Qualitative Structural Changes During Bark Development in Quercus Robur, Ulmus Glabra, Populus Tremula and Betula Pendula*

IAWA Bulletin n.s., Vol. 12 (1),1991: 5-22

QUALITATIVE STRUCTURAL CHANGES DURING BARK DEVELOPMENT IN QUERCUS ROBUR, ULMUS GLABRA, POPULUS TREMULA AND BETULA PENDULA*

M. Trockenbrodt Ordinariat für Holzbiologie der Universität Hamburg und Institut für Holzbiologie und Holzschutz der Bundesforschungsanstalt für Forst- und Holzwirtschaft, Leuschnerstr. 91, 2050 Hamburg 80, Germany

Summary Introduction The deve10pment of bark structure of In spite of its wealth of features and pecu- Quercus robur L., Ulmus glabra Huds., Po- liarities bark anatomy is seldom used for pulus tremula L. and Betula pendula Roth is plant taxonomical considerations (e.g. Zahur being described. Profound structural changes 1959; Richter 1981; van Wyk 1985; Trocken- can be observed during the first years after brodt & Parameswaran 1986). Obtaining bark secondary growth has started. In all four spe- samples authenticated by herbarium vouchers cies the epidermis is replaced by a periderm, is laborious if not impossible because barks the cortex shows intensive dilatation growth, rarely are a part of botanical collections. and the groups of primary bark fibres are Moreover, bark tissue often is an extremely pushed apart. The collapse of sieve tube heterogeneous material, and commonly ap- members starts with the second year. With plied techniques far sampie preparation are proceeding secondary growth, the specific inadequate. However, the main reason far formation of sc1erenchymatic tissue, especi- today's limited use of bark anatomy far ally sc1ereids, and the dilatation growth are taxonomical wark is a lack of knowledge processes which strongly affect the bark about the structure of bark and its develop- structure of Quercus robur, Populus tremula ment. Contrary to wood, bark structure and Betula pendula. In addition, wide, fused changes continuously with age. Information phloem rays develop in Quercus robur. The about the variability of bark structure, especi- structure of Ulmus glabra bark is affected by ally within one individual during its growth, the formation of phloem fibre-/sc1ereid-like is essential for an estimation of the diagnostic cells and mucilage cells and by dilatation value of bark anatomical features. Up to now growth. The histological pattern of Ulmus only a few investigations have dealt with the glabra bark stabilises to a great extent after developmental anatomy of bark. Some of the first few years, the other barks investi- these are on pharmacognostic aspects of cer- gated show further developmental processes tain barks (Speyer 1907; B irn stiel 1922; Has- over many years. In all species the formation ler 1936), and some information can be found of a rhytidome is the last distinct modification in more generalliterature on the anatomy of of bark structure. bark (e. g. Hanstein 1853; Möller 1882; Thore- naar 1926; Chang 1954; Reinders & Reinders- Key words: Quercus robur L., Ulmus glabra Gouwentak 1961; Esau 1969). The varia- Huds., Populus tremula L., Betula pen- bility of certain bark features within one in- dula Roth, bark anatomy, bark develop- dividual tree was analysed by Raskatov and ment. Kosichenko (1968), Kosichenko (1969),

* Dedicated to Prof. Dr. Walter Liese on the occasion of his 65th birthday.

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Nicholls & Phillips (1970), Liese and Para- Table 1. Age and height of the investigated meswaran (1972), Parameswaran and Liese trees. (1974), Ghouse and Siddiqui (l976a, b), Age Height Ghouse and Yunus (1976), Ghouse and (years) (rn) Hashmi (1977), Ghouse and Iqbal (1977, Oak 37 14.5 1981), Yunus etal. (1977), Aday (1978), Ezell Oak 11 30 11.8 and Stewart (1978), Ghouse et al. (1982), III 14 Iqbal and Ghouse (1983) and Röckle (1986). Oak 6.8 Most of these papers are restricted to short Oak IV 14 4.8 descriptions of cell1ength variabi1ity. Oak V 15 2.1 The intention of this paper is to contribute Elm 24 16.0 to the broadening of our knowledge about Pop1ar 12 14.5 structural changes of bark tissue during its Birch 10 5.0 development. First, qualitative changes of the Birch 11 16 10.0 basic bark structure are described. Quantita- tive changes and the diagnostic value of sin- gle bark anatomical features will be discussed in subsequent papers. lar stern diameter intervals, and according to the intactness of the tissue. Quercus robur Material and Methods bark was sampled at 5-9 height levels which Tree species suitable for the investigation correspond to a bark age of 1-33 years, bark had to fulfill certain requirements: thickness of 0.2-9.5 mm and stern diameter of0.4-16.5 cm. Ulmus glabra bark sampies sufficient preservation of bark with age, were taken from 12 height levels representing i.e. no early formation of rhytidome com- bark age of 1-24 years, bark thickness of bined with the loss of bark tissue; 0.7-10.7 mm and stern diameter of0.4-25.0 typical representatives of different struc- cm. Populus tremula bark sampIes derived tural wood and bark types; from 9 height levels which correspond to a sufficiently complex structure, i.e. a high bark age of 1-11 years, bark thickness of number of possibly varying features. 0.6-4.7 mm and stern diameter of 1.0-14.0 Accordingly, the ring-porous hardwood cm. Betula pendula bark was sampled at 12- species Quercus robur L. and Ulmus glabra 13 height levels with a corresponding age of Huds. as weil as the diffuse-porous hard- 1-16 years, bark thickness of 0.4-12.0 mm wood species Populus tremula L. and Betula and stern diameter of 0.3-24.0 cm. Sections pendula Roth were chosen. Initially, five in- from all levels were prepared and analysed dividuals of Quercus robur were analysed. with a light microscope and a serni-automatic The investigation revealed no tree-to-tree dif- image analyser. ferences in their basic bark structure and de- The sampies included bark, cambial zone, velopment. One individual of Ulmus glabra and mostly a narrow zone of adhering xylem. and Populus tremula and two of Betula pen- They were fixed in formalin-acetic acid- du la were examined. For details about the aicohol, penetrated with polyethylene glycol age and height of the selected trees see Table 1. 1500, and sectioned on a sliding microtome, A sampie selection following biological often with the help of adhesive tape. The sec- and mathematical rules (cf. Kucera & Bariska tions were double-stained with astra blue and 1982) is not practicable for working on bark, acridine red-crysoidin. Additional sampies because all structural information is stored in were embedded in glycol-methacrylate (cf. a very small area, and tertiary tissue changes Ruetze & Schmitt 1986). Macerations were impede the removal of exactly defined sam- prepared with Jeffrey's solution (cf. Gerlach pies. Thus, the sampIes were taken at regular 1969). distances along the stern, regular age intervals The terminology follows Trockenbrodt (determined from xylem growth rings), regu- (1990).

