Symplocos kowalewskii (Casp.) Sadowski et Hofmann, 2023

Sadowski, Eva-Maria & Hofmann, Christa-Charlotte, 2023, The largest amber-preserved flower revisited, Scientific Reports 13 (1), pp. 17-17 : 17

Symplocos kowalewskii (Casp.) Sadowski et Hofmann comb. nov. et emend.

Basionym: Stewartia kowalewskii Casp. 1872, p. 17 [no figure].

Holotype: X4088 , figured in Figs. 1–3 . Repository: Federal Institute for Geosciences and Natural Resources (Bundesanstalt für Geowissenschafen und Rohstoffe, BGR), Berlin, Germany.

Plant Fossil Names Registry Number: PFN003014.

Additional references.

1886 Stuartia kowalewskii Casp. —Conwentz, p. 63 [no figure].

1890 Stuartia kowalewskii Casp. —Schenk, p. 517 [no figure].

1921 Stewartia L.—Gothan, p. 391 [no figure].

1929 Stuartia kowalewskii Casp. —Gothan, p. 114, Abb. 1 and figure on p. 128.

1948 Stuartia L.—Gothan, p. 20, Abb. 9a, a1.

1954 Stuartia L.—Gothan and Weyland, p. 417 [no figure].

1957 Stuartia kowalewskii —Kirchheimer, p. 584 [no figure].

1964 Stuartia L.—Gothan and Weyland, p. 455 [no figure].

1970 Stuartia kowalewskii Casp. —Rüffle and Helms, p. 247, pl. 2, fig. 2.

2000 Stuartia kowalewskii Casp. —Rüffle and Litke, p. 451, pl. II, fig. 1.

Emended diagnosis. Petals fused at the base into a ring-like structure. Outer surface of ring covered with few long simple trichomes. Stamens numerous, almost as long as petals, arranged in three consecutive rows. Pollen tricolporate, occasionally tetracolporate, with short colpi (brevicolpate) and conspicuous vestibulate apertures, exine is tectate, perforate and scabrate to verrucate (light microscopy; LM), and perforate to microreticulate on short columellae with occasionally occurring supratectal verrucae and echini (scanning electron microscopy; SEM).

Description. Corolla: 25–28 mm in diameter; petals five, fused at base (gamopetalous), linguiform to obovate, 7.2–9.3 × 11–13 mm, membranaceous, glabrous ( Fig. 1a–e ); at base forming a ring-like structure ( Figs. 1e , 2c ), 2.8 mm in diameter × 1 mm long, rim of ring 0.3 mm wide, covered with few trichomes ( Fig. 2d ). Trichomes simple, unbranched, acute, up to 880 µm long × 20 µm wide ( Fig. 2d ). Receptacle, calyx, and gynoecium: not preserved. Androecium: Stamens arranged in three rows, fused to base of petals ( Fig. 2b ), numerous,> 74 ( Fig. 1c–e ); filaments flattened, (5.3–) 8.22 (–11) mm long × (149–) 220 (–460) µm wide (middle part measured), base dilated ( Fig. 2b ), 240–260 µm wide, apex constricted ( Fig. 2a ); anthers with two thecae, basifixed, subglobose, (832–) 1073 (–1290) µm long × (832–) 911 (–1040) µm wide, base cordate, apex notched ( Figs. 2a , 3a ). Pollen: tricolporate to tetracolporate, with short colpi (= brevicolpate; Fig. 3b,c,e ), oblate to subspheroidal with typical vestibulate apertures, outline in polar view ranges from triangular, triangular convex to circular ( Fig. 3c–g ), equatorial diameter 30–70 µm; the ratio of the length of the polar axes and colpi is variable ranging from 2.3 to 3.2 (N = 6); thickness of ektexine (tectum, columellae and footlayer) ca. 0.6 µm, tectum and columellae 0.2–0.3 µm thick and in apertural region ca. twice as thick (LM). In LM: ektexine seems tectate and shows perforate, scabrate to loosely verrucate sculpture ( Fig. 3f ). In SEM: ektexine sculpture is perforate to microreticulate with occasionally occurring supratectal verrucae [diameter 0.3–0.8 (–1.5 µm)] and few supratectal blunt echini ( Fig. 3h–j ). Colpus length 8–12 µm long, colpus width 3–4 µm in the equator area, colpus apex weakly pointed; supratectal verrucae ofen fused at margo of ectoaperture into a rim-like structure ( Fig. 3j ); colpus membrane is microverrucate; endoporus ca. 5–6 µm high (width not discernable, but endoaperture appears to be more lalongate in outline).

