sign in sign up
<<
Home , Fraxinus americana, Fraxinus angustifolia, Fraxinus anomala, Fraxinus caroliniana, Fraxinus chinensis, Fraxinus cuspidata

studiedagen – journées d’étude: Systematics and fl oral evolution in Fraxinus ()

Eva Wallander 1)

Summary – Th e genus Fraxinus is one of 24 genera in the family Oleaceae. Fraxinus currently consists of 48 accepted and shrubby species distributed from the tropics to temperate regions of the northern hemisphere. About one third of the species is -pollinated and has small, white, scented fl owers borne many together in showy terminal panicles. Th e other two thirds are wind-pollinated, with apetalous and usually unisexual fl owers borne in tight lateral panicles or racemes. Unisexual fl owers have evolved on three separate occasions from bisexual ones in wind-pollinated species. Th e genus is divided into six sections: Fraxinus, Sciadanthus, Paucifl orae, Melioides, Ornus and Dipetalae. Th ese sections contain 45 species plus a few recognised subspecies. Th ree species are unclassifi ed due to uncertain positions in the phylogenetic tree. Th is latest classifi cation of the genus is based on an updated version of Wallander’s (2008) phylogenetic tree, which is based both on molecular and morphological data. A key to the sections is given as well as a systematic table with all accepted taxa, common syno- nyms and geographic distribution. Each section is presented along with some common, botanically interesting or commercially important species.

Oleaceae, the olive family occur in Chionanthus and Fraxinus, and apetalous fl owers occur in Nestegis, Forestiera, Oleaceae is a family of about 600 species in 24 and wind-pollinated species of Fraxinus. Th e extant genera (Wallander & Albert 2000). ovary is syncarpous (carpels fused), consisting Th ey occur all over the world in tropical, sub- of two carpels. types range from loculi- tropical and temperate climates. Phylogeneti- cidal capsules (with two locules), woody schiz- cally, the family is near the base in the order ocarps (a dry fruit type that splits in two . Th e largest genus in the family parts), and samaras to berries and drupes. is Jasminum with about 200 species. Other Most of the species in the family are insect- well-known genera in the family are Forsythia pollinated with petaliferous, fragrant and nec- (11 spp.), Ligustrum (45 spp.), Syringa tariferous fl owers (e.g. Jasminum, Forsythia, (20 spp.), Olea (40+ spp.) and Fraxinus. Ligustrum, Syringa, Chionanthus). Six of the Th e species are , or woody genera in the family contain species with climbers with opposite, simple or compound wind-pollinated fl owers (Fraxinus, Forestiera, without stipules. Th e fl owers are hyp- Priogymnanthus, Nestegis, Phillyrea and Olea). ogynous (petals and sepals attached under the ovary) and four-merous, generally with two 1) Dr Eva Wallander, Nature Conservancy, stamens, but four stamens occur in some spe- County Administrative Board, SE 551 86 Jönköping, cies. Th e corolla is actinomorphic (radial sym- Sweden. metric) and usually sympetalous. Free petals [[email protected], www.oleaceae.info] systematics and floral evolution in FRAXINUS (oleaceae)

Th ese have no corolla, or a reduced open semi-evergreen in tropical climates. Th e fl ow- corolla, with no nectar or fragrance. A calyx ers are borne in panicles or rarely racemes. may be present or not. Some species are both Th ey have four (rarely two), free (united in wind- and insect-pollinated (e.g. species of two species), linear petals and a small synse- Olea and Fraxinus). palous calyx. In wind-pollinated fl owers the petals or both petals and calyx are missing. Th e fruit is a samara, normally one-seeded. The genus FRAXINUS, the ash trees Fraxinus contains both wind- and insect- pollinated species and the breeding systems Since Linnaeus described the genus Fraxinus range from hermaphrodites via androdioecious in 1753, almost 800 taxa (species, subspecies and polygamous to dioecious species (see and varieties) have been described. Obviously Box 1). Th irty-four species are wind-pollinated most of these are synonyms and Wallander and dioecy has evolved on three separate occa- (2008) accepted 43 species. Later, fi ve more sions after the evolution of wind-pollination American and one Chinese species were (Wallander 2001, 2008). Dioecy evolved accepted and two Asian species merged into once via androdioecy and twice via polygamy one so currently there are 48 accepted species as intermediate steps [Ill. 1]. Some of the 14 (table 1). insect-pollinated species might in fact be both Th e species of Fraxinus are distributed wind- and insect-pollinated, as evidenced by around the northern hemisphere, from tropi- the protruding anthers and copious pollen cal to temperate climates. Th e two main cen- production. Many of them are androdioecious, tres of distribution are and and it is hypothesised that this was an impor- . Th ey are mostly large or small trees, but tant prerequisite in the evolution of wind- some shrubby species occur mainly in arid pollination with loss of corolla and later areas. Th e leaves are characteristically oddly completed unisexuality (Wallander 2001). pinnately compound but a few species or Androdioecy is a very rare breeding system subspecies have simple leaves by reduction elsewhere among angiosperms but in Oleaceae (F. anomala 2)). All species are except and in particular Fraxinus there are many F. griffi thii and F. uhdei which are evergreen or androdioecious species (Wallander 2001).

Box 1. Explanation of diff erent breeding systems that occur in Fraxinus.

Hermaphroditism: all trees have only bisexual (hermaphrodite) fl owers Androdioecy: separate male trees (with only male fl owers) and hermaphrodite trees (with only bisexual fl owers) Andromonoecy: only one type of tree with both unisexual male and bisexual fl owers Polygamy: a mixture of trees with only male, or only female, or only hermaphrodite fl owers, or trees with mixed unisexual and bisexual fl owers in the same or diff erent infl orescences Dioecy: separate male trees (with only male fl owers) and female trees (with only female fl owers)

2) Authors of all species names mentioned in the text are given in table 1.

