|Restoration of a member of Williamsoniaceae by Thérèse Ekblom|
|Life restoration of "Williamsonia" sewardiana from the Early Cretaceous of India, which may represent an early member of Cycadeoidaceae|
Bennettitales (also known as cycadeoids) is an extinct order of seed plants that first appeared in the Permian period and became extinct in most areas toward the end of the Cretaceous. Bennettitales are among the most common Mesozoic seed plants, and had morphologies including shrub and cycad-like forms. The foliage of bennettitaleans is superficially nearly indistinguishable from that of cycads, but they are distinguished from cycads by their more complex flower-like reproductive organs, at least some of which were likely pollinated by insects.
Although certainly gymnosperms (cone-bearing seed plants), the relationships of bennettitaleans to other seed plants is debated. Their general resemblance to cycads is contradicted by numerous more subtle features of their reproductive systems and leaf structure. Some authors have linked bennettitaleans to angiosperms (flowering plants) and gnetophytes (a rare and unusual group of modern gymnosperms), forming a broader group known as Anthophyta. Molecular data contradicts this, with gnetophytes found to be much more genetically similar to conifers. Their exact position of Bennettitales remains uncertain.
Bennettitales are divided into two families, Cycadeoidaceae and Williamsoniaceae, which have distinct growth habits. Cycadeoidaceae had stout, cycad-like trunks with bisporangiate (containing both megaspores and microspores) strobili (cones) serving as their reproductive structures. Williamsoniaceae either had bisporangiate or monosporangiate cones, and distinctly slender and branching woody trunks. The Williamsoniaceae grew as woody shrubs with a divaricate branching habit, similar to that of Banksia. It has been suggested that Williamsoniaceae are a paraphyletic (not containing all descendants of a common ancestor) assemblage of all Bennettitales that do not belong to the Cycadeoidaceae.
In general, bennettitalean leaves are attached to the stem with a helical (corkscrew) arrangement. Some leaves (most species of Nilssoniopteris, etc.) are narrow, solitary blades with a smooth-edged ("entire") margin. Most leaf morphotypes (Pterophyllum, Ptilophyllum, Zamites, Otozamites, etc.) are pinnate (feather-shaped), with many small leaf segments attached to a central shaft. Others (Anomozamites, a few species of Nilssoniopteris) are incompletely pinnate (sawtooth-shaped) and transitional between these two end members. One unusual leaf form, Eoginkgoites, even approaches a palmate appearance similar to early species of Ginkgo.
The foliage of bennettitaleans resembles that of cycads to such an extent that the foliage of the two groups cannot be reliably distinguished based on gross morphology alone. However, fossil foliage which preserves the cuticle can be assigned to either group with confidence. The stomata of bennettitaleans are described as syndetocheilic. This means that the main paired guard cells develop from the same mother cells as the subsidiary cells which surround them. This contrasts with the haplocheilic stomata of cycads and conifers. In haplocheilic stomata, the ring of subsidiary cells are not derived from the same original structures as the guard cells. This fundamental difference is the main way to differentiate bennettitalean and cycad foliage.
Cones and seeds
Like other gymnosperms, bennettitalean reproductive inflorescences come in the form of cones, which produce pollen and ovules (unfertilized seeds). The cones have a thick central receptacle surrounded by simple, helically-arranged fertile and infertile structures. Tissue at the base of the cone forms layers of scale-like or petal-like bracts to protect the radiating inner structures. Some authors refer to bennettitalean cones as “flowers”, though they are not equivalent to true angiosperm flowers. Pollen is often enclosed in paired synangia (pollen sacs). The synangia lie on the adaxial (inner) edge of pollen-bearing leaf-like structures known as microsporophylls. This contrasts with cycads, all of which lack discrete synangia and bear pollen on the abaxial (outer) surface of their microsporophylls.
