Neerl. December 481-493 Acta Bot. 25(6), 1976, p.
The secondary phloem of some
Combretaceae and the systematic
position of Strephonema pseudocola
A. Chev.
R.W. den Outer and J.M. Fundter
Botanisch Laboratorium, Wageningen
SUMMARY
The anatomy of the secondary phloem of Strephonema pseudocola A, Chev. has been com- pared with that of some other representatives of the Combretaceae originating from the
Ivory Coast, Africa, This is done because there exist different opinions about the systematic
of the Also the anatomical wood of the concerned position genus. properties species were
investigated and the results compared with those found by others. Although Strephonema pseudocola differs fundamentally from the rest of the family, the anatomy of the secondary
the in phloem, may be more so than that ofthe secondary xylem, leads us to retain genus the
Combretaceae, but as a distinctly separate subfamily. By its bark and anatomical wood
the has claim be ancestral in the Combretaceae. characters, genus some to an type
1. INTRODUCTION
based The tribal and generic classification of the Combretaceae is on Engler and & Diels (1899), as modifiedby Exell (1931) Exell& Stage (1966). In this
system the family is divided into two subfamilies Strephonematoideae, con-
and of four taining a single genus Strephonema, Combretoideae, consisting
tribes:
Combreteae with the Combretum, Pteleopsis, Quisqualis, Guiera genera , Thiloa and Calopyxis;
Terminalieae with the genera Terminalia, Bucida, Buchenavia, Ramatuella,
Conocarpus and Anogeissus ;
with the and Calycopterideae genus Calycopteris
Lagucularieae with the genera Laguncularia, Lumnitzera and Macropteran-
thes.
There are about 500 species in the family. The classification is based upon morphological characters of the flowers, fruits and vegetative shoot. The
geographical range of each genus is stated; all the species belonging to the
Combretaceae are tropical or only in a few cases subtropical.
However, the family is a natural and well-definedtaxon (Exell 1954, Ver-
if exclude with hoeven & van der SCRUFF 1973), only we Strephonema five
species in tropical West-Africa, all trees or shrubs. The genus Strephonema
differs from the rest of the family in its semi-inferiorovary, and was originally placed in the Lythraceae and later in several other families. Other unique 482 R. W. DEN OUTER and J. M. FUNDTER
features of this genus are its revolute domatia, characteristic pattern of epi-
dermal cells, paracytic subsidiary cells and two-armed hairs, none of which is found elsewhere in the family (Stage 1965). Of great importance (Stage 1965)
however, is the possession of typical Combretaceous one-armed compart-
mented hairs by at least two of the five Strephonema species. The two-armed
hairs of theremaining species can easily be visualized as derivatives of the one-
but armed type. This indicates the affinity of this genus with the Combretaceae,
because of the above mentioned other unique features only as a separate sub-
& for family (Stage 1965, Exell Stage 1966). It was not quite possible Liben
(1965) to investigate Strephonema in detail, because the amount of herbarium
material at his disposal was minute. Also the possibility is not excluded that
scattered other material was amongst families, as Strephonema possesses large,
fleshy fruits which do not resemble in any way the typical winged fruits of
the other of the genera family (Liben 1965).
The wood anatomy of Strephonema pseudocola A. Chev. has been compared
with the known members of the Lythraceae and the Combretaceae by Ven-
kateswarlu & Prakasa Rao (1970). This comparison shows that the species
has little in common with the Lythraceae, but certain xylotomical features
point to a relationship between Strephonema and a few of the Combretaceae
taxa. Nevertheless the distinctiveness of the wood structures merit separation
of Strephonema from the Combretaceae into a separate monogeneric family,
the Strephonemataceae. This family is to be considered allied to Combreta-
& So the either ceae (Venkateswarlu Prakasa Rao 1970). genus might con-
stitute a distinct family or belongs to a subfamily of the Combretaceae. This
possibility is to be tested using new evidence. A small piece of new evidence is
found in the comparison of the secondary phloem of Strephonema pseudocola
A. Chev. with that of some other representatives of Combretaceae. The secon-
dary xylem was also investigated and theresults compared with those of Ven-
kateswarlu & Prakasa Rao (1970).
