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Home , Aneuraceae, Hattoria, Jungermanniopsida, Metzgeria, Metzgeriaceae, Metzgeriales

Hattoria 11: 13–21. 2020

Discovery of a simple thalloid liverwort Metzgeriites kujiensis (), a new from Late Japanese amber

Tomoyuki KATAGIRI1 & Hisao SHINDEN2

1 Hattori Botanical Laboratory, Obi 6–1–26, Nichinan, Miyazaki 889–2535, Japan 2 Kuji Kohaku Co., Ltd., Kokuji-cho 19–156–133, Kuji, Iwate 028–0071, Japan Author for correspondence: Tomoyuki KATAGIRI, [email protected]

Abstract An extinct liverwort species Metzgeriites kujiensis T.Katag., sp. nov. is described from the Late Cretaceous (Santonian, ca. 85 Ma) amber from the Kuji district, northern Honshu, Japan. It is characterized by thalloid with a distinct midrib and lamina, narrow thalli of 0.6–0.8 mm wide, regularly 1-pinnate ramification pattern, and presence of discoid branches. The new species represents the first record of the liverwort family Metzgeriaceae (, ) from the Late Cretaceous from East Asia.

Introduction Kuji amber is the largest amber deposit in Japan and one of the most important sources for the reconstruction of terrestrial ecosystems in the Late Cretaceous East Asia continental margin, especially for revealing fauna and flora for microscopic species such as insects and . In spite of its importance in paleontology and evolutionary biology and of their potential abundance with over 800 insect inclusions, few studies have been conducted on amber from the deposit. For its insect inclusions Kawakami et al. (1994) studied 23 specimens of insects and Fursov et al. (2002) reported a fossil species of Mymarommatidae, an extremely rare family of microscopic hymenopteran insects. Recently, Nakamine & Yamamoto (2018) discovered a remarkable new and species of thorny lacewing (Neuroptera, Rhachiberothidae) and stressed the importance of the insect inclusions in Kuji amber. The discovery of a Muscites kujiensis T.Katag. inclusion by Katagiri et al. (2013) also provided valuable information on the Late Cretaceous bryoflora and demonstrated the importance of the Japanese amber for revealing the evolutional history of bryophytes in East Asia. In the present study we describe a new species of fossil liverwort preserved in the Late Cretaceous Kuji amber, the first evidence of a fossilized liverwort shoot found in Kuji amber and only the second record of a from the Late Cretaceous bryoflora in Japan. The new species also represents the first record of the liverwort family Metzgeriaceae (Metzgeriales, Marchantiophyta) from the Late Cretaceous from East Asia.

13 Materials and Methods Geological setting: The fossil described here is from the late Cretaceous Tamagawa Formation of the Kuji Group, which is distributed in the vicinity of Kuji City in Iwate Prefecture, northern Honshu, Japan. The Tamagawa Formation of the Kuji Group has been estimated to be 83–90 Ma (Umetsu & Kurita 2007; Katagiri et al. 2013; Uno et al. 2018). Based on carbon isotope stratigraphy and U–Pb radiometric dating, Arimoto et al. (2018), recently showed that the upper part of the Tamagawa Formation, with abundant ambers occurring in the coaly mudstone, is dated to the middle Santonian, ca. 85.9±0.7 Ma. Technical methods: The ground and polished amber piece of ca. 25×18×6 mm and weighing 1.66 g, which is housed in the herbarium of the Hattori Botanical Laboratory (NICH), was originally mined from Horinai Mine (40°09′01″N,141°44′08″E) in Kokuji-cho, Kuji City in July 2018. It had been selected for decorations and has been subjected to heat and pressure treatment to enhance the properties of the amber. The inclusion containing a single shoot was investigated using a Leica M205C stereomicroscope equipped with a Nikon DS-Fi3 digital camera. In to enhance contrast and avoid cast shadows, a Leica LED3000RL LED ring light and a Leica TL5000 Ergo LED transmitted light base were used.

