Just as the animal kingdom lost some remarkable designs during the mass extinction events that punctuated the Palaeozoic and Mesozoic (consider the disappearance of the novel carapaces of trilobites and the aerofoils of pterosaurs), so too the plant kingdom lost some majestic groups that, had they survived until today, would no doubt have been cultivated as centrepieces in many domestic gardens. One such group is the Bennettitales.
The Bennettitales were enigmatic, seed-bearing plants (gymnosperms) characterised by complex reproductive structures, some of which are not yet fully understood. Bennettitales are historically divided into two families, the Cycadeoidaceae (or Bennettitaceae) and the Williamsoniaceae. The two families are distinguished primarily by their growth habit and the arrangement of their reproductive organs. The former have short, stocky trunks somewhat like modern cycads, whereas the latter had slender, profusely branched stems. 1, 2, 3. The former appear to have been restricted to the Jurassic-Cretaceous of western Laurasia, whereas the latter had a global distribution and greater temporal range. They were neither the smallest plants of the Mesozoic nor the largest. They were one of the important, mid-storey elements of the vegetation. If you care to view almost any artist’s reconstruction of a Jurassic landscape you will no doubt see bennettitaleans growing around the feet of (or being eaten by) a large sauropod or ornithischian dinosaur. 4, 5.
Flowers before there were flowers
Apart from their growth habit, the most remarkable character of Bennettitales is their reproductive structures, which can be most simply described as “flowers”. Although these “flowers” differed in the details of their anatomy from the true flowers of angiosperms, they clearly represented an experiment in plant architecture that preceded, but paralleled in architecture, some of the adaptations of modern flowering plants.
The so-called “flowers” of Bennettitales may be either unisexual or bisexual. The most elaborate forms have a central column bearing a tightly packed array of ovules separated by sterile scales. This central complex is surrounded by a ring of male bracts bearing valve-like pollen sacs. These may be surrounded by further ranks of sterile bracts to form a compact, cup-like, showy “flower”. 6, 7
The first pollinatees?
The benefits of assembling the male and female organs into such a compact reproductive structure are unclear, since it would tend to increase the chances of unfavourable self-pollination. Several palaeobotanists have suggested that bennettitalean flowers were an early experiment in utilizing insects for cross-pollination, a strategy that was to prove so successful for the rise of the flowering plants in the Cretaceous. Certainly it is difficult to prove this hypothesis, but it is interesting to note that many bennettitalean fossils show signs of interactions with insects. Some of these were harmful to the plant – including signs of leaf-eating, leaf-puncture and growth of larvae within the fertile cones. Other evidence is more passive – including signs of emplacement of insect eggs on the underside of leaves. 8. Clearly, insects were regularly interacting with bennettitaleans, so it would not be surprising if some insects were employed as pollen carriers. In particular, Cupedid beetles have been invoked as potential pollinators of bennettitaleans, since social insects (such as bees) and specialist nectar feeders (such as butterflies) diversified later in the geological record.
Bennettitaleans and cycads
The fishbone-shaped leaves of most bennettitaleans led many early palaeobotanists to link these plants to cycads, which have broadly similar foliage. 9, 10, 11. This idea was reinforced by the rather stocky, cycad-like stems of many Northern Hemisphere bennettitaleans (within the Cycadeoidaceae). However, the complex reproductive structures of bennettitaleans were completely at odds with the rather simple cones of cycads. Furthermore, the anatomies of the leaves themselves show microscopic differences between these groups. The waxy cuticle that coats the surface of plant leaves is very robust and can survive extremes of burial pressure and heat during fossilization. In the 1930s, Swedish palaeobotanist, Rudolf Florin, noted that fossil bennettitaleans possessed a peculiar arrangement of the cells bordering the gas exchange pores (stomata) on the leaves. Instead of a ring of many cells surrounding the pore (as we see in cycads), bennettitaleans possessed just one prominent cell on either side of the pore. These cells have a thick coating of cuticle and, when the cuticle is extracted from the fossil leaf with acids and studied from the underside using a scanning electron microscope, the cells flanking the pore form a distinctive butterfly shape. 12, 13. Therefore, the similarities between cycads and bennettitaleans turned out to be entirely superficial. This is not uncommon amongst plants. Many groups have evolved similar leaf forms, similar vein styles and similar growth habits throughout the past 400mys as they adapted to similar environmental pressures.
