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Predator mass mortality events restructure food webs through trophic decoupling

Nature volume 626, pages 335–340 (2024)Cite this article

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Abstract

Predators have a key role in structuring ecosystems1,2,3,4. However, predator loss is accelerating globally4,5,6, and predator mass-mortality events7 (MMEs)—rapid large-scale die-offs—are now emblematic of the Anthropocene epoch6. Owing to their rare and unpredictable nature7, we lack an understanding of how MMEs immediately impact ecosystems. Past predator-removal studies2,3 may be insufficient to understand the ecological consequences of MMEs because, in nature, dead predators decompose in situ and generate a resource pulse8, which could alter ensuing ecosystem dynamics by temporarily enhancing productivity. Here we experimentally induce MMEs in tritrophic, freshwater lake food webs and report ecological dynamics that are distinct from predator losses2,3 or resource pulses9 alone, but that can be predicted from theory8. MMEs led to the proliferation of diverse consumer and producer communities resulting from weakened top-down predator control1,2,3 and stronger bottom-up effects through predator decomposition8. In contrast to predator removals alone, enhanced primary production after MMEs dampened the consumer community response. As a consequence, MMEs generated biomass dynamics that were most similar to those of undisturbed systems, indicating that they may be cryptic disturbances in nature. These biomass dynamics led to trophic decoupling, whereby the indirect beneficial effects of predators on primary producers are lost and later materialize as direct bottom-up effects that stimulate primary production amid intensified herbivory. These results reveal ecological signatures of MMEs and demonstrate the feasibility of forecasting novel ecological dynamics arising with intensifying global change.

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Fig. 1: Food-web biomass responses to predator removals, resource pulses and MMEs.
Fig. 2: Community-wide biomass, density and functional trait responses to predator removals, resource pulses and MMEs.
Fig. 3: Distinct zooplankton and microalgal community biomass trajectories after predator removals, resource pulses and MMEs.

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Data availability

All data for analyses are available at a permanent Zenodo repository (https://doi.org/10.5281/zenodo.10070514). Source data are provided with this paper.

Code availability

All code for analyses is available at a permanent Zenodo repository (https://doi.org/10.5281/zenodo.10070514).

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Acknowledgements

We thank the staff at the Arkansas Game and Fish Commission and University of Arkansas Facilities and Agricultural Facilities, A. J. Alverson, J. D. Willson, E. Ruck, T. Nakov, J. Boyko, K. Smith, A. Ingram, W. Boys and M. Gómez-Llano for helping with the study; M. Cordellier, M. Crook, M. Dahirel, H. N. Eyster, C. Gross, M. Kodis and S. A. Muñoz-Gómez for contributing to PhyloPic. S.P.T. was supported in part by the NSF (GRFP 1842401). S.B.F. was supported by NSF DEB 1856415 and 2236526. J.P.G. was supported by DOE BER DE-SC0020362, NSF DEB 2224819 and Simons Foundation Early Career Fellowship in Microbial Ecology and Evolution LS-ECIAMEE-00001588. A.M.S. was supported by NSF DEB 1748945 and 2306183.

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Authors and Affiliations

  1. Department of Biological Sciences, University of Arkansas, Fayetteville, AR, USA

    Simon P. Tye & Adam M. Siepielski

  2. Department of Biology, Reed College, Portland, OR, USA

    Samuel B. Fey

  3. Department of Biology, Duke University, Durham, NC, USA

    Jean P. Gibert

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  1. Simon P. Tye
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  2. Samuel B. Fey
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Contributions

S.P.T., S.B.F., J.P.G. and A.M.S. developed the idea and experimental approach. A.M.S. secured funding and supervised the project. S.P.T. conducted the experiment, compiled data and conducted analyses. S.P.T., S.B.F., J.P.G. and A.M.S. wrote the manuscript and contributed to revisions.

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Correspondence to Simon P. Tye or Adam M. Siepielski.

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Extended data figures and tables

Extended Data Fig. 1 Time series of mean zooplankton and microalgae density following ecological perturbations.

