Fagus sylvatica f. moesiaca K. Malý

Denk, Thomas, Grimm, Guido W., Cardoni, Simone, Csilléry, Katalin, Schulze, Mirjam Kurz Ernst-Detlef, Simeone, Marco Cosimo & Worth, James R. P., 2024, A subgeneric classification of Fagus (Fagaceae) and revised taxonomy of western Eurasian beeches, Willdenowia 54, pp. 151-181 : 162-167

= Fagus sylvatica f. moesiaca K. Malý in Ascherson &

Graebner, Syn. Mitteleur. Fl. 4: 438. 1911 ≡ Fagus moesiaca (K. Malý) Czeczott in Roczn. Polsk. Towarz. Dendrol. 5: 52. 1933. – Lectotype (designated here): Bulgaria, supra pagum Tvierdica [=Твърдица,

Tvrditsa] (inter Sliven et Elena), in monte Cumerna,

c. 950 m, fruct., 1927, K. Michoff, det. H. Czeczott

(WA [WA00000166143 Fig. 10]); isolectotype: WA

[WA00000166142]). See POWO (2023) for other heterotypic synonyms.

Molecular diagnosis — Lineage IV ITS variants, unspecific. The majority of 5S-IGS variants are specific; B Lineage variants largely surpass A Lineage variants in absolute abundance and number of unique sequence variants ( Fig. 4; Cardoni & al. 2022). Within Lineage B, European B types (Western B2 variants) outnumber Original B types (exclusively comprising shared types); relatively rare Lineage A variants (probably more common in Pleistocene relict populations, Cardoni & al. 2022, unpublished data) with a preference for Western A type (a lineage shared exclusively with Fagus orientalis ) over Shared A type ( Fig. 6, 7). Potentially specific SNPs rare but present in CRC, LFY, and Jiang & al.’s (2022) loci P14, P34, P38, P50, F128, F286 and F289 (see F. orientalis ); P38 shows a 7 nt-long deletion not detected in any other Fagus sample; P14 characterized by a notably distinct sister genotype of the F. grandifolia genotype: both types differ by six C↔T transitions from the basic type of F. subg. Fagus (Table 3). Distinct isoenzyme Gömöry & Paule (2010) and nuclear SSR profiles ( Kurz & al. 2023 marker set at k>2; Fig. 2, 3; see also Budde & al. 2023). Lineage Vb plastomes (species-level plastid type V-Sy; J. Worth & al., work in progress).

Morphological description — Lamina shape rounded to ovate to elliptic to obovate, usually asymmetric, (20–)40–80(–120) mm long in western populations, (40–)60–120(–145) mm in eastern populations, leaf index [length of leaf/width of leaf) × 100] 150 in western populations, 170 in eastern populations; leaf petiole (2–)5–12(–16) mm long, peaks at values 5, 6 and 10; most frequent base/apex pairs obtuse base and acute apex and acute base and acute apex, in addition, cordate base with acuminate apex and cuneate base with acute apex occur; basal leaf margin entire, wavy (to dentate), apical margin (entire to) wavy to inconspicuously dentate or conspicuously dentate in shade leaves; number of secondary veins (5–)6–10(–12); secondary venation pseudocraspedodromous, semicraspedodromous to craspedodromous in shade leaves, brochidodromous to semicraspedodromous and pseudocraspedodromous in sun leaves; length of stomata (16–)19–29(–32) µm, mean 22.5 µm, subsidiary cells incomplete cyclocytic to cyclocytic or actinocytic, dispersed or in groups; cupule peduncle 4–26(–40) mm, mean value 12 mm, length of cupule 12–26(–29) mm, mean value 20 mm in western populations, (12–)16–28(–32) mm, mean value 22.4 mm in eastern populations, basal cupule appendages reddishbrown, narrow (bud scale homologous) and long woody spines with slender apex, apical appendages long woody spines, often twisted.

Distribution — Europe ( Albania, Austria, Belgium, Bosnia and Herzegovina, Bulgaria, Central European Russia [Kaliningrad Oblast], Croatia, Czech Republic, Denmark, France, Germany, Greece, Hungary, Italy, Liechtenstein, Luxembourg, Moldova, Montenegro, Netherlands, North Macedonia, SE Norway [Vest-/ Ostføld], Poland, Romania, Serbia, Slovakia, Slovenia, N Spain, S Sweden, Switzerland, W Ukraine, S United Kingdom).

