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Biodiversity increases ecosystem functions despite multiple stressors on coral reefs

Abstract

Positive relationships between biodiversity and ecosystem functioning (BEF) highlight the importance of conserving biodiversity to maintain key ecosystem functions and associated services. Although natural systems are rapidly losing biodiversity due to numerous human-caused stressors, our understanding of how multiple stressors influence BEF relationships comes largely from small, experimental studies. Here, using remote assemblages of coral reef fishes, we demonstrate strong, non-saturating relationships of biodiversity with two ecosystem functions: biomass and productivity. These positive relationships were robust both to an extreme heatwave that triggered coral bleaching and to invasive rats which disrupt nutrient subsidies from native seabirds. Despite having only minor effects on BEF relationships, both stressors still decreased ecosystem functioning via other pathways. The extreme heatwave reduced biodiversity, which, due to the strong BEF relationships, ultimately diminished both ecosystem functions. Conversely, the loss of cross-system nutrient subsidies directly decreased biomass. These results demonstrate multiple ways by which human-caused stressors can reduce ecosystem functioning, despite robust BEF relationships, in natural high-diversity assemblages.

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Fig. 1: Relationships between biodiversity, ecosystem function and human disturbances on remote coral reefs.
Fig. 2: Effect of human disturbances on BEF relationships on remote coral reefs.
Fig. 3: Links between human-caused stressors, reef characteristics, biodiversity and ecosystem function.
Fig. 4: Hypothesized and observed effects of human-caused stressors on biodiversity and ecosystem function (EF).

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Data availability

The data that support the findings of this study are available on GitHub (github.com/cbenkwitt/bef-reefs).

Code availability

The code that supports the findings of this study is available on GitHub (github.com/cbenkwitt/bef-reefs).

References

  1. Brose, U. & Hillebrand, H. Biodiversity and ecosystem functioning in dynamic landscapes. Phil. Trans. R. Soc. B 371, 20150267 (2016).

    PubMed  Google Scholar 

  2. Duffy, J. E., Godwin, C. M. & Cardinale, B. J. Biodiversity effects in the wild are common and as strong as key drivers of productivity. Nature 549, 261–264 (2017).

    CAS  PubMed  Google Scholar 

  3. van der Plas, F. Biodiversity and ecosystem functioning in naturally assembled communities. Biol. Rev. 94, 1220–1245 (2019).

    PubMed  Google Scholar 

  4. Isbell, F. et al. Linking the influence and dependence of people on biodiversity across scales. Nature 546, 65–72 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Cardinale, B. J., Ives, A. R. & Inchausti, P. Effects of species diversity on the primary productivity of ecosystems: extending our spatial and temporal scales of inference. Oikos 104, 437–450 (2004).

    Google Scholar 

  6. Cardinale, B. J. et al. The functional role of producer diversity in ecosystems. Am. J. Bot. 98, 572–592 (2011).

    PubMed  Google Scholar 

  7. Thompson, P. L., Isbell, F., Loreau, M., O’Connor, M. I. & Gonzalez, A. The strength of the biodiversity–ecosystem function relationship depends on spatial scale. Proc. R. Soc. B 285, 20180038 (2018).

    PubMed  Google Scholar 

  8. Srivastava, D. S. & Vellend, M. Biodiversity–ecosystem function research: is it relevant to conservation? Annu. Rev. Ecol. Evol. Syst. 36, 267–294 (2005).

    Google Scholar 

  9. Barlow, J. et al. The future of hyperdiverse tropical ecosystems. Nature 559, 517–526 (2018).

    CAS  PubMed  Google Scholar 

  10. Clarke, D. A., York, P. H., Rasheed, M. A. & Northfield, T. D. Does biodiversity–ecosystem function literature neglect tropical ecosystems? Trends Ecol. Evol. 32, 320–323 (2017).

    PubMed  Google Scholar 

  11. Brandl, S. J. et al. Coral reef ecosystem functioning: eight core processes and the role of biodiversity. Front. Ecol. Environ. 17, 445–454 (2019).

    Google Scholar 

  12. Murphy, G. E. P. & Romanuk, T. N. A meta-analysis of declines in local species richness from human disturbances. Ecol. Evol. 4, 91–103 (2014).

    PubMed  Google Scholar 

  13. Bellard, C., Bertelsmeier, C., Leadley, P., Thuiller, W. & Courchamp, F. Impacts of climate change on the future of biodiversity. Ecol. Lett. 15, 365–377 (2012).

    PubMed  PubMed Central  Google Scholar 

  14. Bellard, C., Cassey, P. & Blackburn, T. M. Alien species as a driver of recent extinctions. Biol. Lett. 12, 20150623 (2016).