Belgische Dendrologie Belge 2012 39 studiedagen – journées d’étude: FRAXINUS

cubensis (DC.) Voss, (DC.)Voss, (S. Wats.) (S. F. viridis F. berlandieriana L. subsp. subsp. L. Carr. coriacea Mill. subsp. subsp. Mill. Buckl., Buckl., A. J. Willmott J. A. Lam. var. var. Lam. var. var. berlandieriana

F. americana F. F. turkestanica F. Torr. F. trialata F. (Wesmael) Mill. (Wesmael) pubescens F. pallisiae F.

(Griseb.) E. Murray E. (Griseb.) F. caroliniana F. F. Michx. f. f. Michx. Lingelsh. A. Gray, Gray, A. Bunge, Bunge, (Torr.) Lewis & Epling (Torr.) oregona Wenz., Wenz., cubensis texensis pistaciaefolia F. viridis F. F. sogdiana F. F. rehderiana F. F. trifoliata F. lindheimeri L. var. var. L. (Rupr.) S. S. Sun S. S. (Rupr.) (DC.) Wesmael, (DC.)Wesmael, Marsh. subsp. subsp. Marsh. Marsh. var. var. Marsh. (Beadle) J.Wright (Griseb.) Lingelsh., Lingelsh., (Griseb.) Nutt., Nutt., Herder, Herder, M. Bieb. (nom. illeg.), illeg.), (nom. Bieb. M. (Buckley) Schelle Moran, T. S. Brandeg. S. T. Lam. var. var. Lam. (DC.) A. Gray, Gray, (DC.) A. F. americana F. (S. Wats.) Rehd., F. Rehd., Wats.) (S. cubensis cubensis mandshurica F. triptera F. trialata berlandieriana F. parryi F. biltmoreana F. oxyphylla F. potosina

F. pennsylvanica F. F. potamophila F. F. pennsylvanica F. F. (2008). F. pubescens F. coriacea Lam. Mill. var. Mill. Scheele L. var. L. Michx., Michx., L. var. var. L. berlandieriana var. Willd., Willd., Nutt., Nutt., (Gray) Sarg., (Gray) Sarg., Boiss., Boiss., Lingelsh., Lingelsh., Sarg., Sarg., Michx. var. var. Michx. ALLANDER Marsh. subsp. subsp. Marsh. (Gray) G. N. Miller N. G. (Gray) syriaca

F. caroliniana F. F. sambucifolia F. texensis F. F. oregona F. F. velutina velutina F. F. platycarpa F. F. americana F. F. viridis F. Michx. var. var. Michx. F. F. americana F. F. coriariifolia F. nigra F. F. lowelli F. jonesii F. F. oxycarpa F. (Griseb.) Borh., Borh., (Griseb.) (DC.) Wenz., (DC.) Wenz., texensis Based on Table 2 in W 2 in Table Based on (Oleaceae) listing the 48 accepted species and 3 subspecies, their geographical distribution and common synonyms. synonyms. distribution and common their geographical species and 3 subspecies, (Oleaceae) listing the 48 accepted Fraxinus SE USA Cuba(S ), N Mexico to Central Turkey C& E Mexico NE, SW USA, SW , NW Africa SW Europe, SE& C Europe and around the Blackand around Sea cation of cation (Willd.) (Boiss.)Yalt. angustifolia oxycarpa syriaca (Lingelsh.) E. Nikolaev(Lingelsh.) E. (Endl.) Lingelsh. DC. Michx. C Canada E USA, & C Rupr. E Russia Korea, Japan, China, Beadle E USA Vahl subsp. subsp. Vahl Vahl subsp. subsp. Vahl Mill. SE USA Vahl subsp. subsp. Vahl Revised infrageneric classifi L. E USA& SE Canada Torr. ex S. Wats. ex S. Torr. C Mexico SW USA, Buckl. Buckl. ), SW USA(, Griseb. S. Wats. S. NW SW Mexico USA, L. W Russiato N& C Europe Hook. & Arn. Hook. NW SW Mexico USA, Benth. Benth. SW Canada W USA, Melioides Dipetalae Fraxinus Marsh. SE Canada E USA, Table 1. – Table F. cubensis cubensis F. Section F. latifolia F. F. albicans F. F. coriacea F. F. caroliniana F. F. nigra F. F. biltmoreana F. F. americana F. berlandieriana F. F. excelsior F. Sections and speciesSection Geographic distribution Synonyms angustifolia F. F. mandshurica F. F. anomala F. F. quadrangulata F. Section F. angustifolia F. F. dipetala F. angustifolia F. Franco & Rocha Afonso Franco

40 Belgische Dendrologie Belge 2012 systematics and floral evolution in FRAXINUS (oleaceae)

Hance F. stylosa F. Lundell, Lundell, Hemsley, Hemsley, Lingelsh., Lingelsh., M. E. Jones, E. M. Marsh. var. var. Marsh. E. J. Palmer J. E. F. chiapensis F. F. bracteata F. (Bush) A. E. Murray E. (Bush) A. F. szaboana F. F. rhynchophylla F. ashei Hand.-Mazz., Hand.-Mazz., var. var. F. attenuata F. Merr., Merr., profunda S. S. Sun, S. S. Lingelsh., Lingelsh., F. pennsylvanica F. Michx. f. (nom. rej.) (nom. f. Michx. Britt. F. odontocalyx F. F. profunda F. Bush, Bush, Standley & Steyerm., Standley& Steyerm., F. philippinensis F. Marsh. subsp. subsp. Marsh. F. medicinalis F. F. sargentiana F. F. toumeyi F. (Torr.) G. N. Miller, N. G. (Torr.) profunda F. tomentosa F. Lingelsh., Lingelsh., Hayata, Hayata, Blume ex K. Koch ex K. Blume Rehder, Rehder, F. cavekiana F. Rehd., Rehd., Lam., L. var. var. L. velutina velutina (Tang) Chü ex J.Z.Liu Chü (Tang) Champ. ex Benth., ex Benth., Champ. F. hybrida F. Sarg. F. pennsylvanica F. Wenzig, F. japonica F. F. formosana F. F. standleyi F. F. pubescens F. F. retusa F. hopeiensis hopeiensis F. lingelsheimii F. F. americana F. coriacea uhdei Lingelsh. Marsh. subsp. Marsh. J. L. Wu & Z. W. Xie, Xie, W. Z. & Wu L. J. var. Hance, Feng ex P. Y. Bai Y. ex P. Feng Torr., Torr., Lingelsheim Standley L. var. L. L. var. L. S.K. Lee & F.N. Wei F.N. Lee& S.K. Borkh., Borkh., Lingelsh., Lingelsh., Britt., Britt., (Wenzig) Sarg., Sarg., (Wenzig) Hemsl., Hemsl., F. fallax F. J. L. Wu, Wu, L. J. Nakai (Bush) Sudworth, (Bush) Sudworth, huashanensis oridana michauxii