Evolutionary significance — The European beeches represent the sister species of Fagus orientalis (as defined below), the divergence between the sister species has been dated to the late Early Pleistocene by Gömöry & al. (2018), but may have deeper roots ( Renner & al. 2016). It is noteworthy that the palaeobotanical record also points to an Early Pleistocene origin of F. sylvatica ( Denk & al. 2022). Fagus sylvatica is probably the most recently evolved species within the western Eurasian beech lineage. The currently available molecular data fit with a budding-speciation type process, i.e. the first common ancestor(s) of F. sylvatica evolved from a F. orientalis population that got isolated from the main gene pool and underwent a substantial bottleneck before re-radiating into its modern-day range. Fagus sylvatica plastomes are nearly identical across the entire range of the species stretching from Spain, north and south of the Alps into eastern Europe and the Balkans. Increased genetic variation appears to be restricted to the Apennines (Central Italy; Cardoni & al. 2022) and northwestern Greece and the Rhodopes ( Hatziskakis & al. 2009), where it may be para- or sympatric with F. orientalis .

Remarks on nomenclature — Velenovský (1898, 1902) described a new variety of Fagus sylvatica from the surroundings of the village Kozludža (today Suvorovo, Суворово) in northeastern Bulgaria and from Sliven, eastern Bulgaria, as F. sylvatica var. macrophylla . The name macrophylla had earlier been used by Candolle (1868) and hence cannot be used for this taxon. Based on Velenovský’s concept of F. sylvatica var. macrophylla, Maly in Ascherson & Graebner (1911) established the form F. sylvatica forma moesiaca . Later, Czeczott (1933) erected the new species F. moesiaca (Maly) Czeczott and in the protologue cited a number of herbarium vouchers. We could not find these vouchers in any herbarium collection until 2024, when Dr Maja Graniszewska, curator of the herbarium of the University of Warsaw, was able to locate most of the herbarium sheets in Hanna Czeczott’s archive material at the University of Warsaw, did some cleaning and repairing to them, and provided us with high-resolution scans.

Among the syntypes, one collection is from the vicinity of Sliven (K. Michoff s.n. WA00000166143, WA00000166142), and a lectotype and isolectotype were chosen from this collection .

Further remarks — From the surroundings of Tran (Трън), Pernik Province, western Bulgaria, populations with large cupules (30–35 mm) were reported and ascribed to Fagus moesiaca var. borzae Domin ( Jordanov & Kuzmanov 1966) . All currently available molecular and morphological data suggest that the eastern European entity F. moesiaca should be included within F. sylvatica ( Gömöry & al. 2018). In contrast, POWO (2023) treats F. moesiaca as a synonym of F. ×taurica Popl. ( F. orientalis × F. sylvatica ), a name that was originally used only for the Crimean beeches. There is so far little data on the Crimean populations. According to the isoenzyme data of Gömöry & Paule (2010), the Crimean F. ×taurica falls genetically within the overall variation of F. sylvatica as well. More recently, Gömöry & al. (2018) found F. ×taurica to have originated from relatively recent Middle Pleistocene contact between Caucasian beech populations and F. sylvatica s.str. Therefore, F. moesiaca should not be synonymized with F. ×taurica .

Representative specimens — E. Bourgeau 692 (P [P06857192, P06857207, P06858360]); J.-B. Mougeot s.n. (P [P01035946]); P. Jovet s.n. (P [P00504675]); H. Bouby 493 (P [P06850962]); C. Hering s.n. (P [P06858357]); K. Domin 284c ( PRC [ PRC 454888 type of Fagus moesiaca (Maly) Domin var. borzae Domin ]); J. Madalski 42 (P [P06853549]). — Syntypes of F. moesiaca : P. Černjavski s.n. (WA [WA00000166146, WA00000166147]); H. Czeczott s.n. (WA [WA00000166149]); H. Czeczott s.n. (WA [WA00000166150, WA00000166151]); E. Reimesch (WA [WA00000166152, WA00000166153]). — See Shen (1992) for more representative records.

