Evolving Earth 1 (2023) 100017 Contents lists available at ScienceDirect Evolving Earth journal homepage: www.sciencedirect.com/journal/evolving-earth Evolutionary history, biogeography, and extinction of the Cretaceous cheirolepidiaceous conifer, Frenelopsis Josep Marmi a, b, Aixa Tosal c, d, e, *, Carles Martín-Closas c, d a Dinosaur Ecosystems Research Group, Institut Català de Paleontologia Miquel Crusafont, Sabadell-Campus de la UAB, 08193, Cerdanyola del Vallès, Catalonia, Spain b Museu de la Conca Dellà i Dinosfera, C/ del Museu, 4, 25650, Isona, Catalonia, Spain c Departament de Dinàmica de la Terra i de l’Oceà, Facultat de Ciències de la Terra, Universitat de Barcelona-UB, C/ de Martí i Franqués s/n, 08028, Barcelona, Catalonia, Spain d Institut de Recerca de la Biodiversitat- IRBIO, Universitat de Barcelona-UB, C/ de Martí i Franquès s/n, 08028, Barcelona, Catalonia, Spain e Muséum National d’Histoire Naturelle, CR2P, UMR7207, MNHN, Sorbonne Université, CNRS, 57 rue Cuvier, CP 48, 75005, Paris, France A R T I C L E I N F O A B S T R A C T Keywords: Frenelopsis Schenk (family Cheirolepidiaceae†) was among the most widespread conifer genera and a dominant Fossil conifers element of wetland ecosystems in low to mid-palaeolatitudes in the the Northern Hemisphere. It was also one of Macroevolution the more important peat-forming shrubs and trees generating extensive deposits of Cretaceous lignite. The genus Palustrine became extinct at the end of the Cretaceous. Studies of the presence/absence and diversity of Frenelopsis allow us Island biogeography to analyse its evolutionary history, biogeography, and the consider the possible causes of its extinction. During K/Pg boundary the Early Cretaceous, the genus diversified, triggered by the rise of short-lived species and the constraint of endemism. The maximum diversity and species richness were attained in Barremian and Aptian times while the maximum number of global occurrences is documented during the Albian. In the Late Cretaceous, Frenelopsis species richness declined and the genus became progressively more restricted to the Tethyan archipelago in the context of the rise to dominance of angiosperms. In the Maastrichtian, the last representatives of Frenelopsis survived in the coastal wetlands of Iberia as a relictual plant. In northeast Iberia (present-day Pyrenees) the last occurrences from this genus are early to middle Maastrichtian in age and show an intriguing contrast between the abundance of vegetative remains and the lack of Classopollis pollen grains. These data suggest that at the end of its lineage, the plant was reproducing only vegetatively and that male sterility may have contributed to extinction. 1. Introduction evidence that polyploidy might have been crucial for speciation within the Cheirolepidiaceae (Kürschner et al., 2013). The production of The Cheirolepidiaceae was a diverse and widespread Mesozoic unreduced (i.e., diploid gametophytes pollen grains) and whole-genome conifer family. The earliest members date back to the early Late Triassic doubling mechanisms (i.e., polyploidy) is widespread in living flowering and, over 160 million of years, they developed highly variable growth plants, but is rare in other seed plant lineages (Stebbins, 1971; Leitch habits and spread throughout a wide range of ecological niches (Alvin, and Leitch, 2012). Another distinctive feature of the Cheirolepidiaceae 1982; Watson, 1988). They became particularly diverse in low latitudes is the structure of pollen wall of Classopollis Pflug emend. Srivastava, but declined in many areas already by the early Late Cretaceous (Wat­ which is among the most complex in conifers (Srivastava, 1976; Alvin, son, 1988; van der Ham et al., 2003). Their latest representatives 1982). Ovulate cones in Frenelopsis also reveal specialized tissues sug­ occurred in southernmost South America until the early Paleogene, gesting insect pollination (Labandeira et al., 2007). These particular surviving the Cretaceous/Paleogene (K/Pg) mass extinction for a short features render it difficult to understand the origins and phylogenetic period (Barreda et al., 2012). The morphological and ecological plas­ relationships of the Cheirolepidiaceae (Escapa and Leslie, 2017). Hence, ticity of the family may explain their great evolutionary success and Miller (1988) suggested that genus Hirmeriella Hörhammer, a type of resistance to extreme environmental conditions. Moreover, there is cheirolepidiaceous ovulate cone, could be a sister clade to the * Corresponding author. Departament de Dinàmica de la Terra i de l’Oceà, Facultat de Ciències de la Terra, Universitat de Barcelona-UB, C/ de Martí i Franqués s/ n, 08028, Barcelona, Catalonia, Spain. E-mail addresses: jm.marmi@gmail.com (J. Marmi), atosal@ub.edu, aixatosal@gmail.com (A. Tosal), cmartinclosas@ub.edu (C. Martín-Closas). https://doi.org/10.1016/j.eve.2023.100017 Received 14 October 2023; Received in revised form 19 October 2023; Accepted 19 October 2023 Available online 20 October 2023 2950-1172/© 2023 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by- nc-nd/4.0/). J. Marmi et al. Evolving Earth 1 (2023) 100017 Podocarpaceae or Cephalotaxaceae, whereas Alvin (1982) and Watson Female cones were first described from the Cenomanian of Bohemia (1988) indicated putative relationships with the Cupressaceae. More under genus Alvinia Kvaček, and were associated with F. alata (Kvaček, recently, affinities to Araucariaceae and Podocarpaceae have also been 2000). These ovuliferous cones are ovoid, larger (4.5 cm in diameter) proposed based on the presence of a tissue flap covering their seeds than male cones and attached to a robust axis. The megasporophylls are (Escapa et al., 2012). There is disagreement among palaeobotanists as to large (up to 20 mm