Taxonomy Metzgeriites kujiensis T.Katag., sp. nov. Figs. 1 & 2

Diagnosis: Species of Metzgeriites with a distinct midrib and lamina. The species is similar to Metzgeriites yuxianensis X.W.Wu & B.X.Li, but differs by having narrow thalli of 0.6–0.8 mm wide, a regularly 1-pinnate ramification pattern, and the presence of discoid branches. Type: JAPAN. Honshu. Iwate Pref., Kuji City, Kokuji-cho. Inclusion in amber mined from the Horinai Mine (40°09′01″N, 141°44′08″E) in July 2018. Tamagawa Formation. Late Cretaceous (Santonian; approximately 85 Ma). Kuji Kohaku H1 (holotype: NICH-497606). Description: thalloid, dorsiventral, differentiated into midrib and lamina, 11 mm long and 2.0–4.0 mm wide including branches, regularly 1-pinnately branched at an angle of 45–75°, without ventral branches (Fig. 1). thin, lingulate, 1.0–2.0 mm long, (0.4–)0.6– 0.8 mm wide, with midrib 0.2–0.3 mm wide, without hairs on both dorsal and ventral surfaces, without ventral scales or mucilage hairs; margin linear, entire; apices obtuse to rounded (Fig. 2A–C). In the middle of the plant discoid branches ca. 1.0 mm in length and width with retuse or emarginate apices are present (Fig. 2E). These can be sexual branches or gemmae, but detailed morphology not preserved. Rhizoids smooth, present on ventral part of the main thallus lamina (Fig. 2D). Gemmae unknown. Reproductive structures and unknown. Etymology: The species epithet refers to the type locality. [Japanese name: Kuji- futamatagoke] Systematic position: Phylum: Marchantiophyta Stotler & Crand.-Stotl.; Class: Stotler & Crand.-Stotl.; Order: Metzgeriales Chalaud; Family: Metzgeriaceae H.Klinggr.; Genus: Metzgeriites Steere

14 Figure 1. Metzgeriites kujiensis T.Katag. A: Amber inclusion. B: Plant from dorsal view. C: Plant from ventral view. All photographed from NICH-497606, holotype.

Taxonomic changes Metzgeriites Steere, Amer. Midl. Naturalist 36: 306. 1947. ＝Metzgerites X.W.Wu & B.X.Li, Acta Palaeontol. Sin. 31: 276. 1992; nom. illeg., later homonym (Turland et al. 2018, Art. 53.2)

Metzgeriites barkolensis X.W.Wu (Turland et al. 2018, Art. 55.4) ≡Metzgerites barkolensis X.W.Wu, Acta Palaeontol. Sin. 35: 69. 1996.

15 Figure 2. Metzgeriites kujiensis T.Katag. A–B: Branches from dorsal view. C: Apical part of shoot from dorsal view. D: Part of main thallus from ventral view, showing a rhizoid arrowed. E: Median part of main thallus from dorsal view, showing discoid branches. All photographed from NICH-497606, holotype.

16 Metzgeriites exhibens X.W.Wu & B.X.Li (Turland et al. 2018, Art. 55.4) ≡Metzgerites exhibens X.W.Wu & B.X.Li, Acta Palaeontol. Sin. 31: 277. 1992. Metzgeriites multifidus P.C.Wu (Turland et al. 2018, Art. 55.4) ≡Metzgerites multifidus P.C.Wu, Acta Geol. Sin. 91: 1548. 2017. Metzgeriites multirameus G.Sun & Shao L.Zheng (Turland et al. 2018, Art. 55.4) ≡Metzgerites multiramea G.Sun & Shao L.Zheng, Early angiosperms and their associated plants from western Liaoning, China 180. 2001. Metzgeriites yuxianensis X.W.Wu & B.X.Li (Turland et al. 2018, Art. 55.4) ≡Metzgerites yuxianensis X.W.Wu & B.X.Li, Acta Palaeontol. Sin. 31: 276. 1992.

