Effects of herbivory and its timing on reproductive success of a tropical deciduous tree

Abstract

Background and aims: The implications of herbivory for plant reproduction have been widely studied; however, the relationship of defoliation and reproductive success is not linear, as there are many interacting factors that may influence reproductive responses to herbivore damage. In this study we aimed to disentangle how the timing of foliar damage impacts both male and female components of fitness, and to assess when it has greater impacts on plant reproductive success.

Methods: We measured herbivore damage and its effects on floral production, male and female floral attributes as well as fruit yield in three different phenological phases of Casearia nitida (Salicaceae) over the course of two consecutive years. Then we tested two models of multiple causal links among herbivory and reproductive success using piecewise structural equation models.

Key results: The effects of leaf damage differed between reproductive seasons and between male and female components of fitness. Moreover, the impact of herbivory extended beyond the year when it was exerted. The previous season's cumulated foliar damage had the largest impact on reproductive characters, in particular a negative effect on the numbers of inflorescences, flowers and pollen grains, indirectly affecting the numbers of infructescences and fruits, and a positive one on the amount of foliar damage during flowering.

Conclusions: For perennial and proleptic species, the dynamics of resource acquisition and allocation patterns for reproduction promote and extend the effects of herbivore damage to longer periods than a single reproductive event and growing season, through the interactions among different components of female and male fitness.

Keywords: Casearia nitida; Salicaceae; deciduous tree; female fitness; foliar damage; herbivory; male fitness; proleptic species; reproductive success; structural equation model; tropical dry forest.

Fig. 1.

Hypothesized causal relationships among foliar herbivory in different phenological stages and fitness traits in Casearia nitida. Boxes represent measured variables. Black and red arrows denote expected positive and negative relationships, respectively. Folivory_16cu is the cumulated foliar herbivore damage from 2016, i.e. before flowering. Folivory_flo is the foliar damage occurred during the 2017 flowering period. Folivory_fru is the damage during the fructification period. Folivory may influence macro fitness traits like inflorescence number, flower number, vegetative growth, infructescence number and fruit number (A), but also micro fitness traits, both female (flower number, seeds, floral diameter and ovule number) and male (pollen grain size and pollen grain number) (B). Plant height may impact all biological traits. Rainfall could affect the number of reproductive structures produced (flowers, inflorescences, infructescences and fruits).

Fig. 2.

Phenological state and time line.

Fig. 3.

Analysis of major characters: first structural analysis. Boxes represent measured variables. Arrows represent unidirectional relationships among variables. Black arrows denote positive relationships and red arrows negatives ones. Semitransparent arrows indicate non-significant paths (P < 0.05) that were included in the a priori model. Dotted arrows indicate the found missing paths (not included in the a priori model). The thickness of an arrow is proportional to its effect size. R_c² values for component models are given in the boxes of response variables (reported as the conditional based on the variance of both the fixed and random effects). Magnitude coefficients and significance thresholds are shown along paths. The temporal axis is located below with marked sections for each evaluated phenological moment.

Fig. 4.

Analysis of smaller characters: second structural analysis. Boxes represent measured variables. Arrows represent unidirectional relationships among variables. Black arrows denote positive relationships and red arrows negatives ones. Semitransparent arrows indicate non-significant paths (P < 0.05) that were included in the a priori model. Dotted arrows indicate the found missing paths (not included in the a priori model). The thickness of an arrow is proportional to its effect size. R_c² values for component models are given in the boxes of response variables (reported as the conditional based on the variance of both the fixed and random effects). Magnitude coefficients and significance thresholds are shown along paths. The temporal axis is located below with marked sections for each evaluated phenological moment.