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No Mass Extinction for Land Plants at the Permian–Triassic Transition

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No Mass Extinction for Land Plants at the Permian–Triassic Transition ARTICLE https://doi.org/10.1038/s41467-018-07945-w OPEN No mass extinction for land plants at the Permian–Triassic transition Hendrik Nowak 1, Elke Schneebeli-Hermann 2 & Evelyn Kustatscher1,3 The most severe mass extinction among animals took place in the latest Permian (ca. 252 million years ago). Due to scarce and impoverished fossil floras from the earliest Triassic, the common perception has been that land plants likewise suffered a mass extinction, but doubts 1234567890():,; remained. Here we use global occurrence data of both plant macro- and microfossils to analyse plant biodiversity development across the Permian–Triassic boundary. We show that the plant fossil record is strongly biased and that evidence for a mass extinction among plants in the latest Permian is not robust. The taxonomic diversities of gymnosperm macrofossils and of the pollen produced by this group are particularly incongruent. Our results indicate that gymnosperm macrofossils are considerably undersampled for the Early Triassic, which creates the impression of increased gymnosperm extinction in the latest Permian. 1 Museum of Nature South Tyrol, Bindergasse/Via Bottai 1, Bozen, Bolzano 39100, Italy. 2 Paläontologisches Institut und Museum, Karl Schmid-Strasse 4, 8006 Zürich, Switzerland. 3 Department für Geo– und Umweltwissenschaften, Paläontologie und Geobiologie, Ludwig–Maximilians–Universität, and Bayerische Staatssammlung für Paläontologie und Geologie, Richard–Wagner–Straße 10, 80333 Munich, Germany. Correspondence and requests for materials should be addressed to H.N. (email: [email protected]) NATURE COMMUNICATIONS | (2019) 10:384 | https://doi.org/10.1038/s41467-018-07945-w | www.nature.com/naturecommunications 1 ARTICLE NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-018-07945-w he end-Permian mass extinction was the most severe diversities of sporomorph and macrofossil taxa from the Lopin- extinction event in the Phanerozoic, with an estimated loss gian (upper Permian) to the Middle Triassic is presented here. T – of ca. 80 96% of species and ca. 50% of families of marine We show that the extinction of land plants at the invertebrates1,2. On land, tetrapods3 and insects4 were likewise Permian–Triassic boundary was much less severe than previously diminished and also for plants a loss of diversity (or taxonomic thought and that the apparent mass extinction can essentially be richness) has been suggested to occur between the Changhsingian explained by the dearth of data from the Lower Triassic. The (latest Permian) and the Induan (earliest Triassic), with a mag- fossil records of sporomorphs and macrofossils show consider- nitude that is comparable to the losses in marine invertebrates5–7. able differences, primarily concerning gymnosperms, which However, it has been questioned whether the terrestrial and might in part be attributed to taphonomic bias. marine events are coeval8–11. The fossil floras from the Early Triassic are marked by impoverishment and on the northern Results hemisphere often by the dominance of lycopsids (club mosses), especially Pleuromeia12–14. Correspondingly, spores of lycopsids Macrofossil record. Plant macrofossil species (Supplementary and ferns13 often dominate sporomorph (spores and pollen) Data 1) have their highest diversity at the base of the studied stra- assemblages from this time. This is interpreted as a period of tigraphic interval, in the Wuchiapingian (Fig. 1, Supplementary Data 2). Their diversity declines towards the Changhsingian, followed survival, which is followed by the recovery of conifers starting in – the Olenekian (late Early Triassic) at the Smithian-Spathian by a loss of more than half of the species across the Permian Triassic boundary13,15,16. In the southern hemisphere (Gondwana), glos- boundary. Species diversity starts to recover in the Olenekian and sopterids were dominant in the Permian, but they were dimin- continues towards the Ladinian. This pattern would seem to conform – to previous results based on plant macrofossil genera and families ished at the Permian Triassic boundary and replaced by the 5–7 fl 17,18 and common expectations (see refs. ). However, on the genus Dicroidium ora . Lower Triassic successions yielded only a – reduced number of well-preserved macrofossils of land plants and level, diversity loss across the Permian Triassic boundary is not are also notably void of coal measures19. The dearth of fossils catastrophic and diversity even increases slightly between the Wuchiapingian and the Changhsingian. In general, the genus agrees seemingly with a massive loss of vegetation, but it could fl also be accounted for by a severe taphonomic bias. diversity