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Widespread herbivory cost in tropical nitrogen-fixing tree species

Abstract

Recent observations suggest that the large carbon sink in mature and recovering forests may be strongly limited by nitrogen1,2,3. Nitrogen-fixing trees (fixers) in symbiosis with bacteria provide the main natural source of new nitrogen to tropical forests3,4. However, abundances of fixers are tightly constrained5,6,7, highlighting the fundamental unanswered question of what limits new nitrogen entering tropical ecosystems. Here we examine whether herbivory by animals is responsible for limiting symbiotic nitrogen fixation in tropical forests. We evaluate whether nitrogen-fixing trees experience more herbivory than other trees, whether herbivory carries a substantial carbon cost, and whether high herbivory is a result of herbivores targeting the nitrogen-rich leaves of fixers8,9. We analysed 1,626 leaves from 350 seedlings of 43 tropical tree species in Panama and found that: (1) although herbivory reduces the growth and survival of all seedlings, nitrogen-fixing trees undergo 26% more herbivory than non-fixers; (2) fixers have 34% higher carbon opportunity costs owing to herbivory than non-fixers, exceeding the metabolic cost of fixing nitrogen; and (3) the high herbivory of fixers is not driven by high leaf nitrogen. Our findings reveal that herbivory may be sufficient to limit tropical symbiotic nitrogen fixation and could constrain its role in alleviating nitrogen limitation on the tropical carbon sink.

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Fig. 1: Nitrogen-fixing trees exhibit higher herbivory than non-fixers in a tropical moist forest.
Fig. 2: Species differences in leaf herbivory of nitrogen-fixing and non-fixing trees in a tropical moist forest.
Fig. 3: The cost of herbivory for nitrogen-fixing trees in a tropical moist forest.

Data availability

The datasets generated during and/or analysed during the current study are available at the NERC Environmental Information Data Centre repository at https://doi.org/10.5285/67c95112-edee-435f-9355-9d8bab3a5634Source data are provided with this paper.

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Acknowledgements

The authors thank T. R. Baker for his helpful comments and ideas. W.B. acknowledges support from the Society of Experimental Biology Company of Biologists, the Smithsonian Tropical Research Institute and University of Leeds Priestley International Centre for Climate. S.A.B. acknowledges support from the UK Natural Environment Research Council (NE/M019497/1, NE/N012542/1), British Council Grant no. 275556724 and the Leverhulme Trust. Funding for the Barro Colorado Island 50-ha seedling census was provided by the US National Science Foundation (NSF DEB 1464389 to L.S.C.).

Author information

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Contributions

W.B. and S.A.B. designed the work. W.B. carried out field work. S.J.W., L.S.C. and B.E.S. provided additional data. W.B., L.S.C., S.J.W. and S.A.B. analysed the data. W.B. drafted the article and W.B., S.A.B., S.J.W., L.S.C. and O.L.P. contributed to revisions. All authors provided feedback on the final version of the manuscript.

Corresponding author

Correspondence to Sarah A. Batterman.

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Nature thanks Hans ter Steege, Joy Winbourne and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data figures and tables

Extended Data Fig. 1 The difference in herbivory and the carbon cost of herbivory for nitrogen fixer and non-fixer species.

a, The distribution of the predicted probability of herbivory on leaves of 17 fixer species and 19 non-fixer species. b, The distribution of the predicted proportion of leaf area lost to herbivory on attacked leaves of each seedling for 23 fixer species and 20 non-fixer species. c, The distribution of the geometric mean of the herbivory carbon cost as a fraction of net primary production (NPP) across species (17 fixer species, 18 non-fixer species) for fixers (orange) and non-fixers (grey). Fixers are represented in orange and non-fixers in grey. Bars in a and b represent predicted mean values (± standard error of mean) derived from our modelling of Incidence of herbivory and Proportiondamaged. Asterisks denote statistically significant differences (p = 0.02 for a, p = 0.04 for b, p = 0.04 for c) between fixers and non-fixers from two-sided non-parametric Wilcoxon rank tests. Numbers above each bar in panel c represent the number of seedlings sampled per species. Note that the number of leaves (a) and seedlings (b) sampled for each species can be found in the Supplementary Information Table 1.

Extended Data Fig. 2 The herbivory versus metabolic costs of fixation across leaf lifespan.

How the fixation-associated herbivory costs and metabolic cost of fixing nitrogen vary over leaf lifespan. Costs shown as a percentage of annual NPP per year, using the mean herbivory and leaf area for fixers and non-fixers up until the maximum leaf lifespan for shade species recorded in the 50ha plot on Barro Colorado Island (BCI). The photosynthetic opportunity cost was calculated as the accruing photosynthesis forgone until the end of the leaf lifespan (dark blue line). The structural carbon cost remained constant since the cost per year would not vary with leaf lifespan (red line). The metabolic cost represents the percentage of NPP required to replace either 40% of leaf nitrogen (at 40% light, orange line) or 0% (at 16% light, light blue line) paying six grams of carbon per gram nitrogen over one year, depending on leaf lifespan. The mean leaf lifespan for shade species in the BCI 50ha plot is 21.65 months (green line). These values differ from Fig. 3b since they are at the leaf level, use mean values as parameter estimates and consider variation in leaf lifespan.

Extended Data Fig. 3 Leaf traits that are potential drivers of herbivory in mature leaves, and herbivory measurements on young leaves.

Showing both the leaf traits that varied between fixers and non-fixers in mature leaves, and metrics of herbivory and leaf retention on young leaves. For mature leaves, the difference in a, leaf area, b, leaf nitrogen concentration, c, leaf cellulose concentration, d, leaf carbon concentration, e, leaf lignin concentration and, f, leaf potassium concentration. All differences in leaf variables for mature leaves are significant as determined by two-sided Wilcoxon rank test on n = 184 fixer and n = 166 non-fixer species. N = 43 (a), 37 (b), 38 (c), 37 (d), 38 (e) and 37 (f) biologically independent samples. For young leaves, g, the incidence of herbivory; h, the proportion of leaf area lost to herbivory per day for damaged leaves (Proportiondamaged) on each seedling; i, the proportion of leaf area lost to herbivory per day on all leaves (Proportionall) of each seedling; and, j, the proportion of sampled leaves that still remained after three months (i.e. leaves that have not been dropped by the plant). Nitrogen fixers are represented in orange and non-fixers in grey. For the measures of herbivory on young leaves there were no difference between fixers and non-fixers, as determined by two-sided non-parametric Wilcoxon rank test (n = 226 (119 fixers, 107 non-fixers)). Points represent seedlings with the lines representing means (± standard error) across seedlings; bars represent mean (± standard error).

Extended Data Table 1 Fixers undergo greater herbivory than non-fixers
Extended Data Table 2 No relationship between leaf nitrogen concentration and herbivory
Extended Data Table 3 Leaf area drives some measures of herbivory
Extended Data Table 4 No relationship between leaf carbon concentration and herbivory
Extended Data Table 5 No relationship between leaf potassium concentration and herbivory
Extended Data Table 6 No relationship between leaf cellulose concentration and herbivory
Extended Data Table 7 No relationship between leaf lignin concentration and herbivory

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Barker, W., Comita, L.S., Wright, S.J. et al. Widespread herbivory cost in tropical nitrogen-fixing tree species. Nature 612, 483–487 (2022). https://doi.org/10.1038/s41586-022-05502-6

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