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Root and Stump Buds as Structural Faculties for Reinvigoration in Alnus incana (L.) Moench
Flora (1992) 187: 353-367 Gustav Fischer Verlag lena
Root and Stump Buds as Structural Faculties for Reinvigoration in Alnus incana (L.) MOENCH KATRI PAuKKoNENand ANNELI KAUPPI Cniversity of Oulu, Department of Botany, Oulu, Finland and
ARI FERM Finnish Forest Research Institute, Kannus Research Station, Kannus, Finland
Summary The formation, structure and development of sprout-forming buds of Alnus incana (L.) MOENCH and also the sprouting of stumps of different ages were observed after felling. The growth of prevcntitious, i.c. axillary basal buds during dormancy was slight. As a consequence of radial growth of the tree, they were embedded in the wood unless they had bUTst at an early stage and grown into short shoots. Thus the sprout forming buds at the bases of the stumps were mainly adventitious. Sometimes they existed in groups, when a large number of buds formed almost simultaneously on the meristematic tissue activated in the cambium. Meristematic knots also developed on the roots, and many adventitious buds could form in these. The traces of the root buds usually reached the primary xylem, and could branch vigorously. The conglomeration of root buds could grow very large, but usually only about 20 - 30% of them actually burst to form suckers. Stools which had been coppiced once before sprouted much better than those coppiced for the first time. The buds localed above ground level, in particular, often developed into sprouts. 'Intact trees sprouted poorly, on account of the small number of buds, as the adventitious meristems were activated markedly only after felling. Repeated coppicing seems to improve the sprouting ability of Alnus incana stumps.
1. Introduction The buds located near or below ground level are extremely important in the vegetative reproduction of trees, but most morphological and anatomical research deals with buds located higher on the trunk, i.e. axillary ones, and buds developing near them (e.g. GARRISON 1949a, b; KORMANIK & BROWN 1969; CREMER 1972; FINK 1983). Basal buds may differ clearly from upper ones in their structure, e.g. in birches (KAUPPI et a!. 1987), but only limited research into the structure and bursting of buds located at the bases of trees of certain species has been conducted previously (e.g. LOHMATOV 1953; BRUNKENER 1984; KAUPPI et a!. 1987, 1988; PAUKKONEN et a1. 1992) and considerable variations between species have been observed. The bursting dynamics of sprout-fonning buds have been shown to be important for gaining the best results in sprouting and short rotation cultivation (KAUPPI et a\. 1991). Research into alder in Finland and Sweden has included an examination of their use in energy forests (GRANHALL 1982; KORPELAINEN 1982), their suitability for soils in which
354
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other trees will not grow (KORPELAINEN 1982), felling times (HEIKINHEIMO 1930), fertilization (RIKALA & ROSSI 1981) and biomass production (RYTTER 1990, SAARSALMI et al. 1991), but not the morphological basis for vegetative reinvigoration. Not even the sprout-forming buds of the fast-growing American red alder (Alnus rubra) have been investigated in this respect although this species has been examined intensively in the context of short rotation cultivation (e.g. DE BELL et al. 1978; HARRINGTON 1984). In addition to basal buds, Alnus incuna also forms numerous root buds, and thus suckers (e.g. B0RSET 1976; ALI-ALHA 1987). Research into the root buds of trees in general is limited, although the development of the shoot primordia and their anatomy has been monitored to some extent (BROWN 1935, SIEGLER & BOWMAN 1939; SANDBERG & SCHNEIDER 1953; SCHIER 1981). The present paper draws attention to the anatomy and morphology or both stump and root buds of Alnus incanu, their development, bursting and sprouting dynamics.
2. Terminology The basic terminology concerning buds can be seen in KAUPPI ct al. (1987). Bud initials, which possess no leaf primordia, are termed here 'merislematic knots'. When leaf primordia can be observed (microscopically at first), they are called 'bnds'. Buds which have started to grow but possess no foliage leaves arc classified as activated or burst, and when the real foliage leaves with laminae have begun to enlarge and the internodes to lengthen the structure is called a 'sprout' or 'sucker' depending on its origin, the fonner originating from the stump or the base of an earlier sprout and the latter from roots.
3. Material and Methods Different kinds of buds on stumps and roots (for a classification of buds, see KAUPPI et a1. 1987, Table 1), and their bursting were examined in a total of 50 grey alders (Alnus incana (L.) MOENCH) collected from cultivated stands mainly at Kannus- (23" 50' E, 63° 52' N) and some at Haapavesi (25" 38' E, 64° 05' N). The trees were coppiced at the beginning of May leaving stumps 15 em high, and the roots were cut to only 10 em when sampled, whieh must be taken into account when considering the numbers of root buds and suckers originating from them. Stools of five types were used in the experiment on sprouting dynamics, these being sampled three times during the growing season at approximately monthly intervals (Table 1). Three intact plants were also studied. The stumps, sprouts and roots were Tab. 1. :-.lumbers of Alnus incana stools and their collection schedule. Stool type
Collection time 26th May
Intact plants'·) - 20 year old intact plants Coppiced plants 3 year-old stools 7 year-old stools 21 year-old stools, first coppicing I year earlier -- 25 year-old stools, first coppicing 5 years earlier
26th June
4th August
4 4 4 4
3 6
4
4 4
4 4
4
4
a) Coppiced about 3 weeks before first collection, at the beginning of May.
Root and Stump Buds in Alnus incana
355
examined separately. In addition, some one and two years old seedlings were studied to observe the early stage of the axillary (i.e. preventitious) and adventitious buds as named by HARTIG (1878) and described anatomically by FINK (1980a, b). The primary criteria for distinguishing between axillary and adventitious buds were I) the vascular connections from the bud to the primary xylem/pith, and 2) the location of the buds in relation to the normal phyllotaxy (AARON 1946; KORMANIK & BROWN 1969; FINK 1980a, b, 1983). The formation and development of new, first-order sprouts was monitored in three- and seven-year-old seedlings, and new first and second-order sprouts .in 21- and 25-year-old trees. Domlant and burst buds were counted separately both above and below ground level. The stumps were kept in water for six days after sampling so that any buds which had been overlooked would become visible and could be counted. After that the stumps were peeled to reveal any buds existing under the bark. The buds were examined by stereo light microscopy performed on fresh samples, and their surface structures were studied with a JSM 6400 scanning electron microscope. The samples for scanning electron microscopy were fixed in FAA (formalin, ethanol, glacial acetic acid), dehydrated in an alcohol gradient. dried by the critical point method, mounted on SEM adapters with glue, and coated with gold. For identification of bud origin and the early development of root buds, an ontogenetic examination was carried out on light microscopic tissue sections fixed in FAA and mounted in hydroxyethylmethacrylate (Reichert-Jung Historesin). 5-10 Ilill sections were cut with glass knives using a LKB ultramicrotome and stained with 0.05% toluidincblue.
4. Results 4.1. Origin and structure of buds The buds observed at the stem bases of the young grey alder seedlings could be either preventitious or adventitious in their origin (Fig. 1, 2), but it was observed that the new bud primordia which appeared to originate from the vascular trace of an axillary bud were in fact of adventitious origin and had started to grow from the cambium near the trace of the preventitious bud (Fig. 1b, c). The first indication of such a bud was a knot on the bark (Fig. 2d), which grew until the bark finally tore open. No leaf primordia could be detected in the developing bud at this stage, and it also differed from an axillary bud in external appearance. The axillary buds (Fig. 2 b) remained on the bark surface only if they had started to grow, mostly into short shoots (Fig. 2e, f), in which case they grew a scale whorl formed by stipules every year, which then came loose. Later some of these short shoots grew into long shoots (Fig. 2{), which differed from the adventitious sprouts in the fOlm of their base (Fig. 2g), the base of a preventitious shoot being markedly thicker and having more scars than upper part that had grown as a long shoot. Dormant axillary buds (Fig. 2a, c) occurred on thick alder trunks almost exclusively at the bases of the branches. No scars located close to each other could be observed at the bases of adventitious sprouts. The rapidity of development of the adventitious buds, on both stumps and roots, varied markedly depending mainly on decapitation and the environmental conditions in which the tree was growing. Adventitious shoot buds also developed on the roots in this species taking the form of meristematic knots (Fig. 4a) which had a vascular connection extending to the primary xylem and structures typical of buds, e.g. first the apical meristem and later the leaf primordia could be seen buried in the bark (Fig. 3). The root buds could branch from the vascular trace of the original bud (Fig. 3 a, d), and the stem of the root bud could even grow in a curved manner inside the bark (Fig. 3 b, e). When located below ground level, the root buds increased in length (Figs. 4b, e, f) so that a few short internodes were observed in them. Stipules and small axillary buds were observed in the nodes, but no laminae (Fig. 4e). The underground axillary buds (Fig. 4e) differed from the aerial ones (Fig. 2a, c, e) and from all the adventitious buds (Fig. 2b, d). When growing in the light, however, the root buds started to grow vigorously into suckers immediately after maturing and formed foliage leaves at once (Fig. 4c, d).