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Results With secündary grüwth proceeding (Fig. 3) additiünal tangential bands üf secündary Quercus robur L. phlüem fibre grüups üf up to. 8 cells in depth All five üak trees analysed reveal a similar have develüped. They also. are acco.mpanied develüpment üf bark structure. Differences by chambered crystalliferüus cells. Uniseriate are müre üf a quantitative nature than devi- phloem rays traverse the fibre grüups. The atiüns from a basic pattern. Therefüre the first broad phlüem rays develüp when the bark develüpment üf üaks I-V is described cambial initials between 3-5 uniseriate rays tügether. are eliminated. This fusio.n is stro.ngest where The yüungest sampIes represent the shüüt the cambium bends distinctly. Süme fibre shürtly after secündary growth has started groups with a radial width üf 15-20 cells (Fig. 1). The cüurse üf the vascular cambium can be füund elüse tü the broad rays. The is still irregular. Groups üf primary bark rays are subject tü slight dilatatiün, i.e. the fibres are arranged parallel tü the vascular cells enlarge slightly and round o.ff, but they cambium. The individual grüups are linked dü nüt divide. by slightly enlarged selereids. Inside the pri- The cürtex selereids o.f ülder bark develüp mary bark fibre groups, primary phlüem sülitarily or in spherical grüups (Fig. 4). The elements are lücated füllüwed by the first sclereid grüups between the groups üf pri- secündary phlüem elements. The phlüem mary bark fibres enlarge. The fürmatiün üf rays are exelusively uniseriate. The cürtex selereids in the secündary phloem increases, üutside the band üf primary bark fibres cün- especially between adjacent phlüem fibre sists üf an inner zone üf iSüdiametric cürtex groups. The transfürmatiün üf phloem paren- parenchyma cells, slightly enlarged due tü chyma cells intü sclereids is üften initiated by dilatatiün growth, and a narrüw üuter zone üf üne cell, and it proceeds ce'ntrifugally (Figs. sm all cürtex cüllenchyma cells. The üuter- 5 & 6). In transverse sectiüns the sclereid müst layer üf the shüüt is the intact epider- groups üften appear spherical ür stretched mis. Immediately beneath the epidermis the tangentially (Fig. 6), in radial sectiüns also. fürmatiün üf the periderm has started. spherical but stretched axially. Sülitary scle- Caused by the progressing secündary reids are cümmün, too. The sclereids' fürms growth, bark structure already changes with- and dimensio.ns vary a lüt. As a rule, scle- in the first year (Fig. 2). The epidermis is reids in the secündary phloem are larger than ruptured, and remnants adhere tü the inten- the ünes in the cürtex and in the band üf pri- sively developing periderm. The cortex col- mary bark fibres and sclereids. lenchyma primarily expands through antieli- After several years, bark shüws grüwth nal cell divisiün. The parenchyma cells üf the ring patterns (Fig. 6). At the beginning üf the cürtex undergo. intensive dilatatiün growth. growth periüd ünly nün-lignified cells, pre- They are partly enlarged and stretched tan- düminantly sieve tube members are fürmed, gentially ür divided anticlinally. The grüups füllüwed by tangential secündary phlüem üf primary bark fibres are pushed apart and fibre bands (groups) üf different tangential müst üf the gaps are filled with develüping length (O.l-several mm). Subsequently a selereids. These are enlarged ünly slightly. zone üf nün-lignified cells is fürmed, süme- Their shape varies. They üften stretch tan- times füllüwed by a secünd band üf secünd- gentiaIly, rarely radially, or they are iSüdia- ary phlüem fibres. At the end üf the growth metric. The primary phlüem is cüllapsed ür it period a narro.w layer (1-3 cells) üfaxial dilates. First grüups üf secündary phlüem phlüem parenchyma cells is fo.rmed. Hüw- fibres shüw thick-walled, lignified, cham- ever, this sequence is nüt übligato.ry, it might bered, crystal cüntaining cells üf apprüxi- be incümplete. It also. can be disturbed by a mately equallength at their inner and üuter cüllapse üf sieve tube members, sclerifica- sides. In the secündary phlüem a few iSüdia- tiün, and beginning dilatatiün growth. The metric selereids are fürmed. The cüurse üf zigzag cüurse o.f the vascular cambium is the vascular cambium is still irregular. restricted tü the area üf fused rays. The fu-