Remarks. The fossil was first published as Stewartia kowalewskii Casp. (Theaceae; also occasionally spelled Stuartia 20), but not figured and only briefly described as a well preserved pentamerous corolla of 28 mm in diameter with attached stamens 18, 21. Since then, the flower inclusion was frequently mentioned by various authors and occasionally figured over the last decades 22 – 29. However, it was never documented in detail nor its identification thoroughly assessed. Kirchheimer 30 considered the fossil as similar to Stewartia I.Lawson but thought that the corolla did not provide sufficient evidence to demonstrate affinities to Stewartia . Affinities to the Theaceae, specifically the Camellioidae, were further suggested 31, 32 but never unambiguously proven. Indeed, the inclusion resembles members of the Camellioideae (including Stewartia ) in, for example, the basally connate and numerous (uncountable) stamens arranged in rows; the basifixed anthers (basifixed in some Camellia L. species, but dorsifixed in Stewartia ) which lack an apical prolongation of the connective; the length of filaments, which are nearly as long as the petals; and the basally fused corolla 32 – 36 ( Table 1 ). According to Tsou 37, 38, the only diagnostic character of the Camellioideae is the presence of pseudopollen in the connective of the anthers. We could not detect any pseudopollen in the anthers of the amber specimen. However, we are aware that despite the exquisite preservation of the amber specimen, the presence of such pseudopollen would be difficult to assess because it is rather small and inserted into the connective.

The extracted pollen of the fossil shows distinct features of Symplocos Jacq. (Symplocaceae) as it exhibits: tricolporate apertures with short colpi (polar axes/colpus length ratio), oblate to subspheroidal shape with a triangular to circular outline in polar view and conspicuous vestibulum. Tectum sculpture and ornamentation is variable: densely verrucate, rugulate to verrucate, a combination of rugulate to microreticulate, perforate, microverrucate, and microreticulate with or without supratectal ornamentation 39. Additionally, the combination of gross morphological characters is also indicative for Symplocos (Symplocaceae) , including gamopetalous corolla, androecium adnate to corolla, stamen non-monadelphous and numerous in three consecutive series, filaments thin and constricted at apex, anthers subglobose with two thecae 40.

According to Fritsch et al. 40, the Symplocaceae encompass two genera, Symplocos and Cordyloblaste Hensch. Ex Moritzi. However , in Cordyloblaste , the stamens are fused (monadelphous), androecium adnation to the corolla is roughly to the midpoint of the corolla, and petals are coriaceous 40. The pollen of Symplocos and Cordyloblaste share some similarities but can be distinguished by the supratectal ornamentation, which is present in Symplocos and S. kowalewskii , but lacking in Cordyloblaste 40 – 42.

Symplocos subgenus Palura (G.Don) P.W.Fritsch (with only one species, S. paniculata Miq. ) and Symplocos subgenus Symplocos are distinguished by characters that are mainly not preserved in the fossil, e.g., the numbers of carpels of the gynoecium. However, filaments of S. paniculata are terete and not constricted apically 40, whereas they are flattened in the amber specimen and taper towards the anthers. Moreover, in contrast to the amber specimen, the pollen of S. paniculata is rather small (26–28 µm in diameter) and has a triangular to concave triangular outline in polar view. Furthermore, the pollen of S. paniculata is unique in the rugulate to microreticulate sculpture with perforations and fossulae in between the rugulae, producing a bireticulated pattern. Also as opposed to the amber specimen, pollen of S. paniculata has no supratectal ornamentation 43, 44.

