IAWA Journal, Vol. 14 (2),1993: 191-204

STRUCTURE OF STEM AND CAMBIAL VARIANT IN SPATHOLOBUS ROXBURGIill (LEGUMINOSAE)

by

M.N.B. Nair Department of Botany, University of Delhi, Delhi 110 007, India

Summary The stern of Spath%bus roxburghii, a Fisher 1989; Ursem & ter Welle 1992). How­ tropicalliana, has alternating layers of xylem ever, they have also been reported in plants and phloem as a result of formation and activ­ with different habits and habitats (Metcalfe & ity of successive cambia. Successive cambial Chalk 1950, 1983; Fahn & Shchori 1967; rings are developed by dedifferentiation of Wheat 1977, Mikesell 1979; Bailey 1980; groups of parenchyma cells outside the dis­ Carlquist 1988; Nair & Mohan Ram 1990). continuous band of sclereid-fibres. The scle­ The large body of information available on reid-fibre band is formed by the development cambial variants is based on mature stern of sclereids between the primary bark fibres. structure. As very few developmental studies Each successive cambium first produces a have been made to trace the precise manner layer of sclereid-fibres which separates the of initiation of these cambia, the interpretation vascular tissue produced by one cambial ring of their end products becomes problematic from the other. After secondary growth, the (Philipson & Ward 1965). epidermis is replaced by periderm. In the old­ Spath%bus roxburghii (syn. Butea parvi­ er stern phelloderm contributes to the forma­ flora Roxb.) (family Leguminosae) is a gigan­ tion of new cambiallayers. Secondary phloem tic climber that twines around trunks of trees has sieve tube members; companion cells, in Indian sal and teak forests (Fig. 1) and caus­ phloem parenchyma, phloem fibres and se­ es much damage. It attains a diameter of up to cretory cells. The wood shows a tendency I m. The stern yields a red gum that resem­ towards ring-porosity only in the first xy­ bles 'kino' of commerce extracted from Pte­ lem layer. The subsequent layers are diffuse­ rocarpus marsupium (Gamble 1902). porous. The vessels are wide and narrow. The anomalous stern structure in Spatho­ Perforated ray cells or radial vessels are fre­ /obus roxburghii Benth. has been briefly re­ quent in the wood and probably help in ver­ ported earlier (Gamble 1902; Solereder 1908; tical conduction by interconnecting vessel Metcalfe & Chalk 1950). However, no detail­ endings. In this scandent species parenchyma ed study of the cambial variant and structure cells are abundant. It is inferred that they help of the secondary xylem has been done previ­ the vessel segments to remain undamaged ously in this species. when the woody stern twists around sup­ ports. Materials and Methods Key words: Cambial variant, Leguminosae, The sampies for investigation were col­ liana, perforated ray cells, Spath%bus, lected from Cheenikkala (Tropical forest) of successive cambia, vestured pits. Nedumangad forest area, Kerala State, India. Portions of stern of varying diameter (1 to 12 Introduction cm) were collected and fixed in F AA (forma­ Cambial variants (anomalous secondary lin : acetic acid : 50% ethanol = 1 : 1 : 8) and growth) are of common occurrence in tropical evacuated until they sank in the fixative. They lianas and vines (Basson & Bierhost 1967; were sectioned on a sliding microtome, stain­ Dobbins 1969, 1971, 1981; Dobbins & Fisher ed with 0.05% toluidine blue 0 in 0.1 M phos­ 1986; Carlquist 1985, 1988, 1991; Ewers & phate buffer pH 6.8 (O'Brien et al. 1964),

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Table 1. Wood characteristics in Spatholobus roxburghii. S.D.

