IAWA Journal, Vol. 18 (4), 1997: 385-399

BARK ANATOMY OF ARBORESCENT LEGUMINOSAE OF AND GALLERY FOREST OF CENTRAL BRAZIL by

Cecilia G. Costa 1, Vera T. Rauber Coradin 2, Chiudia M. Czarneski2 & Benedito A. da S. Pereira 3

SUMMARY

The bark anatomy of28 of arborescent Leguminosae of 'cerrado' and gallery forest in the Brazilian Federal District was examined. The most significant characteristics for taxonomic purposes were determined to be: delimitation between collapsed and non-collapsed phloem; phloem stratification; type and position of sieve plates; dilatation patterns; ar­ rangement and contents of sc1ereids; and presence of secretory cells. The bark data support the idea that Papilionoideae is the most advanced group of the Leguminosae. Key-words: Bark anatomy, cerrado, Leguminosae, phloem.

INTRODUCTION

Morphological and anatomical bark characteristics have been used for identification and evaluation of the taxonomic position of , e. g. Whitmore (1962), Teixeira et al. (1978), Roth (1981), Trockenbrodt & Parameswaran (1986), Richter (1990), Archer & Van Wyk (1993). There have been more anatomical studies of xylem than of bark because of the economic importance of xylem, its higher decay-resistance and its rela­ tive ease of preparation for anatomical observations. Most wood anatomists use the same terrninology (IAWA 1989), wh ich is not the case for the bark, in spite of the efforts of Esau (1969) and others. Roth (1981) suggested some terms, but her defini­ tions sometimes conflict with already existing ones. Trockenbrodt (1990) critically reviewed the terrninology used in bark anatomy. More recently, Junikka (1994) re­ vised terms used in macroscopical analysis of the bark. The outer bark functions as a thermal insulant that protects the cambium and con­ ducting tissue against high temperatures in forest fires, which is an important role in ecosystems such as the cerrado that are subjected to periodic burnings (MacieI1993). This paper presents an anatomical study of the bark of arborescent Leguminosae occurring in cerrado and in gallery forest of Brazil and aims to deterrnine which fea-

1) Area de Botänica Estrutural, Jardim Botänico do Rio de Janeiro, Rua Jardim Botänico, 1008, 22.460-000 Rio de Janeiro, RJ, Brazil. 2) Laborat6rio de Produtos Florestais, LPF / IBAMA, SAIN Av. L4 Lote 04, 70.818-900 Brasflia, DF, Brazil. 3) Instituto Brasileiro de Geografia e Estatfstica, IBGE, Rod. BR 251 Km 1, 70.000 Brasflia, DF, Brazil.

Downloaded from Brill.com10/04/2021 04:40:51AM via free access 386 IAWA Journal, Vol. 18 (4), 1997 tures are useful for identification. This family was chosen because of its variety in bark structure (Roth 1981) and for its economical importance. Leguminosae are conspicu­ ous in the cerrado and gallery forest, both in terms of species diversity as weIl as abundance of individuals (Kirkbride 1984).

MATERIALS AND METHODS

This investigation is based on material from the central region of Brazil. The Leguminosae species studied are listed below, arranged alphabeticaIly. The samples were obtained from the trunk of adult trees of 10 cm or more in diam­ eter, at a height of 1.0-1.3 m. Two sampIes from different individua1s were used when­ ever possib1e. After impregnation with glycol polyethylene (PEG, DP 1500) (Rupp 1964), the material was cut at a thickness of 10-12 11m and double stained with crysoi­ din/ acridin red and astra blue. Maceration of the phloem elements was obtained by a modification ofFranklin's method (Fedalto 1982). Histochemistry tests for lignin and phenolic compounds were made according to Johansen (1940) and Jensen (1962), re­ spectively. Crystals were observed in polarized light and specific tests were used to determine their chemical composition (Strasburger 1924). The G-layer in the gelati­ nous fibres was detected by chlorozinc iodine (Strasburger 1924) and polarized light. Periderm was observed in only some species studied, because it easily falls out in others. The terminology used in this work follows Trockenbrodt's (1990) recommenda­ tions.

