The Importance of the Caytoniales and Cayton Bay (Yorkshire)

Caytonales are an important extinct group of seed ferns. They were first studied at Cayton Bay and other Yorkshire locations of Jurassic age by Hugh Hamshaw Thomas of Cambridge University in 1925 and by Thomas Harris of Reading University from about 1930 until after 1970.

Reticulate leaf venation and cupule structures bearing the ovules and seeds have suggested to many scholars a relationship of Caytoniales to the flowering plants that dominate the modern world. A recent study by James Doyle of University of California at Davis suggests that the position of Caytonia ovules on the inner adaxial surface of the cupule led to its reduction to become the outer layer of the double seed integument of the early flowering plants. Caytonia was wind-pollinated and had characteristic small wind-dispersed bisaccate pollen, which floated in a pollination droplet in order to achieve fertilization of the ovule. The small pollen grains known by the form genus name Vitreisporites were typically about 25 to 30 micrometres in diameter. They are often found in association with other plant parts - the Caytonia seed-bearing cupule, the pollen organ Caytonanthus, and the large, palmately compound, reticulately veined leaves known as Sagenopteris. It is believed that Caytonia was a tree, but the reproductive parts have seldom or never been found attached to the wood and leaves. Sir Peter Crane (retiring director of Kew Royal Botanical Gardens), palynologist Else-Marie Friis of the Swedish National

Museum and Patrick Herendeen of Smithsonian Institution USA discussed this problem in October 2004 (American Journal of Botany). This is a major reason why additional fieldwork is needed in Yorkshire and elsewhere. The Cayton Bay - Gristhorpe plant beds are reported to extend deeper, and field work in the older Triassic sediments could be informative whether Caytonia evolved from the Permian Glossopterids of the old Southern Continent Gondwana.

The Sagenopteris leaves typically have four to six leaflets palmately arranged each around six centimetres in length. Cupules typically have eight to forty ovules in their interior. A cupule lip near the stalk opens at pollination time, so that pollen grains can float inside for fertilization. It is thought the protective structure of the cupule was homologous to the outer layer of the intergument of the seed of flowering plants.

Professor James A. Doyle, now at the University of California at Davis, around 1970 pioneered electron microscopy of fossil pollens along with James Walker as students with Reed Rollins at Harvard University Herbaria. In recent years he has become a leading authority on many aspects of green plant evolution, with emphasis on the fossil record, correlated with genetic, molecular, and ecological studies of living plants.

In 2004 Professor Doyle discussed evidence that angiosperms diverge quite early (substantially over 250 million years) from living gymnosperms (Conifers, Cycads, Ginkgo) and that Caytoniales, Glossopteris, Pentoxylon, and Bennettitiales are among the more likely candidates for fossil sister groups of flowering plants, while Gnetales, Corystosperms, Conifers are improbable. Adaxial position of ovules on leaf-like structures appears to link the favoured groups.

Around August-September 2004 Professor Doyle was working on a paper that particularly focused on Caytoniales and reproductive organs in groups where ovules are adaxial (on upper leaf surfaces that appear homologous to the carpel of angiosperms) rather than abaxial, and I asked him where one might search for additional fossil evidence of this important group.

Professor Doyle answered that the Cayton Bay area of Yorkshire, England, has been the best single source for Caytoniales, especially when it comes to stratigraphic correlations, and that further work there may still be productive. He recommends the 1993 Paleobotany text of Professors Wilson Stewart and Gar Rothwell, where Caytoniales are discussed [Chapter 15] and the possibly ancestral Glossopteridales among earlier Paleozoic "seed ferns" [Chapter 14]. The Doyle article presents an evolutionary cladogram with Caytonales as sister group of flowering plants (angiosperms) and Glossopteris, Pentoxylon, and Bennettitiales as probable members of a clade distinguished by adaxial placement of ovules on leaflike structures that appear homologous to outer layer of bitegmic carpel of flowering plants.