long) broadly rhomboidal, obtuse, with crenulate the Cretaceous genera that can be placed within the Cheirolepidiaceae. margins, and spirally arranged. A covering flap is distally attached to the However, Frenelopsis Schenk, Pseudofrenelopsis Nath., Tarphyderma adaxial surface of the scale. Each scale encloses a central, single seed. Archang. and Taylor, and Tomaxellia Archang. are unequivocally Kvaček (2000) suggested that the pollination of Alvinia was similar to assigned to the family (Taylor et al., 2009). that of the living representatives of Agathis Salisbury and Araucaria Frenelopsis, with about 20 species, all restricted to the Cretaceous, Jussieu. Likewise, the funnel-like pollen chamber in scales of Alvinia was achieved high diversity and widespread distribution (Mendes et al., lined by trichomes, which caught the Classopollis pollen. Then, pollen 2010). Frenelopsis habits ranged from small shrubs to nearly 20-m-tall tubes grew from the pollen grains at the bottom of the funnel-like trees, and most of them showed evidence of xeromorphy in response structure to the micropyle. Kvaček (2000) also hypothesized that to diverse ecological constraints (e.g., Watson, 1977, 1988; Gomez et al., propagation of Alvinia seeds might have been assisted by cone scales 2001, 2002a; Axsmith and Jacobs, 2005; Bartiromo et al., 2012). For dispersed by wind as in extant Araucaria, Cedrus Trew or Abies Miller. instance, in the Lower Cretaceous of Iberia, different species of Frene­ lopsis grew in a wide range of habitats including marine coastal man­ 2.3. Pollen groves and brackish marshes as well as freshwater floodplains and lakeshores, and probably underwent water stress due to variable salinity Cuticular studies of male cones attached to Frenelopsis axes have or seasonal aridity (Gomez et al., 2002a). Frenelopsis was particularly revealed pollen sacs containing great number of pollen grains with the abundant and diverse in the Tethyan archipelago, and likely comprised distinctive morphology of the group Circumpolles (Pflug) Klaus (Barale large amounts of biomass that led these conifers to be one of the et al., 1988). The genus Classopollis (Pflug) is the most characteristic of dominant peat-forming plants, precursors of coal (lignite), e.g., in the this extinct group (Jarzen and Nichols, 1996) and it is a very common Cretaceous of Iberia (Gomez et al., 2001; Villalba-Breva et al., 2012) and Mesozoic pollen type produced by Cheirolepidiaceae, mainly in Jurassic probably elsewhere in the paratropical belt. In the present paper, we and early Cretaceous palynological assemblages (Hluštík and study the evolutionary and biogeographic history of Frenelopsis in order Konzalová, 1976a,b; Alvin, 1977; Barale et al., 1988; Kvaček, 2000; to better understand its origins, diversification and especially its Gomez et al., 2002a). extinction. The pollen grains of Classopollis can be isolated or, more commonly, arranged in tetrads. These spheroidal grains have a circumpolar sub­ 2. Description of vegetative and reproductive structures equatorial groove that divide two unequal hemispheres. They are cir­ cular in polar view and rather elliptical in equatorial view with a small 2.1. Vegetative system trilete mark in the proximal side and a distal circular cryptopore. The exine has scabrate or reticulate ornamentation with the smallest ele­ Frenelopsis is easily distinguished from fossil and living conifers by ments around the distal pore and the largest in the equatorial band. unique macro- and micro-morphological features (e.g., Gomez et al., Cheirolepidiaceae generally was anemophilous (but putative ento­ 2002a, b). Leafy axes consist of jointed cylindrical units, each formed by mophily was reported by Labandeira et al., 2007), and produced large two or three fused leaves forming relatively short, free, apical tips and amounts of pollen. From an ecological viewpoint, the Cheirolepidiaceae extending to the base in a long sheath showing no suture between the inhabited both freshwater mires and coastal brackish wetlands. In the leaves. These units are arranged in opposite-decussate phyllotaxy when latter, their pollen grains are considered sensitive indicators of the sea leaves are two or whorled (rotating by approximately 60◦ ) when there level changes (Azéma et al., 1981). In the Cretaceous series of the are three. In most species they branch punching a hole in one of the western Portuguese Basin (Taugourdeau-Lanz et al., 1982), the paly­ leaves (Daviero et al., 2001). Cuticles and especially the stomatal ap­ nological assemblages with large amounts of bisaccate pollen grains and paratuses provide the main significant characters to determine Frene­ low representation of Classopollis were indicative of transgressive pe­ lopsis species (e.g., Gomez et al., 2002a). Stomata are bordered by a thick riods. By contrast, these abundances reversed in regressive phases. This stomatal rim and organized in longitudinal stomatal rows, more or less same pattern was observed in the Cenomanian-Turonian deposits of the parallel along the leaf sheath, which converge toward the apex in each Vendée (France) where the regressive phases correspond to an increase free tip. Guard cells are sunken and surrounded by a ring of four to six of Classopollis abundance (Azéma et al., 1981; Néraudeau et al., 2017). subsidiary cells each bearing one outer and often one inner papilla This may reflect the extension of Frenelopsis-dominated wetlands during overhanging and closing the throat of the stomatal pit. Beyond these latter phases. morphological characters, Frenelopsis also appears to show its own The fact that the pollen grains of Classopollis often appear grouped in chemotaxonomic cuticle features (Lafuente-Diaz et al., 2023). tetrads indicates a negligible transport (Stuckins et al., 