F. yunnanensis F. F. americana F. hondurensis F. pennsylvanica F. caudata F. F. fl F. F. lanceolata lanceolata F. F. insularis F. F. guilinensis F. Lingelsh., Lingelsh., ferruginea F. F. americana F. F. borealis F. F. rhynchophylla rhynchophylla F. F. rhynchophylla F. F. pistaciaefolia F. F. retusifoliolata F. var. var. profunda ailand ailand Himalaya through N China, Korea, Japan, Japan, Korea, N China, SE Russia SW Asia China, Korea, , Vietnam, Korea, China, to SE Asia Th

rhynchophylla chinensis Hara Japan Marsh. S Canada C& E USA,

Hemsl.Th China, (Boehm.) DC. Koidz. Japan Sieb. & Zucc. Sieb. Japan Wall. Tang China Diels China Lingelsh. Himalaya Nutt. SE USA DC. China (Bush) Bush Canada E USA, Torr. N& C Mexico SW USA, Lingelsh. N Mexico SW USA, Roxb. subsp. subsp. Roxb. Roxb. subsp. subsp. Roxb. C. B. Clarke B. C. SE Asia Britt. E USA Ornus ora L. & E C Mediterranean, (Wenzig) Lingelsh.(Wenzig) cult. , C America, thii oribunda profunda

F. velutina velutina F. F. paucifl F. F. F. pennsylvanica F. Sections and species papillosa F. Geographic distribution Synonyms F. griffi F. F. chinensis F. F. smallii F. F. lanuginosa F. longicuspis F. F. hopeiensis hopeiensis F. F. fl F. uhdei F. F. micrantha F. ornus F. F. malacophylla F. Section F. baroniana F. bungeana F. chinensis F. F. apertisquamifera F. (Hance) E. Murray (Hance) E.

Belgische Dendrologie Belge 2012 41 studiedagen – journées d’étude: FRAXINUS

Torr. ora F. depauperata F. parvifl W.W. Smith, Smith, W.W. Standley& Steyerm. F. suaveolens F. Schlecht. & Cham. var. var. & Cham. Schlecht. Schlecht. & Cham. Schlecht. F. vellerea F. F. schiedeana F. F. schiedeana F. M. E. Jones, Jones, E. M. Eastw. (Lingelsh.) Hand.-Mazz., (Lingelsh.) Hand.-Mazz., Lingelsh. Coss. & Dur. Coss. Lundell, S. Y. Hu Y. S. Hook. f. Hook. Standley & Steyerm., Standley& Steyerm., F. nummularis F. F. sikkimensis F. F. punctata F. petenensis F. F. mariesii F. F. bicolor F. F. spaethiana F. F. dimorpha F. macropetala F. (Lingelsh.) Z. Wei (Lingelsh.) Z. SW USA N Mexico (), C Mexico E Mexico, Guatemala E Mexico, China (Sonora) (Coss. et Dur.) Lingelsh. et Dur.) (Coss. (Lingelsh.) E. Wallander (Lingelsh.) E. (G. Don) Wall. ex DC. Wall. Don) (G. NW Africa, Himalaya orae Nakai Korea Blume Korea Japan, China, W. W. Smith W. W. China Little Regel C Asia S. Z. Qu, C. B. Shang& B. C. Qu, Z. S. Oliv. Japan China, Torr. N Mexico SW USA, Lingelsh. C Mexico Brandegee Guatemala NE& C Mexico, Lingelsh. China Himalaya, A. Gray A. NE& SW USA(Texas), Paucifl Sciadanthus (Willd. ex Schult. & Schult. f.) f.) & Schult. (Willd. ex Schult. F. greggii F. Sections and species paxiana F. Geographic distribution Synonyms F. gooddingii F. F. raibocarpa F. sieboldiana F. F. purpusii F. P. S. Green & M. Nee & M. Green S. P. F. dubia F. F. trifoliolata F. Section F. rufescens F. Section F. chiisanensis chiisanensis F. platypoda F. F. hubeiensis F. Su L. P. F. xanthoxyloides F. sedis Incertae cuspidata F.

42 Belgische Dendrologie Belge 2012 systematics and floral evolution in FRAXINUS (oleaceae)

1 – Phylogeny of Fraxinus based on molecular and morphological data with some morphological traits mapped on the tree. [E. Wallander]

Phylogeny and classification tional key below (updated from Wallander 2008) gives the diagnostic characters of the A nearly complete phylogeny of the genus sections. More information is given for the Fraxinus was reconstructed based on molecular sections and some species in each section fur- and morphological data (Wallander 2008) ther below. A vegetative key to cultivated spe- and updated for the present article with some cies of Fraxinus in Western Europe is given by missing species (Wallander, unpublished De Langhe (2012). data), see Ill. 1. Th e genus is clearly monophy- letic and has strong molecular support. Th e genus Fraxinus is classifi ed into six Sectional key sections (Wallander 2008): Fraxinus, Sci- adanthus, Paucifl orae, Melioides, Ornus and Th is key to the sections of Fraxinus does not Dipetalae (table 1). Th ese sections contain 45 cover the two unplaced species F. platypoda species and a few subspecies. Th ree species are and F. chiisanensis (some of their traits are unclassifi ed (incertae sedis) due to uncertain found in both the sections Melioides and positions in the phylogenetic tree. Th e sec- Fraxinus).

Belgische Dendrologie Belge 2012 43 studiedagen – journées d’étude: FRAXINUS

1. Infl orescences emerging with the leaves on current year shoots from terminal ; fl owers with 4, free, white petals, or apetalous, always with calyx; hermaphrodites, androdioecious or dioecious; 16 Old World species ...... section Ornus 1. Infl orescences emerging from lateral buds on previous year’s shoot, before or at the same time as the leaves emerge from terminal buds; fl owers with 2-4 united petals or apetalous, with or without calyx; hermaphro- dites, polygamous, or dioecious; New World or Old World species 2. Stems quadrangular; fl owers mostly bisexual, with 2 united petals or without petals; 3 New World species ...... section Dipetalae 2. Stems terete; fl owers uni- or bisexual, with 4 united petals or without petals; New World or Old World species 3. Corolla with 4 united petals; 1 New World species ...... F. cuspidata 3. without petals; New World or Old World species 4. Shrubs or small trees; rachis ± winged; fl owers with calyx; polygamous 5. Few-fl owered, cymose panicles; samaras small (1.5-2.5 cm); 5 New World species ...... section Paucifl orae 5. Many-fl owered and dense, cymose panicles; samaras large (3-5 cm); 2 Old World species ...... section Sciadanthus 4. Mostly large trees; leaf rachis not winged; fl owers with or without calyx; dioecious or polygamous 6. Flowers without calyx or with small and/or deciduous calyx; polygamous or dioecious with rudimentary stamens; cavity of samara fl attened; 3 Old World and 1 New World species ...... section Fraxinus 6. Flowers with calyx; strictly dioecious; seed cavity of samara terete or fl attened; 15 New World species ...... section Melioides