The Glossopteridales produced extremely widespread leaf fossils in most of the old southern Gondwana continent going back to relatively large Gangamopteris leaves of the lower Permian. Up to two hundred species have been proposed, but criteria for distinguishing them are problematical, and pollen and reproductive materials are rarely present. In some cases the pollen though considerably larger than the Vitreisporites pollen of Caytonia is similarly bisaccate, to float on a pollination droplet to reach the ovule. Fossil material related to Caytoniales first appears in Upper Triassic strata widely distributed in the northern hemisphere including Japan, Greenland, and Canada, and vegetative materials from the United States but as of 1993 no flower or seed structures from United States.
The bitgemic ovule is a critical character, as long discussed by Ledyard Stebbins, Armen Takhtajan and others. In October 2004 American Journal of Botany Crane, Herendeen and Friis comment that often the fossil fragments of plants are found detached from each other, so that it is difficult to be sure all fossil material comes from one plant and species and also to know how things are put together.

Knowledge of fossil Caytoniales began in 1925 when the distinguished British paleobotanist H. H. Thomas described compression specimens from mid-Jurassic plant-bearing beds near the coast of Cayton Bay ,Yorkshire. The seed-bearing organs appeared to be possible precursors of the enclosed carpels of flowering plants.

The commonest elements of Cayton Bay flora are palmately compound 3-6 leaflets. lanceolate In the leaf species Sagenopteris serrata narrow, lanceolate leaflets up to 7 cm long have prominent midveins and reticulate venation of anastomozing lateral veins.

Thomas Harris has been the author of many papers on fossils of Caytoniales. The foliage was known many years before the reproductive organs. Sagenopteris williamsi from Kootenai Formation Montana probably grew in swamp habitat associated with lignites according to LaPasha and Miller (1985).

Caytonanthus is the taxonomic designation for pollen-bearing branches. a slender axis bears flattened pinnate lateral branches, and each branch bears one to three elongate synangia each about one cm length with a pointed distal end and 3-4 locules of pollen sacs indicated by striations arranged about a central zone of tissue, as seen in photographs by J. M. Osborn at Cayton Bay (Stewart and Rothwell 1993, chapter 15). The pollen organs, sometimes called anthers, are radially symmetrical, with dehiscence toward centre of synangia. there is an epidermis composed of delicate fusiform cells with indication of thicker fibrous-walled elements beneath the small, bisaccate pollen grains are referred to genus Vitreisporites. In Caytonanthus arberi grains 25 micrometres long contain distinct endoreticulations lining interior of the sacci. According to Pedersen & Friis (1986) at ultrastructural level the pollen sexine is alveolate. According to J. M. Osborn the distal surface has a conspicuous sulcus. Zavada and Crepet 1986 report slightly larger pollen from Caytonanthus kochii 30 micrometres.

The Caytonia ovule-bearing structure axis is 5.0 cm. long bearing stalked multiovulate cupules in subopposite pairs. scars on axis megasporophyll" may indicate cupules were shed. Cupules nearly circular up to 4-5 mm diameter are borne along axis so that cupule is recurved with liplike projection (Harris 1940) near point of attachment 8-30 seeds depending on the species. Radially symmetrical seeds about 2 mm long are borne on delicate stalks in an orthotropous position on midvein of cupule.

The integument is an outer uniseriate epidermis that covers a row of radially aligned thick-walled cells. an inner cuticle has been isolated from C. sewardii (Krassilov 1977). Harris (1951) suggested outer portion of integument was fleshy much like a berry. Beneath epidermis are several rows of longitudinally directed fibers. The nucellus is attached only at base. Macerations suggest seed integument is vascularized. Dispersed seeds are referred taxonomically to form genus Amphorispermum (Harris 1931).

H. H. Thomas (1925) noted pollen grain in association with lipped portion of cupule he called the "stigmatic surface". It was suggested fertilization would take place via a pollen tube that grew from stigmatic surface to pollen chamber of ovules (interpreted as fruit with numerous seeds). Fine strands of cuticle were observed extending from cupule to seeds. These were interpreted as remnants of pollen tubes or extensions of seed micropyles but further discoveries show pollen grains are present inside cupules probably drawn in by pollination droplets that originated at the micropylar end of each seed (Harris 1940). The number of canals is consistent with the number of seeds produced in each cupule -- Caytonanthus swardii has 8; C. nathorstii 15; C. thomasii 30. However modern writers see a multiovulate cupule not angiospermous fruit. Krassilova (1977) sees this as one way for seeds to become enclosed. Reymanowna (1973) describes the histology of Caytonia from specimens in Grojec area of Poland. In Caytonanthus harrissii cupule is vascularized by a flattened plate of tracheids with bordered pits that extend up the middle of the cupule and give off laterals to the seeds. It has a cluster of seeds in the centre of the cupule, and the seed cluster was covered by a cutinized membrane rather than being separated by cupule tissue as in other species. Caytonanthus has been reconstructed as a small tree based on discovery of woody axes with Sagenopteris foliage attached. (Harris 1971). Some sites appear periodically waterlogged. (Retallack & Dilcher 1988)

