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A predictive timeline of wildlife population collapse

Abstract

Contemporary rates of biodiversity decline emphasize the need for reliable ecological forecasting, but current methods vary in their ability to predict the declines of real-world populations. Acknowledging that stressor effects start at the individual level, and that it is the sum of these individual-level effects that drives populations to collapse, shifts the focus of predictive ecology away from using predominantly abundance data. Doing so opens new opportunities to develop predictive frameworks that utilize increasingly available multi-dimensional data, which have previously been overlooked for ecological forecasting. Here, we propose that stressed populations will exhibit a predictable sequence of observable changes through time: changes in individuals’ behaviour will occur as the first sign of increasing stress, followed by changes in fitness-related morphological traits, shifts in the dynamics (for example, birth rates) of populations and finally abundance declines. We discuss how monitoring the sequential appearance of these signals may allow us to discern whether a population is increasingly at risk of collapse, or is adapting in the face of environmental change, providing a conceptual framework to develop new forecasting methods that combine multi-dimensional (for example, behaviour, morphology, life history and abundance) data.

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Fig. 1: Theoretical example of a timeline to collapse.

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Data availability

No original data were used. Literature-based data are properly cited. F.C. can be contacted at francesco.cerini@bristol.ac.uk or francesco.cerini@uniroma3.it. Source data are provided with this paper.

References

  1. Ceballos, G. et al. Accelerated modern human-induced species losses: entering the sixth mass extinction. Sci. Adv. 1, e1400253 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  2. Dereniowska, M. & Meinard, Y. The unknownness of biodiversity: its value and ethical significance for conservation action. Biol. Conserv. 260, 109199 (2021).

    Article  Google Scholar 

  3. Maron, M. et al. Towards a threat assessment framework for ecosystem services. Trends Ecol. Evol. 32, 240–248 (2017).

    Article  PubMed  Google Scholar 

  4. Tilman, D. et al. Future threats to biodiversity and pathways to their prevention. Nature 546, 73–81 (2017).

    Article  CAS  PubMed  Google Scholar 

  5. Taborsky, B. et al. Towards an evolutionary theory of stress responses. Trends Ecol. Evol. 36, 39–48 (2021).

    Article  PubMed  Google Scholar 

  6. van de Leemput, I. A., Dakos, V., Scheffer, M. & van Nes, E. H. Slow recovery from local disturbances as an indicator for loss of ecosystem resilience. Ecosystems 21, 141–152 (2018).

    Article  PubMed  Google Scholar 

  7. Fagan, W. F. & Holmes, E. E. Quantifying the extinction vortex. Ecol. Lett. 9, 51–60 (2005).

    Google Scholar 

  8. Williams, N. F., McRae, L., Freeman, R., Capdevila, P. & Clements, C. F. Scaling the extinction vortex: body size as a predictor of population dynamics close to extinction events. Ecol. Evol. 11, 7069–7079 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  9. Clements, C. F. & Ozgul, A. Indicators of transitions in biological systems. Ecol. Lett. 21, 905–919 (2018).

    Article  PubMed  Google Scholar 

  10. Shaffer, M. L. in Challenges in the Conservation of Biological Resources (eds. Decker, D. J., Krasny, M. E., Goff, G. R., Smith, C. R. & Gross, D. W.) 107–118 (Routledge, 2019).

  11. Scheffer, M. et al. Early-warning signals for critical transitions. Nature 461, 53–59 (2009).

    Article  CAS  PubMed  Google Scholar 

  12. Gardner, T. A. et al. The cost-effectiveness of biodiversity surveys in tropical forests. Ecol. Lett. 11, 139–150 (2008).

    Article  PubMed  Google Scholar 

  13. Coulson, T., Mace, G. M., Hudson, E. & Possingham, H. The use and abuse of population viability analysis. Trends Ecol. Evol. 16, 219–221 (2001).

