Infrageneric Classification of Quercus (Fagaceae) and Typification of Sectional Names Kc Nixon

Infrageneric classification of Quercus (Fagaceae) and typification of sectional names Kc Nixon

To cite this version:

Kc Nixon. Infrageneric classification of Quercus (Fagaceae) and typification of sectional names. An- nales des sciences forestières, INRA/EDP Sciences, 1993, 50 (Suppl1), pp.25s-34s. hal-00882872

HAL Id: hal-00882872 https://hal.archives-ouvertes.fr/hal-00882872 Submitted on 1 Jan 1993

HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Review article

Infrageneric classification of Quercus (Fagaceae) and typification of sectional names

KC Nixon

LH Bailey Hortorium, Cornell University, Ithaca, NY 14853, USA

Summary — The genus Quercus L (the true oaks) is widespread in the Northern hemisphere, in habitats ranging from temperate and tropical forests to dry thorn scrub and semi-desert. As far as is known, all species are anemophilous. The genus is most closely related to Trigonobalanus Forman, Colombobalanus Nixon and Crepet, and Formanodendron Nixon and Crepet, 3 extant tropical mono- typic genera. The oldest unequivocal oak fossils are Oligocene in age, although fossilized catkins and stellate trichomes that may represent earlier Quercus are preserved in Baltic amber, of uncer- tain Early Tertiary age. Trigonobalanoid fossils are known from the Oligocene and Paleocene of North America, and later deposits in Europe. A subgeneric and sectional classification of Quercus that is slightly modified from that proposed by Camus is most consistent with recent phylogenetic analyses within Quercus. Such a classification recognizes 2 subgenera, Quercus and Cyclobalanop- sis (Oersted) Schneider. The latter is restricted to eastern Asia and Malesia. Subgenus Quercus is divided into sections Lobatae Loudon (red oaks: North and South America), Protobalanus (Trelease) Schwarz (intermediate oaks: western North America), and Quercus (white oaks: E and W hemi- spheres). Two groups of white oaks that are sometimes recognized as sections, Ilex (Eurasia), and Cerris (Eurasia) are considered part of section Quercus, but merit subsectional or higher rank follow- ing more complete analyses.

Quercus / taxonomy / phylogeny / subgenera / sections

Résumé — Classification à l’intérieur du genre Quercus et caractérisation des noms de sections. Le genre Quercus (les vrais chênes) couvre l’ensemble de l’hémisphère nord et colonise des habitats allant des forêts tempérées et tropicales aux formations arbustives et semi désertiques. D’après les connaissances acquises à ce jour, toutes les espèces sont anémophiles. Le genre est proche de 3 genres tropicaux monotypiques vivants : Trigonobalanus Forman, Colombobalanus Nixon et Crepet et Formanodendron Nixon et Crepet. Les restes fossiles les plus âgés datent de l’oligocène, bien que des chatons et des trichomes étoilés susceptibles de représenter le genre Quercus et datés de manière imprécise du début du tertiaire aient été préservés dans de l’ambre de la mer Baltique. Des fossiles trigobalanoïdes datant de l’oligocène et du paléogène en Amérique du Nord et des dépôts postérieurs en Europe ont été reconnus. La classification en sous-genres et en sections, tenant compte des analyses phylogénétiques récentes, est proche de celle proposée par Camus. Cette classification comprend 2 sous-genres, Quercus et Cyclobalanopsis (Oersted). Le dernier n’est représenté qu’en Asie. Le sous-genre Quercus est divisé en 3 sections : Lobatae Lou- don (chênes rouges : Amérique du Nord et du Sud), Protobalanus (Trelease) Schwarz (chênes inter- médiaires : Amérique du Nord occidentale) et Quercus (chênes blancs : hémisphères est et ouest). Deux groupes de chênes blancs souvent classés dans les chênes blancs comme sections, Ilex (Eu- rasie) et Cerris (Eurasie) sont considérés comme appartenant à la section Quercus; ils mériteraient cependant d’être classés en sous-sections ou à un niveau supérieur après analyses complémen- taires.