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The adventitious buds usually formed conglomerations, which were smaller and fewer in number on the stools (Fig. 2g) than on the roots (Fig. 41). Buds were able to form rapidly and in considerable numbers on the stools, while the meristematic knots in which they formed on the roots were usually large and were able to grow into conglomerations consisting of dozens of buds. Many bud primordia developed rapidly in the same meristem, and more buds could form later. Thus some buds had burst while other primordia were still developing (Fig.4c).
Fig.!. (see page 357) Fig. I. Initiation of basal buds of Alnus incana. a) Cross-section of a 3-year-old stem. The trace of the preventitious bud reaches the pith (arrow). Bar = 0.25 mm. b) 'Branching' vascular trace of a basal bud (arrows). Note that the section has not been cut entirely longitudinally. Bar = 0.25 mm. c) Close-up view of Fig. I b). The lateral buds (1) do not branch directly from the trace of the primary bud but initiate from the cambium near the trace. Bar = 0.1 mm.
Fig. 2. (see page 358) Fig. 2. Basal buds of Alnus incana. a) Buds located in the leaf scars in the order of phyllotaxy of the dead prcventitious bud (arrows). These buds are of axillary origin concluding from their location. They are probably the lowest axillary buds of the dead bud. Bar = 5 mm.b) A group of three adventitious buds around the original preventitious bud scar (arrows). They are not located in the axils of leaf scars. Bar = 5 mm. c) SEM micrograph of a preventitious basal bud. Bar = 0.5 mm. d) SEM micrograph of basal buds on a current season sprout. p - preventitious bud with numerous scales and leaf primordia, a - adventitious buds of which the smaller aneis very young. Bar = 0.5 mm. e) A preventitious bud at the base of the stem has started to grow as a short shoot (ss). I) A preventitious bud at the base of the stem has started to grow as a short shoot but is now growing as a long shoot (arrow). g) Sprouts initiating from buds located on the root collar. There are numerous buds in the same group, most of them adventitious but some of axillary origin.
Fig. 3. (see page 359) Fig. 3. Root buds of Alnus incilna. a) A shoot bud primordium on a 3-year-old root. The bud trace reaches the primary xylem. This bud seems to be branching (b). There are also signs of another shoot bud (arrow). Note the large bulge in the cortex. t - tracheids. Bar = 0.25 mm. b) Longitudinal section of a root bud growing inside the bark from the same bud conglomeration as in Fig. 3a. The growing bud tears the cortex first and finally the cork. a - apical meristem, s - stem of the bud. Bar = 0.25 mm. c) Close-up view of the other knot indicated by the arrow in Fig. 3a. The section has been taken at a different level. Bar = 0.25 mm. d) Close-up view of the branching vascular trace indicated by t in Fig. 3a. Note the differentiating transversal tracheids (arrow), Bar = 0.1 mm. e) A root bud primordium (meristematic knot) entombed in the cortex. No leaf primordia can be observed yet. a ~ apical meristem. Bar = 0.25 mm.
Fig. 4. (see page 360) Fig. 4. Root buds of Alnus incana. a) SEM micrograph of a meristematic knot on a root, a shoot bud at an early stage. Bar = 0.05 mm. b) A lengthened root bud (arrow): The tip of the bud was green when sampled. r - root. Bar = 5 mm. c) A burst root bud (grown in light). The two small meristematic knots indicate new activated sites of emerging buds (arrows). Bar = 10 mm. d) SEM close-up of the bud group in Fig. 4c from another angle. Bar = 1 mm. e) A growing root bud. Nodes and axillary buds can be seen. The internodes in the upper part of the bud are very short. The Ieaj~like organs are stipules. s - scars ofstipules of the axillary bud (b), which is broad and short. Bar = I mm. I) A large bud conglomeration on the underside of a root. s - suckers, a - activated buds, d - dormant buds.
Root and Stump Buds in Alnus incana
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Root and Stump Buds in Alnus incana
359
360
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361
Root and Stump Buds in Alnus incana
Tab. 2. Numbers of buds and sprouts on stools of Alnus incanu. First sampling 3 weeks after coppicing. Total number of buds
Above ground level on stump on sprouts Below ground level on stumps on sprouts on roots
* significant at 5%
a)
Type of bud
26th May
26th June
4th August
x
S.D.
it
x
Dormant Activated Dormant Activated Dormant Activated Dormant Activated Dormant Activated Dormant Activated Dormant Activated
4.4 0.8 0 0 4.4 0.8 17.1 2.6 4.5 0 1.0 0 11.6 2.6
5.1 1.5 0 0 1.8 0.5 19.1 4.3 3.5 0
2.5 0 16.3 4.3
S.D.
1.7 4.2
3.6 1.4 1.6 3.9 9.0 17.0 2.2
0.6 1.6 3.2 14.9 10.4
1.0 2.9 7.7 3.3 l.l 2.7 6.1 21.4 3.1 1.5 1.7 4.2 14.1 17.4
1.3
13.6 0.8 8.2 0.9 9.9 19.0 6.9 2.7 2.9 1.0 1.3
11.1 2.6
F
S.D. 1.5 7.7 1.3
15.86***
9.3
6.21**
1.4 7.6 16.0 5.3 5.0 4.2 2.8 2.6 9.9 3.2
7.88**
3.60*
level; ** significant at 1% level; *** significant at 0.1 % level
4.2. Number and location of buds The number of buds differed markedly between the types of alder stool. In general, there were a large number of buds - mostly adventitious - on the stools, an average of 25.8 per stool, with a geometrical mean of 21. The 20-year-old intact trees ha
.. ,',",
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Below ground level StumR§ Above ground level Below ground level
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100 150 200 250 300 350 400 450
Total number of buds, sprouts and suckers Fig. 5. Total numbers of dormant and activated buds, sprouts and suckers on different parts of the stool above and below ground level at the three sampling times (26th May, 26th .June, 4th August). 24
Flora, Bd. 187. 5/6
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The numbers of both dormant (mainly adventitious) and activated buds (Fig. 6) increased during the growing season as a consequence of felling in all the trees coppiced once and in the older ones of those coppiced twice, as the bud conglomerations and the numbers of buds in them grew. The intact trees had no bud conglomerations, not even on the roots. Large numbers of buds formed on the stools within three weeks of coppicing, but the number of buds on the sprouts and stools of the samples already coppiced once or twice did not reach its maximum until 14 weeks after coppicing. The number of root buds was largest three weeks after coppicing, then remaining almost the same throughout the growing period. The adventitious buds on the stools were abundant on scars and at the bend in the root collar (Fig. 2g), while the buds on the roots often occurred on bends or at branching sites (Fig. 4b, c). Adventitious buds also commonly developed around the preventitious buds (Fig. 1b, c, 2d) and scars (Fig.2b).
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80 60
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Fig. 6. Numbers of dormant and activated buds, sprouts and suckers in a) intact trees, b) 3-year-old trees coppiced once, c) 7-year-old trees coppiced once, d) 21·year-old trees coppiced for the fist time at 20 years of age, and e) 25-year-old trees coppiced for the first time at 20 years of age. Coppiced by the beginning of May at the latest.
