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Tree phytochemical diversity and herbivory are higher in the tropics

Nature Ecology & Evolution volume 8, pages 1426–1436 (2024)Cite this article

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Abstract

A long-standing but poorly tested hypothesis in plant ecology and evolution is that biotic interactions play a more important role in producing and maintaining species diversity in the tropics than in the temperate zone. A core prediction of this hypothesis is that tropical plants deploy a higher diversity of phytochemicals within and across communities because they experience more herbivore pressure than temperate plants. However, simultaneous comparisons of phytochemical diversity and herbivore pressure in plant communities from the tropical to the temperate zone are lacking. Here we provide clear support for this prediction by examining phytochemical diversity and herbivory in 60 tree communities ranging from species-rich tropical rainforests to species-poor subalpine forests. Using a community metabolomics approach, we show that phytochemical diversity is higher within and among tropical tree communities than within and among subtropical and subalpine communities, and that herbivore pressure and specialization are highest in the tropics. Furthermore, we show that the phytochemical similarity of trees has little phylogenetic signal, indicating rapid divergence between closely related species. In sum, we provide several lines of evidence from entire tree communities showing that biotic interactions probably play an increasingly important role in generating and maintaining tree diversity in the lower latitudes.

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Fig. 1: Geographic location, forest landscapes, and phylogenetic and elevational distributions of chemical profiles across the three forest types.
Fig. 2: Phytochemical variation and diversity (alpha and beta) among three forest types for whole metabolite profiles.
Fig. 3: Herbivory damage and specialization across the elevational gradient.

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Data availability

The MS data (.mzML) have been deposited in the MassIVE public repository and are available under accession number MSV000092950. The datasets analysed in the current study, including the molecular network, sample–sample chemical structural and compositional similarity, plot-species-abundance community data, phytochemical richness and the phylogenetic tree of 206 tree species, are available via Figshare at https://doi.org/10.6084/m9.figshare.22758269 (ref. 69).

Code availability

The R code used in the current study is available via Figshare at https://doi.org/10.6084/m9.figshare.22758269 (ref. 69).

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Acknowledgements

This research was supported by the NSFC China–US Dimensions of Biodiversity Grant (DEB: no. 32061123003 to M.C.); the National Natural Science Foundation of China (grant nos. 32201318 to L.S. and 31870410 to J.Y.); the Chinese Academy of Sciences Youth Innovation Promotion Association (grant no. Y202080 to J.Y.); the Distinguished Youth Scholar of Yunnan (grant no. 202101AV070005 to J.Y.); the Ten Thousand Talent Plans for Young Top-Notch Talents of Yunnan Province (grant no. YNWR-QNBJ-2018-309 to J.Y.); a Postdoctoral Fellowship of Xishuangbanna Tropical Botanical Garden, CAS, to L.S.; the Postdoctoral Science Foundation of Yunnan Province to L.S.; the 14th Five-Year Plan of the Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences (grant nos. XTBG-1450101 and E3ZKFF2B01 to J.Y.); and an NSF US–China Dimensions of Biodiversity Grant (DEB: no. 2124466) to N.G.S. We acknowledge support from Xishuangbanna Station for Tropical Rain Forest Ecosystem Studies, Ailaoshan Station for Subtropical Forest Ecosystem Studies and Lijiang Forest Ecosystem Research Station. We thank the Molecular Biology Experiment Center in Germplasm Bank of Wild Species, Chinese Academy of Sciences, for facilitating the extraction of plant metabolites, and the State Key Laboratory of Phytochemistry and Plant Resources in West China, Chinese Academy of Sciences, for performing the UHPLC–MS/MS analysis. We thank J. Wang, C. Xu, P. Song, T. Liang and many local residents for their assistance in collecting leaf samples. We also thank J. Yang, H. Liu and Y. Tan for their kind assistance during extracting plant metabolites and metabolite analysis.

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Authors and Affiliations

  1. CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, China

    Lu Sun, Yunyun He, Min Cao, Xuezhao Wang & Jie Yang

  2. University of Chinese Academy Sciences, Beijing, China

    Yunyun He & Xuezhao Wang

  3. School of Ethnic Medicine, Key Lab of Chemistry in Ethnic Medicinal Resources, State Ethnic Affairs Commission & Ministry of Education of China, Yunnan Minzu University, Kunming, China

    Xiang Zhou

  4. Department of Biological Sciences, University of Notre Dame, Notre Dame, IN, USA

    Nathan G. Swenson

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Contributions

J.Y., L.S. and N.G.S. designed the study. M.C. set up the forest inventory plots. L.S., X.Z., Y.H. and X.W. collected and processed the metabolomics data. L.S., Y.H. and X.W. collected and processed the leaf samples. L.S. and J.Y. analysed the data with input from all authors. J.Y., N.G.S. and L.S. wrote the paper. All authors provided feedback on the final version of the paper.