Quercus / taxonomie / phylogénie / sous-genres / sections

INTRODUCTION species of Quercus, Trigonobalanus and Colombobalanus (Manos et al, manuscript Recent studies of the phylogeny of Quer- in preparation). The relationships of vari- cus (Nixon, 1984, 1989) (Manos et al, KC ous groups within Quercus are summar- Nixon, P Manos, manuscripts in prepara- ized in figure 1, based on a combination of tion) have provided the basis for a revised the morphological and molecular data infrageneric classification of the genus. analyses that will be presented elsewhere Quercus is most closely related to the re- (KC Nixon, P Manos, manuscript in prepar- cently discovered tropical genera Trigono- ation). The morphological data set allowed balanus Forman, Formanodendron Nixon greater resolution of among-section rela- and Crepet, and Colombobalanus Nixon tionships, while the molecular data set add- and Crepet (Nixon, 1989; Nixon and Cre- ed synapomorphies for sectional groups. In pet, 1989). Cladistic analysis of 17 mor- general, the results of these analyses sup- phological characters (Nixon, 1984) (KC port recognition of 4 monophyletic groups Nixon, P Manos, manuscript in prepara- of oaks, the Cyclobalanopsis, the Lobatae tion) has been undertaken in combination (the red oaks, subg Erythrobalanus of re- with chloroplast (cp) DNA restriction site cent literature), the Protobalanus (the inter- analyses of 92 informative sites among 33 mediate oaks) and the white oaks in the broad sense (variously referred to as Le- some of the taxa Camus recognized. It is pidobalanus, Euquercus, or Leucobalanus important to synonymize some of Loudon’s in recent literature). Note that the "Cerris" sectional names which were published si- and "Ilex" groups are not recognized here multaneously. as sections, and may merit recognition as subsections within section Quercus but the limits of these groups in terms of both spe- FOSSIL HISTORY cies and characters is not clear at this time, particularly when the Asian species The oldest oak fossils are of Quercus are considered. Because of unequivocal acorns, staminate catkins/pollen and com- this uncertainty, I have chosen to defer a leaves from of subsectional treatment within the white pressed Oligocene deposits North America and oaks until more data are available. (Daghlian Crepet, 1983; Crepet, 1989; Crepet and Nixon, Because of the general similarity of the 1989a, b; Nixon and Crepet, 1989). Stami- results of recent to phylogenetic analyses nate catkins and stellate trichomes that re- the classification Ca- previous proposed by semble those of modern oaks are pre- mus and in order to maintain the (1938), served in Baltic amber of northern Europe level of taxonomic I have greatest stability, (Conwentz, 1986), but need further investi- followed her classification as closely as gation, because they occur with fruits possible. However, Camus did not always which appear to be trigonobalanoid. adequately search for the earliest names at the sectional level in Quercus, and Prior to the Oligocene, the oak lineage some of the names which she used must is represented by trigonobalanoid fossils of fruits and be replaced by earlier names. In particular, consisting well-preserved and staminate the sectional name of the red oak group infructescences, pistillate must be changed to the oldest available inflorescences with in situ pollen, and as- name, Lobatae Loudon. In addition to the sociated ’Dryophyllum’ type leaf compres- names accepted below, lectotypification of sions (Crepet and Nixon, 1989a, 1989b). the sectional names proposed by Loudon While these fossils are not identical with (1830, 1835-1838) and others, even though modern trigonobalanoids, they share ples- they are treated as synonyms here, is im- iomorphic features, such as several free portant in order to stabilize the infrageneric triangular fruits in a valved cupule, capitate nomenclature of Quercus. In all cases of stigmas and cupules arranged along an el- lectotypification below, an attempt has ongate axis. been made, where possible, to lectotypify Throughout mid- and late-Tertiary de- these names so that names currently and posits of the northern hemisphere, oak leaf widely in use are not replaced. This has compressions and impressions are abun- not been possible in all cases. dant, and many of these, particularly from Is it beyond the scope of this paper to North America, have been identified as exhaustively review the history of subgen- close relatives of modern species. Wheth- eric and sectional names in Quercus, but er or not the Miocene and Pliocene spe- the synonymy presented below includes all cies are as close to modern species as names which have been used extensively. some authors have presumed, it is clear I present here an infrageneric classification that by this time the oak flora had become of the genus Quercus which broadly fol- prominent and diverse, and at least super- lows that of Camus, but utilizes Loudon’s ficially resembled the assemblages seen in sectional names which have priority for modern subtropical and temperate forests. Futher work is necessary to resolve the 2-3 years; acorn maturation biennial. Sec- phylogenetic affinities of these abundant tion Protobalanus. Tertiary oak leaf fossils. CC. Abortive ovules always basal; leaves deciduous to subpersistent, rarely KEY TO THE SUBGENERA persistent for more than 1 year; acorn mat- AND SECTIONS OF QUERCUS uration biennial or annual. Section Quer- cus.