Downloaded from Brill.com10/01/2021 12:51:00PM via free access via free access (1),1991 (1),1991 12 Vol. n.s., Downloaded from Brill.com10/01/2021 12:51:00PM Bulletin Bulletin --- IAWA IAWA ------8 00 ~---- Trockenbrodt - Structural changes during bark development 9 sion of phloem rays proceeds (15-25 cells), bium. Outwards up to three tangentiallayers they often protrude into the xylem (Fig. 7). ofaxial phloem parenchyma strands are Within the outer secondary phloem the uni- formed, each of them 1-3 cells wide. The seriate phloem rays become indistinguishable cells contain organic material. The layers from the surrounding tissue due to the dila- alternate with two layers of sieve tube mem- tation of both the rays and the surrounding bers, companion cells and crystal containing tissue. phloem parenchyma cells. A distinct pattern With increasing secondary growth the dis- in the radial sequence of these layers has not tance between groups of primary bark fibres developed yet. The layers of predominantly strongly increases and often they are difficult sieve tube members are up to 8 cells deep; to localise. The band of primary bark fibres 1-3 seriate phloem rays run through the and sclereids now mainly comprises sclereid secondary phloem. Outside the outermost groups of irregular width, and it is often tangential phloem parenchyma layer, ele- interrupted by gaps. Dilatation growth and ments of the primary phloem can be found sclerification increase resulting in an irregu- (Fig. 10), some are partly ortotally collapsed. lar, less organised outer secondary phloem Groups of primary bark fibres are located and cortex. The groups of sclereids partly outside the primary phloem. These groups fuse longitudinally. are separated but appear as a continuous tan- During the formation of a rhytidome parts gential band. The cortex consists of a zone of of the first formed periderm, cortex, and round, slightly enlarged cortex parenchyma phloem are isolated from the tissue by se- cells with many intercellular spaces and scat- quent periderms (Fig. 8). If these parts ad- tered secretory cells (mucilage cells) and a here to the last formed periderm, even pri- narrow zone of cortex collenchyma cells. Im- mary elements of the bark may remain in the mediately beneath the epidermis the periderm outer rhytidome (Fig. 8). More often, the is formed. isolated parts are shed, leaving a bark which With proceeding secondary growth a Stra- exclusively consists of living secondary tification of the secondary phloem becomes phloem and the last formed periderm. There- more evident (Fig. 11). The epidermis is rup- fore it contains a few sclereids, and it appears tured within the first year, the periderm be- weil organised because the tissue modified comes a noticeable part of the bark. The cor- by sclerification and dilatation growth is part- tex collenchyma cells expand vigorously and ly shed. divide anticlinally. The cortex parenchyma cells enlarge, stretch tangentially and divide Ulmus glabra Huds. anticlinally; intercellular spaces develop. Due to dilatation growth, the groups of primary The youngest sampie (Fig. 9) shows an bark fibres are pushed apart. The primary almost circular course of the vascular cam- phloem elements and the outermost sieve

Figs. 1-6. Quercus robur L. Transverse section. - I: Bark in the first year of development shortly after secondary growth had started (black asterisks = primary bark fibre groups, white asterisks = cortex collenchyma, black arrow = epidermis, white arrows = sclereids, white arrowheads = periderm, cp = cortex parenchyma). - 2: Bark in the first year of development after proceeding sewndary growth (black asterisks = secondary phloem fibre groups, white asterisks = primary bark fibre groups, white arrows = sclereids). - 3: Few years old bark (black arrows = secondary phloem fibre groups, white arrow = wider secondary phloem fibre group in the prox- imity of fused uniseriate phloem rays). - 4: Several years old bark (asterisks = sclereids in the cortex, arrows = sclereids between primary bark fibre groups). - 5: Centrifugally oriented differentiation of a sclereid group. - 6: Bark with distinct growth rings (arrowheads) and sc1ereid groups in the secondary phloem (partly in the stage of differentiation).

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Figs. 7 & 8. Quercus rabur L. Transverse section. -7: Mu1tiseriate phloem ray protruding into the xylem. - 8: Old bark with distinct rhytidome (black arrows = sequent periderms, white arrows = remnants of the ring formed by primary bark fibres and sclereids).

tube members of the secondary phloem are sieve tube members. They do not contaiQ any collapsed. An entirely different type of cells of the cells mentioned before. Secretory cells is formed resembling phloem fibres in shape are only located in the cortex. Due to the (Figs. 12 & 13) and sclereids because they straight course of the phloem rays and the develop from axial phloem parenchyma stratification of the secondary phloem, the strands (Figs. 13 & 14). A classification as bark presents a regular geometrical pattern either sclereids or phloem fibres appears (Fig. 11). to be impossible (cf. Trockenbrodt 1990). Each following year 3 or 4 tissue zones Close to the vascular cambium, the two new- are formed consisting mainly of sieve tube ly formed tissue zones consist mainly of members. They are separated by tangential

~ Figs. 9-14. Ulmus glabra Huds. Transverse section. - 9: Bark in the first year of development shortly after secondary growth had started (black arrows = epidermis, white arrows = periderm, white asterisks = secretory cells (mucilage cells) of the cortex, ce = cortex collenchyma, cp = cortex parenchyma, sp = secondary phloem). - 10: Bark in the first year of development shortly after secondary growth had started (bf = primary bark fibres, arrows = elements of the primary phloem). - 11: Bark in the first year of development after proceeding secondary growth (white arrows = periderm, black arrows = primary bark fibre groups, black arrowheads = axial phloem

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parenchyma cells with phenolic content, black asterisk = secretory cell (mucilage cell) in the cortex, ce = cortex collenchyma, cp = cortex parenchyma). - 12: Bark in the first year of development after proceeding secondary gtowth (arrowheads = sclerenchyma cells resembling phloem fibres). - 13: Development of phloem fibre-/sclereid-like cells from axial phloem parenchyma strands (arrow = former connection to a neighbouring cell). -14: Development ofphloem fibre- /sc1ereid-like cells from axial phloem parenchyma strands (arrow = slightly elongated cells with blunt ends).