2. MATERIAL AND METHODS
Bark and wood samples used are from the Versteegh and den Outer collection,
Ivory Coast, West-Africa (1969). The collection is housed at the Department
of Botany, Agricultural University, Wageningen, The Netherlands. All materi-
al studied had been vouched. The those of samples, except climbers, were
collected from stems at breast height and immediately fixed in FAA.
Anatomical features were studied in transverse, radial and tangential sec-
tions and macerations. All sections were embeddedin Kaiser’s gelatin-glycerin
(Johansen 1940). Means and ranges of length of sieve-tube members, vessel-
members, fibrous elements and the radial vessel diameter are based on at least
individual made with twenty measurements. Measurements were the help of a
Wild M20 light-microscope. For our research in tropical wood species we have
used the definitionof tracheids and libriform fibres given by Moll& Jansso-
nius (1906-1936), Janssonius (1940) and Reinders (1935). The ray type desig- THE SECONDARY PHLOEM OF SOME COMBRETACEAE 483
nations employed here are those of Kribs (1935); the sieve tube-, sieve area- and companion cell-types were classified according to Zahur (1959).
3. RESULTS
The results of the comparison of the secondary phloem of Strephonema pseu- docola A. Chev. with that of some other representatives of the Combretaceae,
the are given in following three tables: table I, information on sieve tubes; table 2, information on companion cells and mechanical tissue; table 3, infor- mation on phloem parenchyma and phloem rays.
Fig. 1-6. Combretaceae. Drawings of transverse sections of the conducting secondary phloem near the cambium.
Legends /igs. 1-6 and tables 1-3.
+ = present
= - absent bast type: 4mr = orderly sequence in four, multiseriate, regular: PhF
(CrC)-PC-ST-PC-PhF (CrC)
4mi in PhF = orderly sequence four, multiseriate, irregular; (CrC)-PC-ST-PC.... PhF (CrC)....
in 3mi = orderly sequence three, multiseriate, irregular: PhF
(CrC) - PC-ST.... PhF(CrC)....
s = sieve tubes scattered
= sieve tubes in g groups
CA = cambium
CC = companion cell
Cli = climber
companion-cell type classified according to the method of Zahur (1959):
A = the companion cells are much shorter than the sieve-
tube elementsand usually occur singly
B = the companion cells are as long as the sieve-tube ele-
ments they accompany
C = the companion cells are as long as the sieve-tube ele-
but ments, are septated to forma strand of cells so that
more than one companion cell accompanies each sieve-
tube member
CrC = crystalliferous cell
CSCL = contact sclereid
dbh = diameter at breast height
Int = intercellular space
L = libriform fibre
obi.; s. = sieve plate oblique, simple
PC = parenchyma cell 484 R. W. DEN OUTER and J, M. FUNDTER
PhF = phloem fibre phloem-ray type, classified according to the method of Kribs (1935):
He = heterogeneous phloem rays; procumbent and upright
cells are present
Ho = homogeneous phloem rays; only procumbent or only
upright cells are present
I = uniseriate rays and multiseriaterays with long uniseriate
tails
II = uniserate rays and multiseriaterays with short uniseriate
tails
III = only uniseriaterays arepresent
PhR = phloem ray
PhRPC = phloem-ray parenchyma cell
SCL = sclereid
sieve-area type, classified according to the method of Zahur (1959):
small rather sieve Iltg = a number, poorly developed areas on
the side walls, unequally spaced or diffuse. Sieve areas
mostly on tangential walls
III = sieve areas on the side walls entirely absent or obscure
sieve-tube type, classified according to the method of Zahur (1959):
sieve tubes with I = are essentially long (>500 /im), very
oblique sieve plates with 10 or more sieve areas. When
sieve is the numberof areas extremely variable, or when
the sieve the areas are very closely placed, plate length
and the angle of inclinationwere relied upon as defining
features
II = intermediatebetween types I and III
= sieve III tubes are short (100-300 /un), with slightly oblique
to transverse, simple sieve plates
ST = sieve tube
T = tracheid
V = wood vessel vert.; comp.
