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Does the Growth Differentiation Balance Hypothesis Explain Allocation to Secondary Metabolites in Combretum apiculatum , an African Savanna Woody Species?

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Abstract

The growth differentiation balance hypothesis (GDBH) provides a framework that predicts a trade-off between costs of secondary metabolites (SMs) relative to the demand for photosynthate by growth. However, this hypothesis was developed using empirical evidence from plant species in northern boreal and temperate systems, leaving its applicability to species under different abiotic and biotic conditions questionable and generalizations problematic. The objective of this study was to investigate whether the GDBH explains allocation to SMs in the deciduous African savanna woody species C. apiculatum along a 6-point N gradient. The cornerstone prediction of the GDBH, i.e., the parabolic response in SMs along the N gradient, was not observed, with secondary metabolism showing compound-specific responses. Quercetin, myricetin, and kaempferol glycoside concentrations, all produced via the same pathway, responded differently across the N gradient. Flavonol glycoside, cinnamic acid, and quercetin glycoside concentrations decreased as N increased, which provides partial support for the carbon nutrient balance hypothesis. Simulated herbivory had no effect on photosynthesis, decreased foliar N and consequently increased C:N ratio, but did not induce an increase in SMs, with condensed tannins and flavonol glycosides being unaffected. Defoliated plants at low N concentration compensated for lost biomass, which suggests a tolerance response, but as predicted by the limiting resource model, plants at higher N concentration were evidently C limited and thus unable to compensate. Our results show that the GDBH does not explain allocation to SMs in C. apiculatum, and suggest that mechanistic explanations of plant allocation should consider the integrative defensive effect of changed SMs.

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Acknowledgements

This research was funded by the National Research Foundation (South Africa) and the Swedish International Development Agency (Grant 48494 of the NRF Sweden-South Africa Programme). Michael Cramer and William Bond provided advice on the experimental setup. Edward Chirwa assisted with feeding and harvesting the plants. Jeremy Midgley, Christina Skarpe, William Foley, and Pekka Niemelä commented on previous versions of the manuscript. Any opinions, findings and conclusions or recommendations expressed in this material are those of the authors and therefore the NRF does not accept any liability in regard thereto.

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Authors and Affiliations

  1. Department of Biological Sciences, University of Cape Town, Rondebosch, Cape Town, 7701, South Africa

    Dawood Hattas

  2. Department of Agriculture, University of Zululand, Mangeze, South Africa

    Peter F. Scogings

  3. Natural Product Research Laboratory, Department of Biology, University of Eastern Finland, Joensuu, Finland

    Riitta Julkunen-Tiitto

  4. School of Life Sciences, University of KwaZulu-Natal, Private Bag X54001, Durban, 4000, South Africa

    Peter F. Scogings

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  1. Dawood Hattas
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Correspondence to Dawood Hattas.

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Hattas, D., Scogings, P.F. & Julkunen-Tiitto, R. Does the Growth Differentiation Balance Hypothesis Explain Allocation to Secondary Metabolites in Combretum apiculatum , an African Savanna Woody Species? . J Chem Ecol 43, 153–163 (2017). https://doi.org/10.1007/s10886-016-0808-6

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