Therefore, the amber specimen is more closely affiliated with Symplocos subgenus Symplocos . As based on phylogenetic analysis, this subgenus is divided into taxa (corresponding to clades), including Symplocos sections Barberina A.DC., Lodhra G.Don and Symplocos . The latter is divided into series Symplocos and Urbaniocharis (Brand) P.W.Fritsch 40. The fossil can be excluded from sect. Symplocos based on the combination of its large size (thus excluding series Urbaniocharis, the species of which have corollas <10 mm long 45), the non-monadelphous stamens (in series Symplocos , stamens are connate roughly halfway), and the androecial adnation merely at the base of the corolla (androecium is adnate about halfway to the corolla in series Symplocos ). Moreover, within series Symplocos , the informal group (clade) “ Neosymplocos ” is distinguished from the fossil by its pubescent filaments 40.

The remaining sections Barberina and Lohdra can only be effectively compared to the amber fossil on the basis of pollen morphology. About 86 extant Symplocos pollen species have been documented in the literature 41, 42, 44, 46, 47. However, the documentation of sculpture variation of extant as well as fossil Symplocos pollen with SEM is incomplete because most pollen images are depicted only with light microscopy 48. In comparing the available extant Symplocos pollen types with those from S. kowalewskii , only a few Asian species resemble the amber specimen in shape, size, outline and ektexine sculpture and supratectal ornamentation, namely S. obtusa Wall. , S. pergracilis (Nakai) Yamazaki , S. tanakae Matsamura , and to a lesser extent S. pseudobarberina Gontscharow (all of S. section Lodhra ). These species are all characterized by a perforate to microreticulate tectum and supratectal verrucae and occasional supratectal echini 40, 42, which is somewhat similar to S. kowalewskii . However, the density, number and sizes of these supratectal elements differ from those in S. kowalewskii and vary considerably among the named extant species (quite dense in S. tanakae , larger and more loose or regularly distributed in the other species).

In section Barberina , some resemblance occurs in the tectum of S. variabilis 49; however, the overall shape and the rounded apex of the colpus differ from the states of S. kowalewskii .

Among the fossil record, pollen of S. kowalewskii resembles two fossil Symplocos pollen types from the early Oligocene Haselbach locality ( Germany 43, Symplocos sp. 2 and sp. 8) in being microreticulate to foveolate or perforate with supratectal verrucae and baculae. As in S. kowalewskii , these pollen types bear similarities to the extant Asian species S. obtusa , S. pergracilis , S. tanakae and S. pseudobarberina .

All in all, the flower and pollen morphology of the amber inclusion is indicative enough to justify its assignment to Symplocos subgenus Symplocos with the new combination Symplocos kowalewskii (Casp.) Sadowski et Hofmann comb. nov. et emend. Based on the available literature, comparisons of S. kowalewskii with extant and fossil Symplocos indicates affinities to Asian taxa, especially to some species in S. section Lodhra . However, future studies that comprehensively document pollen of Symplocaceae are necessary to elucidate distinct affinities of S. kowalewskii to extinct and modern lineages of the family.

Figures

Figure 1. Flower inclusion of Symplocos kowalewskii comb. nov. et emend. (Symplocaceae; X4088) from late Eocene Baltic amber. (a,b) Overview of the historic preparation of the amber specimen before restauration, showing fissures (b, upper arrowhead) and discoloration. The fractured cover slip had been fixed with tape (b, lower arrowhead). (c) Overview of the amber specimen afer extraction from the glass chamber. (d,e) Flower from the upper (d) and lower side (e) afer preparation. Note the fused staminate ring on the underside (e, arrowhead). Scale bars 1 cm in (a‒e).