A. Stigmas capitate to subcapitate or dis- coid, terete without adax- styles generally TAXONOMIC TREATMENT ial staminate catkins stigmatic groove; OF QUERCUS usually with prominent bracteoles, these subpersistent to caducous; scales of cupule in concentric or spiral rings, usually Quercus encino, obviously connate laterally to form lamel- (oak, chêne) lae; east Asian. Subgenus Cyclobalanop- sis. Quercus L, Syst PI ed 2, II, 994. 1753. [for complete synonymy at the generic AA. Stigmas usually linear ampliate or level, see Camus (1938)]. - Type: Quer- broadly ampliate, styles grooved, or with a cus robur L (fide ING) short stigmatic groove extending from the stigma; staminate catkins with inconspicu- Trees or shrubs, flowers monoecious; ous, caducous bracteoles, or these some- wood ring-porous or diffuse-porous; termi- times lacking; scales of cupule various, im- nal buds prominent, quadrangular to pen- bricately arranged and free; widespread in tangular or rounded in cross-section; bud the northern hemisphere. Subgenus Quer- scales imbricate, bud stipules sometimes cus. persistent; axillary buds often closely associated with and subtending terminal bud; B. Base of pistillate perianth (perigon) leaves spirally arranged, craspedodro- free, forming a skirt or flange; styles usual- mous, mixed craspedodromous or campy- ly elongate, linear-ampliate; endocarp al- lodromous, rarely bronchidodromous, often ways tomentose; cup scales typically flat, with parallel secondary veins, marginal unkeeled; teeth of leaves if present usually teeth (if present) simple, aristate, mucro- aristate or spinose, rarely mucronate. Sec- nate or oblique, 1 associated with each tion Lobatae. secondary vein, or in some species the secondary vein branching and terminating BB. Base of pistillate perianth (perigon) in several teeth; staminate inflorescences adnate to ovary/style bases, not forming a lax-spicate (catkins), clustered at the base flange or skirt; styles elongate and linear- of new growth or occurring singly in the ax- ampliate or short and broadly ampliate or ils of some of the lower leaves, emerging cuneate; endocarp tomentose or glabres- at vernation; staminate flowers single or in cent; cup scales typically keeled or tuber- groups of 1-3 along rachis, subtending culate or both; teeth of leaves if present ar- bracteole prominent and often exceeding istate, pungent, or mucronate. perianth and persistent past anthesis, or inconspicuous and caducous; stamens 6 C. Abortive ovules apical to lateral, (2-12), usually exserted at anthesis, sur- rarely appearing basal; leaves persistent rounding a tuft of simple trichomes inter- preted as representative of a rudimentary China and southeast Asia (150?); fewer pistillode: pollen tricolporate (-tricolpate), species are found in the western United spheroidal to subprolate or suboblate, ex- States (ca 25) and temperate Europe and ine sculpture generally rugulate or sca- North Africa (8-12?); 1 species is found in brate, often microscabrate; pistillate inflo- northern South America (Colombia). rescence borne in the axils of leaves of young branches, usually stiff, with 1- several partial influorescences, each sub- Subgenus Cyclobalanopsis — tended by a cupule, only the single central (cycle-cup oaks) flower of each influorescence developing; pistillate perianth cupped to campanulate Quercus subgenus Cyclobalanopsis (Oerst- or rotate, shallowly to deeply 5-6 lobed, or ed) Schneider, Handb Laubh, I, 210. 1906. the lobes obscure, basally adnate to the ovary or free; ovary 3 (-6+) carpellate, in- - Cyclobalanopsis Oersted (as genus), Bi- ferior; styles 3 (-6+), linear or subsessile, drat til Kundskab om Egefamilien, 69. stigmas capitate to linear-ampliate and ex- 1871. -Quercus section Cyclobalanopsis tending along adaxial stylar suture; fruit an Bentham and Hooker, Gen PI III, I p 408. acorn, a single rounded indehiscent nut 1880. -Type: Quercus velutina Lindley ex subtended by a cupule that lacks suture Wallich, non Lamarck. (fide ING) zones and does not separate into valves, Trees or shrubs; bark usually smooth or cupule with external imbricate or concen- furrowed, hard, gray or