2017; Stuckins, 2022). This evidence and good preservation suggest autochthony and 2.2. Reproductive structures have been used altogether to infer proximity to the growth area. Reports of cones bearing pollen grains are rarer than vegetative or­ 3. Materials and methods gans. Microsporangiate cones were found attached to leafy axes in Fre­ nelopsis oligostomata Romariz emend. Alvin (Lauverjat and Pons, 1978), This study is based on a literature survey, which was used to F. alata (Feistmantel) Knobloch (Kvaček, 2000), F. turolensis Gomez et al. construct a dataset of Frenelopsis global occurrences during the Creta­ (2002a), F. ugnaensis Gomez et al. (2002a) and F. ramosissima Fontaine ceous (Table 1). Only species that have been described based on cutic­ emend. Watson (Axsmith and Jacobs, 2005). Male cones of Frenelopsis ular characters and figured have been included in the analysis, while (e.g., Classostrobus Alvin et al.) show little morphological variability species described or reported only on the basis of general shoot (Gomez et al., 2002a; Axsmith and Jacobs, 2005). They are small morphology were not considered. The dataset includes information on (3.5− 13 mm long and 2.5− 11 mm wide) and round to ellipsoidal or the age, taxonomy, geographic location and references. The occurrences elongated. Their microsporophylls are triangular to rhomboidal, spirally were plotted on seven global and four regional (Tethyan archipelago) arranged or peltate. The number of pollen sacs per microsporophyll is palaeogeographic maps in order to display the biogeographic history of unknown for all aforementioned species. Frenelopsis during the Cretaceous. Species richness, origination and 2 J. Marmi et al. Evolving Earth 1 (2023) 100017 Table 1 Dataset of Frenelopsis occurrences during the Cretaceous. Age Species Taxonomy Country Locality Area/Region Reference revisited Berriasian occidentalis occidentalis Germany Hildesheim Lower Saxony Watson and Alvin (1999) Berriasian- malaiana malaiana Malaysia Maran Pang Smiley (1970); Lejal-Nicol (1987); Uyop and Che Valangian Aziz (2000) Berriasian- malaiana malaiana Malaysia Panti Pang Smiley (1970); Uyop and Che Aziz (2000) Valangian Valanginian teixeirae teixerae Portugal Sesimbra Sesimbra Rey (1972); Alvin and Pais (1978) Valanginian sp. sp. Portugal S. Lourenço Ericeira Teixeira (1948); Rey (2006) Valanginian to early sp. sp. Portugal Zambujeiro Cercal Teixeira (1948); Rey (1993) Albian Hauterivian sp. sp. Czech Republic Beskyd Mts. north Moravia Hluštík (1978) Hauterivian sp. sp. France La Crapaudière Chapelle-aux-Pots Carpentier (1933) Hauterivian sp. sp. France Plaines Pays de Bray Carpentier (1933) Hauterivian hoheneggeri hoheneggeri Poland Przenosza Skrzydlna, Beskid Reymanówna (1965); Reymanówna and Watson Sredni (1976) Hauterivian hoheneggeri hoheneggeri Poland Wiśniowa Beskid Srekid Reymanówna (1965); Reymanówna and Watson (1976) Hauterivian hoheneggeri hoheneggeri Poland Srekid Beskid Srekid Reymanówna (1965); Reymanówna and Watson (1976) early Hauterivian sp. sp. Portugal S. Sebastião Runa Teixeira (1948); Rey (2006) Hauterivian teixeirae teixerae Portugal Vale Cortiço clay Torres Vedras Rey (1993); Mendes et al. (2010); Lafuente-Diaz pit et al. (2023) late Hauterivian- sp. sp. Spain Vallazmorra Hortezuelos, Santo Sender et al. (2011) early Aptian Domingo de Silos Hauterivian - early hoheneggeri hoheneggeri Poland Lipnik Bielsko Schenk (1869); Reymanówna (1965) Barremian Early Cretaceous sifloana sifloana Sudan Darfur Watson and Alvin (1976); Watson (1983) Hauterivian? - atlantica atlantica Ireland DSDP site 549 – Batten et al. (2014) Barremian Barremian hoheneggeri hoheneggeri Czech Republic Leipnik Wernsdor Reymanówna and Watson (1976); Carpentier (1937) Barremian hoheneggeri hoheneggeri Czech Republic, Murk Neutitschein; Reymanówna and Watson (1976); Carpentier Austria, Croatia Wernsdorf (1937) Barremian sp. sp. Germany Hildesheim Lower Saxony Lipps (1923); Carpentier (1937) early Barremian rubiesensis rubiesensis Spain La Cabroa Vilanova de Meià Barale (1973); Barale et al. (1984) early Barremian rubiesensis rubiesensis Spain La Pedrera de Meià Vilanova de Meià Gomez et al. (2002a) late early Barremian choshiensis choshiensis Japan Choshi Chiba Prefect., Honshu Kimura et al. (1985); Chow and Tsao (1977) late Barremian ugnaensis ugnaensis Spain Las Hoyas Cuenca Gomez et al. (2001, 2002a) late Barremian ugnaensis ugnaensis Spain Uña Cuenca Gomez et al. (2001, 2002a) early Aptian alata alata Spain Vallibona Morella Gomez et al. (2001); Aucour et al. (2008) Barremian-Aptian sp. sp. Czech Republic – – Carpentier (1937) late Aptian sp. sp. France Arnayon – Barale and Bréhéret (1995) late Aptian sp. sp. France Etoile – Barale and Bréhéret (1995) late Aptian sp. sp. France Ribeyret – Barale and Bréhéret (1995) late Aptian-early antunesii antunesii Portugal Carregueira mine Juncal Mendes and Kvaček (2022) Albian late Aptian cusanensis profetiensis Italy Peschera Cusano Mutri Bartiromo et al. (2012); Barral et al. (2019) early-middle Aptian profetiensis profetiensis Italy Profeti Campania Bartiromo et al. (2009) late Aptian to early sp. sp. Portugal Almas do Juncal Montemor-o-Velho Pais and Trincão (1983); Dinis (2001) Albian late Aptian sp sp Brazil Nova Olinda Araripe Basin Kunzmann et al. (2006) late Aptian - Albian ramosissima ramosissima USA Fredericksburg Virginia Berry (1910); Watson (1977); Upchurch and Doyle (1981) late Aptian - Albian ramosissima ramosissima USA Baltimore Maryland Upchurch and Doyle (1981) Aptian/Albian ramosissima ramosissima USA Hood County Texas Axsmith and Jacobs (2005) boundary late Aptian-middle sp. sp. Portugal Milheiro Cercal Teixeira (1948); Saporta and Choffat (1894) Albian late Albian sp. sp. Portugal Aguda Azenhas do Mar Reymanówna and Watson (1976); Hasenboehler (1981) Aptian-Albian occidentalis occidentalis Portugal Almargem Belas Heer (1881); Saporta and Choffat (1894); Rey (1972); Alvin (1977); Watson (1988); Watson and Alvin (1999), Mendes et al. (2010) early-middle Albian sp. sp. Portugal Cavadinha Caranguejeira Teixeira (1948); Dinis (2001) early Albian sp. sp. Portugal Ceramic factory Nazaré Teixeira (1948); Dinis (2001) early-middle Albian sp. sp. Portugal Pimenteira Caranguejeira Teixeira (1948); Dinis (2001) late Albian alata alata Portugal Sítio Nazaré Alvin (1977); Dinis (2001) early Albian sp. sp. Portugal Tavarede Teixeira (1948); Dinis (2001) Albian sp. sp. Spain La Cierva Cuenca Álvarez-Ramis (1981) early-middle sp. Spain Llosa del Bisbe Valencia Pla et al. (2008) Albian? early-middle Albian turolensis turolensis Spain Rubielos de Mora Rubielos de Mora Gomez et al. (2002a) middle-early late justae justae Spain San Just Teruel Barral et al. (2019) Albian (continued on next page) 3 J. Marmi et al. Evolving Earth 1 (2023) 100017 Table 1 (continued ) Age Species Taxonomy Country Locality Area/Region Reference revisited late Albian- early sp. sp. Portugal Bairro Alcanede Teixeira (1948) Cenomanian Cenomanian sp. sp. Czech Republic Bohdánkov Bohemia Velenovský and Viniklář (1926); Kvaček (2000) Cenomanian alata sp. Czech Republic Brickkiln Hloubètin, Praha Hluštík and Konzalova (1976b) Cenomanian? sp. sp. Czech Republic Drázdany Moravia Kvaček (2000) Cenomanian alata alata Czech Republic Kamenná Panna Horousany Kvaček (2000) clay pit Cenomanian harrisii harrisii Tajikistan Darvaz range Bokodara gorge Doludenko and Reymanówna (1978) early late alata alata Czech Republic Pecinov quarry Praha, near Rynholec Uličný et al. (1997); Kvaček (2000) Cenomanian early late alata alata Czech Republic Pecinov quarry Praha, near Rynholec Uličný et al. (1997); Kvaček (2000) Cenomanian Cenomanian sp. sp. Czech Republic Peruc – Velenovský and Viniklář (1926); Carpentier (1937) Middle Cenomanian sp. sp. France Brouillard quarry Maine-et-Loire, Anjou Broutin and Pons (1975), Pons (1979) (Ecoufland) early Cenomanian sp. sp. France Charras Charentes Koeniguer (1981) early Cenomanian sp. sp. France Île d’Oléron Charente-Maritime Koeniguer (1981) early Cenomanian sp. sp. France La Revardière Charentes Koeniguer (1981) Cenomanian sp. sp. France Monts-sur-Guesnes Vienne Lecointre and Carpentier (1938) latest Albian-earliest alata sp. France Font-Benon Quarry Archingeay and Aucour et al. (2008) Cenomanian Renardières, Charente- Maritime early Cenomanian sp. sp. France Rochefort Charente-Maritime Koeniguer (1981) early Cenomanian sp. sp. France St. Clément Charentes Koeniguer (1981) late Cenomanian sp. sp. Italy Colle di Monfalcone, Gorizia Tentor and Tentor (2007) Moschenizza late Cenomanian sp. sp. Portugal Campolide Alcântara Saporta and Choffat (1894); Teixeira (1948) middle Cenomanian occidentalis sp. Portugal Caranguejeira Leiria Choffat (1900); Crosaz-Galletti (1979); Callapez (1998) middle Cenomanian occidentalis sp. Portugal Monsanto Lisboa Saporta and Choffat (1894); Teixeira (1948); Berthou (1973) middle Cenomanian sp. sp. Portugal Murganhal Caxias Teixeira (1948); Berthou (1973) late Cenomanian sp. sp. Portugal Padrão Leiria Teixeira (1948); Callapez (1998) late Cenomanian sp. sp. Portugal Ratão Alcântara Saporta and Choffat (1894); Teixeira (1948) late Cenomanian sp. sp. Portugal Vila Flor Miranda do Corvo Teixeira (1948); Cunha (1992) Cenomanian? sp. sp. Spain – Guadalix de la Sierra Álvarez-Ramis (1981); Almendros et al. (1982) Cenomanian- sp. sp. Spain Cerro de la Mesa Guadalix de la Sierra Álvarez-Ramis (1981); Almendros et al. (1998) Turonian quarry middle-late sp. sp. Spain Fuentelespino de Cuenca Álvarez-Ramis (1981) Cenomanian Haro Cenomanian- sp. sp. Spain Villadiego Burgos Álvarez-Ramis (1981) Campanian Cenomanian/ veneta veneta Italy Bonarelli Belluno Gomez et al. (2002b) Turonian? Cenomanian/ sp. sp. Italy Ca’ Trenta di Schio Vicenza Pigozzo (2001); Gomez et al. (2002b) Turonian Cenomanian/ alata sp. Italy Carcoselle Possagno, Treviso Bizzarini and Coccioni (1990); Pigozzo (2002); Turonian Gomez et al. (2002b) Turonian sp. sp. Portugal Vila Verde Tentúgal Soares (1966); Callapez (1998) Turonian-Coniacian aff. alata sp. Czech Republic Dymokury Nymburk, Bohemia Hluštík (1974) Coniacian occidentalis sp. Portugal Verba Vagos Saporta and Choffat (1894) Coniacian- königii sp. Italy Vernasso Cividale and San Pietro Bozzi (1891); Gomez et al. (2002b) Santonian de Natisone, Udine Coniacian- sp. sp. Germany – Westphalia Hosius and von der Marck (1880); Carpentier Campanian (1937) Coniacian- sp. sp. Spain Chotacabras Torrelaguna Barale et al. (1988); Álvarez-Ramis et al. (1987) Campanian quarry Santonian to early sp. sp. Portugal Vale de Madeira Poiares Alvin (1977); Cunha and Reis (1995) Campanian early Campanian- occidentalis sp. Portugal Casal dos Alhadas Lima (1900); Antunes and Pais (1978); Antunes Maastrichtian Bernardos and de Broin (1988); Cunha and Reis (1995) early Campanian- sp. sp. Portugal Taveiro Coimbra Antunes and Pais (1978); Antunes and de Broin Maastrichtian (1988); Cunha and Reis (1995) Campanian- sp. sp. Spain Fumanya Sud Vallcebre Riera et al. (2010), Villalba-Breva et al. (2012) Maastrichtian boundary Campanian- sp. sp. Spain Mina Esquirol Vallcebre Riera et al. (2010) Maastrichtian boundary Maastrichtian aff. sp. Portugal Aradas Aveiro Teixeira (1948); Bernardes and Corrochano occidentalis (1987); Antunes and de Broin (1988) Maastrichtian occidentalis sp. Portugal Mataduços Aveiro Choffat (1900); Bernardes and Corrochano (1987); Moron (1981) (continued on next page) 4 J. Marmi et al. Evolving Earth 1 (2023) 100017 Table 1 (continued ) Age Species Taxonomy Country Locality Area/Region Reference revisited Maastrichtian oligostomata oligostomata Portugal Olho de