    Article  CAS  PubMed  Google Scholar 

  14. Clements, C. F., Drake, J. M., Griffiths, J. I. & Ozgul, A. Factors influencing the detectability of early warning signals of population collapse. Am. Nat. 186, 50–58 (2015).

    Article  PubMed  Google Scholar 

  15. Patterson, A. C., Strang, A. G. & Abbott, K. C. When and where we can expect to see early warning signals in multispecies systems approaching tipping points: insights from theory. Am. Nat. 198, E12–E26 (2021).

    Article  PubMed  Google Scholar 

  16. Vinton, A. C., Gascoigne, S. J. L., Sepil, I. & Salguero-Gómez, R. Plasticity’s role in adaptive evolution depends on environmental change components. Trends Ecol. Evol. https://doi.org/10.1016/j.tree.2022.08.008 (2022).

  17. Levin, S. A. The problem of pattern and scale in ecology: the Robert H. MacArthur Award lecture. Ecology 73, 1943–1967 (1992).

    Article  Google Scholar 

  18. Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. & West, G. B. Toward a metabolic theory of ecology. Ecology 85, 1771–1789 (2004).

    Article  Google Scholar 

  19. Gillooly, J. F., Brown, J. H., West, G. B., Savage, V. M. & Charnov, E. L. Effects of size and temperature on metabolic rate. Science 293, 2248–2251 (2001).

    Article  CAS  PubMed  Google Scholar 

  20. Haberle, I., Marn, N., Geček, S. & Klanjšček, T. Dynamic energy budget of endemic and critically endangered bivalve Pinna nobilis: a mechanistic model for informed conservation. Ecol. Model. 434, 109207 (2020).

    Article  Google Scholar 

  21. Gislason, H., Daan, N., Rice, J. C. & Pope, J. G. Size, growth, temperature and the natural mortality of marine fish. Fish Fish. 11, 149–158 (2010).

    Article  Google Scholar 

  22. Jennings, S. & Blanchard, J. L. Fish abundance with no fishing: predictions based on macroecological theory. J. Anim. Ecol. 73, 632–642 (2004).

    Article  Google Scholar 

  23. Valderrama, D. & Fields, K. H. Flawed evidence supporting the metabolic theory of ecology may undermine goals of ecosystem-based fishery management: the case of invasive Indo-Pacific lionfish in the western Atlantic. ICES J. Mar. Sci. 74, 1256–1267 (2017).

    Article  Google Scholar 

  24. Marshall, D. J. & McQuaid, C. D. Warming reduces metabolic rate in marine snails: adaptation to fluctuating high temperatures challenges the metabolic theory of ecology. Proc. R. Soc. B 278, 281–288 (2011).

    Article  PubMed  Google Scholar 

  25. Rombouts, I., Beaugrand, G., Ibaňez, F., Chiba, S. & Legendre, L. Marine copepod diversity patterns and the metabolic theory of ecology. Oecologia 166, 349–355 (2011).

    Article  PubMed  Google Scholar 

  26. Allen, A. P. & Gillooly, J. F. The mechanistic basis of the metabolic theory of ecology. Oikos 116, 1073–1077 (2022).

    Article  Google Scholar 

  27. Lawton, J. H. From physiology to population dynamics and communities. Funct. Ecol. 5, 155–161 (1991).

    Article  Google Scholar 

  28. Ames, E. M. et al. Striving for population-level conservation: integrating physiology across the biological hierarchy. Conserv. Physiol. 8, coaa019 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  29. Berger-Tal, O. et al. Integrating animal behavior and conservation biology: a conceptual framework. Behav. Ecol. 22, 236–239 (2011).

    Article  Google Scholar 

  30. Baruah, G., Clements, C. F., Guillaume, F. & Ozgul, A. When do shifts in trait dynamics precede population declines? Am. Nat. 193, 633–644 (2019).