    PubMed  PubMed Central  Google Scholar 

  15. Butchart, S. H. M. et al. Global biodiversity: indicators of recent declines. Science 328, 164–1168 (2010).

    Google Scholar 

  16. Vitousek, P. M., Mooney, H. A., Lubchenco, J. & Melillo, J. M. Human domination of Earth’s ecosystems. Science 277, 494–499 (1997).

    CAS  Google Scholar 

  17. Hughes, T. P. et al. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359, 80–83 (2018).

    CAS  PubMed  Google Scholar 

  18. Pratchett, M. S., Hoey, A. S., Wilson, S. K., Messmer, V. & Graham, N. A. J. Changes in biodiversity and functioning of reef fish assemblages following coral bleaching and coral loss. Diversity 3, 424–452 (2011).

    Google Scholar 

  19. Towns, D. R., Atkinson, I. A. E. & Daugherty, C. H. Have the harmful effects of introduced rats on islands been exaggerated? Biol. Invasions 8, 863–891 (2006).

    Google Scholar 

  20. Graham, N. A. J. et al. Seabirds enhance coral reef productivity and functioning in the absence of invasive rats. Nature 559, 250–253 (2018).

    CAS  PubMed  Google Scholar 

  21. Graham, N. A. J. & McClanahan, T. R. The last call for marine wilderness? BioScience 63, 397–402 (2013).

    Google Scholar 

  22. Maire, E. et al. How accessible are coral reefs to people? A global assessment based on travel time. Ecol. Lett. 19, 351–360 (2016).

    PubMed  Google Scholar 

  23. Head, C. E. I. et al. Coral bleaching impacts from back-to-back 2015–2016 thermal anomalies in the remote central Indian Ocean. Coral Reefs 38, 605–618 (2019).

    Google Scholar 

  24. Benkwitt, C. E., Wilson, S. K. & Graham, N. A. J. Seabird nutrient subsidies alter patterns of algal abundance and fish biomass on coral reefs following a bleaching event. Glob. Change Biol. 25, 2619–2632 (2019).

    Google Scholar 

  25. 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).

    Google Scholar 

  26. Allgeier, J. E., Wenger, S. J., Rosemond, A. D., Schindler, D. E. & Layman, C. A. Metabolic theory and taxonomic identity predict nutrient recycling in a diverse food web. Proc. Natl Acad. Sci. USA 112, E2640–E2647 (2015).

    CAS  PubMed  Google Scholar 

  27. Tilman, D., Isbell, F. & Cowles, J. M. Biodiversity and ecosystem functioning. Annu. Rev. Ecol. Evol. Syst. 45, 471–493 (2014).

    Google Scholar 

  28. Bellwood, D. R., Streit, R. P., Brandl, S. J. & Tebbett, S. B. The meaning of the term ‘function’ in ecology: a coral reef perspective. Funct. Ecol. 33, 948–961 (2019).

    Google Scholar 

  29. O’Connor, M. I. et al. A general biodiversity–function relationship is mediated by trophic level. Oikos 126, 18–31 (2017).

    Google Scholar 

  30. Mora, C., Danovaro, R. & Loreau, M. Alternative hypotheses to explain why biodiversity–ecosystem functioning relationships are concave-up in some natural ecosystems but concave-down in manipulative experiments. Sci. Rep. 4, 5427 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Mora, C. et al. Global human footprint on the linkage between biodiversity and ecosystem functioning in reef fishes. PLoS Biol. 9, e1000606 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Lefcheck, J. S. et al. Tropical fish diversity enhances coral reef functioning across multiple scales. Sci. Adv. 5, eaav6420 (2019).

    PubMed  PubMed Central  Google Scholar 

  33. Wilson, S. K., Robinson, J. P. W., Chong-Seng, K., Robinson, J. & Graham, N. A. J. Boom and bust of keystone structure on coral reefs. Coral Reefs 38, 625–635 (2019).

    Google Scholar 

  34. Morais, R. A. & Bellwood, D. R. Pelagic subsidies underpin fish productivity on a degraded coral reef. Curr. Biol. 29, 1521–1527 (2019).

    CAS  PubMed  Google Scholar 

  35. Brandl, S. J. et al. Demographic dynamics of the smallest marine vertebrates fuel coral reef ecosystem functioning. Science 364, 1189–1192 (2019).

    CAS  PubMed  Google Scholar 

  36. Graham, N. A. J. et al. Dynamic fragility of oceanic coral reef ecosystems. Proc. Natl Acad. Sci. USA 103, 8425–8429 (2006).

    CAS  PubMed  Google Scholar 

  37. Robinson, J. P. W., Wilson, S. K., Jennings, S. & Graham, N. A. J. Thermal stress induces persistently altered coral reef fish assemblages. Glob. Change Biol. 25, 2739–2750 (2019).