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Figs. 15-20. Ulmus glabra Huds. Transverse seetion. - 15: Last formed growth ring of the bark (early phloem sieve tubes with larger diameter than late phloem sieve tubes, sclerenchymatic cells absent in this growth ring). - 16: Tangential agglomerates of the phloem fibre-/sclereid-like cells. -17: Phloem fibre-/sclereid-like cells (arrows) in the last formed growth ring. -18: Secre- tory (mucilage) cells (arrows) in early phloem. -19: Dilatation restricted to wedge-shaped areas beneath the periderm (outlines of dilated area redrawn). - 20: Bark after the formation of a rhytidome. Secondary phloem up to the last formed sequent periderm (arrows) appears homogeneous.

Downloaded from Brill.com10/01/2021 12:51:00PM via free access Trockenbrodt - Structural changes during bark development 13 layers (2-4 cells wide) ofaxial phloem pa- bium is circular. The secondary phloem con- renchyma strands. The width of the zones as sists of sieve tube members, companion well as cell dimensions decrease from early cells, axial phloem parenchyma cells and uni- to late phloem (Fig. 15). The tissue is char- seriate phloem rays. Outside the secondary acterised by a collapse of sieve tube mem- phloem primary phloem elements and primary bers, the formation of phloem fibre-/sclereid- bark fibres are located. The areas of primary like cells, the formation of secretory cells, phloem are strongly pushed apart by dilata- and dilatation growth. Most of the sieve tube tion growth. In the secondary phloem only members collapse during the second year. phloem rays dilate. In the cortex all cells are Those of the late phloem collapse completely, affected, they are conspicuously enlarged and whereas some of the early phloem remain rounded off. Tangential rows of closely re- intact for some years. When the sieve tube lated cells reveal that anticlinal divisions of members collapse, phloem fibre-/sclereid- cortex parenchyma cells are frequent. The like cells develop and protrude into the space outer cortex consists of tangentially stretched formerly occupied by the sieve tube mem- collenchyma cells and a few slightly enlarged bers. These cells appear as tangential ag- sclereids. The outermost layer of the shoot is glomerates in transverse sections (Fig. 16). the newly formed periderm with adhering But they are not as closely connected to each rernnants of the epidermis. other as the secondary phloem fibres (e.g. in Groups of secondary phloem fibres up to oak bark), because they develop from axial 15 cell wide develop within the first year phloem parenchyma strands (Figs. 13 & 14). (Fig. 22). Some of these groups are very They always occupy less space than non- close to each other, resembling a nearly con- collapsed sieve tube members. Thus the growth tinuous tangential band. They are accompan- rings become compressed. The time when ied by thick-walled, lignified, chambered cells start to develop varies within the tree. In crystalliferous cells. Phloem rays run through younger sampies first developmental stages the fibre groups and undergo sclerification may be present in the periphery of the current when in direct contact with the secondary growth ring (Fig. 17). In old sampies the phloem fibres. Numerous sm all groups of phloem fibre-/sclereid-like cells develop in sclereids are scattered immediately beneath the preceding year's growth ring (Fig. 18). the periderm. Some groups of sclereids With increasing secondary growth more develop in the cortex. Most sclereids are secretory cells are formed (Fig. 18), yet they rounded irregularly or isodiametric. Some are absent close to the cambium. Dilatation sclereids develop between the groups of sec- growth is mainly restricted to wedge-shaped ondary phloem fibres, the first formed al- zones at the periphery of the bark (Fig. 19). ways in contact with the fibre groups. Dila- Here the cells are tangentially stretched, some tation growth proceeds; some phloem rays divide anticlinally. In adjacent bark areas tan- exhibit a funnel-shaped dilatation growth, gential growth stress is compensated by a others only partly dilate, and some rays radial compression of the tissue, tangential remain unchanged (Fig. 22). expansion of cells and the formation of inter- With increasing secondary growth the cellular spaces. Due to a constant repetition oIdest groups of secondary phloem fibres are of these processes, even older samples ap- connected by sclereid groups (Fig. 23). These pear to be relatively homogeneous. When a sclereids develop from axial phloem paren- rhytidome is formed in older bark, this homo- chyma cells and dilated phloem rays. Thus, geneity is ir.tensified by the separation of in transverse sections some sclereids appear tissue modified by dilatation growth (Fig. 20). more or less isodiametric and some tangentially extended. In radial sections most scle- Populus tremula L. reids are round, and sclereid groups are often axially elongated. The youngest sample represents the bark Even young bark exhibits growth rings shortly after secondary growth has started (Fig. 24). They resuIt from a sequential de- (Fig. 21). The course of the vascular cam- velopment of different cell types during one

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Figs. 26-29. Betula pendula Roth. Transverse section. - 26: Bark in the first year of development shortly after secondary growth had started (white asterisks = cortex collenchyma, black asterisks = primary bark fibre groups, arrows = sc1ereids, pe = periderm, cp = cortex parenchyma). - 27: Bark in the first year of development after proceeding secondary growth (small white asterisks = cortex collenchyma, large white asterisks = sclereids, black asterisks = primary bark fibre groups, pe = periderm, cp = cortex parenchyma). - 28: Three year old bark (arrowhead = growth ring boundary, arrow = continuous band of sclereids and primary bark fibres) . - 29: Several year old bark. Extensive sc1erification.

f- Figs. 21-25. Populus tremula L. Transverse section. - 21: Bark in the first year of development shortly after secondary growth had started (white arrows = periderm, black arrow = primary phloem elements, asterisks = primary bark fibre group, ce = cortex collenchyma, cp = cortex parenchyma, sp = secondary phloem). - 22: Bark in the first year of development after proceeding secondary growth (small black asterisks = sclereids in the cortex, large black asterisk = funnel-shaped phloem ray dilatation, small white asterisks = primary bark fibre groups, large white asterisks = secondary phloem fibre groups, black arrow = unchanged phloem ray, white arrow = sclerified phloem ray traversing a group of secondary phloem fibres, black arrowhead = phloem ray dilatation restricted to a certain area). - 23: Secondary phloem fibre groups (large white asterisks) connected by sclereid groups (black asterisks). Small white asterisks = primary bark fibre groups. - 24: Growth rings (arrowheads = growth ring boundaries) in several years old bark. - 25: Old bark after formation of a rhytidome.

