on scion chronological age within forward selections was significant (at = 0.01) in all years for Figure a and only year 4 for Figure b.
256 of all 9 locations. The trend within the forward selections was similar to that found between the backward and forward selections in years 5 and 6 (Figure 4b). General discussion and conclusions Differences in ramet growth were consistent with the commonly accepted effects of maturation in conifers (Bolstad and Libby 1982; Greenwood 1984; Burris et al. 1991). Chronologically older scions had fewer branches, grew less and seemed to produce more female strobili than chronologically younger material. Even after 6 years of growth under the same conditions, there was a significant difference in scion height and scion diameter growth due to scion chronological age. Similar behavior was found in radiata pine. Bolstad and Libby (1982) noticed that chronologically older material achieved less diameter growth than chronologically younger material even after 8–10 growing seasons, and the older material developed fewer lateral branches. Younger scions initially attained more height growth than the older scions, but after 1 to 3 years additional growth the difference in height was not highly significant (Bolstad and Libby 1982). They also found that strobilus production was lowest on seedlings and highest on scion from mature clones. After several years of strobilus production, however, the seedlings produced more strobili because of their larger size and greater number of branches. Greenwood (1984) found that chronologically older grafts of loblolly pine had significantly less growth in height and diameter increment and fewer branches than younger material when grafted onto similar rootstock. A study that was looking at methods to increase scion production in loblolly pine clone banks found that first generation clones (average chronological age of 76) were significantly smaller in diameter and height than second-generation clones (average chronological age of 18) (McKeand et al. 1988). Franklin’s (1969) study on scion maturation effects on grafted slash pine found consistently negative correlations between scion age and height and diameter, which is consistent with the results of this study. However, the effects of scion chronological age on the reproduction of grafts were not examined in that study. Greenwood (1984) found, when looking at scion with chronological ages of 1, 4, 8 and 12 years, that catkin and female strobili production were only significantly lower in the 1-year-old scion. Greenwood (1981) suggested that loblolly pine exhibits complete juvenile behavior only for the first year and then enters a transitional period. Slash pine might exhibit similar maturation behavior. Forward selections in this study were mostly over 6 years old when
257 grafted and could have nearly completed their transitional period. Thus, the significantly greater catkin production of chronologically younger scion is possibly due to their larger size and greater number of branches. A lack of extremely young scion clones may also explain why the backward selections only produced significantly more female strobili in year 5. Many of the studies on the effects of scion maturation on growth and reproduction of conifers included 1-year-old scion, which seem to exhibit completely juvenile behavior (Greenwood 1981; Bolstad and Libby 1982; Greenwood 1984; Burris et al. 1991). It is possible that over the next few years the differences in catkin production between the backward and forward selections might decrease as the backward selections grow larger. On the other hand annual growth of forward selections will likely continue to exceed that of backward selections and produce an increasingly larger crown, with an increasingly greater number of catkin clusters. It is also likely that over the next few years the difference in female strobilus production between backward and forward selections will decrease, since the larger forward selections will have an increased number of possible sites on which female strobili might develop (Bolstad and Libby 1982). There are several likely impacts on slash pine clone banks and seed orchards due to chronological age effects. Chronological age effects persist for at least 6 years after grafting, and can have profound effects on growth. Differences in diameter growth exist at 6 years (Figure 1) and are likely to continue. The greater number of branches on chronologically younger selections is informative, but could be of limited practical importance in a managed orchard since pruning may equalize the number of branches per unit height between backward and forward selections (Figure 3). Branching differences could be important, however, in the upper crowns in later years, when the younger scion have more potential sites on which strobili might form. In terms of reproductive growth, chronologically older selections produced only a few more female strobili at 5 years after grafting (Figure 4a). At the present, we can only say that older scions might be slightly more precocious than younger scions. If measurements are made through ramet age 10, it should be possible to determine whether older scions actually have higher fecundity. It is possible, however that the younger scions will produce more female strobili than the older scions due to their increasingly larger size and greater number of branches. Also of future interest will be the production of catkin clusters, since in years 5 and 6, the younger scions produced significantly more catkin clusters per tree (Figure 4b). If this trend continues for several more years, younger scions will produce a great deal more pollen than the older material. Thus, it
258 may be desirable operationally to have chronologically younger scions in an orchard to help reduce pollen contamination in the early production years of a seed orchard. This study demonstrates that there are significant effects due to scion chronological age within slash pine clone banks. Although significant increases in female strobili production were only evident in year 5, the modest increases in other years could shorten breeding cycles by one year. Backward selections probably will not produce enough early female strobili to reduce the time to operational seed production. The larger, more highly branched, chronologically younger scion are likely to continue to produce more pollen, and could eventually produce more female strobili, since their increased size should provide more sites on which primordia might form. This study clearly demonstrates the presence and persistence of chronological age effects in slash pine due to scion maturation stage. The size and breadth of this study lends strong support to the idea that this pattern of growth will occur for slash pine in any location throughout its native range.
Acknowledgement We gratefully acknowledge the support of the Cooperative Forest Genetics Research Program.
