Laboratory 13 * The Cycads, Cycadeoids (Bennettitales) and Ginkgophytes
 
This week's laboratory is on the cycads, a gymnospermous group for which we have living representatives, the cycadeoids, an extinct Mesozoic group, and the ginkgophytes, a group characterized by the extant monotypic genus Ginkgo and numerous fossil relatives.
 
Today the cycads represent a relatively small group of about half a dozen genera (including Cycas, Bowenia, Dioon, Zamia, Ceratozamia, Encephalartos) that are found worldwide in disjunct tropical and semitropical areas. This group of plants was much more widespread during the Mesozoic (Triassic, Jurassic, Cretaceous), which is sometimes called the "Age of Cycads". The cycads have frequently been compared to the Cycadeoidales (Bennettitales) which also occurred during the Mesozoic, and collectively these two groups are sometimes called cycadophytes.Although they are superficially similar to cycads in growth habit and leaf morphology they have entirely different reproductive structures. The third group, the ginkgophytes, today represented by Ginkgo, were also an important component of the Mesozoic flora.
 
I.  Cycadopsida  
 A. The cycads
Cycads are typically trees with short trunks and large pinnately compound frond-like leaves, although some forms are have more slender stems and occasionally can be rhizomatous and scrambling. They have endarch steles that produce leaf traces that "girdle" or surround the stele as they diverge to vascularize the leaf. Girdling leaf traces are characteristic of cycads and not known in other gymnospermous groups. Cycads typically produce a small amount of manoxylic wood, with broad parenchymatous rays and often contain abundant resinous cells and resin canals. To the periphery of the stem, cycads produce a "leaf armour" consisting of the tightly packed, helically arranged leaf bases. Look at the live plants, herbarium sheets and other materials of cycads in the lab.
 
Cycads are dioecious and, when fertile, produce a terminally positioned cone that bears either pollen sacs or ovules. Sometimes the vegetative apex of a cycad can bifurcate and continue to grow, pushing the cone to the side. This is called sympodial branching, and is relatively rare among seed plants. 
 
In one species, Cycas revoluta, the megasporangiate structures are not cones, but helically arranged megasporophylls which bear several seeds pinnately on the modified leaf. Other cycads are characterized by large cones composed of modified leaves (sporophylls) with peltate heads that bear two ovules each. In some genera, such as Dioon, the peltate head may have a small spiny projection on the distal side of the head. It has been suggested that these variations among the living cycads may represent an evolutionary series. Look at seed cones in the lab. 
 
Pollen cones of cycads consist of helically arranged, tightly packed peltate sporophylls that bear a number of pollen sacs on their surfaces. Pollen is ovate and monocolpate (with a single elongate germination furrow) and lacks the air bladders typically seen in pinaceous conifers. The pollen contains unusual, large top-shaped sperm with helically arranged rows of flagella. When pollination occurs a branched pollen tube is ruptured by the swimming sperm on their path to fertilize the egg. This haustorial pollen tube is quite unlike the straight, rarely branched siphonogamous pollen tube we encountered in the conifers. You may recall that the conifers had pollen grains that contained non-motile sperm that were delivered directly to the pollen chamber of the ovule by their pollen tubes. Cycad pollination biology is thought to be more primitive. When we get to Ginkgo, you will see that it too, has motile sperm. Look at the pollen cones we have in the lab.
 
B. The fossil record of the cycads:
Although there has been some suggestion that cycads originated in the Carboniferous (possibly from the medullosan seed ferns) the first strong evidence for cycads occurs in the Permian. Mamay (1976) has suggested that the earliest seed-bearing cycadaceous foliage was Spermopteris, an entire-margined, strap-shaped leaf with parallel veins very similar to the vegetative leaf Taeniopteris. Mamay documented the occurrence of other cycadaceous seed-bearing foliage types in the Permian, including the genera Phasmatocycas and Archaeocycas, which also have an entire, or slightly crenulate leaf margin. Since later Mesozoic cycad vegetative foliage types (Nilssonia, Ctenis, Pseudoctenis) are pinnately compound, as are modern forms, Mamay suggested an evolutionary trend toward progressive dissection of cycad fronds.
 
