CANELLALES Cronq

Winterales A. C. Sm. ex Reveal in Phytologia 74: 174. 25 Mar 1993; Winteranae Doweld, Tent. Syst. Plant. Vasc.: xxiii. 23 Dec 2001; Winteridae Doweld, Tent. Syst. Plant. Vasc.: xxiii. 23 Dec 2001; Winterineae Shipunov in A. Shipunov et J. L. Reveal, Phytotaxa 16: 64. 4 Feb 2011

Habit Usually bisexual (rarely monoecious, polygamomonoecious or dioecious), evergreen trees (rarely shrubs). Aromatic.

Vegetative anatomy Mycorrhiza? Phellogen ab initio superficial. Primary stem with eustele or (pseudo)siphonostele, with continuous vascular cylinder. Vessel elements absent in Winteraceae. Vessel elements in Canellaceae with scalariform, opposite or reticulate perforation plates; lateral pits scalariform or opposite, bordered pits. Imperforate tracheary xylem elements tracheids with bordered pits, non-septate (often also vasicentric tracheids). Wood rays uniseriate or multiseriate, homocellular or heterocellular. Axial parenchyma apotracheal diffuse or diffuse-in-aggregates, or paratracheal aliform, confluent or vasicentric, or in bands. Sieve tube plastids Ss, Psc or Psf type. Nodes usually 3:3, trilacunar with three leaf traces (rarely bilacunar). Parenchyma with oil cells. Prismatic calciumoxalate crystals often frequent.

Leaves Alternate (spiral or distichous), simple, entire, coriaceous, with supervolute ptyxis. Stipules and leaf sheath absent. Petiole vascular bundle transection arcuate to amphicribral. Venation pinnate, brochidodromous. Stomata usually paracytic (sometimes anomocytic). Cuticular wax crystalloids as rodlets or tubuli (often as clustered tubuli of Berberis type), chemically dominated by nonacosan-10-ol. Mesophyll with calciumoxalate druses, and idioblasts with sclereids (often branched), ethereal oils or resins. Leaf margin entire.

Inflorescence Terminal or axillary, compound, fasciculate, or raceme-like, or flowers solitary.

Flowers Actinomorphic. Hypogyny. Outer tepals two to four (to six), spiral or whorled, with valvate or imbricate aestivation, sepaloid, free or connate at base; inner tepals (one or) two to more than 50, with imbricate aestivation, usually petaloid, spiral or in one, two or four whorls, usually free (sometimes connate in lower parts; rarely absent). Nectary absent. Disc absent.

Androecium Stamens three to more than 100, spiral or whorled. Filaments free from each other or connate into tube, free from tepals. Microsporangia adaxial, abaxial, lateral or apical, non-versatile, usually tetrasporangiate (rarely disporangiate), usually latero-extrorse (sometimes extrorse or subintrorse), longicidal (dehiscing by longitudinal slits). Tapetum secretory or amoeboid-periplasmodial. Staminodia absent.

Pollen grains Microsporogenesis usually simultaneous (rarely successive). Pollen grains monoporate or monosulcate to trichotomosulcate, shed as monads or tetrads, bicellular at dispersal. Exine tectate or semitectate (rarely intectate), usually with columellate (rarely intermediary) infratectum, reticulate, microreticulate, or perforate.

Gynoecium Carpels one to more than 50, spiral, free or more or less connate, often not differentiated into ovary and style, often incompletely closed at anthesis, or carpels two to six connate into pistil; carpel conduplicate to plicate (rarely ascidiate), postgenitally completely or incompletely closed with or without an open canal filled with secretions. Ovary superior, unilocular to 20-locular. Style single, simple, or absent (pollen tube transmitting tissue well developed). Stigma apical or stigmas decurrent, papillate, Wet type. Pistillodium absent.

Ovules Placentation axile, laminar-lateral, submarginal or parietal. Ovules (one or) two to more than 100 per carpel, anatropous, hemianatropous or campylotropous, descending to ascending, apotropous, bitegmic, crassinucellar. Micropyle bistomal, often Z-shaped (zig-zag). Nucellar cap at least usually present. Megagametophyte monosporous, Polygonum type. Synergids at least usually with a filiform apparatus. Endosperm development cellular. Endosperm haustoria? Embryogenesis often irregular.