References Bancroft, T. A. 1968. Chapter 1. In: Topics in Intermediate Statistical Methods. Iowa State Univ. Press, Ames, IA. Bolstad, P. V. and Libby, W. J. 1982. Comparisons of radiata pine cuttings of hedge and tree-form origin after seven growing seasons. Silvae Genet. 31(1): 9–13. Bozivich, H., Bancroft, T. A. and Hartley, H. O. 1956. Power of analysis of variance test procedures for certain incompletely specified models, I. Ann. Math. Stat. 27: 1017–1043. Brink, R. A. 1962. Phase change in higher plants and somatic cell heredity. Q. Rev. Biol. 37(1): 1–22. Burris, L. C., Williams, C. G. and Douglas, S. D. 1991. Flowering response of juvenile selections in loblolly pine, pp. 110–119. In: Proc. 21st South. For. Tree Improv. Conf. Knoxville, TN. Eggler, W. A. 1961. Stem elongation and time of cone initiation in southern pines. Forest Science 7: 149–158. Fortanier, E. J. and Jonkers, H. 1976. Juvenility and maturity of plants as influenced by their ontogenetical and physiological ageing. Acta Hortic. 56: 37–44. Franklin, E. C. 1969. Ortet age has strong influence on growth of vegetative propagules of Pinus elliottii. In: Proc. Second World Consultation on Forest Tree Breeding, August 7–16. Washington DC, IUFRO Paper FO-FTP-69-718. Greenwood, M. S. and Nussbaum, E. S. 1981. Rooting ability and vegetative growth performance of stem cuttings from one- and five-year-old ortets of loblolly pine, pp. 176–183. In: Proc. 16th South. For. Tree Improv. Conf., May 27–29. Blacksburg, VA.
259 Greenwood, M. S. 1981. Reproductive development in loblolly pine. II. The effect of age, gibberellin plus water stress and out-of-phase dormancy on long shoot growth behavior. Am. J. Bot. 68(9): 1184–1190. Greenwood, M. S. 1984. Phase change in loblolly pine: Shoot development as a function of age. Physiol. Plant 61: 518–522. Greenwood, M. S., Hopper, C. A. and Hutchison, K. W. 1989. Maturation in larch I. Effect of age on shoot growth, foliar characteristics, and DNA methylation. Plant Physiol. 90: 406–412. Greenwood, M. S. and Hutchison, K. W. 1993. Maturation as a developmental process, pp. 15– 33. In: Ahuja, M. R. and Libby, W. J. (Eds) Clonal Forestry I, Genetics and Biotechnology. Springer-Verlag, Berlin. Hackett, W. P. 1985. Juvenility, maturation, and rejuvenation in woody plants. Hortic. Rev. 7: 109–155. Hackett, W. P., Murray, J. R., Woo, H., Stapfer, R. E. and Geneve, R. 1990. Cellular, biochemical and molecular characteristics related to maturation and rejuvenation in woody species, pp. 147–153. In: Rodriguez, R., Tames, R. S. and Durzan, D. J. (Eds) Plant Aging: Basic and Applied Approaches. Plenum Press, New York, NY. Hood, J. V. and Libby, W. J. 1978. Continuing effects of maturation state in radiata pine and a general maturation model, pp. 221–233. In: Hughes, K. W., Henke, R. and Constantin, M. (Eds) Propagation of higher plants through tissue culture: A bridge between research and application. Technical Information Center United States Dept. of Energy, Springfield, VA. McKeand, S. E., Sprague, J. R., and Jett, J. B. 1988. Management of loblolly pine clone banks for scion production. South. J. App. For. 12(4): 231–234. Meier-Dinkel, A. and Kleinschmit, J. 1990. Aging in tree species: present knowledge, pp. 51– 63. In: Rodriguez, R., Tames, R. S. and Durzan, D. J. (Eds) Plant Aging: Basic and Applied Approaches. Plenum Press, New York, NY. Milliken, G. A. and Johnson, D. E. 1984. Analysis of Messy Data Volume I: Designed Experiments. Lifetime Learning Publications, Belmont, California, 473 p. Olesen, P. O. 1973. On transmission of age changes in woody plants by vegetative propagation, pp. 64–70. In: Royal Veterinary and Agricultural University Yearbook 1973. Royal Veterinary and Agricultural Univ., Copenhagen. Oliveira, C. M. and Browning, G. 1993. Studies on the induction of flowering in juvenile Prunus avium L. J. Hortic. Sci. 68(5): 731–739. SAS Institute. 1989. SAS/STAT – User’s Guide, Version 6, Fourth Edition, Volume 2. SAS Institute Inc. Cary, NC, 846 p. Snowball, A. M., Halligan, E. A., Warrington, I. J. and Mullins, M. G. 1994. Phase change in citrus: Growth and flowering of citrus seedlings from thirteen genetically diverse seedling families. J. Hortic. Sci. 69(1): 141–148. Thorpe, T. A. and Harry, I. S. 1990. Special problems and prospects in the propagation of woody species, pp. 67–74. In: Rodriguez, R., Tames, R. S. and Durzan, D. J. (Eds) Plant Aging: Basic and Applied Approaches. Plenum Press, New York, NY. Visser, T. 1964. Juvenile phase and growth of apple and pear seedlings. Euphytica 13: 119–129. Visser, T. 1965. On the inheritance of the juvenile period in apple. Euphytica 14: 125–134. Zimmerman, R. H. 1972. Juvenility and flowering in woody plants: A review. HortScience 7(5): 447–455.
