Takhtajan Armen. Flowering Plants

Подождите немного. Документ загружается.

Superorder RUTANAE 393

4 Small trees and shrubs with very long axillary

spines and bitter bark. Leaves alternate, leathery,

petiolate, 2-foliolate, leaﬂ ets coriaceous, entire;

stipules absent. Stomata anomocytic. Flowers in

axillary 3–9-ﬂ owered racemose inﬂ orescences,

small, greenish-yellow, bisexual, actinomorphic,

usually 5-merous. Sepals free, imbricate, cadu-

cous. Petals free, narrow oblong, spreading, imbri-

cate. Stamens usually ten, inserted in the grooves

below the outside of the nectary disc; ﬁ laments

free, ﬁ liform; anthers dorsiﬁ xed, introrse. Pollen

grains usually 2-cellular, 3-colporate or 6-rugo-

rate. Nectary disc intrastaminal, thick, shortly

cupular or cushion-shaped, 10-grooved.

Gynoecium of ﬁ ve carpels, with very short, subu-

late style; stigma minute; ovary usually partly

immersed in the disc, 5-locular, with one anatro-

pous ovule per locule, pendulous from the axis

below the apex of the loculi; micropyle zig-zag.

Endothelium present. Fruits 1-seeded drupes with

very thick, bony, 5-angled, 1 locular endocarp sur-

rounded by oily mesocarp. Seeds with subﬁ brous

testa, seed-coat consists of isodiametrical paren-

chyma cells with scattered ligniﬁ ed sclerenchyma

elements, green embryo; endosperm wanting,

n = 9.. . . . . . . . . . . . . . . . . . . . . 2. balanitaceae.

4 Small succulent annual herbs. Fibers with rare

simple pits. Leaves with two minute, lateral, color-

less outgrowths at the base; two lowest pairs of

leaves of the basal rosette opposite, decussate,

entire, spatulate, cauline ones alternate, usually

slightly dissected, often with two basal, earlike

lobes, the uppermost ones entire; stipules minute.

Flowers very small, subsessile in the axils of the

basal leaﬂ ike bracts, forming a scorpioid terminal

inﬂ orescence, bisexual, actinomorphic, 4-merous

or rarely 3-merous. Sepals basally connate, imbri-

cate, persistent. Petals free, very shortly clawed,

imbricate, persistent. Stamens attached to the

intrastaminal, annular, slightly lobed nectary disc;

ﬁ laments free, long, slender; anthers subglobose.

Microsporogenesis simultaneous. Pollen grains

3- colporate, with striate ornamentation. Gynoecium

of four carpels alternating with the sepals; style

simple, arising from the apical depression of the

ovary; stigma clavate, 4-sulcate, with four short,

decurrent, double series of papillae; ovary superior,

on very short obconic gynophore, slightly 4-lobed,

4-locular; each locule contains 6 ovules hanging

on the 6-branched free placentas attached to the

center and directed toward the dorsal sides of the

ovary; 4 branches of each placenta are situated

along the median line of the locule and bear four

ovules, each of the two other branches is directed

to the lateral locelli and bears one ovule close to

the ovary wall. During the fruit development two

lateral ovules of each placenta become included in

the tissues of the ovary wall that completely frame

the developing seed; as a result, the developing

seed turns out to be completely within an endo-

carplike chamber connected with the middle cham-

ber by a squeezed oriﬁ ce; thus four ovules of each

locule are in the middle chamber and two other

ovules are in the lateral one. Ovules hemitropous,

bitegmic, crassinucellate; the outer integument

contains speciﬁ c cells that accumulate mucilage.

Endothelium absent. Female gametophyte of

Polygonum-type. Endosperm nuclear. The fruit is

at ﬁ rst ﬂ eshy and red but after maturing becomes

dry, capsulelike; it is of very unique structure,

dehiscence, and seed dispersal. At ﬁ rst it is opening

loculicidally and discharges four seeds of the mid-

dle chamber while the lateral seeds are still in their

chambers; the discharge of the lateral seeds of each

locule takes place at the later stage of the ripening

of the fruit; dehiscence of the lateral chambers

occurs as a result of a mechanical rupture of the

epicarp tissues around the seed and the seed dis-

charges together with a part of the surrounding tis-

sues including the epidermis of the wall of the

locule; part of the epidermis becomes a membra-

nous edging around the seed and serves as an

anemochorous adaptation. Thus dispersing seeds

are of two kinds: with or without membranous

wings. The anemochorous seeds are adapted for

more distant dispersal (Bunge 1840; Yanishevsky

1940). Seeds small, oblong, dimorphic; those from

the middle chambers of the fruit with tuberculate

and mucous surface, whereas those from the lat-

eral chambers are almost glabrous and not mucous;

testa thin; embryo straight, in ﬂ eshy endosperm,

n = 7.. . . . . . . . . . . . . . . . . .5. tetradiclidaceae.

1. ZYGOPHYLLACEAE

R. Brown 1814 (including Tribulaceae Trautvetter

1853). 24/240. Mostly tropical and subtropical regions,

394 Subclass VI. ROSIDAE

but also in warm-temperate regions, mainly in arid and

subarid areas.

1.1 ZYGOPHYLLOIDEAE

Shrubs, herbs, or rarely trees. Leaves alternate

(Sericodes and Plectrocarpa) or more often opposite,

paripinnate or imparipinnate, often 2-foliolate, some-

times unifoliolate or simple, stipulate. Nectary disc

usually present, often small. Pollen grains 3-colporate

or rarely (Seetzenia) 3-colpate. Gynoecium of 5–2

carpels. Fruits capsular, dehiscing septicidally or

breaking into cocci. Seeds usually with endosperm. –

seetzenieae: Seetzenia; sisynditeae: Sisyndite;

sericodeae: Sericodes; zygophylleae: Zygophyllum

(including Halimiphyllum), Miltianthus, Pintoa,

Roepera, Sarcozygium, Plectrocarpa, Metharme,

Fagonia; larreae: Guaiacum, Bulnesia, Porlieria,

Larrea; morkillieae: Morkillia, Viscalnoa. Widely

distributed.

1.2 TETRAENOIDEAE

Shrubs with very tortuous branches and short, lateral

branchlets. Young shoots and leaves covered by

2-armed trichomes. Axial parenchyma scanty

metatracheal and vasicentric. Leaves alternate,

2- foliolate. Flowers solitary in the leaf axils, 4-merous

with a very short androgynophore. Sepals imbricate.

Petals valvate. Stipules membranous, lacerate.

