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Brachiopods and forams reduced calcification costs through morphological simplification during mass extinction events

Nature Ecology & Evolution volume 9, pages 1456–1468 (2025)Cite this article

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Abstract

Environmental stressors have exacerbated the collapse of marine ecosystems during mass extinctions. However, the survival strategies of marine species during mass extinctions remain unclear. Here, we investigated morphological evolution of brachiopods across the Permian–Triassic mass extinction (PTME) using a database of 3,225 specimens representing 1,061 species and foraminifera across the PTME and early Toarcian oceanic anoxic event (T-OAE) using a database of 757 specimens representing 12 species. We found a significant reduction in the number and proportion (plicae length/shell length) of shell plicae of brachiopods (36.4% and 60.0%, respectively) across the PTME and a significant decrease in the shell thickness of foraminifera (18.9% and 42.4% across the PTME and 36.9–61.8% across the T-OAE). We calculated that these adaptive strategies could reduce the energetic costs of calcification by more than half for brachiopods across the PTME, and by ~20–62% for foraminifera across the PTME and T-OAE, to compensate for the elevated cost of calcification due to environmental and ecological pressures. We propose that simplification of morphological features, such as reduced shell ornamentation and shell thinning, serves as a potential economic strategy for calcifying organisms to cope with extinction events by reducing energy demands, but further studies with a broader range of taxa and extinction events are needed to confirm the generality of this bioenergetic strategy.

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Fig. 1: Species-level plicae distribution of brachiopods and energy of calcification in response to the PTME.
Fig. 2: Shell thickness of foraminifera in response to the PTME and T-OAE.
Fig. 3: Energy of calcification of foraminifera in response to the PTME and T-OAE.
Fig. 4: Ocean acidification events and global average temperature during the last 300 Myr.

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Data availability

All data supporting the findings of this study are available within the article, Extended Data Figs. 1–5, Extended Data Tables 1–5 and Supplementary Information. Source data are provided with this paper.

Code availability

The code needed to run the cGENIE model is available via Github at https://github.com/derpycode/cgenie.muffin and additional configuration codes to replicate the model results are available via Zenodo at https://doi.org/10.5281/zenodo.14169287 (ref. 107).

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Acknowledgements

This study was supported by the National Natural Science Foundation of China (42325202, 42072010, 92155201, 92255303), State Key R&D Project of China (2023YFF0804000), Natural Science Foundation of Hubei (2023AFA006) and the Fundamental Research Funds for the Central Universities, China University of Geosciences (Wuhan).

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Authors and Affiliations

  1. State Key Laboratory of Geomicrobiology and Environmental Changes, School of Earth Sciences, China University of Geosciences, Wuhan, China

    Fengyu Wang, Jacopo Dal Corso, Yuyang Wu, Shouyi Jiang, Li Tian, Xu Dai, Daoliang Chu, Huyue Song, Jinnan Tong & Haijun Song

  2. Department of Integrative Biology, University of California, Berkeley, CA, USA

    Seth Finnegan

  3. School of Earth, Atmospheric and Life Sciences, Faculty of Science, Medicine and Health, University of Wollongong, Wollongong, New South Wales, Australia

    Facheng Ye

  4. Yifu Museum, China University of Geosciences, Wuhan, China

    Jing Chen

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F.W. and Haijun Song designed the research. F.W. collected brachiopod data. Haijun Song, J.T. and S.J. provided modern brachiopods and Permian, Triassic and Jurassic foraminifera data. F.W., Haijun Song, X.D. and Y.W. analysed the data. F.W., Haijun Song, S.F., J.D.C., Y.W. and X.D. discussed the data. F.W. and Haijun Song wrote the paper with input from all authors. F.W., Haijun Song, S.F., J.D.C., F.Y., Y.W., X.D., S.J., J.C., L.T., D.C., Huyue Song and J.T. further revised the original manuscript.

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Correspondence to Haijun Song.

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Nature Ecology & Evolution thanks Nicholas Hebdon, Pedro Monarrez and Anshuman Swain for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Relationships between shell mass and the number and proportion of plicae.

Different colors and shapes of symbols represent shells with different proportions of Plicae. PP represents the proportion of plicae.