Section FRAXINUS In Europe, the Common ash F. excelsior [Ill. 2a-c] is the most common and well- Th e section Fraxinus comprises four species; known species. It is a large tree (normally up one American (F. nigra), two mainly Euro- to 35 m but even taller trees up to 46 m can be pean (F. excelsior and F. angustifolia) and one found) distributed in central and northern East Asian species (F. mandshurica). Th ey are Europe and commercially important in central all relatively large and wind-pollinated trees. Europe. In the last decade, however, an ash Th e species of this section are either polyga- disease caused by the fungus Chalara fraxinea mous (F. nigra and F. excelsior), andromonoe- (Pautasso et al. 2013) has spread fast, aff ect- cious (F. angustifolia) or dioecious (F. mand- ing its survival and future use. Th e fl owers shurica). Th e male fl owers consist of two are either male, hermaphrodite or female and stamens, the hermaphrodite fl owers of one normally occur in sexually pure infl orescences, pistil and two stamens, and the female fl owers but mixes of male and hermaphrodite fl owers of one pistil and more or less rudimentary sta- are not uncommon. Female fl owers may have mens. Th e fl owers are without a calyx, or have a continuum of more or less rudimentary a reduced or deciduous calyx. Th ey are distin- stamens, ranging from functionally female guished from the strictly dioecious species of to hermaphrodite. Th e species has therefore the section Melioides in having a fl attened seed been termed polygamous but recent research cavity of the samara (versus terete in the sec- has shown that it is functionally dioecious tion Melioides) and foliar terminal scales (FRAXIGEN 2005, Bochenek & Eriksen (versus entire in the section Melioides). 2010, Bochenek 2011). Th e protogynous

44 Belgische Dendrologie Belge 2012 systematics and floral evolution in FRAXINUS (oleaceae)

2 – (a) Male infl orescences (panicles) of shedding pollen in spring, (b) female infl orescences with rudimentary stamens, and (c) foliage with young and green (samaras) in early summer. Göteborg, Sweden [E. Wallander, 6-05-2006, 6-05-2006 & 5-06-1997]

3 – (a) Hermaphrodite fl owers of in a raceme (as opposed to F. excelsior’s panicle) and (b) leaves with narrow and serrate leafl ets. Göteborg, Sweden [E. Wallander, 4-05-1995] and Ronda, [E. Wallander, 31-03-2000]

Belgische Dendrologie Belge 2012 45 studiedagen – journées d’étude: FRAXINUS hermaphrodite fl owers have stamens with fer- tile pollen but are rendered functionally female because the pollen of pure male trees is released earlier and thus outcompete the later hermaphrodite pollen in cross-pollinations on other females and hermaphrodites. However, hermaphrodites can successfully self-pollinate if no male trees are in the vicinity. Fraxinus angustifolia, the Narrow-leaved ash, includes a complex of taxa that have not yet been fully clarifi ed due to large variation in morphology. Th ree geographical subspecies are 4 – Fraxinus pallisiae, with pubescent leaves and shoots, is recognised: F. angustifolia subsp. angustifolia in treated as a synonym of F. angustifolia subsp. oxycarpa. In southwestern Europe and northwestern Africa, F. angustifolia it is common to fi nd buds and leaves in whorls F. angustifolia subsp. oxycarpa in southeastern of three instead of opposite. Von Gimborn Arboretum, The Netherlands [E. Wallander, 6-10-2012] and central Europe and F. angustifolia subsp. syriaca from Turkey to Central Asia. Th e trees can reach over 30 m in height. Th e leafl ets are angustifolia diff ers morphologically from relatively narrow with a distinct serrate or F. excelsior and is andromonoecious (FRAXI toothed margin [Ill. 3b] but leaf and shoot GEN 2005). In contrast to all other taxa of the pubescence and leafl et morphology within this genus, which have compound paniculate infl o- complex is too variable to deserve specifi c rescences, F. angustifolia (including all its syno- recognition. Th erefore F. pallisiae [Ill. 4], nyms) has simple, unbranched racemes with pubescent leaves and shoot, is treated as [Ill. 3a]. Also, it usually has leaves and buds in a synonym of F. angustifolia subsp. oxycarpa. whorls of three [Ill. 4] instead of the normal Fraxinus potamophila and F. sogdiana in the opposite leaves. Th e bud colour is brown Turkestan region are treated as synonyms of contrasting to the black colour of F. excelsior F. angustifolia subsp. syriaca but more studies buds. Additional characters for distinguishing are needed to confi rm their status. Fraxinus between F. angustifolia and F. excelsior are listed

5 – (a) Female fl owers of Fraxinus mandshurica, with rudimentary anthers. (b) The leaves are relatively large, up to 40 cm long, with conspicuous tufts of rufous hair where the leafl ets attach to the rachis. Göteborg Botanical Garden, Sweden [E. Wallander, 8-05-2000 & 2-07-1997]

46 Belgische Dendrologie Belge 2012 systematics and floral evolution in FRAXINUS (oleaceae) by FRAXIGEN (2005). Fraxinus angustifolia is closely related to F. excelsior and they have also been shown to be able to hybridise (Raquin et al. 2002, Fernandez-Manjarres et al. 2006, Heuertz et al. 2006). Th e Manchurian ash F. mandshurica is a large (up to 30 m), commercially important, timber tree in eastern Asia (China, eastern Russia, Japan and Korea). It is dioecious with anther rudiments in female fl owers [Ill. 5a]. It is most closely related to F. nigra (Black ash) in eastern North America [Ill. 6].

Section SCIADANTHUS

Th e section Sciadanthus, which is sister to the section Fraxinus, consists of only two Old World species: F. xanthoxyloides [Ill. 7], dis- tributed from Morocco and Algeria through the Middle East to the Himalayas, and F. 6 – Leaves of , hubeiensis, which is a threatened species which is closely related to F. mandshurica. [K. Kanoti, Maine Service, Bugwood.org] endemic to the Hubei province in China. Th ey are both relatively small trees or shrubs, and characterised by apetalous fl owers with calyx, ers in their congested, cymose panicles, and except that the male fl owers of F. xanthoxyloi- larger samaras. Th e leaves are relatively small des lack calyx. Th e fl owers are polygamous and (7-15 cm) with a more or less winged leaf- wind-pollinated. Th ey resemble the New rachis. Compared to the next section the World Paucifl orae, but have many more fl ow- samaras are in larger clusters.

7 – (a) A hermaphrodite infl orescence of Fraxinus xanthoxyloides and (b) its foliage with small compound leaves. Göteborg Botanical Garden, Sweden [E. Wallander, 28-04-2004 & 26-06-1997]

Belgische Dendrologie Belge 2012 47 studiedagen – journées d’étude: FRAXINUS

Section PAUCIFLORAE central Mexico). Th e other two, F. dubia and F. purpusii, occur in Mexico and Guatemala. Th e section Paucifl orae consists of fi ve New Except for F. greggii, the species in this section World species that occur in arid regions of are poorly known and especially the latter two southwestern USA, Mexico, and Guatemala. species are in need of a deeper study. Th ey are shrubs or small trees with small cori- aceous leaves. In common with the two species of section Sciadanthus , the leaves have winged Section MELIOIDES rachises, but in contrast they have few-fl ow- ered panicles [Ill. 8b]. Th e fl owers are polyga- Th e section Melioides contains 15 American mous, apetalous, and wind-pollinated. Th e species. Th ey are all medium-sized to large samaras are relatively small and have a persis- dioecious trees. Th e unisexual fl owers are tent calyx. apetalous and wind-pollinated. Th e female Fraxinus greggii (Gregg’s ash, or Littleleaf fl owers consist of a calyx and one pistil, and ash) [Ill. 8a-b], occurring in Texas and north- the male fl owers of two stamens with elon- eastern and central Mexico, is closely related gated anthers and a small calyx. Th ere are no to F. gooddingii (restricted to Arizona in USA rudimental organs of the opposite sex in the and Sonora in Mexico) and F. rufescens (in fl owers [Ill. 13b]. Th e calyx is persistent in the samaras, which have a distinctly terete seed cavity in most species (more fl attened in F. caroliniana and F. paucifl ora). Th e wing may be decurrent along the seed cavity or not. Th e species can roughly be divided into two geographical groups (not a phylogenetical division). Th e western and southwestern spe- cies are F. albicans (Texas ash) [Ill. 9], F. ber- landieriana (Mexican ash), F. coriacea (Leather-leaved ash, Ill. 10a), F. latifolia (Ore- gon ash) [Ill. 11a], F. papillosa (Chihuahuan ash) and F. velutina (Desert ash) [Ill. 10b]. Th is group can also include F. uhdei (Tropical ash) [Ill. 12] which is distributed in Central America and cultivated in the Neotropics. Th e eastern and southeastern species are F. ameri- cana (White ash), F. smallii (Small’s ash), F. biltmoreana (Biltmore ash), F. caroliniana (Water ash), F. cubensis (Cuban water ash), F. paucifl ora (Swamp ash), F. pennsylvanica (Green ash, Red ash) [Ill. 13] and F. profunda ( ash) [Ill. 11b]. Fraxinus albicans [Ill. 9] is the correct name 8 – (a) Fraxinus greggii has small pinnate leaves and occurs in for the Texas ash previously known as F. texen- Texas and Mexico. (b) The fl owers are apetalous. JC Raulston Arboretum at NC State University, USA [M. sis (Nesom 2010b). In USA it occurs only in Weathington, 11-07-2008 & T. Alderton, 25-03-2011] Texas and Oklahoma and in northern Mexico.

48 Belgische Dendrologie Belge 2012 systematics and floral evolution in FRAXINUS (oleaceae)

9 – Fraxinus albicans is a small tree distributed in Texas and Oklahoma in USA and northern Mexico. It has 3-5 long-petiolulate and ovate leafl ets. Texas, USA [E. Wallander, 12-08-1999]

10 – (a) Fraxinus coriacea and (b) F. velutina are both distributed in southwestern USA and northern Mexico. The leafl ets are more leathery and thick in F. coriacea which also has a more eastern distribution in the USA from to Texas. Arboretum Wespelaar, Belgium [E. Wallander, 7-10-2012]

11 – (a) Fraxinus latifolia with its sessile and hairy leafl ets is distributed in western USA. (b) Fraxinus profunda is hexaploid and the relatively large leaves and the whole shoot is velvety hairy. It occurs in wet areas of southeastern USA. Von Gimborn Arboretum, The Netherlands [E. Wallander, 6-10-2012]

Belgische Dendrologie Belge 2012 49 studiedagen – journées d’étude: FRAXINUS

Fraxinus coriacea [Ill. 10a] has been treated sylvanica. All three species can be found in the as a variety of F. latifolia [Ill. 11a] and of F. vicinity of each other (Nesom 2010e) but they velutina [Ill. 10b] until Nesom (2010c) recog- diff er in morphology of the fruits, leaf and twig nised it at specifi c rank. Th e three species vestiture, and shape and thickness of occur in diff erent parts of western USA and base (giving rise to diff erent leaf scars). northern Mexico. Fraxinus profunda [Ill. 11b] is hexaploid , the Tropical or Shamel ash (Nesom 2010a) and thought to be either [Ill. 12], is a large semi-evergreen tree that a derivative of tetraploid F. americana (= occurs naturally from central Mexico to Gua- F. smallii) and diploid F. pennsylvanica or temala (Francis 1990). It has also been intro- autopolyploid of F. pennsylvanica. duced into cultivation or as a street tree in Fraxinus paucifl ora and F. cubensis were dis- Costa Rica, in northern parts of the Andes tinguished from F. caroliniana s.s. by Nesom (Colombia and Venezuela), on Puerto Rico (2010d). All three water ashes are similar in and Hawaii. Th ere has been some confusion overall morphology and occur in swampy or about the name of the cultivated species. riverine habitats. For some unknown reason it was thought to and F. pennsylvanica be F. chinensis in the Andes but has now been [Ill. 13] are the two most common species of verifi ed as F. uhdei (Wallander, personal ash in USA. Many species are commercially observation and unpublished data). important and especially the of F. amer- Th e Melioides contains some polyploid icana which is used for making baseball bats. species complexes. F. americana is diploid, However, most species of ash in North Amer- F. smallii is tetraploid and F. biltmoreana is ica are now threatened by the Emerald ash hexaploid (Nesom 2010e). Th e latter two poly- borer (Agrilus planipennis), a that is ploids were not recognised by Wallander spreading fast across the eastern USA and has (2008) until Nesom (2010e) made a detailed already killed tens of millions of ash trees study of the F. americana (White ash) complex. (www.emeraldashborer.info). Huge eff orts are Th e polyploids are hypothesised to be derived being made to try to stop this disaster. Expedi- from crosses between F. americana and F. penn- tions have been made to China in order to make collections of ash species there that could be used for breeding resistance genes into the American ashes (Aiello 2012).