Agua, Aveiro, Beira Littorale Romariz (1946); Broutin and Pons (1975); Alvin Esgueira (1977); Lauverjat and Pons (1978); Bocherens et al. (1994) Maastrichtian oligostomata oligostomata Spain Torrelaguna Madrid Álvarez-Ramis (1981); Álvarez -Ramis et al. (1987) Maastrichtian sp. sp. Spain Pla de la Barranca Vallcebre Riera et al. (2010) Maastrichtian sp. sp. Spain St. Corneli Vallcebre Riera et al. (2010) Maastrichtian sp. sp. Spain Isona Isona Marmi et al. (2014) Figueira da Foz. extinction rates were estimated from stratigraphic ranges of 18 species species, F. malaiana Kon’no, was described in this interval, precisely in of Frenelopsis based on the methods described by Foote (2000). Origi­ the Berriasian-Valanginian of western Malaysia (Smiley, 1970). The nation and extinction rates were calculated from the van Valen metrics data available suggest that, from its origin, genus Frenelopsis was prob­ (van Valen, 1984; Foote, 2000). In order to perform these estimations, ably widespread, at least in a tropical to paratropical belt between the specimens have been grouped in time-homogeneous intervals (ca. 0◦ and 40◦ N ranging from the Tethyan archipelago to present south­ 14 Ma duration). eastern Asia (Figs. 2 and 3A). 4. Diversification and distribution of Frenelopsis in space and 4.2. Barremian–Aptian time During this time interval, new species appeared in the Tethyan ar­ 4.1. Berriasian–Hauterivian chipelago, such as F. atlantica Batten et al. in Ireland, F. rubiesensis Barale, F. ugnaensis Gomez et al. and F. antunesi Mendes et Kvaček in Frenelopsis sp. remains have been reported from many European lo­ Iberia and F. profetiensis Bartiromo in exposed areas from the Apennine calities, including Poland, Czech Republic, Germany, France, and platform (Figs. 1, 2A and 3A; Table 1). In addition, F. hoheneggeri spread Portugal (Table 1). However, three species of Frenelopsis have been and colonised other areas of the archipelago (Figs. 2B–C, 3A, Table 1) formally described from Berriasian to Hauterivian times in Europe such as present-day Croatia, Austria and the Czech Republic (Rey­ (Figs. 1, 2A and 3A, Table 1). F. occidentalis is the oldest species and it manówna and Watson, 1976; Carpentier, 1937). More occurrences were has been documented from the Berriasian of Germany (Watson and reported as Frenelopsis sp. from some islands of the archipelago, such as Alvin, 1999). F. teixeirae occurred from the Valanginian to Hauterivian Iberia and France (Fig. 2B–C, 3A). In Asia, F. choshiensis Kimura et al. of Portugal (Alvin and Pais, 1978; Mendes et al., 2010) and was restricted in Japan (Chow and Tsao, 1977; Kimura et al., 1985), F. hoheneggeri occurred in the Hauterivian of Poland (Reymanówna, while F. ramosissima Fontaine has been reported in the late Aptian of 1965). In Africa, Frenelopsis sifloana is known from an unprecise stage in North America and lasted until early Albian (e.g., Upchurch and Doyle, the Early Cretaceous of Sudan (Watson and Alvin, 1976; Watson, 1983). 1981). Some of the species of the Tethyan archipelago (e.g., F. atlantica Here it has been provisionally included in this interval. In Asia, only one and F. ugnaensis) as well as the Asian F. choschiensis were likely endemic Fig. 1. Chronostratigraphic ranges of Frenelopsis species. The dashed line represents imprecise chronostratigraphic attribution within the range. 5 J. Marmi et al. Evolving Earth 1 (2023) 100017 Fig. 2. Biogeography of Frenelopsis from the Berriasian to the Aptian plotted on global Early Cretaceous palaeogeographic maps. The dashed line represents the track line of Frenelopsis distribution. Palaeogeographic maps modified from https://deeptimemaps.com. 6 J. Marmi et al. Evolving Earth 1 (2023) 100017 Fig. 3. Biogeographic distribution of Frenelopsis species in the Tethyan archipelago during the Cretaceous. In white Frenelopsis sp. occurrences, in orange Frenelopsis occurrences identified at the species level. Palaeogeographic maps modified from https://deeptimemaps.com. and short-lived (Fig. 1). Available data (Fig. 2B–C, 3A, Table 1) suggest 4.4. Turonian− Santonian that the Tethyan archipelago was the area where Frenelopsis was more widespread during the Barremian–Aptian. During this time interval, a decrease in species richness occurred. The Friuli platform was still inhabited by F. veneta, which went extinct at 4.3. Albian− Cenomanian the end of the Turonian (Gomez et al., 2002b). Other species, such as F. alata disappeared before the early Turonian. The number of occur­ During this time interval, the Frenelopsis species richness decreased. rences of Frenelopsis sp. continued to be important in the Tethyan ar­ However, new but short-lived species appeared in particular islands of chipelago (Portugal, Spain, Italy, Czech Republic, Germany) but the Tethyan archipelago, where they were likely endemic. This is the diminished in comparison to previous periods (Figs. 3, 4B and 6A; case for the Albian F. turolensis and F. justae in eastern Iberia and the Table 1). Cenomanian F. veneta Gomez et al. in emerged lands of the Friuli plat­ form (Fig. 3B− C). In contrast, F. alata, which appeared in the previous 4.5. Campanian− Maastrichtian interval, increased its biogeographic range to several islands of the ar­ chipelago, from western Iberia to the Bohemian Basin. During the Near the end of the Cretaceous, the new species F. oligostomata arose Albian, another long-lived species, F. occidentalis, appeared in western in western Iberia, where it inhabited coastal wetlands (Figs. 1, 3C− D, 4C Iberia (Portugal) and lasted until the Cenomanian. In Asia, F. harrisii and 5) (Mendes et al., 2010). Additionally, Frenelopsis sp. was very Doludenko and Reymanówna occurred in the Tajikistan (Doludenko and abundant in freshwater coastal habitats from northeastern Iberia (pre­ Reymanówna, 1978) (Figs. 1 and 4B). In North America F. ramosissima sent-day South Pyrenees, Catalonia), where until the end of the early persisted. The analysis of occurrences indicates that, during Albian and Maastrichtian it constituted a peat-forming plant, the peat turning after Cenomanian, Frenelopsis was again abundant and widespread in the diagenesis into thick lignite deposits of the so called “Grey Unit” from Tethyan archipelago (Fig. 3B and C; Table 1), especially in a paratropical the Tremp Formation (Villalba-Breva et al., 2012). The latest occur­ belt, between 25◦ and 40◦ northern palaeolatitudes (Fig. 3B–C). rences of Frenelopsis suggest that it was only restricted to the Iber­ oarmorican domain (Figs. 3D and 5), a large island composed of 7 J. Marmi et al. Evolving Earth 1 (2023) 100017 Fig. 4. Biogeography of Frenelopsis from Albian to Campanian, plotted on global Late Cretaceous palaeogeographic maps. The dashed line represents the track line of Frenelopsis biogeographic distribution. Palaeogeographic maps modified from https://deeptimemaps.com. 8 J. Marmi et al. Evolving Earth 1 (2023) 100017 origins, at the beginning of the Cretaceous. Frenelopsis diversified throughout the Early Cretaceous, as suggested by the number of occurrences, the number of species per unit of time and the mean standing diversity (Fig. 6A− C). However, it is noteworthy that the origination rate decreased between the Berriasian and Aptian and, especially, between the Albian and Santonian (Fig. 6D). From the Aptian interval onwards, the extinction rate exceeded the origination rate (Fig. 6D). The biogeographic range of Frenelopsis began to decrease during the Albian–Cenomanian, and during the Late Cretaceous it was confined to the Tethyan archipelago (Figs. 3B− C and 4A− C). All these results support the hypothesis that the decline of Frenelopsis could have already started during the late Early Cretaceous, coinciding with the rise to dominance of angiosperms and the expansion of megathermal forests from low to middle latitudes, which was driven by the mid-Cretaceous increase in global temperatures (Coiffard and Gomez, 2012; Coiffard Fig. 5. Biogeography of Frenelopsis during the Maastrichtian, plotted on a et al., 2012). It is well documented that flowering plants colonised worldwide palaeogeographic map at 80 Ma. The dashed line represents the habitats in which Frenelopsis was previously dominant such as coastal track line of Frenelopsis biogeographic distribution. Palaeogeographic maps wetlands, floodplains and freshwater swamps during the modified from https://deeptimemaps.com. Albian− Cenomanian (Gomez et al., 2001, 2002a, 2004; Coiffard et al., 2006; Barral et al., 2016). Notwithstanding, during the Maastrichtian, at emerged lands of Iberia and parts of France that was located in the the end of its evolutionary history, Frenelopsis still formed important western edge of the southern Tethyan archipelago. vegetations in coastal wetlands of Iberia, successfully competing with angiosperms, such as palms and monocot reeds (Villalba-Breva et al., 5. Discussion 2012; Marmi et al., 2016). 5.1. Origins, diversification and decline of the genus Frenelopsis 5.2. The role of the Tethyan archipelago in Frenelopsis biogeography Eighteen species of Frenelopsis have been analysed based on mega At least half of the known species of Frenelopsis inhabited the Tethyan and micromorphological features of vegetative parts (Table 1, Fig. 1). archipelago (Fig. 1− 5, Table 1). Eustatic fluctuations, which charac­ The earliest records are from the Berriasian of Germany (Watson and terised most of the Cretaceous, probably promoted first the isolation and Alvin, 1999) and Berriasian-Valanginian of Malaysia (Smiley, 1970; later the spread of Frenelopsis populations in this area, enhancing allo­ Uyop and Che Aziz, 2000). Frenelopsis could also be present in Africa patric speciation mechanisms. Some species, such as F. teixeirae, (Sudan) but a detailed chronostratigraphic study is necessary to confirm F. justae, F. turolensis, F. ugnaensis, F. occidentalis and F. oligostomata this occurrence (Watson and Alvin, 1976; Watson, 1983). The present appear to have been endemic of Iberia (Fig. 3, Table 1). Other species, dataset suggests that Frenelopsis was already widely distributed from its such as F. profetiensis and F. veneta were likely restricted to small, Fig. 6. Abundance and diversity of Frenelopsis during the Cretaceous. A: Total number of occurrences per time intervals (stages). B: Total number of species per time interval. C: Diversity curve. D: Curves of origination and extinction rates. 9 J. Marmi et al. Evolving Earth 1 (2023) 100017 emerged areas in the Apennine and Friuli platforms (Gomez et al., Tremp Basin (Médus, 1970, 1972; Fernández-Marrón, 2009; Villal­ 2002b; Bartiromo et al., 2009, 2012). This suggests that Iberia and other ba-Breva et al., 2012). The only locality where Classopollis was islands from the Apennine and Friuli platforms could be important areas mentioned as an extremely rare element of the palynological assemblage for Frenelopsis speciation, favouring endemism and the divergence of was Barranc La Posa in the Tremp Basin (de Porta et al., 1985). To short-lived species during most of the Cretaceous (Fig. 3). By contrast, explain the absence of Classopollis in latest Cretaceous pollen assem­ other species had wider geographic ranges. This is the case of F. alata blages and the mismatch with rich Frenelopsis megafossil assemblages of that spread from Iberia to the Bohemian and Friuli lands (Fig. 3). The the same outcrops, Friis et al. (2011) and Villalba-Breva et al. (2012) biogeographic range of other species, such as F. hoheneggeri, is more suggested taphonomic biases or low production of Classopollis pollen by difficult to interpret