Chris Mays and Stephen McLoughlin (Sweden)

Caught between mass extinctions - the rise and fall of Dicroidium

n the aftermath of Earth’s greatest southern latitudes in the Early during the twentieth century have biotic crisis 251.9 million years Triassic and they overwhelmingly intergradational features. Moreover, Iago - the end-Permian mass dominated the southern vegetation some species may have hybridised, extinction - a group of plants arose by the Middle and Late Triassic. resulting in progeny that had different that would come to dominate the The Dicroidium plant had leaves that leaflet morphologies even on separate flora of the Southern Hemisphere. were superficially fern-like (Fig. 1). parts of the same frond (Fig. 1C). Recovery of the vegetation from the However, unlike ferns, these plants The world experts on this group, end-Permian crisis was slow; but produced pollen and seeds, and Heidi Anderson-Holmes and John steadily, one group of seed plants, are commonly lumped into an ill- Anderson, who have collected some typified by the leaf fossil Dicroidium, defined group called the ‘seed-ferns’. 40,000 Triassic plant fossils during began to diversify and fill the Dicroidium leaves are characterised their careers, have recognised 23 dominant canopy-plant niches left by the presence of a distinctive species and 16 sub-species categories vacant by the demise of the Permian fork near the base of the frond. or ‘forma’ of Dicroidium (Anderson glossopterid forests (Fielding et Numerous types of Dicroidium are and Anderson, 1983). al, 2019). Eventually, Dicroidium recognised, but one of the difficulties Many of these species can be found re-established a rich peat-forming involved in separating species is all over southern Gondwana (Fig. vegetation across Gondwana through their considerable variation in leaf 1). This suggests that these plants the Late Triassic, dominating the flora form. Many of the species established were part of a relatively monotonous between 30°S and the South Pole (Kustatscher et al., 2018). Indeed, few fossil plant assemblages of this age can be found in Gondwana that do not contain this plant. The importance of Dicroidium is not just its role in showing biogeographic and tectonic linkages between southern lands or its value in determining the age of continental strata. Dicroidium and its associated plant groups were so successful that they were major contributors to the development of thick coal seams in the Late Triassic that are now mined to produce electricity. Although Dicroidium is generally envisaged as a plant of cool temperate climates, the very first fossils that might belong to this group are from the Permian-Triassic transition of Jordan, located near the palaeoequator (Blomenkemper et al., Fig. 1. The same species of Dicroidium (D. odontopteroides) from three southern continents: (A) Birds River, 2018). Nevertheless, the distribution South Africa; (B) Ipswich, Australia; (C) Transantarctic Mountains, Antarctica - this frond features both the of Dicroidium soon shifted to high typical rounded leaflets, but also elongated forms (arrow), which may indicate hybridisation.

Deposits Magazine - Issue 59 (2019) - Page 42 Deposits Magazine - Issue 59 (2019) - Page 43 flora that spanned the cool, high- of metres thick and no forests exist forests today. Polar forests, like those latitude regions of the Southern for thousands of kilometres in any of Dicroidium during the Triassic, Hemisphere (Fig. 2), much like the direction. Moreover, the modern have been the norm since the first Author (Country) boreal conifer forests that dominate boreal forests are dominated forest ecosystems of the Devonian, Canada, Scandinavia and northern by members of the pine family whereas forbidding polar ice caps Russia today. But here, our modern (Pinaceae), which have needle-like have been the exception. Despite analogues seem to break down. The leaves adapted for cold temperatures their common occurrence in Earth’s climate of the Triassic was generally and are mostly evergreen. This history, the specifics of how ancient much warmer than today, with contrasts with Dicroidium, whose polar forest ecosystems survived and Dicroidium forests thriving at 80 leaves were broader and probably thrived still elude us. The present to 85°S, and possibly stretching all deciduous, being shed along with is not always the key to the past, the way to the South Pole. At these their fertile parts in the polar autumn. particularly when the present climate latitudes today, the south polar region These features are like birch trees, is exceptional. is covered by ice sheets thousands which dominate some cool-temperate Just how the leaves of these plants should be classified remains controversial. Some palaeobotanists have divided Dicroidium-type leaves into several additional genera (for example, Dicroidiopsis, Diplasiophyllum, Zuberia, Xylopteris, Johnstonia and Tetraptilon), but these all appear to be just morphological variants of the same basic leaf plan and can be comfortably accommodated in Dicroidium (Anderson and Anderson, 1983). The practice of establishing all these redundant or synonymous genera based on very minor differences in leaf shape is problematic because it leads to ‘taxonomic inflation’. Thus, the disappearance of a single plant group in the fossil record might be mistaken for a mass-extinction of genera if all the redundant taxa are Fig. 2. Map of Triassic Gondwana showing the distribution of Dicroidium. counted from the literature. At the other extreme, by adhering to general descriptions for a taxon, you may accumulate a broad range of different leaf forms under one generic banner, potentially hiding crucial differences

