Morphological Selectivity of the Permian-Triassic Ammonoid Mass

https://doi.org/10.1130/G48788.1

Manuscript received 5 January 2021 Revised manuscript received 30 March 2021 Manuscript accepted 1 April 2021

Morphological selectivity of the Permian-Triassic ammonoid mass extinction Xu Dai1, Dieter Korn2 and Haijun Song1* 1State Key Laboratory of Biogeology and Environmental Geology, School of Earth Sciences, China University of Geosciences, Wuhan 430074, China 2Museum für Naturkunde Berlin, Leibniz-Institut für Evolutions- und Biodiversitätsforschung, Invalidenstraße 43, 10115 Berlin, Germany

ABSTRACT lineages, episageceratids, xenodiscids, and otoc- Ammonoids suffered a diversity bottleneck during the Permian-Triassic mass extinction eratids (Wiedmann, 1973; Teichert and Roches- (PTME) and experienced a rapid diversification in the Early Triassic. However, the kinds of ter, 1986; Brayard et al., 2009). The PTME was ammonoids that were more likely to survive the PTME and that fueled subsequent diversi- thought to be nonselective in terms of ammonoid fication are still poorly known. We compiled a comprehensive morphological data set and conch morphology, because geometric ratios of used the nonmetric multidimensional scaling method to reveal the impact of the PTME on ammonoid conchs showed little change across the morphological selectivity of ammonoids. Our results show that postextinction taxa oc- the PTME (Villier and Korn, 2004; Korn et al., cupied a quite different morphospace when compared with the pre-extinction assemblages. 2013; Monnet et al., 2015). However, whether The survivors were mainly smooth and weakly ornamented forms, while the late Permian selectivity occurred on other morphological species were dominated by coarsely ornamented forms. Contrary to previously recognized characters, e.g., shell ornamentation and aper- nonselective patterns, these results suggest a morphological selectivity of the Permian-Triassic ture shape, was not clear. Shell ornamentation crisis. Newcomers in the Griesbachian were mainly compressed and smooth forms. This mor- and aperture shape are important morphologi- phological shift from the coarsely ornamented ammonoids dominating the Changhsingian to cal parameters because they may significantly the smooth ammonoids dominating the Griesbachian possibly suggests an ecological turnover affect hydrodynamic properties (Chamberlain of ammonoids during the PTME. and Westermann, 1976; Hebdon et al., 2020). In our study, we performed morphometric analy- INTRODUCTION The PTME was the most severe crisis in the ses based on a comprehensive morphological Can we predict which kinds of organisms are Phanerozoic; it killed more than 80% of marine data set encompassing 127 ammonoid species to more likely to survive extinctions? The answer species (Stanley, 2016; Fan et al., 2020). It coin- quantify the morphological evolution of ammo- would be quite different with regard to back- cided with large environmental and climatic noids across the Permian-Triassic boundary and ground and mass extinctions. For example, taxa upheavals; e.g., global warming and oceanic test the morphological selectivity of the PTME. with wide geographic ranges can buffer against anoxia (e.g., Song et al., 2012; Sun et al., 2012). background extinction, but not for mass extinc- Therefore, the PTME can provide an excel- DATA AND METHODS tions (Dunhill and Wills, 2015). Mass extinc- lent deep-time experiment for testing selective We compiled a discrete morphological data tions in geological history usually act as a ran- extinction patterns. The PTME affected both taxa set from published literature that contained 87 dom nonselective pattern, affecting different with wide and narrow geographic ranges without Changhsingian and 40 Griesbachian ammonoid clades simultaneously and globally (Payne and selectivity (Payne and Finnegan, 2007; Dai and species (Table S1 in the Supplemental Material 1), Finnegan, 2007). However, some clades with Song, 2020); it did not show obvious selectiv- covering all valid genera known in this interval. specific ecological traits show higher resilience ity on bivalves with different lifestyles, feeding Taxa in open nomenclature or with problematic to mass extinctions than others; for example, types, or habitats (Huang et al., 2014). How- classification were also included when they had physiologically buffered groups were less ever, the PTME exhibited strong selectivity on a distinct morphology. We portioned the Gries- affected by the Permian-Triassic mass extinc- other specific groups and ecological traits; e.g., bachian ammonoids into two groups: survivors tion (PTME) than unbuffered groups (Bam- marine invertebrates had much higher extinc- and newcomers. Survivors were defined as initial bach et al., 2002). Greater understanding of the tion rates than chondrichthyan fishes (Vázquez postextinction species belonging to the surviving selectivity of mass extinctions can shed light on and Clapham, 2017). The degree of selectivity families and superfamilies; i.e., Otocerataceae, extinction mechanisms and predict the extinc- was thus highly variable among different clades, Episageceratidae, and Xenodiscidae (Wiedmann, tion risk of living species. ecological traits, and geographic ranges. 1973; Teichert and Rochester, 1986). Newcom- Ammonoids suffered a diversity bottleneck ers were all derived species and representatives *E-mail: [email protected] during the PTME, with the survival of only three of the newly originated families after the PTME;

