Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

The interspecific growth–mortality trade-off is not a general framework for tropical forest community structure

Abstract

Resource allocation within trees is a zero-sum game. Unavoidable trade-offs dictate that allocation to growth-promoting functions curtails other functions, generating a gradient of investment in growth versus survival along which tree species align, known as the interspecific growth–mortality trade-off. This paradigm is widely accepted but not well established. Using demographic data for 1,111 tree species across ten tropical forests, we tested the generality of the growth–mortality trade-off and evaluated its underlying drivers using two species-specific parameters describing resource allocation strategies: tolerance of resource limitation and responsiveness of allocation to resource access. Globally, a canonical growth–mortality trade-off emerged, but the trade-off was strongly observed only in less disturbance-prone forests, which contained diverse resource allocation strategies. Only half of disturbance-prone forests, which lacked tolerant species, exhibited the trade-off. Supported by a theoretical model, our findings raise questions about whether the growth–mortality trade-off is a universally applicable organizing framework for understanding tropical forest community structure.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Conceptual model of the between- and within-species relationships between mortality and growth for trees.
Fig. 2: Within-species relationships between individual mortality and prior growth for six exemplar tropical tree species.
Fig. 3: The interspecific growth–mortality trade-off for 1,097 woody tree species in ten forests.
Fig. 4: Variation among forests in tree species’ tolerance and responsiveness strategies.
Fig. 5: Analysis of a theoretical demographic allocation model showing the consequences of variation in resource allocation strategies for the growth–mortality trade-off.

Similar content being viewed by others

Data availability

The data supporting the findings of this study are deposited at https://forestgeo.github.io/fgeo/.

Code availability

The programming code supporting the findings of this study is deposited at https://forestgeo.github.io/fgeo/.

References

  1. Loehle, C. Tree life history strategies: the role of defenses. Can. J. For. Res. 18, 209–222 (1988).

    Article  Google Scholar 

  2. Kitajima, K. Relative importance of photosynthetic traits and allocation patterns as correlates of seedling shade tolerance of 13 tropical trees. Oecologia 98, 419–428 (1994).

    Article  PubMed  Google Scholar 

  3. Kobe, R. K., Pacala, S. W., Silander, J. A. & Canham, C. D. Juvenile tree survivorship as a component of shade tolerance. Ecol. Appl. 5, 517–532 (1995).

    Article  Google Scholar 

  4. Rees, M., Condit, R., Crawley, M., Pacala, S. & Tilman, D. Long-term studies of vegetation dynamics. Science 293, 650–655 (2001).

    Article  CAS  PubMed  Google Scholar 

  5. Russo, S. E., Brown, P., Tan, S. & Davies, S. J. Interspecific demographic trade-offs and soil-related habitat associations of tree species along resource gradients. J. Ecol. 96, 192–203 (2008).

    Article  Google Scholar 

  6. Wright, S. J. et al. Functional traits and the growth–mortality trade-off in tropical trees. Ecology 91, 3664–3674 (2010).

    Article  PubMed  Google Scholar 

  7. Hubbell, S. P. & Foster, R. B. Short-term dynamics of a neotropical forest: why ecological research matters to tropical conservation and management. Oikos 63, 48–61 (1992).

    Article  Google Scholar 

  8. Stephenson, N. L. et al. Causes and implications of the correlation between forest productivity and tree mortality rates. Ecol. Monogr. 81, 527–555 (2011).

    Article  Google Scholar 

  9. Adler, P. B., HilleRisLambers, J. & Levine, J. M. A niche for neutrality. Ecol. Lett. 10, 95–104 (2007).

    Article  PubMed  Google Scholar 

  10. Hubbell, S. P. The Unified Neutral Theory of Biodiversity and Biogeography (Princeton Univ. Press, 2001).

  11. Chesson, P. Mechanisms of maintenance of species diversity. Annu. Rev. Ecol. Syst. 31, 343–366 (2000).

    Article  Google Scholar 

  12. Poorter, L. et al. Are functional traits good predictors of demographic rates? Evidence from five neotropical forests. Ecology 89, 1908–1920 (2008).

    Article  CAS  PubMed  Google Scholar 

  13. Paine, C. E. T. et al. Globally, functional traits are weak predictors of juvenile tree growth, and we do not know why. J. Ecol. 103, 978–989 (2015).