Mean diameter of larger vessels (width 100 ~m and above) 322.0 ~m* 57.5

Mean length of the larger vesseI element (width 100 ~m or above) 324.0 ~m* 105.96

Mean diameter of narrow vessels (width below 100 ~m) 56.8 ~m* 15.8

Mean length of the narrow vessel elements (width below 100 ~m) 392.0 ~m* 93.1 Frequency of vesseIs/mm2 (wide) 4.9 1.9 Frequency of vessels/mm2 (narrow) 29.7* 7.3

Mean diameter of pits on the vessel element wall 10.8 ~m* 0.9 Maximum ray height 186 cells Maximum ray width 7 cells Mean diameter of the stern at the time of initiation of first 2.67 cm** 0.23 additional cambium Mean thickness of the phloem layer 1.9 mm** 0.27 Mean thickness of the xylem layer IOmm**

* = average of 60 readings; ** = average of 20 readings.

safranin 0 alone, and with safranin 0 and fast phloem rays and secretory cells (Figs. 5, 7). green FCF (Berlyn & Miksche 1976). Mate­ In older bark the phloem has several tangen­ rials were prepared for scanning electron mi­ tially arranged groups of secondary phloem croscopy as described earlier (Nair 1987). fibres (Figs. 5-7). Phloem rays show limited Measurements were taken using a calibrated dilation growth towards the outside (Fig. 5). eyepiece micrometer (Table 1). The presence The sieve tube members usually collapse in of heartwood was tested by TTC (2,3,5-tri­ the previous year's phloem (Figs. 5,6). Sev­ phenyl tetrazolium chloride) (Fahn & Amone eral secretory cells are present in the secondary 1963). PAS reaction was carried out accord­ phloem (Figs. 5, 7, 11, 12). They develop ing to the method suggested by Jensen (1962). from the cambium and can be distinguished even in the early stages of deveIopment. Results These cells contain insoluble polysaccharides The woody stern of Spatholobus rox­ (Fig. 10) as confirmed by PAS reagent. As burghii has alternating layers of xylem and secondary growth proceeds, the periderm phloem (Figs. 2, 40a, b, d). The mean thick­ replaces the epidermis. Sc1ereids or sc1ereid ness of the phloem layer is 1.9 rum (Table 1). groups develop in the cortex (Fig. 14). Rhyti­ Each phloem layer is accompanied by cam­ dome is present in the old bark (Fig. 15). bium internally (Fig. 3). The cambium asso­ ciated with old inner phloem layer shows de­ Development 0/ cambial variant generation at certain regions (Fig. 4). Initially the secondary growth in Spatho­ lobus roxburghii is normal. However, initi­ Structure 0/ bark ation of an additional cambium occurs by The secondary phloem consists of sieve dedifferentiation of a few cortical parenchy­ tube members (Figs. 8, 9), companion cells ma cells peripheral to the tangential band of (Fig. 8), secondary phloem fibres (Figs. 6, 7), axial phloem parenchyma cells, multiseriate (text continued on page 200)

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Legend 0/ Figures 1-39 (pages 4-9):

Fig. 1. The seandent habit of Spatholobus roxburghii (arrow). - Fig. 2. Transverse seetion (TS) of stern showing alternating layers of xylem and phloem. Arrow indieates the selereid-fibre layer. Seale bar = 355 ~m. - Fig. 3. Magnified view of portion of TS of stern depicting addi­ tional eambium and its derivatives. Seale bar = 130 ~m. - Fig. 4. TS of stern showing degen­ eration of portion of old eambium. Seale bar = 130 ~m.

Figs. 5 & 6. Portion of TS of seeondary phloem showing erushed sieve tube members, phloem parenehyma, seeondary phloem fibres and phloem rays. Seale bar for 5 = 330 ~m; for 6 = 105 ~m. - Fig. 7 . TS of stern showing seeondary phloem with seeretory eells (arrow). Seale bar = 130 ~m. - Fig. 8. TS of portion of eambium and eurrent years phloem showing sieve tube mem­ bers and eompanion eells. Seale bar = 36 ~m. - Fig. 9. Longitudinal seetion: surfaee view of lateral wall of a sieve tube member showing sieve areas. Seale bar = 24 ~m. - Fig. 10. Devel­ oping seeretory eells showing PAS positive eontents. Seale bar = 67 ~m. - Fig. 11. TS of phloem showing a group of seeretory eells. Seale bar = 75 ~m. - Fig. 12. LS of portion of seeondary phloem showing seeretory eells. Arrows indieate the darldy stained gum in the seere­ tory eells. Seale bar = 285 ~. - Fig. 13. Portion of bark showing the tangential selereid-fibre layer (arrow) and site of initiation of additional eambium. Seale bar = 130 ~m.