    Google Scholar 

  38. Wilson, S. K., Graham, N. A. J., Pratchett, M. S., Jones, G. P. & Polunin, N. V. C. Multiple disturbances and the global degradation of coral reefs: are reef fishes at risk or resilient? Glob. Change Biol. 12, 2220–2234 (2006).

    Google Scholar 

  39. Taylor, B. M. et al. Synchronous biological feedbacks in parrotfishes associated with pantropical coral bleaching. Glob. Change Biol. 26, 1285–1294 (2020).

    Google Scholar 

  40. Graham, N. A. J. et al. Human disruption of coral reef trophic structure. Curr. Biol. 27, 231–236 (2017).

    CAS  PubMed  Google Scholar 

  41. Morais, R. A. & Bellwood, D. R. Global drivers of reef fish growth. Fish Fish. 19, 874–889 (2018).

    Google Scholar 

  42. Gust, N., Choat, J. & Ackerman, J. Demographic plasticity in tropical reef fishes. Mar. Biol. 140, 1039–1051 (2002).

    Google Scholar 

  43. Clifton, K. Asynchronous food availability on neighboring Caribbean coral reefs determines seasonal patterns of growth and reproduction for the herbivorous parrotfish Scarus iserti. Mar. Ecol. Prog. Ser. 116, 39–46 (1995).

    Google Scholar 

  44. Doughty, C. E. et al. Global nutrient transport in a world of giants. Proc. Natl Acad. Sci. USA 113, 868–873 (2016).

    CAS  PubMed  Google Scholar 

  45. Cardinale, B. J. et al. Biodiversity loss and its impact on humanity. Nature 486, 59–67 (2012).

    CAS  PubMed  Google Scholar 

  46. Sheppard, C. R. C. et al. Reefs and islands of the Chagos Archipelago, Indian Ocean: why it is the world’s largest no-take marine protected area. Aquat. Conserv. Mar. Freshw. Ecosyst. 22, 232–261 (2012).

    CAS  Google Scholar 

  47. Sheppard, C. R. C. et al. Coral bleaching and mortality in the Chagos Archipelago. Atoll Res. Bull. 613, 1–26 (2017).

    Google Scholar 

  48. Polunin, N. V. C. & Roberts, C. M. Greater biomass and value of target coral-reef fishes in two small Caribbean marine reserves. Mar. Ecol. Prog. Ser. 100, 167–176 (1993).

    Google Scholar 

  49. Wilson, S. K., Graham, N. A. J. & Polunin, N. V. C. Appraisal of visual assessments of habitat complexity and benthic composition on coral reefs. Mar. Biol. 151, 1069–1076 (2007).

    Google Scholar 

  50. Chao, A. et al. Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecol. Monogr. 84, 45–67 (2014).

    Google Scholar 

  51. Hsieh, T. C., Ma, K. H. & Chao, A. iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol. Evol. 7, 1451–1456 (2016).

    Google Scholar 

  52. Hsieh, T. C., Ma, K. H. & Chao, A. iNEXT: iNterpolation and EXTrapolation for species diversity. R package version 2.0.19 http://chao.stat.nthu.edu.tw/blog/software-download/ (2019).

  53. Chao, A. & Jost, L. Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology 93, 2533–2547 (2012).

    PubMed  Google Scholar 

  54. Chao, A. Nonparametric estimation of the number of classes in a population. Scand. J. Stat. 11, 265–270 (1984).

    Google Scholar 

  55. Chao, A. Estimating the population size for capture-recapture data with unequal catchability. Biometrics 43, 783–791 (1987).

    CAS  PubMed  Google Scholar 

  56. Froese, R. & Pauly, D. FishBase (2018); www.fishbase.org

  57. D’agata, S. et al. Human-mediated loss of phylogenetic and functional diversity in coral reef fishes. Curr. Biol. 24, 555–560 (2014).

    PubMed  Google Scholar 

  58. Richardson, L. E., Graham, N. A. J., Pratchett, M. S., Eurich, J. G. & Hoey, A. S. Mass coral bleaching causes biotic homogenization of reef fish assemblages. Glob. Change Biol. 24, 3117–3129 (2017).

    Google Scholar 

  59. Yeager, L. A., Deith, M. C. M., McPherson, J. M., Williams, I. D. & Baum, J. K. Scale dependence of environmental controls on the functional diversity of coral reef fish communities. Glob. Ecol. Biogeogr. 26, 1177–1189 (2017).

    Google Scholar 

  60. Hobson, E. S. Feeding relationships of teleostean fishes on coral reefs in Kona, Hawaii. Fish Bull. 72, 915–1031 (1974).