black, rarely light- tric scales, the 2 lateral abortive flowers of colored; leaves persistent or subpersistent, the partial influorescence within the cu- entire or serrate-toothed, teeth if present pule; fruit maturation biennial or annual, or mucronate or rarely setate; foliar trichomes occasionally ’pseudoannual’ as in some thin-walled and glandular, uniseriate, fas- species of section Protobalanus; endocarp ciculate, multiradiate or rosulate, rarely if sericeo-tomentose to glabrescent, columel- ever thick-walled and/or stellate; staminate la and remnants of the septa of the carpels flowers usually distributed in groups of 1-3 often impressed on the seed, forming irreg- along rachis, subtending bracteole usually ular longitudinal grooves; seed coats usu- prominent and often exceeding perianth ally brownish, adhering tightly to the seed and persistent, staminate perianth often at maturity or adhering to the endocarp regularly 6-lobed; anthers apiculate or re- wall; cotyledons free or sometimes fused tuse; pollen exine sculpture typically rugu- completely: abortive ovules apical, lateral late, often microscabrate; pistillate perianth or basal; cupule scales arranged in con- 5-6 lobed, base adnate to ovary; styles 3 centric rows and partially or wholly connate (-6+), usually linear with an expanded flat to form concentric or im- laterally, lamellae, or subcapitate stigma, the stigmatic sur- bricate and free, sometimes reflexed and face extending only partially along stylar n = 12. spinose. suture or sometimes not extending along Distribution: north temperate and sub- suture at all, in any case not forming a tropical, tropical montane, and particularly prominent stigmatic groove; stylopodial in Asia sometimes lowland tropical (subge- umbo often annulate with 1-3 (-5) distinct nus Cyclobalanopsis); the greatest con- rings; fruit maturing the 2 season or in the centrations of species are in eastern North 1 year, but at least sometimes ’pseudoan- America (ca 60), highland Mexico and cen- nual’ as in some species of section Proto- tral America (150-200), and montane sub- balanus; endocarp sericeo-tomentose, tropical Eurasia from the Middle East to remnants of the septa of the carpels often impressed on the seed, forming irregular podial umbo often annulate with 1-3 (-5) longitudinal grooves, or subglabrous; seed distinct rings; fruit solitary in each cupule, coats usually brownish, adhering tightly to rounded in cross-section, maturing the 1 or the seed at maturity or adhering to the en- 2 season; abortive ovules apical, or in docarp wall; cotyledons free; abortive some species variable in position or basal; ovules apical; cupule scales arranged in cupule hemispheric, cup-shaped to flat; cu- concentric or spiral rows and partially or pule scales variable, spirally or concentri- wholly connate laterally, to form concentric cally arranged; laterally connate or free. lamellae, often densely vestitured. I follow Camus in her broad interpreta- Distribution: subtropical, montane tropical tion of subgenus Quercus, to include all and lowland tropical east Asia and Malay- oak species except the Cyclobalanopsis sia. group, although American workers usually I recognize the possible utility of generic recognize 3 subgenera in North America. Camus’ classification is with re- rank for Cyclobalanopsis as proposed by compatible sults of Certain Schwarz (1936). Until careful studies pro- phylogenetic analyses. Eurasian oaks Q as well as duce stronger evidence that Quercus as (eg coccifera) Protobalanus are ’interme- broadly defined is polyphyletic, the conser- morphologically diate’ in certain characters between red vative stance of recognizing a single ge- oaks and white oaks sensu and this nus is appropriate. stricto, further supports the closer relationship of these oaks to each other than to Cyclobal- Subgenus Quercus: (scale-cup oaks) anopsis. If Cyclobalanopsis is included in Quercus as a subgenus, prudence recom- mends that the remainder of Quercus be Quercus subgenus Euquercus (Hickel accomodated in a The 3 and Camus) A Camus, Les Chênes. single subgenus. major groups of oaks in North America Monographie du genre Quercus. Vol I. then be as sections 373. 