List of studied species Each name is followed by subfamily, habitat, geographical origin, collection date and herbarium number. Acacia polyphylla A.DC.: , cerrado, Brasilia (DF) / Brazil, 01109/94, IBGE 32283 - gallery forest, Palmital (MG) / Brazil, 16/11194, IBGE 32474. - Acosmium dasycarpum (Vog.) Yakovl.: Papilionoideae, cerrado, Brasilia (DF) / Brazil, 16/11194, IBGE 32477. - Ana­ denanthera peregrina (L.) Speg.: Mimosoideae, cerrado, Brasilia (DF) / Brazil, 07/93, IBGE 32295 - gallery forest, Palmital (MG) / Brazil, 16/11194, IBGE 32469. - leiocarpa (Vog.) Macbr.: , gallery forest, Palmital (MG) / Brazil, 25/03/92, IBGE 29032 - gallery forest, Brasilia (DF) / Brazil, 01/09/94, IBGE 32478. - Bowdichia virgilioides Kunth: Papilionoideae, cerrado, Brasilia (DF) / Brazil, 07/93, IBGE 32296. - Centrolobium to­ mentosum Guilles ex Benth.: Papilionoideae, gallery forest, Brasilia (DF) / Brazil, 01109/94, IBGE Carp. 287. - Copaijera langsdorffii Desf.: Caesalpinioideae, gallery forest, Brasilia (DF) / Brazil, 07/93, IBGE 32293. - Dalbergia miscolobium Benth.: Papilionoideae, cerrado, Brasilia (DF) / Brazil, 23/06/94, IBGE 32287. - gardneriana Tu!.: Caesalpinioideae, gallery forest, Dian6polis (TO) / Brazil, 12/92, IBGE 29049. - Dimorphandra mollis Benth.: Caesalpinioideae, cerrado, Brasilia (DF) / Brazil, 07/91, IBGE 30218 - cerrado, Brasilia (DF) / Brazil, 16/11194, IBGE 32475. - Dipteryx alata Vog.: Papilionoideae, cerrado, Dian6polis (TO) / Brazil, 06/12/91, IBGE 28783 - cerrada, Sao Joao da Alian<;a (GO) / Brazil, 10/09/94, IBGE 32352. - Enterolobium contortisiliquum (VelI.) Morong.: Mimosoideae, cer­ rada / gallery forest, Brasilia (DF) / Brazil, 01/09/94, IBGE 32297. - Enterolobium gummijerum

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(Mart.) Macbr.: Mimosoideae, cerrado, Brasilia (DF) 1 Brazil, 16/11/94, IBGE 32470 - cerra­ do, Brasilia (DF) 1 Brazil, 16/11/94, IBGE 32461. - Erythrina verna Vell.: Papilionoideae, cerrado, Brasilia (DF) 1 Brazil, 01/91, IBGE 30101 - gallery forest, Brasilia (DF) 1 Brazil, 01/ 09/94, IBGE 32288. - Hymenaea courbaril L.: Caesalpinioideae, gallery forest, Brasilia (DF) 1 Brazil, 07/93, IBGE 32289. - Hymenaea stigonocarpa Mart. ex Hayne: Caesalpinioideae, cerrado, Brasilia (DF) 1 Brazil, 07/93, IBGE 32294. - Machaerium opacum Vog.: Papilionoideae, cerrado, Brasilia (DF) 1 Brazil, 12/91, IBGE 27153 - cerrado, Brasilia (DF) 1 Brazil, 16/11/94, IBGE 32473 - cerrado, Brasilia (DF) 1 Brazil, 16/11/94, IBGE 32471. -Mi­ mosa laticifera Rizzini & Mattos: Mimosoideae, cerrado, Dian6polis (TO) 1 Brazil, 01/92, w 1n. - Parkia platycephala Benth.: Mimosoideae, cerrado, Dian6polis (TO) 1Brazil, 03/12/91, IBGE 29079. - Plathymenia reticulata Benth.: Mimosoideae, cerrado, Brasilia (DF) 1 Brazil, 01/091 94, IBGE 32282. - Platymisciumfloribundum Vog.: Papilionoideae, gallery forest, Brasilia (DF) 1 Brazil, 01/09/94, IBGE 32284. - Platypodium elegans Vog.: Papilionoideae, gallery forest, Brasilia (DF) 1Brazil, 07/93, IBGE 32290. - Pterodon emarginatus Vog.: Papilionoideae, cerrado, Brasilia (DF) 1 Brazil, 16/11/94, IBGE 32472. - Sclerolobium aureum (Tu!.) Benth.: Caesalpinioideae, cerrado, Barreiros (DF) 1 Brazil, 12/91, IBGE 28985 - cerrado, Barreiros (DF) 1 Brazil, 02/92, IBGE 31323 - cerrado, Barreiros (DF) 1 Brazil, 07/93, IBGE 32291.­ Sclerolobium paniculatum var. rubiginosum (Mart. ex Tu!.) Benth.: Caesalpinioideae, gallery forest, Brasilia (DF) 1 Brazil, 12/1 0/92, IBGE 31134 - gallery forest, Brasilia (DF) 1 Brazil, 071 93, IBGE 32292. - Sclerolobium paniculatum var. subvelutinum Benth.: Caesalpinioideae, cerrado, Brasilia (DF) 1 Brazil, 06/94, IBGE 32285. - Slryphnodendron adstringens (Mart.) Covile: Mimosoideae, cerrado, Brasilia (DF) 1 Brazil, 23/06/94, IBGE 26999 - cerrado, Brasilia (DF) 1 Brazil, 23/06/94, IBGE 26107. - Vatairea macrocarpa (Benth.) Ducke: Papilionoideae, cerrado, Brasilia (DF) 1 Brazil, 16/11/94, IBGE 32476.