    Article  PubMed  Google Scholar 

  31. Dakos, V. et al. Methods for detecting early warnings of critical transitions in time series illustrated using simulated ecological data. PLoS ONE 7, e41010 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Ward, R. J., Griffiths, R. A., Wilkinson, J. W. & Cornish, N. Optimising monitoring efforts for secretive snakes: a comparison of occupancy and N-mixture models for assessment of population status. Sci. Rep. 7, 18074 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  33. Thompson, W. Sampling Rare or Elusive Species: Concepts, Designs, and Techniques for Estimating Population Parameters (Island Press, 2013).

  34. Clements, C. F., Blanchard, J. L., Nash, K. L., Hindell, M. A. & Ozgul, A. Body size shifts and early warning signals precede the historic collapse of whale stocks. Nat. Ecol. Evol. 1, 0188 (2017).

    Article  Google Scholar 

  35. Burant, J. B., Park, C., Betini, G. S. & Norris, D. R. Early warning indicators of population collapse in a seasonal environment. J. Anim. Ecol. 90, 1538–1549 (2021).

    Article  PubMed  Google Scholar 

  36. Tuomainen, U. & Candolin, U. Behavioural responses to human-induced environmental change. Biol. Rev. 86, 640–657 (2011).

    Article  PubMed  Google Scholar 

  37. Mazza, V., Dammhahn, M., Lösche, E. & Eccard, J. A. Small mammals in the big city: behavioural adjustments of non-commensal rodents to urban environments. Glob. Change Biol. 26, 6326–6337 (2020).

    Article  Google Scholar 

  38. Hendry, A. P., Farrugia, T. J. & Kinnison, M. T. Human influences on rates of phenotypic change in wild animal populations. Mol. Ecol. 17, 20–29 (2008).

    Article  PubMed  Google Scholar 

  39. Speakman, J. R., Król, E. & Johnson, M. S. The functional significance of individual variation in basal metabolic rate. Physiol. Biochem. Zool. 77, 900–915 (2004).

    Article  PubMed  Google Scholar 

  40. Péron, G. et al. Evidence of reduced individual heterogeneity in adult survival of long-lived species. Evolution 70, 2909–2914 (2016).

    Article  PubMed  Google Scholar 

  41. Fleming, A. H., Clark, C. T., Calambokidis, J. & Barlow, J. Humpback whale diets respond to variance in ocean climate and ecosystem conditions in the California Current. Glob. Change Biol. 22, 1214–1224 (2016).

    Article  Google Scholar 

  42. Kirkwood, T. B. L., Rose, M. R., Harvey, P. H., Partridge, L. & Southwood, S. R. Evolution of senescence: late survival sacrificed for reproduction. Phil. Trans. R. Soc. Lond. B 332, 15–24 (1991).

    Article  CAS  Google Scholar 

  43. Mallela, A. & Hastings, A. The role of stochasticity in noise-induced tipping point cascades: a master equation approach. Bull. Math. Biol. 83, 53 (2021).

    Article  PubMed  Google Scholar 

  44. Burthe, S. J. et al. Do early warning indicators consistently predict nonlinear change in long-term ecological data? J. Appl. Ecol. 53, 666–676 (2016).

    Article  Google Scholar 

  45. Vucetich, J. A. & Waite, T. A. Erosion of heterozygosity in fluctuating populations. Conserv. Biol. 13, 860–868 (1999).

    Article  Google Scholar 

  46. Kramer, A. M. & Drake, J. M. Experimental demonstration of population extinction due to a predator-driven Allee effect. J. Anim. Ecol. 79, 633–639 (2010).

    Article  PubMed  Google Scholar 

  47. Oram, E. & Spitze, K. Depth selection by Daphnia pulex in response to Chaoborus kairomone. Freshw. Biol. 58, 409–415 (2013).

    Article  Google Scholar 

  48. Trites, A. W. & Donnelly, C. P. The decline of Steller sea lions Eumetopias jubatus in Alaska: a review of the nutritional stress hypothesis. Mammal. Rev. 33, 3–28 (2003).