Fruit A syncarp with berry-like fruitlets, capsule, an assemblage of berries or a berry with persistent outer tepals.

Seeds Aril usually absent. Seed coat exotestal. Exotesta palisade, sclerotic. Mesotesta and endotesta unspecialized. Tegmen usually unspecialized. Perisperm not developed. Endosperm copious, oily (sometimes ruminate). Embryo small to large, straight or slightly curved, well differentiated, chlorophyll? Cotyledons two. Germination phanerocotylar.

Phytochemistry Flavonols (quercetin, dihydroquercetin), flavones, cyanidin monoterpenes, drimane sesquiterpenoids, proanthocyanidins, aporphine alkaloids, N-(cinnamoyl)-tryptamines, and lignoids present. Ellagic acids not found.

Winteranaceae Warb. in Engler et Prantl, Nat. Pflanzenfam., III, 6: 314. 14 Mai 1895 [’Winteranaceae (Canellaceae)’], nom. illeg.

Distribution Tropical East Africa, northeastern South Africa, Madagascar, southeastern United States, the West Indies, tropical South America.

Fossils Eocene wood, Wilsonoxylon edenense, was found in Wyoming (Boonchai & Manchester 2012). An ambiguous pollen fossil from the Oligocene of Puerto Rico is ascribed to Pleodendron (Friis & al. 2011).

Vegetative anatomy Phellogen ab initio superficial. Primary stem with continuous vascular cylinder a (pseudo)siphonostele. Cortical vascular system present. Vessel elements with scalariform, opposite or reticulate perforation plates; lateral pits scalariform or opposite, bordered pits. Vestured pits? Imperforate tracheary xylem elements tracheids with bordered pits, non-septate. Wood rays uniseriate, homocellular or heterocellular. Axial parenchyma apotracheal diffuse or diffuse-in-aggregates, or paratracheal aliform, confluent or vasicentric. Sieve tube plastids usually Psc type (in Canella Psf type, with fibrils but without protein crystalloids). Nodes usually 3:3, trilacunar with three leaf traces (sometimes bilacunar). Parenchyma with oil cells. Heartwood with gum-like substances etc. Prismatic calciumoxalate crystals abundant.

Leaves Alternate (spiral or distichous), simple, entire, coriaceous, with supervolute? ptyxis. Stipules and leaf sheath absent. Petiole vascular bundle transection arcuate. Lamina often gland-dotted. Venation pinnate. Stomata anomocytic (Cinnamosma, Warburgia) or paracytic (Canella, Cinnamodendron, Pleodendron). Cuticular wax crystalloids as rodlets or clustered tubuli (Berberis type), chemically dominated by nonacosan-10-ol. Mesophyll with crystal druses, and idioblasts with ethereal oils (and idioblasts with branched sclereids?). Leaf margin entire.

Inflorescence Terminal or axillary, compound, cymose (Canella) or raceme-like, or flowers solitary axillary. Floral prophylls (bracteoles) two, lateral.

Flowers Actinomorphic. Hypogyny. Outer tepals (bracts?) three, with imbricate aestivation, alternate or whorled, sepaloid, coriaceous, free or connate at base; inner tepals (three to) five to twelve, with imbricate aestivation, petaloid, spiral or in one, two or four series, usually free (in Canella connate at base; in Cinnamosma connate to a tube at lower part). Nectary absent. Disc absent.

Androecium Stamens usually six to twelve (in Cinnamosma c. 35 to 40), whorled. Filaments connate into a tube, free from tepals. Anthers abaxial (inserted at abaxial side of staminal tube), non-versatile, tetrasporangiate, extrorse, longicidal (dehiscing by longitudinal valves); connective often prolonged. Tapetum secretory. Staminodia absent.

Pollen grains Microsporogenesis simultaneous. Pollen grains monosulcate to trichotomosulcate, shed as monads, bicellular at dispersal. Exine usually tectate (sometimes semitectate), with columellate to intermediary infratectum, perforate to psilate (in Cinnamosma intectate, reticulate).

Gynoecium Pistil composed by two to six paracarp and connate carpels; carpel plicate, postgenitally incompletely fused, occluded by secretion, with open canal filled by secretions; internal compitum present. Ovary superior, unilocular. Style single, simple, short, thick. Stigmatic lobes two to six, papillate, type? Pistillodium absent.