Fig. 14. Portion ofthe TS ofbark showing sclereids. (arrows). Seale bar = 145 ~. - Fig. 15. Portion of old bark showing part of seeondary phloem, periderm and rhytidome. Seale bar = 265 ~m. - Fig. 16. TS of the old bark showing phelloderm giving rise to additional eambial layer. Seale bar = 105 ~m. - Figs. 17 & 18. TS of stern showing initiation of additional eam­ bium outside the sclereid-fibre layer. Seale bar for 17 = 250 ~m; for 18 = 125 ~m. - Fig. 19. LS of portion of the newly formed additional eambium. Seale bar = 22 ~m. - Figs. 20 & 21. TS of stern showing vaseular tissue produeed from the additional eambium. The sclereid-fibre layer (arrows) separates the newly formed vaseular tissue from the previous one. Seale bar for 20 = 315 ~m; for 21 = 357~. - Fig. 22. LS ofthe stern showing the diseontinuous sclereid­ fibre layer. Seale bar = 165 ~m.

Figs. 23 & 24. Longitudinal seetion of the sclereid-fibre layer. Figure 23 shows only selereids and figure 24 shows fibres and sclereids. Seale bar for 23 = 55 ~m; for 24 = 105 ~m. - Fig. 25. Portion of TS of stern showing tendeney for ring porosity in the first xylem layer. Seale bar = 250 ~m. - Fig. 26. TS of wood showing vessel dimorphism. Seale bar = 250 ~m.

Fig. 27. Vestured intervessel pits in narrow vessel, viewed from outside the vessel. Seale bar = 7 ~m. - Fig. 28. Vestured intervessel pits of wide vessel, viewed from outside the vessel. Seale bar = 3.3 ~m. - Fig. 29. Sealariform intervessel pits near the end of the vessel element, view­ ed from outside the vessel. Seale bar = 7 ~m. - Fig. 30. Vestured intervessel pits, viewed from inside the vessel. Seale bar = 4 ~m. - Fig. 31. TLS of wood showing axial parenehyma strand having 4 or 5 eells. Seale bar = 67 ~m. - Figs. 32 & 33. TLS of wood showing erystals in the ehambered axial parenehyma eell (arrows). Seale bar for 32 =45 ~m; for 33 =24 ~m.

Fig. 34. TLS of wood showing uniseriate and multiseriate rays. Seale bar = 250 ~m. - Fig. 35. Ray eells with perforations on the radial wall. Scale bar = 50 ~m. - Fig. 36. Perforated ray eells intereonneeting two vertieal vessels. Seale bar = 50 ~m. - Fig. 37. Portion of ray show­ ing a ray eell with perforation on the tangential wall. Seale bar = 48 ~m. - Fig. 38. Perforated ray eells tangentially intereonneeting two vertieal vessels. Seale bar = 72 ~m. - Fig. 39. Ray eells with perforations on the radial wall. Seale bar = 50 ~; pp = perforation plate.