1938 may recognized (see below). Large trees, shrubs or sometimes low rhizomatous shrubs; bark variable, from Quercus Quercus smooth to scally or furrowed; leaves per- subgenus section Lobatae sistent, subpersistent or deciduous, entire, (red oaks) serrate-toothed or lobed, teeth if present setate, aristate, pungent or mucronate; fo- Quercus section Lobatae Loudon, Hort Brit liar trichomes thin-walled and glandular, 385. 1830. Lectotype (here chosen): Quer- uniseriate, fasciculate, multiradiate or ros- cus aquatica Wait (= Q nigra L). The 4 spe- ulate, and/or thick-walled and/or stellate; cies which Loudon included in this section staminate flowers distributed singly along are red oaks. This eliminates any possibili- rachis, the single subtending bracteole ty of lectotypifying the section so that it is a caducous or sometimes lacking, staminate synonym of the ’type’ section, the white perianth irregularly or regularly 2-6 lobed; oaks. Thus, this name must stand as the anthers retuse, or with an apiculate or at- earliest name for the red oaks if they are tenuate connective; pollen exine sculpture recognized at the level of section. typically scabrate with obscure or obvious perforations; styles 3 (-6+), with expanded Quercus section Integrifoliae Loudon, Hort stigmatic surface, capitate to linear ampli- Brit 384. 1830. Lectotype (here chosen): ate with an adaxial stigmatic groove; stylo- Quercus phellos L. Quercus section Mucronatae Loudon, Hort late, multiradiate or rosulate, rarely if even Brit 385. 1830. Lectotype (here chosen): thick-walled and/or stellate; staminate flow- Quercus rubra L. ers usually distributed singly along rachis, subtending bracteole caducous or lacking, Quercus section Rubrae Loudon, Arbor staminate perianth irregularly, often deeply Frut Brit 3, 1877. [1835-]1838. - Type: 2-6 lobed; anthers usually somewhat apic- Quercus rubra L. Loudon’s concept of Q ulate, occasionally retuse; pollen exine rubra was that of the northern red oak, not sculpture typically rugulate and microsca- of the southern red oak (= Q falcata), as brate to scabrate; pistillate perianth 5-6 the name Q rubra was applied by some lat- lobed, the base not adnate to the ovary, er authors (eg Sargent, 1922). therefore forming a minute free skirt or flange, the inner cupule scales often insert- Quercus section Nigrae Loudon, Abor Frut ed beneath this flange; styles 3(-6+), line- Brit 3, 1980. [1835-]1838. - Type: Q nigra ar-spatulate, the stigmatic surface extend- L. Loudon followed Michaux in his concept ing proximally along stylar suture, forming of Q nigra as the blackjack oak (= Q mari- a darkened stigmatic groove; stylopodial landica), but included the real Q nigra in umbo often annulate with 1-3 (-5) distinct this section as Q aquatica. rings; fruit maturing the 2 season, or in several species in the 1 year; endocarp se- Quercus section Phellos Loudon, Arbor riceo-tomentose, remnants of the septa of Frut Brit 3, 1894. [1835-]1838. - Type: the carpels often impressed on the seed, Quercus phellos L. forming irregular longitudinal grooves; seed coats reddish or brownish, adhering Quercus section Erythrobalanus Spach, tightly to the seed at maturity; cotyledons Hist veg Phan 11, 160. 1842. - Quercus free or rarely partially connate; abortive subgenus Erythrobalanus (Spach) Endlich- ovules apical, or rarely in some species er, Gen Plant suppl 4, 24. 1847. - Quercus variable in position or subbasal; cupule subsection Erythrobalanus (Spach) Post scales thin, flat, only rarely keeled or tuber- and Kuntze, Lexicon generum Phaner 474. culate, imbricate, never spinescent. 1904. - Genus Erythrobalanus (Spach) Distribution: restricted to temperate, sub- Schwarz, Notizbl Bot Gard Berlin 13, 8. tropical and montane tropical parts of the 1936. Lectotype (here chosen): Quercus new world, from Colombia, South America rubra L. (1 sp) through central America to forests of southeastern Canada, and westward to Quercus Melanobalanus subgenus Engel- southern Oregon; largely absent from the man, Trans St Louis Acad Sci 3, 388. Mountain area, for Arizona 1877. Rocky except and New Mexico.