Fig. 4. An impression of Dicroidium Fig. 3. Paper shales from the Upper Triassic Leigh Creek Coal Measures. Like an autumn forest odontopteroides from New South Wales, floor of the Triassic, compression and impression fossils of Dicroidium cover almost the entire Australia, with the characteristic venation area of the bedding surface. pattern.

Deposits Magazine - Issue 5859 (2019) - Page 44 Deposits Magazine - Issue 5859 (2019) - Page 45 between distinct natural plant groups. For example, this can result in species being recognised long after the rest of Author (Country) the genus has gone extinct, some of which are clear cases of convergent evolution, rather than survivors of an otherwise long-dead lineage. The ‘to-split-or-to-lump’ dilemma is particularly tricky when discussing plant leaves, such as Dicroidium, that have so few morphological characters. Reconstructing Dicroidium It is difficult to visualise the Dicroidium plant because few artistic reconstructions have been published (Retallack and Dilcher, 1988). As noted above, it seems to have been Fig. 5. A fossil log recovered from Dicroidium-rich Triassic strata at Leigh Creek, South deciduous; the leaves are commonly Australia. preserved as stacked matted sheets, like thousands of autumnal forest or ‘peduncles’ bearing rounded (Anderson and Anderson, 1983). The floors frozen in time, with the leaflets heads, each enclosing a single seed only exceptions to this general rule blowing away in the wind once you (Anderson and Anderson, 2003). The are those landmasses which have crack open a rock along the bedding seed-bearing heads of these organs migrated far northwards since the plane (Fig. 3). The leaves have commonly have a dimpled or wrinkled Triassic (for example, the Indian distinctive ‘odontopteroid’ venation appearance (Fig. 7) suggesting they subcontinent and the Arabian - with several veins emerging from were fleshy or leathery in life, then Peninsula). In Australia, good the base of the leaflets, and arching splitting and shrivelling on releasing collecting sites are available around and branching towards the margins their seeds. The seeds were less than the old clay pits and coal mines at (Fig. 4). Fossil wood associated with one centimetre long, pear-shaped and Ipswich, west of Brisbane, along the the leaves has prominent growth had narrow wings – again, like their coastal cliff sections to the north of rings indicating growth in a strongly pollen, for wind dispersal. This group Sydney, and at the old Leigh Creek seasonal environment. Some of the of plants is of particular interest to Coal Mine in South Australia (Fig. associated petrified logs can reach palaeobotanists, as its possession of 10). In New Zealand, Dicroidium 10m long and over half a metre in seeds tightly enclosed within a head or has been collected in Triassic diameter (Fig. 5) - so we can assume ‘cupule’ is similar to the architecture exposures at Tank Gully, Long Gully that these plants were probably large of the seeds of flowering plants (which and Benmore Dam in southern trees. Palaeobotanists have also found have two tightly fused layers forming Canterbury and northern Otago. In the male, pollen-bearing, organs of the seed wall). South Africa, numerous collecting these plants and given them the name Dicroidium also has a role to play in sites have been documented Pteruchus (Figs. 6 and 7). The pollen understanding insect evolution. Since from exposures of the Molteno grains contained inside these organs Triassic fossil deposits containing Formation in the Karoo Basin. In are winged, indicating dispersal by insects are few and far between, Argentina, well-studied Dicroidium the wind and are given the name the feeding damage preserved on assemblages have been collected Falcisporites (Fig. 7). The female the leaves of this dominant plant from outcrops of the Ischigualasto organs are given the name Umkomasia helps us understand the guilds of Formation north of Mendoza. In (Figs. 7 and 8) and consist of a stalk insect herbivores that were active India, Dicroidium is most commonly with numerous swan-like branches following the end-Permian extinction. found in the Panchet, Parsora and Dicroidium leaves host almost all the Tiki formations of the South Rewa major types of damage that we see in and Damodar basins in the northeast modern plants, for example, galling of the country. Some logistically (Fig. 9A), hole feeding (Fig. 9B) margin challenging options are the excellent, feeding, leaf mining and surface windswept rock outcrops of Victoria feeding (Labandeira et al., 2018). Such Land in East Antarctica, from which damage enables the reconstruction several species of Dicroidium have of complex food webs from past been recovered. ecosystems, even in the absence of the So what happened to these plants? body fossils of the insects themselves. Near the height of Dicroidium Where can I find Dicroidium today? diversity at the end of the Triassic, Since Dicroidium was essentially a the Earth faced another of its ‘big five’ Gondwanan plant, most of the localities mass extinctions - this event being Fig. 6. Pteruchus, the male pollen organ associated from which one can collect this fossil commonly linked to volcanism in the with the Dicroidium plant. are in the Southern Hemisphere Central Atlantic Magmatic Province.