Discussion The epiphytic simple thalloid liverwort genus Raddi has a worldwide distribution and is a main component of the family Metzgeriaceae (Metzgeriales) which includes three genera: Metzgeria, Steereella Kuwah. with two species (Kuwahara 1973, 1986), and Vandiemenia Hewson with one species (Furuki & Dalton 2008). Recent molecular phylogenetic studies have suggested that Metzgeriaceae/Metzgeriales originated in the Permian, 285 Ma, and its crown group diversification took place in the Cretaceous, followed by Cenozoic radiations (Cooper et al. 2012; Laenen et al. 2014; Bechteler et al. 2019). In spite of the extant diversity of Metzgeria/Metzgeriaceae with ca. 100 species worldwide

Table 1. Fossil species in the family Metzgeriaceae. The species originally described under the genus Metzgerites, which is here considered to be a later homonym of Metzgeriites, were shown with an asterisk (*). Species name Period Country Reference Metzgeriothallus sharonae Middle USA Hernick et al. (2007) Hernick, Landing & Bartowski Metzgeriothallus metzgerioides (J.Walton) Late England Walton (1928), R.M.Schust. Schuster (1981) Metzgeriites glebosus (T.M.Harris) Early Greenland Harris (1931), Steere Steere (1947) Metzgeriites barkolensis X.W.Wu* Middle Jurassic China Wu (1996) Metzgeriites exhibens X.W.Wu & B.X.Li* Middle Jurassic China Wu & Li (1992) Metzgeriites yuxianensis Middle Jurassic China Wu & Li (1992) X.W.Wu & B.X.Li* Metzgeriites multirameus Late Jurassic China Sun et al. (2001) G.Sun & Shao L.Zheng* as M. multiramea Metzgeriites infracretaceus (Saporta) Early Cretaceous Portugal Saporta (1894), Oostend. Oostendorp (1987) Metzgeriites multifidus P.C.Wu* Early Cretaceous China Guo et al. (2017) Metzgeriites kujiensis T.Katag. Late Cretaceous Japan present study