Many bennettitaleans are bisporangiate, where the pollen and ovules are hosted on the same (bisexual or hermaphrodite) cone. Cavities filled with curved synangia-bearing microsporophylls are encased by thin radiating structures, including thick, infertile interseminal scales and fertile sporophylls with ovules at their tips. The presence of ovules at the tips of sporophylls, rather than the tips of stems, is a major difference between the cones of bennettitaleans and gnetophytes. As the cone is fertilized and matures, the microsporophylls wither away and the ovules transform into seeds.
Most bennettitaleans in the family Williamsoniaceae are instead monosporangiate, with separate pollen and ovule-producing (unisexual) cones on the same plant. The ovule-producing (female) cones (Williamsonia, etc.) are similar to mature bisporangiate cones, with interseminal scales and ovule-tipped sporophylls enclosed by bracts. Pollen-producing (male) cones (Weltrichia, etc.), on the other hand, feature an exposed crown of tapering microsporophylls with adaxial rows of synangia. The microsporophylls may host a single linear row of paired synangia, or instead synangia arranged in a pinnate (feather-shaped) pattern.
Seeds are dicotyledonous (possess two embryonic leaves), with a central embryo surrounded by three layers: the thin megagametophyte, the slightly thicker nucellus, and the protective integument. The upper tip of the seed is tapered and opens through a thin and often extended micropyle. A long, narrow micropyle extending out of the seed is superficially similar to the condition in living gnetophytes. Once the seed is fertilized, the micropyle is sealed by a plug-shaped extension of the nucellus. Unlike living gymnosperms, the tip of the nucellus lacks a pollen chamber (receptacle for stored pollen). The integument is dense and thick, with many layers of differentiated cells. This contrasts with the thin, biseriate (two cell-layer) integument of gnetophytes. Bennettitaleans also lack another gnetophyte-like trait: a sheath of fused bracteoles enveloping the seed. Most integument cells are not unusual in size or shape. However, near the micropyle the innermost layer of integument cells become radially-oriented and elongated, partially closing in on the micropyle. The nucellus and integument are unfused above the chalaza (base of the seed), unlike cycads or gnetophytes, where the layers are fused for much of their height.
Cycadeoidaceans were likely self-pollinating, with their stems and cones buried underground. The flower-like williamsoniacean male reproductive structure Weltrichia is associated with the female reproductive structure Williamsonia, though it is uncertain whether the parent plants were monoecious (male and female reproductive structures being present on the same plant) or dioecious (where each plant has only one gender of reproductive organ). Weltrichia was likely primarily wind-pollinated, with some species possibly pollinated by beetles. Several groups of Jurassic and Early Cretaceous insects possessed a long proboscis, and it has been suggested that they fed on nectar produced by bennettitalean reproductive structures, such as the bisexual williamsoniacean reproductive structure Williamsoniella, which had a long, narrow central receptacle which was likely otherwise inaccessible. Early Cretaceous bennettitalean pollen has been found directly associated with a proboscis bearing fly belonging to the extinct family Zhangsolvidae, providing evidence that this family acted as pollinators for the group.
The Cycadeoideaceae (originally “Cycadeoideae”) were named by English geologist William Buckland in 1828, from fossil trunks found in Jurassic strata on the Isle of Portland, England, which Buckland gave the genus name Cycadeoidea. Buckland provided a description of the family and two species, but failed to give a description of the genus, which has led to Buckland's description of the family being considered invalid by modern taxonomic standards. In publications in 1870, Scottish botanist William Carruthers and English paleobotanist William Crawford Williamson described the first known reproductive organs of the Bennettitales from Jurassic strata of Yorkshire and Jurassic-Cretaceous strata of the Isle of Wight and the Isle of Portland. Caruthers was the first to recognise that Bennettitales had distinct differences from cycads, and established the tribes "Williamsonieae" and "Bennettiteae", with the latter being named after the genus Bennettites named by Caruthers in the same publication, the name being in honour of British botanist John Joseph Bennett. The order Bennettitales was erected by German botanist Adolf Engler in 1892, who recognised the group as separate from the Cycadales. The Anthophyte hypothesis erected by Arber and Parking in 1907 posited that angiosperms arose from Bennettitales, as suggested by the wood-like structures and rudimentary flowers. Based on morphological data, however, Bennettitales were classified as a monophyletic group when paired with Gnetales. a study in 2006 suggested that Bennettitales, Angiosperms, and Gigantopteridales form a clade based on the presence of oleanane. A 2007 study examining phase-contrast X-ray images of gymnosperm seeds supported the Anthophyte hypothesis. Evidence from seed coats suggest that Bennettitales form a clade with the gymnosperm orders of Gnetales and Erdtmanithecales. Molecular evidence has consistently contradicted the Anthophyte hypothesis, finding that Angiosperms are the sister group to all living gymnosperms, including Gnetales. A 2017 phylogeny based on molecular signatures of fossilised cuticles found that Bennettitales were more closely related to the Ginkgo+Cycads clade than conifers, and were closely related to Nilssonia and Ptilozamites.