363
Root and Stump Buds in Alnus incana
4.3. Sprouting potential of stumps
The buds burst rapidly after coppicing (Table 3a), the activated ones being located mostly at the base of a stump or sprout, but rarely further up (Fig. 2g), and in the large conglomerations on the roots, where only some of them burst (Fig. 41). The root buds which remained dormant over the season in which they developed seldom burst later. The root buds burst more quickly than the stump buds. When many of the root buds on the trees already coppiced twice had burst within three weeks of coppicing, almost all the buds on those coppiced once were still dormant. Buds were activated gradually over the whole growing period in the other parts of the plant, i.e. on the sprouts and stumps, but they seldom grew into sprouts (Fig. 6). A clear difference in sprouting existed between the types of alder stool, with 29 out of the 53 stools sprouting (55%), to gain an average of four sprouts per stool. The stools that did not sprout did not die during the experiment, however. In spite of the high number of buds, only four of the stools coppiced once sprouted, mostly fonning two sprouts, giving an average of only 0.2 sprouts and a sprouting intensity of less than 1 (Table 3b). Sprouting intensity (KAUPPI et al. 1988) is defined as follows:
Tab. 3. Sprouting of Alnus incana. a) Rapidity of sprouting after coppicing. b) Sprouting intensity of seed- and sprout-origin stools in relation to age and part of stool. a) . Sampling date
26th May, control 26th May, 3 weeks after coppicing 23th June, 8 weeks after coppicing 4th August, 14 weeks after coppicing
No. of stools
3 18 16 16
No. of sprouts ') per stool it
min.
max.
0.3 6.3 1.4 3.9
0 0 0 0
1 12 7 12
b) Types and parts of stools from which sprouts and suckers grow
Stools coppiced once 3 year old - 7 year old - stumps - roots . Stools coppiced twice (first coppicing at 20 years of age first coppicing I year earlier first coppicing 5 years earlier sprouts stumps roots 20 year old intact plants Total
No. of stools
Total no. Total no. of buds of sprouts·)
Sprouting intcnsity')
0.8 2.2
26 14 12 25 26 24
608 219 389 294 314 755
5 5 0 3 2 198
0.2 0.4 0 0.1 0.1 8.3
1.0 0.6 20.8
12 12 198 24 24h) 3 53
496 259 269 159 327 4 1367
138 60 131 56 11
11.5 21.6 0.7 2.3 0.5 0.3 3.8
21.8 18.8 32.8 26.1 3.3 20.0 13.0
a) Including suckers; b) Number of stools; C) Defined in the text 24°
Total no. of sprouts') per stool
I
204
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K. PAUKKONEN and A. KAUPPI
where SI is sprouting intensity, Ns is the number of single buds forming sprouts, N g is the number of grouped buds forming sprouts and Nd is the number of dormant buds. On the other hand, all the stools coppiced twice sprouted, the minimum number of sprouts on them being two, the maximum 21 and the average 8.3. The trees coppiced for the first time a year earlier sprouted very well after the second coppicing, as almost 2/3 of all the sprouts were located on them. These sprouts were mainly of second order, but there were quite a number of new, first-order sprouts on the root collars well. The sprouting intensity was highest in these parts (Table 3 b), and the average sprouting intensity reached 20 for whole stools that had been coppiced twice. Only one of the 20-year-old intact trees sprouted, growing one sprout, the high sprouting intensity of these being due to the very small number of buds. There were only a few suckers, despite the large number of buds, both dormant and activated, on the roots of all the stools examined (Fig. 6). The highest number of sprouts was observed three weeks after coppicing on every type of stool, and observations made later showed the number to have diminished by about 50% due to high mortality among the sprouts of adventitious origin, which were only weakly attached to the wood and thus easily came loose.
5. Discussion Trees in<:rease their diameter even during the dormant period, so that if the basal buds do not lengthen they will become buried in the bark and finally in the wood. In some species, e.g. birches (KAUPPI et al. 1987), the basal buds grow and stay on the bark, but in grey alder studied here they grew extremely poorly and were buried in the bark, as were the buds of Salix alba (FINK 1983). The preventitious buds of the grey alder remained on the bark only if they burst and started to grow soon after maturing. The stipule whorls of the short shoots came loose in the alder, but remained attached in birch (KAUPPI et al. 1987). In Acer saccharum (CHURCH & GODMAN 1966) and Liquidambar styraciflua (KORMANIK & BROWN 1969) semidormant buds may grow as short shoots, too. It has been noted that felling induces these buds of Liquidumbar styraciflua to grow into long shoots (KORMAN!K & BROWN 1969), as was also noted in Alnus incana. The grey alder formed sprouts from both preventitious axillary buds and adventitious buds, but those of the former type were scarce because the axillary buds in this species was not observed to branch in the same manner as in Betula pubescens (KAUPPI et £11. 1987), willows (BRUNKENER 1984; PAUKKONEN et a1. 1992), Acer saccharum (CHURCH & GODMAN 1966) or Liquidambar styraciflua (KORMANIK & BROWN 1969). The clustering of alder buds is not caused by branching of the primary buds but by the formation of many adventitious buds almost simultaneously. The largest tufts of sprouts on the stools grew on the root collar, as in Quercus chrysolepi.l' (PAYSEN et a!. 1991). The tissue on the border of a thickening root and stem can become irritated and it may be that the pressure induces large bud conglomerations. On the other hand, ~ome field observations (FERM, unpub!. data) suggest that many sprouts may grow near the cutting surface on an alder stump, as in the case of Ailanthus glandulosa (BORY et a!. 1991). On the other hand, suckers appear only after two or three cuts in Ailanthus glandulosa, while in the grey alder they may exist even in intact trees, though they are more numerous after cutting. According to field observations (FERM, unpub!. data), the majority of suckers of the grey alder grow some distance from the stump, and thus the number of suckers would be higher if longer sections of the roots were examined. Many shoot buds were observed on the roots of grey alder, often at bends. The bud conglomerations also started to develop early and enlarged as they aged. All the root buds examined had a trace to the primary xylem of the root, as is the case in the apple, too (SIEGLER & BOWMAN 1939). This is due to the fact that shoot buds start to develop on
Root and Stump Buds in Alnus incana
365
very young roots, probably beginning their growth from the pericycle, as in the aspen (SANDIlERG & SCHNEIDER 1953) and in Araucaria cunninghamii (BURROWS 1990). Buds initiating directly from the phellogen, as in poplars (BROWN 1935), were not observed in the alder, although it remained unsolved whether existing changes in the phellogen and cortex tissue, e.g. increased cell activity, would lead to bud initiation. The lengthening root buds formed nodes, and the leaves of these nodes were retarded. Thus, the initiation of the lowest axillary buds of a sucker corresponds to that of the basal buds of birches (KAUPPI et al. 1987). The grey alder sucker can branch from these buds, but very seldom does so spontaneously. Generally only a few buds in a conglomeration burst and the majority remain as dormant reserve buds which will either burst under favourable conditions or not at all. Thus, the adventitious meristems located on the roots, stools and bases of sprouts may remain dormant for years before they reach the real bud stage in their development, but once activated, e.g. as a consequence of coppicing, and having started to develop into buds, they will usually burst even though they do not always continue to grow into sprouts. The intact 20-year-old trees examined here had very few buds, but the number increased as a consequence of repeated coppicing as has been noted earlier in the birch (KAUPPI et al. 1988). It is possible that sprout-forming buds do not develop until the physiological state of the tree changes as a consequence of decapitation, and that meristem activation already occurs after the first coppicing even though the buds do not develop and burst on a large scale until after the second coppicing. The shoot primordia on the roots of the apple (SIEGLER & BOWMAN 1939) and poplar (BROWN 1935) can stay in a semi dormant stage during plant dormancy. The grey alder seems to be able to control the number of sprouts on each stool, as there were not more than ten sprouts during the first growing season even though there were many more activated buds. SAARSALMI et al. (1991) observed 5~8 sprouts per Alnus incana stool after the sixth growing season, and the present grey alder stools which had been coppiced twice carried very many more sprouts than those coppiced once. As in Quercus alba (MCGEE 1978) and Alnus rubra (HARRINGTON 1984), the sprouting results· achieved by the grey alder dependend on the age of the tree, especially in those coppiced twice, the younger ones sprouting better. Biomass production capacity has also been noted to be better after the second coppicing than after the first in young Populus plants (STRONG 1989). The results of this experiment are also similar to those for Alnus rubra, 4-year-old seedlings of which sprout poorly after the first coppicing (HEILMAN & STETTLER 1985). Apical dominance, which controls the bursting and growth of both sprouts and suckers (STENEKER 1974), is probably not as strong in sprout-origin stems as in the original seed-origin main stem, and partly for this reason the formation of new shoots could be stronger in trees of the former kind. The sprouts of the grey alder usually formed right at the base of existing ones, as in the red alder (HARRINGTON 1984), i.e. on the part of the stem where most of the buds on the stumps of Alnus incana were located. The fact that the buds located above ground level generally sprouted better than those located under the ground is due to the more favourable light conditions (e.g. KHAYAT & ZIESLIN 1982; JUNTTILA & JENSEN 1988). The birch similarly sprouts best from its aerial buds (KAUPPI et al. 1991), although this is partly due to the poor sprouting ability of underground buds, which very often exist in large clusters (KAUPPI et al. 1988). In the alder, too, the underground buds are usually found in large conglomerations, and the resulting competition between individual buds and the weak vascular connections mean that some of them die easily, which is also true of the above-ground sprouts, especially if they exist in large tufts. SAARSALMI et al. (1991) likewise observed that many alder sprouts die. Thus adventitious buds seem ~o be highly disposed to deterioration and die easily, as also seen by KORMANIK & BROWN (1967) and DEBELL & ALFORD (1972). Alnus incana may be a good alternative when reforestating, especially in wet (DESMET & MATON 1989) and poor soils (KORPELAINEN 1982) because of its remarkable biomass produc-
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K.PAUKKONEN and A. KAUPPI
tion ability (BJORKLUND & FERM 1982, RYTTER 1990, SAARSALMI et al. 1991). According to this study, it has a high budding capacity, ability to produce suckers, and ability to withstand repeated coppicings so that coppicing can even enhance sprouting and thus also productivity.