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40c 40d

Fig. 40. Diagrammatie representation of initiation and aetivity of sueeessive eambia in the stern of Spatholobus resulting in the formation of alternate layers of xylem and phloem. PH = phloem, SC = sclereid-fibre layer, XY = xylem.

primary bark fibres/sclereids (Figs. 13, 17- 20, 21). The new cambium is always pro­ 19). This development is observed when the duced external to this sclereid-fibre layer. The stem has an average diameter of 2.67 em. phelloderm eontributes to the formation of the The formation of the eambium takes plaee at eambial ring in the older stern (Fig. 16). 4 or 5 loei in the form of ares (Figs. 17-19, 40a, e). These ares extend tangentially to form Structure oi wood a eomplete cambial ring. This additional eam­ The wood of Spatholobus roxburghii is bi al ring funetions as anormal bidirectional brown. Heartwood is absent as eonfirmed by eambium, produeing xylem internally and a positive TTC test indieating respiring eells phloem externally (Figs. 20, 21, 40b). Eaeh in the eentral xylem. The mean thiekness of a sueeessive eambium first produces a diseon­ xylem layer is 10.0 mm (Table 1). The wood tinuous layer of selerenehyma or fibres ex­ shows a tendency for ring-porosity only in ternally (Figs. 22-24) whieh separates the the first xylem layer (Fig. 25), the subsequent vaseular tissue produeed by one cambium layers are diffuse-porous. There are two dis­ from the produet of the next eambium (Figs. tinet types of vessels: extremely wide and

Downloaded from Brill.com09/29/2021 04:58:37PM via free access Nair - Cambial variant in Spatholobus 201 very narrow ones (Figs. 25, 26). The wide gested that interxylary phloem or incJuded vessels are round or oval in cross-sectional phloem is the product of a single cambium. view and are usually solitary and rarely in He stated that when successive cambia are in­ radial multiples (Figs. 25, 26). The narrow volved in the formation of concentric, alter­ vessels occur predominantly in radial multi­ nating layers of phloem and xylem, the con­ ples or in clusters (Figs. 25, 26). junctive tissue separates the vascular tissue of The vessels have simple perforation plates. one cambium from the product of the next and Intervessel pits are bordered, alternate and ves­ therefore, the term 'included' phloem is a rnis­ tured (Figs. 27-30). The wider vessels have nomer. In other words, phloem is not includ­ smaller pit borders (Fig. 28) than the narrow ed between xylem layers. In S. roxburghii ones (Fig. 27). The mean pit diameter is 10.8 xylem and phloem produced by one cambium 11m (SD: 0.85 11m). The vestured pits belong are separated from the products of the next by to type 2 (i) as per the classification proposed a tangential sclereid-fibre band. Therefore, the by Nair and Mohan Ram (1989). Occasion­ term included phloem or interxylary phloem ally scalariform pits are observed near the tip is not used for describing the cambial variant of the vessel elements (Fig. 29). Vestures are in this species. present in the inner pit apertures also but are The study of the cambial variant in the absent on the vessel element wall (Fig. 30). axis of Spath%bus roxburghii reveals that The axial parenchyma is paratracheal, the 'anomalous' distribution of vascular tis­ banded (Figs. 25, 26), storied (Fig. 34) and sue in the stern (alternating layers of xylem abundant. Each parenchyma strand has 4 or 5 and phloem separated by sclereid-fibre layer) cells (Fig. 31). The axial parenchyma cells results from the activity of successive cambia. sometimes develop septa and some segments Although secondary growth in Spatholobus contain crystals (Figs. 32, 33). Fibres form is initially normal, successive cambia are dif­ islands between axial and ray parenchyma ferentiated in the cortex outside the tangential cells (Figs. 25, 26). Rays are homocellular layer of sclereid-fibres. After the formation of (Fig. 34) having procumbent cells. There are periderm the successive cambia are formed narrow uniseriate rays and very wide and very from the phelloderm. I have studied initiation tall multiseriate rays (Fig. 34) that are up to 7 of only four layers of successive cambia. The cells wide; height ranges from 2 to 186 cells. secondary thickening of the stern in Spath%­ Perforated ray cells (radial vessel elements) bus occurs by the activity of these successive are frequently observed in the wood (Figs. cambia, each of which produces phloem ex­ 35-39). They have simple perforation plates ternally and xylem intemally. and bordered pits (Figs.35-39). Perfora­ Balfour (1965), Philipson and Ward (1965) tions are present in radial (Figs. 35, 36, 39), and Studholme and Philipson (1966) have tangential (Figs. 37,38) and horizontal walls. proposed that cambial variants in the stern of Perforated ray cell(s) connect(s) one vessel Amaranthaceae, Chenopodiaceae and Nycta­ ending to the other, both radially and tangen­ ginaceae are the result of the activity of a uni­ tially (Figs. 35-39). These interconnections directional cambium that produces both xylem usually occur between narrow vessels. and phloem internally. They suggested that phloem does not differentiate from the exter­ Discussion nal derivatives of cambium and interpreted The term 'cambial variant' is used here in the cambium as a self-perpetuating meristem­ place of 'anomalous secondary growth' as it atic zone. However, studies on Chenopodium is suggested that the anomalous structures are album (Artschwager 1920), Beta vulgaris a regular feature in the taxa in which they are (Artschwager 1926), Boerhaavia diffusa (Ma­ found (Carlquist 1988; Wheeler et al. 1989). heshwari 1930) and Bougainvillea (Esau & The term 'interxylary phloem' or 'included Cheadle 1969) have shown that this anomaly phloem' has been used to designate alternating is due to the activity of successive cambia. In layers of xylem and phloem where successive Dalbergia paniculata the anomalous stern struc­ cambia are involved in their formation (Met­ ture results from the formation and activity of calfe & Chalk 1983). Carlquist (1988) sug- successive cambia developed from the second-

