Abstract
Two new fossil taxa referable to the basal eudicot grade are described from the Kamikitaba locality (ca. 89 MYBP, early Coniacian: Late Cretaceous) of the Futaba Group in Japan. These charcoalified mesofossils exhibit well-preserved three-dimensional structure and were analyzed using synchrotron-radiation X-ray microtomography to document their composition and internal structure. Cathiaria japonica sp. nov. is represented by infructescence segments that consist of an axis bearing three to four fruits. The capsular fruits are sessile and dehiscent and consist of a gynoecium subtended by a bract. No perianth parts are present. The gynoecium is monocarpellate containing two pendulous seeds. The carpel is ascidiate in the lower half and conduplicate in the upper part, and the style is deflected abaxially with a large, obliquely decurrent stigma. Pollen grains are tricolpate with a reticulate exine. The morphological features of Cathiaria are consistent with an assignment to the Buxaceae s. l. (including Didymelaceae). Archaestella verticillatus gen. et sp. nov. is represented by flowers that are small, actinomorphic, pedicellate, bisexual, semi-inferior, and multicarpellate. The floral receptacle is cup shaped with a perigynous perianth consisting of several tepals inserted around the rim. The gynoecium consists of a whorl of ten conduplicate, laterally connate but distally distinct carpels with a conspicuous dorsal bulge, including a central cavity. The styles are short, becoming recurved with a ventrally decurrent stigma. Seeds are ca. 10 per carpel, marginal, pendulous from the broad, oblique summit of the locule. Pollen grains are tricolpate with a reticulate exine pattern, suggesting a relationship to eudicots. The morphological features of Archaestella indicate a possible relationship to Trochodendraceae in the basal grade of eudicots. The fossil currently provides the earliest record of the family and documents the presence of Trochodendraceae in eastern Eurasia during the middle part of the Late Cretaceous.
Similar content being viewed by others
Change history
07 June 2017
An erratum to this article has been published.
References
APG III (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants:APG III. Bot Linn Soc 161:105–121
APG IV (2016) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot J Linn Soc 181:1–20
Chase MW, Soltis DE, Olmstead RG, Morgan D, Les DH, Mishler BD, Duvall MR, Price RA, Hills HG, Qiu Y-L, Kron KA, Rettig JH, Conti E, Palmer JD, Manhart JR, Sytsma KJ, Michaels HJ, Kress WJ, Karol KG, Clark WD, Hedren M, Gaut BS, Jansen RK, Kim K-J, Wimpee CF, Smith JF, Furnier GR, Strauss SH, Xiang Q-Y, Plunkett GM, Soltis PS, Swensen SM, Williams SE, Gadek PA, Quinn CJ, Eguiarte LE, Golenberg E, Learn GH Jr, Sean W, Graham SW, Barrett SCH, Dayanandan S, Albert VA (1993) Phylogenetics of seed plants; an analysis of nucleotide sequences from the plastid gene rbcL. Ann Missouri Bot Gard 80:528–580
Chen L, Ren Y, Endress PK, Tian XH, Zhang XH (2007) Floral organogenesis in Tetracentron sinense (Trochodendraceae) and its systematic significance. Pl Syst Evol 264:183–193
Cohen KM, Finney SC, Gibbard PL, Fan J-X (2013) The ICS International Chronostratigraphic Chart. Episodes 36:199–204 (updated 2016)
Crabtree DR (1987) Angiosperms of the northern Rocky Mountains: Albian to Campanian (Cretaceous) megafossil floras. Ann Missouri Bot Gard 74:707–747
Crane PR (1989) Paleobotanical evidence on the early radiation of nonmagnoliid dicotyledons. Plant Syst Evol 162:165–191
Crane PR, Manchester SR, Dilcher DL (1990) A preliminary survey of fossil leaves and well-preserved reproductive structures from the Sentinel Butte Formation (Paleocene) near Almont, North Dakota. Fieldiana Geol NS 20:1–63
Crane PR, Manchester SR, Dilcher DL (1991) Reproductive and vegetative structure of Nordenskioldia (Trochodendraceae), a vesselless dicotyledon from the Early Tertiary of the Northern Hemisphere. Am J Bot 78:1311–1334
Crane PR, Friis EM, Pedersen KR (1994) Paleobotanical evidence on the early radiation of magnoliid angiosperms. Plant Syst Evol 8(Suppl.):51–72
Crane PR, Friis EM, Pedersen KR (2004) Fossils and plant phylogeny. Am J Bot 91:1683–1699
Crepet WL, Nixon KC, Gandolfo MA (2004) Fossil evidence and phylogeny: the age of major angiosperm clades based on mesofossil and macrofossil evidence from Cretaceous deposits. Am J Bot 91:1666–1682.