    Article  Google Scholar 

  14. Cailleret, M. et al. A synthesis of radial growth patterns preceding tree mortality. Glob. Change Biol. 23, 1675–1690 (2017).

    Article  Google Scholar 

  15. Wyckoff, P. H. & Clark, J. S. The relationship between growth and mortality for seven co-occurring tree species in the southern Appalachian Mountains. J. Ecol. 90, 604–615 (2002).

    Article  Google Scholar 

  16. Kobe, R. K. Intraspecific variation in sapling mortality and growth predicts geographic variation in forest composition. Ecol. Monogr. 66, 181–201 (1996).

    Article  Google Scholar 

  17. Kobe, R. K. Light gradient partitioning among tropical tree species through differential seedling mortality and growth. Ecology 80, 187–207 (1999).

    Article  Google Scholar 

  18. Chapin, F. S., Autumn, K. & Pugnaire, F. Evolution of suites of traits in response to environmental stress. Am. Nat. 142, S78–S92 (1993).

    Article  Google Scholar 

  19. Grime, J. P. Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary biology. Am. Nat. 111, 1169–1194 (1977).

    Article  Google Scholar 

  20. Westoby, M., Warton, D. & Reich, P. B. The time value of leaf area. Am. Nat. 155, 649–656 (2000).

    Article  PubMed  Google Scholar 

  21. Zera, A. J. & Harshman, L. G. The physiology of life history trade-offs in animals. Annu. Rev. Ecol. Syst. 32, 95–126 (2003).

    Article  Google Scholar 

  22. Russo, S. E., Davies, S. J., King, D. A. & Tan, S. Soil-related performance variation and distributions of tree species in a Bornean rain forest. J. Ecol. 93, 879–889 (2005).

    Article  CAS  Google Scholar 

  23. Obeso, J. R. The costs of reproduction in plants. N. Phytol. 155, 321–348 (2002).

    Article  Google Scholar 

  24. Roxburgh, S. H., Shea, K. & Wilson, J. B. The intermediate disturbance hypothesis: patch dynamics and mechanisms of species coexistence. Ecology 85, 359–371 (2004).

    Article  Google Scholar 

  25. Lambers, H. & Poorter, H. Inherent variation in growth rate between higher plants: a search for physiological causes and ecological consequences. Adv. Ecol. Res. 34, 187–261 (1992).

    Article  Google Scholar 

  26. Metcalf, C. J. E. Invisible trade-offs: Van Noordwijk and de Jong and life-history evolution. Am. Nat. 187, iii–v (2016).

    Article  PubMed  Google Scholar 

  27. Van Noordwijk, A. J. & Jong, G. D. Acquisition and allocation of resources: their influence on variation in life history tactics. Am. Nat. 128, 137–142 (1986).

    Article  Google Scholar 

  28. Condit, R. et al. Importance of demographic niches to tree diversity. Science 313, 98–101 (2006).

    Article  CAS  PubMed  Google Scholar 

  29. Ricklefs, R. E. Community diversity: relative roles of local and regional processes. Science 235, 167–171 (1987).

    Article  CAS  Google Scholar 

  30. Bormann, F. H. & Likens, G. E. Pattern and Process in a Forested Ecosystem (Springer, 1979).

  31. Salguero-Gómez, R. et al. Fast–slow continuum and reproductive strategies structure plant life-history variation worldwide. Proc. Natl Acad. Sci. USA 113, 230–235 (2016).

    Article  PubMed  CAS  Google Scholar 

  32. Rüger, N. et al. Beyond the fast–slow continuum: demographic dimensions structuring a tropical tree community. Ecol. Lett. 21, 1075–1084 (2018).

    Article  PubMed  Google Scholar 

  33. McGill, B. J., Enquist, B. J., Weiher, E. & Westoby, M. Rebuilding community ecology from functional traits. Trends Ecol. Evol. 21, 178–185 (2006).

    Article  PubMed  Google Scholar 

  34. McMahon, S. M., Metcalf, C. J. E. & Woodall, C. W. High-dimensional coexistence of temperate tree species: functional traits, demographic rates, life-history stages, and their physical context. PLoS ONE 6, e16253 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Reich, P. B. The world-wide ‘fast–slow’ plant economics spectrum: a traits manifesto. J. Ecol. 102, 275–301 (2014).