Ovules Placentation parietal, with two to six massive placentae. Ovules two to more than 100 per carpel, hemianatropous to campylotropous, horizontal to ascending, bitegmic, crassinucellar. Micropyle bistomal, Z-shaped (zig-zag). Outer integument two to four cell layers thick. Inner integument two or three cell layers thick. Ovules in Cinnamosma possibly pachychalazal? Nucellar cap absent. Megagametophyte monosporous, Polygonum type. Endosperm development cellular? Endosperm haustoria? Embryogenesis?

Seeds Seeds in Canella and Pleodendron with rudimentary aril. Seed coat exotestal. Exotesta sclerotic (other parts indistinct). Mesotesta and endotesta unspecialized. Tegmen unspecialized. Perisperm not developed. Endosperm copious (in Canella and Cinnamosma ruminate), oily. Embryo small to relatively large, straight or slightly curved, well differentiated, chlorophyll? Cotyledons two. Germination?

Phytochemistry Monoterpenes, drimane sesquiterpenoids, aporphine alkaloids, N-(cinnamoyl)-tryptamines, and lignoids present. Flavonols, ellagic acid and proanthocyanidins not found. Aluminium not accumulated.

Systematics Canella (1; C. winterana; southern part of Florida Keys, Cape Sable, the West Indies Yucatan, Central America), Pleodendron (7; P. costaricense: Costa Rica; P. ekmanii, ‘Cinnamodendron angustifolium’, ‘Cinnamodendron ekmanii’: Hispaniola; P. macranthum: Puerto Rico; ‘Cinnamodendron corticosum’: Jamaica; ‘Cinnamodendron cubense’: Cuba), Cinnamosma (3; C. fragrans, C. macrocarpa, C. madagascariensis; Madagascar), Warburgia (4; W. elongata, W. salutaris, W. stuhlmannii, W. ugandensis; tropical East Africa, northeastern South Africa), Cinnamodendron (6; C. venezuelense: northeastern Venezuela; C. tenuifolium: Suriname; C. axillare, C. dinisii, C. occhionianum, C. sampaioanum: southern Brazil).

Canellaceae are sister to Winteraceae. The Central American-West Indian species Canella winterana is sister to the remaining Canellaceae, according to Marquínez & al. (2009) and Müller & al. (2015).

Drimyidaceae (Baill.) Baill. in Adansonia 7: 383, 384. Aug 1867 [‘Drimydeae’]; Takhtajaniaceae (J.-F. Leroy) J.-F. Leroy in Adansonia, sér. 2, 20: 20. 30 Mai 1980

Distribution Northern Madagascar, the Philippines, Malaysia, Indonesia, New Guinea, Moluccas to Solomon Islands, eastern Australia, Tasmania, Lord Howe, New Caledonia, New Zealand, Mexico to Magellan’s Strait, Juan Fernández Islands, with their highest diversity in Queensland and New Caledonia. Mainly in subtropical montane forests.

Fossils Walkeripollis are fossil pollen tetrads with reticulate exine and columellate infratectum described from the Late Barremian or the Early Aptian of Gabon and from the Late Aptian to the Early Albian of Israel. Pseudowinterapollis was described from the Campanian to the Maastrichtian of Australia. The fossil wood Winteroxylon has been found in Late Santonian to Early Campanian layers from James Ross Island, Antarctica. Cenozoic records of Winteraceae are known from Germany, South Africa, Australia, New Zealand, Antarctica and South America.

Habit Usually bisexual (sometimes monoecious or polygamomonoecious; Tasmannia usually dioecious), evergreen trees or shrubs (rarely epiphytic; Drimys piperita with lignotuber). Wood aromatic.