Cronquist A (1981) An integrated system of classification of flowering plants. Columbia Univeristy Press, New York
Dowd BA, Campbell GH, Marr RB, Nagarkar VV, Tipnis SV, Axe L, Siddons DP (1999) Developments in synchrotron X-ray computed microtomography at the National Synchrotron Light Source. In: Bonse U (ed) Developments in X-Ray Tomography II, vol 3772. Proc SPIE, pp 224–236
Doweld AB (1998) Carpology, seed anatomy and taxonomic relationships of Tetracentron (Tetracentraceae) and Trochodendron (Trochodendraceae). Ann Bot 82:413–443
Doyle JA (2012) Molecular and fossil evidence on the origin of angiopserms. Ann Rev Earth Planet Sci 40:301–326
Doyle JA, Endress PK (2010) Integrating early Cretaceous fossils into the phylogeny of living angiosperms: Magnoliidae and eudicots. J Syst Evol 48:1–35
Doyle JA, Upchurch GR (2014) Angiosperm clades in the Potomac Group: what have we learned since 1977? Bull Peabody Musem Nat Hist 55:111–134
Drinnan AN, Crane PR, Friis EM, Pedersen KR (1991) Angiosperm flowers and tricolpate pollen of buxaceous affinity from the Potomac Group (mid-Cretaceous) of eastern North America. Am J Bot 78:153–176
Endress PK (1986) Floral structure, systematics, and phylogeny in Trochodendrales. Ann Missouri Bot Gard 73:297–324
Endress PK (1990) Patterns of floral construction in ontogeny and phylogeny. Biol J Linn Soc 39:153–175
Friis EM, Pedersen KR, Crane, PR (1994) Angiosperm floral structures from the Early Cretaceous of Portugal. Pl Syst Evol 8:31–49 (Suppl)
Friis EM, Pedersen KR, Crane PR (2006) Cretaceous angiopserm flowers: innovation and evolution in plant reproduction. Palaeogeogr Palaeoclimatol Palaeoecol 232:251–293
Friis EM, Crane PR, Pedersen KR, Bengtson S, Donoghue PCJ, Grimm GW, Stampanoni M (2007) Phase contrast enhanced synchrotron-radiation X-ray analyses of Cretaceous seeds link Gnetales to extinct Bennettitales. Nature 450:549–552
Friis EM, Pedersen KR, von Balthazar M, Grimm GW, Crane PR (2009) Monetianthus mirus gen. et sp. nov., a Nymphaealean flower from the Early Cretaceous of Portugal. Int J Plant Sci 10:1086–1101
Friis EM, Pedersen KR, Crane PR (2011) Early flowers and angiosperm evolution. Cambridge University Press, Cambridge
Golovneva IB, Oskolski AA (2007) Infructescences of Cathiaria gen n. from the late Cretaceous of North Kazakhstan and Siberia (Russia). Acta Paleobot 47:57–87
Grímsson F, Denk T, Zetter R (2008) Pollen, fruits, and leaves of Tetracentron (Trochodendraceae) from the Cainozoic of Iceland and western North America and their palaeobiogeographic implications. Grana 47:1–14
Herendeen PS, Doyle JA, Endress PK, Takahashi M (2016) Cecilanthus polymerus, a novel multiparted flower from the mid-Cretaceous Rocky Point locality, Maryland. Botany 94:787–803
Hsu Y-C, Jane W-N, Chen S-H (2017) Infrorescence and floral development in Trochodendron aralioides (Trochodendraceae). Plant Syst Evol 303:403–412
Hutchinson J (1964) The genera of flowering plants (Angiospermae), vol 1. Clarendon Press, Oxford
Li H-F, Chaw S-M, Du C-M, Ren Y (2011) Vessel elements present in the secondary xylem of Trochodendron and Tetracentron (Trochodendraceae). Flora 206:595–600