Why are botanists in a battle over bennettitaleans?
While cases of “parallel evolution”, such as the growth habits of cycads and bennettites, are interesting ecologically, they just add to the difficulties in sorting out the biological relationships of extinct groups. Unravelling the relationships of the major plant groups has currently reached an impasse amongst botanists. Evolutionary “trees” constructed on the basis of molecular (DNA) data from living plants commonly invoke different relationships to those constructed on the basis of morphological data from living and fossil plants. Since we cannot obtain DNA data from extinct plants, advances in our understanding of seed plant relationships must now depend on obtaining new and better structural data from the many poorly known fossil groups, key among which is the Bennettitales. The characters most informative of evolutionary relationships generally lie within the reproductive structures, but the shape or even the presence or absence of a floral character, when studied from fossils, is often in the eye of the beholder. Current debate concerning the relationships of seed-bearing plants places the Bennettitales at centre stage. Some argue that this group has seeds with, among other features, a two-layered coat (integument) and radial symmetry, which would relate them closely to the flowering plants and the enigmatic living Gnetales (for example, Gnetum, Ephedra and Welwitschia). Others dispute the details of these interpretations and place Bennettitales in a loose alliance of other extinct “seed-ferns”, more remote from the flowering plants. Still a few cling to the notion of affiliation with the cycads. Clearly, the case is not yet closed on the position of the Bennettitales.
Origins and extinctions
The earliest convincing records of Bennettitales date to the early Late Triassic (about 230mya) from famous localities such as Lunz, in Austria. However, two factors suggest that they might have had even earlier origins: firstly, the great diversity and abundance of Bennettitales in those earliest assemblages; and secondly, episodic reports of leaves strikingly similar to bennettitaleans in rocks as old as Permian and Carboniferous in places such as China and India. Whenever they originated, the group certainly diversified greatly in the latter part of the Triassic and came to dominate some floras of the Jurassic and Early Cretaceous. Although the Jurassic is sometimes called “the age of cycads”, it should more appropriately be called “the age of Bennettitales”, since this group was generally more abundant.
The demise of the group is also intriguing. Most bennettitalean genera show a dramatic decline through the mid-Cretaceous, contemporaneous with the rise of the flowering plants. Traditionally, the Bennettitales were considered to have gone extinct at the end of the Cretaceous as one of the casualties of the environmental upheavals accompanying an asteroid impact in Yucatan. However, a few leaf impressions discovered over the course of the past 130 years in south-eastern Australia hint that this group may have lingered on in moist high-latitude refugia until the middle of the Caenozoic. This striking discovery, if confirmed, would be the botanical equivalent of finding a dinosaur in the Oligocene!
Bennettitales have been studied since the ‘Golden Age of Palaeobotany’ in the 1820s to 1830s, but only recently have we begun to appreciate the full diversity and complexity of the group. Current research at the Natural History Museum in Stockholm aims to understand the micro-anatomy of the Bennettitales better, to help resolve the controversies surrounding their evolutionary relationships. Because many bennettitalean stems and cones are preserved by siliceous permineralization, they can be sectioned and studied in three dimensions revealing the fine details of the various stages in the development of the plants and their organs – right down to the cellular details of their developing seed embryos. 14, 15, 16. While undertaking these investigations, other useful information has come to light. It turns out that Bennettitales have a range of micro-anatomical features on their leaves ranging from hairs and knobs to stomata placed in deeply sunken pits that are useful for interpreting the nature of Mesozoic environments. 17. Heavy protection of the stomata by sinking them into the leaf surface and surrounding them with hairs is a common strategy of plants experiencing physiological drought. Other studies, charting the distribution of the leaves through successive beds in southern Sweden and Australia reveal that the many species of this group may be useful for age categorization and correlation of continental strata between sedimentary basins. In each line of investigation, Bennettitales look set to continue their role on palaeobotany’s centre stage, so the harvesting of bennettitalean fossils from around the world looks set to continue.
Stephen McLoughlin and Christian Pott work in the Paleobotany Department of the Swedish Museum of Natural History and can be contacted at: Paleobotany Department, Swedish Museum of Natural History, Box 50007, 104 05 Stockholm, Sweden, or email@example.com and firstname.lastname@example.org.