Deposits Magazine - Issue 5859 (2019) - Page 44 Deposits Magazine - Issue 5859 (2019) - Page 45 Author (Country)

Fig. 7. A schematic reconstruction of the Dicroidium plant with different parts given separate names.

Millions of cubic kilometres of just after, the end-Triassic crisis. Flood volcanism in the Atlantic magma were extruded as ‘flood Thus, at the end of the Permian, region, and associated doubling basalts’ or intruded into the crust a major mass extinction left an of greenhouse gas concentrations as dikes and sills, the evidence for ecological vacuum for Dicroidium in the atmosphere, is commonly which is spread across much of to fill, only for this group of plants considered to have caused abrupt modern-day western Africa, and the to be vanquished by the next major eastern regions of the Americas. global crisis. However, during The prevalence of Dicroidium in the intervening 50 million years, the vegetation of the Southern Dicroidium reigned supreme as a Hemisphere came to an abrupt end true emblem of the Gondwanan and the genus was thought to have Triassic. been one of the major casualties A final consideration is to ponder of the end-Triassic crisis (Fig. 11). just what caused the demise of this However, recent findings suggest once hugely successful plant group. that Dicroidium may have lingered on in small populations into the earliest part of the Jurassic in Antarctica (Bomfleur et al., 2018). There is also a recent suggestion that this group of plants persisted into the Cretaceous in Mongolia, where reproductive structures similar to Umkomasia have been discovered. However, not all researchers agree with the identifications of these late Mesozoic fossils (Anderson et al., Fig. 9. Insect damage trace fossils on Dicroidium 2019) and it seems more likely that Fig. 8. Umkomasia (U. polycarpa), a female seed- reveal complex ecological interactions during the Dicroidium met its demise at, or bearing organ of the Dicroidium plant. Triassic: (A) galling and (B) hole feeding.