Figure 2. Details of Symplocos kowalewskii comb. nov. et emend. (Symplocaceae; X4088) from late Eocene Baltic amber. (a) Anther. (b) Basally fused and broadened filaments, arranged in three rows and forming a fused ring. (c) Underside of the fused staminate ring with trichomes (arrowhead). (d) Simple, long, acute trichome (right arrowhead), magnified from (c); lef arrowhead indicates fungal hyphae. Scale bars 200 µm in (a), (b), (d); 1 mm in (c).

Figure 3. Pollen extracted from anthers and the surrounding amber of Symplocos kowalewskii comb. nov. et emend. (Symplocaceae; X4088) from late Eocene Baltic amber. (a) Anther, releasing pollen. (b‒g) Pollen under LM; note the protrusions from the apertures (c), which were likely caused by the excreted internal cell content. (h) Pollen under electron microprobe, with exposed intine (arrowhead). (i,j) Pollen under electron microprobe, showing perforate to microreticulate ornamentation with few supratectal blunt echini. Note the fused verrucae at the margo of the ectoaperture, forming a rim-like structure (j). Scale bars 500 µm in (a); 50 µm in (b); 20 µm in (c–g); 10 µm in (h), 1 µm in (i,j).

Tables

Table 1. Comparison of Symplocos kowalewskii comb. nov. et emend. from late Eocene Baltic amber to fossil and extant flowers of the Symplocaceae and Theaceae. Information that was not available is indicated with ‒. Data from29,32,33,35–38,40,55–57,74,76,96,97. Flower diameter of S. bureauana measured from the holotype MNHN.F-2170.2.

Genus	Symplocos kowalewskii	Symplocos bureauana	Symplocos subspicata	Symplocos subg. Symplocos	Stewartia (Ɯeaceae)
Distribution	Samland Peninsula (Kalini- grand, Russia)	Sézanne, Châlons (Marne, France); Wimmelburg near Eisleben (Saxony-Anhalt, Germany)	Wimmelburg near Eisleben (Saxony-Anhalt, Germany)	Americas, eastern Asia, Australasia	China, Japan, Korea, South Eastern United States
Age	Late Eocene (Priabonian)	Early Eocene, early Oligocene	Early Eocene, early Oligocene	Extant	Extant
Flower size (mm)	25 ‒ 28	(7 ‒) 8 (‒ 1)	‒	(3 ‒) 13 (‒ 50)	20 ‒ 50
Petals	5; basally fused forming a low ring	5; short tube	5; basally fused, forming a short, pentagonal tube	(3 ‒) 5 (‒ 15); basally fused or connate beyond base	5; basally slightly connate, imbricate
Shape	Obovate, rounded	Ovate-oblong, lanceolate, acute	Linguiform	Oblong	Obovate
Stamens	> 74	18	25 ‒ 30	(4 ‒ 15 ‒) 40 ‒ 100	Numerous
Arrangement	Arranged in three rows; basally adnate to petals	In 5 groups, each with 3 stamens, alternating with petals, arranged in one row; non-fused	In groups, each with 5–6 sta- mens, antepetalous, arranged in one row, basally fused with the tube	Uniseriate or 2–4-seriate; basally adnate to petals	Adnate to petals or free
Filaments	Non-monadelphous, flattened, broadening towards base, api- cally constricted; glabrous	Non-monadelphous, no broadening towards base	Non-monadelphous, wider towards base	(Non-)monadelphous; terete or tangentially flattened; apically constricted or not; glabrous	Basally connate, forming a tube
Anthers	Apically notched, base cor- date; subglobose, basifixed	Apically rounded, base cordate	Globose	Basifixed	Dorsifixed, versatile
Pseudo pollen	Absent	‒	‒	Absent	Present