Mean density (ln[individuals/L]) of zooplankton (A) and microalgae (B) following predator mass mortality events (MMEs, light green), predator removals (light blue), and resource pulses (dark green), as well as the undisturbed system (control, dark blue). Points and lines indicate mean values and +/− 1 SE for each sampling period and treatment, with points jittered to reduce overlap within sample periods. Solid lines and shaded regions indicate model predictions and 95% confidence intervals, respectively. Relative to the control, MMEs (t11.42 = 7.51, p < 0.01), predator removals (t11.42 = 7.35, p < 0.01), and, to a lesser extent, resource pulses (t11.42 = 3.73, p < 0.01) increased mean zooplankton density. MMEs (t13.36 = −7.95, p < 0.01), predator removals (t13.36 = −5.28, p < 0.01), and, to a lesser extent, resource pulses (t13.36 = −2.43, p = 0.02) decreased mean microalgae density. Dashed lines indicate when perturbations were induced (i.e., live fish and/or fish carrion added and/or removed). Data were analysed from 355 biologically independent zooplankton samples (A) and microalgae samples (B) for a control (n = 96), predator removal (n = 80), resource pulse (n = 80), and MME (n = 99), respectively, from one experiment. General additive mixed model (GAMM, A-B).

Extended Data Fig. 2 Time series of mean zooplankton body size and microalgae biovolume following ecological perturbations.

Mean zooplankton body size (mm, A) and microalgae biovolume (ln[μm2], B) following predator mass mortality events (MMEs, light green), predator removals (light blue), and resource pulses (dark green), as well as the undisturbed system (control, dark blue). Points and lines indicate mean values and +/− 1 SE for each sampling period and treatment, with points jittered to reduce overlap within sample periods. Solid lines and shaded regions indicate model predictions and 95% confidence intervals, respectively. Relative to the control, MMEs (t8 = 8.42, p < 0.01), predator removals (t8 = 6.29, p < 0.01), and resource pulses (t8 = 4.99, p < 0.01) increased mean zooplankton body size. MMEs (t15.06 = 2.58, p = 0.02) and predator removals (t15.06 = 2.48, p = 0.02), but not resource pulses (t15.06 = 1.32, p = 0.19), increased mean microalgae biovolume. Dashed lines indicate when perturbations were induced (i.e., live fish and/or fish carrion added and/or removed). Data were analysed from 355 biologically independent zooplankton samples (A) and microalgae samples (B) for a control (n = 96), predator removal (n = 80), resource pulse (n = 80), and MME (n = 99), respectively, from one experiment. General additive mixed model (GAMM, A-B).

Extended Data Fig. 3 Time series of mean biomass across five major zooplankton families following ecological perturbations.

Zooplankton biomass (ln[μg/L]) of Bosminidae (A), Brachionidae (B), Cyclopoida (C), Cyprididae (D), and Daphniidae (E) following predator mass mortality events (MMEs, light green), predator removals (light blue), and resource pulses (dark green), as well the undisturbed system (control, dark blue). Points and lines indicate mean values and +/− 1 SE for each sampling period and treatment, with points jittered to reduce overlap within sample periods. Solid lines and shaded regions indicate model predictions and 95% confidence intervals, respectively. Relative to the control, MMEs increased mean biomass of Bosminidae (t8.36 = 5.74, p < 0.01; A), Brachionidae (t9.78 = 2.31, p = 0.02; B), Cyclopoida (t9.59 = 8.33, p < 0.01; C), Cyprididae (t15 = 2.98, p < 0.01; D), and Daphniidae (t9.34 = 9.31, p < 0.01; E). Predator removals increased mean biomass of Bosminidae (t8.36 = 2.70, p = 0.008; A), Cyclopoida (t9.59 = 10.49, p < 0.01; C) and Daphniidae (t9.34 = 8.84, p < 0.01; E). Resource pulses increased mean biomass of Cyclopoida (t9.59 = 8.42, p < 0.01; C), Cyprididae (t15 = 2.30, p = 0.01; D), and Daphniidae (t9.34 = 5.23, p < 0.01; E). Dashed lines indicate when perturbations were induced (i.e., live fish and/or fish carrion added and/or removed). Taxa silhouettes and their colours correspond with major zooplankton families as in main figures. Data were analysed from 355 biologically independent zooplankton samples (A-E) for a control (n = 96), predator removal (n = 80), resource pulse (n = 80), and MME (n = 99), respectively, from one experiment. General additive mixed model (GAMM, A-E).