RESULTS

Usually the boundary between collapsed and non-collapsed phloem is gradual. A few species have a sharp dei imitation between the two regions, e. g. Acacia polyphylla, Co­ paifera langsdorffii, Dimorphandra mollis, Hymenaea courbaril and Mimosa laticifera. The phloem is usually storied in Papilionoideae (Fig. 1), and non-storied in Caesal­ pinioideae and in Mimosoideae. Among the Caesalpinioideae observed, only Apuleia leiocarpa has storied phloem (Fig. 2). In the majority of Papilionoideae, the conduc­ tive elements, parenchyma cells, fibres and secretory cells are organized in short tan­ gential bands and these bands present a radial pattern, demarcated laterally by phloem rays. Only one member ofPapilionoideae studied, Erythrina verna, presents very large bands ofthose elements (Fig. 3). Gelatinous fibres usually occur in the phloem (Fig. 3, 13, 14); generally they form larger bands in the collapsed phloem, whose walls often are flattened and impregnated by phenolic compounds. The sieve elements can occur isolated or in groups of 2-4 or more elements, in tangential, radial or crowded arrangement. The sieve elements in trans verse section have an irregular shape; in the Caesalpinioideae, they are 268-527 f.lIll in length and 20-37 /lm in diameter, in the Mimosoideae 228-420 f.lIll in length and 20-51 f.lIll in diameter, and in the Papilionoideae 153-304/lm in length and 18-42/lm in diameter (Table I). The Papilionoideae and one Caesalpinioideae, Apuleia leiocarpa, have sim­ ple sieve plates, horizontal or slightly inclined (Fig. 1, 2, 11); the other Caesalpinioideae

Downloaded from Brill.com10/04/2021 04:40:51AM via free access Table 1. Sieve elements; sieve plates; lateral sieve areas. I~ Subfamily Sieve elements Sieve plates Lateral sieve areas Species Length Diameter S es eR es/eR es/ Number areas Shape Dimension (flm) (flm) eR/eRD per plate Caesalpinioideae Apuleia leiocarpa 188 - 256 - 323 14-20-24 + elliptie large (14 J.Im) Copaijera langsdorffii 212 - 361- 494 23 - 35 -45 + + + 8 - 20 (or +) elliptic large (15 J.Im) Dimorphandra gardneriana 399 - 487 - 608 25 -35 -43 + + + 10 -18 eireular small ( 6 J.Im) D. mollis 371 - 527 - 616 22 -30- 38 + + + + 5 -20 eireular small ( 7 J.Im) Hymenaea courbaril 180 - 370 - 516 20-32 -43 + 2-6(+f3) elliptic large (19 J.Im) H. stigonocarpa 189 - 268 - 380 15 - 26 -43 + 2-6(+f3) elliptie large (13 J.Im) Sclerolobium aureum 227 - 380 - 544 19-28-37 + + + 8 - 18 eire./ ellip. small ( 5 J.Im) S. paniculatum var. rubiginosum 191 -342 -519 25 -37 -56 + + 8 - 30 (or +) elliptie small ( 7 J.Im) var. subvelutinum 254 - 424 - 568 20-30-41 + + 10-28 eireular small ( 5 J.Im) Mimosoideae Acacia polyphylla 224 - 298 - 375 17-27-34 + + + 8 - 12 elliptie large (14 J.Im) Anadenanthera peregrina 367 - 420 - 505 18-23-30 + + 6 -12 elliptie medium ( 9 J.Im) Enterolobium contortisiliquum 169 - 218 - 264 43 -51-91 + + + 10- 15 eire./ ellip. small ( 7 J.Im) E. gummiferum 237 - 349 - 483 21-34-45 + + + 7 -20 elliptic small ( 8 J.Im) Mimosa laticijera 181-238-296 19-28-33 + + + ±20 elliptie medium (11 J.Im) Parkia platycephala 271 - 375 - 494 24 - 31 - 38 + + 6 - 15 elliptie medium (11 J.Im) Plathymenia reticulata 308 - 369 - 508 10-20- 29 + + 14- 20 eireular small ( 7 J.Im) Stryphnodendron adstringens 248 - 313 - 358 19 - 28 - 37 + + 8 - 15 elliptie medium (20 J.Im) Papilionoideae

Downloaded fromBrill.com10/04/2021 04:40:51AM Acosmium dasycarpum 141 - 190 - 282 14 -18 - 24 + eireular small ( 5 J.Im) ~ Bowdichia virgilioides 195 - 264 - 310 14-24-35 + cireular small ( 6 J.Im) >' Centrolobium tomentosum 216 - 288 26 - 32 - 44 '-< 251- + eireu1ar small ( 6 J.Im) 0 Dalbergia miscolobium 154 - 219 - 273 26 -35 -44 + eire. / ellip. small ( 6 J.Im) c Dipteryx alata 159 - 216 - 266 19-25-34 + elliptie large (14 J.Im) a Erythrina verna 177 - 216 - 245 34 -42 -49 + elliptie medium (10 J.Im) ? Machaerium opacum 110 - 153 - 275 19-27-37 + eireular small ( 5 J.Im) ~ Platymiscium floribundum 160 - 227 - 287 20 -31- 45 + elliptie medium ( 9 J.Im) ~ Platypodium elegans 145 - 214 - 257 J.Im) ...... 15-26-35 + eireular small ( 5 00 Pterodon emarginatus 165 - 304 - 381 23-33-46 + eireular small ( 6 J.Im) Vatairea macrocarpa 169 - 268 - 343 20- 29 -41 + eire./ ellip. small ( 6 J.Im) ~ ...... S = simple; es = eompound sealariform; eR =eompound retieulate; eRD =eompound radiate; + =present; - =absent; f = more frequent. 'Ci via freeaccess 'Ci 03-08 J.Iffi(smalI); 09-13 J.Im (medium); > 14 J.Im(large). --l Costa, Rauber Coradin, Czarneski & Pereira - Bark of Leguminosae 389