Vegetative anatomy Phellogen ab initio superficial. Primary stem with continuous vascular cylinder as eustele or (pseudo)siphonostele. Medulla sclerenchymatous. Pericyclic sclerenchyma of various origin. Vessels absent. Vestured pits present. Imperforate tracheary elements tracheids with usually two or three rows of circular bordered pits (in some species of Zygogynum sometimes with scalariform perforation plates), non-septate (also vasicentric tracheids). Wood rays multiseriate (up to more than 10-seriate), heterocellular. Axial parenchyma apotracheal diffuse, diffuse-in-aggregates or in tangential bands. Sieve tube elements without sharp distinction between sieve surfaces of sieve plates and lateral sieve surfaces. Sieve tube plastids Ss type (Drimys, Pseudowintera) or Psc type (Drimys, Tasmannia, Zygogynum), with few to numerous starch grains. Nodes 3:3, trilacunar with three leaf traces. Parenchyma with oil cells. Sclereids and calciumoxalate crystals (prismatic?, druses?) often abundant.

Leaves Alternate (spiral), simple, entire, coriaceous, with supervolute ptyxis. Stipules and leaf sheath absent. Petiole vascular bundle transection arcuate or hippocrepomorphic to amphicribral. Venation pinnate, brochidodromous. Stomata usually paracytic (in Takhtajania mostly anomocytic). Cuticular wax crystalloids as clustered tubuli (Berberis type), chemically dominated by nonacosan-10-ol. Mesophyll with idioblasts with ethereal oils, sclerenchymatic idioblasts (with branched sclereids) and cells with isoprenoid resins. Lamina often gland-dotted. Leaf margin entire.

Inflorescence Terminal or axillary, fasciculate or other cymose inflorescence types, or flowers solitary. Floral prophylls (bracteoles)?

Flowers Usually actinomorphic (sometimes slightly bisymmetric). Hypogyny. Outer tepals two to four (to six), spiral to almost whorled, with valvate aestivation, sepaloid, caducous, often connate in bud to an early dehiscent calyptra; inner tepals two to more than 50 (rarely one), with imbricate aestivation, usually petaloid, usually free (rarely absent). Nectary absent. Disc absent.

Androecium Stamens three to more than 100 (very rarely up to c. 370), spiral. Filaments thick, foliaceous, free from each other and from tepals. Microsporangia dorsal, lateral or apical, non-versatile, usually tetrasporangiate (rarely disporangiate), usually latero-extrorse (sometimes subintrorse; thecae sometimes transversely arranged; ’sides’ of thecae sometimes erect), longicidal (dehiscing by longitudinal slits); connective often undeveloped (in Zygogynum sometimes prolonged). Tapetum secretory or amoeboid-periplasmodial. Staminodia absent.

Pollen grains Microsporogenesis usually simultaneous (in Drimys and Pseudowintera successive). Pollen grains usually monoporate (rarely monosulcate; in Takhtajania monoporate to trichotomosulcate), usually shed as acalymmate tetrads (in four species of Zygogynum as monads), bicellular at dispersal. Exine usually semitectate (rarely tectate), with columellate infratectum, usually reticulate (in Zygogynum sometimes microreticulate).

Gynoecium Carpels few to more than 50 (in Pseudowintera traversii usually one; in Takhtajania two), spiral, free or partially connate (in Zygogynum syncarpously connate; in Takhtajania paracarpously connate forming usually unilocular pistil); carpel usually plicate (sometimes secondarily? ascidiate), without canal, foliaceous, stipitate or sessile, often not differentiated into ovary and style, incompletely closed during anthesis and postgenitally completely occluded, or completely closed and with short stylodium; internal compitum present in Takhtajania, partial compitum present in Pseudowintera and Zygogynum. Ovary superior, unilocular (often apocarpy, rarely monomerous), or bi- to 20-locular. Style single or absent. Stigma apical (on style) or stigmas decurrent (on ovaries without style), papillate, Wet type. Pistillodium absent.

Ovules Placentation axile (when ovary syncarpous) or laminar-lateral, laminar-diffuse or submarginal (apical-subapical?; in Takhtajania parietal). Ovules (one to) five to more than 100 per carpel, anatropous, descending, apotropous, bitegmic, crassinucellate. Micropyle bistomal. Outer integument three two five cell layers thick. Inner integument two to four cell layers thick. Nucellar cap present. Parietal tissue two to six cell layers thick. Hypostase present. Megagametophyte monosporous, Polygonum type. Synergids with a filiform apparatus. Endosperm development cellular. Endosperm haustoria? Embryogenesis irregular.

Fruit A syncarp with berry-like fruitlets (sometimes hard due to presence of stone cells), a capsule or an assemblage of berries.