Stamens eight in two cycles; ﬁ laments with membra-

nous scaly appendage at the base. Pollen grains

3-colporate. Nectary disc annular. Gynoecium of

4-carpels with long, simple, persistent style and capi-

tate stigma; ovary deeply lobed, with 3–5 ovules per

locule; ovules orthotropous, with long, curved funi-

cles. Fruits deeply 4-lobed, breaking into four one-

seeded indehiscent cocci, with the style in the middle,

indehiscent; exocarp spongy, densely villose. Seeds

one in each locule, oblong, with thick testa; embryo

oblong-ovoid, green, with ﬂ eshy cotyledons; endosperm

wanting, n = 14. – Tetraena. Arid regions of China

(Inner Mongolia).

1.3 TRIBULOIDEAE

Shrubs (Kelleronia) or biennial prostrate herbs. Leaves

alternate (Kelleronia) or opposite, pinnate, stipulate.

Trichomes of two markedly different sizes: short and

pointed, or much longer and wider and growing from a

basal “plinth” of epidermal cells. Pollen grains panto-

colpate. Nectary disc present, lobed. Fruits breaking

up into ﬁ ve cocci (Kelleronia), dividing by oblique

transverse septa into 5–3 one-seeded compartments

(Tribulus) or separating into 12–5 indehiscent 1- or

rarely 2-seeded cocci. Seeds without endosperm. –

Kelleronia, Kallstroemia, Tribulopis, Tribulus. Widely

distributed.

1.4 NEOLUEDERITZIOIDEAE

Shrubs with axillary thorns. Leaves alternate, imparip-

innate. Flowers dioecious. Filaments with a deeply

2-lobed hairy scale at the base. Pollen grains 3- colporate.

Disc in the female ﬂ owers hyaline, embracing the

young fruits. Gynoecium of ﬁ ve carpels. Fruits densely

silky-villous, breaking up into ﬁ ve cocci. Seeds with-

out endosperm. – Neoluederitzia. Southwestern

Africa.

1.5 AUGEOIDEAE

Very succulent annual herbs with jointed branches.

Leaves opposite, clavate, connate at the base, simple,

semiterete, estipulate. Petals 3-lobed. Nectary disc

urceolate, stipitate, membranous, with ten subulate

teeth. Stamens with 3-ﬁ d ﬁ laments, the lateral lobes

longer than the oblong anthers. Pollen grains 3- colporate.

Gynoecium of 10 carpels. Ovary 10-locular. Fruits

10-ribbed capsules. Seeds without endosperm. –

Augea. Dry regions of South Africa.

The family is very diversiﬁ ed and specialized in

various directions. Perhaps the Morkillioideae are

relatively the least advanced. Seeds of both Viscainoa

and Morkillia have endosperm and their fruits are sep-

ticidal capsules whereas

Sericodes is devoid of

endosperm and its villous fruits are breaking into

indehiscent cocci. The Zygophylloideae are also less

specialized than the three next subfamilies, especially

Seetzenia, Zygophyllum, and Guaiacum. Palyno-

logically Seetzenia and Sysindite are the most primi-

tive (3-colpate pollen grains), but Seetzenia is an

apetalous prostrate herb with brittle branches, whereas

Sysindite is a Spartium-like shrub and its seeds are

without endosperm. The genus is rather isolated

within the Zygophylloideae. The subfamily

Tetraenoideae is close to the Zygophylloideae but

very specialized.

Tribuloideae, although differing in many respects

from the rest of the family, do not deserve the status of

a separate family.

The monotypic African subfamily Neoluederitzioideae

is connected with the Tribuloideae, and El Hadidi

Superorder RUTANAE 395

(1977) includes both of them in the family Tribulaceae.

Besides, the subfamily Neoluederitzioidieae comprises

both Neoluedentzioideae and Sisyndite, which are not

closely related.

Augeoideae are the most specialized subfamily of

the Zygophyllaceae. Augea capensis is one of the most

remarkable African succulent plants.

2. BALANITACEAE

Endlicher 1841. 1/25. Tropical and North Africa (from

Mauritania to Egypt) and from western Asia through

India to Burma.

Balanites.

Sheahan and Chase (1996, 2000) include Balanites

in the Zhygophyllaceae – Tribuloideae, but from the

Zygophyllaceae it markedly differs in so many respects

(including estipulate leaves, wood anatomy, pollen

morphology, structure of drupaceous fruits, and seed-

coat anatomy) that they deﬁ nitely constitute a separate

family. According to Boesewinkel (1994), in the struc-

ture of ovule and seed anatomy there are many simi-

larities with the members of Linales.

3. PEGANACEAE

van Tieghem ex Takhtajan 1987. 2/6. Southern Europe,

North Africa, arid and semi-arid regions of Asia and

North America (northwestern Texas and northern

Mexico); monotypic genus Malacocarpus is endemic

to northern Iran and central Asia.

Peganum, Malacocarpus.

Both genera are usually included in the Zygophyllaceae.

However, they differ from the Zygophyllaceae in many

characters, including multicellular, capitate trichomes,

elongated leaf epidermal cells alternating with shorter

cells, the presence of a hypodermis in the stem, angular,

thin-walled pericyclic ﬁ bers that sometimes form a

complete cylinder, and the absence of bracysclereids,

raphid sacs in the leaf tissue (see Sheahan and Cutler

1993), the absence of ligular appendages at the base of

stamens, the absence of the endothelium (and other

embryological differences – see Kapil and Ahluwalia

1963; Kamelina 1959, 1991), pollen morphology

(Erdtman 1959; Agababian 1965), the structure of

stigma, and spongy seed coat.

4. NITRARIACEAE

Berthold et J. Presl 1820. 1/10. From North Africa and

southeastern Europe to Siberia, Afghanistan, central

Asia, and 1 sp. in arid and coastal regions of southern

Australia.

Nitraria.

Probably related to the Zygophyllaceae, but differ

in the absence of endothelium (Kamelina 1991), leaf

morphology, pollen morphology (Agababian 1965),

structure of the drupe and seed. The family is relatively

isolated within the order.

5. TETRADICLIDACEAE

Takhtajan 1986. 1/1. North Africa and Irano-Turanian

region.

Tetradiclis.

Tetradiclis has historically been included in such dif-

ferent families as Crassulaceae, Elatinaceae,

Zygophyllaceae, and Rutaceae. Endlicher (1841),

Lindley (1853), and Le Maout and Decaisne (1868)

placed Tetradiclis in the Elatinaceae whereas in Engler’s

(1896) system it is included in Zygophyllaceae as a

monotypic subfamily Tetradiclidoideae. Fenzl (1841),

Hallier (1908, 1912) and Takhtajan (1966) spoke in

favor of Rutaceae, but the majority of modern system-

atists follow Engler. In 1987 I still accepted the rutalean

afﬁ nity of Tetradiclis but separated it into a family of its

own. Later I came to the conclusion that Tetradiclidaceae

differ from the Rutales in so many respects, that it prob-

ably must be raised to the ordinal level. The structure of

the gynoecium and fruits, a very unique type of placen-

tation, and no less the unique type of fruit dehiscence

conﬁ rm a very isolated position of the family. No less

unique are some embryological characters, including

the very speciﬁ c type of tapetum (Kamelina 1991,

1994). Kamelina also has come to the conclusion that

Tetradiclis deserves the rank of an order that would be

placed between Rutales and Linales.