Extended Data Fig. 4 Time series of mean biomass across five major microalgae phyla following ecological perturbations.

Microalgae biomass (ln[μg/L]) of Charophyta (A), Chlorophyta (B), Cyanobacteria (C), Dinoflagellata (D), and Euglenozoa (E) following predator mass mortality events (MMEs, light green), predator removals (light blue), and resource pulses (dark green), as well the undisturbed system (control, dark blue). Points and lines indicate mean values and +/− 1 SE for each sampling period and treatment, with points jittered to reduce overlap within sample periods. Solid lines and shaded regions indicate model predictions and 95% confidence intervals, respectively. Relative to the control, MMEs decreased mean biomass of Charophyta (t12.81 = −9.93, p < 0.01; A) and Dinoflagellata (t22.1 = −5.04, p < 0.01; D), and had relatively low mean Cyanobacteria biomass (t22.1 = −1.85, p = 0.07; C). Predator removals decreased mean biomass of Charophyta (t12.81 = −5.69, p < 0.01; A) and Dinoflagellata (t22.1 = −2.47, p = 0.01; D). Resource pulses increased mean biomass of Chlorophyta (t10.01 = 3.19, p = 0.01; B) and Cyanobacteria (t22.1 = 2.05, p = 0.04; C), and decreased mean biomass of Charophyta (t12.81 = −6.07, p < 0.01; A) and Dinoflagellata (t22.1 = −4.89, p < 0.01; D). Dashed lines indicate when perturbations were induced (i.e., live fish and/or fish carrion added and/or removed). Taxa silhouettes and their colours correspond with major microalgae phyla as in main figures. Data were analysed from 355 biologically independent zooplankton samples (A-E) for a control (n = 96), predator removal (n = 80), resource pulse (n = 80), and MME (n = 99), respectively, from one experiment. General additive mixed model (GAMM, A-E).

Extended Data Fig. 5 Time series of mean density across five major zooplankton families following ecological perturbations.

Zooplankton density (ln[individuals/L]) of Bosminidae (A), Brachionidae (B), Cyclopoida (C), Cyprididae (D), and Daphniidae (E) following predator mass mortality events (MMEs, light green), predator removals (light blue), and resource pulses (dark green), as well as the undisturbed system (control, dark blue). Points and lines indicate mean values and +/− 1 SE for each sampling period and treatment, with points jittered to reduce overlap within sample periods. Solid lines and shaded regions indicate model predictions and 95% confidence intervals, respectively. Relative to the control, MMEs increased mean density of all major zooplankton families including Bosminidae (t10.4 = 8.05, p < 0.01; A), Brachionidae (t11.13 = 3.00, p < 0.01; B), Cyclopoida (t9.53 = 5.70, p < 0.01; C), Cyprididae (t7.44 = 2.09, p = 0.04; D), and Daphniidae (t9.4 = 4.38, p < 0.01; E). Predator removals increased mean density of Bosminidae (t10.4 = 8.36, p < 0.01; A), Brachionidae (t11.13 = 4.12, p < 0.01; B), Cyclopoida (t9.53 = 8.34, p < 0.01; C), and Daphniidae (t9.4 = 5.95, p < 0.01; E) as well as reduced mean Cyprididae density (t7.44 = −1.98, p = 0.05; D). Resource pulses increased mean density of Brachionidae (t11.13 = 2.99, p < 0.01; B) and Cyclopoida (t9.53 = 3.13, p < 0.01; C). Dashed lines indicate when perturbations were induced (i.e., live fish and/or fish carrion added and/or removed). Taxa silhouettes and their colours correspond with major zooplankton families as in main figures. Data were analysed from 355 biologically independent zooplankton samples (A-E) for a control (n = 96), predator removal (n = 80), resource pulse (n = 80), and MME (n = 99), respectively, from one experiment. General additive mixed model (GAMM, A-E).

Extended Data Fig. 6 Time series of mean density across five major microalgae phyla following ecological perturbations.