The oldest confirmed fossils of bennettitaleans are leaves of Nilssoniopteris shanxiensis, a species from the upper part of the Upper Shihhotse Formation in Shanxi Province, China. This strata is dated to the early Kungurian stage of the early Permian (Cisuralian), around 281 million years ago. Supposed Carboniferous-Permian records of Pterophyllum do not have conclusive bennettitalean affinities or have been reinterpreted as cycad foliage in the form genus Pseudoctenis. True Permian records of benettitalean leaves are rare; outside of the Shihhotse Formation they are only found in the Late Permian (likely Changhsingian)-age Umm Irna Formation in Jordan. This formation is notable for the early occurrence of other Mesozoic-style flora, including the earliest records of corystospermalean foliage (Dicroidium), podocarpacean conifer branches (Elatocladus), and Triassic-style zamiinean cycads.
The bennettitalean fossil record reappeared in the Middle Triassic, and williamsoniaceans became globally distributed by the end of the period. The oldest bennettitalean reproductive structures are small Williamsonia "flowers" from the Middle Triassic Esk Formation of Australia. While Williamsoniaceae had a global distribution, Cycadeoidaceae appear to have been primarily confined to the western parts of Laurasia, and are primarily known from the Cretaceous. Bennettitales were widespread and abundant during the Jurassic and Early Cretaceous, however Bennettitales severely declined during the Late Cretaceous, coincident with the rise of flowering plants, being mostly extinct by the end of the period, with the final known remains from the Northern Hemisphere being found in the polar latitude Kakanaut Formation in Chukotka, Russia, dating to the Maastrichtian, assignable to Pterophyllum. A possible late record has been reported from the early Oligocene of eastern Australia and Tasmania, assignable to the genus Ptilophyllum, but no cuticle was preserved, making the referral inconclusive.
Fossil leaf of Zamites mariposana from the Jurassic.
Restoration of Weltrichia magna from the Jurassic of Mexico
Leaf of Anomozamites
Trunk of Cycadeoidea
Fossil of Ptilophyllum grandifolium
- Arens NC, Stromberg C, Thompson A. "Introduction to the Bennettitales". University of California Museum of Paleontology. Retrieved 16 April 2018.
- Peñalver E, Arillo A, Pérez-de la Fuente R, Riccio ML, Delclòs X, Barrón E, Grimaldi DA (July 2015). "Long-Proboscid Flies as Pollinators of Cretaceous Gymnosperms". Current Biology. 25 (14): 1917–23. doi:10.1016/j.cub.2015.05.062. PMID 26166781.
- Rothwell, Gar W.; Crepet, William L.; Stockey, Ruth A. (2009). "Is the anthophyte hypothesis alive and well? New evidence from the reproductive structures of Bennettitales". American Journal of Botany. 96 (1): 296–322. doi:10.3732/ajb.0800209. ISSN 1537-2197. PMID 21628190.
- Pott, Christian; McLoughlin, Stephen (2014-06-01). "Divaricate growth habit in Williamsoniaceae (Bennettitales): unravelling the ecology of a key Mesozoic plant group". Palaeobiodiversity and Palaeoenvironments. 94 (2): 307–325. doi:10.1007/s12549-014-0157-9. ISSN 1867-1608. S2CID 84440045.