Acknowledgements The authors wish to thank the Kannus Research Station of the Finnish Forest Research Institute for providing the stump material PAIVI RINNE for some of the scanning electron micrographs and for technical assistance, ANTTT SAARENPAA, MARITTA KIVINIITTY and CHRISTINA TIGERSTEDT for their tcchnical assistance, and Mr. MALCOLM HICKS for revising the language of this paper.
References AARON, l. (1946): Dormant and adventitious buds. Science 104: 329. Au-AUlA, T. (1987): Kaatoajankohdan vaikutus lehtipuiden vesomiseen. (Effect of felling time on the sprouting of deciduous trees). M. Sc. Thesis, Faculty of Forestry, University of Helsinki, Helsinki, Finland. (in Finnish). BJORKLUND, T., & FERM, A. (1982): Pienikokoisen koivun ja harmaalepan biomassa ja tekniset ominaisuudet. Abstract: Biomass and technical properties of small sized birch and alder. Folia Forestalia 500: 1-37: B0RSET, O. (1976): Bj0rk, asp, or. Institutt for skogskj0tsel. Norges Lantbruksh0gskole. BORY, G., SIDIBE, M. D., & CLAIR-MACZULAJTYS, D. (1991): Effets du recepage sur les reserves glucidiques et lipidiqucs du 'faux-vernis du Japon' (Ailanthus glandulosa DESF., Simarubacees). Ann. Sci. For. 48: 1-13. BROWN, A. B. (1935): Cambial activity, root habit and sucker shoot development in two species of poplar. New Phytol. 34: 163-179. BRUNKENER, L. (1984): Gross morphology and anatomy of current shoots of Salix. Energy Forestry Project, Dcp. Eco!. Envir. Res., Swedish UI~iversity of Agricultural Sciences. Report 34. BURROWS, G. E. (1990): Anatomical aspects of root bud devciopment in hoop pine (Araucaria cunninghamii). Aust. J. Bot. 38: 73-78. CHURCH, T. W., & GODMAN, R. M. (1966): The formation and development of dormant basal buds in sugar maple. For. Sci. 12: 301-306. CREMER, K. W. (1972): Morphology and development of the primary and accessory buds of Eucalyptus regnans. Ausl. J. Bot. 20: 175-195. DEBELL, D. S., & ALFORD, L. T. (1972): Sprouting characteristics and cutting practices evalnated for cottonwood. Tree Planters' Notes, November 1972. -, STRAND, R. F., & REUKEMA, D. L. (1978): Short-rotation production of red alder: Some options for future forest management. USDA For. Servo Gen. Tech. Rep. PNW-70. pp. 231-245. DRS~lET, J., & MATON, A. (1989): A quantitative study of the possibility of afforestation with poplar, willow and alder on arable land and grassland in West and East Flanders, Belgium. Soil Technology 2: 91-100. fINK. S. (1980a): Anatomische Untersuchungen iiber das Vorkommen von SproG- und Wurzelanlagen im Stamm bereich von Laub- und Nadelbaumen. 1. Proventive Anlagen. Allg. Forst- u. Jagd-Ztg. 151: 160-180. (1980b): Anatomische Untersuchungen tiber das Vorkommen von Spro13- und Wurzelanlagen im Stamm bereich von Laub- und Nadelbaumen. II. Adventive Anlagen. AUg. Forst- u. Jagd-Ztg. 151: 181-197. (1983): The occurrence of adventitious and preventitious buds within the bark of some temperate and tropical trees. Am. J. Bot. 70: 532- 542. GARRISON, R. (1949a): Origin and development of axillary buds: Syringa vulgaris L. Am. J. Bot. 36: 205-213. - (1949 b): Origin and development ofaxillary buds: Betula papYri/era MARSH. and Eupte/ea polyandra SIEB. et Zucco Am. J. Bot. 36: 379-389. GRANHALL, U. (1982): Use of Alnus in energy forest production. In: The Second National Symposium on Biological Nitrogen Fixation, Helsinki 8th-10th of June 1982. The Finnish Fund for Research and Development. Nitrogen Project. Report I. pp. 273 - 285.
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HARRINGTON, C. A. (1984): Factors influencing initial sprouting of red alder. Can. J. For. Res. 14: 357 - 361. HARTIG, TH. (1978): Anatomie und Physiologie der Holzpflanzen. Berlin. HEIKINHEIMO, O. (1930): Kaatoajan vaikutus lehtipuiden vesojen syntyyn ja kasvuun. (Effect of felling time on development and growth of sprouts of deciduous trees). Tapio, Helsinki. pp. 113 -117. (In Finnish). HElLMAN, P., & STETTLER, R. F. (1985): Mixed short rotation culture of red alder and black cottonwood: Growth, coppicing, nitrogen fixation and allelopathy: For. Sci. 31: 607-616. JUNTTILA, 0., & JENSEN, E. (1988): Gibberellins and photoperiodic control of shoot elongation in Salix. Physiol. Plant. 74: 371-376. KAUPPI, A., PAUKKONEN, K., & RINNE, P. (1991): Sprouting ability of aerial and underground dormant basal buds of Betula pendula. Can. 1. For. Res. 21: 528-533. -, RINNE, P., & FERM, A. (1987): Initiation, structure and sprouting of dormant basal buds in Betula pubescens. Flora 179: 55 -83. - (1988): Sprouting ability and significance for coppicing of dormant buds on Betula pubescens EHRH. stumps. Scand. J. For. Res. 3: 343-354. KHAYAT, E., & ZIESLIN, N. (1982): Environmental factors involved in the regulation of sprouting of basal buds in rose plants. J. Exp. Bot. 33: 1286-1292. KORMANIK, P. P., & BROWN. C. L. (1967): Adventitious buds on mature trees. USDA For. Serv., Southeastern For. Exp. Stat., Res. Note SE-82. - (1969): Origin and development ofcpicormic branches in sweetgum. USDA For. Servo Res. Paper SE-54. KORPELATNEN, H. (1982): Experiments with Alnus hybrides in Finland. In The Second National Symposium on Biological Nitrogen Fixation, Helsinki 8th-10th of June 1982. The Finnish Fund for Research and Development. Nitrogen Project. Report 1: pp. 287 - 291. LOHMATOV, N. A. (1953) Pricini rannei poteri berezoi borodavcatoj poroslevoj sposobnosti. Lesnoe Hozjaistvo 2: 42-44. MCGEE, C. E. (197&): Size and age of tree affect white oak stump sprouting. South. For. Exp. Stat. Res. Note SO-239. PAUKKONEN, K., KAUPPI, A., & FERM, A. (1992): Origin, structure and shoot-formation ability of buds in cutting-origin stools of Salix 'Aquatica'. Flora 186: 53-65. PAYSEN, T. E., NAROG, M. G., TISSELL, R. G., & LARDNER, M. A. (1991): Trunk and root sprouting on residual trees after thinning a Quercus chrysolepis stand. For. Sci. 37: 17 - 27. RIKALA, R., & Ross], P. (1981): Sprouting of Alnus incana. Abstract in PERA-symposium, March 3-4, 1981, Helsinki. Abstract available from the Faculty of Forestry, University of Helsinki, Helsinki, Finland. RYTTER, L. (1990): Biomass and nitrogen dynamics of intensively grown grey alder plantations on peatland. Ph. Dr. thesis, Dcp. Eco!. Envir. Res., Agric. Univ. of Sweden. Report 37. SAARSALMI, A., PALMGREN, K.,& LEVULA, T. (1991): Harmaalepan vesojen biomassan tuotos ja ravinteiden kayttii. Summary: Biomass production and nutrient consumption of the sprouts of Alnus incana. Folia Forestalia 768. SANDBERG, D., & SCHNEIDER, A. E. (1953): The regeneration of aspen by suckering. Minnesota Forestry Notes No. 24, University of Minnesota. SUITER, G. A. (1981): Physiological research on adventitious shoot development in aspen roots. USDA, For. Serv .. Int. For. Range Exp. Stat., Gen Tech. Rep. INT-107. SIEGLER, E. A., & BOWMAN, J. J. (1939): Anatomical studies of root and shoot primordia in I-year apple roots. 1. Agr. Res. (Wash. D.C.) 58: 795-803. . STENEKER, G. A. (1974): Factors affecting the suckering of trembling aspen. For. Chron. 1974: 32-34. STRONG, T. (1989): Rotation length and repeated harvesting influence Populus coppice production. USDA For. Serv., North Central For. Exp. Stat., Res. Note NC-350. Received August 4, 1992 KATRI PAUKKONEN and ANN ELl KAUPPI,* Department of Botany, University of Oulu, SF-90570 Oulu, Finland, and ARI FERM, Finnish Forest Research Institute, Kannus Research Station, SF-69 100 Kannus, Finland.