Bibliography

Agababian VS. 1965. Pollen structure and systematics in the

family Zygophyllaceae. Trudy Bot. Inst. Armenian Acad.

Sci. 15: 66–90 (in Russian).

396 Subclass VI. ROSIDAE

Barker RM. 1998. Notes on the genus Tribulopsis

(Zygophyllaceae) in Australia including the descriptions of

ﬁ ve new species and one new subspecies, revised keys and

typiﬁ cations. J. Adelaide Bot. Gard. 18: 43–74

Beier B-A, MW Chase, and M Thulin. 2003. Phylogenetic rela-

tionships and taxonomy of subfamily Zygophylloideae

(Zygophyllaceae) based on molecular and morphological

data. Plant Syst. Evol. 240: 11–39.

Bobrov EG. 1944. On the Asiatic species of the genus Nitraria

L. Sov. Bot. 14: 19–30 (in Russian).

Bobrov EG. 1965. On the origin of the ﬂ ora of deserts of the Old

World in relation to the revision of the genus Nitraria L. Bot.

Zhurn. 50: 1053–1067 (in Russian).

Boesewinkel FD. 1994. Ovule and seed characters of Balanites

aegyptiaca and the classiﬁ cation of the Linales – Geraniales –

Polygalales assembly. Acta Bot. Neerl. 43: 15–25.

Bunge A. 1840. Über die Gattung Tetradiclis Stev. Linnaea 14:

161–178, Taf. I.

Carlquist S. 2005. Wood anatomy of Krameriaceae with com-

parisons with Zygophyllaceae: phylesis, ecology and sys-

tematics. Bot. J. Linn. Soc. 149: 257–270.

El Hadidi MN. 1977. Tribulaceae as a distinct family. Publ.

Cairo Univ. Herb. (7 and 8): 103–108.

Fenzl E. 1841. Die Gattung Tetradiclis Stev. und ihre Stellung

im naturlichen Systeme. Linnaea 15: 289–299.

Iljin MM. 1951. On the systematic position of the genus Tetraena

Maxim. Trudy Tomsk State Univ. 116: 143–144 (in Russian).

Inamdar JA. 1969. Epidermal structure, stomatal ontogeny, and

relationship of some Zygophyllaceae and Simaroubaceae.

Flora 158B: 360–368.

Inamdar JA and RC Patel. 1970. Epidermal structure and devel-

opment of stomata in vegetative and ﬂ oral organs of Fagonia

oretica Linn. Flora 159B: 63–70.

Kamelina OP. 1959. Zygophyllaceae, Nitrariaceae, Ba-lanitaceae.

In: MS Yakovlev, ed. Comparative embryology of ﬂ owering

plants: Brunelliaceae-Tremandraceae, pp. 145–157. Nauka,

Leningrad (in Russian).

Kamelina OP. 1991. Comparative morphological analysis as a

method of phylogenetic systematics of ﬂ owering plants.

Ph.D. dissertration, University of Tashkent (in Russian).

Kamelina OP. 1994. Embryology and systematic position of

Tetradiclis (Tetradiclidaceae). Bot Zhurn. 79(5): 11–27 (in

Russian with English summary).

Kamelina OP. 1996. Tetradiclidaceae. In: A. Takhtajan, ed.

Comparative seed anatomy, vol. 5, pp. 377–381. St. Petersburg

(in Russian).

Kapil RN and K Ahluwalia. 1963. Embryology of Peganum har-

mala Linn. Phytomorphology 13: 127–140.

Lia VV, VA Confalonieri, CI Comas, and JH Hunziker. 2001.

Molecular phylogeny of Larrea and its allies

(Zygophyllaceae): Reticulate evolution and the probable

time of the creosote bush arrival to North America. Molecular

Phylog. Evol. 21: 309–320.

Ma Yu-chuan and S Zhang. 1990. Study on the systematic posi-

tion of Tetraena Maxim. Acta Phytotax. Sinica 28(2):

89–95.

Maksoud SA and MN El Hadidi. 1988. The ﬂ avonoids of

Balanites aegyptiaca (Balanitaceae) from Egypt. Plant Syst.

Evol. 160: 153–158.

Mauritzon J. 1934. Etwas über die Embryologie der

Zygophyllaceen sowie einige Fragmente über die der

Humiriaceen. Bot. Not. 87: 407–422.

Nag TN et al. 1986. Free endogenous ascorbic acid from

Zygophyllaceous plants growing in the arid zone of

Rajasthan. J. Indian Bot. Soc. 9: 112–113.

Nair NC and RK Jain. 1956. Floral morphology and embryology

of Balanites roxburghii Planch. Lloydia 19: 269–279.

Nair NC and KS Nathawat. 1958. Vascular anatomy of the

ﬂ ower or some species of Zygophyllaceae, part l. J. Indian

Bot. Soc. 37: 172–180.

Narayana HS and CG Prakasa Rao. 1963. Floral morphology

and embryology of Seetzenia orientalis Decne.

Phytomorphology 13: 197–205.

Narayana L, P Satyauarayana, and H Radhakrishnaiah. 1990.

Systematic position of Balanitaceae. In: K Bilgrami and J

Dogra, eds. Phytochemistry and plant taxonomy, pp. 157–

164. CBS, Delhi.

Nemirovich-Danchenko EN. 1996. Nitrariaceae, Balanitaceae,

Peganaceae. In: A Takhtajan, ed. Comparative seed anatomy,

vol. 5, pp. 399–405. Nauka, St. Petersburg (in Russian).

Parameswaran N and H Conrad. 1992. Wood and bark anatomy

of Balanites aegyptiaca in relation to ecology and taxonomy.

IAWA Bull. 3: 75–88.

Phatak VG. 1971. Embryology of Zygophyllum coccineum L.

and Z. fabago L. Proc. Kon. Nederl. Akad. Wetensch. 74C:

379–397.

Poggio L. 1978. Estudios cromosómicos en Bulnesia, Pintoa,

Porlieria, Plectrocarpa y Sericodes (Zygophyllaceae).

Darwiniana 21: 139–151.

Porter DM. 1972. The genera of Zygophyllaceae in the south-

eastern United States. J. Arnold Arbor. 53: 531–552.

Porter DM. 1974. Disjunct distributions in the New World

Zygophyllaceae. Taxon 23: 339–346.

Praglowski J. 1987. Pollen morphology of Tribulaceae. Grana

26: 193–211.