Seeds Aril absent. Seed coat exotestal. Exotesta palisade, sclerotic, composed of epidermis of outer integument. Mesotesta and endotesta unspecialized. Exotegmen unspecialized. Endotegmen sometimes subfibrous. Perisperm not developed. Endosperm copious, oily. Embryo very small, well differentiated, chlorophyll? Cotyledons two. Germination phanerocotylar.

Cytology n = 13 (Tasmannia), 18 (Takhtajania), 43 (Drimys) – Polyploidy rarely occurring (Zygogynum baillonii, 2n = 172).

Phytochemistry Flavonols (quercetin, dihydroquercetin), flavones, prenylated flavanones, cyanidin, monoterpenes, drimane sesquiterpenoids, proanthocyanidin, and lignoids present. Alkaloids not found (or present in some species?). Ellagic acid not found. Aluminium accumulated in some species.

Systematics

Winteraceae are sister group to Canellaceae with very high support.

The absence of vessels in the wood (replaced by tracheids) and the presence of plicate carpels are secondarily derived (Young 1981; Marquínez & al. 2009). The stomata in many species of Winteroideae are provided with plugs of wax and cutin, that close the stomatal apertures in order to prevent them from rain water. This is interpreted as a secondary adaptation to moist (southern) temperate and mountainous habitats (Marquínez & al. 2009).

Winteraceae have a very disjunct distribution. Takhtajania occurs in a small rainforest area in northeastern Madagascar. Tasmannia has its main distribution in eastern Australia, Tasmania and New Guinea, but is also present on Borneo, Sulawesi and in the Philippines. Drimys is distributed from southern Mexico to northernmost Peru, in southeastern Brazil and in the southern parts of Chile, and Juan Fernández. Pseudowintera is endemic in New Zealand. Zygogynum (now including Belliolum, Bubbia and Exospermum) occurs in eastern Australia, New Guinea, New Caledonia and the Moluccas. Fossil Winteraceae are known from many places outside their extant distribution: Central and southern Africa, Israel, Germany, Argentina and Antarctica. This indicates that the group was widely distributed during the Cretaceous and the Paleogene, above all on the Gondwanan continents. From the Oligocene onwards the distribution seems to have declined gradually, most probably accompanied by large-scale extinctions. Much of the speciation of, e.g., Drimys and Pseudowintera, probably took place after the Miocene uplift of the Central Andes and New Zealand (Marquínez & al. 2009).

Takhtajanioideae J.-F. Leroy in Adansonia, sér. 2, 17: 393. 1978

1/1. Takhtajania (1; T. perrieri; northeastern Madagascar). – Dioecious tree. Stomata usually anomocytic. Pollen grains monoporate to trichotomosulcate. Pollen tetrads larger than in Winteroideae. Carpels two, paracarpously connate. Placentation subapical-parietal. Outer integument four or five cell layers thick. Inner integument two to four cell layers thick. Parietal tissue five or six cell layers thick. n = 18. – Takhtajania perrieri is sister to the remaining Winteraceae.

Winteroideae

4/c 110. Tasmannia (c 40; the Philippines, Borneo, Sulawesi, New Guinea, eastern Australia), Drimys (c 8; southern Mexico to southern Patagonia), Pseudowintera (3; P. axillaris, P. colorata, P. traversii; New Zealand, Stewart Island), Zygogynum (c 60; New Caledonia). – Disjunct distribution on the Southern Hemisphere. Bisexual or dioecious (most species of Tasmannia) trees or shrubs. Vestured pits sometimes present in tracheids. Sieve elements with non-dispersive protein bodies. Stomata usually paracytic. Carpels (one to) five to numerous. Outer integument three or four cell layers thick. Inner integument two or three cell layers thick. Parietal tissue two to five cell layers thick. Fruit berry-like (sometimes a follicle). Sesquiterpene dialdehyde cinnamates present. n = 13, 43. – Tasmannia, sister to the clade [Drimys+[Pseudowintera+Zygogynum]], has larger chromosomes, and the interphase nuclei are different from those in Drimys (Ehrendorfer & Lambrou 2000).

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PIPERANAE Reveal

CANELLALES Cronq.

CANELLACEAE Mart.

WINTERACEAE R. Br. ex Lindl.