The mid-Jurassic Gristhorpe plant beds of Cayton Bay have other important groups of seed plant fossils, notably Bennettitiales. The temperature, seasonal precipitation pattern, winds, and paleolatitudes need to be understood, and similar studies are needed for the older southern hemisphere Glossopteridales, which may be ancestral. The compound leaves of Caytoniales [Sagenopteris] are an indication that at some phase water conservation was advantageous, at least seasonally. In the Triassic, it is believe large areas of the interior of the Pangaea supercontinent were hot and desert-like, as indicated perhaps by the evolutionary effects on the complex thalloid
Marchantialian liverworts as well as other groups. At some stage Caytoniales must have had Pangaean or Gondwanan ancestors.

The majority of Glossopteridales were in southern hemisphere paleolatitudes, and some show signs of deciduous leaves and seasonal varves in wood. It would be interesting to know if some of them diversified for high and low sun environments, and if any of them were adapted to hot, dry, and equatorial climates. Levels of oxygen and carbon dioxide may have been higher than today. Studies of paleosols nutrients could be informative.

The Glossopteridales showed greatest success and diversity in the Permian, but some appear in Triassic strata up to perhaps 225 million years ago. The mid-Jurassic is around 170 million years ago. The 1993 Wilson Stewart - Gar Rothwell text "Paleobotany and the Evolution of Plants" is an excellent source on the Glossopterids, and other possibly related groups such as Pentoxylon.
It calls attention to a relatively late appearing of Glossopteris-like foliage from the Middle Jurassic Zorrillo Formation of Oaxaca, Mexico, placed in a new genus Mexiglossa by Delevoryas and Person (1975). Leaves are as large as 26 cm. long. This may have spread from earlier Gondwana sites. Delevoryas and Gould (1971) publish a drawing of a suggested reconstruction of a probably related pollen organ Perezlaria oaxacensis "as an axis with laterals that bear whorls of saclike bodies that were probably pollen sacs." "Isolated organs resembling the synangia of Caytonanthus" appear in vicinity of Glossopteris-like foliage. The sporangia were about 3 mm long and appeared to dehisce as units. The panicle-like structure shows some resemblance to that of Caytonanthus. Bennettitiales are believed to have been understory plants that may have grown along stream margins and perhaps to have been insect pollinated, though it some cases it is wondered if they self-pollinated, as there is no obvious way for pollen to reach the ovules. The plant morphology has been compared to living Cycads, but reproduction clearly was different, and they are not closely related.

A Natural History magazine article June 2000, by Foster and Barker, discussed Pentoxylon fossils from the Jurassic of Miles, Australia: "A tree with long leaves on short stalks, Pentoxylon was unlike any tree known today. Its fossilized pollen resembles that of ginkgoes and cycads. Columns of vascular tissue are visible here in a cross section of trunk. The colours of the chert (the variety of quartz that has replaced the wood) are imparted primarily by iron oxides."


Caytonia bibliography :-

Bowman, J. L. 2000. The YABBY gene family and abaxial cell fate. Curr. Opin. Plant Biol. 3: 17–22.

Crane, P. R., H Patrick and E M Friis, 2004. Fossils and plant phylogeny Am. J. Bot. 91: 1683-1699.

Delevoryas, T. and R E Gould, 1971. An Unusual Fossil Fructification from the Jurassic of Oaxaca, Mexico. American Journal of Botany 58, 7.

