Trends in Ecology & Evolution
ReviewMass extinction events and the plant fossil record
Introduction
Global marine biodiversity has been devastated five times during Earth history, first at the end-Ordovician (446 Mya) and then again at the Frasnian–Famennian (FFB, 371 Mya), the Permian–Triassic (PTB, 251 Mya), the Triassic–Jurassic (TJB, 200 Mya) and Cretaceous–Paleogene boundaries (KPB, 65 Mya). These events, termed ‘mass extinctions’, reset the evolutionary trajectories of marine families and orders and resulted in the collapse and reordering of entire marine ecosystems [1]. They are characterized in the palaeontological record by the global extinction of higher taxonomic groups at rates and magnitudes greatly exceeding background levels [2]. Although there is currently no clear consensus on the precipitating causes of these ‘big five’ mass extinction events, there is growing acceptance that they were probably forced by abiotic change of a magnitude similar to the greenhouse-induced climate change anticipated in the near future [3] (Table 1), making them a model for understanding biotic response to all forms of extreme environmental change.
Among terrestrial faunas, mass extinctions have closely paralleled those of marine biota, occurring relatively synchronously and with similar magnitudes of biodiversity loss [4] (Table 1). By marked contrast, global taxonomic losses above the rank of genus are relatively rare among plants across faunal mass extinction boundaries 5, 6, 7 (Table 1). Prior reviews of the fossil plant record have identified numerous reproductive, physiological and behavioural traits unique to plants that enable small populations, and hence plant species, to persist in the face of extreme environmental changes 6, 7, 8, 9.
Although the loss of plant diversity is less than that observed in the faunal record, recent palaeoecological studies of local and regional vegetation dynamics across three of the ‘big five’ marine mass extinction events, at the PTB 10, 11, 12, TJB [13] and KPB 14, 15, 16, 17, strongly challenge the long-held view that terrestrial vegetation remained unscathed after these events. These new studies, focusing on changes in abundance and community structure in addition to taxonomic richness, indicate ecological instability in plant communities and collapse, before or coincident with peak faunal extinction at the PTB 10, 11, 12, TJB 13, 14, 15, 16, 17, 18 and KPB 14, 15, 16, 17. The results are forcing us to question whether global compilations of plant diversity 5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, now over 20 years old, are the appropriate means of understanding past vegetation changes. Taxonomic diversity, often used as a metric of ecosystem health for modern communities, may not be the best measure of ecological change or response in the fossil record. Furthermore, the survival of a plant clade across a mass extinction event does not ensure provision of the same quantity or quality of primary productivity if a once ecologically dominant clade becomes rare. In this regard, regional palaeoecological records incorporating changes in abundance structure of a community may provide a more informative method of assessing past vegetation change and feedback effects on faunal extinctions.
Here, we explore the apparently contradictory evidence for the remarkable persistence of higher plant taxa across mass extinction boundaries, despite growing indications of concurrent ecological upheaval in terrestrial plant communities. Eighteen years since Traverse's initial observation [9] we ask, do plants really ‘dance to a different beat’ during these unique intervals in Earth history? We compare the evolutionary and macroecological dynamics of terrestrial vegetation associated with extreme environmental and global climatic change spanning three of the big five marine mass extinction events (the PTB, TJB and KPB), for which detailed plant palaeoecological studies are available. These extinction boundaries share several abiotic attributes, which were probably caused by intense episodes of flood basalt volcanism, or a meteorite impact in the case of the KPB (Table 2). The end-Ordovician and FFB extinctions are excluded, as vascular land plants had not yet evolved in the case of the former and no quantitative plant palaeoecological data are available in the case of the latter. We also do not focus on time intervals for which there is good evidence for increased plant extinctions but an absence of faunal mass extinction, such as the Westphalian–Stephanian boundary (305 Mya) 20, 21, early Oligocene (29 Mya, Niklas,1997) and many others. An excellent summary of these noncoincident plant extinctions is available in [6]. The primary focus of our review is on contrasting macroevolutionary and macroecological patterns between flora and fauna in the context of the extreme environmental change associated with the PTB, TJB and KPB.
Section snippets
Vegetation dynamics across marine mass extinction boundaries
In the following section we review a suite of recent studies documenting the taxonomic composition, palaeoecology and structure of ancient plant communities (based predominantly on fossil leaves, pollen and spores) representing time intervals before, during and after the three most recent marine mass extinction events in Earth history, at the PTB, TJB and KPB.
Looking for common patterns of vegetation responses
Terrestrial systems experienced destabilization and collapse at the PTB, TJB and KPB. A common macroecological pattern was the permanent or temporary loss of ecological dominants from terrestrial plant communities at local to regional spatial scales, which took place over thousands to millions of years. The recovery intervals after all three reviewed mass extinction boundaries also highlight important similarities but also many unknowns. Although species diversity rebounded relatively rapidly
Conclusions
In the marine realm, mass extinctions removed the dominant incumbent genera, families and even orders via extinction [72]. For terrestrial plants, the majority of dominant incumbent genera and families at the PTB, TJB and KPB did not become extinct, but rather were relegated to a lesser ecological role or were replaced by related species or genera. In marked contrast to the animal kingdom, these events have not had a primary role in the trajectory of plant evolution, having had little
Acknowledgements
We thank I. Glasspool, R. Barclay and two anonymous reviewers for extremely helpful feedback and constructive criticism on the article. J. McElwain acknowledges funding from an EU Marie Curie Excellence Grant, MEXT-CT-2006–042531 (MassExtinct). Funding for S. Punyasena was provided by a US EPA STAR Fellowship FP-91637701–0.
Glossary
- Autochthonous
- formed or originating in the place where found.
- Bennettites
- a group of gymnosperms with cycad-like foliage and reproductive structures arranged into ‘flowerlike’ sometimes bisexual structures, which were probably insect pollinated.
- Clastic
- fragments of pre-existing rocks that have been produced by the processes of weathering and erosion and in general transported to a point of deposition.
- Corystosperms (Corystospermales)
- a group of Mesozoic seed ferns that were most abundant in the
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