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ary phloem (Nair & Mohan Ram 1990). In­ 1991). It is also reported that woody sterns formation on the variability of bark characters with 'included phloem' show little or no ill with regard to age, thickness, stern height, effects due to girdling because transport of stern diameter and physiological causes is assimilates is maintained through included rather scanty and there is a need for detailed phloem (Zamski & Tsivion 1977; Dobbins & studies (Trockenbrodt 1992). Fisher 1986). Vessels in Spath%bus roxburghii are dis­ tinctly narrow and wide, a condition described Acknowledgements as 'vessel dimorphism' by Carlquist (1981). This study was supported by the Uni­ The narrow vessels outnumber the wider ones. versity Grants Commission, New Delhi. The The presence of wide and narrow vessels scanning electron microscope facility provided could be of adaptive value in ensuring effi­ by the National Bureau of Plant Genetic Re­ cient transport and conductive safety. Zimmer­ sources, New Delhi, is gratefully acknowl­ mann (1982, 1983), Carlquist (1985) and edged. I thank Professor H. Y. Mohan Ram Baas et al. (1983) have suggested that wide for going through the text and for his critical vessels are efficient conductors but are vul­ comments. nerable to air emboli sm. Narrow vessels have considerable potential for safety, being less References vulnerable to air embolism. The stern of Spa­ Artschwager, E.F. 1920. On the anatomy of th%bus roxburghii used in the present study Chenopodium album L. Amer. J. Bot. 7: was collected from a high rainfall area (3500- 252-260. 4000 mm per annum) where no water stress Artschwager, E.F. 1926. Anatomy of vege­ or frost occurs. Carlquist (1985) suggested tative organs of the sugar beet. J. Agric. that the abundance of narrow vessels in scan­ Res. 33: 143-176. dent dicotyledons is reminiscent of the abun­ Baas, P., E. Werker & A. Fahn. 1983. Some dance of latewood vessels in non-scandent ecological trends in vessel characters. species. Redundancy of conducting elements IAWA Bull. n.s. 4: 141-160. is also reported to be of selective value in lia­ Bailey, D.C. 1980. Anomalous growth and nas and vines (Dobbins & Fisher 1986). vegetative anatomy of Simmondsia chinen­ In S. roxburghii ray cells show perfora­ sis. Amer. J. Bot. 6: 147-161. tions on radial, tangential and horizontal walls, Balfour, E. 1965. Anomalous secondary indicating that they interconnect vessels radi­ thickening in Chenopodiaceae, Nyctagina­ ally and tangentially aiding vertical transport. ceae and Amaranthaceae. Phytomorphol­ Perforated ray cells have been reported in ogy 15: 111-122. many species, but Gamble (1902), Solereder Basson, P.W. & D.W. Bierhorst. 1967. An (1908) and Metcalfe and Chalk (1950) did analysis of differential lateral growth in not mention the presence of perforated ray the stern of Bauhinia surinamensis. Bull. cells in S. roxburghii. Torrey Bot. Club 94: 404-411. The presence of wide rays and the abun­ Berlyn, G.P. & J.P. Miksche. 1976. Botan­ dance ofaxial parenchyma in scandent spe­ ical microtechnique and cytochemistry. cies are reported to perrnit sterns to twist with­ Iowa State Univ. Press, Ames. out damage (Carlquist 1975, 1985, 1988; Carlquist, S. 1975. Ecological strategies of Sieber & Kue:era 1980; Fisher & Ewers 1991, xylem evolution. Univ. California Press, 1992). The presence of cambial variant also Berkeley. helps in sheathing vessel groups with soft Carlquist, S. 1981. Wood anatomy of Nepen­ tissues, aUowing for flexibility. The sterns thaceae. Bull. Torrey Bot. Club 108: 324- of lianas are under high risk of bark injury, 330. vascular interruption and girdling. Therefore, Carlquist, S. 1985. Observations on func­ inclusion of living tissues within the xylem is tional wood histology of vines and lianas: advantageous because it helps rapid and vigor­ vessel dimorphism, tracheids, vasicentric ous regeneration following wounding (Dob­ tracheids, narrow vessels and parenchy­ bins & Fisher 1986; Fisher & Ewers 1989, ma. Aliso 11: 139-157.