* corresponding author
Root and Stump Buds as Structural Faculties for Reinvigoration in Alnus incana (L.) MOENCH KATRI PAuKKoNENand ANNELI KAUPPI Cniversity of Oulu, Department of Botany, Oulu, Finland and
ARI FERM Finnish Forest Research Institute, Kannus Research Station, Kannus, Finland
Summary The formation, structure and development of sprout-forming buds of Alnus incana (L.) MOENCH and also the sprouting of stumps of different ages were observed after felling. The growth of prevcntitious, i.c. axillary basal buds during dormancy was slight. As a consequence of radial growth of the tree, they were embedded in the wood unless they had bUTst at an early stage and grown into short shoots. Thus the sprout forming buds at the bases of the stumps were mainly adventitious. Sometimes they existed in groups, when a large number of buds formed almost simultaneously on the meristematic tissue activated in the cambium. Meristematic knots also developed on the roots, and many adventitious buds could form in these. The traces of the root buds usually reached the primary xylem, and could branch vigorously. The conglomeration of root buds could grow very large, but usually only about 20 - 30% of them actually burst to form suckers. Stools which had been coppiced once before sprouted much better than those coppiced for the first time. The buds localed above ground level, in particular, often developed into sprouts. 'Intact trees sprouted poorly, on account of the small number of buds, as the adventitious meristems were activated markedly only after felling. Repeated coppicing seems to improve the sprouting ability of Alnus incana stumps.
1. Introduction The buds located near or below ground level are extremely important in the vegetative reproduction of trees, but most morphological and anatomical research deals with buds located higher on the trunk, i.e. axillary ones, and buds developing near them (e.g. GARRISON 1949a, b; KORMANIK & BROWN 1969; CREMER 1972; FINK 1983). Basal buds may differ clearly from upper ones in their structure, e.g. in birches (KAUPPI et a!. 1987), but only limited research into the structure and bursting of buds located at the bases of trees of certain species has been conducted previously (e.g. LOHMATOV 1953; BRUNKENER 1984; KAUPPI et a!. 1987, 1988; PAUKKONEN et a1. 1992) and considerable variations between species have been observed. The bursting dynamics of sprout-fonning buds have been shown to be important for gaining the best results in sprouting and short rotation cultivation (KAUPPI et a\. 1991). Research into alder in Finland and Sweden has included an examination of their use in energy forests (GRANHALL 1982; KORPELAINEN 1982), their suitability for soils in which
354
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KAUPPI
other trees will not grow (KORPELAINEN 1982), felling times (HEIKINHEIMO 1930), fertilization (RIKALA & ROSSI 1981) and biomass production (RYTTER 1990, SAARSALMI et al. 1991), but not the morphological basis for vegetative reinvigoration. Not even the sprout-forming buds of the fast-growing American red alder (Alnus rubra) have been investigated in this respect although this species has been examined intensively in the context of short rotation cultivation (e.g. DE BELL et al. 1978; HARRINGTON 1984). In addition to basal buds, Alnus incuna also forms numerous root buds, and thus suckers (e.g. B0RSET 1976; ALI-ALHA 1987). Research into the root buds of trees in general is limited, although the development of the shoot primordia and their anatomy has been monitored to some extent (BROWN 1935, SIEGLER & BOWMAN 1939; SANDBERG & SCHNEIDER 1953; SCHIER 1981). The present paper draws attention to the anatomy and morphology or both stump and root buds of Alnus incanu, their development, bursting and sprouting dynamics.
2. Terminology The basic terminology concerning buds can be seen in KAUPPI ct al. (1987). Bud initials, which possess no leaf primordia, are termed here 'merislematic knots'. When leaf primordia can be observed (microscopically at first), they are called 'bnds'. Buds which have started to grow but possess no foliage leaves arc classified as activated or burst, and when the real foliage leaves with laminae have begun to enlarge and the internodes to lengthen the structure is called a 'sprout' or 'sucker' depending on its origin, the fonner originating from the stump or the base of an earlier sprout and the latter from roots.
3. Material and Methods Different kinds of buds on stumps and roots (for a classification of buds, see KAUPPI et a1. 1987, Table 1), and their bursting were examined in a total of 50 grey alders (Alnus incana (L.) MOENCH) collected from cultivated stands mainly at Kannus- (23" 50' E, 63° 52' N) and some at Haapavesi (25" 38' E, 64° 05' N). The trees were coppiced at the beginning of May leaving stumps 15 em high, and the roots were cut to only 10 em when sampled, whieh must be taken into account when considering the numbers of root buds and suckers originating from them. Stools of five types were used in the experiment on sprouting dynamics, these being sampled three times during the growing season at approximately monthly intervals (Table 1). Three intact plants were also studied. The stumps, sprouts and roots were Tab. 1. :-.lumbers of Alnus incana stools and their collection schedule. Stool type
Collection time 26th May
Intact plants'·) - 20 year old intact plants Coppiced plants 3 year-old stools 7 year-old stools 21 year-old stools, first coppicing I year earlier -- 25 year-old stools, first coppicing 5 years earlier
26th June
4th August
4 4 4 4
3 6
4
4 4
4 4
4
4
a) Coppiced about 3 weeks before first collection, at the beginning of May.
Root and Stump Buds in Alnus incana
355
examined separately. In addition, some one and two years old seedlings were studied to observe the early stage of the axillary (i.e. preventitious) and adventitious buds as named by HARTIG (1878) and described anatomically by FINK (1980a, b). The primary criteria for distinguishing between axillary and adventitious buds were I) the vascular connections from the bud to the primary xylem/pith, and 2) the location of the buds in relation to the normal phyllotaxy (AARON 1946; KORMANIK & BROWN 1969; FINK 1980a, b, 1983). The formation and development of new, first-order sprouts was monitored in three- and seven-year-old seedlings, and new first and second-order sprouts .in 21- and 25-year-old trees. Domlant and burst buds were counted separately both above and below ground level. The stumps were kept in water for six days after sampling so that any buds which had been overlooked would become visible and could be counted. After that the stumps were peeled to reveal any buds existing under the bark. The buds were examined by stereo light microscopy performed on fresh samples, and their surface structures were studied with a JSM 6400 scanning electron microscope. The samples for scanning electron microscopy were fixed in FAA (formalin, ethanol, glacial acetic acid), dehydrated in an alcohol gradient. dried by the critical point method, mounted on SEM adapters with glue, and coated with gold. For identification of bud origin and the early development of root buds, an ontogenetic examination was carried out on light microscopic tissue sections fixed in FAA and mounted in hydroxyethylmethacrylate (Reichert-Jung Historesin). 5-10 Ilill sections were cut with glass knives using a LKB ultramicrotome and stained with 0.05% toluidincblue.