Microalgae density (ln([ndividuals/L]) of Charophyta (A), Chlorophyta (B), Cyanobacteria (C), Dinoflagellata (D), and Euglenozoa (E) following predator mass mortality events (MMEs, light green), predator removals (light blue), and resource pulses (dark green), as well as the undisturbed system (control, dark blue). Points and lines indicate mean values and +/− 1 SE for each sampling period and treatment, with points jittered to reduce overlap within sample periods. Solid lines and shaded regions indicate model predictions and 95% confidence intervals, respectively. Relative to the control, MMEs decreased mean density of Charophyta (t12.42 = −9.83, p < 0.01; A) and Dinoflagellata (t9.87 = −5.18, p < 0.01; D), as well as had relatively low mean density of Cyanobacteria (t21.86 = −1.67, p = 0.10; C). Predator removals decreased density of Charophyta (t12.42 = −5.63, p < 0.01; A), Chlorophyta (t17.14 = −2.47, p = 0.02; B), and Dinoflagellata (t9.87 = −5.18, p < 0.01; D). Resource pulses increased mean density of Chlorophyta (t17.14 = 2.86, p = 0.01; B) and reduced mean density of Charophyta (t12.42 = −5.98, p < 0.01; A) and Dinoflagellata (t9.87 = −5.11, p < 0.01; D), as well as had relatively high mean density of Cyanobacteria (t21.86 = 1.93, p = 0.06; C). Dashed lines indicate when perturbations were induced (i.e., live fish and/or fish carrion added and/or removed). Taxa silhouettes and their colours correspond with major microalgae phyla as in main figures. Data were analysed from 355 biologically independent zooplankton samples (A-E) for a control (n = 96), predator removal (n = 80), resource pulse (n = 80), and MME (n = 99), respectively, from one experiment. General additive mixed model (GAMM, A-E).

Extended Data Fig. 7 Time series of mean body size across five major zooplankton families following ecological perturbations.

Zooplankton body size (mm) of Bosminidae (A), Brachionidae (B), Cyclopoida (C), Cyprididae (D), and Daphniidae (E) following predator mass mortality events (MMEs, light green), predator removals (light blue), and resource pulses (dark green), as well as the undisturbed system (control, dark blue). Points and lines indicate mean values and +/− 1 SE for each sampling period and treatment, with points jittered to reduce overlap within sample periods. Solid lines and shaded regions indicate model predictions and 95% confidence intervals, respectively. Relative to the control, MMEs increased mean body size of Bosminidae (t5 = 2.98, p < 0.01; A), Cyclopoida (t12.93 = 7.57, p < 0.01; C), and Daphniidae (t5 = 6.71, p < 0.01; E). Predator removals increased mean body size of Cyclopoida (t12.93 = 6.98, p < 0.01; C) and Daphniidae (t5 = 5.09, p < 0.001; E), as well as decreased mean body size of Brachionidae (t5 = −3.17, p < 0.01; B). Resource pulses increased mean body size of Cyclopoida (t12.93 = 2.68, p = 0.01; C), Cyprididae (t9.74 = 2.16, p = 0.03; D), and Daphniidae (t5 = 3.88, p < 0.01; E), as well as decreased mean body size of Brachionidae (t5 = −2.14, p = 0.03; B). Dashed lines indicate when perturbations were induced (i.e., live fish and/or fish carrion added and/or removed). Taxa silhouettes and their colours correspond with major zooplankton families as in main figures. Data were analysed from 355 biologically independent zooplankton samples (A-E) for a control (n = 96), predator removal (n = 80), resource pulse (n = 80), and MME (n = 969, respectively, from one experiment. General additive mixed model (GAMM, A-E).

Extended Data Fig. 8 Time series of mean biovolume across two major microalgae phyla following ecological perturbations.

