An explanation for conflicting records of Triassic–Jurassic plant diversity Luke Mandera,1, Wolfram M. Kürschnerb, and Jennifer C. McElwaina aSchool of Biology and Environmental Science, University College Dublin, Belfield, Dublin 4, Ireland; and bSection Palaeoecology, Laboratory of Palaeobotany and Palynology, Utrecht University, Budapestlaan 4, 3584 CD Utrecht, The Netherlands Edited by Paul E. Olsen, Columbia University, Palisades, NY, and approved July 15, 2010 (received for review March 30, 2010) Macrofossils (mostly leaves) and sporomorphs (pollen and spores) efforts to decipher the causes of mass extinctions and also ques- preserve conflicting records of plant biodiversity during the end- tions the extent to which plants are more persistent than animals Permian (P-Tr), Triassic–Jurassic (Tr-J), and end-Cretaceous (K-T) in the face of global change. Additionally, these observations mass extinctions. Estimates of diversity loss based on macrofossils raise doubts about the potential of the fossil record to provide are typically much higher than estimates of diversity loss based on accurate and consistent data on the response of terrestrial vege- sporomorphs. Macrofossils from the Tr-J of East Greenland indicate tation to episodes of major environmental change, which raises that standing species richness declined by as much as 85% in the doubts about the utility of the fossil record as a source of infor- Late Triassic, whereas sporomorph records from the same region, mation from which we can augment our understanding and man- and from elsewhere in Europe, reveal little evidence of such cata- agement of the current climate and biodiversity crises. To explore strophic diversity loss. To understand this major discrepancy, this issue, we have investigated the macrofossil and sporomorph we have used a new high-resolution dataset of sporomorph assem- records of vegetation change during the Triassic–Jurassic mass blages from Astartekløft, East Greenland, to directly compare the extinction (Tr-J; ∼200 Ma). macrofossil and sporomorph records of Tr-J plant biodiversity. Our The Tr-J coincided with massive volcanism associated with the results show that sporomorph assemblages from the Tr-J boundary opening of the Atlantic Ocean (13–15), which led to a four-fold interval are 10–12% less taxonomically diverse than sporomorph increase in atmospheric CO2 levels (16) and a consequent rise in assemblages from the Late Triassic, and that vegetation composi- global temperatures of between 3 and 6 °C (16–18). Compilations GEOLOGY tion changed rapidly in the boundary interval as a result of emigra- of stratigraphic ranges of animal taxa indicate that 23% of marine tion and/or extirpation of taxa rather than immigration and/or families (5), 63% of marine invertebrate genera (19), and 22% of origination of taxa. An analysis of the representation of different terrestrial families suffered extinction at this time (5). In contrast, plant groups in the macrofossil and sporomorph records at Astar- family-level compilations of plant diversity indicate that only the tekløft reveals that reproductively specialized plants, including cy- Peltaspermaceae, a clade of seed-ferns, was lost from the Earth’s cads, bennettites and the seed-fern Lepidopteris are almost absent biota at the Tr-J (e.g., ref. 9). Investigations of macrofossils in from the sporomorph record. These results provide a means of Jameson Land, East Greenland, have shown a genus-level extinc- ECOLOGY reconciling the macrofossil and sporomorph records of Tr-J vegeta- tion rate of ∼17% and have revealed that standing species rich- tion change, and may help to understand vegetation change dur- ness across the region declined by ∼85% at the Tr-J (20, 21). ing the P-Tr and K-T mass extinctions and around the Paleocene– Plants with specialized reproductive biology (insect pollinated) Eocene Thermal Maximum. were among those taxa at greatest risk of extinction or extirpation (21), and relative abundance distributions of macrofossil genera extinction ∣ palaeobotany ∣ palynology ∣ taphonomy ∣ Triassic–Jurassic have shown that the pace of biodiversity loss in this region was abrupt rather than gradual (22). The Tr-J in the Newark Basin, North America, records a regional sporomorph diversity loss of ompilations of stratigraphic ranges of land plants through ∼60% Cgeological time do not show abrupt declines in taxonomic (23), but existing sporomorph records spanning the Tr-J in diversity (1–3). This contrasts sharply with the history of animal East Greenland, although qualitative, provide little evidence of life, which is marked by five geologically rapid decreases in global such catastrophic diversity loss (24, 25). There is also little evi- taxonomic diversity, known as mass extinctions (4, 5). This fun- dence for abrupt biodiversity loss in sporomorph records from damental difference between the evolutionary histories of plants nearby sections in Europe (e.g., ref. 26), where the Tr-J is char- and animals may be due to the persistence of higher plant taxa, acterized by compositional change (e.g., refs. 26 and 27). and has led to the suggestion that plants are more resistant to Using a new high-resolution dataset of sporomorph assem- mass extinction than animals (1, 6–9). Despite this, studies of fos- blages from a Tr-J section at Astartekløft, East Greenland, we sil plants during times of faunal mass extinction have revealed present a case study that offers broad insights into the tapho- extensive ecological disruption and decreased plant genus/species nomic processes causing discrepancies between the macrofossil diversity on local and regional scales (8, 9), suggesting that plants and sporomorph records of plants. Specifically, this study aims are not immune to the myriad environmental changes accompa- to provide (i) quantitative estimates of Tr-J terrestrial plant diver- sity at within- and among-sample scales; (ii) an assessment of the nying mass extinctions. However, plant fossils preserve conflicting records of diversity nature and timing of compositional change in the source vegeta- tion; and (iii) an analysis of the agreement between the macro- loss during these critical intervals in Earth history. Estimates of fossil and sporomorph records of the source vegetation. Our diversity loss based on macrofossils (mostly leaves) are typically results show that the sporomorph record does not preserve an much higher than estimates of diversity loss based on sporo- morphs (pollen and spores). The end-Permian mass extinction [P-Tr; ∼251 million years ago (Ma)] in Australia saw a 97% regio- Author contributions: L.M., W.M.K., and J.C.M. designed research; L.M., W.M.K., and J.C.M. nal diversity loss of macrofossils but a 19% loss of sporomorph performed research; L.M. analyzed data; and L.M. wrote the paper. diversity (8, 10), and the end-Cretaceous mass extinction (K-T; The authors declare no conflict of interest. ∼65 Ma) in North America resulted in a 70–90% diversity loss This article is a PNAS Direct Submission. of macrofossils but a 25–30% loss of sporomorph diversity (11, 1To whom correspondence should be addressed. E-mail: [email protected]. 12). These discrepancies present a barrier to understanding floral This article contains supporting information online at www.pnas.org/lookup/suppl/ change during episodes of faunal mass extinction. This hampers doi:10.1073/pnas.1004207107/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1004207107 PNAS Early Edition ∣ 1of6 Downloaded by guest on October 2, 2021 Downloaded by guest on October 2, 2021 fossils wereEarly recorded Jurassic (Hettangian) in agesents (Fig. situ the 1). topmost A from total upper of Rhaetian plant 2,898 and macro- plant beds beds 6 1 and 7 are of and sporomorphs were recorded from 40at productive samples 10 (Table 1 cmDataset intervals S1 within each plant bed and a total of 14,579 beds 1 bed 5 (following recommendations in ref. 32). Accordingly, plant Median records the highest median richnesscords in the the entire lowest section median (Fig.bed richness 1). 1 in to the plant section(Fig. 1). bed and Median 5 plant richness (Fig. declines bedSimpson through 7 1). the Plant Triassic from bed plant 6 (earliest Jurassic) re- ian and interquartile range.at Whiskers 301 counted represent sporomorphs, maximum and Simpson andref. 31). minimum. Box and whisker plotFig. of 1. rarefied within-sample sporomorph richness Floral Diversity and Composition. of the pollen morphospecies boundary at Astartekløft is approximatedJameson by Land, the first Eastfrom occurrence Greenland eight (Fig. horizons 1 richThe in macrofossils and plant and ref. sporomorphs macrofossils analyzedResults 21). at here Astartekløft The were in collected Tr-J change. tween macrofossil andrecord, sporomorph and this records provides one ofLepidopteris explanation for Tr-J the vegetation discrepancy be- include cycadsin (28), the boundary interval. bennettites Reproductively specializedGreenland, (29, plants, which and that 30), the vegetationabrupt and changed loss composition of the rapidly terrestrial plant seed-fern biodiversity across the Tr-J in East 2of6 and bed 1 (Fig. 1). The(Fig. interquartile 1). ranges The of lowest within-sample richness richness (KW is no statistically significantsamples difference from each in plant median bed. within-sample Using a Kruskal Dataset S2 D ∣ – Schematic sedimentary log of the Astartekløft section (adapted from Meters are large, demonstrating considerable variation within- 4 are of Late Triassic (Rhaetian) age, plant bed 5 repre- 10 20 30 40 50 60 70 ’ D s diversity index values ( www.pnas.org/cgi/doi/10.1073/pnas.1004207107 ). Rock samples for sporomorph analysis were taken Sand Plant Bed is lowest in plant bed 6 and highest in plant bed 7 (Kap Stewart Group)Triassic (Rhaetian) Jurassic (Hettangian) (21), are underrepresented in the sporomorph fossil ¼ ). 12 Mud 1 1.5 2 3 4 5 6 7 15 20 25 30 35 0.5 0.7 0.9 D . 319 values are recorded in samples from plant 6 Expected Richness Index Simpson’s ; 1 ; 4 ; 7 ; 6 Cerebropollenites thiergartii – ; 9 ; 3 ; D 4 ) fluctuate through the section Within-sample richness and ’ s diversity index.