4. Results 4.1. Origin and structure of buds The buds observed at the stem bases of the young grey alder seedlings could be either preventitious or adventitious in their origin (Fig. 1, 2), but it was observed that the new bud primordia which appeared to originate from the vascular trace of an axillary bud were in fact of adventitious origin and had started to grow from the cambium near the trace of the preventitious bud (Fig. 1b, c). The first indication of such a bud was a knot on the bark (Fig. 2d), which grew until the bark finally tore open. No leaf primordia could be detected in the developing bud at this stage, and it also differed from an axillary bud in external appearance. The axillary buds (Fig. 2 b) remained on the bark surface only if they had started to grow, mostly into short shoots (Fig. 2e, f), in which case they grew a scale whorl formed by stipules every year, which then came loose. Later some of these short shoots grew into long shoots (Fig. 2{), which differed from the adventitious sprouts in the fOlm of their base (Fig. 2g), the base of a preventitious shoot being markedly thicker and having more scars than upper part that had grown as a long shoot. Dormant axillary buds (Fig. 2a, c) occurred on thick alder trunks almost exclusively at the bases of the branches. No scars located close to each other could be observed at the bases of adventitious sprouts. The rapidity of development of the adventitious buds, on both stumps and roots, varied markedly depending mainly on decapitation and the environmental conditions in which the tree was growing. Adventitious shoot buds also developed on the roots in this species taking the form of meristematic knots (Fig. 4a) which had a vascular connection extending to the primary xylem and structures typical of buds, e.g. first the apical meristem and later the leaf primordia could be seen buried in the bark (Fig. 3). The root buds could branch from the vascular trace of the original bud (Fig. 3 a, d), and the stem of the root bud could even grow in a curved manner inside the bark (Fig. 3 b, e). When located below ground level, the root buds increased in length (Figs. 4b, e, f) so that a few short internodes were observed in them. Stipules and small axillary buds were observed in the nodes, but no laminae (Fig. 4e). The underground axillary buds (Fig. 4e) differed from the aerial ones (Fig. 2a, c, e) and from all the adventitious buds (Fig. 2b, d). When growing in the light, however, the root buds started to grow vigorously into suckers immediately after maturing and formed foliage leaves at once (Fig. 4c, d).
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The adventitious buds usually formed conglomerations, which were smaller and fewer in number on the stools (Fig. 2g) than on the roots (Fig. 41). Buds were able to form rapidly and in considerable numbers on the stools, while the meristematic knots in which they formed on the roots were usually large and were able to grow into conglomerations consisting of dozens of buds. Many bud primordia developed rapidly in the same meristem, and more buds could form later. Thus some buds had burst while other primordia were still developing (Fig.4c).
Fig.!. (see page 357) Fig. I. Initiation of basal buds of Alnus incana. a) Cross-section of a 3-year-old stem. The trace of the preventitious bud reaches the pith (arrow). Bar = 0.25 mm. b) 'Branching' vascular trace of a basal bud (arrows). Note that the section has not been cut entirely longitudinally. Bar = 0.25 mm. c) Close-up view of Fig. I b). The lateral buds (1) do not branch directly from the trace of the primary bud but initiate from the cambium near the trace. Bar = 0.1 mm.
Fig. 2. (see page 358) Fig. 2. Basal buds of Alnus incana. a) Buds located in the leaf scars in the order of phyllotaxy of the dead prcventitious bud (arrows). These buds are of axillary origin concluding from their location. They are probably the lowest axillary buds of the dead bud. Bar = 5 mm.b) A group of three adventitious buds around the original preventitious bud scar (arrows). They are not located in the axils of leaf scars. Bar = 5 mm. c) SEM micrograph of a preventitious basal bud. Bar = 0.5 mm. d) SEM micrograph of basal buds on a current season sprout. p - preventitious bud with numerous scales and leaf primordia, a - adventitious buds of which the smaller aneis very young. Bar = 0.5 mm. e) A preventitious bud at the base of the stem has started to grow as a short shoot (ss). I) A preventitious bud at the base of the stem has started to grow as a short shoot but is now growing as a long shoot (arrow). g) Sprouts initiating from buds located on the root collar. There are numerous buds in the same group, most of them adventitious but some of axillary origin.
Fig. 3. (see page 359) Fig. 3. Root buds of Alnus incilna. a) A shoot bud primordium on a 3-year-old root. The bud trace reaches the primary xylem. This bud seems to be branching (b). There are also signs of another shoot bud (arrow). Note the large bulge in the cortex. t - tracheids. Bar = 0.25 mm. b) Longitudinal section of a root bud growing inside the bark from the same bud conglomeration as in Fig. 3a. The growing bud tears the cortex first and finally the cork. a - apical meristem, s - stem of the bud. Bar = 0.25 mm. c) Close-up view of the other knot indicated by the arrow in Fig. 3a. The section has been taken at a different level. Bar = 0.25 mm. d) Close-up view of the branching vascular trace indicated by t in Fig. 3a. Note the differentiating transversal tracheids (arrow), Bar = 0.1 mm. e) A root bud primordium (meristematic knot) entombed in the cortex. No leaf primordia can be observed yet. a ~ apical meristem. Bar = 0.25 mm.
Fig. 4. (see page 360) Fig. 4. Root buds of Alnus incana. a) SEM micrograph of a meristematic knot on a root, a shoot bud at an early stage. Bar = 0.05 mm. b) A lengthened root bud (arrow): The tip of the bud was green when sampled. r - root. Bar = 5 mm. c) A burst root bud (grown in light). The two small meristematic knots indicate new activated sites of emerging buds (arrows). Bar = 10 mm. d) SEM close-up of the bud group in Fig. 4c from another angle. Bar = 1 mm. e) A growing root bud. Nodes and axillary buds can be seen. The internodes in the upper part of the bud are very short. The Ieaj~like organs are stipules. s - scars ofstipules of the axillary bud (b), which is broad and short. Bar = I mm. I) A large bud conglomeration on the underside of a root. s - suckers, a - activated buds, d - dormant buds.
Root and Stump Buds in Alnus incana
357
358
K. PAUKKONEN
and A.
KAUPPI
Root and Stump Buds in Alnus incana
359
360
K. PAUKKONEN
and A.
KAUPPI
361
Root and Stump Buds in Alnus incana
Tab. 2. Numbers of buds and sprouts on stools of Alnus incanu. First sampling 3 weeks after coppicing. Total number of buds
Above ground level on stump on sprouts Below ground level on stumps on sprouts on roots
* significant at 5%
a)
Type of bud
26th May
26th June
4th August
x
S.D.
it
x
Dormant Activated Dormant Activated Dormant Activated Dormant Activated Dormant Activated Dormant Activated Dormant Activated
4.4 0.8 0 0 4.4 0.8 17.1 2.6 4.5 0 1.0 0 11.6 2.6
5.1 1.5 0 0 1.8 0.5 19.1 4.3 3.5 0
2.5 0 16.3 4.3
S.D.
1.7 4.2
3.6 1.4 1.6 3.9 9.0 17.0 2.2
0.6 1.6 3.2 14.9 10.4
1.0 2.9 7.7 3.3 l.l 2.7 6.1 21.4 3.1 1.5 1.7 4.2 14.1 17.4
1.3
13.6 0.8 8.2 0.9 9.9 19.0 6.9 2.7 2.9 1.0 1.3
11.1 2.6
F
S.D. 1.5 7.7 1.3
15.86***
9.3
6.21**
1.4 7.6 16.0 5.3 5.0 4.2 2.8 2.6 9.9 3.2
7.88**
3.60*
level; ** significant at 1% level; *** significant at 0.1 % level
4.2. Number and location of buds The number of buds differed markedly between the types of alder stool. In general, there were a large number of buds - mostly adventitious - on the stools, an average of 25.8 per stool, with a geometrical mean of 21. The 20-year-old intact trees ha
.. ,',",
Above ground level
'.:
Below ground level StumR§ Above ground level Below ground level
IIII!I tilll
Sprouts or suckers
E;;:3
Dormant buds
Activated buds
":,',
Roots Below ground level
,,::.. :.
o
50
100 150 200 250 300 350 400 450
Total number of buds, sprouts and suckers Fig. 5. Total numbers of dormant and activated buds, sprouts and suckers on different parts of the stool above and below ground level at the three sampling times (26th May, 26th .June, 4th August). 24
Flora, Bd. 187. 5/6
362
K. PAUKKONEN
and A.