    Google Scholar 

  61. Gajdzik, L., Parmentier, E., Sturaro, N. & Frédérich, B. Trophic specializations of damselfishes are tightly associated with reef habitats and social behaviours. Mar. Biol. 163, 249 (2016).

    Google Scholar 

  62. Alwany, M. Distribution and feeding ecology of the angelfishes (Pomacanthidae) in Shalateen region, Red Sea, Egypt. Egypt. J. Aquat. Biol. Fish. 13, 79–91 (2009).

    Google Scholar 

  63. Depczynski, M., Fulton, C. J., Marnane, M. J. & Bellwood, D. R. Life history patterns shape energy allocation among fishes on coral reefs. Oecologia 153, 111–120 (2007).

    PubMed  Google Scholar 

  64. Pauly, D. On the interrelationships between natural mortality, growth parameters, and mean environmental temperature in 175 fish stocks. ICES J. Mar. Sci. 39, 175–192 (1980).

    Google Scholar 

  65. Zuur, A. F., Ieno, E. N., Walker, N. J., Saveliev, A. A. & Smith, G. M. Mixed Effects Models and Extensions in Ecology with R (Springer, 2009).

  66. Fox, J. & Weisberg, S. An R Companion to Applied Regression 3rd edn (Sage, 2019).

  67. Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & R Core Team nlme: linear and nonlinear mixed effects models. R package version 3.1-141 (2019).

  68. Lüdecke, D. ggeffects: tidy data frames of marginal effects from regression models. J. Open Source Softw. 3, 772 (2018).

    Google Scholar 

  69. Rosseel, Y. lavaan: an R package for structural equation modeling. J. Stat. Softw. 48, 1–36 (2012).

    Google Scholar 

  70. Epskcamp, S. semPlot: unified visualizations of structural equation models. Struct. Equ. Model. 22, 474–483 (2015).

    Google Scholar 

  71. Hu, L. & Bentler, P. M. Cutoff criteria for fit indexes in covariance structure analysis: conventional criteria versus new alternatives. Struct. Equ. Model. 6, 1–55 (1999).

    Google Scholar 

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Acknowledgements

We thank the United Kingdom Foreign and Commonwealth Office and the British Indian Ocean Territory Administration for granting us permission to undertake this research. This project was funded by the Australian Research Council, Royal Society and the Bertarelli Foundation and contributed to the Bertarelli Programme in Marine Science. We thank R. Morais for help with productivity calculations and R. Evans, C. Mora and J. Robinson for constructive feedback on the manuscript. Fish illustrations are from Tracey Saxby, Integration and Application Network, University of Maryland Center for Environmental Science (ian.umces.edu/imagelibrary/).

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C.E.B. and N.A.J.G. conceived this study; C.E.B., N.A.J.G. and S.K.W. collected the data; C.E.B. conducted the analyses; C.E.B. wrote the manuscript with input from N.A.J.G. and S.K.W.

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Correspondence to Cassandra E. Benkwitt.

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Extended data

Extended Data Fig. 1 Estimated effects of biodiversity and human disturbance on biomass of fishes on remote coral reefs.

Models were run using observed species richness (dark blue) and estimated species richness (light blue). Points represent scaled estimates (mean-centered and scaled by one standard deviation) from linear mixed-effects models, thick lines represent 75% confidence intervals, and thin lines represent 95% CIs. For non-scaled estimates of all explanatory variables, see Supplementary Tables 1 and 2.

Extended Data Fig. 2 Estimated effects of biodiversity and human disturbance on productivity of fishes on remote coral reefs.

Models were run using a, observed species richness and b, estimated species richness. Productivity was calculated in four ways, assuming: no difference in Kmax between rat-free versus rat-infested islands (‘0%’), 10% higher Kmax around rat-free islands, 25% higher Kmax around rat-free islands, and 45% higher Kmax around rat-free islands (see Methods). Separate models were run for each productivity estimate, and colours represent these different models. Points represent scaled estimates from linear mixed-effects models, thick lines represent 75% confidence intervals, and thin lines represent 95% CIs. For non-scaled estimates of all explanatory variables from models assuming no difference in Kmax, see Supplementary Tables 1 and 2.

Extended Data Fig. 3 Estimated effects of human disturbance on biodiversity on remote coral reefs.

Models were run using observed species richness (dark blue) and estimated species richness (light blue) as response variables. Points represent scaled estimates from linear mixed-effects models, thick lines represent 75% confidence intervals, and thin lines represent 95% CIs. For non-scaled estimates of all explanatory variables, see Supplementary Table 1.

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Benkwitt, C.E., Wilson, S.K. & Graham, N.A.J. Biodiversity increases ecosystem functions despite multiple stressors on coral reefs. Nat Ecol Evol 4, 919–926 (2020). https://doi.org/10.1038/s41559-020-1203-9

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