Ronse Decraene LP and EF Smets. 1991. Morphological studies

in Zygophyllaceae: I. The ﬂ oral development and vascular

anatomy of Nitraria retusa. Am. J. Bot. 78: 1438–1448.

Ronse Decraene LP, J De Laet, and EF Smets. 1996.

Morphological studies in Zygophyllaceae. II. The ﬂ oral

development and vascular anatomy of Peganum harmala.

Am. J. Bot. 83: 201–215.

Saﬁ na LI and EN Nemirovich-Danchenko. 1996. Zygophyllaceae.

In: A Takhtajan, ed. Comparative seed anatomy, vol. 5,

pp. 392–399. Nauka, St. Petersburg (in Russian).

Saleh NAM and MN El Hadidi. 1977. An approach to the

chemosystematics of the Zygophyllaceae. Biochem. Syst.

Ecol. 5: 121–128.

Saleh N, MN El Hadidi, and A Ahmed. 1982. The chemosys-

tematics of Tribulaceae. Biochem. Syst. Ecol. 10: 313–317.

Sarma V and RS Rao. 1991. Taxonomic importance of epidermis

in Simaroubaceae-Zygophyllaceae with special reference to

position of Balanites. Feddes Repert. 102: 579–585.

Sheahan MC. 2007. Zygophyllaceae. In: K Kubitzki, ed. The

families and genera of vascular plants, vol. 9, pp. 488–500.

Springer, Berlin/Heidelberg/New York.

Sheahan MC and MW Chase. 1996. A phylogenetic analysis of

Zygophyllaceae R.Br. based on morphological, anatomical

and rbcL DNA sequence data. Bot. J. Linn. Soc. 122:

279–300.

Sheahan MC and MW Chase. 2000. Phylogenetic relationships

within Zygophyllaceae based on DNA sequences of three

plastid regions, with special emphasis on Zygophylloideae.

Syst. Bot. 25: 371–384.

Superorder RUTANAE 397

Sheahan MC and DF Cutler. 1993. Contribution of vegetative

anatomy to the systematics of the Zygophyllaceae R. Br. Bot.

J. Linn. Soc. 113: 227–262.

Shulda RD. 1955. On the morphology of the two abnormal

gynoecia of Peganum harmala. J. Indian Bot. Soc. 34 (4):

382–387.

Singh BP and I Kaur. 1999. Systematic position of the genus

Peganum. J. Econ. Taxon. Bot. 22(3): 705–708.

Singh BP, I Kaur, and DP Gauchan. 2002. Floral anatomy and

systematic position of the genus Balanites. Acta Bot. Hung.

44(1–2): 137–143.

Thulin M. 1993. Zygophyllaceae (including Tribulaceae). In:

M Thulin, ed. Flora of Somalia, vol. 1. Royal Botanic

Gardens, Kew.

Vasilevskaya VK and MP Petrov. 1963. Centralasiatic endemic

Tetraena mongolica Maxim. Bot. Zhurn. 49: 1506–1513 (in

Russian).

Vijayalakshmi S and S Raja Shanmukha Rao. 1991. Taxonomic

importance of epidermis in Simaroubaceae – Zygophyllaceae

with special reference to position of Balanites. Feddes

Repert. 102: 579–585.

Wei N. 1991. A comparative anatomy on the vegetative organs

of Tetraena mongolica Maxim. and Zygophyllum xanthoxy-

lum (Bunge) Maxim. Acta Sci. Natur. Univ. Intramongolicae

22: 528–533.

Wu S and L Tu. 1990. The embryology of Tetraena mongolica

Maxim. Acta Sci. Natur. Univ. Intramongolicae 21:

177–183.

Xi Y and S Zhou. 1989. Pollen morphology and its exine ultra-

structure of the Zygophyllaceae in China. Bot. Research

(China) 4: 75–86.

Xi Y and S Zhou. 1992. A contribution to the pollen morphol-

ogy of Tetraena and Malpighiaceae, with discussion of the

afﬁ nity and taxonomic position of Tetraena. Chinese J. Bot.

4: 6–12.

Yanishevski DE. 1940. Tetradiclis tenella (Ehrenb.) Litv. as the

example of an ephemeral on the solonchaks of the

Mediterranean desert regions. Trudy Bot. Inst. Akad. Nauk

SSSR, 4th ser., 4: 236–248 (in Russian).

Order 99. LINALES

Trees, shrubs, woody lianas, or herbs. Vessels with

scalariform or simple perforations; lateral pitting

usually alternate. Fibers with distinctly bordered pits,

rarely with simple pits. Rays heterogeneous or homo-

geneous. Axial parenchyma of diverse types. Sieve-

element plastids of Ps- (Erythroxylaceae and

Rhizophoraceae), Pcs- (Humiriaceae), or more often

of S-type. Nodes trilacunar or unilacunar, or rarely

(Rhizophoraceae) multilacunar. Leaves alternate or

less often opposite, simple and often entire, with

stipules or estipulate; stipules bearing colleters on the

adaxiale face (Erythroxylaceae and some

Rhizophoraceae – see Thiebaut and Hoffmann 2005).

Stomata mostly paracytic. Flowers in terminal or

axillary inﬂ orescences (mostly more or less cymose),

bisexual or sometimes unisexual, actinomorphic or with

dissimilar sepals, 5-merous or sometimes 4- merous.

Sepals free or more or less connate, mostly imbricate.

Petals free, often clawed, imbricate or contorted, some-

times appendaged. Nectary disc mostly present, of

staminal origin, intra- or extrastaminal. Stamens in one

or two cycles or less often in three or four cycles or even

numerous; ﬁ laments usually connate at the base or into

a short tube (except in the Ixonanthaceae); anthers tet-

rasporangiate, introrse, basiﬁ xed or dorsiﬁ xed, opening

longitudinally. Tapetum secretory. Microsporo genesis

simultaneous or rarely (Gynotrocheae – Rhizo-

phoraceae) successive. Pollen grains 3-celled or

sometimes 2-celled, 3(-4)-colporate or less often, pan-

tocolpate, pantocolporate or pantoporate. Gynoecium

of 2-5(-20) united carpels, with free or more or less

connate stylodia; ovary superior, rarely semi-inferior

to inferior, mostly 2–5-locular, with 1–2 or more pen-

dulous ovules per locule. Ovules anatropous to

hemitropous, rarely campylotropous or epitropous,

bitegmic, crassinucellate or sometimes tenuinucellate,

often with endothelium (lacking in Humiriaceae and

Rhizophorea). Female gametophyte of Polygonum-

type. Endosperm nuclear. Fruits usually drupaceous or

capsular, sometimes schizocarps, rarely baccate. Seeds

typically with ﬁ brous exotegmen, sometimes arillate

or winged, with straight or slightly curved embryo;

endosperm copious, ﬂ eshy and oily to scanty or want-

ing. Plants with ellagic acid and proanthocyanins,

sometimes producing alkaloids.