curve is rather at. Even more important, genus originations Local and regional studies have repeatedly delivered results that in the Changhsingian exceed extinctions, which means that net raise doubts about the importance of the end-Permian event for diversity increases during this stage. Extinctions only exceed origi- land plants20–25. Data on sporomorphs from the Permian–Triassic nations in the Induan, which is also the stage with the highest boundary interval are much more abundant than macrofossils, number of extinction events (Fig. 2). Conversely, origination num- providing valuable information about the development of terres- bers are very low, which results in the overall lower total diversity in trial floras during this critical time. The potential of these datasets theInduan.Thenormalizeddiversitycurvesuggeststhatthemean is still mostly unused, for in most cases, sporomorph diversity has standing diversity declined far less (Fig. 3). The results of shareholder quorum subsampling indicate a protracted decline between the only been studied on local or regional scales until now. fi In order to gain a more coherent picture of land plant history, a Changhsingian and Olenekian, but the con dence bounds are too detailed, comparative assessment of the stratigraphic ranges and large for robust conclusions (Fig. 3). Compared to an earlier diversity analysis on the level of genera by Rees7,ourcurveshowssimilar Species diversity Genus diversity Macrofossil Sporomorph Inferred Macrofossil Sporomorph Macrofossil Sporomorph rangethrough + rangethrough + genera genus diversity genus diversity data entries data entries boundary boundary (‘‘Lazarus taxa”) by group by group per stage per stage crossing genera crossing genera 100 200 300 400 500 50 150 0 25 50 75 100 125 0 50 100 150 200 10 30 50 0 500 1000 1500 2000 0 2500 5000 7500 10,000 12,500 0 0 100 200 250 0 20 40 0 25 50 75 100 0 25 50 75 100 125 Ma ∼237 Ladinian ∼242 Middle Anisian Triassic Triassic 247.2 Olene- kian Lower 251.2 Induan 252.902 Chang- hsingian 254.14 Wuchia- Permian Lopingian pingian 259.1 Macrofossils sampled-in-bin Rangethrough Macrofossils Spore Mega- plants spores Macrofossils total Boundary crossers Sporomorphs Macrofossil species incl. genera Gymno- Micro-/ isospores Sporomorph sampled-in-bin sperms Sporomorph total Pollen Fig. 1 Diversity indices and distribution of data entries per stage. Results for sporomorphs and plant macrofossil taxa from the Wuchiapingian to the Ladinian 2 NATURE COMMUNICATIONS | (2019) 10:384 | https://doi.org/10.1038/s41467-018-07945-w | www.nature.com/naturecommunications NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-018-07945-w ARTICLE Macrofossil Sporomorph macrofossil Sporomorph Single-stage genus genus genus genus genera turnover turnover turnover turnover rates per Myr rates per Myr 0 20 40 60 80 0 20 40 60 80 0 20 40 60 0 20 40 60 80 100 0 20 40 Ma ∼242 Anisian Middle 247.2 Triassic Olene- kian Lower 251.2 Induan 252.902 Chang- P. Lop. hsingian 254.14 Extinctions Originations Turnover Sporomorphs Macrofossils Fig. 2 Origination, extinction, turnover and single-stage genera. Counts and rates per million years stage duration for plant macro- and microfossils. P. = Permian, Lop. = Lopingian Normalized Estimated SQS: SQS: genus diversity sampling coverge macrofossil sporomorph (Good's u) genera genera 0 100 200 250 0 50 150 0.0 0.2 0.4 0.6 0.8 1.0 10 20 30 40 50 0 10 20 30 40 50 60 Ma ∼237 Ladinian ∼242 Middle Anisian Tr iassic Tr 247.2 Olene- kian Lower 251.2 Induan 252.902 Chang- hsingian 254.14 Wuchia- Permian pingian Lopingian 259.1 Sporomorphs Macrofossils Fig. 3 Normalized genus diversity, sampling coverage and shareholder quorum subsampling. Shareholder quorum subsampling (SQS) uses ‘sqsbyref’ function (with: quorum = 0.4, trials = 500, sample.quota = 5, merge.repeats = TRUE; see methods), showing median line and 95% confidence interval trends, but with a mostly (except for the Wuchiapingian) higher macrofossil diversity (Fig. 1), which is expected due to the generally diversity and less pronounced decline at the Permian–Triassic higher preservation potential of sporomorphs, their transportability boundary (Figs. 4, 5a). The differences are explainable by the use of by wind and water even from distant habitats to favourable deposi- different sources, updated taxonomy and dating, while the two tional settings, their sheer abundance and the possibility of a single datasets clearly have a common underlying structure. plant species to produce multiple spore or pollen taxa. The Plant macrofossil family diversity shows trends similar to genus Wuchiapingian record presents an exception with the number of diversity but with the peculiarity of a distinct decline between the sampled-in-bin species and generabeingslightlylowerforspor- Anisian and Ladinian, which contrasts with the trends seen
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