Large trees, shrubs or sometimes low rhizomatous shrubs; bark usually smooth Quercus subgenus Quercus section or furrowed, hard, gray or black, rarely Protobalanus (intermediate oaks, light-colored; leaves persistent, subpersis- golden cup oaks) tent, or deciduous, entire, serrate-toothed or lobed, teeth if present usually aristate or setate, a terminal seta often present even Subgenus Protobalanus Trelease, in Stan- on untoothed leaves; foliar trichomes thin- dley, Contr U S Natl Herb 23, 176. 1922. - walled and glandular, uniseriate, fascicu- Quercus section Protobalanus (Trelease) Schwarz, Notizbl Bot Gart Berlin 13, 21. celled rays emerging from the epidermis 1936. - Quercus section Protobalanus together, or multicellular glandular uniseri- (Trelease) Camus, Les Chênes, vol 1, ate; staminate flowers with 4-12 stamens, 157. 1938. - Type: Quercus chrysolepis the anthers apiculate; pollen exine sculp- Liebm. Both Camus and Schwarz inter- ture rugulate to scabrate, with nanno-striae preted Trelease’s Protobalanus as a sec- on rugulae; (fide Solomon, 1983a, 1983b); tion, and attributed this rank to Trelease. pistillate flowers 1-3, usually sessile, pe- Confusion regarding the original rank of duncule sometimes developed; styles this name apparently arose from ambiguity short and ampliate to long with ampliate in Trelease’s presentation of the name in stigma (Q palmen); fruit maturing in 2nd his 1924 monograph. Trelease used sev- year, but often the fertile branches do not eral infrageneric names that had been pro- grow in 2nd year, so that the fruit may ap- posed by earlier authors, eg, Leucobala- pear annual (pseudoannual maturation); nus Engelmann, without reference to the endocarp tomentose to appearing gla- original authority, publication, or rank at brous, the seed coats usually attached to which the names were published. Proto- the seed but sometimes attached to the balanus was presented in the 1924 mono- endocarp; cotyledons furrowed, subequal. graph in a similar ’naked’ manner, leading Distribution: western North America from later authors to believe that this was the southern Oregon, south to northern Baja original publication of the name. However, California, Mexico, eastward to central Ari- the first use by Trelease of the name Pro- zona, and barely into adjacent Chihuahua; tobalanus dates to 1916 in Proc Natl Acad also present on the channel islands of Sci 2, 627, where he clearly referred to it southern California, and the only group of as a subgenus, as well as referring to the oaks present on the islands of Guadalupe type of Protobalanus as Q chrysolepis (loc and Cedros off the coast of Baja California. cit, p 629). Protobalanus was used again Protobalanus is a distinctive group of Trelease in 1918 Bot Gard by (Brooklyn about 5 species, 1 of which (Q chrysolepis Mem and in 1, 497), again Standley’s Liebm) is widely distributed and highly vari- Trees and Shrubs of Mexico, 1922. No de- able. The distribution of this group, which in the earlier scription appeared publica- is restricted to western North America, tions, but in the latter, Trelease included suggests a possible common biogeograph- the name in a key to the species of Mexi- ical history with Lithocarpus densiflora and co, with clear diagnostic characters. The Chrysolepis sempervirens and C chryso- 1922 publication therefore must be consid- phylla of the California region. The latter 3 ered the first valid of the publication name, species are apparently relicts of a previ- and there is no in the earlier ambiguity ously richer Asian element in western as to the rank at publications (subgenus) North America that is no longer prevalent. which the name was intended. Protobalanus is undoubtedly the most in- Evergreen shrubs or trees, bark usually teresting group of oaks in North America scaly and rough (as in various white oaks) from the standpoint of phylogeny and bio- on older branches; twigs tomentose to gla- geography. The phylogenetic affinities of brous; leaves persistent 2 or more years this distinctive and unique group are uncer- coriaceous, glaucous and waxy on the ab- tain, although for the present, Protobala- axial surface, entire or toothed, often spi- nus must be considered a part of the nomi- nescent, never lobed as in Q robur, foliar nal subgenus. They appear to be closely trichomes thin-walled, semi-glandular, sim- related to but intermediate between the red ple or with 2-several fasciculate single- oaks and the white oaks. In this respect, Protobalanus closely parallels the some- Quercus section Lepidobalanus Endlicher, what intermediate groups of Eurasian oaks Gen Plant, suppl 4, part 2, p 24. 1847, pro that center around Q cerris, Q suber, and parte. Lectotype (here chosen): Quercus Q coccifera. Protobalanus species appear robur L. to be strongly reproductively isolated from the other groups of North American oaks, Quercus section Leucobalanus Engel- as no verified natural or artificial hybrids mann, Trans Acad Sci St Louis 3, 381. are known. 1876.