1Supplemental Material. Figures S1 and S2, and Tables S1 and S2. Please visit https://doi.org/10.1130/GEOL.S.14582730 to access the supplemental material, and contact [email protected] with any questions.

CITATION: Dai, X., Korn, D., and Song, H., 2021, Morphological selectivity of the Permian-Triassic ammonoid mass extinction: Geology, v. 49, p. 1112–1116, https:// doi.org/10.1130/G48788.1

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Downloaded from http://pubs.geoscienceworld.org/gsa/geology/article-pdf/49/9/1112/5387032/g48788.1.pdf by guest on 25 September 2021 tabulate venter rounded venter

Figure 1. Representa- tives of Changhsingian and Griesbachian ammonoids and their typical shell ornamentations. (A,B) Pseudotirolites acu- ticostatus from the Dalong Formation (Changhsin- gian), Guizhou, China. (C,D) Pseudogastrio- ceras szechuanense ventral keel striation from the Dalong Forma- C D tion (Changhsingian), Sichuan, China. (E) A B Tapashanites floriformis from the Dalong Forma- nodes width (W) tion (Changhsingian), Sichuan, China. (F,G) Vish- nuites pralambha from the lower Daye Formation (H) (Griesbachian), Guizhou, ) H I China. (H,I) Anotoceras nala from the lower Daye (D

height Formation (Griesbachian), ribs Guizhou, China. (J,K) Ophiceras tibeticum from the lower Kangshare For- mation (Griesbachian), diameter South Tibet, China.

umbilical E diameter (U) 5 cm F G J K

i.e., Ophiceratidae, Proptychidae, Mullericerati- method is based on a two-dimensional morpho- sampling biases for SOV and SOR. We set a null dae, and a family incertae sedis species Anoto- space. It can be quantified by three parameters: hypothesis simulation wherein, given a random ceras nala. sum of range (SOR), sum of variance (SOV), extinction of species with 10,000 replicates, the Morphological characteristics employed and position of centroid (POC). Three theoreti- number of survivors is the same as the number in our study were based on the analysis by cal modes of extinction can lead to reductions in of empirical survivors. Then, we compared the McGowan and Smith (2007) with some modi- morphological disparity: random, marginal, and change of the centroid positions between the fications (see Table S2). These characteristics lateral extinctions. At the same extinction mag- null hypothesis and empirical survivors. The encompass conch geometry, ornamentation, nitude, SOR and SOV will show the smallest distance between the centroids was calculated shape of the aperture and ontogeny (Fig. 1). decrease in random extinction mode, an inter- by Euclidean distance using their two NMDS Size was not included in this analysis because mediate decrease in lateral extinction mode, coordinates. The simulations were performed ammonoid shells were usually damaged dur- and the largest reduction in marginal extinction using R version 3.5.3 (https://cran.r-project.org/ ing postmortem transportation and taphonomic mode; POC will not show prominent changes in bin/windows/base/old/3.5.3/). processes. We usually coded the studied spe- random and marginal modes, but it will exhibit cies based on its holotype, when it was well remarkable change in lateral mode. RESULTS preserved. Non-holotype specimens were used We used the nonmetric multidimensional The morphospace of the Changhsingian in case of incomplete preservation of the holo- scaling (NMDS) method to construct an ammo- and Griesbachian ammonoids showed signifi- type. Intraspecific variation was not considered noid morphospace, because this is widely cant differences (Fig. 2A). The one-way per- here owing to three reasons: (1) most of the adopted for analyzing discrete morphological mutational multivariate analysis of variance studied species were described on the basis of data. Two distance metrics (i.e., Euclidean and (PERMANOVA) test of their morphological a few specimens; (2) adding more specimens of Gower) were used to calculate pairwise distances characters also showed significant differences well-sampled species will cause strong sampling in PAST 3.0 software (Hammer et al., 2001). (p << 0.001). The Changhsingian ammonoids biases, which will misrepresent the centroid of The performance of NMDS based on the Euclid- are mainly concentrated on the left side, repre- related morphospace; and (3) intraspecific varia- ean distance matrix (stress value = 0.157) was sented by coarsely ornamented species, while tion is usually less than interspecific variation better than the Gower distance matrix (stress the Griesbachian ammonoids are mainly clus- (Tanabe et al., 2003), and thus has little effect value = 0.216). Our analysis was therefore tered on the right side, dominated by smooth on the holistic morphospace. mainly based on the Euclidean distance matrix. forms. Both the SOR and SOV of the Gries- We adopted the extinction space method Morphological diversity was calculated as the bachian ammonoids are smaller than the SOR (Korn et al., 2013) to quantify the morphological SOV and the SOR on the two NMDS axes. The and SOV of the Changhsingian ammonoids evolution of ammonoids during the PTME. This bootstrap method was adopted to test the effect of (Figs. 3A and 3B).