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Correspondence to Jie Yang.

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Extended data

Extended Data Fig. 1 Observed phytochemical alpha diversity for seven biosynthetic pathway categories within each climatic zone (tropical, sub-tropical and sub-alpine) with diverse q exponents (Qorder = 0, 1, 2).

(a) terpenoids (n = 20 in tropical zone, n = 20 in sub-tropical zone, n = 20 in sub-alpine zone, for one of q exponents), (b) shikimates and phenylpropanoids (n = 20 in tropical zone, n = 20 in sub-tropical zone, n = 20 in sub-alpine zone, for one of q exponents), (c) polyketides (n = 20 in tropical zone, n = 20 in sub-tropical zone, n = 20 in sub-alpine zone, for one of q exponents), (d) alkaloids (n = 20 in tropical zone, n = 20 in sub-tropical zone, n = 20 in sub-alpine zone, for one of q exponents), (e) fatty acids (n = 20 in tropical zone, n = 20 in sub-tropical zone, n = 17 in sub-alpine zone, for one of q exponents), (f) amino acids/peptides (n = 18 in tropical zone, n = 19 in sub-tropical zone, n = 12 in sub-alpine zone, for one of q exponents), (g) carbohydrates (n = 17 in tropical zone, n = 20 in sub-tropical zone, n = 17 in sub-alpine zone, for one of q exponents). In all panels, the significance of difference of phytochemical alpha diversity across forest type pairs were tested using a one-way ANOVA with a post-hoc Tukey test. In boxplots: the centre line represents the median; the lower and upper hinges correspond to the 25th and 75th percentiles; the lower and upper whiskers extend to the lowest and highest points to a limit of 1.5× the interquartile range from the closest hinge.

Extended Data Fig. 2 Observed phytochemical beta diversity for seven biosynthetic pathway categories within each climatic zone (tropical, sub-tropical and sub-alpine) with diverse q exponents (Qorder = 0, 1, 2).

(a) terpenoids (n = 190 in tropical zone, n = 190 in sub-tropical zone, n = 190 in sub-alpine zone, for one of q exponents), (b) shikimates and phenylpropanoids (n = 190 in tropical zone, n = 190 in sub-tropical zone, n = 190 in sub-alpine zone, for one of q exponents), (c) polyketides (n = 190 in tropical zone, n = 190 in sub-tropical zone, n = 190 in sub-alpine zone, for one of q exponents), (d) alkaloids (n = 190 in tropical zone, n = 190 in sub-tropical zone, n = 190 in sub-alpine zone, for one of q exponents), (e) fatty acids (n = 190 in tropical zone, n = 190 in sub-tropical zone, n = 136 in sub-alpine zone, for one of q exponents), (f) amino acids/peptides (n = 153 in tropical zone, n = 171 in sub-tropical zone, n = 66 in sub-alpine zone, for one of q exponents), (g) carbohydrates (n = 136 in tropical zone, n = 190 in sub-tropical zone, n = 136 in sub-alpine zone, for one of q exponents). In all panels, the significance of difference of phytochemical beta diversity across forest type pairs were tested using a one-way ANOVA with a post-hoc Tukey test. In boxplots: the centre line represents the median; the lower and upper hinges correspond to the 25th and 75th percentiles; the lower and upper whiskers extend to the lowest and highest points to a limit of 1.5× the interquartile range from the closest hinge.

Extended Data Fig. 3 Distance-decay curves for the whole plant specialized metabolites with diverse q exponents of 0, 1, 2.

The rate of decay (slope) and corresponding significance level were estimated by regressing the chemical similarity against elevational distance via generalized linear model with link log and a quasi-binomial family. The trend lines represent linear fits from regressions, and coloured shaded areas indicate 95% confidence interval (CI) of the prediction. Colours denote whole study region (grey), tropical zone (red), sub-tropical zone (blue) and sub-alpine zone (yellow). Panels, a, d, g and j show the slope of the relationship when q exponents is 0. Panels, b, e, h and k. show the slope of the relationship when q exponents is 1. Panels, c, f, i and l show the slope of the relationship when q exponents is 2.

Extended Data Fig. 4 Distance-decay curves for the plant specialized metabolites on terpenoids with diverse q exponents of 0, 1, 2.

The rate of decay (slope) and corresponding significance level were estimated by regressing the chemical similarity against elevational distance via generalized linear model with link log and a quasi-binomial family. The trend lines represent linear fits from regressions, and coloured shaded areas indicate 95% confidence interval (CI) of the prediction. Colours denote whole study region (grey), tropical zone (red), sub-tropical zone (blue) and sub-alpine zone (yellow). Panels, a, d, g and j show the slope of the relationship when q exponents is 0. Panels, b, e, h and k. show the slope of the relationship when q exponents is 1. Panels, c, f, i and l show the slope of the relationship when q exponents is 2.