Manchester SR, Chen I (2006) Tetracentron fruits from the Miocene of western North America. Int J Plant Sci 167:601–660
Manchester SR, Crane PR, Dilcher DL (1991) Nordenskioldia and Trochodendron (Trochodendraceae) from the Miocene of northwestern North America. Bot Gaz 152:357–368
Mohr BAR, Friis EM (2000) Early angiosperms from the Aptian Crato Formation (Brazil), a preliminary report. Int J Plant Sci 161(6 Suppl.):S155–S167
Pedersen KR, von Balthazar M, Crane PR, Friis EM (2007) Early Cretaceous floral structures and in situ tricolpate-striate pollen: new early eudicots from Portugal. Grana 46:176–196
Pigg KB, Wehr WC, Ickert-Bond SM (2001) Trochodendron and Nordenskioeldia (Trochodendraceae) from the Middle Eocene of Washington State, USA. Int J Plant Sci 162:1187–1198
Pigg KB, Dillhoff RM, DeVore ML, Wehr WC (2007) New diversity among the Trochodendraceae from the Early/Middle Eocene Okanogan Highlands of British Columbia, Canada, and northeastern Washington State, United States. Int J Plant Sci 168:521–532
Ren Y, Chen L, Tian XH, Zhang XH, Lu AM (2007) Discovery of vessels in Tetracentron (Trochodendraceae) and its systematic significance. Pl Syst Evol 267:155–161
Schönenberger J, von Balthazar M, Takahashi M, Xiao X, Crane PR, Herendeen PS (2012) Glandulocalyx upatoiensis, a fossil flower of Ericales (Actinidiaceae/Clethraceae) from the Late Cretaceous (Santonian) of Georgia, USA. Ann Bot 109:921–936
Shipunov AB, Shipunova E (2011) Haptanthus story: rediscovery of enigmatic flowering plant from Honduras. Am J Bot 98:761–763
Stevens PF (2001) Angiosperm Phylogeny Website. Version 12, July 2012 [and more or less continuously updated since]. http://www.mobot.org/MOBOT/research/APweb/. Accessed 1 Dec 2016
Sutton DA (1989) The Didymelales: a systematic review. In: Crane PR, Blackmore S (eds) Evolution, systematics, and fossil history of the Hamamelidae, vol 1. Clarendon Press, Oxford, pp 279–284
Suzuki M, Joshi L, Fujii T, Noshiro S (1991) The anatomy of unusual tracheids in Tetracentron wood. IAWA J 12:23–33
Takahashi M, Crane PR, Ando H (1999a) Fossil flowers and associated plant fossils from the Kamikitaba locality (Ashizawa Formation, lower Coniacian, Upper Cretaceous) Northeast Japan. J Plant Res 112:187–206
Takahashi M, Crane PR, Ando H (1999b) Esgueiria futabaensis sp. nov.; a new angiosperm flower from the upper Cretaceous (lower Coniacian) of northeastern Honshu, Japan. Paleontol Res 3:81–87
Takahashi M, Herendeen PS, Crane PR (2001) Lauraceous fossil flowers from the Kamikitaba locality (Lower Coniacian; Upper Cretaceous) on northeastern Japan. J Plant Res 114:429–434
Takahashi M, Crane PR, Manchester SR (2002) Hironoia fusiformis gen. et sp. nov.; a cornalean fruit from the Kamikitaba locality (upper Cretaceous, lower Coniacian) in northeastern Japan. J Plant Res 115:463–473
Takahashi M, Friis EM, Crane PR (2007) Fossil seeds of Nymphaeales from the Tamayama Foramtion (Futaba Group), upper Cretaceous (early Santonian) of Northeastern Honshu, Japan. Int J Plant Sci 168:341–350