Fig. 1-4. - 1: Machaerium opacum (tangential longitudinal section): storied phloem; simple sieve plates in slightly inclined walls (~); fused ray (white arrow). - 2: Apuleia leiocarpa (tan­ gentiallongitudinal section): storied phloem; simple sieve plates in slightly inclined walls (~); lateral sieve areas (*). - 3: Erythrina vema (transverse section): sieve elements in groups (0; fibres near cambial zone have thin and scantly lignified walls (~). - 4: Enterolobium gummiferum (tangential longitudinal section): sieve elements with compound sieve plates in inclined walls (~); lateral sieve areas (*). - Scale bar of Fig. 1 & 2 = 11 0 ~; of Fig. 3 & 4 = 55 ~.

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Fig. 5-8. - 5: Apuleia leiocarpa (radial longitudinal section): druses in square cells in the extremity of the ray (~); axial parenchyma cells with phenolic compounds (dark cells). - 6: Copaifera langsdorffii (radial longitudinal seetion): compound scalariform and reticulate sieve plates (~). - 7: Enterolobium gummiferum (transverse section): non-collapsed phloem showing simple sieve plates (-7). - 8: Mimosa laticifera (tangential longitudinal section): conspicuous secretory el­ liptic cells with phenolic compounds (thin arrow); axial strands of crystalliferous parenchyma (thicker arrow). - Scale bar of Fig. 5 & 6 = 110 f.lIIl; of Fig. 7 & 8 = 55 f.lIIl.

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Fig. 9-12. - 9: Dipteryx alata (transverse section): Fibre bands (white arrow) accompanied by sclereid groups (~) in collapsed phloem. - 10: Dalbergia miscolobium (trans verse section): groups of gelatinous fibres (~). -11: Dimorphandra mollis (transverse section): regular phellem showing tabular cells with thickened tangential walls (thin arrow); phelloderm cells (thicker arrow); cluster of sclereids in the periphery of cortical zone (*). - 12: Enterolobium con­ tortisiliquum (transverse section): phellem with layers oftabular cells (*) altemating with layers of thinner and taller cells with phenolic compounds (white arrow). - Scale bar of Fig. 9 & 11 = 110 JlIIl; of Fig. 10 & 12 = 55 JlIIl.

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and the Mimosoideae have compound and inc1ined sieve plates (Fig. 4, 9); sometimes in Hymenaea courbaril and Enterolobium gummiferum sieve elements have a com­ pound sieve plate in one end and a simple one in the other. Some sieve elements have a different pattern of sieve plates (Table 1). The number of sieve areas varies in differ­ ent species; Caesalpinioideae have up to 20 or more sieve areas in the sieve plates (Table I), with the exception of Hymenaea courbaril and Hymenaea stigonocarpa (Table 1) with 2-6 sieve areas. Lateral sieve areas (Fig. 4) occur in all studied species; they are large (more than 13 11m) in Caesalpinioideae; medium (8-13 11m) in Mimo­ soideae and small (3-8 11m) in Papilionoideae; the Papilionoideae can have lateral sieve areas in an alternate arrangement, forming double or simple rows; the lateral sieve areas are elliptic or circular and their arrangement is scalariform, straight or curved. The axial parenchyma can be diffuse or can occur near the sieve elements, or make up tangential bands, e.g. Apuleia leiocarpa and Sclerolobium aureum. When the axial parenchyma is adjacent to fibres, it is chambered and crystalliferous, forming long strands (30-35 cells); usually, the walls ofthes axial parenchyma cells have secondary thickenings and are lignified. The longest crystalliferous series (40-50 or more cells) occur in Acacia polyphyl/a, Copaifera langsdoiffii, Mimosa laticifera (Fig. 12) and Sclerolobium paniculatum var. subvelutinum. When axial parenchyma cells are adja­ cent to the rays, they also can be chambered and crystalliferous, e.g. Anadenanthera peregrina, Apuleia leiocarpa, Bowdichia virgilioides, Dimorphandra gardneriana, Dimorphandra mol/is, Erythrina verna, Machaerium opacum, Platypodium elegans and Vatairea macrocarpa. In this situation, chambered axial parenchyma cell walls are neither thickened nor lignified. In Acacia polyphylla, Apuleia leiocarpa, Mimosa laticifera, Sclerolobium paniculatum var. subvelutinum and Stryphnodendron adstrin­ gens, phenolic compounds abound. Starch grains occur in the axial parenchyma in the majority of the studied species. Phloem rays can be uniseriate or up to 5 cells wide; Erythrina verna is unusual as it has rays up to 14 cells. Most Papilionoideae have storied rays; among Caesalpinioideae only Apuleia leiocarpa has this character; storied rays are not observed in the Mimosoideae (Table 2). Fused rays (Fig. 1) frequently occur in the 3 subfamilies. The rays can be composed of only procumbent cells or square, upright and procumbent cells (Table 2; Fig. 8). Square and upright cells, when present, occur at the ray margins. Some species have crystals or phenolic compounds in the ray cells (Fig. 8). The dilatation growth is formed by proliferative and expansion tissues. The charac­ teristic parenchymatous wedges are conspicuous in Acacia polyphyl/a, Anadenanthera peregrina, Centrolobium tomentosum, Dimorphandra mollis, Enterolobium gummi­ ferum, Erythrina verna, Hymenaea courbaril, Sclerolobium aureum and Vatairea macrocarpa. In other species, e.g. Acosmium dasycarpum and Copaifera langsdoiffii, some rays remain unaltered while others have a moderate dilatation; in Copaifera langsdoiffii, extensive radial bands of sc1ereids also occur among the dilatated rays. In Parkia platycephala, Plathymenia reticulata and Stryphnodendron adstringens, the parenchyma dilatation appears to be a function of the cortical cells; in these species, the parenchymatous elements present irregular organization and are partitioned by