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Carlquist, S. 1988. Comparative wood ana­ Gamble, J.S. 1902. A manual of Indian tim­ tomy. Systematic, ecological and evolu­ bers. London. tionary aspects of dicotyledon wood. Jensen, W.A. 1962. Botanical histochem­ Springer-Verlag, Berlin. istry. San Francisco, London, Freeman. Carlquist, S. 1991. Anatomy ofvine and lia­ Maheshwari, P. 1930. Contributions to the na stems: a review and synthesis. In: F.E. morphology of Boerhaavia diffusa (11). Putz & H.A. Mooney (eds.), The biology J. Indian Bot. Soc. 9: 42-61. of vines: 53-71. Cambridge Univ. Press, Metcalfe, C. R. & L. Chalk. 1950. Anatomy Cambridge. of the dicotyledons. Clarendon Press, Ox­ Dobbins, D.R. 1969. Studies on anomalous ford. cambial activity in Doxantha unguis-cati Metcalfe, C.R. & L. Chalk. 1983. Anatomy (Bignoniaceae). Development of the vas­ of dicotyledons. Ed. 2, vol. 2. Wood struc­ cular pattern. Can. J. Bot. 47: 2101-2106. ture and conclusion of the general intro­ Dobbins, D.R. 1971. Studies on the anoma­ duction. Clarendon Press, Oxford. lous cambial activity in Doxantha unguis­ Mikesell, J.E. 1979. Anomalous secondary cati (Bignoniaceae). H. A case of differen­ thickening in Phytolacca americana L. tial production of secondary tissue. Amer. (Phytolaccaceae). Amer. J. Bot. 66: 997- J. Bot. 58: 697-705. 1005. Dobbins, D.R. 1981. Anomalous secondary Nair, M.N.B. 1987. Occurrence of helical growth in lianas of the Bignoniacae is cor­ thickenings on the vessel element walls of related with the vascular pattern. Amer. J. dicotyledonous woods. Ann. Bot. 60: 23- Bot. 68: 142-144. 32. Dobbins, D.R. & J.B. Fisher. 1986. Wound Nair, M.N.B. & H.Y. Mohan Ram. 1989. responses in girdled stems of lianas. Bot. Vestured pits and vestured vessel member Gaz. 147: 278-289. walls in some Indian dicotyledonous Esau, K. & V.I. Cheadle. 1969. Secondary woods. Bot. J. Linn. Soc. 100: 323-336. growth in Bougainvillea. Ann. Bot. 33: Nair, M.N.B. & H.Y. Mohan Ram. 1990. 807-819. Structure of wood and cambial variant in Ewers, F. W. & J.B. Fisher. 1989. Variation the stem of Dalbergia paniculata Roxb. in vessel length and diameter in stems of IAWA BuH. n.s. 11: 379-391. six tropical and subtropicallianas. Amer. O'Brien, T.P., N. Feder & M.E. McCuHy. J. Bot. 76: 1452-1459. 1964. Polychromatic staining ofplant cell Fahn, A. & N. Arnone. 