Takahashi M, Friis EM, Herendeen PS, Crane PR (2008a) Fossil flowers of Fagales from the Kamikitaba Locality (Early Coniacian; Late Cretaceous) of Northeastern Japan. Int J Plant Sci 169:899–907
Takahashi M, Friis EM, Uesugi K, Suzuki Y, Crane PR (2008b) Floral evidence of Annonaceae from the Late Cretaceous of Japan. Int J Plant Sci 169:908–917
Takahashi M, Herendeen PS, Xiao X, Crane PR (2014) Lauraceous fossil flowers from the Kamikitaba assemblage (Coniacian, Late Cretaceous) of northeastern Japan. Syst Bot 39:715–724
Uemura K (1988). Late Miocene Floras in Northeast Honshu, Japan. National Science Museum, Tokyo
Upchurch GR, Wolfe JA (1987) Mid-Cretaceous to Early Tertiary vegetation and climate: evidence from fossil leaves and woods. In: Friis EM, Chaloner WG, Crane PR (eds) The origins of angiosperms and their biological consequences. Cambridge University Press, Cambridge, pp 75–105
von Balthazar M, Endress PK (2002) Development of inflorescences and flowers in Buxaceae and the problem of perianth interretation. Int J Plant Sci 163:847–876
von Balthazar M, Endress PK, Qiu U-L (2000) Pylogenetic relaltionships in Buxaceae based on nuclear internal transcribed spacers and plastid ndhF sequences. Int J Plant Sci 161:785–792
von Balthazar M, Schatz GE, Endress PK (2003) Female flowers and inflorescences of Didymelaceae. Plant Syst Evol 237:199–208
von Balthazar M, Pedersen KR, Crane PR, Stampanoni M, Friis EM (2007) Potomacanthus lobatus gen. et sp. nov., a new flower of probable Lauraceae from the Early Cretaceous (Early to Middle Albian) of Eastern North America. Am J Bot 94:2041–2053
Wang YH, Ferguson DK, Feng GP, Wang YF, Zhilin SG, Li CS, Svetlana PT, Yang J, Ablaev AG (2009) The phytogeography of the extinct angiosperm Nordenskioeldia (Trochodendraceae) and its response to climate changes. Palaeogeog Palaeoclimatol Palaeoecol 280:183–192
Wu H-C, Su H-J, Hu J-M (2007) The identification of A-, B-, C-, and E-class MADS-box genes and implications for perianth evolution in the basal eudicot Trochodendron aralioides (Trochodendraceae). Int J Plant Sci 168:775–799
Acknowledgements
The authors thank Peter R Crane and Stephen R Manchester for constructive and helpful comments on the manuscript. The study was funded by Grants-in-Aid for Scientific Research (21570092, 24570097 and 16K07477) from Japan Society for the Promotion of Science to M. T. and NSF Grant DEB-1348456 to P.S.H. Use of the Advanced Photon Source, an Office of Science User Facility operated for the US Department of Energy (DOE) Office of Science by Argonne National Laboratory, was supported by the US DOE under Contract No. DE-AC02-06CH11357.
Author information
Authors and Affiliations
Corresponding author
Additional information
An erratum to this article is available at https://doi.org/10.1007/s10265-017-0957-x.
Rights and permissions
About this article
Cite this article
Takahashi, M., Herendeen, P.S. & Xiao, X. Two early eudicot fossil flowers from the Kamikitaba assemblage (Coniacian, Late Cretaceous) in northeastern Japan. J Plant Res 130, 809–826 (2017). https://doi.org/10.1007/s10265-017-0945-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10265-017-0945-1