Journal of Plant Research

, Volume 130, Issue 5, pp 809–826 | Cite as

Two early eudicot fossil flowers from the Kamikitaba assemblage (Coniacian, Late Cretaceous) in northeastern Japan

  • Masamichi Takahashi
  • Patrick S. Herendeen
  • Xianghui Xiao
Regular Paper


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.


Angiosperms Archaestella verticillatus Cathiaria japonica Futaba group Japan Kamikitaba assemblage Coniacian Cretaceous Buxaceae s. lMesofossil Synchrotoron-radiation X-ray microtomography (SRXTM) Trochodendraceae 



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.


  1. APG III (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants:APG III. Bot Linn Soc 161:105–121CrossRefGoogle Scholar
  2. 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 181:1–20CrossRefGoogle Scholar
  3. 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 80:528–580CrossRefGoogle Scholar
  4. Chen L, Ren Y, Endress PK, Tian XH, Zhang XH (2007) Floral organogenesis in Tetracentron sinense (Trochodendraceae) and its systematic significance. Pl Syst Evol 264:183–193CrossRefGoogle Scholar
  5. Cohen KM, Finney SC, Gibbard PL, Fan J-X (2013) The ICS International Chronostratigraphic Chart. Episodes 36:199–204 (updated 2016) Google Scholar
  6. Crabtree DR (1987) Angiosperms of the northern Rocky Mountains: Albian to Campanian (Cretaceous) megafossil floras. Ann Missouri Bot Gard 74:707–747CrossRefGoogle Scholar
  7. Crane PR (1989) Paleobotanical evidence on the early radiation of nonmagnoliid dicotyledons. Plant Syst Evol 162:165–191CrossRefGoogle Scholar
  8. 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 20:1–63Google Scholar
  9. 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 78:1311–1334CrossRefGoogle Scholar
  10. Crane PR, Friis EM, Pedersen KR (1994) Paleobotanical evidence on the early radiation of magnoliid angiosperms. Plant Syst Evol 8(Suppl.):51–72Google Scholar
  11. Crane PR, Friis EM, Pedersen KR (2004) Fossils and plant phylogeny. Am J Bot 91:1683–1699CrossRefPubMedGoogle Scholar
  12. 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.CrossRefPubMedGoogle Scholar
  13. Cronquist A (1981) An integrated system of classification of flowering plants. Columbia Univeristy Press, New YorkGoogle Scholar
  14. 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 224–236Google Scholar
  15. Doweld AB (1998) Carpology, seed anatomy and taxonomic relationships of Tetracentron (Tetracentraceae) and Trochodendron (Trochodendraceae). Ann Bot 82:413–443CrossRefGoogle Scholar
  16. Doyle JA (2012) Molecular and fossil evidence on the origin of angiopserms. Ann Rev Earth Planet Sci 40:301–326CrossRefGoogle Scholar
  17. Doyle JA, Endress PK (2010) Integrating early Cretaceous fossils into the phylogeny of living angiosperms: Magnoliidae and eudicots. J Syst Evol 48:1–35CrossRefGoogle Scholar
  18. Doyle JA, Upchurch GR (2014) Angiosperm clades in the Potomac Group: what have we learned since 1977? Bull Peabody Musem Nat Hist 55:111–134CrossRefGoogle Scholar
  19. 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 78:153–176CrossRefGoogle Scholar
  20. Endress PK (1986) Floral structure, systematics, and phylogeny in Trochodendrales. Ann Missouri Bot Gard 73:297–324CrossRefGoogle Scholar
  21. Endress PK (1990) Patterns of floral construction in ontogeny and phylogeny. Biol J Linn Soc 39:153–175CrossRefGoogle Scholar
  22. Friis EM, Pedersen KR, Crane, PR (1994) Angiosperm floral structures from the Early Cretaceous of Portugal. Pl Syst Evol 8:31–49 (Suppl) Google Scholar
  23. Friis EM, Pedersen KR, Crane PR (2006) Cretaceous angiopserm flowers: innovation and evolution in plant reproduction. Palaeogeogr Palaeoclimatol Palaeoecol 232:251–293CrossRefGoogle Scholar
  24. 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 450:549–552CrossRefPubMedGoogle Scholar
  25. 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 10:1086–1101CrossRefGoogle Scholar
  26. Friis EM, Pedersen KR, Crane PR (2011) Early flowers and angiosperm evolution. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  27. Golovneva IB, Oskolski AA (2007) Infructescences of Cathiaria gen n. from the late Cretaceous of North Kazakhstan and Siberia (Russia). Acta Paleobot 47:57–87Google Scholar
  28. 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 47:1–14CrossRefGoogle Scholar
  29. Herendeen PS, Doyle JA, Endress PK, Takahashi M (2016) Cecilanthus polymerus, a novel multiparted flower from the mid-Cretaceous Rocky Point locality, Maryland. Botany 94:787–803CrossRefGoogle Scholar