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Table 2. Characteristics of rays.

Subfamily Height Width Stratifi- Fused Constitution Species (firn) (no. cells) cation rays

Caesalpinioideae Apuleia leiocarpa 148 -177 - 205 2-3-4 + PC/UC Copaiferalangsdo1.fzi 156 - 291 - 422 1-3 + PCI SC/UC Dimorphandra gardneriana 170 - 271 - 364 1-3-4 + PC/UC D. mollis 214 - 335 - 534 1-2 + PC I SC I UC Hymenaea courbaril 115 - 246 - 386 1-4-6 PC/US H. stigonocarpa 184 - 308 - 393 1-3-5 PCI SC/UC Sclerolobium aureum 154 - 280 - 488 1-2-3 + PCI SC S. paniculatum var. rubiginosum 157 - 240 - 321 1 + PC var. subvelutinum 159 - 229 - 339 1-2 + PC Mimosoideae Acacia polyphylla 64-337 - 587 1-4-7 + PC Anadenanthera peregrina 274 - 389 - 554 2-5-6 PC Enterolobium contortisiliquum 158 - 214 - 281 1-2-3 + PC E. gummiferum 159 - 215 - 283 1-2-4 + PC Mimosa laticifera 113 - 158 - 229 1-2-3 + PC/SC Parkia platycephala 103 - 186 - 278 2-5-6 + PC Plathymenia reticulata 217-297-401 2-3-4 + PC/SC Stryphnodendron adstringens 117 - 164 - 258 1 PC/SC Papilionoideae Acosmium dasycarpum 146 -196 - 262 1-2-3 + PC/SC Bowdichia virgilioides 216 - 258 - 333 2-3-4 + + PCI SC Centrolobium tomentosum 139 - 209 - 247 1-2 + PC Dalbergia miscolobium 156 - 194 - 242 1-3 + + PC/UC Dipteryx alata 128 - 183 - 223 1-2-3 + + PCISC Erythrina verna 600-1085-1164 3 -9-14 PC Machaerium opacum 96-155 -284 1-2-3 + PC/UC Platymiscium floribundum 102 - 184 - 256 1-2 + PC Platypodium elegans 73 -146- 205 1 + PC Pterodon emarginatus 153 - 233 - 381 1-2 + + PC Vatairea macrocarpa 108 - 195 - 296 1-2 + + PCI SC/UC + = present; - = absent; I = irregular; PC = procurnbent cells; UC = upright cells; SC = square cells.

secondary walls at various orientations. In that region phenolic compounds usually occur as weIl as many sclereids. In Mimosa laticifera and in the majority of the Papilionoideae, successive periderms occur outside the collapsed phloem and the dila­ tation of rays is inconspicuous. In Centrolobium tomentosum, moreover, dilatation of rays is observed in addition to the successive periderms. Often the axial parenchyma cells of cortex are confused with ray dilatation cells and also with the elements of phelloderm. In the cortical region, phenolic compounds and clustered sclereids usually occur, sometimes forming tangential bands in the periphery of the cortex.