Most probably derived from some relatively primi-

tive members of the Rutales with scalariform perfora-

tion of the vessels and free stylodia. The Hugoniaceae

are the most archaic member of the order.

Key to Families

1 Petals not appendaged. Fibers always with bordered

pits. Ovary locules all fertile. Plants not producing

alkaloids.

2 Stylodia more or less free or when they are united

into a simple style, it is evidently cleft. Petals

contorted, caducous. Nectary disc extrastaminal

or wanting.

3 Trees, shrubs, or woody lianas. Fruits drupa-

ceous or capsular. Anthers dorsoversatile.

Ovules two per locule.

4 Fruits drupaceous. Trees or more often

woody lianas (the lower inﬂ orescence

398 Subclass VI. ROSIDAE

branches modiﬁ ed into hooks), rarely

shrubs. Hairs, if present, simple, uniseriate,

or multiseriate with multicellular, glandular

heads; tufted hairs absent. Vessels in

Indorouchera with scalariform perforations

that have 15–25 bars, but in all other genera

perforations predominantly or (Hugonia)

exclusively simple. Nodes trilacunar.

Leaves alternate, entire, with lateral, cadu-

cous stipules. Stomata paracytic, subsidiary

cells are lobed underneath the guard cells.

Flowers in terminal or axillary racemes,

spikes or panicles, small to large, 5-merous.

Sepals often more or less unequal, imbri-

cate. Petals free, rarely basally clasping, con-

torted. Extrastaminal nectary disc absent or

some-rimes represented by glands, adnate to

staminal tube. Stamens 10 or 15, alternately

shorter or longer; ﬁ laments basally connate

into a tube. Pollen grains 3-colporate.

Gynoecium of 3-5(-8) carpels; stylodia free

or basally connate, with capitate stigma;

ovary 2–5-locular, locules without ‘false

septa’; ovules two per locule, pendulous,

anatropous, with ventral raphe. Fruits ﬂ eshy,

indehiscent or rarely splitting ﬁ nally into

indehiscent mericarps. Seeds sometimes

with an arillode; mesotesta with sclerotic

cells, endotesta ligniﬁ ed or tegmen obliter-

ated; embryo straight or slightly curved;

cotyledons large; endosperm copious or

scanty, n = 6, 12, 13. . . . . 1. hugoniaceae.

4 Fruits 1-locular capsules with woody peri-

carp ﬁ nally lengthwise splitting into two

valves. Trees with stellately tufted and sim-

ple hairs on the young shoots, stipules, and

the outsides of the sepals and petals. Vessels

with scalariform perforations. Leaves oppo-

site, leathery, entire, coriaceous, with inter-

petiolar, large, caducous stipules. Stomata

anomocytic to anisocytic. Flowers in termi-

nal or axillary cymes or racemes, 5-merous.

Sepals shortly connate, persistent. Petals

free, thick, imbricate, spoon-shaped at the

base. Extrastaminal nectary disc well devel-

oped, cuplike. Stamens ten, free, adnate at

base to inner side of the disc, alternately

longer and shorter; anthers with broad con-

nective; anthers introrse. Pollen grains

3–9- colporate. Gynoecium of two carpels;

stylodia more or less free or connate, with

capitate stigma; ovary 2- locular, ovules two

in each locule, pendulous. Fruits 1-seeded,

with seed persisting after falling of pericarp

and pendulous from the top of a long ﬁ li-

form funiculus. Seeds with papillose arilloid

surrounding their lower half; exotestal cells

palisade; embryo straight; endosperm

copious; cotyledons very large, folded.

. . . . . . . . . . . . . . . 3. ctenolophonaceae.

3 Mostly herbs, seldom subshrubs, shrublets, or

(Tirpitzia) small shrubs. Vessels with simple

perforations. Nodes unilacunar with one trace

(Linum), or trilacunar. Leaves alternate or oppo-

site, entire; stipules lateral, small and incon-

spicuous, sometimes (Linum and Hesperolinon)

modiﬁ ed into glands, or wanting; epidermis

often somewhat mucilaginous. Stomata com-

monly paracytic. Flowers in cymose inﬂ ores-

cences or rarely (Anisadenia) racemes, bisexual,

actinomorphic, 5-merous or rarely (Radiola)

4-merous. Sepals free or basally connate, per-

sistent, imbricate (quincuncial). Petals free,

usually clawed, imbricate or contorted, usually

caducous. Small nectary glands usually present

external to the stamens or at the inner base of

the petals. Stamens 5, 10, or 15, or rarely

(Radiola) 4, usually alternate the petals or rarely

(Anisadenia) opposite the petals, sometimes

alternating with ﬁ liform or toothed staminodia;

ﬁ laments expanded below and more or less

connate into a tube; anthers introrse. Pollen

grains 3-colpate, pantocolpate or pantoporate.

Gynoecium of 3–5 carpels, very rarely (Linum

digynum) of 2 carpels; stylodia free or shortly

connate below, with terminal stigma; ovary

(2)3–5-locular, sometimes unilocular at the

very top, ovules 2 in each locule, usually (but

not in Anisadenia) separated by an incomplete

secondary septum extending inward from the

ovary wall; ovules crassinucellate or tenuinu-

cellate, bitegmic, outer integument not contrib-

uting to the micropyle. Fruits septicidal capsules

(Lineae) or of two indehiscent, 1-seeded meri-

carps (Anisadenia). Seeds often mucilaginous,

exotesta with outer walls massively thickened;

embryo a straight, spatulate, oily, green;

endosperm scanty, n = 6, 8–12. . . 2. linaceae.

Superorder RUTANAE 399

2 Stylodia more or less completely united into a

style. Petals imbricate or contorted. Nectary disc

intrastaminal or rarely (Ochthocosmus in the

Ixonanthaceae) nectary is represented by inter-

staminal glands.

5 Fruits capsular. Trees (sometimes to 30 m tall)

or shrubs, sometimes with slender stems, wiry,

wandlike, with sparse leaves; mucilage cells

present. Vessels with simple perforations.

Leaves alternate, petiolate, simple, entire or

toothed, with small lateral stipules, or stipules

wanting. Stomata paracytic. Flowers small, un

axillary inﬂ orescences, mostly bisexual, acti-

nomorphic or nearly so, commonly 5-merous.