    Article  Google Scholar 

  49. Sibly, R. M., Barker, D., Hone, J. & Pagel, M. On the stability of populations of mammals, birds, fish and insects. Ecol. Lett. 10, 970–976 (2007).

    Article  PubMed  Google Scholar 

  50. Dakos, V. et al. Ecosystem tipping points in an evolving world. Nat. Ecol. Evol. 3, 355–362 (2019).

    Article  PubMed  Google Scholar 

  51. Dingemanse, N. J., Kazem, A. J. N., Réale, D. & Wright, J. Behavioural reaction norms: animal personality meets individual plasticity. Trends Ecol. Evol. 25, 81–89 (2010).

    Article  PubMed  Google Scholar 

  52. Tanner, R. L. & Dowd, W. W. Inter-individual physiological variation in responses to environmental variation and environmental change: integrating across traits and time. Comp. Biochem. Physiol. A 238, 110577 (2019).

    Article  CAS  Google Scholar 

  53. Patrick, S. C., Martin, J. G. A., Ummenhofer, C. C., Corbeau, A. & Weimerskirch, H. Albatrosses respond adaptively to climate variability by changing variance in a foraging trait. Glob. Change Biol. 27, 4564–4574 (2021).

    Article  CAS  Google Scholar 

  54. Fayet, A. L., Clucas, G. V., Anker‐Nilssen, T., Syposz, M. & Hansen, E. S. Local prey shortages drive foraging costs and breeding success in a declining seabird, the Atlantic puffin. J. Anim. Ecol. https://doi.org/10.1111/1365-2656.13442 (2021).

  55. Pierce, C. L. Predator avoidance, microhabitat shift, and risk-sensitive foraging in larval dragonflies. Oecologia 77, 81–90 (1988).

    Article  CAS  PubMed  Google Scholar 

  56. Leibold, M. & Tessier, A. J. Contrasting patterns of body size for Daphnia species that segregate by habitat. Oecologia 86, 342–348 (1991).

    Article  PubMed  Google Scholar 

  57. Charmantier, A. & Gienapp, P. Climate change and timing of avian breeding and migration: evolutionary versus plastic changes. Evol. Appl. 7, 15–28 (2014).

    Article  PubMed  Google Scholar 

  58. Kopp, M. & Matuszewski, S. Rapid evolution of quantitative traits: theoretical perspectives. Evol. Appl. 7, 169–191 (2014).

    Article  PubMed  Google Scholar 

  59. Williams, J. W., Ordonez, A. & Svenning, J.-C. A unifying framework for studying and managing climate-driven rates of ecological change. Nat. Ecol. Evol. 5, 17–26 (2021).

    Article  PubMed  Google Scholar 

  60. Jaureguiberry, P. et al. The direct drivers of recent global anthropogenic biodiversity loss. Sci. Adv. 8, eabm9982 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  61. Chevin, L.-M., Collins, S. & Lefèvre, F. Phenotypic plasticity and evolutionary demographic responses to climate change: taking theory out to the field. Funct. Ecol. 27, 967–979 (2013).

    Article  Google Scholar 

  62. Ferriere, R. & Legendre, S. Eco-evolutionary feedbacks, adaptive dynamics and evolutionary rescue theory. Phil. Trans. R. Soc. B 368, 20120081 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  63. Rebecchi, L., Boschetti, C. & Nelson, D. R. Extreme-tolerance mechanisms in meiofaunal organisms: a case study with tardigrades, rotifers and nematodes. Hydrobiologia 847, 2779–2799 (2020).

    Article  Google Scholar 

  64. Hansson, B. & Westerberg, L. On the correlation between heterozygosity and fitness in natural populations. Mol. Ecol. 11, 2467–2474 (2002).

    Article  PubMed  Google Scholar 

  65. Mammola, S., Carmona, C. P., Guillerme, T. & Cardoso, P. Concepts and applications in functional diversity. Funct. Ecol. 35, 1869–1885 (2021).

    Article  CAS  Google Scholar 

  66. McClanahan, T. R. et al. Highly variable taxa-specific coral bleaching responses to thermal stresses. Mar. Ecol. Prog. Ser. 648, 135–151 (2020).

    Article  Google Scholar 

  67. Reside, A. E. et al. Beyond the model: expert knowledge improves predictions of species’ fates under climate change. Ecol. Appl. 29, e01824 (2019).

    Article  PubMed  Google Scholar 

  68. Desjonquères, C., Gifford, T. & Linke, S. Passive acoustic monitoring as a potential tool to survey animal and ecosystem processes in freshwater environments. Freshw. Biol. 65, 7–19 (2020).

    Article  Google Scholar 

  69. Sequeira, A. M. M. et al. A standardisation framework for bio-logging data to advance ecological research and conservation. Methods Ecol. Evol. 12, 996–1007 (2021).

    Article  Google Scholar 

  70. Shimada, T. et al. Optimising sample sizes for animal distribution analysis using tracking data. Methods Ecol. Evol. 12, 288–297 (2021).

    Article  Google Scholar 

  71. Wauchope, H. S. et al. Evaluating impact using time-series data. Trends Ecol. Evol. 36, 196–205 (2021).

    Article  PubMed  Google Scholar 

  72. Krause, D. J., Hinke, J. T., Perryman, W. L., Goebel, M. E. & LeRoi, D. J. An accurate and adaptable photogrammetric approach for estimating the mass and body condition of pinnipeds using an unmanned aerial system. PLoS ONE 12, e0187465 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  73. Besson, M. et al. Towards the fully automated monitoring of ecological communities. Ecol. Lett. https://doi.org/10.1111/ele.14123 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  74. Cavender-Bares, J. et al. Integrating remote sensing with ecology and evolution to advance biodiversity conservation. Nat. Ecol. Evol. 6, 506–519 (2022).

    Article  PubMed  Google Scholar 

  75. Ingram, D. J., Ferreira, G. B., Jones, K. E. & Mace, G. M. Targeting conservation actions at species threat response thresholds. Trends Ecol. Evol. 36, 216–226 (2021).

    Article  PubMed  Google Scholar 

  76. Keith, S. A. et al. Synchronous behavioural shifts in reef fishes linked to mass coral bleaching. Nat. Clim. Change 8, 986–991 (2018).

    Article  Google Scholar 

  77. Drake, J. M. & Griffen, B. D. Early warning signals of extinction in deteriorating environments. Nature 467, 456–459 (2010).

    Article  CAS  PubMed  Google Scholar 

  78. Enquist, B. J. et al. in Advances in Ecological Research Vol. 52 (eds Pawar, S. et al.) 249–318 (Academic Press, 2015).

  79. Wei, W. W. S. Multivariate Time Series Analysis and Applications (John Wiley & Sons, 2018).

  80. Holmes, E. E., Ward, E. J. & Wills, K. MARSS: multivariate autoregressive state-space models for analyzing time-series data. R J. 4, 11–19 (2012).

    Article  Google Scholar 

  81. Zhu, M., Yamakawa, T. & Sakai, T. Combined use of trawl fishery and research vessel survey data in a multivariate autoregressive state-space (MARSS) model to improve the accuracy of abundance index estimates. Fish. Sci. 84, 437–451 (2018).

    Article  CAS  Google Scholar 

  82. Lai, G., Chang, W.-C., Yang, Y. & Liu, H. Modeling long- and short-term temporal patterns with deep neural networks. In The 41st International ACM SIGIR Conference on Research & Development in Information Retrieval 95–104, https://doi.org/10.1145/3209978.3210006 (ACM, 2018).

  83. Bury, T. M. et al. Deep learning for early warning signals of tipping points. Proc. Natl Acad. Sci. USA 118, e2106140118 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Lara-Benítez, P., Carranza-García, M. & Riquelme, J. C. An experimental review on deep learning architectures for time series forecasting. Int. J. Neural Syst. 31, 2130001 (2021).

    Article  PubMed  Google Scholar 

  85. Guo, Q. et al. Application of deep learning in ecological resource research: theories, methods, and challenges. Sci. China Earth Sci. 63, 1457–1474 (2020).

    Article  Google Scholar 

  86. Rogers, T. L., Johnson, B. J. & Munch, S. B. Chaos is not rare in natural ecosystems. Nat. Ecol. Evol. 6, 1105–1111 (2022).

    Article  PubMed  Google Scholar 

  87. Samplonius, J. M. et al. Phenological sensitivity to climate change is higher in resident than in migrant bird populations among European cavity breeders. Glob. Change Biol. 24, 3780–3790 (2018).

    Article  Google Scholar 

  88. Menzel, A. et al. Climate change fingerprints in recent European plant phenology. Glob. Change Biol. 26, 2599–2612 (2020).

    Article  Google Scholar 

  89. Koleček, J., Adamík, P. & Reif, J. Shifts in migration phenology under climate change: temperature vs. abundance effects in birds. Clim. Change 159, 177–194 (2020).

    Article  Google Scholar 

  90. Altermatt, F. et al. Big answers from small worlds: a user’s guide for protist microcosms as a model system in ecology and evolution. Methods Ecol. Evol. 6, 218–231 (2015).

    Article  Google Scholar 

  91. Beermann, A. J. et al. Multiple-stressor effects on stream macroinvertebrate communities: a mesocosm experiment manipulating salinity, fine sediment and flow velocity. Sci. Total Environ. 610611, 961–971 (2018).

    Article  PubMed  Google Scholar 

  92. Clements, C. F. & Ozgul, A. Including trait-based early warning signals helps predict population collapse. Nat. Commun. 7, 10984 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Jacquet, C. & Altermatt, F. The ghost of disturbance past: long-term effects of pulse disturbances on community biomass and composition. Proc. R. Soc. B 287, 20200678 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  94. Greggor, A. L. et al. Research priorities from animal behaviour for maximising conservation progress. Trends Ecol. Evol. 31, 953–964 (2016).

    Article  PubMed  Google Scholar 

  95. Couvillon, M. J., Schürch, R. & Ratnieks, F. L. W. Waggle dance distances as integrative indicators of seasonal foraging challenges. PLoS ONE 9, e93495 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  96. Hamilton, C. D., Lydersen, C., Ims, R. A. & Kovacs, K. M. Predictions replaced by facts: a keystone species’ behavioural responses to declining Arctic sea-ice. Biol. Lett. 11, 20150803 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  97. Holt, R. E. & Jørgensen, C. Climate change in fish: effects of respiratory constraints on optimal life history and behaviour. Biol. Lett. 11, 20141032 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  98. Gauzens, B. et al. Adaptive foraging behaviour increases vulnerability to climate change. Preprint at https://doi.org/10.1101/2021.05.05.442768 (2021).

  99. Lenda, M., Witek, M., Skórka, P., Moroń, D. & Woyciechowski, M. Invasive alien plants affect grassland ant communities, colony size and foraging behaviour. Biol. Invasions 15, 2403–2414 (2013).

    Article  Google Scholar 

  100. Hertel, A. G. et al. Don’t poke the bear: using tracking data to quantify behavioural syndromes in elusive wildlife. Anim. Behav. 147, 91–104 (2019).

    Article  Google Scholar 

  101. Tini, M. et al. Use of space and dispersal ability of a flagship saproxylic insect: a telemetric study of the stag beetle (Lucanus cervus) in a relict lowland forest. Insect Conserv. Divers. 11, 116–129 (2018).

    Article  Google Scholar 

  102. Kunc, H. P. & Schmidt, R. Species sensitivities to a global pollutant: a meta-analysis on acoustic signals in response to anthropogenic noise. Glob. Change Biol. 27, 675–688 (2021).

    Article  Google Scholar 

  103. Anestis, A., Lazou, A., Pörtner, H. O. & Michaelidis, B. Behavioral, metabolic, and molecular stress responses of marine bivalve Mytilus galloprovincialis during long-term acclimation at increasing ambient temperature. Am. J. Physiol. 293, R911–R921 (2007).

    CAS  Google Scholar 

  104. Pacherres, C. O., Schmidt, G. M. & Richter, C. Autotrophic and heterotrophic responses of the coral Porites lutea to large amplitude internal waves. J. Exp. Biol. 216, 4365–4374 (2013).

    PubMed  Google Scholar 

  105. Ban, S. S., Graham, N. A. J. & Connolly, S. R. Evidence for multiple stressor interactions and effects on coral reefs. Glob. Change Biol. 20, 681–697 (2014).

    Article  Google Scholar 

  106. Singh, R., Prathibha, P. & Jain, M. Effect of temperature on life-history traits and mating calls of a field cricket, Acanthogryllus asiaticus. J. Therm. Biol. 93, 102740 (2020).

    Article  PubMed  Google Scholar 

  107. Pellegrini, A. Y., Romeu, B., Ingram, S. N. & Daura-Jorge, F. G. Boat disturbance affects the acoustic behaviour of dolphins engaged in a rare foraging cooperation with fishers. Anim. Conserv. 24, 613–625 (2021).

    Article  Google Scholar 

  108. McMahan, M. D. & Grabowski, J. H. Nonconsumptive effects of a range-expanding predator on juvenile lobster (Homarus americanus) population dynamics. Ecosphere 10, e02867 (2019).

    Article  Google Scholar 

  109. Vilhunen, S., Hirvonen, H. & Laakkonen, M. V.-M. Less is more: social learning of predator recognition requires a low demonstrator to observer ratio in Arctic charr (Salvelinus alpinus). Behav. Ecol. Sociobiol. 57, 275–282 (2005).

    Article  Google Scholar 

  110. Ortega, Z., Mencía, A. & Pérez-Mellado, V. Rapid acquisition of antipredatory responses to new predators by an insular lizard. Behav. Ecol. Sociobiol. 71, 1 (2017).

    Article  Google Scholar 

  111. Fox, R. J., Donelson, J. M., Schunter, C., Ravasi, T. & Gaitán-Espitia, J. D. Beyond buying time: the role of plasticity in phenotypic adaptation to rapid environmental change. Phil. Trans. R. Soc. B 374, 20180174 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  112. Pigeon, G., Ezard, T. H. G., Festa-Bianchet, M., Coltman, D. W. & Pelletier, F. Fluctuating effects of genetic and plastic changes in body mass on population dynamics in a large herbivore. Ecology 98, 2456–2467 (2017).

    Article  PubMed  Google Scholar 

  113. Lomolino, M. V. & Perault, D. R. Body size variation of mammals in a fragmented, temperate rainforest. Conserv. Biol. 21, 1059–1069 (2007).

    Article  PubMed  Google Scholar 

  114. Gardner, J. L., Peters, A., Kearney, M. R., Joseph, L. & Heinsohn, R. Declining body size: a third universal response to warming? Trends Ecol. Evol. 26, 285–291 (2011).

    Article  PubMed  Google Scholar 

  115. Sheridan, J. A. & Bickford, D. Shrinking body size as an ecological response to climate change. Nat. Clim. Change 1, 401–406 (2011).

    Article  Google Scholar 

  116. Thoral, E. et al. Changes in foraging mode caused by a decline in prey size have major bioenergetic consequences for a small pelagic fish. J. Anim. Ecol. 90, 2289–2301 (2021).

    Article  PubMed  Google Scholar 

  117. Stirling, I. & Derocher, A. E. Effects of climate warming on polar bears: a review of the evidence. Glob. Change Biol. 18, 2694–2706 (2012).

    Article  Google Scholar 

  118. Spanbauer, T. L. et al. Body size distributions signal a regime shift in a lake ecosystem. Proc. R. Soc. B 283, 20160249 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  119. Bjorndal, K. A. et al. Ecological regime shift drives declining growth rates of sea turtles throughout the West Atlantic. Glob. Change Biol. 23, 4556–4568 (2017).

    Article  Google Scholar 

  120. Eshun-Wilson, F., Wolf, R., Andersen, T., Hessen, D. O. & Sperfeld, E. UV radiation affects antipredatory defense traits in Daphnia pulex. Ecol. Evol. 10, 14082–14097 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  121. Zhang, H., Hollander, J. & Hansson, L.-A. Bi-directional plasticity: rotifer prey adjust spine length to different predator regimes. Sci. Rep. 7, 10254 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  122. Simbula, G., Vignoli, L., Carretero, M. A. & Kaliontzopoulou, A. Fluctuating asymmetry as biomarker of pesticides exposure in the Italian wall lizards (Podarcis siculus). Zoology 147, 125928 (2021).

    Article  PubMed  Google Scholar 

  123. Leary, R. F. & Allendorf, F. W. Fluctuating asymmetry as an indicator of stress: implications for conservation biology. Trends Ecol. Evol. 4, 214–217 (1989).

    Article  CAS  PubMed  Google Scholar 

  124. Gavrilchuk, K. et al. Trophic niche partitioning among sympatric baleen whale species following the collapse of groundfish stocks in the Northwest Atlantic. Mar. Ecol. Prog. Ser. 497, 285–301 (2014).

    Article  Google Scholar 

  125. Kershaw, J. L. et al. Declining reproductive success in the Gulf of St. Lawrence’s humpback whales (Megaptera novaeangliae) reflects ecosystem shifts on their feeding grounds. Glob. Change Biol. 27, 1027–1041 (2021).

    Article  CAS  Google Scholar 

  126. Rode, K. D., Amstrup, S. C. & Regehr, E. V. Reduced body size and cub recruitment in polar bears associated with sea ice decline. Ecol. Appl. 20, 768–782 (2010).

    Article  PubMed  Google Scholar 

  127. Obbard, M. E. et al. Re-assessing abundance of Southern Hudson Bay polar bears by aerial survey: effects of climate change at the southern edge of the range. Arct. Sci. 4, 634–655 (2018).

    Article  Google Scholar 

  128. Hutchings, J. A. The cod that got away. Nature 428, 899–900 (2004).

    Article  CAS  PubMed  Google Scholar 

  129. Zhang, F. Early warning signals of population productivity regime shifts in global fisheries. Ecol. Indic. 115, 106371 (2020).

    Article  Google Scholar 

  130. Fulton, G. R. The Bramble Cay melomys: the first mammalian extinction due to human-induced climate change. Pac. Conserv. Biol. 23, 1–3 (2017).

    Article  Google Scholar 

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Acknowledgements

F.C., D.Z.C. and C.F.C. are supported by NERC grant NE/T006579/1. All the Experimental Ecology and Conservation Lab (Duncan, Pol, Marc, Ellie) are gratefully acknowledged for the help in writing this piece.

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C.F.C. and D.Z.C. formulated the framework. F.C. developed the ideas, reviewed the literature and wrote the first draft of the manuscript. All authors contributed substantially to revisions.

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Correspondence to Francesco Cerini.

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Source Data Fig. Box 1 and 2

Sheet Box1_figure(a): Comparison of mean values + standard errors of two behaviours at two different sea-ice extensions. Sheet Box1_figure(b): comparison of probabilities of intra and interspecific attack, average P values and 95% confidence intervals at two coral covers. Sheet Box2_figure(a): time series of average bear weight with standard deviations. Sheet Box2_figure(b): comparison of average asymmetry index with standard errors between lizards living in fields with treatment versus control.

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Cerini, F., Childs, D.Z. & Clements, C.F. A predictive timeline of wildlife population collapse. Nat Ecol Evol 7, 320–331 (2023). https://doi.org/10.1038/s41559-023-01985-2

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