Delevoryas, T., C. P. Person, 1975. Mexiglossa varia gen. et sp. nov., a new genus of glossopteroid leaves from the Middle Jurassic of Oaxaca, Mexico. Palaeontographica Abt. B 154:114-120. [ Cited by Stewart and Rothwell 1993 Paleobotany and the Evolution of Plants, Chapter 14]

Doyle, J.A. 1978. Origin of Angiosperms. Ann. Rev. Ecol. Syst. 9, 365-392.

Doyle, J.A., 2006 [in press]. Seed ferns and the origin of angiosperms. Journal of the Torrey Botanical Society.

Foster, G and N Barker 2000. Inner Beauty - When minerals seep into fossils, nature is transformed into art. Natural History magazine June 2000 [page number not available]

Harris, T.M. 1931. Amphorispermum- an Enigmatic Assemblage. Palaeobotanist 28- 29, 210-217.

Harris, T.M. 1932. The Fossil Flora of Scoresby Sound East Greenland, Part 3: Caytoniales, Cycadales and Bennittitales. Medd. Gronland 85 (5), 1-333.

Harris, T.M. 1940. Caytonia. Ann. Bot. 4, 713-734.

Harris, T.M. 1941. Caytonanthus, the Microsporophyll of Caytonia. Ann. Bot. 5, 47- 58.

Harris, T.M. 1951. The Relationships of Caytoniales. Phytomorphology 1, 29-39.

Harris, T.M. 1964. The Yorkshire Jurassic Flora II: Caytoniales, Cycadales and Pteridosperms. British Museum (Natural History) London. pp. 1-38.

Harris, T.M. 1971. The Stem of Caytonia. Geophytology 1, 23-29.

Kim, J.H. and T. Kimura. 1987. Cuticle of Sagenopteris (Caytoniales), an Extinct Gymnospermous Plant, First Observed in Japan. Proc. Japan Acad. Ser.B 63, 179-182.

Krassilov, V.A. 1977. Contributions to the knowledge of the Caytoniales. Rev. Palaeobot. Palynol. 24, 155-178.

LaPasha, C.A. and C.N. Miller. 1985. Flora of the Early Cretaceous Kootenai Formation in Montana; Bryophytes and Tracheophytes Excluding Conifers. Palaeontography 196 B, 111-145.

Pederson, K.R. and E.M. Friis. 1986. Caytonanthus Pollen from the Lower and Middle Jurassic; In Twenty-five Years of Geology in Aarhus (J.T. Moller, ed.). Gevskrifter Dept. Geol. Aarhus Univ. 24, 225-267.

Retallack, G. J., Dilcher, D. L., 1988. Reconstruction of selected seed ferns. Ann. Missouri Bot. Gard. 75: 1010-1057. [Cited by Stewart and Rothwell in Paleobotany and the Evolution of Plants 1993 Chapter 15 "Mesozoic Seed Ferns - Caytoniales" p. 579. ]

Reymanowna, M. 1973. The Jurassic Flora from Grojec Near Krakow in Poland Part II: Caytoniales and the Anatomy of Caytonia. Acta Palaeobotanica 14, 46-87.

Stewart, W, and Rothwell, G 1993 Paleobiology and the Evolution of Plants . Cambridge University Press

Taylor, T.N. and E.L. Taylor. 1993. The Biology and Evolution of Fossil Plants. Simon and Schuster Co. NJ, USA.pp. 575-579.

Thomas, H.H. 1925. The Caytoniales; A New Group of Angiospermous Plants from the Jurassic Rocks of Yorkshire. Phil. Trans. Roy. Soc. London. 213, 299-363.

Tomlinson P B, J E Braggins and J A Rattenbury 1997. Reproductive Biology - Contrasted pollen capture mechanisms in Phyllocladaceae and certain Podocarpaceae (Coniferales). American Journal of Botany, 84, 214.

Tomlinson P.B. 1994. Functional morphology of saccate pollen in conifers with special reference to Podocarpaceae. Int. J. Plant. Sci. 155, 699-715.

Zadava, M.S. and W.L. Crepet. 1986. Pollen Wall Structure of Caytonanthus. Plant Syst. Evol. 153, 259-264.

Author's address:-
John B. Barrett, 300 Evergreen Loop, Forks, Washington, WA 98331-9680, USA.

copyright Hull Geological Society 2006

Humberside Geologist Online