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High herbivore pressure favors constitutive over induced defense

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ABSTRACT

Theoretical and empirical studies show that, when past or current herbivory is a reliable cue of future attack and defenses are costly, defenses can be induced only when needed and thereby permit investment in other functions such as growth or reproduction. Theory also states that, in environments where herbivory is constantly high, constitutive defenses should be favored. Here, we present data to support the second aspect of the induced resistance hypothesis. We examined herbivore‐induced responses for four species of Inga (Fabaceae), a common canopy tree in Neotropical forests. We quantified chemical defenses of expanding leaves, including phenolic, saponin and toxic amino acids, in experimental field treatments with and without caterpillars. Because young leaves lack fiber and are higher in protein than mature leaves, they typically lose >25% of their leaf area during the few weeks of expansion. We predicted that the high rates of attack would select for investment in constitutive defenses over induction. Our data show that chemical defenses were quite unresponsive to herbivory. We demonstrated that expanding leaves showed no or only small increases in investment in secondary metabolites, and no qualitative changes in the phenolic compound profile in response to herbivory. The proteinogenic amino acid tyrosine, which can be toxic at high concentrations, showed the greatest levels of induction. Synthesis: These results provide some of the first support for theoretical predictions that the evolution of induced vs. constitutive defenses depends on the risk of herbivory. In habitats with constant and high potential losses to herbivores, such as tropical rainforests, high investments in constitutive defenses are favored over induction.

No MeSH data available.


Fitness under a range of herbivory environments for two defense regimes. Adapted from Karban et al. (1999). Species that evolved with low or intermittent herbivore pressure will have higher fitness if they rely on induced defenses whereas species that have evolved with high or constant herbivore pressure will have higher fitness using constitutive defenses.
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ece32208-fig-0001: Fitness under a range of herbivory environments for two defense regimes. Adapted from Karban et al. (1999). Species that evolved with low or intermittent herbivore pressure will have higher fitness if they rely on induced defenses whereas species that have evolved with high or constant herbivore pressure will have higher fitness using constitutive defenses.

Mentions: Plants have evolved a wide diversity of antiherbivore defenses (Johnson 2011; Mithöfer and Boland 2012) and face an inherent dilemma in how they invest in those defenses (Herms and Mattson 1992). High investment in defense may result in reduced loss to herbivores, but also reduced resources for growth or reproduction. Empirical evidence has demonstrated that the cost of investing in defense can be quantified in reduced growth, lower photosynthetic production, and reduced plant fitness (Redman et al. 2001; Moore et al. 2003; Preisser et al. 2007). The fitness consequences of investing in constitutive defense are context dependent and are addressed by several hypotheses, including optimal defense, resource availability, and carbon/nutrient balance (McKey 1974, 1979; Rhoades 1979; Bryant et al. 1983; Coley et al. 1985). These hypotheses predict that plants maximize their fitness by balancing allocation to constitutive defense versus other functions based on available resources, herbivore pressure, tissue value, and cost of defense (Stamp 2003). Under conditions of low herbivore pressure, plant fitness would be maximized by investing little in constitutive defenses. In contrast, under conditions of high herbivore pressure, the fitness benefits of constitutive defenses could outweigh the fitness costs (Fig. 1).


High herbivore pressure favors constitutive over induced defense
Fitness under a range of herbivory environments for two defense regimes. Adapted from Karban et al. (1999). Species that evolved with low or intermittent herbivore pressure will have higher fitness if they rely on induced defenses whereas species that have evolved with high or constant herbivore pressure will have higher fitness using constitutive defenses.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC5016630&req=5

ece32208-fig-0001: Fitness under a range of herbivory environments for two defense regimes. Adapted from Karban et al. (1999). Species that evolved with low or intermittent herbivore pressure will have higher fitness if they rely on induced defenses whereas species that have evolved with high or constant herbivore pressure will have higher fitness using constitutive defenses.
Mentions: Plants have evolved a wide diversity of antiherbivore defenses (Johnson 2011; Mithöfer and Boland 2012) and face an inherent dilemma in how they invest in those defenses (Herms and Mattson 1992). High investment in defense may result in reduced loss to herbivores, but also reduced resources for growth or reproduction. Empirical evidence has demonstrated that the cost of investing in defense can be quantified in reduced growth, lower photosynthetic production, and reduced plant fitness (Redman et al. 2001; Moore et al. 2003; Preisser et al. 2007). The fitness consequences of investing in constitutive defense are context dependent and are addressed by several hypotheses, including optimal defense, resource availability, and carbon/nutrient balance (McKey 1974, 1979; Rhoades 1979; Bryant et al. 1983; Coley et al. 1985). These hypotheses predict that plants maximize their fitness by balancing allocation to constitutive defense versus other functions based on available resources, herbivore pressure, tissue value, and cost of defense (Stamp 2003). Under conditions of low herbivore pressure, plant fitness would be maximized by investing little in constitutive defenses. In contrast, under conditions of high herbivore pressure, the fitness benefits of constitutive defenses could outweigh the fitness costs (Fig. 1).

View Article: PubMed Central - PubMed

ABSTRACT

Theoretical and empirical studies show that, when past or current herbivory is a reliable cue of future attack and defenses are costly, defenses can be induced only when needed and thereby permit investment in other functions such as growth or reproduction. Theory also states that, in environments where herbivory is constantly high, constitutive defenses should be favored. Here, we present data to support the second aspect of the induced resistance hypothesis. We examined herbivore‐induced responses for four species of Inga (Fabaceae), a common canopy tree in Neotropical forests. We quantified chemical defenses of expanding leaves, including phenolic, saponin and toxic amino acids, in experimental field treatments with and without caterpillars. Because young leaves lack fiber and are higher in protein than mature leaves, they typically lose >25% of their leaf area during the few weeks of expansion. We predicted that the high rates of attack would select for investment in constitutive defenses over induction. Our data show that chemical defenses were quite unresponsive to herbivory. We demonstrated that expanding leaves showed no or only small increases in investment in secondary metabolites, and no qualitative changes in the phenolic compound profile in response to herbivory. The proteinogenic amino acid tyrosine, which can be toxic at high concentrations, showed the greatest levels of induction. Synthesis: These results provide some of the first support for theoretical predictions that the evolution of induced vs. constitutive defenses depends on the risk of herbivory. In habitats with constant and high potential losses to herbivores, such as tropical rainforests, high investments in constitutive defenses are favored over induction.

No MeSH data available.