    Article  Google Scholar 

  36. Marks, C. O. & Lechowicz, M. J. Alternative designs and the evolution of functional diversity. Am. Nat. 167, 55–66 (2006).

    Article  PubMed  Google Scholar 

  37. Visser, M. D. et al. Functional traits as predictors of vital rates across the life cycle of tropical trees. Funct. Ecol. 30, 168–180 (2016).

    Article  Google Scholar 

  38. Detto, M. & Xu, X. Optimal leaf life strategies determine Vc,max dynamic during ontogeny. New Phytol. https://doi.org/10.1111/nph.16712 (2020).

  39. Poorter, L. & Bongers, F. Leaf traits are good predictors of plant performance across 53 rain forest species. Ecology 87, 1733–1743 (2006).

    Article  PubMed  Google Scholar 

  40. Anderson-Teixeira, K. J. et al. CTFS-ForestGEO: a worldwide network monitoring forests in an era of global change. Glob. Change Biol. 21, 528–549 (2015).

    Article  Google Scholar 

  41. R Core Team R: A Language and Environment for Statistical Computing version 3.6.1 (R Foundation for Statistical Computing, 2017).

  42. Warton, D. I., Wright, I. J., Falster, D. S. & Westoby, M. Bivariate line-fitting methods for allometry. Biol. Rev. 81, 259–291 (2006).

    Article  PubMed  Google Scholar 

  43. Warton, D. I., Duursma, R. A., Falster, D. S. & Taskinen, S. smatr 3— an R package for estimation and inference about allometric lines. Methods Ecol. Evol. 3, 257–259 (2012).

    Article  Google Scholar 

  44. Gelman, A., Carlin, J. B., Stern, H. S. & Rubin, D. B. Bayesian Data Analysis 2nd edn (Chapman and Hall/CRC, 2004).

  45. Kenfack, D., Chuyong, G., Condit, R., Russo, S. & Thomas, D. Demographic variation and habitat specialization of tree species in a diverse tropical forest of Cameroon. For. Ecosyst. 1, 22 (2014).

    Article  Google Scholar 

  46. Condit, R. et al. Tropical forest dynamics across a rainfall gradient and the impact of an El Niño dry season. J. Trop. Ecol. 20, 51–72 (2004).

    Article  Google Scholar 

  47. Hartig, F. DHARMa: Residual Diagnostics for Hierarchical (Multi-Level / Mixed) Regression Models. R package version 0.3.3.0 (2020).

  48. Robinson, D. broom: An R Package for Converting Statistical Analysis Objects Into Tidy Data Frames. R package version 2 (2014); https://arxiv.org/abs/1412.3565

  49. Nagelkerke, N. J. D. A note on a general definition of the coefficient of determination. Biometrika 78, 691–692 (1991).

    Article  Google Scholar 

  50. Long, J. S. Regression Models for Categorical and Limited Dependent Variables (Sage, 1997).

  51. Paul-Victor, C., Züst, T., Rees, M., Kliebenstein, D. J. & Turnbull, L. A. A new method for measuring relative growth rate can uncover the costs of defensive compounds in Arabidopsis thaliana. New Phytol. 187, 1102–1111 (2010).

    Article  PubMed  CAS  Google Scholar 

  52. Coomes, D. A. & Allen, R. B. Effects of size, competition and altitude on tree growth. Ecol. Lett. 95, 1084–1097 (2007).

    Google Scholar 

  53. Björklund, M. Are ‘comparative methods’ always necessary? Oikos 80, 607–612 (1997).

    Article  Google Scholar 

  54. Losos, J. B. Uncertainty in the reconstruction of ancestral character states and limitations on the use of phylogenetic comparative methods. Anim. Behav. 58, 1319–1324 (1999).

    Article  CAS  PubMed  Google Scholar 

  55. Losos, J. B. Seeing the forest for the trees: the limitations of phylogenies in comparative biology. Am. Nat. 177, 709–727 (2011).