Quercus section Mesobalanus Camus, Quercus subgenus Quercus Monographe Genre Quercus, Atlas I, p 49. section Quercus (white oaks) 1936.

Quercus section Dentatae Loudon, Hort Quercus section Euquercus Hickel and Ca- Brit 384. 1830. Lectotype (here chosen): mus, Ann Sci Nat Bot, 9e ser. III, p 379. 1921. - Quercus robur L. Quercus prinus L. Loudon included a Type: broad array of white oaks, including both American and Eurasian species, in this Quercus subgenus Heterobalanus Oerst- section. ed, Bidr til Kundskab Om Engefamilien. 1871 Quercus section Ilex Loudon, Arbor Frut Brit 3, 1899. [1835-]1838 . Type: Quercus Trees or shrubs: bark smooth, rough, scaly ilex L. or flaky, relatively soft, occasionally hard and furrowed; leaves persistent, sub- Quercus section Cerris Loudon, Arbor Frut persistent, or deciduous, entire, serrate- Brit 3, 1730. [1835-]1838. - Type: Quer- toothed or lobed, teeth if present mucro- cus cerris L. nate, pungent, or sometimes on juvenile growth aristate, or rarely (Cerris and Ilex Quercus section Albae Loudon, Arbor Frut groups) consistently aristate; foliar tri- Brit 3, 1730, 1863. [1835-]1838. Type: chomes thin-walled and glandular, uniseri- Quercus alba L. ate, fasciculate, multiradiate or rosulate, and often thick-walled and/or stellate; Quercus section Robur Loudon, Arbor Frut staminate flowers usually distributed singly Brit 3, 1730, 1731. [1835-]1838. Type: along rachis, subtending bracteole cadu- Quercus robur L. cous or lacking, staminate perianth regularly to irregularly, often deeply 2-6 lobed; Quercus section Prinus Loudon, Arbor Frut anthers usually retuse, rarely apiculate; Brit 3, 1730, 1872. [1835-]1838. Type: pollen exine sculpture scabrate or rugu- Quercus prinus L. late-scabrate; pistillate perianth 5-6 lobed, the base adnate to the ovary; styles 3(- Quercus section Lanatae Loudon, Arbor 6+), usually abruptly ampliate or dilated, Frut Brit 3, 1730, 1920. [1835-]1838. sometimes more gradually ampliate or Type: Quercus lanata Smith. subulate, stigmatic surface extending proximally along stylar suture, the stigmatic Quercus section Virentes Loudon, Arbor surface often cuneate in shape; stylopodial Frut Brit 3, 1730, 1918. [1835-]1838. umbo usually not annulate; fruit maturing Type: Quercus virens Aiton. in the 1st year, occasionally (Ilex and Cer- ris) maturing in the 2nd year; endocarp Crepet WL (1989) History and implications of the North American fossil record of glabrate or with minute tomentose vesti- early Fag- aceae. In: Evolution, Systematics, and Fossil ture near apex and base, but obscured by History of the Hamamelidae. Vol 2. ’Higher’ the seed or adhering coats, occasionally Hamamelidae (Crane PR, Blackmore S, (Ilex and Cerris) tomentose-sericeous; col- eds), Clarendon Press, Oxford, 45-66 umellar scar not on lateral typically present Crepet WL, Nixon KC (1989a) Eearliest mega- part of seed or endocarp; seed coats at fossil evidence of Fagaceae: phylogenetic maturity adhering to endocarp, or (Ilex and and biogeographic implications. Am J Bot 76, Cerris) to seed; cotyledons equal or une- 842-855 qual, free, or connate (Virentes and Glau- Crepet WL, Nixon KC (1989b) Extinct transition- coideae); abortive ovules basal; cupule al Fagaceae from the Oligocene and their scales keeled or tuberculate, imbricate, phylogenetic implications. Am J Bot 76, usually with thickened corky base, some- 1493-1505 times reflexed and spinescent. Daghlian CP, Crepet WL (1983) Oak catkins, leaves, and fruits from the Cata- Distribution: the most section Oligocene widespread houla Formation and their evolutionary signif- favorable of Quercus, occurring throughout icance. Am J Bot 70, 639-649 habitats in and temperate, subtropical tropi- Loudon J (1830) Hortus Brittanicus. Longman, of North and Central cal montane parts Rees, Orme, Brown and Green, London America, and Asia. Europe (extratropical) Loudon J (1835-1838) Arboretum et Fruticetum It is clear, based on morphological and Botanicum. Longman, Rees, Orme, Brown molecular data, that the Cerris and Ilex and Green, London groups of oaks are part of the broader Nixon KC (1984) A Biosystematic Study of Quer- white oak group, sharing the synapomor- cus Series Virentes with Phylogenetic Analy- phy of basal abortive ovules. Because the ses of Fagales, Fagaceae and Quercus. Ph D of Texas, Austin exact relationships of these groups are un- Dissertation, University certain (Ilex may be paraphyletic to one or Nixon KC (1989) Origins of Fagaceae. In: Syst Assoc vol 40B. Evolution, more other groups within the white oaks), Spec Systematics and Fossil History of the Hamamelidae. Vol 2 it seems best at this time to recognize only (Crane PR, Blackmore S, eds) Clarendon one section for the white oaks sensu lato. Press, Oxford, 23-43 As more data within the white oaks be- Nixon KC, Crepet WL (1989) Trigonobalanus come a subsectional classifica- available, (Fagaceae): taxonomic status and phyloge- tion will be proposed, and the variation en- netic relationships. Am J Bot 76, 826-841 the Ilex, Cerris, Virentes, compassed by Sargent CS (1922) Manual of the Trees of North Glaucoideae and other groups of white America (Exclusive of Mexico). Houghton oaks can be formally recognized based on Mifflin Co, New York phylogenetic pattern. Schwarz O (1936) Entwurf zu einem naturlichen System der Cupuliferen und der Gattung Quercus L. Notizbl Bot Gart Berl 13, 1-22 REFERENCES Solomon AM (1983a) Pollen morphology and plant taxonomy of white oaks in eastern North America. Am J Bot 70, 481-494 Camus A (1938) Les Chênes. Monographie du Genre Quercus. 2 vols. Lechevalier and Fils, Solomon AM (1983b) Pollen morphology and Paris (cited as 1936-1938, but not released plant taxonomy of red oaks in eastern North until 1938, fide Stafleu and Cowan, 1976) America. Am J Bot 70, 495-507 Conwentz H (1986) Die flora des Bernsteins, Stafleu FA, Cowan RS (1976) Taxonomic Litera- Zweiter Band; Die Angiospermen des Bern- ture. 2nd edn, vol 1. Bohn, Scheltema and steins. Engelmann, Danzig Holkema, Utrecht