- Ray MM, Rothwell GW, Stockey RA (September 2014). "Anatomically Preserved Early Cretaceous Bennettitalean Leaves: Nilssoniopteris corrugata n. sp. from Vancouver Island, Canada". Journal of Paleontology. 88 (5): 1085–93. doi:10.1017/S002233600005767X. S2CID 232349931 – via ResearchGate.
- Pott, Christian; Axsmith, Brian J. (February 2015). "Williamsonia carolinensis sp. nov. and Associated Eoginkgoites Foliage from the Upper Triassic Pekin Formation, North Carolina: Implications for Early Evolution in the Williamsoniaceae (Bennettitales)". International Journal of Plant Sciences. 176 (2): 174–185. doi:10.1086/679471. ISSN 1058-5893. S2CID 44559347.
- Blomenkemper, Patrick; Bäumer, Robert; Backer, Malte; Abu Hamad, Abdalla; Wang, Jun; Kerp, Hans; Bomfleur, Benjamin (2021). "Bennettitalean Leaves From the Permian of Equatorial Pangea—The Early Radiation of an Iconic Mesozoic Gymnosperm Group". Frontiers in Earth Science. 9: 162. Bibcode:2021FrEaS...9..162B. doi:10.3389/feart.2021.652699. ISSN 2296-6463.
- Osborn JM, Taylor ML (2010). "Pollen and coprolite structure in Cycadeoidea (Bennettitales): implications for understanding pollination and mating systems in Mesozoic cycadeoids". Plants in deep Mesozoic time: morphological innovations, phylogeny, and ecosystems. Bloomington, IN: Indiana University Press. pp. 34–49. ISBN 978-0-253-00199-3.
- Popa, Mihai Emilian (2019-02-27). "Review of the bennettitalean genus Weltrichia". Journal of Palaeogeography. 8 (1): 12. doi:10.1186/s42501-019-0023-9. ISSN 2524-4507.
- Khramov, Alexander V.; Lukashevich, Elena D. (July 2019). "A Jurassic dipteran pollinator with an extremely long proboscis". Gondwana Research. 71: 210–215. doi:10.1016/j.gr.2019.02.004. ISSN 1342-937X.
- Doweld, Alexander B. (2016-05-03). "The nomenclature of Cycadeoidea (fossil Spermatophyta: Cycadeoideopsida)". Taxon. 65 (2): 372–379. doi:10.12705/652.16. ISSN 0040-0262.
- Carruthers, Wm (May 1870). "XVIII. On Fossil Cycadean Stems from the Secondary Rocks of Britain". Transactions of the Linnean Society of London. 26 (4): 675–708. doi:10.1111/j.1096-3642.1870.tb00201.x.
- Williamson, W. C. (May 1870). "XVII. Contributions towards the History of Zamia Gigas, Lindl. & Hutt.*". Transactions of the Linnean Society of London. 26 (4): 663–674. doi:10.1111/j.1096-3642.1870.tb00200.x.
- McLoughlin, Stephen; Pott, Christian; Sobbe, Ian H. (2018-03-01). "The diversity of Australian Mesozoic bennettitopsid reproductive organs" (PDF). Palaeobiodiversity and Palaeoenvironments. 98 (1): 71–95. doi:10.1007/s12549-017-0286-z. ISSN 1867-1608. S2CID 135237376.
- Britten, James; Boulger, George Simonds (1893). A biographical index of British and Irish botanists. London: West, Newman & co. p. 14. doi:10.5962/bhl.title.56947.
- Engler, H.G.A. 1892. Syllabus der Vorlesungen über specielle und medicinisch-pharmaceutische Botanik. xxiii + 184 pp. Gebr. Borntraeger, Berlin
- Arber EN, Parkin J (July 1907). "On the Origin of Angiosperms". Botanical Journal of the Linnean Society. 38 (263): 29–80. doi:10.1111/j.1095-8339.1907.tb01074.x.