Source data

Extended Data Fig. 2 Relationships between shell length and shell thickness and change in shell thickness of foraminifera during the PTME and T-OAE.

a, Scaling relationship of Diplosphaerina inaequalis. b, Shell thickness of D. inaequalis. c, Scaling relationship of Globivalvulina lukachiensis. d, Shell thickness of G. lukachiensis. e, Scaling relationship of Siphovalvulina colomi. f, Shell thickness of S.a colomi. g, Scaling relationship of Siphovalvulina gibraltarensis. h, Shell thickness of S. gibraltarensis. i, Scaling relationship of Glomospira tetragona. j, Shell thickness of G. tetragona. k, Scaling relationship of Glomospira tingriensis. l, Shell thickness of G. tingriensis. m, Scaling relationship of Glomospira sinensis. n, Shell thickness of G. sinensis. o, Scaling relationship of Glomospirella pavida. p, Shell thickness of G. pavida. q, Scaling relationship of Textularia dollfussi. r, Shell thickness of T. dollfussi. s, Scaling relationship of Mesoendothyra croatica. t, Shell thickness of M. croatica. u, Scaling relationship of Valvulina triangularis. v, Shell thickness of V. triangularis. w, Scaling relationship of Duotaxis birmanica. x, Shell thickness of D. birmanica. The shaded area around the regression curve represents the 95% confidence interval. Statistical test: two-sided Mann–Whitney U -test. Each boxplot displays the 25th percentile, median, and 75th percentile, with whiskers extending to the 5th and 95th percentiles.

Source data

Extended Data Fig. 3 Species-level distribution of percentage of calcium shell mass of living brachiopods and bivalves.

The percentage of calcium shell mass is calculated from the ratio of ash-free dry mass to total dry mass. All data collected from published literatures. Each boxplot displays the 25th percentile, median, and 75th percentile, with whiskers extending to the 5th and 95th percentiles.

Source data

Extended Data Fig. 4 Illustration of statistical indicators.

a, Brachiopoda, NP, the number of plicae; PP, the proportion of plicae; L1, the length of plicae; L2, the length of ventral or dorsal valve; PHP, the relative height of plicae; H1, the maximum height of plicae; H2, the height of shell. b, Foraminifera, ST, shell thickness, L, shell length, RST, relative shell thickness.

Extended Data Fig. 5 The relationship between the number of plicae and the relative height of plicae.

Red dashed line represents regression line, which is plotted for all species in the Changhsingian.

Source data

Extended Data Table 1 Marine organisms adopted the reduced shell ornamentation and thinned the shell during the Mesozoic and Cenozoic environmental crises109
Full size table
Extended Data Table 2 Shell organic content of living brachiopods under normal and acidified culture conditions
Full size table
Extended Data Table 3 Akaike Information Criterion (AIC) score of the regression analysis between shell length and shell thickness of foraminifera across the PTME and T-OAE
Full size table
Extended Data Table 4 Interaction analysis tests the slope of and ANOVA goodness-of-fit test of the foraminiferal regression equation across the PTME and T-OAE
Full size table
Extended Data Table 5 Calcification energy of brachiopods across the PTME
Full size table

Supplementary information

Source data

Source Data Fig. 1 (download XLSX )

Source data of brachiopod plicae and calcification energy.

Source Data Fig. 2 (download XLSX )

Source data of foraminiferal relative shell thickness.

Source Data Fig. 3 (download XLSX )

Source data of foraminiferal calcification energy.

Source Data Extended Data Fig. 1 (download XLSX )

Source data of simulated shell mass of brachiopods.

Source Data Extended Data Fig. 2 (download XLSX )

Source data of foraminiferal shell length and thickness.

Source Data Extended Data Fig. 3 (download XLSX )

Source data of calcium shell mass of living brachiopods and bivalves.

Source Data Extended Data Fig. 5 (download XLSX )

Source data of brachiopod plicae during the Changhsingian.

Source Data Extended Data Table 2 (download XLSX )

Source data of living brachiopod microstructure.

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Wang, F., Finnegan, S., Dal Corso, J. et al. Brachiopods and forams reduced calcification costs through morphological simplification during mass extinction events. Nat Ecol Evol 9, 1456–1468 (2025). https://doi.org/10.1038/s41559-025-02749-w

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