When resources don't rescue: flowering phenology and species interactions affect compensation to herbivory in Ipomopsis aggregata

Abstract

The ability of plants to tolerate, or compensate for, herbivore damage is highly variable and has been the subject of much research. Although many plants can compensate for herbivore damage, and some even overcompensate, we cannot yet generalize about the conditions that promote a positive response to damage. Here, we asked how abiotic resources (i.e. plant nutrient status) coupled with biotic interactions – i.e. subsequent interactions with pollinators, seed predators and nectar robbing bumble bees – affect the compensatory ability of Ipomopsis aggregata, a monocarpic herb that has been the subject of much previous debate. We hypothesized that compensation to herbivore damage in I. aggregata (Polemoniaceae) would depend first on plants having an ample supply of resources and, second, on the outcome of subsequent interactions with mutualist pollinators and enemy pre‐dispersal seed predators and nectar robbing bumble bees. We used a fully‐factorial experiment in which plants were watered, fertilized or left as unmanipulated controls, crossed with clipping to simulate herbivore damage to the apical meristem. Resource addition enhanced both male and female components of fitness, but resource enhancement did not provide the means for plants to fully compensate for simulated herbivory. Clipped plants produced significantly more inflorescences, but at the expense of a delay in flowering and fewer total flowers. Clipping significantly reduced losses to dipteran pre‐dispersal seed predators by delaying flowering time, but early flowering plants produced higher numbers of seeds despite incurring higher rates of predation. Clipped plants incurred a higher risk to nectar robbers in one of two years. Overall, clipped plants suffered severe reductions (a nearly 50% reduction in total seed set) in female success, but clipping combined with nutrient addition enhanced male function through increases in per‐flower pollen production. However, because clipped plants produced significantly fewer flowers than unclipped plants, whole‐plant pollen production was significantly reduced by clipping. Pollinator visitation and nectar robbing were variable between clipping treatments and between years and (nectar robbing) among sites. Our results demonstrate that the variability in plant response to herbivory can, at least in part, be driven by plant interactions with mutualists and enemies. Thus, accounting for such interactions and their variability is important to fully understanding plant compensation for herbivore damage and will likely go far to explain variation in plant response that appears to be independent of resources.

Overcompensation for insect herbivory: a review and meta‐analysis of the evidence

“…In order to confirm that insects can select for overcompensation, ecologists need a better understanding of the costs and benefits (i.e., trade-offs) of reproductive and vegetative overcompensation on lifetime plant fitness (Tewari et al 2013, Scholes et al 2017b, West and Louda 2018. Other specific areas that need more research include (1) plant overcompensatory growth effects on pollination services (Lay et al 2011, Brody and Irwin 2012, Thomsen and Sargent 2017, (2) tradeoffs between male and female plant fitness (Gronemeyer et al 1997, Strauss et al 2003, (3) trade-offs between resource allocation to overcompensatory responses and chemical and physical defenses (Poveda et al 2012, Mesa et al 2017, (4) overcompensatory responses to damage by multiple herbivore species (Anderson and Paige 2003, Stephens et al 2013, Gagic et al 2016), (5) the role of fungal associations in plant overcompensatory responses (Borowicz 2013, Allsup andPaige 2016), and (6) the effects of damage timing Whitham 1989, Trumble et al 1993) and damage frequency (Scholes et al 2017a) on overcompensatory responses. In addition, ecologists evaluating overcompensation need to demonstrate that overcompensation is both genetically controlled and heritable in natural populations.…”

Cumulative herbivory outpaces compensation for early floral damage on a monocarpic perennial thistle

“…Apical damage has led to compensation, and occasionally overcompensation, for herbivore damage in other systems. Haphazard variation in the timing and duration of insect herbivory and flowering delays due to apical damage can, however, reduce the likelihood of successful seed production and limit the reliability of fitness gains from compensation (Huhta et al 2000;Brody and Irwin 2012;Adhikari and Russell 2014). This variability increases the potential value of strong early-season apical investment, relative to fitness costs spread across multiple later flowering heads, when fitness must be realized under cumulative season-long insect pressure.…”

“…Although C. canescens plants had the potential to tolerate loss of the large, early apical flower head investment, such tolerance was insufficient on average to override the fitness costs imposed by cumulative floral herbivory. The relative advantage of high early investment, that escapes herbivores, compared to that of releasing additional investment to other flowers, likely varies extensively in time and space (i.e., Brody and Irwin 2012;Klimešová et al 2014;Krimmel and Pearse 2016). For instance, Adhikari and Russell (2014) found a greater proportion of flowering heads developed in response to apical damage in another native thistle (Cirsium altissimum), but the fecundity of axillary flower heads was insufficient to provide compensatory seed production.…”

Predicting Compensatory Growth and Reproduction in Agricultural Weeds Using a Plant’s Growth Rate Trajectory: A Test with Defoliation of Abutilon theophrasti

“…[10], or the compensatory continuum hypothesis [5], but rather provide a reason that variables, such as net assimilation rate and leaf area ratio, are related to compensatory responses, and why compensatory growth is not always positively related to resource level [11].…”