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2mm 32

Figs. 30-32. Betula pendula Roth. Transverse seetion. - 30: Growth rhythm in sc1ereid groups (arrows = sc1ereid group boundaries). Radially elongated sc1ereids. - 31: Few growth rings visible in the not sc1erified secondary phloem between the sc1ereid groups. - 32: Old bark with extensive formation of a rhytidome (arrows = last formed sequent periderm).

Downloaded from Brill.com10/01/2021 12:51:00PM via free access Trockenbrodt - Structural changes during bark development 17 growth period accompanied by the collapse em elements between the secondary phloem of sieve tube members. At the beginning of a and groups of primary bark fibres are com- growth period a zone of predominantl y sieve pletely collapsed. The fibre groups are push- tube members is formed followed by tangen- ed apart due to the dilatation of phloem rays tially arranged groups of secondary phloem and especially of the cortex parenchyma fibres. The size of these groups varies a lot, cells. The latter enlarge, round off and divide but their radial width (3-15 cells) tends to anticlinally, the cortex collenchyma cells ex- decrease with age. A second zone of sieve pand tangentially or divide anticlinally. Some tube members, companion cells, and axial slightly enlarged selereids develop between phloem parenchyma cells develops. At the the groups of primary bark fibres. The outer- end of the growth period a narrow layer of most layer of the shoot is a distinct periderm 1-3 axial phloem parenchyma cells is form- with adhering remnants of the epidermis. ed. The sieve tube members usually start Selerification and dilatation growth pro- collapsing in the last year's phloem but intact ceeds (Fig. 27) in the first year. Funnel- ones may still be present in older parts of the shaped phloem ray dilatation occurs. The dis- phloem. The growth ring pattern is signifi- tance between groups of primary bark fibres cantly disturbed by increasing selerification increases and the gaps are partly filled with and dilatation growth. Groups of selereids selereid groups. Together they form an irreg- develop in the entire secondary phloem ex- ular tangential band. Sclereids also develop in cept the current growth ring. They fuse and the cortex. form large, irregularly shaped groups. Fre- With increasing secondary growth the bark quently selereid groups start developing elose exhibits growth rings (Fig. 28). In every to secondary phloem fibres. Their develop- growth period a zone consisting of sieve tube ment is sirnilar to the one in oak bark. The memtJers, companion cells, axial phloem pa- patterns of dilatation growth are maintained renchyma cells and phloem rays is formed. with increasing age. Cortex cells enlarge and The diameter of the sieve tube members de- divide, axial phloem parenchyma cells round creases from the beginning to the end of the off and enlarge only slightly. The phloem ray growth period. At the end of the growth dilatation is funnel-shaped in the outer sec- period a layer of 1-4 axial phloem paren- ondary phloem. It is restrlcted to parts of the chyma cells is formed. Secondary phloem ray in the inner secondary phloem. Primary fibres are absent. The collapse of sieve tube elements of the bark are still present but more members starts in the preceding year's sec- and more segregated. ondary phloem, but it remains incomplete for In old bark a rhytidome is formed but the several years. The latest growth ring is free numerous sequent periderms lie very elose to of selereids. Funnel-shaped phloem ray dila- each other separating only small parts of the tation starts in the last year's secondary phlo- tissue (Fig. 25). em and is restrlcted to multiseriate rays. Cells of the uniseriate rays enlarge slightly but they Betula pendula Roth do not divide. The band of sclereids and primary bark fibres is nearly continuous (Fig. Because both sampie trees do not differ 28). Beneath this band sclereid groups have very much with regard to their basic bark developed and have partly fused with the structure their development is described to- band. gether. The influence of sclerification on bark The youngest sampie shows the shoot a structure increases with growth. Huge, most- short time after secondary growth has started ly radially oriented groups of sclereids de- (Fig. 26). From the vascular cambium a nar- velop (Fig. 29). Sclerification proceeds from row zone of secondary phloem is formed initial cells outwards. When an older sclereid consisting of sieve tube members, compan- group is reached, both groups fuse. Thus ion cells, axial phloem parenchyma cells and large sclereid groups exhibit growth rhythms. 1-3 seriate phloem rays. The primary phlo- Sclereids not fully differentiated may lie be-