Sepals free or connate only at the base, imbri-

cate or contorted. Petals free, imbricate or

contorted, persistent. Stamens 5, or 10, or 20;

ﬁ laments widened at the base, free or basally

adnate to the conspicuous annular or cupular

nectary disc. Pollen grains 2-locular and 3-col-

porate. Gynoecium of (4-)5 or rarely 2 carpels;

style with a more or less capitate stigma; ovary

superior or semiinferior, 2- or (4-)-5 locular,

sometimes apically unilocular and sometimes

the locules are divided into locelli by incom-

plete secondary septa as in the Linaceae; style

and ﬁ laments folded in the bud. Ovules one

(Allantospermum) or two per locule, pendu-

lous, anatropous, with ventral raphe, the

micropyle directed upward and outward. Fruits

septicidal capsules, sometimes also loculicidal

by secondary septa, with or without a persis-

tent central column. Seeds with an obvious

basal wing (Ixonanthes and Ochthocosmus) or

aril arising between the hilum and micropyle

(laciniate and covers the seed in Phyllocosmus

and 2-lobed and membranous in Cyrillopsis);

endotegmen with sinuous anticlinal walls.

Embryo straight, endosperm scanty or absent;

cotyledons large. Proanthocyanidins and

ellagic acid present. . . . .4. ixonanthaceae.

5 Fruits drupaceous. Evergreen trees and shrubs,

often with an aromatic juice, but without

secretory structures (except often in the fruits).

Vessels usually with scalariform perforations

that have mostly 15–25 bars. Leaves alternate,

coriaceous, entire or toothed, with tiny and

caducous stipules or estipulate; leaves often

aromatic, with balsamic juice. Stomata ano-

macytic or paracytic. Flowers bisexual, acti-

nomorphic or nearly so, 5-merous. Sepals

persistent, more or less connate, imbricate,

two outer ones often smaller than others, rarely

the lobes suppressed. Petals free, thick, usu-

ally 3–5 veined, imbricate or contorted.

Stamens numerous in fascicles (Vantanea) or

more often 10–30, sometimes in 5 antesepal-

ous groups of 3, plus 5 antepetalous singles;

ﬁ laments connate into a tube; some of the sta-

mens sometimes staminodial; anthers basiﬁ xed

or dorsiﬁ xed or attached near the base, with

expanded, prolonged connective, versatile.

Pollen grains 3(4)-colporate or seldom

3(4)-porate. The intrastaminal nectary disc

free or adnate to the base of the ovary or to the

base of the ﬁ laments, usually cupulate to tubu-

lar or toothed or lobed, or sometimes of 10–20

free scales. Gynoecium of (4)5(-7) carpels;

style with a lobed or cleft stigma; ovary

(4-)5(-7)-locular, sometimes apically 1-locu-

lar, with 1(-2) pendulous ovule per locule.

Fruits with more or less ﬂ eshy, thin exocarp

and hard, woody, multilocular, and usually

1–2-seeded stone (pyrene) sometimes contain-

ing numerous resinous secretory cavities and

adapted to the water dispersal; the stone with

as many longitudinal valves as carpels, 1 or

more being pushed off at germination. Seeds

with nucellar remnants; exotestal cells thick-

walled, ligniﬁ ed, tegmen multiplicative, cross

layer beneath exotegmen; embryo straight or

slightly curved; endosperm copious oily.

Ellagic acid present, n = 12. 5. humiriaceae.

1 Petals appendages. Fibers with simple or bordered

pits. Plants contain alkaloids.

6 Nectary disc absent. Evergreen or deciduous,

glabrous, small trees and shrubs; wood hard,

commonly with silicium grains. Vessels with

simple perforations. Fibers with distinctly bor-

dered to sometimes simple pits. Nodes unilacu-

nal. Leaves alternate or rarely (Aneulophus)

opposite, entire, simple, sometimes accompanied

by scale leaves, with intrapetiolar, abaxially bico-

sytate, often caducous stipules. Stomata paracytic.

Flowers small, in axillary fascicles or solitary in

the axils, bisexual or seldom unisexual (plant

dioecious), actinomorphic, 5-merous, often

heterostylous; bracteoles small, scarious. Sepals

400 Subclass VI. ROSIDAE

persistent, connate below into a tube with imbri-

cate or valvate lobes. Petals free, imbricate or con-

torted, caducous, mostly with an adaxial more or

less basal ligular appendage. Stamens ten, in two

whorls of ﬁ ve, the outer whorl alternate with petals;

ﬁ laments united at least at the base, usually forming

a short tube; anthers dorsiﬁ xed, versatile, introrse.

Pollen grains 3- colporate. Gynoecium of three or

less often two carpels; stylodia free or more or less

connate into a style, stigmas capitellate, rarely ses-

sile; ovary superior, (2-)-3- locular, usually only

with one fertile locule, the others empty. Ovules

solitary or less often two in the fertile locule, pen-

dulous, anatropous to hemitropous, with an

endothelium. Fruits 1-, or sometimes 2-seeded

drupes. Seeds with more or less thickened exot-

estal cells; embryo straight, green; cotyledons

two, ﬂ at; endosperm copious, starchy, or rarely

lacking. Present alkaloids, proanthocyanidins

(cyanidin), ﬂ avonols (kaempferol and quercetin)

n = 12.. . . . . . . . . . . . . . . . 6. erythroxylaceae.

6 Intrastaminal nectary disc present. Shrubs or trees

(up to 50 m tall) of dry to wet forests or mangrove

swamps, mostly with aerial roots and unicellular

hairs. Vessels with scalariform or less often sim-

ple perforations; lateral pitting scalariform to

opposite and alternate. Fibers with simple or bor-

dered pits. Rays nearly always heterogeneous,

usually mixed uniseriate and pluriseriate with

short ends. Axial parenchyma typically scanty

paratracheal. Sieve-element plastids of Pc-type

with about 20 or more square or polygonal pro-

tein bodies. Nodes trilacunar or multilacunar with

split-lateral traces. Leaves opposite or sometimes

verticillate, simple, entire, crenate or dentate,

with well-developed interpetiolar stipules, imbri-

cate (Rhizophoreae), or valvate (Macarisieae),

sheathing the terminal bud; stipules bear colleters

on the inner surface at the base that secrete

gummy substances onto the buds. Stomata para-

cytic or (Rhizophoreae) encyclocytic. Flowers in

axillary and fundamentally cymose few-ﬂ owered

inﬂ orescence or (in large- ﬂ owered species of

Bruguiera) solitary, clearly articulated at juncture

with pedicel, bisexual or rarely unisexual (plants

monoecious), actinomorphic, most often 4–5-mer-

ous, with well- developed ﬂ oral tube that is some-

times prolonged beyond the ovary; both the calyx

and the ovary have a layer of hypodermal laticif-

erous cells, which in Gynotroches and Pellacalyx

are represented by many idioblastic secretory

cells. Sepals (3)4-5(-16), fused at base, valvate,

thick, usually ﬂ eshy or leathery. Petals as many as

and alternate with the sepals, fused at base, com-

monly ﬂ eshy and often shorter than the sepals,

contorted or infolded in bud, generally condupli-

cate, mostly distally divided or appendaged, each

petal individually enclosing 1–5 stamens.