Mean microalgae biovolume (ln[μg2]) of Charophyta (A) and Chlorophyta (B) following predator mass mortality events (MMEs, light green), predator removals (light blue), and resource pulses (dark green), as well as the undisturbed system (control, dark blue). Points and lines indicate mean values and +/− 1 SE for each sampling period and treatment, with points jittered to reduce overlap within sample periods. Solid lines and shaded regions indicate model predictions and 95% confidence intervals, respectively. Relative to the control, MMEs increased mean biovolume of Charophyta (t8.83 = 2.47, p = 0.01; A) and Chlorophyta (t20.96 = 2.93, p < 0.01; B). Predator removals increased mean biovolume of Chlorophyta (t20.96 = 4.32, p < 0.01; A). Dashed lines indicate when perturbations were induced (i.e., live fish and/or fish carrion added and/or removed). Taxa silhouettes and their colours correspond with major microalgae phyla as in main figures. Data were analysed from 240 biologically independent samples of Charophyta (A) for a control, (n = 80), predator removal (n = 54), resource pulse (n = 54), and MME (n = 52), as well as 283 biologically independent samples of Chlorophyta (B) for a control, (n = 79), predator removal (n = 59), resource pulse (n = 70), and MME (n = 75), from one experiment. General additive mixed model (GAMM, A-B).

Extended Data Fig. 9 Raw biomass estimates during sample periods before ecological perturbations were induced (i.e., the first three sample periods).

Chlorophyll-a (ln[μg/L], A), zooplankton biomass (ln[μg/L], B), and microalgae biomass (ln[μg/L], C) in mesocosms that would receive treatments to become predator mass mortality events (MMEs, light green), predator removals (light blue), and resource pulses (dark green), as well as the undisturbed system (control, dark blue). Large points and lines indicate mean values and 95% CIs, with smaller jittered points (to reduce overlap) indicating individual samples. There were no effects of treatment on average chlorophyll-a (F1,3 = 0.11, p = 0.65; A), zooplankton biomass (F1,3 = 0.03, p = 0.99; B), or microalgae biomass (F1,3 = 0.94, p = 0.45; C) during the first three sample periods of the experiment. Data were analysed from 54 biologically independent samples for a control, (n = 15), predator removal (n = 12), resource pulse (n = 12), and MME (n = 15). Two-way, two-sided ANOVA (A-B).

Extended Data Fig. 10 Raw (non-smoothed) and smoothed biomass estimates following ecological perturbations.

Chlorophyll-a (ln[μg/L], A-B), zooplankton biomass (ln[μg/L], C-D), and microalgae biomass (ln[μg/L], E-F) following predator mass mortality events (MMEs, light green), predator removals (light blue), and resource pulses (dark green), as well as the undisturbed system (control, dark blue). Points and lines indicate mean values and 95% CIs, with points jittered to reduce overlap. Raw data (A, C, E) were similar to smoothed data (B, D, F, as in Fig. 1f–h). Specifically, relative to the experimental control, predator removals decreased average chlorophyll-a (F1,14 = 5.50, p = 0.03; A), resource pulses increased average chlorophyll-a (F1,14 = 151.48, p < 0.01), and there was no significant interaction between predator removals and resource pulses (i.e., MMEs) on chlorophyll-a (F1,14 = 0.26, p = 0.62). Additionally, predator removals increased zooplankton biomass (F1,14 = 5.03, p = 0.04; C), but there was no effect of resource pulses on zooplankton biomass (F1,14 = 0.56, p = 0.47) nor was there a significant interaction between predator removals and resource pulses on zooplankton biomass (F1,14 = 0.07, p = 0.80). Lastly, there was strong evidence that predator removals reduced microalgae biomass (F1,14 = 4.16, p = 0.06; E), but there was no effect of resource pulses on microalgae biomass (F1,14 = 0.64, p = 0.43) nor was there a significant interaction between predator removals and resource pulses on microalgae biomass (F1,14 = 0.01, p = 0.94). Results for the analysis of the smoothed data are shown in the main text. Raw data were analysed from 391 biologically independent samples for a control (n = 106), predator removal (n = 88), resource pulse (n = 88), and MME (n = 109). Smoothed data were analysed from 355 biologically independent samples for a control (n = 96), predator removal (n = 80), resource pulse (n = 80), and MME (n = 99), from one experiment. Two-way, two-sided ANOVA (A-B).

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Tye, S.P., Fey, S.B., Gibert, J.P. et al. Predator mass mortality events restructure food webs through trophic decoupling. Nature 626, 335–340 (2024). https://doi.org/10.1038/s41586-023-06931-7

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