15-20 s.a. = sieve plate almost vertical, compound, with 15-20
closely placed sieve areas
V O number = number of the bark sample and corresponding her-
barium materialofthe Versteegh and den Outer collec-
tion, Ivory Coast, West-Africa, 1969
WR = wood ray
cell WRPC = wood-ray parenchyma THE SECONDARY PHLOEM OF SOME COMBRETACEAE 485
mi). mr-4
4 (bast-type
Don
G. grandiflorum Combretum
2.
Fig.
mr).
4 (bast-type
L. catappa Terminalia
1.
Fig. 486 R. W. DEN OUTER and J. M. FUNDTER
mi)
3 (bast-type
Don
G smeathmannii
cf. Combretum
4. Fig.
mi)
4 (bast-type
Perr,
et Guill.
(DC.) leiocarpus Anogeissus
3.
Fig. THE SECONDARY PHLOEM OF SOME COMBRETACEAE 487
g) (bast-type
L. indica Quisqualis
6. Fig.
mi)
3 (bast-type
Chev.
A. pseudocola Strephonema
5. Fig. 488 R. W, DEN OUTER and J. M. FUNDTER
g g g tgt tgt tgt tg
type sieve area + + + + + + + + + + + 111 iiII + + + + + + + iiII iiII iiII + /imlllpm on of wallswalls tube areas side sieve horizontal diameter sieve sieve sieve thethe 35 — - — - - — — - - 15 12 12 -
s.a. sievesieve ± comp. s.a. obi.; average member lengthlength pm 535 290 245 390 390 230 130 190 340 275 335 205 405 360 375 350 type III-II III-II type III111 III111 111-II 111-II III111 III111 III111 111 III111 III111 III111 II III111 I II II11 II 4mr-4mi bast- type 3mi 4mi 4mi 4mi 4mi s-g 4mi 3mi 4mi 4mr 4mi 4mi 4mi s g 30 60 5 30 and and and 2 25, and 3, dbh cmcm 20 4,3, and 30,25, 100 25 25 3 3 10 3 3 3 25 30, 20 30 - - 3- - 6- 7- - 4,- - - - 808 427 528 422 O and and and (Cli) (Cli) 374 560 (Cli) (Cli) (Cli) 310, 512 + 300,310,422 number 525 115,115,374 103 189 V 667 357 363 733 204 529 467 and 220 769 300, and 617 244 Don ex Chev. Engl, Don G. Diels Kotschy ex (Welw.) G. Lepr. (Welw.) et A. Diels Lepr. Planch, Chev. et (DC.) Lepr. cola elliottii nigricans A, Engl, smealhmannii L. Aubrev. nigricans Dalz. smeathmannii L. pseudo leiocarpus binderianum dolichopetalum grandiflorum hypopilinum nigricans var. var. platypterum leiocarpus M. spec. glaucescens studied Perr. cf. cf. indica catappa ivorensis superba Perr. Diels) J. et Perr. et et 1 et et Guill. Diels Benth. Table Specimens Strephonema Anogeissus Combretum Combretum Combretum Combretum Combretum Guill. (Engl, Combretum Guill. Combretum Hutch, Combretum Combretum Quisqualis Terminalia Terminalia Terminalia Terminalia et Guill. et ex THE SECONDARY PHLOEM OF SOME COMBRETACEAE 489 number per strand cells averageaverage crystal >12 of cell 30 1515 2222 30 18 24 >l2 17 30 3232 36 2121 25 20 22 20 of cell pm averageaverage length crystalcrystal strand 610 400 380 610 500 435 ? 230 480480 375375 465 375375 495 420 435 550 tissue cell • mechanical stone + + + - + + + + _ + - - - - pm average fibre- sclereid length 10201020 580580 725 930 — - - - + + - average length fibre pmfim — - 2030 - - 2030 14501450 1015 10151015 2030 1115 1160 1510 wall wall of ------cell in tube tg. rd. cell wall wall wall to to place comer sieve + + + + + + rd. rd. + + + rd. + + + + companion type type C + + + + + + + + + + + + + + + + Don ex Chev. Engl,Engl. Don G. Diels Kotschy ex G. Diels Lepr. (Welw.) et A. Planch,Planch. Chev. (DC.)(DC.) Lepr. Chev. nigricans A. Engl, elliottii smeathmannii L. Aubrev. nigricans Dalz. L.L. pseudocola leiocarpus binderianum dolichopetalum grandiflorum hypopilinum nigricans var. var. platypterum M. spec.spec. glaucescens studied cf. cf. indica catappa ivorensis superba Perr. Perr. Diels) Perr. J. tumturn et et 2 et et et Diels Benth.Benth. Table Specimens Strephonema AnogeissusAnogeissus Guill. CombretumComhretum Combre Combretum CombretumComhretum Combretum Guill. (Engl, Combretum Combretum Hutch, CombretumComhretum Combretum QuisqualisQuisqualis Terminalia Terminalia TerminaliaTerminalia Terminalia etet (Engl, Guill. ex 490 R. W. DEN OUTER and J. M. FUNDTER upright upright layers upright are seldom are are crystals tg. seldom seldom areare crystals seldom are seldom in cells cells cells are cells are are cells are ray large cells ray ray cells rayray cells cells ray cells most many stone ray ray mostmost most ray most ray 3-seriate most 2-seriate 3-seriate; 2-seriate; uniseriate; 2-seriate; 2-seriate uniseriate; uniseriate; uniseriate; 2-seriate; 2-seriate;2-seriate; uniseriate 2-seriate; 2-seriate uniseriate oftenoften 3-seriate 3-seriate; mostly seldom seldom mostly seldom seldom mostly mostly mostly seldom seldomseldom mostly rather often often seldom information 3-seriate, 3-seriate, 3-seriate, ray 3-seriate, 2-seriate, 2-seriate, 2-seriate, 2-seriate, 3-seriate, 2-seriate, 2-seriate, 2-seriate, 2-seriate,2-seriate, 3-seriate, 4-seriate,4-seriate, 4-seriate, 4-seriate, 2-seriate, < < procumbent < < < < < procumbent < procumbent < < < < < procumbent phloem further rays rays upright rays rays upright rays rays rays rays rays raysrays raysrays rays raysrays rays rays rays II- III111 III111 III111 III111 III II 111III II- I I 111 II II II- II I I I I I II II type He He HoHoi He He He HeHe He HeHe HoHoi Ho He He He He He Ho Ho of per average number cells strandstrand 6 parenchyma 8 6 5 5 5 4 4 5 4 5 6 4 5 6 6 6 of phloem cell average lengthlength strand pmpm 610 380 330 520 465 375375 230 205 425425 375 375375 390 405 440 495 375 Don ex Chev. Don G. Diels Engl, ex Kotschy G. (Welw.) Diels Lepr. et A. Planch,Planch, Chev. (DC.) Lepr. elliottii nigricans A, L. Engl, Aubrev. nigricans Dalz. smeathmannii L. pseudocolapseudocola binderianum dolichopetalum grandiflorum hypopilinum nigricans var. var. platypterumplatypterum leiocarpus M. glaucescens ivorensis studied cf. cf. spec.spec. indica catappa ivorensis superba Perr. Perr. Diels) Perr. J. et et et 3 et et et Diels Benth. Table Specimens Strephonema Anogeissus Guill. Combretum Combretum Combretum Combretum Combretum Guill. (Engl, Combretum Guill. CombretumCombretum Hutch, CombretumCombretum CombretumCombretum Quisqualis TerminaliaTerminalia Terminalia Terminalia Terminalia et ex THE SECONDARY PHLOEM OF SOME COMBRETACEAE 491 The structure of the conducting secondary phloem near the cambiumof Stre- phonema pseudocola provides an image which fits quite well within the varia- tion of bast types as they occur in the investigated species of the family (fig. 1-6). Yet Strephonema pseudocola is the only species possessing sieve-tube members of type I (Zahur 1959). They are much longer than thoseof the other species, while the almost vertical sieve plates are compound, with more than ten sieve areas. Moreover, the sieve areas in the side walls are clearly visible and large. The companion cells tend to occur against the tangential walls of the sieve-tube member, besides the more general position in the corners. The crystalliferous parenchyma strands and the parenchyma strands are long with many cells per strand. Yet the last phenomenon is also present in Combretum Diels. The of dolichopetalum Engl, et phloem rays Strephonema pseudocola are in general 2-seriate, whereas those of the other species mostly uniseriate or 3-seriate ( Terminalia). We also compared the wood anatomical properties of the species listed in table 1. It appears that Strephonema pseudocola differs from theother investigated species in the following characteristic features: the ground tissue consists of tracheids, at least the percentage of tracheids is much than in the other very higher species; the wood rays are exclusively heterogeneous, while homogeneous rays often occur in the other species; the number of vessels per square mm in small compared with most other spe- cies, except with those of Combretum dolichopetalum Engl, et Diels and Ter- minalia superba Engl, et Diels. 