- Crane PR (September 1985). "Phylogenetic relationships in seed plants". Cladistics. 1 (4): 329–348. doi:10.1111/j.1096-0031.1985.tb00432.x. PMID 34965681. S2CID 85709030.
- Taylor DW, Li H, Dahl J, Fago FJ, Zinniker D, Moldowan JM (March 2006). "Biogeochemical evidence for the presence of the angiosperm molecular fossil oleanane in Paleozoic and Mesozoic non-angiospermous fossils". Paleobiology. 32 (2): 179–90. doi:10.1666/0094-8373(2006)32[179:BEFTPO]2.0.CO;2.
- Friis EM, Crane PR, Pedersen KR, Bengtson S, Donoghue PC, Grimm GW, Stampanoni M (November 2007). "Phase-contrast X-ray microtomography links Cretaceous seeds with Gnetales and Bennettitales". Nature. 450 (7169): 549–52. Bibcode:2007Natur.450..549F. doi:10.1038/nature06278. PMID 18033296. S2CID 1198220.
- Ran JH, Shen TT, Wang MM, Wang XQ (June 2018). "Phylogenomics resolves the deep phylogeny of seed plants and indicates partial convergent or homoplastic evolution between Gnetales and angiosperms". Proceedings. Biological Sciences. 285 (1881): 20181012. doi:10.1098/rspb.2018.1012. PMC 6030518. PMID 29925623.
- Vajda, Vivi; Pucetaite, Milda; McLoughlin, Stephen; Engdahl, Anders; Heimdal, Jimmy; Uvdal, Per (August 2017). "Molecular signatures of fossil leaves provide unexpected new evidence for extinct plant relationships". Nature Ecology & Evolution. 1 (8): 1093–1099. doi:10.1038/s41559-017-0224-5. ISSN 2397-334X. PMID 29046567. S2CID 3604369.
- Wu, Qiong; Ramezani, Jahandar; Zhang, Hua; Wang, Jun; Zeng, Fangui; Zhang, Yichun; Liu, Feng; Chen, Jun; Cai, Yaofeng; Hou, Zhangshuai; Liu, Chao (2021-02-05). "High-precision U-Pb age constraints on the Permian floral turnovers, paleoclimate change, and tectonics of the North China block". Geology. 49 (6): 677–681. Bibcode:2021Geo....49..677W. doi:10.1130/G48051.1. ISSN 0091-7613. S2CID 234064909.
- Pott, Christian; McLoughlin, Stephen; Lindström, Anna (2009). "Late Palaeozoic Foliage from China Displays Affinities to Cycadales Rather than to Bennettitales Necessitating a Re-Evaluation of the Palaeozoic Pterophyllum Species". Acta Palaeontologica Polonica. 55 (1): 157–168. doi:10.4202/app.2009.0070. ISSN 0567-7920. S2CID 52253114.
- Blomenkemper P, Kerp H, Abu Hamad A, DiMichele WA, Bomfleur B (December 2018). "A hidden cradle of plant evolution in Permian tropical lowlands". Science. 362 (6421): 1414–1416. Bibcode:2018Sci...362.1414B. doi:10.1126/science.aau4061. PMID 30573628.
- Kustatscher, Evelyn; van Konijnenburg-van Cittert, Johanna H.A. (2005). "The Ladinian Flora (Middle Triassic) of the Dolomites: palaeoenvironmental reconstructions and palaeoclimatic considerations" (PDF). Geo.Alp. 2: 31–51.
- Gnilovskaya, Anastasia A.; Golovneva, Lina B. (February 2018). "The Late Cretaceous Pterophyllum (Bennettitales) in the North-East of Russia". Cretaceous Research. 82: 56–63. doi:10.1016/j.cretres.2017.09.013.
- McLoughlin S, Carpenter RJ, Pott C (April 2011). "Ptilophyllum muelleri (Ettingsh.) comb. nov. from the Oligocene of Australia: last of the Bennettitales?". International Journal of Plant Sciences. 172 (4): 574–85. doi:10.1086/658920. S2CID 52885618.