  30. Hsu Y-C, Jane W-N, Chen S-H (2017) Infrorescence and floral development in Trochodendron aralioides (Trochodendraceae). Plant Syst Evol 303:403–412CrossRefGoogle Scholar
  31. Hutchinson J (1964) The genera of flowering plants (Angiospermae), vol 1. Clarendon Press, OxfordGoogle Scholar
  32. 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 206:595–600CrossRefGoogle Scholar
  33. Manchester SR, Chen I (2006) Tetracentron fruits from the Miocene of western North America. Int J Plant Sci 167:601–660CrossRefGoogle Scholar
  34. Manchester SR, Crane PR, Dilcher DL (1991) Nordenskioldia and Trochodendron (Trochodendraceae) from the Miocene of northwestern North America. Bot Gaz 152:357–368CrossRefGoogle Scholar
  35. Mohr BAR, Friis EM (2000) Early angiosperms from the Aptian Crato Formation (Brazil), a preliminary report. Int J Plant Sci 161(6 Suppl.):S155–S167CrossRefGoogle Scholar
  36. 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 46:176–196CrossRefGoogle Scholar
  37. Pigg KB, Wehr WC, Ickert-Bond SM (2001) Trochodendron and Nordenskioeldia (Trochodendraceae) from the Middle Eocene of Washington State, USA. Int J Plant Sci 162:1187–1198CrossRefGoogle Scholar
  38. 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 168:521–532CrossRefGoogle Scholar
  39. Ren Y, Chen L, Tian XH, Zhang XH, Lu AM (2007) Discovery of vessels in Tetracentron (Trochodendraceae) and its systematic significance. Pl Syst Evol 267:155–161CrossRefGoogle Scholar
  40. 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 109:921–936CrossRefPubMedPubMedCentralGoogle Scholar
  41. Shipunov AB, Shipunova E (2011) Haptanthus story: rediscovery of enigmatic flowering plant from Honduras. Am J Bot 98:761–763CrossRefPubMedGoogle Scholar
  42. Stevens PF (2001) Angiosperm Phylogeny Website. Version 12, July 2012 [and more or less continuously updated since]. Accessed 1 Dec 2016
  43. 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 279–284Google Scholar
  44. Suzuki M, Joshi L, Fujii T, Noshiro S (1991) The anatomy of unusual tracheids in Tetracentron wood. IAWA J 12:23–33CrossRefGoogle Scholar
  45. 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 112:187–206CrossRefGoogle Scholar
  46. 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 3:81–87Google Scholar
  47. Takahashi M, Herendeen PS, Crane PR (2001) Lauraceous fossil flowers from the Kamikitaba locality (Lower Coniacian; Upper Cretaceous) on northeastern Japan. J Plant Res 114:429–434CrossRefGoogle Scholar
  48. 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 115:463–473CrossRefPubMedGoogle Scholar
  49. 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 168:341–350CrossRefGoogle Scholar
  50. 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 169:899–907CrossRefGoogle Scholar
  51. 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 169:908–917CrossRefGoogle Scholar
  52. Takahashi M, Herendeen PS, Xiao X, Crane PR (2014) Lauraceous fossil flowers from the Kamikitaba assemblage (Coniacian, Late Cretaceous) of northeastern Japan. Syst Bot 39:715–724CrossRefGoogle Scholar
  53. Uemura K (1988). Late Miocene Floras in Northeast Honshu, Japan. National Science Museum, TokyoGoogle Scholar
  54. 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 75–105Google Scholar
  55. von Balthazar M, Endress PK (2002) Development of inflorescences and flowers in Buxaceae and the problem of perianth interretation. Int J Plant Sci 163:847–876CrossRefGoogle Scholar
  56. 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 161:785–792CrossRefGoogle Scholar
  57. von Balthazar M, Schatz GE, Endress PK (2003) Female flowers and inflorescences of Didymelaceae. Plant Syst Evol 237:199–208CrossRefGoogle Scholar
  58. 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 94:2041–2053CrossRefGoogle Scholar
  59. 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 280:183–192CrossRefGoogle Scholar
  60. 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 168:775–799CrossRefGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan 2017

Authors and Affiliations

  • Masamichi Takahashi
    • 1
  • Patrick S. Herendeen
    • 2
  • Xianghui Xiao
    • 3
  1. 1.Department of Environmental Sciences, Faculty of ScienceNiigata UniversityNiigataJapan
  2. 2.Chicago Botanic GardenGlencoeUSA
  3. 3.Advanced Photon SourceArgonneUSA

Personalised recommendations