Extended Data Fig. 5 Distance-decay curves for the plant specialized metabolites on shikimates and phenylpropanoids with diverse q exponents of 0, 1, 2.

The rate of decay (slope) and corresponding significance level were estimated by regressing the chemical similarity against elevational distance via generalized linear model with link log and a quasi-binomial family. The trend lines represent linear fits from regressions, and coloured shaded areas indicate 95% confidence interval (CI) of the prediction. Colours denote whole study region (grey), tropical zone (red), sub-tropical zone (blue) and sub-alpine zone (yellow). Panels, a, d, g and j show the slope of the relationship when q exponents is 0. Panels, b, e, h and k. show the slope of the relationship when q exponents is 1. Panels, c, f, i and l show the slope of the relationship when q exponents is 2.

Extended Data Fig. 6 Distance-decay curves for the plant specialized metabolites on polyketides with diverse q exponents of 0, 1, 2.

The rate of decay (slope) and corresponding significance level were estimated by regressing the chemical similarity against elevational distance via generalized linear model with link log and a quasi-binomial family. The trend lines represent linear fits from regressions, and coloured shaded areas indicate 95% confidence interval (CI) of the prediction. Colours denote whole study region (grey), tropical zone (red), sub-tropical zone (blue), sub-alpine zone (yellow). Panels, a, d, g and j show the slope of the relationship when q exponents is 0. Panels, b, e, h and k. show the slope of the relationship when q exponents is 1. Panels, c, f, i and l show the slope of the relationship when q exponents is 2.

Extended Data Fig. 7 Distance-decay curves for the plant specialized metabolites on alkaloids with diverse q exponents of 0, 1, 2.

The rate of decay (slope) and corresponding significance level were estimated by regressing the chemical similarity against elevational distance via generalized linear model with link log and a quasi-binomial family. The trend lines represent linear fits from regressions, and coloured shaded areas indicate 95% confidence interval (CI) of the prediction. Colours denote whole study region (grey), tropical zone (red), sub-tropical zone (blue) and sub-alpine zone (yellow). Panels, a, d, g and j show the slope of the relationship when q exponents is 0. Panels, b, e, h and k. show the slope of the relationship when q exponents is 1. Panels, c, f, i and l show the slope of the relationship when q exponents is 2.

Extended Data Fig. 8 Distance-decay curves for the plant specialized metabolites on fatty acids with diverse q exponents of 0, 1, 2.

The rate of decay (slope) and corresponding significance level were estimated by regressing the chemical similarity against elevational distance via generalized linear model with link log and a quasi-binomial family. The trend lines represent linear fits from regressions, and coloured shaded areas indicate 95% confidence interval (CI) of the prediction. Colours denote whole study region (grey), tropical zone (red), sub-tropical zone (blue) and sub-alpine zone (yellow). Panels, a, d, g and j show the slope of the relationship when q exponents is 0. Panels, b, e, h and k. show the slope of the relationship when q exponents is 1. Panels, c, f, i and l show the slope of the relationship when q exponents is 2.

Extended Data Fig. 9 Distance-decay curves for the plant specialized metabolites on amino acids/ peptides with diverse q exponents of 0, 1, 2.

The rate of decay (slope) and corresponding significance level were estimated by regressing the chemical similarity against elevational distance via generalized linear model with link log and a quasi-binomial family. The trend lines represent linear fits from regressions, and coloured shaded areas indicate 95% confidence interval (CI) of the prediction. Colours denote whole study region (grey), tropical zone (red), sub-tropical zone (blue) and sub-alpine zone (yellow). Panels, a, d, g and j show the slope of the relationship when q exponents is 0. Panels, b, e, h and k. show the slope of the relationship when q exponents is 1. Panels, c, f, i and l show the slope of the relationship when q exponents is 2.

Extended Data Fig. 10 Distance-decay curves for the plant specialized metabolites on carbohydrates with diverse q exponents of 0, 1, 2.

The rate of decay (slope) and corresponding significance level were estimated by regressing the chemical similarity against elevational distance via generalized linear model with link log and a quasi-binomial family. The trend lines represent linear fits from regressions, and coloured shaded areas indicate 95% confidence interval (CI) of the prediction. Colours denote whole study region (grey), tropical zone (red), sub-tropical zone (blue) and sub-alpine zone (yellow). Panels, a, d, g and j show the slope of the relationship when q exponents is 0. Panels, b, e, h and k. show the slope of the relationship when q exponents is 1. Panels, c, f, i and l show the slope of the relationship when q exponents is 2.

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Supplementary Figs. 1–6, Tables 1–7, materials and methods.

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Sun, L., He, Y., Cao, M. et al. Tree phytochemical diversity and herbivory are higher in the tropics. Nat Ecol Evol 8, 1426–1436 (2024). https://doi.org/10.1038/s41559-024-02444-2

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