Fagus orientalis Lipsky in Trudy Imp. S. - Peterburgsk. Bot. Sada 14: 300. 1898 ≡ Fagus sylvatica subsp. orientalis (Lipsky) Greuter & Burdet in Willdenowia 11: 279. 1981. – Lectotype (designated by Yaltırık 1982: 658): Turkey, Iter orientale, Paphlagonia, Vilayet Kastambuli [Kastamonu province], Kure-Nahas [ Küre district ], in sylvis ad Topschi-Chan, 41°48'21.528''N, 33°42'36.972''E, 9 Sep 1892, P. Sintenis 5113 (LE [ LE00011314 ]; isolectotypes: A [A00033880], G [G00358034-36] [ Fig. 11], P [P06812072, P06812074], US [NMNH-00409670 = old no. US 2501956]).

– Fagus sylvatica var. asiatica A. DC. in Candolle, Prodr. 16(2): 119. 1864, pro parte.

Molecular diagnosis — Lineage IV ITS variants, may include specific variants (cf. Denk & al. 2002) but better sampled data would be needed. Lineage B variants more abundant than Lineage A variants, the latter more frequent and more diverse than in Fagus sylvatica ; Lineage A variants either shared exclusively or highly similar to F. sylvatica variants (dominant Western A type), or representing types ancestral within the western Eurasian lineage ( Cardoni & al. 2022; Shared A in Fig. 6, 7); Lineage B variants of the European B lineage subdominant and either related to, or occasionally shared with F. sylvatica (Western B 2 type); Original B lineage much more diverse than in F. sylvatica comprising sequentially distinct types: Shared B1 and related types found across all western Eurasian beeches, Western B 1 types exclusively shared with F. hohenackeriana p.p., other evolved (sequentially distinct) Caucasian types (Hohenackeriana B1a, B1b, B3) rare to very rare but present while absent in F. sylvatica ( Fig. 6, 7; Cardoni & al. 2022). Currently no CRC data, and a single LFY accession, differing by a unique T-dominated length-polymorphic sequence motif at pos. 737–764 (supplementary content, file Genotypification.xlsx, sheet LFY LP-patterns). The individual included in Jiang & al. (2022) differs consistently by 26 point mutations from the F. sylvatica samples in the nuclear loci P14 (13), P34 (1), P38 (4), P50 (1), P97 (1), F202 (1) and F289 (5). Distinct isoenzyme ( Gömöry & Paule 2010) and nuclear SSR profiles ( Kurz & al. 2023, at k =3), the latter involving a west-east gradient (k =2–6, Fig. 3). Lineage V plastomes, subtype yet to be determined.

Morphological description — Lamina shape elliptic to obovate, usually symmetric, (30–)50–120(–170) mm long, leaf index 196; leaf petiole (2–)3–10(–15) mm long; most frequent base/apex pairs “obtuse base and acute or acuminate apex” and “acute base and acuminate apex”, sun leaves with acute base and apex; leaf margin entire or with blunt triangular or sharp teeth (shade leaves); number of secondary veins (5–)7–12(–15); secondary venation pseudocraspedodromous, semicraspedodromous to craspedodromous; length of stomata (13–)18– 25(–33) µm, mean 22.5 µm, subsidiary cells incomplete cyclocytic to cyclocytic or actinocytic, dispersed or in groups; cupule peduncle (5–)12–14(–75) mm, mean value 25 mm, length of cupule (10–)18–28(–45) mm, mean value 22.5 mm, basal cupule appendages leaf-like, wintergreen (not turning brown in autumn) or summergreen (turning brown during cupule development), spathulate or petiolate, oblong to elliptic in shape, venation dichotomous (in spathulate leaflets) or brochidodromous, area of leaflets decreasing at higher altitudes, apical appendages woody, spine-like.

Distribution — NE Greece (Thrace), SE Bulgaria, W and N Turkey, S Turkey (Kahramanmaraş, Hatay, Osmanye,? Adana, Mersin).