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Small groups of primary phloem fibres occur scattered in the collapsed phloem and in the cortex. Occasionally, these fibres are inserted between sclereids. Phloem secondary fibres are gelatinous. In transverse section, they usually occur in tangential bands, generally in groups of2-4 cells wide (Fig. 3). In Centrolobium tomen­ tosum, Erythrina verna, Pterodon emarginatus and Plathymenia reticulata, they can be up to 6 cells in width and up to 10 in Platypodium elegans. Generally, the fibre bands are accompanied by axial strands of crystalliferous parenchyma, but in Cen­ trolobium tomentosum and Dipteryx alata (Fig. 13), they are accompanied by sclereid groups. Usually the number of fibres is greater in the collapsed phloem and cortex. In Acosmium dasycarpum, the fibres are scanty and only occur in the collapsed phloem and cortex; in Apuleia leiocarpa, they are frequent in these regions and they are un­ usual in the non-collapsed phloem. Acacia polyphylla has abundant fibres throughout the whole bark. In Erythrina verna (Fig. 3) and Platypodium elegans, fibres were ob­ served with thin and scantily lignified walls, near the cambium. Sclereids with thickened and polylamellate walls and branched pits occur in most studied species, especially in the collapsed phloem, dilatation tissue and cortex. These sclereids are not observed in Machaerium opacum and Platypodium elegans. Often the sclereids have larger tangential diameters, particularly at the level of dilatation tissue and in the cortex. In trans verse seetion, the sclereids have circular or radial arrangement, as in Dimorphandra gardneriana and Sclerolobium aureum; in Apuleia leiocarpa and Hymenaea courbaril, sclereids occur in tangential groups. In Dimor­ phandra mollis, sclereids tend to form tangential bands in the periphery of the cortex, and in Copaifera langsdoiffii and Hymenaea stigonocarpa, they constitute extensive radial bands. In Erythrina verna, sclereids have scantily thickened walls; in this spe­ eies, they occur in small groups, scattered throughout the collapsed phloem and in the cortex or in thin radial bands in the peripheral cortical region. Small groups of sclereids are observed in Platymiscium floribundum. In Centrolobium tomentosum, they are scanty and occur in groups near fibres or in large groups in the dilatation tissue. In Acosmium dasycarpum, Dipteryx alata and Vatairea macrocarpa, sclereids occur in the collapsed phloem, near the crystalliferous parenchyma. Sclereids have large prismat­ ic crystals in Apuleia leiocarpa and Hymenaea courbaril and phenolic compounds in Sclerolobium aureum, Sclerolobium paniculatum var. rubiginosum and Sclerolobium paniculatum var. subvelutinum. Calcium oxalate crystals occur in several forms (prisms, druses or styloids) and sizes. They can be isolated or paired. Prisms and styloids are more frequent and occur in series ofaxial parenchyma, near the fibres and occasionally, near the sclereids. They can be present in a few short parenchyma strands near the rays in Anadenan­ thera peregrina, Erythrina verna, Machaerium acutifolium, Platypodium elegans and Vatairea macrocarpa. Druses occur in axial parenchyma near the rays or in the ray pa­ renchyma in Apuleia leiocarpa (Fig. 8), Bowdichia virgilioides, Dimorphandra gard­ neriana and Dimorphandra mol/iso Large prisms of calcium oxalate were observed in the sclereids in Apuleia leiocarpa, Copaifera langsdorffii and Hymenaea courbaril. Phenolic compounds usually are present in axial and ray parenchyma, in cortical cells and also in the dilatation tissue. These compounds are particularly abundant and

Downloaded from Brill.com10/04/2021 04:40:51AM via free access Costa, Rauber Coradin, Czarneski & Pereira - Bark of Legurninosae 395 their localization is sharply defined in several species. In Apuleia leiocarpa (Fig. 8) and Mimosa laticifera (Fig. 12), they occur in the axial parenchyma cells; in Acacia polyphylla and Stryphnodendron adstringens, they are present in the axial parenchyma, rays and cortex; in Sclerolobium aureum, Sclerolobium paniculatum var. rubiginosum and Sclerolobium paniculatum var. subvelutinum, they occur in the sclereids. Conspicuous secretory cells with abundant phenolic compounds occur in Apuleia leiocarpa, Centrolobium tomentosum, Dipteryx alata, Machaerium opacum, Mimosa laticifera (Fig. 12), Platypodium elegans, Pterodon emarginatus, Vatairea macrocar­ pa and Stryphnodendron adstringens. They are elliptic, long or short and thin-walled. In transverse section, they appear as clusters and in longitudinal direction they form more or less extensive rows. The length of secretory cells is equivalent to the sieve elements; they are longer in Caesalpinioideae and Mimosoideae and shorter in Papilionoideae. Periderm structure, when present, showed some differences. In Acosmium dasy­ carpum and Dimorphandra mollis (Fig. 15), the phelloderm has 4-5 celllayers in regular arrangement and the internallayers are similar to cortical cells; the phellern is very regular and has weakened zones of thin-walled cells alternating with zones of cells with thick tangential walls; clusters of sclereids can occur in the phellern. In Enterolobium contortisiliquum (Fig. 16), layers of tabular cells alternate with layers of thinner and taller cells with phenolic compounds. Dimorphandra gardneriana has pa­ renchymatic isodiametric cells with phenolic compounds, scattered into the phellern. In Anadenanthera peregrina and Bowdichia virgilioides, a variable number of succes­ sive periderms occur and they have included bands of cortical parenchyma. In Dalbergia miscolobium, Erythrina verna, Machaerium opacum, Plathymenia reticulata, Platy­ miscium jloribundum, Platypodium elegans, Stryphnodendron adstringens and Vatairea macrocarpa, there is collapsed phloem between the rows of successive periderms.