Deposits Magazine - Issue 5859 (2019) - Page 46 Deposits Magazine - Issue 5859 (2019) - Page 47 global warming at the end of Crowley, J.L. 2019. Age and pattern of the Labandeira, C.C., Anderson, J.M. & Anderson, the Triassic. Since plants are southern high-latitude continental end- H.M. 2018. Expansion of arthropod herbivory in Permian Authorextinction (Country)constrained by multiproxy Late Triassic South Africa: The Molteno Biota, particularly responsive to climate, analysis. Nature Communications 10:385. Aasvoëlberg 411 Site and developmental biology perhaps the polar environments of https://doi.org/10.1038/s41467-018-07934-z of a gall. In: Tanner, L.H., ed., The Late Triassic Antarctica provided the last refuge for Kustatscher, E., Ash, S.R., Karasev, E., Pott, World. Earth in a Time of Transition. Topics in these moisture-loving cool temperate C., Vajda, V., Yu, J. & McLoughlin, S. 2018. Geobiology 46, Springer, Cham, Switzerland, plants in the earliest Jurassic. In Flora of the Late Triassic. In: Tanner, L.H., 623–719. ed., The Late Triassic World. Earth in a Retallack, G.J. & Dilcher, D.L. 1988. the modern world, atmospheric CO 2 Time of Transition. Topics in Geobiology 46, Reconstructions of selected seed ferns. Annals concentrations have maintained an Springer, Cham, Switzerland, 545–622. of the Missouri Botanical Garden 75, 1010–1057. accelerating upward trajectory from 280 parts per million (by volume; ppmv) during the pre-industrial era (ending about 1750) to 315 ppmv in

1960. This year, CO2 concentrations have reached 415 ppmv, the highest for millions of years. It is, therefore, pertinent to remember the lessons that can be learned from the fossil record about the ‘points of no return’ for major biomes under a changing climate. About the authors Dr Chris Mays (Research Fellow) and Professor Stephen McLoughlin (Senior Curator) are researchers at the Swedish Museum of Natural History. Both originally from Australia, they are presently investigating the patterns of vegetation turnover and recovery associated with the end-Permian and end-Triassic mass extinction events in palaeopolar regions. Further Fig. 10. Australian Triassic outcrops rich in Dicroidium and their associated fossils: (A) details of their research can be found at: ht t p:// Lower Triassic Terrigal Formation outcrop, north of Sydney - the arrow indicates a series of www.nrm.se/en/forskningochsamlingar/ fossiliferous horizons; and (B) Leigh Creek open-cut coal mine (now closed), South Australia, paleobiologi/medarbetareochkontakt/ exposing numerous thick, Upper Triassic coal seams. chrismays.9004589.html and ht t p:// www.nrm.se/en/forskningochsamlingar/ paleobiologi/medarbetareochkontakt/ stephenmcloughlin.333.html. References

Anderson, J.M. & Anderson, H.M. 1983. Palaeoflora of southern Africa: Molteno Formation (Triassic), Vol. 1: Part 1, Introduction, Part 2, Dicroidium. Balkema, Rotterdam. 227 pp. Anderson, J.M. & Anderson, H.M. 2003. Heyday of the gymnosperms: systematics and biodiversity of the Late Triassic Molteno fructifications. Strelitzia 15. National Botanical Institute, Pretoria, 398 pp. Anderson, H.M., Barbacka, M.K., Bamford, M.K., Holmes, W.B.K., Anderson, J.M. 2019. Umkomasia (megasporophyll): part 1 of a reassessment of Gondwana Triassic plant genera and a reclassification of some previously attributed. Alcheringa 43, 43–70. Blomenkemper, P., Kerp, H., Hamad, A.A., DiMichele, W.A., Bomfleur, B. 2018. A hidden cradle of plant evolution in Permian tropical lowlands. Science 362, 1414–1416. Bomfleur, B., Blomenkemper, P., Kerp, H. & McLoughlin, S. 2018. Polar regions of the Mesozoic–Paleogene greenhouse world as refugia for relict plant groups. In: Krings, M., Harper, C.J., Cúneo, N.R., Rothwell, G.W., eds, Transformative Paleobotany: Papers to Commemorate the Life and Legacy of Thomas N. Taylor. Elsevier, Amsterdam, 593–611. Fielding, C.R., Frank, T.D., McLoughlin, S., Vajda, V., Mays, C., Tevyaw, A.P., Winguth, Fig. 11. Triassic timeline showing the relative dominance of some of the main terrestrial groups A., Winguth, C., Nicoll, R.S., Bocking, M., and key extinction events.

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