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Downloaded from http://pubs.geoscienceworld.org/gsa/geology/article-pdf/49/9/1112/5387032/g48788.1.pdf by guest on 25 September 2021 0.2 A B Figure 2. Ammonoid morphospaces and distances 0.1 2000 between centroids based on Euclidean distance

y matrix. (A) Morphospaces of Changhsingian and 0.0 Griesbachian ammo-

1000 noids. (B) Distribution of

Frequenc distances between null

NMDS DIM2 -0.1 hypothesis simulation 1 (random extinction with 40 survivors) and Chang- -0.2 0 hsingian centroid. Blue All Changhsingian species (n = 87) 0.00 0.05 0.10 0.15 arrow is the empirical dis- All Griesbachian species (n = 40) Distance tance between centroids of Changhsingian and -0.2 -0.1 0.00.1 0.2 Griesbachian species. (C) NMDS DIM1 Morphospaces of Chang- hsingian ammonoids, 0.2 C D survivors and newcomers. (D) Distribution of distances between null

0.1 800 hypothesis simulation 2 (random extinction with 12 survivors) and Chang- y hsingian centroid. Blue 0.0 arrow is the empirical dis-

400 tance between centroids of Changhsingian species Frequenc

NMDS DIM2 -0.1 and survivors. Red lines indicate 95% quantile. White symbols in A and All Changhsingian species (n = 87) 0 -0.2 0.00 0.05 0.10 0.15 C are the centroid of each Survivors (n = 12) group. NMDS—nonmetric Newcomers (n = 28) Distance multidimensional scaling; DIM1—dimension 1; -0.2 -0.1 0.00.1 0.2 DIM2—dimension 2. NMDS DIM1

0.012 0.6 A B 0.010 0.5 Figure 3. (A,B) Dispar- 0.008 0.4 ity of all Changhsingian species, survivors, new- 0.006 0.3 comers, and all 0.004 0.2 Griesbachian species. Vertical bars represent Sum of rang e

Sum of varianc e 0.002 0.1 95% confidence inter- vals. (C) Morphospace 0.000 0.0 of the Changhsingian All Changhsingian species (n=87) Newcomers (n=28) ammonoids and three Survivors (n=12) All Griesbachian species (n=40) earliest postextinction representative species 0.2 C D of each surviving lineage. NMDS—nonmetric multidimensional scal- 0.1 ing; DIM1—dimension 1;

40 0 DIM2—dimension 2. (D) Histogram of distance 0.0 between centroids of Changhsingian ammonoids and random 20 0

Frequency survivors (n = 3). Blue

NMDS DIM2 -0.1 arrow indicates the distance between Chang-

0 hsingian species and All Changhsingian species (n = 85) -0.2 0.00 0.05 0.10 0.15 0.20 representative species of Representatives of surviving each surviving lineage. lineages (n = 3) Distance Red line indicates 90% quantile. -0.2 -0.1 0.00.1 0.2 NMDS DIM1