Androecium diplostemonous to polyandrous; ﬁ l-

aments free or sometimes basally connate, borne

around the base of a ﬂ eshy, often conspicuously

lobed, intrastaminal nectary disc; anthers tet-

rasporangiate, 2-locular or (Rhizophora) multilo-

cellate, cross-partitioned and dehiscent by a

separating longitudinal valve. Microsporogenesis

simultaneous or also successive in most

Gynotrocheae. Pollen grains 2-celled, 3(4)-col-

porate, with relatively thick tectum and rugulate-

punctate to psilate surface; endoapertures with

some degree of fusion. Gynoecium of (2) 3-5(-

20) united carpels, with a terminal simple style;

stigma capitate or with pronounced lobes (in

Gynotroches the stigmatic lobes may be rather

long), generally papillate; ovary superior

(Macarisieae) or semi-inferior to inferior, with as

many locules as carpels, or the locules often

incompletely or not at all separated by septa at

anthesis. Ovules 2–6 or more per carpel, usually

apical-axial, pendulous, anatropous to hemitrop-

ous or rarely campylotropous, bitegmic, crassinu-

cellate or (Gynotroches and Pellacalyx)

tenuinucellate; micropyle zig-zag or endostomal.

Endothelium present (except for Rhizophoreae).

Fruits capsular (Macarisieae and Crossostylis),

baccate (Gynotrocheae), or hard-walled and inde-

hiscent (Rhizophoreae). Seeds arillate or winged

(in capsular fruits) or nonappendaged (in baccate

or indehiscent hard-walled fruits); seed coat in

Macarisieae and Gynotrocheae with well-devel-

oped exotesta and (ﬁ brous) exotegmen and is

either exotestal or exotestal-exotegmic; seed coat

in Rhizophoreae is not histologically differenti-

ated and entirely lacking a tegmen; embryo

straight, in the mangrove genera viviparous and

with an enlarged hypocotyl; endosperm well

developed, ﬂ eshy, oily. Plants contain pyrroliz-

idine alkaloids and ellagic acid, n = (13), 14, 16,

18, 21. . . . . . . . . . . . . . . . . .7. rhizophoraceae.

Superorder RUTANAE 401

1. HUGONIACEAE

Arnott 1834. 5/55–60. From tropical Africa and

Madagascar to New Caledonia, Fiji, and tropical South

America.

Indorouchera, Roucheria, Philbornea, Hebepetalum,

Hugonia (including Durandea).

Probably the most archaic member of the order.

2. LINACEAE

A. P. de Candolle ex Perleb 1818. 8/250. Widely dis-

tributed, especially in temperate and subtropical

regions.

lineae: Tirpitzia, Reinwardtia, Linum, Cliococca,

Sclerolinon, Hesperolinon, Radiola; anisadenieae:

Anisadenia.

Linaceae has probably derived from the nearest ances-

tor of the Hugoniaceae. The most primitive members of

the Linaceae are Tirpitzia (southwestern China, northern

Vietnam) and Reinwardtia (northern India and China).

3. CTENOLOPHONACEAE

Exell et Mendonça 1951. 1/4. Tropical West Africa

and Malesia.

Ctenolophon.

Related to the Linaceae and also like Humiriaceae

(Link 1992a).

4. IXONANTHACEAE

Planchon ex Miquel 1858. 5/35. Tropical Africa

(Phyllocosmus), Himalayas, northeastern India, south-

ern China, Southeast Asia, New Guinea (Ixonanthes),

and tropical America (Cyrillopsis and Ochtocosmus).

Allantospermum (2) occurs in Madagascar (1) and

Borneo (1).

Cyrillopsis, Ixonanthes, Ochthocosmus, Phyllo-

cosmus, Allantospermum.

Related to the Linaceae and especially to the

Humiriaceae. According to Link (1992b), the

Ixonanthaceae have more or less prominent discs in

common only with the Humiriaceae whereas the

nectaries of the Linaceae sensu stricto (and the

Erythroxylaceae) are clearly parts of the staminal tubes.

5. HUMIRIACEAE

A. H. L. de Jussieu 1829. 8/65. Tropical South America,

north to Costa Rica, but mostly in the Amazon basin

and with 1 species (Sacoglottis gabonensis) in tropical

West Africa.

vantaneeae: Vantanea (20); humirieae: Duckesia,

Endopleura, Hylocarpa, Humiria, Sacoglottis (11),

Schistostemon, Humiriastrum (17).

Close to the Linaceae and have also much in com-

mon with Ixonanthaceae. According to Boesewinkel

(1985), the Humiriaceae seem to be more primitive

than the Erythroxylaceae and the Linaceae because of

the large persistent nucellus, the lack of an endothe-

lium, the absence of repeated divisions in the original

middle layer of the inner integument, and perhaps also

because of the strongly ligniﬁ ed exotesta.

6. ERYTHROXYLACEAE

Kunth 1822 (including Nectaropetalaceae Exell et

Mendonça 1951). 4/250–260. Pantropical, but most

abundant in the Andes, in the Amazon Basin of South

America, and in Madagascar.

Erythroxylum, Aneulophus (2), Nectaropetalum (8),

Pinacopodium (2).

Related to the Linaceae, Ixonanthaceae, and

Humiriaceae.

7. RHIZOPHORACEAE

C. H. Persoon 1806 (including Cassipoureaceae J. Agardh

1858, Macarisiaceae J. Agardh 1858, Mangiaceae

Raﬁ nesque 1837). 15/140. Pantropical, but extend into

the subtropics of North America and Asia; the greatest

diversity in the paleotropics.

macarisieae: Anopyxis, Macarisia Blepha-

rostemma, Comiphyton, Dactylopetalum, Cassipourea,

Sterigmapetalum; gynotrocheae: Carallia,

Gynotroches, Pellacalyx;

crossostylideae:

Crossostylis; rhizophoreae: Bruguiera, Ceriops,

Kandelia, Rhizophora.

According to Tobe and Raven (1988), the genera of

Macarisieae retain many plesiomorphic features,

including a superior ovary. The most specialized are

Rhizophoreae: endothelium not formed, outer integu-

ment vascularized, endosperm overﬂ owing, viviparous

402 Subclass VI. ROSIDAE

seedlings, testa not differentiated histologically, and

tegmen lacking. The cladistic analysis indicates that

Rhizophoreae have direct relationships with

Gynotrocheae (not including Crossostylis) rather than

with Macarisieae (Tobe and Raven 1988).

Setoguch et al. (1999) and Schwarzbach and

Ricklefs (2000) identify the Rhizophoraceae and

Erythroxylaceae as sister group within the Malpighiales

sensu the APG II.

Bibliography

Behnke H-D. 1982. Sieve-element plastids of Cyrillaceae,

Erythroxylaceae, and Rhizophoraceae: Description and sig-

niﬁ cance of subtype PV plastids. Plant Syst. Evol. 141:

31–39.