See p. 343 of your text for illustrations of Permian cycadophyte leaves.
 
Recently however, new cycad remains have been discovered in China that demonstrate Permian aged cones with megasporophylls strikingly similar to those of modern Cycas media. You may recall that this is the one genus of cycads that has helically arranged megasporophylls rather than a compact seed cone (see p. 341, fig. A in your text). Look at the photos of Crossozamia in your text on p. 344. These fossils demonstrate that cycad cones bearing megasporophylls much like those of modern Cycas media (but borne in a cone) were present at the same time (Permian) as Mamay's various entire-margined cycad sporophylls. Gao Zhifeng & Thomas suggest that instead of a simple reduction series toward dissected foliage and compaction into a cone, two separate trends occurred in cycad megasporophyll evolution, one toward the cone compaction and the other that toward less compact inflorescence of Cycas media. If this interpretation is correct, then modern Cycas media structure can no longer be considered the primitive condition.
 
A number of cycad stems are known from Triassic sediments from several localities. Leptocycas, a plant from the Upper Triassic of North Carolina, is known from compressions that show stems and leaf attachment and provide information about the growth habit of the plant. This plant was apparently a small, slender tree with a more elongate stem than is typical in modern cycads. See the reconstruction of Leptocycas in your text on p. 345.
 
Several of the Triassic and younger cycads are known from anatomically preserved material. These include an anatomically preserved cycad stem from the Petrified Forest and Antarctica, Antarcticycas. Both of these fossil stems have typical cycad stem anatomy, including a small amount of manoxylic wood, a broad pith, and resin canals.
 
Cycadaceous foliage such as Nilssonia is a common component of Mesozoic floras in both the northern and southern hemisphere. See the figure on p. 347 of your text for a general idea about the structure of this foliage.
 
II. Cycadeoideales 
 
Along with the cycads a second fossil group, the cycadeoids, produces what has been called cycadophyte foliage. The cycadeoids (Bennettitales) are a group of extinct seed plants that bore pinnately compound leaves that look superficially much like cycad leaves. However, cuticular studies have demonstrated that these two groups can be distinguished from one another on the basis of epidermal and stomatal differences. 
 
Starting with Thomas and Bancroft (1913) in the early part of the century, researchers began to recognize that some major groups of gymnosperms could be delimited by structural details of their epidermis and cuticle. Cycads have epidermal cells with straight margins, thin cuticle, and irregularly oriented stomata. Generally, cycads, conifers, seed ferns, Ephedra, Ginkgo, and the angiosperms all have haplochelic stomata, where the guard cells of the stoma develop from one epidermal initial and the associated subsidiary cells from another initial. In contrast, cycadeoids, Gnetum and Welwitschia have syndetochelic stomata (where guard cells and adjacent subsidiaries come from the same initial). Cycadeoids are also characterized by epidermal cells patterns with wavy margins, thick cuticles and cells aligned in rows, and stomata occurring at right angles to the veins.
 
Compare diagrams of a haplochelic stoma of cycads (p. 340 Fig. C) and syndetochelic stoma of cycadeoids (p. 352 fig. A).
 
Cycadeoid foliage is a common component of the Triassic Chinle Formation, the Triassic rock formation of the Petrified Forest National Park, Arizona. Look at two representatives of this foliage Otozamites and Podozamites, in the lab. You can see how this foliage would be easily assigned to cycad-like plants, based on its similarity to that of living cycads. Cycadophyte leaves (of both cycads and cycadeoids) are widespread from the Triassic to the Upper Cretaceous in Western Europe, Greenland, North America, and a number of southern hemisphere localities.
 