DISCUSSION

According to Esau (1977), the most primitive sieve elements are long, have inclined terminal walls and compound sieve plates with sieve areas that are similar to the lateral sieve areas, and the most advanced sieve elements have large simple sieve plates in transverse walls, and their lateral sieve areas present low specialization. In the material examined, the most advanced sieve elements occur in Papilionoideae and the least advanced ones occur in Caesalpinioideae and Mimosoideae. These observations sup­ port Metcalfe and Chalk (1950) who regarded the Papilionoideae as the most advanced group among Leguminosae. In the examined species of Caesalpinioideae and Mi­ mosoideae, sieve elements with compound sieve plates occur with scalariform, reticu­ late or radial patterns, as well as other sieve elements with two or three patterns in the same sieve plate. This more complex model is frequent among these subfamilies, but is not referred to in the consulted literature. Among the examined Papilionoideae, the sieve elements are shorter with simple sieve plates in transverse walls, and their lateral sieve areas are less specialized. Usually among Caesalpinioideae, the number of sieve areas per plate is large (50 or over), with the exception of Apuleia leiocarpa, which has

Downloaded from Brill.com10/04/2021 04:40:51AM via free access 396 IAWA Journal, Vol. 18 (4), 1997 simple sieve plates in transverse walls, and Hymenaea courbaril and Hymenaea stigonocarpa, which have only compound scalariform sieve plates with 3-6 lateral sieve areas per plate. Apuleia leiocarpa, on the other hand, has large and conspicuous lateral sieve areas that represent a primitive character (Esau 1977). Storied phloem is another advanced feature also observed among most of the stud­ ied Papilionoideae. However, in Erythrina verna, only the sieve elements and axial parenchyma are storied, while the rays are non-storied, because of their height. In Va­ tairea macrocarpa, there is a great number of fused rays, so the storied structure is less evident. Apuleia leiocarpa is unique among the studied Caesalpinioideae in having storied phloem. Metcalfe and Chalk (1950) described the occurrence of storied phloem in some genera of this subfamily. The boundary between non-collapsed and collapsed phloem is sharply defined in a few species, e.g. Acacia polyphylla, Copaifera langsdoiffii, Dimorphandra mollis, Hy­ menaea courbaril and Mimosa laticifera, although this feature was not mentioned in the consulted literature. Metcalfe & Chalk (1950) state that the rays seem highly specialized in the Mi­ mosoideae, while in Caesalpinioideae and Papilionoideae, there are species with spe­ cialized rays and others with less specialized ones. The presence of storied rays in Apuleia leiocarpa confirms the report of Metcalfe and Chalk (1950) who mentioned storied rays in some Caesalpinioideae genera. There is a predominance of narrow rays (1-3 and 1-4 cells wide) among Caesal­ pinioideae species, except in Hymenaea courbaril and Hymenaea stigonocarpa that have wider rays (3-6 cells); Papilionoideae species, confirming Roth's (1977) obser­ vations, have rays with 1-2 cells wide, except in Erythrina verna, whose rays are very taU and wide (up to 14 ceUs). Mauseth (1988) states that the circumferential expansion of the bark results from dilatation tissue formation that can be originated by division ofaxial parenchyma or ray cells, and that often the cells that resurne division are mixed with others that do not divide. Esau (1977) also associates ray enlargement with the increase ofaxis thick­ ness. In some species, e.g. Sclerolobium aureum, the rays dilatation is evident, while in other species this feature is not c1early observed. In the latter cases, rays are scat­ tered and become intermixed with the cortical parenchyma cells that are divided into several planes to adjust to radial enlargement of the axis. Certain species are character­ ized by an abundance of phenolic compounds, arrangement of sc1ereids and presence of gelatinous fibres in dilatation tissue. Esau (1964) pointed out that sc1erenchymatous cells are characteristic of secondary phloem. Fibres and sc1ereids are frequent in the species examined, an observation that confirms references by Roth (1987b) and Metcalfe & Chalk (1950) about the family. Usually, there is a greater number of fibres in collapsed phloem. Certain species can be characterized by abundance or scarcity of fibres. These elements are less frequent in Acosmium dasycarpum, where they occur only in the coUapsed phloem and cortex; in Apuleia leiocarpa and Enterolobium gummiferum, fibres are scanty and almost ab­ sent.

