Plant defence as a complex and changing phenotype throughout ontogeny

Abstract

Background and Aims Ontogenetic changes in anti-herbivore defences are common and result from variation in resource availability and herbivore damage throughout plant development. However, little is known about the simultaneous changes of multiple defences across the entire development of plants, and how such changes affect plant damage in the field. The aim of this study was to assess if changes in the major types of plant resistance and tolerance can explain natural herbivore damage throughout plant ontogeny. Methods An assessment was made of how six defensive traits, including physical, chemical and biotic resistance, simultaneously change across the major transitions of plant development, from seedlings to reproductive stages of Turnera velutina growing in the greenhouse. In addition, an experiment was performed to assess how plant tolerance to artificial damage to leaves changed throughout ontogeny. Finally, leaf damage by herbivores was evaluated in a natural population. Key Results The observed ontogenetic trajectories of all defences were significantly different, sometimes showing opposite directions of change. Whereas trichome density, leaf toughness, extrafloral nectary abundance and nectar production increased, hydrogen cyanide and compensatory responses decreased throughout plant development, from seedlings to reproductive plants. Only water content was higher at the intermediate juvenile ontogenetic stages. Surveys in a natural population over 3 years showed that herbivores consumed more tissue from juvenile plants than from younger seedlings or older reproductive plants. This is consistent with the fact that juvenile plants were the least defended stage. Conclusions The results suggest that defensive trajectories are a mixed result of predictions by the Optimal Defence Theory and the Growth-Differentiation Balance Hypothesis. The study emphasizes the importance of incorporating multiple defences and plant ontogeny into further studies for a more comprehensive understanding of plant defence evolution.

Future directions in the ontogeny of plant defence: understanding the evolutionary causes and consequences

“…; Barton ; Ochoa‐Lopez et al . ). If ontogenetic trajectories in plant defence are indeed adaptive, the regulatory mechanisms behind their expression are likely to be important targets of selection.…”

“…Similarly, myrmecophytic plants often have greater reward production in extrafloral nectaries of leaves close to reproductive structures, suggesting a more intense selective pressure of herbivores during the reproductive stage (Ochoa‐Lopez et al . ), although this remains to be formally tested. Overall, there is a lack of data on stage‐specific herbivore selection pressures, and this represents a fair challenge for our understanding of the evolution of defence ontogenetic trajectories.…”

“…; Ochoa‐Lopez et al . ), as soon as cotyledon resources are depleted, seedlings are predicted to forgo production of secondary metabolites until enough photosynthetic tissue is produced to reach a balance between below‐ and above‐ground biomass (Bryant et al . ).…”

“…When ontogenetic trajectories are not linear (Ochoa‐Lopez et al . ), however, finding a parameter to synthesise the ontogenetic trajectories can represent a greater challenge. Although there are some studies reporting genetic variation in the degree of ontogenetic change in plant defence (Bowers & Stamp ; Schappert & Shore ; Goodger et al .…”

Ontogenetic changes in the phenotypic integration and modularity of leaf functional traits

“…Ontogenetic changes in laminar area:perimeter ratio, specific leaf area, percent of parenchyma and stomatal length and density have been also reported in different habitats, as is the case for Lasthenia species associated with terrestrial or vernal pool habitats (Forrestel et al., ). Because the expression of multiple plant defences can also vary throughout plant ontogeny (see Barton, ; Ochoa‐López, Villamil, Zedillo‐Avelleyra, & Boege, ; Quintero, Lampert, & Bowers, ), changes in trade‐offs and correlations between leaf economic and defensive traits during plant development are expected (Arntz & Delph, ). For example, Mason and Donovan () demonstrated that ontogenetic changes in leaf economic traits are conditioned by resource trade‐offs with plant defence in three species of Helianthus .…”