Section DIPETALAE

Th is section contains three superfi cially not very similar species: F. dipetala, F. quadrangu- lata and F. anomala. But in the genus Fraxi- nus, they are unique in having quadrangular or four-angled twigs (due to development of corky ridges) and hermaphrodite fl owers occurring in leafl ess lateral infl orescences. 12 – Fraxinus uhdei is distributed and cultivated in tropi- cal Americas. It has large leaves with petiolulate leafl ets. Other morphological similarities include Oaxaca, Mexico [E. Wallander, 12-02-2004] oval to ovate shaped wings of the samaras,

50 Belgische Dendrologie Belge 2012 systematics and floral evolution in FRAXINUS (oleaceae)

13 – (a) A staminate (male) infl orescence of and (b) a detail of a male fl ower, consisting only of two stamens and a small calyx. Göteborg Botanical Garden, Sweden [E. Wallander, 28-04-2004] contrasting to the more elongated wings the young leaves [Ill. 15a]. Th ey are apparently characteristic of the samaras of the other sec- wind-pollinated. tions. In other characters, such as petal num- ber, leaf morphology, and growth habit, they are quite unlike each other. Fraxinus dipetala (Two-petal ash) is a or small tree restricted to dry areas of south- western USA and northwestern Mexico. It is the only Fraxinus species having two petals, which are united and tubular by fusion with the fi laments. Sometimes the petals are lack- ing and the two forms may occur in the same panicle. Th e fl owers are fragrant and occur in many-fl owered and showy infl orescences [Ill. 14]. Th e anthers are relatively large and protrude from the corolla, an indication that the fl owers might be both wind- and insect- pollinated. Fraxinus anomala (Single-leaf ash) is also a shrub or small tree, predominantly occurring in desert areas in southwestern USA and cen- tral Mexico. It is the only Fraxinus species where simple leaves [Ill. 15b] are the normal condition. Th ere is a variety (var. lowelli) which has 3-5 leafl ets [Ill. 15a]. Fraxinus anomala has bisexual or sometimes unisexual fl owers 14 – A sweet-scented infl orescence with two-petaled with a persistent calyx, but lack corolla, and fl owers of Fraxinus dipetala. , USA they appear in lateral panicles before or with [“Eric in SF” Wikimedia Commons CC-BY-SA-3.0, 18-04-2009]

Belgische Dendrologie Belge 2012 51 studiedagen – journées d’étude: FRAXINUS

15 – (a) Flowering Fraxinus anomala var. lowellii with trifoliate leaves and (b) normal F. anomala with its unifoliate leaves. California, USA [Stan Shebs, Wikimedia Commons, 1-04-2007] & New Mexico, USA [R. Sivinski, June unknown year]

Fraxinus quadrangulata (called Blue ash pollinated, without petals. Both groups have because early European settlers in the USA calyx and the latter group has evolved from made blue dye from the inner bark) is a large the former. Th ere is a transition from her- tree with conspicuously quadrangular twigs maphrodite via androdioecious to dioecious [Ill. 16], occurring in eastern and central species. Some of the insect-pollinated are North America. Th e fl owers are mostly her- androdioecious as well as some of the wind- maphrodite, apetalous and wind-pollinated. pollinated species and dioecy has evolved after the evolution of wind-pollination [Ill. 1]. Th e 12 species with petalous fl owers are Section ORNUS F. apertisquamifera, F. bungeana, F. fl oribunda, F. griffi thii, F. hopeiensis, F. lanuginosa, F. mala- Within the genus Fraxinus, the 16 species of cophylla, F. ornus, F. paxiana, F. raibocarpa, the section Ornus are unique in that the infl o- F. sieboldiana and F. trifoliolata. All are andro- rescences are borne on current year shoots, dioecious except F. griffi thii, F. malacophylla together with the leaves, which emerge from and F. raibocarpa which are hermaphrodite. Th e terminal buds [Ill. 17]. In contrast, in all the former has evolved from the latter. Th e four other sections the infl orescences are borne lat- species with apetalous fl owers are F. baroniana, erally on previous year’s shoots. Th ere are two F. chinensis, F. longicuspis and F. micrantha. Th e morphological groups in the section Ornus: fi rst two are dioecious and have evolved from the insect-pollinated species (or both wind- the latter two, which are androdioecious. and insect-pollinated), with four white linear Th e section Ornus contains most of the petals in each fl ower [Ill. 18b], and the wind- species with showy fl owers and they are there-

52 Belgische Dendrologie Belge 2012 systematics and floral evolution in FRAXINUS (oleaceae)

16 – (a) The shoots of are four-ridged and in young shoots (b) this is very pronounced. Arboretum Wespelaar, Belgium [E. Wallander, 7-10-2012] & Von Gimborn Arboretum, The Netherlands [E. Wallander, 6-10-2012]

17 – The terminal buds of all species in the section Ornus contain the new shoot with both leaves and infl orescences. (a) The insect-pollinated F. ornus and (b) the wind-pollinated F. longicuspis. Göteborg Botanical Garden, Sweden. [E. Wallander, 23-05-1997] & Chichibu Mountains, Japan. [E. Wallander, 10-05-1999]

18 – occurs in southern Europe and (a) the insect-pollinated fl owers have a sweet scent. The species is androdioecious, meaning that trees have either (b) male or hermaphrodite fl owers. Sicily, [E. Wallander, 2-05-1996] & Göteborg Botanical Garden, Sweden [E. Wallander, 17-05-2000]

Belgische Dendrologie Belge 2012 53 studiedagen – journées d’étude: FRAXINUS fore sometimes called the “fl owering ashes”. Fraxinus chinensis is a complex of taxa with A well-known and ornamental species of this uncertain status and there may be polyploidy kind is F. ornus, the Manna ash [Ill. 18], in the involved. Two subspecies are accepted: F. chin- Mediterranean area. It is called so because it ensis subsp. chinensis and F. chinensis subsp. is or used to be cultivated, especially on Sicily, rhynchophylla (including F. rhynchophylla and for its dried sap which is harvested through F. japonica). Th e former has a more southern incisions in the bark to produce the sugar distribution in Asia (China, Korea, Vietnam mannitol. Two other species with ornamental and Th ailand) and the latter more northern value are F. fl oribunda [Ill. 19a] (widespread (China, Korea, Japan and southeastern Russia). from Afghanistan through Himalaya to Fraxinus chinensis [Ill. 22a] belongs to the ), and F. paxiana [Ill. 19b] wind-pollinated group and the fl owers are (Himalaya and China). Especially the latter apetalous and unisexual. Th e Japanese F. lon- species has large and showy infl orescences. gicuspis [Ill. 17b & 22b] is also wind-polli- Also F. sieboldiana (China, Japan and nated but androdioecious (at least morpho- Korea) [Ill. 20a] and F. lanuginosa ( Japan) logically so) (Wallander 2001). In the [Ill. 20b] are ornamental. Th ese two species are Himalayas occurs the similar F. micrantha. distinguished from each other by the former Fraxinus baroniana is relatively unknown having entire margins of the leafl ets and two but has very attractive foliage with long nar- pairs of inner bud scales and the latter having row leafl ets with beautiful autumn colour serrate margins and one pair of inner bud [Ill. 23]. It is a rare, small tree and occurs on scales. Related to them are F. apertisquamifera slopes and along rivers and streams in central ( Japan) and the recently resurrected F. hopei- China (Sichuan, Gansu and Shaanxi). ensis in northern China (Lee et al. 2012). of this species have been collected and spread Fraxinus griffi thii is one of the two ever- to researchers and arboreta (Aiello 2012). green ashes. It occurs in tropical southeastern A DNA analysis (Wallander, unpublished Asia [Ill. 21]. Th e shoot has no winter buds data) of this accession showed that it is related and a more or less continuous growth. Th e to F. chinensis and the other apetalous species fl owers are fragrant, hermaphrodite and insect- in the section Ornus. pollinated.

19 – (a) Flowering Fraxinus fl oribunda and (b) fruiting F. paxiana. Arboretum Wespelaar, Belgium [Ph. de Spoelberch, 16-05-2006] & north , China [Ph. de Spoelberch, 5-07-2008]

54 Belgische Dendrologie Belge 2012 systematics and floral evolution in FRAXINUS (oleaceae)

20 – (a) Hermaphrodite Fraxinus sieboldiana (with an enlarged male fl ower from another tree) and (b) F. lanuginosa. Chichibu Mountains, Japan [E. Wallander, 8-05-1999] & Göteborg Botanical Garden, Sweden [E. Wallander, 16-05-2000]

21 – Fraxinus griffi thii, occurring in tropical Asia, is evergreen. (a) The shoots have no winter buds and a more or less continuous growth. (b) The fl owers are fragrant, hermaphrodite and insect-pollinated. Arboretum Wespelaar, Belgium [E. Wallander, 7-10-2012] & Kyoto University Garden, Japan [S. Nanami, 11-07-1999]

22 – (a) Male Fraxinus chinensis and (b) hermaphrodite F. longicuspis. The fl owers are wind-pollinated and borne in lax infl orescences which emerge at the same time as the leaves, but fl ower while the leaves are still small and not so much in the way for pollen dispersal. Göteborg Botanical Garden, Sweden [E. Wallander, 13-05-2000] & Chichibu Mountains, Japan [E. Wallander, 5-05-1999]

Belgische Dendrologie Belge 2012 55 studiedagen – journées d’étude: FRAXINUS

23 – The rare Fraxinus baroniana in autumn colours. Jia Ling River, Gansu Province, China [Kunso Kim, 6-10-2011]

INCERTAE SEDIS

Th ree species are still unplaced in the present classifi cation. Th e American species F. cuspi- data [Ill. 24] is a small insect-pollinated tree occurring in Mexico and southwestern USA. Although having four petals, its fl owers are not 24 – Fraxinus cuspidata is a small tree with fragrant fl owers in similar to those of the insect-pollinated species arid areas of southwestern USA and Mexico. Sacramento in the section Ornus. Th e petals are united and Mountains, New Mexico, USA [R. Sivinski 28-04-2005] form a tube about one third of the length of the corolla, not free as in the section Ornus. Th e two stamens are united with the corolla tube and shorter than the petals. Th e fragrant and hermaphrodite fl owers are borne termi- nally in lateral, leafy panicles developed from the axils of the leaves of the previous year, not in terminal panicles on current year shoots as in the section Ornus. Fraxinus cuspidata is more similar to F. dipetala. Th e latter also has a sympetalous corolla fused with the fi laments but with two instead of four petals. Th ey both have infl orescences on lateral shoots but they are not leafy in F. dipetala. However, molecular data (several diff erent loci) show that they are not closely related (Wallander 2008). Fraxinus chiisanensis is endemic to Korea and has some primitive characters such as the naked terminal bud [Ill. 25]. It is a wind-pol- linated tree with lateral infl orescences on the 25 – Fraxinus chiisanensis from Korea with its shoot of previous year. Th e bisexual or uni- characteristically naked bud. Arboretum Wespelaar, Belgium sexual fl owers are apetalous and with a calyx [E. Wallander, 7-10-2012]

56 Belgische Dendrologie Belge 2012 systematics and floral evolution in FRAXINUS (oleaceae) which is persistent on the samaras. In most of Acknowledgements its morphological characters, and also leaf fl a- vonoids (Min et al. 2001, Chang et al. 2002), I thank Dr. Piet de Jong of the Dutch Den- it resembles the Melioides, but the molecular drology Society and Philippe de Spoelberch, data (Wallander 2008) does not place it in president of the Belgian Dendrology Society, that section. for inviting me to the study days of Fraxinus Fraxinus platypoda is a large wind-polli- in the two societies. I also thank Philippe de nated tree, occurring in China and Japan. It Spoelberch for allowing me to make collec- has lateral infl orescences with polygamous tions of Fraxinus in the Arboretum Wespelaar and apetalous fl owers. Calyx is present only in and Dr. Koen Camelbeke for sending me pistillate fl owers and persistent on the samaras, additional samples. I am indebted to Dr. Johan which have a fl attened seed cavity. Th e species Rova, Göteborg University, Sweden, for doing has characteristically swollen petiole bases the DNA analysis of the collected samples. covering the lateral buds [Ill. 26]. Previous molecular work (Wallander 2008) sug- gested that F. platypoda in China was closely References related to F. mandshurica and that F. spaethiana ( Japan) was a separate species, but a recent Aiello A.S. – (2012) – In search of Chinese ashes. re-analysis (Wallander, unpublished data) Th e Plantsman 11 (3): 188-193. showed that they should be treated as the Bochenek G.M. & Eriksen B. – (2010) – First come, same species (as done by Nakaike 1972 and fi rst served: delayed fertilization does not enhance Wei & Green 1996). Th e name F. platypoda pollen competition in a wind-pollinated tree, has nomenclatural priority over F. spaethiana. Fraxinus excelsior L. (Oleaceae). Int. J. Pl. Sci. 172 (1): 60-69. Th e fl avonoid study by Min et al. (2001) was Bochenek G.M. (2011) Reproductive biology and inconclusive about the sectional affi liation and population genetics of Common ash Fraxinus unfortunately the most recent molecular anal- excelsior L. Ph. D. Th esis, Göteborg University, ysis (Wallander, unpublished data) did not Sweden. shed more light on the position. Chang C.S., Min W.K. & Jeon J.I. – (2002) – Spe- cies relationships of Fraxinus chiisanensis Nakai and subsect. Melioides of sect. Fraxinus - as revea- led by morphometrics and fl avonoids. Korean J. Tax. 32 (1): 55-76. De Langhe J. – (2012) – Th e genus Fraxinus L. (Oleaceae): Vegetative key to species cultivated in Western Europe. pdf available at http://www.arbo- retumwespelaar.be/userfi les/fi le/pdf/Key_Fraxinus_ JDL.pdf Fernandez-Manjarres J.F., Gerard P.R., Dufour J., Raquin C. & Frascaria-Lacoste N. – (2006) – Diff erential patterns of morphological and molecular hybridization between Fraxinus excelsior L. and Fraxinus angustifolia Vahl (Oleaceae) in eastern and western France. Mol. Ecol. 15: 3245- 26 – Fraxinus platypoda with characteristically swollen leaf petioles protecting the next year’s fl oral buds. Arboretum 3257. Wespelaar, Belgium [Ph. de Spoelberch, 22-05-2012]

Belgische Dendrologie Belge 2012 57 studiedagen – journées d’étude: FRAXINUS

Francis J.K. – (1990) – Fraxinus uhdei (Wenzig) Lin- Nesom G.L. – (2010c) – Taxonomic status of Fraxi- gelsh. Fresno, tropical ash. SO-ITF-SM-28. 4 p. nus coriacea (Oleaceae). Phytoneuron 2010-37: 1–9. New Orleans, LA: U.S. Department of Agricul- Nesom G.L. – (2010d) – of the water ture, Forest Service, Southern Forest Experiment ashes: Fraxinus caroliniana, F. cubensis, and F. pau- Station. cifl ora (Oleaceae). Phytoneuron 2010-39: 1-13. FRAXIGEN – (2005) – Ash species in Europe: bio- Nesom G.L. – (2010e) – Fraxinus biltmoreana and logical characteristics and practical guidelines for Fraxinus smallii (Oleaceae), forest trees of the eas- sustainable use. 128 p. Oxford Forestry Institute, tern . Phytoneuron 2010-51: 1–30. University of Oxford, UK. Pautasso M., Aas G., Queloz V. & Holdenrieder Heuertz M., Carnevale S., Fineschi S., Sebas- O. – (2013) – European ash (Fraxinus excelsior) tini F., Hausman J.F., Paule L. & Vendramin dieback – A conservation biology challenge. Biol. G.G. – (2006) – Chloroplast DNA phylogeo- Cons. 158: 37-49. graphy of European ashes, Fraxinus sp. (Oleaceae): Raquin C., Brachet S., Jeandroz S., Vedel F. & roles of hybridization and life history traits. Mol. Frascaria-Lacoste N. – (2002) – Combined Ecol. 15 (8): 2131-2140. analyses of microsatellite and RAPD markers Lee H.-S., Park S.-H., Wallander E. & Chang demonstrate possible hybridisation between C.S. – (2012) – A fl avonoid survey of Fraxinus Fraxinus excelsior L. and Fraxinus angustifolia Vahl. (Oleaceae) in eastern Asia, and the overlooked For. Gen. 9 (2): 111-114. species Fraxinus hopeiensis T. Tang in northern Wallander E. – (2001) – Evolution of wind-polli- China. Biochem. Syst. Ecol. 41: 150-156. nation in Fraxinus (Oleaceae) – an ecophylogene- Min W.K., Jeon J.I. & Chang C.S. – (2001) – A tic approach. PhD thesis, Göteborg University, taxonomic reconsideration of Fraxinus chiisanensis Sweden. (Oleaceae) in Korea. J. Korean For. Soc. 90 (3): Wallander E. – (2008) – Systematics of Fraxinus 266-276. (Oleaceae) and evolution of dioecy. Pl. Syst. Evol. Nakaike T. – (1972) – A synoptical study on the 273: 25-49. genus Fraxinus from Japan, Korea and Formosa. Wallander E. & Albert V.A. – (2000) – Phylogeny Bull. Natn. Sci. Mus. Tokyo 15 (3): 475-512. and classifi cation of Oleaceae based on rps16 and Nesom G.L. – (2010a) – Notes on Fraxinus profunda trnL-F sequence data. Amer. J. Bot. 87 (12): 1827- (Oleaceae). Phytoneuron 2010-32: 1-6. 1841. Nesom G.L. – (2010b) – Observations on Fraxinus Wei Z. & Green P.S. – (1996) – Fraxinus. In Wu Z. albicans Buckley (Oleaceae), the correct botanical & Raven P. H. (eds) , vol. 15. name for Texas ash. Phytoneuron 2010-33: 1-12. Science Press and Botanical Garden, Missouri: 273–279.

58 Belgische Dendrologie Belge 2012