1963. The living walls by toluidine blue O. Protoplasma 59: wood fibres of Tamarix aphylla and the 367-373. changes occurring in them in transition Philipson, W.R. & J.M. Ward. 1965. The on­ from sapwood to heartwood. New Phy­ togeny of the vascular cambium in the stem tol. 62: 99-105. of seed plants. Biol. Rev. 40: 534-579. Fahn, A. & Y. Shchori. 1967. The organiza­ Sieber, M. & L.J. Kul:era. 1980. On the stem tion of the secondary conducting tissue in anatomy of Clematis vitalba L. IAWA some species of Chenopodiaceae. Phyto­ Bull. n.s. 1: 49-54. morphology 17: 147-154. Solereder, H. 1908. Systematic anatomy of Fisher, J. & F. Ewers. 1989. Wound healing the dicotyledons (English Ed.). Vol. I. in stems of lianas after twisting and gird­ Clarendon Press, Oxford. ling injuries. Bot. Gaz. 150: 251-265. Studholme, W.P. & W.R. Philipson. 1966. Fisher, J. & F. Ewers. 1991. Structural re­ A comparison of the cambium in two sponses to stem injury in vines. In: F.E. woods with included phloem Heimerlio­ Putz & H.A. Mooney (eds.), The biology dendron brunonianum and Avicennia resi­ ofvines: 91-116. Cambridge Univ. Press, nifera. New Zeal. J. Bot. 4: 355-365. Cambridge. Trockenbrodt, M. 1992. Qualitative structural Fisher,J. & F.Ewers.1992. Xylem pathways changes during bark development in Quer­ in liana stems with variant secondary cus rubur and Betula pendula. IAWA Bull. growth. Bot. J. Linn. Soc. 108: 181-202. n.s. 12: 5-22.

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Ursern, B.W.N.J. & B.J.H. ter Welle. Zamski, E. & T. Tsivion. 1977. Transloca­ 1992. Anomalous growth patterns in tion in plants possessing supernumerary South American lianas with special refer­ phloem. I. 14-C-assimilates and auxin in ence to their ontogeny. Proc. 2nd Pacific the internal phloem of tobacco (Nicotiana Regional Wood Anatomy Conf., 15-21 tabacum L.). J. Exp. Bot. 28: 117-126. Oct. 1989. F.P.R.D.I. College. Laguna, Zimmermann, M.H. 1982. Functional xylem Philippines. anatomy of angiosperm trees. In: P. Baas Wheat, D. 1977. Successive cambia in the (ed.), New perspectives in wood anatomy: stern of Phytolacca dioica. Amer. J. Bot. 59 -70. Nijhoff / Junk, The Hague, Bos­ 64: 1209-1217. ton. Wheeler, E.A., P. Baas & P.E. Gasson Zimmermann, M.H. 1983. Xylem structure (eds.). 1989. IAWA list of rnicroscopic and ascent of sap. Springer Series in Wood features for hardwood identification. Science l. Springer Verlag, Berlin, Heidel­ IAWA Bull. n.s. 10: 226-332. berg, New York.

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