4. DISCUSSION The anatomical wood evidence used by Venkateswarlu & Prakasa Rao (1970), to place Strephonema pseudocola A. Chev. in a newly constituted mono- is generic family, the Strephonemataceae, not entirely convincing to us. Although the values of their measurements are somewhat higher in general other The differences in number of vessels than ours, there are points. per between and square mm Lumnitzera, Laguncularia Macropteranthes and the other investigated genera found by the above mentioned authors, are much than those between and the The greater Strephonema same remaining genera. cross-sectional diameters of vessel elements of 330-400 /mi for Strephonema much than the values of 50-160 measured The last values are greater pm by us. fit quite well within therange of the other diameters found. On the other hand Venkateswarlu and Prakasa Rao emphasized the importance of the length of the vessel elements. These elements, like the fibrous elements of the ground tissue of the secondary xylem, of Strephonema are long, distinctly separated from the other Combretacean taxa with perhaps the exception of Pteleopsis and Ramatuella. But also important is the fact, mentionedby us, that Strepho- is in the of tissue nema pseudocola possession a ground mainly composed of tracheids, whereas all the other specimens possess libriform fibres. Bark be used wood anatomy can complementary to anatomical criteria 492 R. W. DEN OUTER and J. M. FUNDTER (Thorenaar 1925; Lawton & Lawton 1971; Lawton 1972; Parameswaren & Liesse 1968, 1974). Strephonema pseudocola differs clearly from the other of sieve-tube members. Like all genera investigated by the possession type I the elements of the axial system, these sieve-tube members are longer than those of the other Furthermore the cells often genera. companion are quite placed against the tangential walls of the sieve-tube member. Also these com- panion cells, septated to form a strand of cells, are not as long as the sieve-tube members but often shorter. So a tendency towards Zahur’s (1954) type A can benoticed. The arrangement and types of the elements of the secondary phloem of Strephonema pseudocola on the other hand, are clearly characteristic for the Combretaceae. For instance the frequently present druses, the orderly se- of elements and the small width of the Moller’s features quence rays. (1882) for the secondary phloem of the Combretaceae such as phloem rays not wider than 2-seriate; short, wide sieve-tube members with simple sieve plates, some- times compound with a few sieve areas, will not do for Strephonema but neither for Terminalia.But of course, one has to bear in mindthat we only investigated species of about twenty percent of the genera belonging to the family. The bark and wood anatomical characteristics all plead for a more primitive, less specialized status of Strephonema compared with the other investigated genera of the family (Zahur 1959, den Outer 1967, Carlquist 1975). Also its semi-inferior the has claim be ancestral only by ovary genus some to an type in the Combretaceae(Exell & Stage, 1966). So the anatomyof the secon- of be dary phloem Strephonema pseudocola, may more than that of the secon- leads retain the in the but dary xylem, us to genus Combretaceae, as a distinctly detach the from the of the separate subfamily. To genus rest Combretacean taxa and place it in a newly constituted monogeneric family as suggested by Venkateswarlu & Prakasa Rao (1970), does not seem entirely justified. ACKNOWLEDGEMENTS Our sincere thanks for Mrs. I. vanTouw-Koeten, who prepared most of the slides used for this Furthermore Prof, Willemse, who study. we are most grateful to Dr. M. T. M. critically read the manuscript and to Mrs. T. Peterkamp-Kuijt who typed it. REFERENCES Carlquist, S. (1975). Ecological strategies of xylem evolution. Un. California Press, Ber- keley, Los Angeles and London, Engler, A. and L. Diels (1899). 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