    Article  PubMed  Google Scholar 

  56. Stearns, S. C. The Evolution of Life Histories (Oxford Univ. Press, 1992).

  57. Rose, K. E., Atkinson, R. L., Turnbull, L. A. & Rees, M. The costs and benefits of fast living. Ecol. Lett. 12, 1379–1384 (2009).

    Article  PubMed  Google Scholar 

  58. Makana, J.-R. et al. Demography and biomass change in monodominant and mixed old-growth forest of the Congo. J. Trop. Ecol. 27, 447–461 (2011).

    Article  Google Scholar 

Download references

Acknowledgements

This research was conducted during Analytical Workshops held by the Smithsonian Center for Tropical Forest Science ForestGEO programme, supported by the National Science Foundation of the United States, grant no. DEB-1046113. S.E.R. was supported by a Faculty Development Leave Fellowship from the University of Nebraska–Lincoln and a Short-Term Fellowship from the Japan Society of the Promotion of Science. We thank A. Zera for insightful discussions of trade-offs and constructive comments on an earlier version of this manuscript. This work was generated using data from the Center for Tropical Forest Science/Smithsonian Institution Forest Global Earth Observatory network (http://www.forestgeo.si.edu/). Individual plot data collection and management and authors were supported by grants from the National Science Foundation of the United States (grant nos EF-1137366, BSR-9015961, DEB-1516066, BSR-8811902, DEB-9411973, DEB-008538, DEB-0218039 and DEB-0620910), the Council of Agriculture of Taiwan (grant nos 93AS-2.4.2-FI-G1(2) and 94AS-11.1.2-FI-G1(1)), the Ministry of Science and Technology of Taiwan (grant nos NSC92-3114-B002-009, NSC98-2313-B-029-001-MY3 and NSC98-2321-B-029-002), the Forestry Bureau of Taiwan (grant nos 92-00-2-06 and TFBM-960226), the Taiwan Forestry Research Institute (grant no. 97 AS- 7.1.1.F1-G1), the Mellon Foundation, the International Institute of Tropical Forestry of the USDA Forest Service, the University of Puerto Rico, the 1923 Fund, the Centre for Ecology and Hydrology, the German Academic Exchange Services (DAAD), Sarawak Forest Department, Sarawak Forestry Corporation, Global Environment Research Fund of the Ministry of the Environment Japan (grant no. D-0901), Japan Society for the Promotion of Science (grant no. 17H04602), The Wildlife Conservation Society, the Institut Congolais pour la Conservation de la Nature, the Thai National Parks Wildlife and Plant Conservation Department, the Center for Tropical Forest Science Arnold Arboretum Asia Program, the Smithsonian Tropical Research Institute, and the Luquillo Long Term Ecological Research programme (LuqLTER). We also thank the hundreds of people who contributed to the collection and management of the data from the plots.

Author information

Authors and Affiliations

Authors

Contributions

S.E.R. conceived and designed the study, assembled and analysed the data, and wrote the manuscript. S.E.R., G.L. and M.D. designed and analysed the theoretical model. R.S.C., S.J.D., M.D., S.M.M. and S.J.W. made important contributions to interpreting the results and to writing and revising the manuscript. R.S.C., S.J.D., P.S.A., S.B., C.-H.C.-Y., S.E., C.E.N.E., C.F., R.B.F., C.V.S.G., I.A.U.N.G., T.H., C.-F.H., S.P.H., A.I., A.R.K., Y.T.L., Y.C.L., J.-R.M., M.B.M., P.O., A.S., I.-F.S., S.T., J.T., T.Y., S.L.Y. and J.K.Z. contributed to the acquisition of the data used in the paper and in writing the manuscript. All authors have given final approval to publish this manuscript and agree to be accountable for the aspects of the work that they conducted.

Corresponding author

Correspondence to Sabrina E. Russo.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Appendix 1 containing Results and Discussion, Figs. 1–3, and Tables 1–4; and Appendix 2 containing model description, Figs. 4–7 and Table 5.

Reporting Summary

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Russo, S.E., McMahon, S.M., Detto, M. et al. The interspecific growth–mortality trade-off is not a general framework for tropical forest community structure. Nat Ecol Evol 5, 174–183 (2021). https://doi.org/10.1038/s41559-020-01340-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-020-01340-9

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing