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Revision of Icacinaceae from the Early Eocene London Clay Flora

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Revision of Icacinaceae from the Early Eocene London Clay Flora 713 ARTICLE Revision of Icacinaceae from the Early Eocene London Clay flora based on X-ray micro-CT1 Gregory W. Stull, Neil F. Adams, Steven R. Manchester, Dan Sykes, and Margaret E. Collinson Abstract: The Early Eocene (Ypresian) London Clay Formation contains one of the most important fruit and seed assemblages from the Paleogene, including a large diversity of taxa (>350 spp.) preserved as pyrite permineralizations retaining 3D structure as well as anatomical detail. Despite the importance of the flora for understanding angiosperm biogeographic and evolutionary history, the majority of the fossil material has not been revisited since the original taxonomic treatments by E.M. Reid and M.E.J. Chandler. Given subsequent advances in our understanding of angio- sperm phylogeny and fruit morphology, coupled with technological advances in imaging/visualizing fossil material, many of the taxa represented in the flora deserve further study. Here we present a revision of the pantropical family Icacinaceae using X-ray micro-computed tomography (micro-CT) images of 21 species from the flora. Based on the results, four new combinations are made, a new fossil-genus is established for a distinctive species with affinities to the Phytocreneae, and emended diagnoses are provided for eight taxa. Of the seven genera recognized from the flora, only one, Iodes Blume, is extant. This study offers important insights on the biogeographic and evolutionary history of Icacinaceae, which is one of the most abundant and diverse components of the flora from the London Clay Formation. Key words: endocarps, Eocene, Icacinaceae, Iodes, London Clay, X-ray tomography. Résumé : La formation d’argile de Londres (London Clay Formation) de l’Éocène précoce (Yprésien) comprend un des assemblages de fruits et de graines du Paléogène le plus important, comprenant une grande diversité de taxons (>350 spp.) préservés sous forme de minéralisations de pyrite qui conservent la structure en 3D de même que le détail anatomique. Malgré l’importance de la flore pour comprendre l’histoire biogéographique et évolutive des angiospermes, la majorité du matériel fossile n’a pas été revisité depuis les descriptions taxonomiques originales de E.M. Reid et M.E.J. Chandler. Compte tenu des progrès subséquents quant a` notre compréhension de la phylogénie des angiospermes et de la morphologie des fruits, couplés aux progrès technologiques en imagerie/ For personal use only. visualisation du matériel fossile, plusieurs taxons représentés dans la flore méritent d’être étudiés davantage. Les auteurs présentent ici une révision de la famille pantropicale des Icacinaceae a` l’aide d’images en micro- tomographie aux rayons-X assistée par ordinateur (micro-CT) de 21 espèces de la flore. Selon les résultats, quatre nouvelles combinaisons sont faites, un nouveau genre fossile est établi pour une espèce distinctive ayant des affinités avec les Phytocreneae, et des diagnostics amendés sont fournis pour huit taxons. Des sept genres recon- nus de la flore, un seul, Iodes Blume existe toujours. Cette étude offre un important aperçu de l’histoire bio- géographique et évolutive des Icacinaceae, qui constituent une des composantes les plus abondantes et diverses de la flore de la formation de l’argile de Londres. [Traduit par la Rédaction] Mots-clés : endocarpes, Éocène, Icacinaceae, Iodes, argile de Londres, tomographie par rayons-X. Introduction blages from the Paleogene, including more than 350 de- Botany Downloaded from www.nrcresearchpress.com by 5.151.196.72 on 10/23/16 The London Clay Formation (Early Eocene, Ypresian: scribed species (Collinson and Cleal 2001a). The flora is 56.0–47.8 Ma; Cohen et al. 2013) of southeast England exceptional not only for its diversity, which is unparal- contains one of the most important fruit and seed assem- leled by other well-studied Paleogene fossil floras (e.g., Received 2 March 2016. Accepted 17 May 2016. G.W. Stull and S.R. Manchester. Department of Biology and Florida Museum of Natural History, Dickinson Hall (FLMNH), 1659 Museum Road, P.O. Box 117800, University of Florida, Gainesville, FL 32611-7800, USA. N.F. Adams. Departments of Earth Sciences and Geography, Royal Holloway University of London, Egham, Surrey, TW20 0EX, UK. D. Sykes.* Imaging and Analysis Centre, Natural History Museum, London, SW7 5BD, UK. M.E. Collinson. Department of Earth Sciences, Royal Holloway University of London, Egham, Surrey, TW20 0EX, UK; Department of Earth Sciences, Natural History Museum, Cromwell Road, London, SW7 5BD, UK. Corresponding author: Gregory W. Stull (email: [email protected]). *Present address: School of Materials, University of Manchester, Oxford Road, Manchester, M13 9PL, UK. 1This Article is part of a Special Issue entitled “Mesozoic and Cenozoic Plant Evolution and Biotic Change,” a collection of research inspired by, and honouring, Ruth A. Stockey. Copyright remains with the author(s) or their institution(s). Permission for reuse (free in most cases) can be obtained from RightsLink. Botany 94: 713–745 (2016) dx.doi.org/10.1139/cjb-2016-0063 Published at www.nrcresearchpress.com/cjb on 7 September 2016. 