Behnke H-D. 1988. Sieve-element plastids and systematic rela-

tionships of Rhizophoraceae, Anisophylleaceae and allied

groups. Ann. Missouri Bot. Gard. 75: 1387–1409.

Boesewinkel FD. 1980a. Development of ovule and testa of

Linum usitatassimum L. Acta Bot. Neerl. 29: 17–32.

Boesewinkel FD. 1980b. Development of ovule and seed coat of

Erythroxylum coca Lamk. Acta Bot. Neerl. 29: 231–241.

Boesewinkel FD. 1985. The ovule and seed of Humiria balsam-

ifera (Aubl.) St.Hil. Acta Bot. Neerl. 34: 183–191.

Boesewinkel FD. 1994. Ovules and seed characters of Balanites

aegyptiaca and the classiﬁ cation of the Linales-Geraniales-

Polygalales assembly. Acta Bot. Neerl. 43: 15–25.

Boesewinkel FD and F Bauman. 2000. Hugoniaceae, Linaceae,

Ctenolophonaceae, Ixonanthaceae, Humariaceae,

Erythroxylaceae. In: A Takhtajan, ed. Comparative seed

anatomy, vol. 6, pp. 9–20. Nauka, St. Petersburg (in

Russian).

Boesewinkel FD and J Geenen. 1980. Development of ovule

and seed coat of Erythroxylum coca Lamk. Acta Bot. Neerl.

29: 231–241.

Bove CP. 1997. Phylogenetic analysis of Humiriaceae with notes

on the monophyly of Ixonanthaceae. J. Comp. Biol. 2:

19–24.

Bove CP and TS Melhem. 2000. Humiriaceae Juss. World Pollen

Spore Flora 22: 1–35.

Chase MW, S Zmarzty, MD Lledó, KJ Wurdack, SM Swensen,

and MF Fay. 2002. When in doubt, put it in Flacourtiaceae:

A molecular phylogenetic analysis based on plastid rbcL

DNA sequences. Kew Bull. 57: 141–181.

Cuatrecasas J. 1961. A taxonomic revision of the Humiriaceae.

Contr. U.S. Natl. Herb. 35: 25–214.

Dahlgren RMT. 1988. Rhizophoraceae and Anisophylleaceae:

summary statement, relationships. Ann. Missouri Bot. Gard.

75: 1259–1277.

Daly DC. 2004. Erythroxylaceae. In: N Smith, SA Mori,

A Henderson, DW Stevenson, and SV Heald, eds. Flowering

plants of the Neotropics, pp. 143–145. The New York

Botanical Garden, Princeton University Press, Princeton.

Ding Hou D. 1958. Rhizophoraceae. In: CGGJ van Steenis, ed.

Flora Malesiana, ser. 1, 5: 429–493. Noordhoff, Djakarta.

Dorr LJ. 1994. The identity and neotypiﬁ cation of Endosteira

Turcz. (Rhizophoraceae). Taxon 43: 639–640.

Floret J-J. 1989. Cassipourea Aublet (Rhizophoraceae-

Macarisieae): Organisation ﬂ orale et divisions subgen-

eriques. Adansonia, ser. 2, 11: 1–83.

Forman LL. 1965. A new genus of Ixonanthaceae with notes on

the family. Kew Bull. 19: 517–526.

Graham SA. 1964. The genera of Rhizophoraceae and

Combretaceae in the southeastern United States. J. Arnold

Arbor. 45: 285–301.

Grigorieva VV. 1990. The pollen grain morphology in members

of the Linaceae family. Bot. Zhurn. 75: 1345–1352 (in

Russian with English summary).

Gustafsson MHG. 2004. Rhizophoraceae. In: N Smith, SA Mori,

A Henderson, DW Stevenson, SV Heald, eds. Flowering

plants of the Neotropics, pp. 324–326. The New York

Botanical Garden, Princeton University Press, Princeton.

Hallier H. 1923. Beiträge zur Kenntnis der Linaceae (DC. 1819)

Dumort. Beih. Bot. Centralbl. 39: 1–178.

Ham RWJM van der. 1989. New observations on the pollen of

Ctenolophon Oliver (Ctenolophonaceae), with remarks on

the evolutionary history of the genus. Rev. Palaeobot.

Palynol. 59: 153–160.

Heimsch C and EE Tschabold. 1972. Xylem studies in the

Linaceae. Bot. Gaz. 133: 242–253.

Hooren AMN van and HP Nooteboom. 1988. Linaceae,

Ctenolophonaceae. In: CGGJ van Steenis, ed. Flora Malesiana,

ser. 1, 10: 607–619, 629–634. Noordhoff, Groningen.

Jardim AG. 1999. A revision of Roucheria Planch. and

Hebepetalum Benth. (Hugoniaceae). University of Michigan,

Ann Arbor, MI.

Jardim A. 1999. A revision of Roucheria Planch. and

Hebepetalum Benth. (Hugoniaceae). M.Sc. Thesis,

University of Missouri, St. Louis.

Jayeola AA, JR Thorpe, TA Adenegan. 2001. Macro-

morphological and micromorphological studies of the

West African Rhizophora L. Feddes Repert. 112(5–6):

349–356.

Juncosa AM. 1988. Floral development and character evolution in

Rhizophoraceae. In: R Leins, SC Tucker, and RK Endress, eds.

Aspects of ﬂ oral development, pp. 83–101. Springer, Berlin.

Juncosa AM and H Tobe. 1988. Embryology of tribe

Gynotrocheae (Rhizophoraceae) and its developmental and

systematic implications. Ann. Missouri Bot. Gard. 75:

1410–1424.

Juncosa AM and PB Tomlinson. 1987. Floral development in

mangrove Rhizophoraceae. Am. J. Bot. 74: 1263–1279.

Juncosa AM and PB Tomlinson. 1988a. Systematic comparison

and some biological characteristics of Rhizophoraceae and

Anisophylleaceae. Ann. Missouri Bot. Gard. 75: 1296–1318.

Juncosa AM and PB. Tomlinson. 1988b. A historical and taxo-

nomic synopsis of Rhizophoraceae and Anizophylleaceae.

Ann. Missouri Bot. Gard. 75: 1278–1295.

Keating RC and V Randrianosola. 1988. The contribution of leaf

architecture and wood anatomy to classiﬁ cation of the

Rhizophoraceae and Anisophylleaceae. Ann. Missouri Bot.

Gard. 75: 1343–1368.

Kool R. 1980. A taxonomic revision of the genus Ixonanthes

(Linaceae). Blumea 26: 191–204.

Kool R. 1986. Ixonanthaceae. In: CGGJ van Steenis, ed. Flora

Malesiana, ser. 1, 10: 621–627. Kluwer, Dodrecht.