KAUPPI
The numbers of both dormant (mainly adventitious) and activated buds (Fig. 6) increased during the growing season as a consequence of felling in all the trees coppiced once and in the older ones of those coppiced twice, as the bud conglomerations and the numbers of buds in them grew. The intact trees had no bud conglomerations, not even on the roots. Large numbers of buds formed on the stools within three weeks of coppicing, but the number of buds on the sprouts and stools of the samples already coppiced once or twice did not reach its maximum until 14 weeks after coppicing. The number of root buds was largest three weeks after coppicing, then remaining almost the same throughout the growing period. The adventitious buds on the stools were abundant on scars and at the bend in the root collar (Fig. 2g), while the buds on the roots often occurred on bends or at branching sites (Fig. 4b, c). Adventitious buds also commonly developed around the preventitious buds (Fig. 1b, c, 2d) and scars (Fig.2b).
a
c
b
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140
140
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120
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80
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26th 4th June August
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20 0 26th May
26th 4th June August
-tr Dormant buds
100
.. n
80 60
..
40 20
Activated buds Sprouts and suckers
0
26th May
26th 4th June August
Fig. 6. Numbers of dormant and activated buds, sprouts and suckers in a) intact trees, b) 3-year-old trees coppiced once, c) 7-year-old trees coppiced once, d) 21·year-old trees coppiced for the fist time at 20 years of age, and e) 25-year-old trees coppiced for the first time at 20 years of age. Coppiced by the beginning of May at the latest.
363
Root and Stump Buds in Alnus incana
4.3. Sprouting potential of stumps
The buds burst rapidly after coppicing (Table 3a), the activated ones being located mostly at the base of a stump or sprout, but rarely further up (Fig. 2g), and in the large conglomerations on the roots, where only some of them burst (Fig. 41). The root buds which remained dormant over the season in which they developed seldom burst later. The root buds burst more quickly than the stump buds. When many of the root buds on the trees already coppiced twice had burst within three weeks of coppicing, almost all the buds on those coppiced once were still dormant. Buds were activated gradually over the whole growing period in the other parts of the plant, i.e. on the sprouts and stumps, but they seldom grew into sprouts (Fig. 6). A clear difference in sprouting existed between the types of alder stool, with 29 out of the 53 stools sprouting (55%), to gain an average of four sprouts per stool. The stools that did not sprout did not die during the experiment, however. In spite of the high number of buds, only four of the stools coppiced once sprouted, mostly fonning two sprouts, giving an average of only 0.2 sprouts and a sprouting intensity of less than 1 (Table 3b). Sprouting intensity (KAUPPI et al. 1988) is defined as follows:
Tab. 3. Sprouting of Alnus incana. a) Rapidity of sprouting after coppicing. b) Sprouting intensity of seed- and sprout-origin stools in relation to age and part of stool. a) . Sampling date
26th May, control 26th May, 3 weeks after coppicing 23th June, 8 weeks after coppicing 4th August, 14 weeks after coppicing
No. of stools
3 18 16 16
No. of sprouts ') per stool it
min.
max.
0.3 6.3 1.4 3.9
0 0 0 0
1 12 7 12
b) Types and parts of stools from which sprouts and suckers grow
Stools coppiced once 3 year old - 7 year old - stumps - roots . Stools coppiced twice (first coppicing at 20 years of age first coppicing I year earlier first coppicing 5 years earlier sprouts stumps roots 20 year old intact plants Total
No. of stools
Total no. Total no. of buds of sprouts·)
Sprouting intcnsity')
0.8 2.2
26 14 12 25 26 24
608 219 389 294 314 755
5 5 0 3 2 198
0.2 0.4 0 0.1 0.1 8.3
1.0 0.6 20.8
12 12 198 24 24h) 3 53
496 259 269 159 327 4 1367
138 60 131 56 11
11.5 21.6 0.7 2.3 0.5 0.3 3.8
21.8 18.8 32.8 26.1 3.3 20.0 13.0
a) Including suckers; b) Number of stools; C) Defined in the text 24°
Total no. of sprouts') per stool
I
204
364
K. PAUKKONEN and A. KAUPPI
where SI is sprouting intensity, Ns is the number of single buds forming sprouts, N g is the number of grouped buds forming sprouts and Nd is the number of dormant buds. On the other hand, all the stools coppiced twice sprouted, the minimum number of sprouts on them being two, the maximum 21 and the average 8.3. The trees coppiced for the first time a year earlier sprouted very well after the second coppicing, as almost 2/3 of all the sprouts were located on them. These sprouts were mainly of second order, but there were quite a number of new, first-order sprouts on the root collars well. The sprouting intensity was highest in these parts (Table 3 b), and the average sprouting intensity reached 20 for whole stools that had been coppiced twice. Only one of the 20-year-old intact trees sprouted, growing one sprout, the high sprouting intensity of these being due to the very small number of buds. There were only a few suckers, despite the large number of buds, both dormant and activated, on the roots of all the stools examined (Fig. 6). The highest number of sprouts was observed three weeks after coppicing on every type of stool, and observations made later showed the number to have diminished by about 50% due to high mortality among the sprouts of adventitious origin, which were only weakly attached to the wood and thus easily came loose.
5. Discussion Trees in<:rease their diameter even during the dormant period, so that if the basal buds do not lengthen they will become buried in the bark and finally in the wood. In some species, e.g. birches (KAUPPI et al. 1987), the basal buds grow and stay on the bark, but in grey alder studied here they grew extremely poorly and were buried in the bark, as were the buds of Salix alba (FINK 1983). The preventitious buds of the grey alder remained on the bark only if they burst and started to grow soon after maturing. The stipule whorls of the short shoots came loose in the alder, but remained attached in birch (KAUPPI et al. 1987). In Acer saccharum (CHURCH & GODMAN 1966) and Liquidambar styraciflua (KORMANIK & BROWN 1969) semidormant buds may grow as short shoots, too. It has been noted that felling induces these buds of Liquidumbar styraciflua to grow into long shoots (KORMAN!K & BROWN 1969), as was also noted in Alnus incana. The grey alder formed sprouts from both preventitious axillary buds and adventitious buds, but those of the former type were scarce because the axillary buds in this species was not observed to branch in the same manner as in Betula pubescens (KAUPPI et £11. 1987), willows (BRUNKENER 1984; PAUKKONEN et a1. 1992), Acer saccharum (CHURCH & GODMAN 1966) or Liquidambar styraciflua (KORMANIK & BROWN 1969). The clustering of alder buds is not caused by branching of the primary buds but by the formation of many adventitious buds almost simultaneously. The largest tufts of sprouts on the stools grew on the root collar, as in Quercus chrysolepi.l' (PAYSEN et a!. 1991). The tissue on the border of a thickening root and stem can become irritated and it may be that the pressure induces large bud conglomerations. On the other hand, ~ome field observations (FERM, unpub!. data) suggest that many sprouts may grow near the cutting surface on an alder stump, as in the case of Ailanthus glandulosa (BORY et a!. 1991). On the other hand, suckers appear only after two or three cuts in Ailanthus glandulosa, while in the grey alder they may exist even in intact trees, though they are more numerous after cutting. According to field observations (FERM, unpub!. data), the majority of suckers of the grey alder grow some distance from the stump, and thus the number of suckers would be higher if longer sections of the roots were examined. Many shoot buds were observed on the roots of grey alder, often at bends. The bud conglomerations also started to develop early and enlarged as they aged. All the root buds examined had a trace to the primary xylem of the root, as is the case in the apple, too (SIEGLER & BOWMAN 1939). This is due to the fact that shoot buds start to develop on
Root and Stump Buds in Alnus incana
365