since many occurrences of this species lack suffi­ the source plants. However, taphonomic bias is a rather improbable cient cuticular data to be confirmed (Table 1). situation to explain the absence of pollen in coastal wetlands, where All these data suggest that Frenelopsis was conspicuous in Iberia transport through tractive currents was reduced and other types of during the whole Cretaceous (Fig. 3). It seems clear that this palaeo- transport, such as floatation, could hardly make the abundant and island played an important role in the radiation of the genus and pro­ thick-walled Classopollis pollen grain completely disappear from the vided refugia for these conifers during their Late Cretaceous decline, palynofloras. Thus, the second hypothesis gains probability. Frenelopsis until holding its last representatives in the Maastrichtian. relictual populations of Iberia might have been affected by low pollen production or even male sterility, being these factors the coup de grace that led to extinction. In fact, high number of Classopollis pollen tetrads 5.3. Hypotheses on the extinction of Frenelopsis with abortive or malformed individual pollen grains have been recog­ nized from uppermost Triassic to Lower Cretaceous deposits (e.g., The long-lasting evolutionary success of Frenelopsis throughout the Stuckins, 2022; Galasso et al., 2023). For instance, in the middle Jurassic Cretaceous in Europe was promoted by their ecological plasticity, high deposits from Neuquén Basin (Argentina), the malformations of Class­ adaptability to environmentally constraints as well as strong competi­ opollis grains are significantly high i.e., 2.8–8.4% in tetrads and tiveness, having negative feedback on the richness and abundance of 30.9–57.7% of individual grains (Jin et al., 2020; Stuckins, 2022). The other taxa living in the same habitats (Gomez et al., 2002a; Barral et al., production of aborted pollen grains from Classopollis increases in 2016). It appears that the diversification and rise to dominance of an­ particular time intervals during the Early Cretaceous (Kürschner et al., giosperms in low and middle latitudes could have played an important 2013; Galasso et al., 2023). role in the decline of Frenelopsis during the Late Cretaceous. However, Male sterility has been suggested as a possible cause for the decline of even the last known Frenelopsis were still competing successfully with some extant conifer species. For instance, unreduced and abortive pollen certain angiosperms, such as palms, in freshwater coastal swamps of grains are thought to have led to the endangered Mediterranean cypress, Iberia (Villalba-Breva et al., 2012), before becoming extinct during the Cupressus dupreziana A. Camus, to natural extinction (Pichot and Maastrichtian. Another genus within the Cheirolepidiaceae crossed the Maâtaoui, 2000; Maâtaoui and Pichot, 2001). Similarly, the decline of Cretaceous/Paleogene boundary, and survivors of this family still played Taiwanese populations of the Cupressaceae Taiwania cryptomerioides a significant role in Paleocene plant communities of southernmost South Hayata are attributed to male sterility (Chen et al., 2006). More pre­ America (Barreda et al., 2012). cisely, the latter authors explained that in T. cryptomerioides sterile mi­ One may wonder why this did not happen for Frenelopsis. Evidence crospores remained as tetrads due to the absence of callose in the tetrad could come from the Maastrichtian of northeastern Iberia, where Fre­ cross walls. nelopsis leafy axes are very abundant and the accumulation of these re­ In order to test the hypothesis of extinction through male sterility in mains formed the peat precursory of large amounts of lignite in the Frenelopsis it is necessary to increase the search for fossil Classopollis in Tremp and Vallcebre basins, Catalonia (Villalba-Breva et al., 2012). the Maastrichtian of Iberia and document if pollen malformations, such Among the latest known records of Frenelopsis from Iberia are those as tetrads with abortive grains, or other morphologically recognizable reported from the lower Maastrichtian of Fumanya and Mina Esquirol, in teratologies occur. the Vallcebre Basin (Villalba-Breva et al., 2012) (Fig. 7) and the middle Maastrichtian of Isona, in the Tremp basin (Marmi et al., 2014). How­ 6. Conclusions ever, while some Early Cretaceous palynofloras from Iberia reached up to 80− 90% of Classopollis (Solé de Porta et al., 1994; Gomez et al., The compilation of over a century of taxonomic, biogeochemical and 2001), these characteristic pollen grains were almost absent in the palaeoecological studies about the extinct conifer Frenelopsis allows us to Iberian Maastrichtian, e.g., Vallcebre Basin, Coll de Nargó Basin and Fig. 7. Vegetative remains of Frenelopsis sp. from the Maastrichtian of Mina Esquirol (Catalan Pyrenees, Spain). A: Abundant Frenelopsis vegetative shoots almost covering completely the base of a coal seam (only a few cuticles are preserved). B: Detail of internode showing one free tip of leaf folded down. C: SEM picture of cuticle showing two rows of stomata aligned (arrows) and detail of a stomatal apparatus (insert) showing rim around sunken stomata. Papillae are not preserved, which renders it difficult determination at the species level. 10 J. Marmi et al. Evolving Earth 1 (2023) 100017 reconstruct its evolution in terms of diversity and species richness, Alvin, K.L., 1977. The conifers Frenelopsis and manica in the cretaceous of Portugal. Palaeontology 20, 387–404. biogeographic history and to infer about the causes of its extinction. Alvin, K.L., 1982. Cheirolepidiaceae: biology, structure and palaeoecology. Rev. The oldest record of Frenelopsis dates back to Berriasian. From the Palaeobot. Palynol. 