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side completely developed ones, or the inner caused by dilatation growth or "during the sclereids of an old group are smaller than the formation of the rays." In the present investi- outer ones of a young group (Fig. 30). But gation the study of the phloem ray formation these growth rhythms do not correspond revealed that the broad rays develop by fu- to the annual ring pattern of the secondary sion of narrow phloem rays. The fusion is phloem. The axial dimension of the sclereid caused by the elimination of cambium initials groups often exceeds several millimetres. In as it was described for wood rays by Braun addition, the groups enlarge tangentially and (1955). Reinders and Reinders-Gouwentak therefore compress the remaining secondary (1961) describe 1,2,5, and 42 year old bark phloem. Rarely more than 3 or 4 growth sampIes of Quercus robur and Q. petraea. rings are discernible (Fig. 31). The individ- According to these authors the two species ual sclereids vary a lot in form and shape, but show no differences in their basic bark struc- they often are radially extended (Fig.31). ture. This is supported by observations by Remnants of the former continuous band of Holdheide (1951). Ouring the first year the sclereids and primary bark fibres are still groups of primary bark fibres are connect- visible. Because of the intensive sclerification ed to a circle by sclereids. Already in the 5 dilatation growth is restricted to the cortex cells year old sampie the ring consists mainly of and a slight tangential enlargement of phloem sclereids. Remnants of this ring are present in ray cells outside the latest growth ring. rhytidome parts of the 42 year old bark. The In older bark a massive rhytidome is intensity of sclerification and dilatation var- formed. Large parts of the bark are isolated ies considerably between the developmental by sequent periderms, but adhere to the re- stages. The stages correspond to those de- maining bark (Fig. 32). scribed above. The primary elements of the bark are dealt Discussion with in the papers of Möller (1882), Speyer Literature data on the bark of the investi- (1907), and Reinders & Reinders-Gouwen- gated tree species often correspond to one of tak (1961); Holdheide (1951) does not men- the developmental stages described above, tion them at all. but sometimes they deviate. Oescriptions of other Quercus species of- According to Hanstein (1853), isolated ten differ from those on Quercus robur, see groups of primary bark fibres are arranged in Howard (1977) and Nanko & Cote (1980) on a circle in the bark of Quercus robur. A few several oak species from North America, sclereids lie between the groups. Groups of Babos (1979) on Quercus cerris Loud. and sclereids are scattered in the tissue. The Röckle (1986) on Quercus rubra L. Part of amount of sclereids increases with growth. these deviations might be due to genetic dif- Möller (1882) observed the same arrange- ferences between species or species groups; ment of primary bark fibres. He mentions Chang (1954) proposed this for the oak sub- that the sclereid groups of the secondary genera Erythrobalanus and Lepidobalanus, phloem are re1ative1y small. Both authors in- but the characteristics he classifies as general vestigated young bark. Speyer (1907) de- differences (e.g. the arrangement of scle- scribes the structure of young and old bark of renchyma) were not confirrned by Howard Quercus robur. The first does not show a (1977). Möller (1882) and Röckle (1986) dif- continuous sclereid-fibre ring, whereas the ferently describe the presence of a sclereid- old bark does. The bark of Quercus robur ex- fibre-ring and the degree of sclerification in amined by Holdheide (1951) does not show bark sampIes of Quercus rubra. These differ- any such ring-like structure but his descrip- ences might be caused by a different develop- tion corresponds to the older sampIe of the mental stage of the sampies. present study. He observed growth layers, Oevelopmental studies of elm bark are not broad phloem rays protruding into the xylem, available. The description of mature bark of and an intensive dilatation growth close to Ulmus glabra by Holdheide (1951) corre- these rays. According to Holdheide (1951), sponds to the older, thicker bark sampIes de- the 'splitting' of the broad phloem rays is scribed above.

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Hanstein (1853), Möller (1882), Chang large tangential distance between the second- (1954), and Nanko & Cote (1980) describe ary phloem fibre groups in the young bark of bark of different developmental stages of Ul- the investigated poplar tree. Most observations mus laevis, U. campestris and U. americana. of Kosichenko (1969) stand in accordance Hanstein (1853) observes primary bark fibres with the bark description above. However, forming a continuous ring whereas Möller his conclusion that tissue starts changing (1882) reports isolated groups. The authors earlier in young bark than in older bark is do not mention any dilatation growth for elm, untenable. The fact that in young bark of only Holdheide (1951) finds wedge-shaped the higher stern phloem ray dilatation starts dilatation areas in older bark of Ulmus glabra. closer to the cambium than in older bark of The analysis of Ulmus americana and U. the stern base should not be related to time alata by Nanko and Cote (1980) is very simi- but to a response to an increase of girth lar to the one of Ulmus glabra by Holdheide which is considerably stronger in a young (1951). tree. Moreover, the present study does not Literature data on the presence of muci- reveal an earlier sclerification with increasing lage cells in Ulmus bark differ to a great ex- height. tent. According to Möller (1882), Solereder The observations for the development of (1899), and Metcalfe & Chalk (1950) muci- bark of Populus tremuloides described by lage cells are often present in the bark of the Rees and Shiue (1957/58) corresponds with Ulmaceae, but individuals without these cells ours. According to Bosshard and Stahel may be found. Möller (1882) describes muci- (1969), sclerification is a modification of the lage cells in the bark of Ulmus pro cera and bark of Populus robusta, especially in a juve- U. rubra, Melchior (1927) in Ulmus laevis, nile stage of development. The forms of scle- U. glabra and U. rubra, Holdheide (1951) in rification observed during the present investi- Ulmus g labra and U. minor, and Chang (1954) gation are similar to those found by Bosshard in Ulmus americana and U. rubra. Möller and Stahel (1969) but, in contrast, the scleri- (1882) does not mention any mucilage cells fication is more intensive in the older bark in his descriptions of the bark of Ulmus lae- than in the juvenile stage. vis. Neither do Nanko and Cote (1980) fot Other papers on the anatomy of poplar Ulmus alata and U. americana. In addition, bark are those of Möller (1882) on Populus Metcalfe and Chalk (1950) report of groups alba, P. nigra, P. pyramidalis and P. tremula, of mucilage cells which coalesce to cavities in Perredes (1903) on 11 different poplars, Hold- the cortex of the genus Ulmus. Such cavities heide (1951) on Populus nigra and Chang were not observed in the investigated bark (1954) on Populus tremuloides. In most of sampies of Ulmus glabra. these studies only one developmental stage is Compared to the descriptions of oak bark described, mostly that of thin, young bark those of elm bark show more similarities be- (Möller 1882; Perredes 1903). Especially cause in elm bark enlarged sclereids are not Perredes (1903) mainly analyses cortex, pri- formed, only slight dilatation growth occurs mary bark fibres and young secondary phlo- and the main changes of the tissue take place em. He finds only funnel-shaped phloem ray within the first few years. dilatation. But, dilatation growth restricted to Developmental studies of poplar bark were small parts is not clearly visible before an age conducted by Kosichenko (1969), Rees & of approximately 10 years. Perredes (1903) Shiue (1957/58), and Bosshard & Stahel mentions 'older' barks with 5 layers of sec- (1969). According to Kosichenko (1969), ondary phloem fibres, so his bark is still elliptic groups of secondary phloem fibres quite young. Holdheide (1951) and Chang are formed in Populus tremula dtiring the (1954) analyse old secondary phloem without first 10 years. These groups are located at further information on primary elements of considerable tangential distance. After the the bark. 10th year the fibre groups become narrower The anatomical structure of the bark of and connect to tangential bands. Therefore different birch species is subject of only a age and dilatation growth seem to cause the few investigations. There are no develop-