714 Botany Vol. 94, 2016 Manchester 1994; Collinson et al. 2012), but also its su- utility and importance of this method for studying the perb preservation. The fossil fruits and seeds are pre- London Clay material. served predominantly as pyrite permineralizations and The flowering plant family Icacinaceae (Icacinales: retain cellular detail as well as uncompressed, three- Stevens 2001 onward; APG 2016) is an important compo- dimensional morphology (Reid and Chandler 1933; nent of the London Clay flora needing revision in light of Chandler 1961), thereby offering excellent taxonomic new phylogenetic and morphological data. Icacinaceae resolution. Given its diversity and quality of preserva- are a pantropical clade of woody trees, shrubs, and tion, the flora offers unique insight into the vegetation climbers including 23 genera and ϳ160 species (Stull present in Europe during the long- and short-term hyper- et al. 2015). One of the most diverse and abundant fami- thermals of the early Eocene (Zachos et al. 2001, 2008), lies in the London Clay flora, the Icacinaceae are repre- when increased global temperatures permitted the pole- sented by at least seven genera and 27 species, according ward expansion of thermophilic taxa. to the original works of Reid and Chandler (1933) and Numerous clades that are now largely confined to Chandler (1961, 1964, 1978). The family, in the traditional tropical latitudes, e.g., Annonaceae, Arecaceae, Burser- sense (Engler 1893; Howard 1940; Sleumer 1942), was aceae, Icacinaceae, and Menispermaceae, are well- grossly polyphyletic (Soltis et al. 2000; Kårehed 2001), but documented in the flora (Reid and Chandler 1933; recent phylogenetic work has greatly clarified the com- Chandler 1961). The London Clay fossils, in combination position of the family and relationships within it (Byng with records from other Eocene fruit and seed floras et al. 2014; Stull et al. 2015). Furthermore, recent and from Europe (e.g., Messel: Collinson et al. 2012) and ongoing studies of fruit morphology have highlighted North America (e.g., the Clarno Nut Beds: Scott 1954; characters useful for diagnosing clades within the family Manchester 1994), provide important data on historical (e.g., Stull et al. 2011, 2012; Allen et al. 2015). distributions of tropical plants. London Clay fossils also We present a systematic revision of Icacinaceae from constitute the oldest reliable calibration points for many the flora of the London Clay based on examinations of clades (e.g., Weeks et al. 2014). The flora has therefore new micro-CT images of 21 (out of 27) of the previously greatly informed studies of angiosperm biogeographic recognized fossil species (mostly focused on their holo- and evolutionary history. types) in the context of new information on fruit mor- The London Clay flora was extensively monographed phology across all modern and fossil genera of the by Reid and Chandler (1933), who described nearly family. New combinations are established for three spe- 300 species primarily from Sheppey, which is one of cies from the flora, several of which have important four major London Clay sites. Subsequent works (e.g., nomenclatural consequences for other fossils of Icaci- Chandler 1961, 1964, 1978) expanded on this original naceae from North America (Manchester 1994; Tiffney For personal use only. monograph, describing new species from the original 1999; Allen et al. 2015) and Europe (Kvacˇek and Bu˚ zekˇ sites and from additional sites of the London Clay Forma- 1995); these are discussed herein. A new combination is tion (e.g., Herne Bay and Bognor Regis). In her field guide also made for a species of Iodes from the Eocene of west- to the flora, Collinson (1983) provided information on ern North America with close affinities to a species from the relative stratigraphic positions within the London the London Clay (Iodes corniculata Reid et Chandler). We Clay Formation of the various sites from which the flora establish a new genus to accommodate a distinctive phy- has been collected. Herne Bay (division A2) is one of the tocrenoid taxon previously placed in the fossil genus oldest sites (ca. 55.0–54.6 Ma), whereas Sheppey (divi- Icacinicarya. Additionally, emended diagnoses are provided sions D and E) is one of the youngest (ca. 53.5–51.5 Ma) for eight taxa emphasizing characters found to be taxo- (Collinson 1983; Collinson and Cleal 2001a, 2001b). nomically useful in surveys of fossil and modern fruits Botany Downloaded from www.nrcresearchpress.com by 5.151.196.72 on 10/23/16 More recent studies (e.g., Mai 1980; Manchester et al. across the family. Finally, the evolutionary and biogeo- 2007, 2010; Manchester 2011) have clarified the system- graphic implications of these fossils are discussed within atic affinities of selected fossil taxa from the London the broader context of the family’s phylogeny and fossil Clay. However, the majority of the fossil material has not and modern distributions.
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