17 (Söderström et al. 2016), fossil records of Metzgeria/Metzgeriaceae are extremely limited. They include two species of Metzgeriites Steere, five species of Metzgerites X.W.Wu & B.X.Li, and two species of Metzgeriothallus R.M.Schust. See Table 1 for details. The fossil-genus Metzgeriites was originally proposed by Steere (1947) for the thalloid fossil liverworts, based on the family Metzgeriaceae with the characters of the “Order Anacrogynae”. He included only M. glebosus (T.M.Harris) Steere [≡ Hepaticites glebosus T.M.Harris] (Harris 1931) from the Early Jurassic. The second genus Metzgerites X.W.Wu & B.X.Li [type: M. yuxianensis X.W.Wu & B.X.Li] was proposed by Wu & Li (1992) for fossil plants with the character of extant species of Metzgeria. The species of Metzgerites have all been known from the Jurassic to Cretaceous in China. However, we consider the genus Metzgerites should be treated as a later homonym of Metzgeriites Steere [type: M. glebosus] (Steere 1947) because both have been applied to fossil plants with the character of extant species of Metzgeria/Metzgeriaceae and are sufficiently alike to be confused (Turland et al. 2018, Art. 53.2). The genus Metzgeriothallus R.M.Schust. has become widely known because of the finding of well-preserved , Metzgeriothallus sharonae Hernick, Landing & Bartowski from Late Middle Devonian of eastern New York, USA. The genus was proposed by Schuster (1981, p. 185) with M. metzgerioides (J.Walton) R.M.Schust. (Schuster 1981) [≡Hepaticites metzgerioides J.Walton (Walton 1928)] as the type species for the fossil plants similar to the modern genus Metzgeria, segregating it from Hepaticites, while Hepaticies was lectotypified by Schuster (1966, p. 354) using H. langii J.Walton (Walton 1925) as the type, a species that exhibits no distinction between thallus wings and a costa and is thus similar to Gray of the family H.Klinggr., the only other family of Metzgeriales, together with Metzgeriaceae. In the present study, we consider Metzgeriothallus should be recognized as an independent genus from Metzgeriites for the Paleozoic Metzgeria- like fossils. Metzgeriites which has included only fossils to the present time. The new species is represented by a single fragment of a shoot, but the characteristics of the morphology of the thallus, such as having narrower thalli (usually less than 2 mm wide) with a clear differentiation between the thallus wings and midribs, lack of ventral scales or mucilage hairs, and round thallus apices that are not usually markedly attenuate, fully match the range of morphological variation of the species of Metzgeriaceae of the order Metzgeriales. The new species also superficially resembles species of the Pallaviciniales W.Frey & M.Stech, with a clear differentiation between the thallus wings and midribs, but the species of Pallaviciniales typically have wider thalli (usually more than 2 mm wide), an undulate lamina and a thallus margin with teeth or hairs, and numerous rhizoids on the midrib (Schuster 1992; Paton 1999; Damsholt 2002; Crandall-Stotler et al. 2009; Katagiri 2015). Based on morphological information, Metzgeriites yuxianensis X.W.Wu & B.X.Li is considered to be most closely related to M. kujiensis among the members of the Metzgeriaceae, where our inclusion in amber is assigned. Both species have narrow thalli and a midrib ca. 0.3 mm wide. M. yuxianensis is, however, distinguished from M. kujiensis by the thalli being a little wider, 1.0–2.0 mm wide, and the presence of numerous hairs on the ventral surface of the midrib. In M. kujiensis, thalli are (0.4–)0.6–0.8 mm wide (Fig. 1B) and apparently lack appendages on the midrib except for a rhizoid (Fig. 2D), and it exhibits a regularly 1-pinnate ramification pattern (Fig. 1B) and presence of discoid branches (Fig. 2E),

18 both of which are not known in M. yuxianensis. A poorly known Early Cretaceous species Metzgeriites infracretaceus (Saporta) Oostend. might have thalli similar to M. kujiensis, with narrow thalli and a rather regularly 1-pinnate ramification pattern, but the species lacks discoid branches. Another Early Cretaceous species, Metzgeriites multifidus P.C.Wu can be distinguished from M. kujiensis by its branching angle of less than 30°, while in M. kujiensis the branching angle is 45–75° (Fig. 2A–B). Other members of the family, Metzgeriothallus metzgerioides (J.Walton) R.M.Schust., Metzgeriothallus sharonae Hernick, Landing & Bartowski, Metzgeriites glebosus (T.M.Harris) Steere, Metzgeriites exhibens X.W.Wu & B.X.Li, Metzgeriites barkolensis X.W.Wu, Metzgeriites multirameus G.Sun & Shao L.Zheng can be easily distinguished from M. kujiensis by their wider thalli, usually more than 1.5 mm wide. Metzgeriites kujiensis from Japanese amber provides the first evidence that the family Metzgeriaceae (Metzgeriales, Marchantiophyta) was by the Late Cretaceous already present in Japan. The present study sheds light on the Late Cretaceous diversification of simple thalloid liverworts, especially of Metzgeriaceae, and also contributes to the further age calibration of the diversification of simple thalloid lineages. Further careful examination of bryophyte inclusions in the Japanese amber will provide further direct evidence of the Late Cretaceous bryoflora in East Asia and of the morphological evolution of bryophytes.

Acknowledgements We greatly appreciate the contribution of Ms. Satsuki Shimodate (Kuji Kohaku Co., Ltd.) for her immense support throughout the course of this study. We also thank to Prof. Rod Seppelt for his constructive comments and for checking the English text. This work was supported by JSPS KAKENHI Grant Number JP16K18604 and Grant-in-Aid for Scientific Research (Specially Designated Research Promotion) of Japan Society for the Promotion of Science (JSPS).

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