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The G-layer that characterizes the gelatinous fibres was confirmed in the material examined, by histochemical tests and polarized light. Gelatinous fibres have been as­ sociated with tension wood (Milanez & Miranda Bastos 1960). Metcalfe and Chalk (1950) refer to the presence of fibres with occasional mucilaginous layers in species of Papilionoideae. It is not known whether the occurrence of gelatinous fibres in cerrado and gallery forest is the result of tension forces or whether they might represent an adaptation to seasonal dry periods. Roth (1987b) discussed a common relationship between secondary formation of sclereids and dilatation tissue. In the analysed species, we postulate that sclereids were originated by redifferentiation and division of parenchyma cells. This assumption is based on the most common localization of sclereids - dilatation tissue and cortex - and their morphological characteristics. Sclereids in this material are generally isodiametric or elongated. Roth (1969) drew attention to the fact that sclereids and fibres in the phloem consti­ tute an important aid to species determination. Among the legume species studied, the form, arrangement and cell content can contribute to species characterization. Sclereids occur in more or less circular groups in Dimorphandra gardneriana and Sclerolobium aureum, in tangential arrangement in Apuleia leiocarpa and Hymenaea courbaril; in Dimorphandra mollis, this arrangement forms extensive radial bands in the periphery. Sclereids in Apuleia leiocarpa and Hymenaea courbaril have large prismatic crystals; in Hymenaea stigonocarpa, Sclerolobium aureum, S. paniculatum var. rubiginosum and S. paniculatum var. subvelutinum, they contain phenolic compounds. According to Metcalfe and Chalk (1950), clustered crystals distinguish Cae­ salpinioideae from Mimosoideae and Papilionoideae. However, Roth (1987b) did not observe these forms of crystals among Caesalpinioideae. In the species of Caesalpin­ ioideae, analysed here, clustered crystals (druses) were seen in Dimorphandra gardneri­ ana and Dimorphandra mollis. Prismatic crystals, isolated or juxtaposed were always present in the analysed species; they occured in chambered cells ofaxial parenchyma near the fibres or sclereids. Clustered crystals were not observed in the Papilionoideae, although Roth (1987b) had observed these forms in the bark of some species of this subfamily. Axial strands of crystalliferous parenchyma were particularly long in Aca­ cia polyphylla, Copaijera langsdorffii and Sclerolobium paniculatum var. subvelutinum. Large crystals were present in sclereids in Apuleia leiocarpa and Hymenaea courbaril, while small crystals occured in chambered cells ofaxial parenchyma, near the rays, in Machaerium opacum, Platypodium elegans and Vatairea macrocarpa. Milanez (1932) mentions the occurrence of crystals only in the parenchymatous cells of the xylem in the majority of leguminous species. This author suggests that calcium oxalate makes the cellular walls thicker. It is confirmed in the present study, where idioblasts of calcium oxalate have thick cellular walls. However, thicker walls were observed in parenchyma strands near sclerified elements, but not in the cells near the rays. Van Wyk (1985) described thickening and lignification of crystalliferous cell walls near phloem fibres in Acacia senegal (L.) Will., but did not for the phloem of Myrtaceae species.

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Metealfe and Chalk (1950) mention the variable loealization of seeretory eells in the phloem of leguminous genera and reeord the presenee of indeterminate eontents in Mimosa speeies and phenolie eompounds in the other genera. The presenee of phe­ nolie eontent here was observed in the speeies that have seeretory eells. The form and size of these seeretory eells varies in several speeies, but generally they have the form and size of adjaeent eells. Aeeording to Roth (1977, 1987 a, b), periderm ean be useful in ; however, in the present study it was not possible draw eonclusions about the taxonomie value of periderm strueture. There is a great struetural variability in periderm eonstitution in the studied speeies. Sclereids were observed seattered in groups among phellern ele­ ments (Acosmium dasycarpum and Dimorphandra mollis) or eells with phenolie eom­ pounds (Dimorphandra gardneriana). In other speeies (Anadenanthera peregrina, Bow­ dichia virgilioides, Dalbergia miscolobium, Machaerium opacum, Plathymenia retic­ ulata, Platymisciumfloribundum, Platypodium elegans, Stryphnodendron adstringens and Vatairea macrocarpa), included bands of eortical parenehyma or eollapsed phloem were observed among sequential periderms. In these eases, there is an authentie rhytidome, as pointed out by Metealfe & Chalk (1950) for some speeies of the family. The results of this study show that some anatomieal eharaeteristies of bark ean be useful for taxonomie purposes. The most important features are delimitation between eollapsed and non-eollapsed phloem; phloem stratifieation; type and position of sieve plates; dilatation patterns; arrangement and eontents of sclereids; presenee of seere­ tory eells; and oeeurrenee of sequential periderms. We did not observe any differenees between bark anatomy of eerrado and gallery forest speeimens.

ACKNOWLEDGEMENTS

The authors would like to express their appreciation to the National Council for the Scientific and Technological Development - CNPq, for its support; to Dr. Haroldo C. de Lima for the botanical determination; to Dr. Roberta Cunha de Mendona, curator of IBGE herbarium, for logistic aid; to Dr. Raul D. Machado and Prof. Osnir Marquete for their efficient aid in the preparation of photographs; to the technicians Eudmar Curado Lopes for slides preparation and Diacis Alvarenga for his assistance in collecting material; to the Forest Engineer Daniela de Oliveira e Silva, for efficient collaboration.

REFERENCES

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