Downloaded from Brill.com10/01/2021 12:51:00PM via free access 20 IA WA Bulletin n. s., Vol. 12 (1), 1991 mental studies. The description of primary investigated, do not allow to consider the elements of Betula pendula bark by Möller details of bark development observed in the (1982) corresponds to that given above, his present investigation to be generally valid. It information on how sclereid groups are ar- is unknown whether the structural variability ranged in the secondary phloem reveals that observed here reflects only a part of the vari- his sampIes were young. The observations of ation possible in bark structure. Additional Holdheide (1951) show many similarities studies on the variability and development of with those of the older sampIes of the present bark structure are urgently needed. investigation. He describes the same mechan- ism of sclereid group development. The study Acknowledgements by Bhat (1982) on' Betula pendula and B. This work is part of the author's Ph.D. pubescens is not sufficiently informative with thesis, and he wishes to express his gratitude regard to basic bark structure. Only he ob- to the Deutsche Forschungsgemeinschaft for serves secondary phloem fibres in birch financial support. bark. All the other authors never observed any secondary phloem fibres. Only these three papers deal with Betula pendula bark. Refereooes In all the other papers different species are Aday, J. U. 1978. Variability of fibre length analysed. of Moluccan Sau (Albizia falcataria (L.) According to Chang (1954), the sclereid Fosb.) wood and bark. Forpride Digest 7: group formation in Betula alleghaniensis and 86-87. B. papyrijera is similar to the centrifugal one Babos, K 1979. Anatomische Untersuchun- observed in Quercus robur and Populus tre- gen der Rinde bei den Stämmen von Quer- mula. In general, the sclerification appears to cus cerris var. cerris Loud. und Quercus be less intensive than in the Betula pendula cerris var. austrica (Willd.) Loud. Folia trees of the present investigation. While dendrologica 6: 60-78. Chang's (1954) description of the young Bhat, KM. 1982. Anatomy, basic density bark agrees with the above observations, that and shrinkage of birch bark. IAWA Bull. of the older bark reveals large differences. n.s. 3: 207-213. These may be due to the selection of different Birnstiel, W. 1922. Vergleichende Anatomie species or to differences in age or the sam- der Cinnamomumrinden (unter besonderer pIes' thickness. Berücksichtigung ihrer Entwicklungsge- schichte). Diss. Phi!. Fak. Univ. Basel. The variety of developmental processes in Bosshard, H.H. & J. Stahel. 1969. Modifi~ bark and the variability of bark characters kationen in der sekundären Rinde von within and between species were studied in Populus robusta. Holzforsch. Holzver- relation to bark age, bark thickness, stern wert. 5: 1-5. height, and stern diameter. It is impossible to Braun, H.J. 1955. Beiträge zur Entwick- determine the degree of influence of each lungsgeschichte der Markstrahlen. Bot. separate factor. These quantifiable factors Stud. 4: 73-131. only affect but do not determine the physio- Chang, Y.P. 1954. Anatomy of common logical causes of variation. Every variation North American pulpwood barks. T APPI depends on the different supply with carbo- Monographs Series No. 14. hydrates, phytohormones, water and nu- Esau, K 1969. The phloem. Handbuch der trients, which is caused by a varying meta- Pflanzenanatomie. V/2. Gebr. Borntraeger, bolism. The metabolism changes with a Berlin, Stuttgart. number of abiotic and biotic factors like tem- Ezell, A.W. & J.L. Stewart. 1978. The perature, light intensity, precipitation, etc. length of phloem fibres in Sweetgum There is not much information available on (Liquidambar styraciflua L.). A research the relations between these factors and the note. Wood Fiber 10: 186-187. structure with regard to tree bark or phloem. Gerlach, D. 1969. Botanische Mikrotechnik. This, and the small number of individuals Thieme Verlag, Stuttgart.