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Downloaded from http://pubs.geoscienceworld.org/gsa/geology/article-pdf/49/9/1112/5387032/g48788.1.pdf by guest on 25 September 2021 Compared with the overall Changhs- et al., 2013). In contrast to previous studies, Gower distance were very similar to the Euclid- ingian ammonoid morphospace, the mor- our new results reveal that the survivors and ean distance (Fig. 4A). The significantly selec- phospace of the survivors is significantly all Griesbachian ammonoid species exhibit tive signal also exists in this analysis (p = 0.002; reduced (Fig. 2C), reflecting differences in significantly lower disparity than those in the Fig. 4B). their morphological characters (one-way Changhsingian. Suture lines were not included In our data set, the two species O. concavum PERMANOVA test, p = 0.01). Survivors in this study, but previous studies documented and H. triviale have uncertain age constraints. predominately belong to smooth or weakly a significant drop in mean suture line complex- Their occurrences are probably younger than ornamented morphotypes. The SOV of survi- ity, associated with eliminations of the most the diverse Changhsingian assemblages from vors does not decrease remarkably, because complex and simplest suture lines during the South China and Transcaucasia but older than the survivors belong to morphologically dis- PTME (Saunders et al., 1999). This extinction the typical earliest Griesbachian assemblage. tinct clades. Their SOR shows a significant modality in ammonoid suture lines fits with Unfortunately, their stratigraphic correlation reduction (Figs. 3A and 3B). Newcomers are the marginal selective extinction mode (Korn with the conodont biostratigraphy is not highly mainly smooth and compressed forms, when et al., 2013). resolved (Orchard and Tozer, 1997). Regardless compared with Changhsingian ammonoids If we compare all Griesbachian species or of whether they were treated as Changhsingian (one-way PERMANOVA test, p << 0.001; species in surviving families/superfamilies with or Griesbachian species, the results were very Fig. 2C). SOR and SOV of newcomers are Changhsingian species to discuss selectivity, similar (Figs. S1 and S2). very low (Figs. 3A and 3B). some postextinction species are involved in The morphological shift from the Chang- The centroid of the Griesbachian ammonoids the analysis. This does influence the discussion hsingian coarsely ornamented ammonoids to is far away from the Changhsingian ammonoid of selectivity, since selective extinction only the Griesbachian smooth ammonoids may centroid (Fig. 2A), and their distance in the relates to pre-extinction taxa. Another potential reflect an ecological turnover. The relation- morphospace is ∼0.072, which is significantly problem is the huge magnitude of the PTME, ship between ammonoid conch morphol- larger than the null hypothesis simulation (p which killed nearly all ammonoids, with only ogy and their life mode has received a lot << 0.001; Fig. 2B). The survivors also have three lineages surviving (Wiedmann, 1973; of attention (Chamberlain and Westermann, a significantly distant centroid ∼( 0.047) com- Teichert and Rochester, 1986; Brayard et al., 1976; Jacobs, 1992; Klug et al., 2016; Heb- pared to the Changhsingian species (p = 0.031; 2009). For a maximal reduction of the recov- don et al., 2020). However, due to the lack of Fig. 2D). Therefore, a nonselective extinction ery effect and fitting with the huge magnitude preservation of their soft body, our understand- mode is rejected. Our new results support a lat- of the PTME, we used three species, the oldest ing of their ecology is still incomplete (Naglik eral selective extinction. postextinction representative of each surviving et al., 2015). The loss of coarsely ornamented lineage, i.e., Otoceras concavum, Episageceras ammonoids during the PTME suggests that DISCUSSION dalailamae, and Hypophiceras triviale, for a they were more vulnerable to environmental Our results reveal a lateral morphologi- test. The distance between their centroid and perturbations, e.g., warming and anoxia (e.g., cal selective mode for the PTME. Species the centroid of the Changhsingian species was Sun et al., 2012; Song et al., 2012). Another with weak ornamentation or smooth shells larger than the mean shift of random survival possible explanation is phenotypic response were more likely to survive. Villier and Korn of three species (p = 0.084; Figs. 3C and 3D). to environmental stress, but clear evidence (2004) did not detect remarkable differences Therefore, a selective extinction model is sup- is lacking. Changhsingian ammonoids from between the morphospaces of Changhsin- ported at species, family/superfamily, and Iran exhibited ornament simplification and size gian and Griesbachian ammonoid conchs; whole-stage levels. reduction prior to the PTME (Kiessling et al., their results suggested that the postextinction To test the robustness of our analysis, we 2018), which may suggest that being smooth assemblage shows slightly increased SOR used an alternative distance metric (Gower dis- can be an effective survival strategy under and SOV. Subsequent works showed that tance) to rerun the same analysis. Except for environmental stress. It is noted that more data Griesbachian ammonoids had low diversity more overlap between the morphospaces of sur- are needed to test this pre-PTME morphologi- but high disparity (McGowan, 2004; Brosse vivors and newcomers, the results based on the cal change. During the late Smithian crisis,

Figure 4. Ammonoid morphospaces and distances between centroids based A B on the Gower distance 0.1 matrix. (A) Morphospaces 00 of Changhsingian ammonoids, survivors, and newcomers. White sym- 0.0 bols are the centroid of each group. (B) Distribu- tion of distances between 40 0 null hypothesis simulation NMDS DIM2 -0.1 Frequency 2 (random extinction with 12 survivors) and Chang- hsingian centroid. Blue All Changhsingian species (n = 87) 08 arrow is the empirical dis- -0.2 Survivors (n = 12) 0.00 0.05 0.10 0.15 tance between centroids Newcomers (n = 28) Distance of Changhsingian species and survivors. Red -0.2 -0.1 0.00.1 line indicates 95% quantile. NMDS—nonmetric NMDS DIM1 multidimensional scaling; DIM1—dimension 1; DIM2—dimension 2.