Evolutionary significance — Sister species of Fagus sylvatica (see above), geographically and genetically ( Kurz & al. 2023, supplement fig. 4) forming the bridge between the eastern species and the beeches of Europe. Morphologically, individuals in lowlands and at mid-elevations are characterized by conspicuous, green, spathulate, leaf-like appendages on the lower parts of the cupule and long cupule peduncles ( Fig. 12A, B; Table 4). Similar appendages are also found in the Japanese species F. crenata (F. subg. Fagus ) and in the East Asian ( China, S Korea) species F. engleriana and F. multinervis (F. subg. Englerianae). From the current still limited data, it can be expected that F. orientalis is genetically richer than its western sister species despite its much smaller overall range and population size. Furthermore, the species appears to be generally closer to the common ancestor of F. sylvatica - orientalis , demonstrated by a higher amount of shared genetic types and stronger morphological affinities to fossil members of its lineage ( F. castaneifolia , F. haidingeri ) but also, in contrast to F. sylvatica , to the fossil-species F. gussonii ( Denk & al. 2002). Fagus gussonii is a Miocene fossil-species of ambiguous phylogenetic affinities and hypothetical vector for past trans-Atlantic gene flow ( Cardoni & al. 2022; Schulze & Grimm 2022). The SSR data clustering results of Kurz & al. 2023 (k ≥3) indicate that the former range of this species may have been much larger, potentially including the disjunct Nur Mountains populations in the Hatay province, southeastern Turkey ( Fig. 2). Both the isoenzyme and SSR clustering patterns are possibly affected by (sub)recent gene flow with the Caucasian beech, F. hohenackeriana (in agreement with occasionally found eastern 5S-IGS variants), between their respective ancestors, or incomplete lineage sorting within the ancestor(s) of F. orientalis (- sylvatica ) and F. hohenackeriana . Potential hybrid or contact zones include or have included the Nur Mountains and, more importantly, the Parhar Mountains (western extension of the Pontic Mountains) in the hinterland of the Turkish Black Sea coast east of Zonguldak and into southwestern Georgia ( Kurz & al. 2023). More in-depth population-level studies are needed to discern to which degree the higher genetic affinity of F. orientalis with its eastern cousin, F. hohenackeriana , than found in its western sister F. sylvatica , is due to (ongoing) gene flow or a generally lower genetic drift (e.g. because of fewer Pleistocene bottleneck events).

Further remarks — This species is genetically severely understudied in its core range, with most research having focussed on the Bulgarian-Romanian Fagus moesiaca as a putative hybrid or intermediate form between F. sylvatica and F. orientalis . Morphologically, the green, stalked leaflets persisting on the cupule ( Table 4) appear to be a most conserved trait, never seen in suggested hybrids outside the known range of the species as shown in Fig. 2. Ongoing research on the Greek side of the eastern Rhodopes has nonetheless revealed mixed stands (individuals lacking or showing green cupule leaflets) of F. sylvatica and F. orientalis that show private 5S-IGS variants in addition to those shared with F. sylvatica or F. orientalis and may be transitional between the sister species (A. Papageorgiou & al., work in progress).

Representative specimens — BULGARIA: P. Frost-Olsen 1151 (P [P06812193, P06853547]). — TURKEY: J. Bornmüller & F. Bornmüller (E [E00401534]); G. D. Sag 887A (P [P00043490]); P. H. Davis, M. Coode & F. Yaltırık D. 37622 (E [E00401528]); P. H. Davis 18492 (E [E00401511]); B. Balansa 1141 (P [P06812090], US [NMNH-03400246]); J. Manissadjian 369b (P [P06812088 two specimens, one typical F. orientalis , another with transitional cupule appendages, see below]); Det. I. V. Palibin (P [P06812092]); Nur Mountains: P. H. Davis 16398 (E [E00401507]). — Transitional morphologies to Fagus hohenackeriana : Ordu: P. H. Davis & O. Polunin 24935 (E [E00401509]); Amasya: J. Manissadjian 369b (P [P06812041]); Trabzon: A. Stainton 8408 (E [E00401551]); Nur Mountains: Fannie P. A. Shepard 10308853 ( US [NMNH-03400252]). — GBIF entries with photographs verify transitional forms to F. hohenackeriana from the provinces of Ordu and Giresun; very rarely transitional forms occur further west (Bolu): C. Aedo 6175 (B [B 10 1167842], MA [MA688421], PRN [PRN2022-024]).