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Ghouse, A.K.M. & S. Hashmi. 1977. Cell Iqbal, M. & A.K.M. Ghouse. 1983. An length variation of phloem fibres within analytical study on cell size variation in the bark of some evergreen and deciduous some arid zone trees of India: Acacia trees. Bot. Jahrb. Syst. 97: 503-507. nilotica and Prosopis spicigera. IAWA Ghouse, A.K.M. & M. Iqbal. 1977. Trends Bull. n. s. 4: 46-52. of size variation in phloem fibres and sieve- Kosichenko, N.E. 1969. Changes with age tube cells within the bark of some arid- in the anatomical structure of phloem of zone trees. Flora 166: 517-521. Populus tremula L. (In Russian.) Nauc. Ghouse, A.K.M. & M. Iqbal. 1981. Cell Dokl. Vyss. Skoly (Biol. Nauki) Moskva length variation within the bark and wood 1: 61-68. with respect to the development of trees. Kut':era, L. 1. & M. Bariska. 1982. Zur Topo- In: Advances in forest genetics (ed. P.K. graphie der Holzeigenschaften im Baum- Khosla): 191-212. Ambeka, New Delhi. körper. Forstarchiv 53: 136-141. Ghouse, A.K.M., P.R. Khan, F.A. Khan Liese, W. & N. Parameswaran. 1972. On the & M. Salahuddin. 1982. Study on the variation of celllength within the bark of length of phloem fibres in Bombax ceiba some tropical hardwood species. In: [B. malabaricum], with reference to girth Research trends in plant anatomy - K. A. increase.1. Tree Sci. 1: 128-129. Chowdhury Commemoration Vol. (eds. Ghouse, A.K.M. & F.A. Siddiqui. 1976a. A.K.M. Ghouse & M. Yunus): 83-89. Cell length variation in phloem fibres Tata McGraw-Hill, New Delhi. within the bark of four tropical trees- Melchior, H. 1927. Schleime. In: Die Roh- Aegle marmelos, Mangifera indica, Syzy- stoffe des Pflanzenreiches (ed. 1. von gium cumini, Zizyphus mauritiana. Blumea Wiesner). 4th ed.: 1831-1912. W. Engel- 23: 13-16. mann, Leipzig. Ghouse, A.K.M. & F.A. Siddiqui. 1976b. Metcalfe, C.R. & L. Chalk. 1950. Anatomy Cell length variation in phloem fibres of the dicotyledons. Vol. 1 and Vol. 2. within the bark of some tropical fruit trees Clarendon Press, Oxford. I. Anona squamosa, Eblica officinalis, Möller, J. 1882. Anatomie der Baumrinden. Feronia limonia, and Grewia asiatica. Phy- 1. Springer, Berlin. tomorphology 26: 109-111. Nanko, H. & W.A. Cote. 1980. Bark struc- Ghouse, A.K.M. & M. Yunus. 1976. Cell ture of hardwoods grown on Southern length variation in the secondary phloem Pi ne sites. Renewable Materials Institute of Dalbergia spp. with increasing age of Series. Syracuse University Press, Syra- the vascular cambium. Ann. Bot. 40: 13- cuse. 16. Nicholls, J.W.P. & F.H. Phillips. 1970. Hanstein, J. 1853. Untersuchungen über den Preliminary study of coppice-grown Bau und Entwicklung der Baumrinde. Eucalyptus viminalis as a source of chip G.W.1. Müller, Berlin. material. CSIRO Div. For. Prod. Tech- Hasler, O. 1936. Entwicklungsgeschichte und nol. Paper 58. vergleichende Anatomie der pharmako- Parameswaran, N. & W. Liese. 1974. Varia- gnostisch wichtigen Rharnnusrinden unter tion of cell length in bark and wood of besonderer Berücksichtigung der Calcium- tropical trees. Wood Sci. Technol. 8: 81- oxalat-Bildung. Ber. Schweiz. Bot. Ges. 90. 45: 519-593. Perredes, P. E. S. 1903. Comparative anat- Holdheide, W. 1951. Anatomie mitteleuro- omy of the barks of the Salicaceae. Part I. päischer Gehölzrinden. In: Handbuch der Pharmaceut. 1. 71: 171-182. Mikroskopie in der Technik, Vol. V/I Raskatov, P.B. & N.E. Kosichenko. 1968. (ed. H. Freund): 193-367. Umschau, Characteristics of phloem elements in dif- Frankfurt a. M. ferent parts of Aspen (Populus tremula) Howard, E. T. 1977. Bark structure of sterns (In Russian.) Bot. Zh. (Leningrad) Southern Upland Oaks. Wood Fiber 9: 53: 1612-1616. Abstract in: Ber. Biochem. 172-183. Biol. 310: 59.

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Rees, L.W. & C.l. Shiue. 1957/58. The Strasburger, E. 1891. Ueber den Bau und die structure and development of the bark of Verrichtungen der Leitungsbahnen. Quaking Aspen. Proc. Minnesota Acad. Histolog. Beitr. 3. G. Fischer, Jena. Sci. 25/26: 113-125. Thorenaar, A. 1926. Onderzoek naar bruik- Reinders, E. & C.A. Reinders-Gouwentak. bare kenmerken ter identificatie van 1961. Handleiding bij de Plantenanato- boomen naar hun bast. Meded. Proefstat. mie. 5th ed. Landbouwhogeschool Cen- Boschwezen 16. Batavia-Wageningen. traal Magazijn, Wageningen. Trockenbrodt, M. 1990. Survey and discus- Richter, H.G. 1981. Anatomie des sekun- sion of the terminology used in bark anat- dären Xylems und der Rinde der Laura- omy. IAWA Bull. n.s. 11: 141-166. ceae. Sonderbände des Naturwissen- Trockenbrodt, M. & N. Parameswaran. 1986. schaftlichen Vereins in Hamburg 5. P. A contribution to the taxonomy of the Parey, Hamburg-Berlin. genus Inga Scop. (Mimosaceae) based on Röckle, H. 1986. Veränderungen der Rin- the anatomy of the secondary phloem. den struktur in Abhängigkeit von der To- IAWA Bull. n.s. 7: 62-71. pographie, am Beispiel von Quercus rubra Wyk, A. E. van. 1985. The genus Eugenia L. Dipl.-Arbeit, Fachber. Biologie, Univ. (Myrtaceae) in southern Africa: Structure Hamburg. Unpublished. and taxonomic value of bark. S. Afr. J. Ruetze, M. & U. Schmitt. 1986. Glykol- Bot. 51: 157-180. Methacrylat (GMA) als Einbettungssys- Yunus, M., M. Iqbal & D. Yunus. 1977. tem für histologische Untersuchungen von Cell length variation in the secondary Koniferen-Nadeln. Eur. 1. For. Path. 16: phloem of some medicinally important 321-324. lropical trees. J. Israel For. Assoc. 27: Solereder, H. 1899. Systematische Anatomie 60-65. der Dicotyledonen. F. Enke, Stuttgart. Zahur, M. S. 1959. Comparative study of Speyer, J. 1907. Beiträge zur Entwicklungs- secondary phloem of 423 species of geschichte der Rinde pharmakognostisch woody dicotyledons belonging to 85 interessanter Pflanzen. Diss. Phil. Fak. families. Comell Univ. Agr. Expt. Stat. Univ. Bem. Mem.358.

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