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Downloaded from http://pubs.geoscienceworld.org/gsa/geology/article-pdf/49/9/1112/5387032/g48788.1.pdf by guest on 25 September 2021 which was a secondary extinction event in nament: Paleobiology, v. 2, p. 316–331, https:// Orchard, M.J., and Tozer, E.T., 1997, Triassic con- the Triassic (Stanley, 2009), spherical ammo- doi.org/10.1017/S0094837300004954. odont biochronology, its calibration with the noids disappeared (Brosse et al., 2013). The Dai, X., and Song, H., 2020, Toward an understanding ammonoid standard, and a biostratigraphic of cosmopolitanism in deep time: A case study summary for the Western Canada Sedimentary loss of spherical forms also happened during of ammonoids from the middle Permian to the Basin: Bulletin of Canadian Petroleum Geolo- the Triassic-Jurassic mass extinction (Smith Middle Triassic: Paleobiology, v. 46, p. 533–549, gy, v. 45, p. 675–692, https://doi.org/10.35767/ et al., 2014). 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Jacobs, D.K., 1992, Shape, drag, and power in ammo- and conodonts for multiple Early Triassic noid swimming: Paleobiology, v. 18, p. 203–220, mass extinctions: Proceedings of the National ACKNOWLEDGMENTS https://doi.org/10.1017/S009483730001397X. Academy of Sciences of the United States of We acknowledge Michael J. Benton and Li Tian for Kiessling, W., Schobben, M., Ghaderi, A., Hairape- America, v. 106, p. 15264–15267, https://doi teaching morphometric methods during the short tian, V., Leda, L., and Korn, D., 2018, Pre–mass .org/10.1073/pnas.0907992106. course in Wuhan (China) in 2019. We thank Kath- extinction decline of latest Permian ammo- Stanley, S.M., 2016, Estimates of the magni- leen Ritterbush, Matthew E. Clapham, Christian noids: Geology, v. 46, p. 283–286, https://doi tudes of major marine mass extinctions in Klug, and an anonymous reviewer for their construc- .org/10.1130/G39866.1. Earth history: Proceedings of the National tive suggestions. This research was funded by the Klug, C., De Baets, K., and Korn, D., 2016, Explor- Academy of Sciences of the United States of National Natural Science Foundation of China (grant ing the limits of morphospace: Ontogeny and America, v. 113, p. E6325–E6334, https://doi 41821001), the State Key R&D Project of China (grant ecology of late Viséan ammonoids from the .org/10.1073/pnas.1613094113. 2016YFA0601100), the Strategic Priority Research Tafilalt (Morocco): Acta Palaeontologica Po- Sun, Y., Joachimski, M.M., Wignall, P.B., Yan, C., Program of Chinese Academy of Sciences (grant lonica, v. 61, p. 1–14, https://doi.org/10.4202/ Chen, Y., Jiang, H., Wang, L., and Lai, X., 2012, XDB26000000), and the Fundamental Research app.00220.2015. Lethally hot temperatures during the Early Tri- Funds for National University, China University of Korn, D., Hopkins, M.J., and Walton, S.A., 2013, assic greenhouse: Science, v. 338, p. 366–370, Geosciences (Wuhan), and the Deutsche Forschun- Extinction space—A method for the quan- https://doi.org/10.1126/science.1224126. gsgemeinschaft (Ko1829/18–1 and FOR 2332). This is tification and classification of changes in Tanabe, K., Landman, N.H., and Yoshioka, Y., 2003, Center for Computational and Modeling Geosciences morphospace across extinction boundaries: Intra- and interspecific variation in the early in- (BGEG) publication 4. Evolution, v. 67, p. 2795–2810, https://doi ternal shell features of some Cretaceous ammo- .org/10.1111/evo.12162. noids: Journal of Paleontology, v. 77, p. 876–887, REFERENCES CITED McGowan, A.J., 2004, Ammonoid taxonomic and https://doi.org/10.1017/S0022336000044735. 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