The cycadeoids are an extinct group of gymnosperms that are mostly known from Jurassic to Cretaceous strata in England, Europe, Greenland, India, the Black Hills of South Dakota, and Mexico. There are two families within this group, the older family, the Williamsoniaceae from the Upper Triassic to Jurassic, and the the younger family, the Cycadeoidaceae from the late Jurassic to the Cretaceous. The Williamsoniaceae are generally plants with longer, more slender branching stems, while the Cycadeoidaceae are shorter, unbranched trunks. 
 
Cycadeoid trunks such as that of Cycadeoidea from the Black Hills of South Dakota are sometimes called "fossil bee hives". They are large columnar trunks (up to 2 meters) that bear numerous tightly-appressed leaves and intermixed, helically arranged cones on the trunks (p. 357 of the textbook). Look at the specimens of Cycadeoidia trunks we have in the laboratory. Many of these trunks are permineralized and provide information about the internal anatomy of the plant. Cycadeoids bear bisporangiate (or less often, monosporangiate) cones that consist of a central axis (receptacle) which bears hundreds of tiny stalked ovules that alternate with scales. Microsporophylls are fused structures that bear synangiate pollen organs with monocolpate pollen somewhat similar to that of cycads and Ginkgo. The typically bisporangiate nature and general organization of the cycadeoid cones has at various times suggested a potential relationship to the angiosperms. Recent cladistic analyses of the seed plants (e.g., Crane, Doyle and Donoghue) have revived an interest in this group in relation to the angiosperm flower. Members of the Williamsoniaceae had cones that opened, that are sometimes called "flowers" because of their organization. Cones of the Cycadeoidaceae, with their large, fused microsporophylls, probably did not open to the external environment. Researchers have suggested that their primary means of pollination was selfing, although evidence of insect burrowings suggests they may have also been insect pollinated. See diagrams and photos in your text on p. 359-360.
 
III. Ginkgopsida 
 
The modern plant Ginkgo biloba is characterized as a small tree that bears fan-shaped leaves on long and short (spur) shoots. Ginkgo leaves are quite variable in their morphology and may be anywhere from entire-margined to highly dissected. They have an open dichotomizing venation pattern than only occasionally sows reticulations or anastomoses. In this regard they are markedly different from the leaves of Glossopteris, a Mesozoic seed fern, in which the interconnections or reticulations form a major part of the construction of the leaf's venation. In any case, both Ginkgo and glossopterid venation structure is built on a plan where the veins are all of a single size order, rather than being in a hierarchy, such as occurs in dicotyledonous leaves.
 
The fertile structures of Ginkgo occur on separate trees, with lax pollen cones in which microsporophylls bear pollen sacs with simple monosulcate pollen occurring on one tree (dioecy) and obnoxious ovules occurring on a separate tree. The ovules are borne, usually in pairs, on the tips of branch-like structures that have been homologized with megasporophylls. Ovules are subtended by a "collar" and are obnoxious because they have a modified integument with a fleshy sarcotesta (the outermost seed coat) that breaks down to produce a nasty smell as they ripen.
 
Look at herbarium sheets and other materials of Ginkgo in the lab.
 
The fossil record of ginkgophytes extends from at least the Triassic and perhaps the lower Permian. The earliest ginkgophyte is considered to be Tricholpitys, a ovulate branching structure which bears ovules with small collars like those of Ginkgo, and has highly dissected leaves. There is a general trend in the ginkgophyte leaves toward younger, broader and more entire leaves, which is consistent with the fossil record. One of the most common, older foliage types that is highly dissected is called Sphenobaiera. See p. 389 in your text.
 
 Foliage of Ginkgo-like plants is common and widespread throughout the Mesozoic. Unfortunately, however, although there is some fertile material known in the fossil record, it is not clear whether leaves of this general type are always indicative of plants with the fertile structures of Ginkgo.