very young roots, probably beginning their growth from the pericycle, as in the aspen (SANDIlERG & SCHNEIDER 1953) and in Araucaria cunninghamii (BURROWS 1990). Buds initiating directly from the phellogen, as in poplars (BROWN 1935), were not observed in the alder, although it remained unsolved whether existing changes in the phellogen and cortex tissue, e.g. increased cell activity, would lead to bud initiation. The lengthening root buds formed nodes, and the leaves of these nodes were retarded. Thus, the initiation of the lowest axillary buds of a sucker corresponds to that of the basal buds of birches (KAUPPI et al. 1987). The grey alder sucker can branch from these buds, but very seldom does so spontaneously. Generally only a few buds in a conglomeration burst and the majority remain as dormant reserve buds which will either burst under favourable conditions or not at all. Thus, the adventitious meristems located on the roots, stools and bases of sprouts may remain dormant for years before they reach the real bud stage in their development, but once activated, e.g. as a consequence of coppicing, and having started to develop into buds, they will usually burst even though they do not always continue to grow into sprouts. The intact 20-year-old trees examined here had very few buds, but the number increased as a consequence of repeated coppicing as has been noted earlier in the birch (KAUPPI et al. 1988). It is possible that sprout-forming buds do not develop until the physiological state of the tree changes as a consequence of decapitation, and that meristem activation already occurs after the first coppicing even though the buds do not develop and burst on a large scale until after the second coppicing. The shoot primordia on the roots of the apple (SIEGLER & BOWMAN 1939) and poplar (BROWN 1935) can stay in a semi dormant stage during plant dormancy. The grey alder seems to be able to control the number of sprouts on each stool, as there were not more than ten sprouts during the first growing season even though there were many more activated buds. SAARSALMI et al. (1991) observed 5~8 sprouts per Alnus incana stool after the sixth growing season, and the present grey alder stools which had been coppiced twice carried very many more sprouts than those coppiced once. As in Quercus alba (MCGEE 1978) and Alnus rubra (HARRINGTON 1984), the sprouting results· achieved by the grey alder dependend on the age of the tree, especially in those coppiced twice, the younger ones sprouting better. Biomass production capacity has also been noted to be better after the second coppicing than after the first in young Populus plants (STRONG 1989). The results of this experiment are also similar to those for Alnus rubra, 4-year-old seedlings of which sprout poorly after the first coppicing (HEILMAN & STETTLER 1985). Apical dominance, which controls the bursting and growth of both sprouts and suckers (STENEKER 1974), is probably not as strong in sprout-origin stems as in the original seed-origin main stem, and partly for this reason the formation of new shoots could be stronger in trees of the former kind. The sprouts of the grey alder usually formed right at the base of existing ones, as in the red alder (HARRINGTON 1984), i.e. on the part of the stem where most of the buds on the stumps of Alnus incana were located. The fact that the buds located above ground level generally sprouted better than those located under the ground is due to the more favourable light conditions (e.g. KHAYAT & ZIESLIN 1982; JUNTTILA & JENSEN 1988). The birch similarly sprouts best from its aerial buds (KAUPPI et al. 1991), although this is partly due to the poor sprouting ability of underground buds, which very often exist in large clusters (KAUPPI et al. 1988). In the alder, too, the underground buds are usually found in large conglomerations, and the resulting competition between individual buds and the weak vascular connections mean that some of them die easily, which is also true of the above-ground sprouts, especially if they exist in large tufts. SAARSALMI et al. (1991) likewise observed that many alder sprouts die. Thus adventitious buds seem ~o be highly disposed to deterioration and die easily, as also seen by KORMANIK & BROWN (1967) and DEBELL & ALFORD (1972). Alnus incana may be a good alternative when reforestating, especially in wet (DESMET & MATON 1989) and poor soils (KORPELAINEN 1982) because of its remarkable biomass produc-
366
K.PAUKKONEN and A. KAUPPI
tion ability (BJORKLUND & FERM 1982, RYTTER 1990, SAARSALMI et al. 1991). According to this study, it has a high budding capacity, ability to produce suckers, and ability to withstand repeated coppicings so that coppicing can even enhance sprouting and thus also productivity.
Acknowledgements The authors wish to thank the Kannus Research Station of the Finnish Forest Research Institute for providing the stump material PAIVI RINNE for some of the scanning electron micrographs and for technical assistance, ANTTT SAARENPAA, MARITTA KIVINIITTY and CHRISTINA TIGERSTEDT for their tcchnical assistance, and Mr. MALCOLM HICKS for revising the language of this paper.
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HARRINGTON, C. A. (1984): Factors influencing initial sprouting of red alder. Can. J. For. Res. 14: 357 - 361. HARTIG, TH. (1978): Anatomie und Physiologie der Holzpflanzen. Berlin. HEIKINHEIMO, O. (1930): Kaatoajan vaikutus lehtipuiden vesojen syntyyn ja kasvuun. (Effect of felling time on development and growth of sprouts of deciduous trees). Tapio, Helsinki. pp. 113 -117. (In Finnish). HElLMAN, P., & STETTLER, R. F. (1985): Mixed short rotation culture of red alder and black cottonwood: Growth, coppicing, nitrogen fixation and allelopathy: For. Sci. 31: 607-616. JUNTTILA, 0., & JENSEN, E. (1988): Gibberellins and photoperiodic control of shoot elongation in Salix. Physiol. Plant. 74: 371-376. KAUPPI, A., PAUKKONEN, K., & RINNE, P. (1991): Sprouting ability of aerial and underground dormant basal buds of Betula pendula. Can. 1. For. Res. 21: 528-533. -, RINNE, P., & FERM, A. (1987): Initiation, structure and sprouting of dormant basal buds in Betula pubescens. Flora 179: 55 -83. - (1988): Sprouting ability and significance for coppicing of dormant buds on Betula pubescens EHRH. stumps. Scand. J. For. Res. 3: 343-354. KHAYAT, E., & ZIESLIN, N. (1982): Environmental factors involved in the regulation of sprouting of basal buds in rose plants. J. Exp. Bot. 33: 1286-1292. KORMANIK, P. P., & BROWN. C. L. (1967): Adventitious buds on mature trees. USDA For. Serv., Southeastern For. Exp. Stat., Res. Note SE-82. - (1969): Origin and development ofcpicormic branches in sweetgum. USDA For. Servo Res. Paper SE-54. KORPELATNEN, H. (1982): Experiments with Alnus hybrides in Finland. In The Second National Symposium on Biological Nitrogen Fixation, Helsinki 8th-10th of June 1982. The Finnish Fund for Research and Development. Nitrogen Project. Report 1: pp. 287 - 291. LOHMATOV, N. A. (1953) Pricini rannei poteri berezoi borodavcatoj poroslevoj sposobnosti. Lesnoe Hozjaistvo 2: 42-44. MCGEE, C. E. (197&): Size and age of tree affect white oak stump sprouting. South. For. Exp. Stat. Res. Note SO-239. PAUKKONEN, K., KAUPPI, A., & FERM, A. (1992): Origin, structure and shoot-formation ability of buds in cutting-origin stools of Salix 'Aquatica'. Flora 186: 53-65. PAYSEN, T. E., NAROG, M. G., TISSELL, R. G., & LARDNER, M. A. (1991): Trunk and root sprouting on residual trees after thinning a Quercus chrysolepis stand. For. Sci. 37: 17 - 27. RIKALA, R., & Ross], P. (1981): Sprouting of Alnus incana. Abstract in PERA-symposium, March 3-4, 1981, Helsinki. Abstract available from the Faculty of Forestry, University of Helsinki, Helsinki, Finland. RYTTER, L. (1990): Biomass and nitrogen dynamics of intensively grown grey alder plantations on peatland. Ph. Dr. thesis, Dcp. Eco!. Envir. Res., Agric. Univ. of Sweden. Report 37. SAARSALMI, A., PALMGREN, K.,& LEVULA, T. (1991): Harmaalepan vesojen biomassan tuotos ja ravinteiden kayttii. Summary: Biomass production and nutrient consumption of the sprouts of Alnus incana. Folia Forestalia 768. SANDBERG, D., & SCHNEIDER, A. E. (1953): The regeneration of aspen by suckering. Minnesota Forestry Notes No. 24, University of Minnesota. SUITER, G. A. (1981): Physiological research on adventitious shoot development in aspen roots. USDA, For. Serv .. Int. For. Range Exp. Stat., Gen Tech. Rep. INT-107. SIEGLER, E. A., & BOWMAN, J. J. (1939): Anatomical studies of root and shoot primordia in I-year apple roots. 1. Agr. Res. (Wash. D.C.) 58: 795-803. . STENEKER, G. A. (1974): Factors affecting the suckering of trembling aspen. For. Chron. 1974: 32-34. STRONG, T. (1989): Rotation length and repeated harvesting influence Populus coppice production. USDA For. Serv., North Central For. Exp. Stat., Res. Note NC-350. Received August 4, 1992 KATRI PAUKKONEN and ANN ELl KAUPPI,* Department of Botany, University of Oulu, SF-90570 Oulu, Finland, and ARI FERM, Finnish Forest Research Institute, Kannus Research Station, SF-69 100 Kannus, Finland.
* corresponding author