37, 71–98. beginning of its history (Berriasian− Hauterivian), Frenelopsis was well Alvin, K.L., Pais, J.C., 1978. A Frenelopsis with opposite decussate leaves from the Lower distributed in the Tethyan archipelago and soon extended to Asia in the Cretaceous of Portugal. Palaeontology 21, 873–879. Antunes, M.T., de Broin, F., 1988. Le Crétacé terminal de Beira Litoral, Portugal: paratropical climatic belt of the Northern Hemisphere. In the Aptian it remarques stratigraphiques et écologiques, étude complémentaire de Rosasia soutoi reached North and South America, while the stage when Frenelopsis (Chelonii, Bothremydidae). Cien. Terra 9, 153–200. colonized Africa remains to be documented with more precision. Until Antunes, M.T., Pais, J., 1978. Notas sobre os depósitos de Taveiro. Estratigrafia, paleontologia, idade, paleoecologia. Cien. Terra 4, 109–128. the Aptian the species richness and standing diversity of Frenelopsis Aucour, A.M., Gomez, B., Sheppard, S., Thévenard, F., 2008. δ13C and stomatal number increased, while the maximum number of occurrences is reported from variability in the Cretaceous conifer Frenelopsis. Palaeogeogr. Palaeoclimatol. Albian-Cenomanian times. The Tethyan archipelago was the area with Palaeoecol. 257, 462–473. Axsmith, B.J., Jacobs, B.F., 2005. The conifer Frenelopsis ramosissima (Cheirolepidiaceae) more species and occurrences. Particularly Iberia was the one of the in the Lower Cretaceous of Texas: systematic, biogeographical, and Paleoecological most important diversity hotspots and hold many endemic species, such implications. Int. J. Plant Sci. 166, 327–337. as F. teixeirae, F. ugnaensis, F. justae or F. turolensis. Azéma, C., Fauconier, D., Viaud, J.M., 1981. Microfossils from the upper cretaceous of Vendée (France). Rev. Palaeobot. Palynol. 35, 237–281. After the Cenomanian the species richness and the number of oc­ Barale, G., 1973. Contribution à l’étude de la flore des calcaires lithographiques de la currences of Frenelopsis drastically diminished and its biogeographic province de Lérida (Espagne): Frenelopsis rubiesensis nov. sp. Rev. Palaeobot. Palynol. range became constrained to the Tethyan archipelago. This trend 16, 271–287. Barale, G., Blanc-Louvel, C., Buffetaut, E., Courtinat, B., Peybernes, B., Boada, L., exacerbated in the Maastrichtian, when Frenelopsis only survived relict Wenz, S., 1984. Les gisements de calcaires lithographiques du Crétacé inferieur du in the Iberian paleoisland. The last occurrence in coastal wetlands of the Montsech (Province de Lerida, Espagne) considérations paléoécologiques. Geobios 8, middle Maastrichtian of the Tremp Basin (Catalan Pyrenees) may be 275–283 (Mémoire Spéciale). considered a refuge for this genus. Populations were significant enough Barale, G., Bréhéret, J.G., 1995. Découverte de Cheirolepidiaceae dans l’Aptien des marnes bleues de la zone vocontienne (SE de la France). Comptes Rendus des to constitute the main peat-forming plant from the Pyrenean Maas­ Academie des Sciences Paris, série IIa 321, 433–439. trichtian coal, exploited in gallery and opencast mines until the past Barale, G., Fernández-Marrón, T., Álvarez-Ramis, C., 1988. Etude de cônes mâles de century, while its pollen (Classopollis) was almost absent. This suggests Frenelopsis Schenk emend. Reymanόwna & Watson 1976 (Cheirolepidiaceae) du Crétacé supérieur de Torrelaguna (Province de Madrid, Espagne). Geobios 21, that male sterility could have been one of the main causes of its 187–199. extinction before the K/Pg boundary, while another closely related Barral, A., Gomez, B., Zorrilla, J.M., Serrano, J.M., Yans, J., Cazedebat, M., Daviero- genus survived this boundary shortly in South America. Future paly­ Gomez, V., Ewin, T.A.M., Lécuyer, C., 2016. Local-scale analysis of plant community from Early Cretaceous riparian ecosystems of Hautrage, Belgium. Palaeogeogr. nological studies about the importance of malformations and frequency Palaeoclimatol. Palaeoecol. 443, 107–122. of abortive pollen grains of Classopollis in the last populations of Frene­ Barral, A., Gomez, B., Daviero-Gomez, V., Lécuyer, C., Mendes, M.M., Ewin, T.A.M., lopsis could help to test this hypothesis. 2019. New insights into the morphology and taxonomy of the Cretaceous conifer Frenelopsis based on a new species from the Albian of San Just, Teruel, Spain. Cretac. Res. 95, 21–36. Barreda, V.D., Cúneo, N.R., Wilf, P., Currano, E.D., Scasso, R.A., Brinkhuis, H., 2012. Declaration of competing interest Cretaceous/Paleogene floral turnover in Patagonia: drop in diversity, low extinction, and a Classopollis spike. PLoS One 7, e52455. Bartiromo, A., Barale, G., Barone Lumaga, M.R., Bravi, S., Barattolo, F., 2009. The early The authors declare that they have no known competing financial cretaceous flora from profeti, caserta, southern Italy. Rev. Palaeobot. Palynol. 158, interests or personal relationships that could have appeared to influence 101–116. the work reported in this paper. Bartiromo, A., Barale, G., Barone-Lumaga, M.R., Bravi, S., Barattolo, F., 2012. An early cretaceous flora from cusano mutri, benevento, southern Italy. Cretac. Res. 33, 116–134. Data availability Batten, D.J., Zhou, Z.-Y., Li, W.-B., 2014. Plant remains from early cretaceous deposits on the goban spur, bay of biscay, north atlantic ocean, and their palaeoenvironmental significance. Palaeoworld 23, 162–186. Data will be made available on request. Bernardes, C.A., Corrochano, A., 1987. A sedimentologia da "Formação arenitos e argilas de Aveiro" ‒ Cretácico Superior, Bacia Ocidental Portuguesa. Geociencias 2, 9–26. Berthou, P.Y., 1973. Le Cénomanien de l’Estremadure portugais. Memorias dos Serv. Acknowledgements Geol. Port. 23, 169. Berry, E.W., 1910. The epidermal characters of Frenelopsis ramosissima. Bot. Gaz. 50, Bernard Gomez (Univ. 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