Costs of defense and a test of the carbon-nutrient balance and growth-differentiation balance hypotheses for two co-occurring classes of plant defense

Abstract

One of the goals of chemical ecology is to assess costs of plant defenses. Intraspecific trade-offs between growth and defense are traditionally viewed in the context of the carbon-nutrient balance hypothesis (CNBH) and the growth-differentiation balance hypothesis (GDBH). Broadly, these hypotheses suggest that growth is limited by deficiencies in carbon or nitrogen while rates of photosynthesis remain unchanged, and the subsequent reduced growth results in the more abundant resource being invested in increased defense (mass-balance based allocation). The GDBH further predicts trade-offs in growth and defense should only be observed when resources are abundant. Most support for these hypotheses comes from work with phenolics. We examined trade-offs related to production of two classes of defenses, saponins (triterpenoids) and flavans (phenolics), in Pentaclethra macroloba (Fabaceae), an abundant tree in Costa Rican wet forests. We quantified physiological costs of plant defenses by measuring photosynthetic parameters (which are often assumed to be stable) in addition to biomass. Pentaclethra macroloba were grown in full sunlight or shade under three levels of nitrogen alone or with conspecific neighbors that could potentially alter nutrient availability via competition or facilitation. Biomass and photosynthesis were not affected by nitrogen or competition for seedlings in full sunlight, but they responded positively to nitrogen in shade-grown plants. The trade-off predicted by the GDBH between growth and metabolite production was only present between flavans and biomass in sun-grown plants (abundant resource conditions). Support was also only partial for the CNBH as flavans declined with nitrogen but saponins increased. This suggests saponin production should be considered in terms of detailed biosynthetic pathway models while phenolic production fits mass-balance based allocation models (such as the CNBH). Contrary to expectations based on the two defense hypotheses, trade-offs were found between defenses and photosynthesis, indicating that studies of plant defenses should include direct measures of physiological responses.

Figure 1. Schematic of experimental design.

Seeds were planted individually or in competition with four conspecific neighbors and growth at low, intermediate, or high nitrogen levels. There were ten replicate pots per nitrogen x competition combination, five of which were grown in a shadehouse, and five of which were grown in full sunlight. The two light levels were analyzed as separate experiments (a). The photograph shows a sun-grown (left) and shade-grown plant (right) side by side (b).

Figure 2. Means (SE) of photosynthesis, dark respiration, biomass, and carbon-based metabolites.

Values are from Pentaclethra macroloba seedlings grown in shade (a, c) or full sunlight (b, d) with and without competition.

Figure 3. Interactions between experimental treatments and trade-offs in photosynthesis, growth, and defense production.

Path diagrams showing causal relationships (single headed arrows) and correlations (double headed arrows) between competition, fertilizer, photosynthesis (A_max), flavans, saponins, and biomass in Pentaclethra macroloba seedlings grown in the shade (A; χ² = 0.8, df = 5, P = 0.98) or the sun (B; χ² = 0.02, df = 1, P = 0.89). Bullets indicate negative relationships and arrows indicate positive relationships. Numbers are the standardized parameter estimates for relationships between variables. All relationships were significant with t-values >1.96 except where smaller t-values are indicated.