Tolerance of a perennial herb, Pimpinella saxifraga, to simulated flower herbivory and grazing: immediate repair of injury or postponed reproduction?

Abstract

Perennial, polycarpic herbs can respond to herbivory either by (1) regrowth in the same season in order to compensate for lost reproductive structures or by (2) postponing reproduction until the following growing season. We tested these response patterns with the perennial umbellifer Pimpinella saxifraga by simulating flower herbivory and shoot grazing both in the field and in a common garden experiment. In the field, both simulated flower herbivory and grazing effectively suppressed current reproduction, whereas no statistically significant effects of previous-year treatments on growth or reproduction were found in the following year. In the common garden, in the first year the species fully compensated for simulated flower herbivory in vegetative parameters but seed set was reduced by 26%. After 2 years of flower removal, the plants overcompensated in shoot and root biomass by 47 and 46%, respectively, and compensated fully in reproductive performance. Simulated grazing resulted in 21% lower shoot biomass in the first season, but the root biomass was not affected. In the second season the root biomass increased by 43% as compared to the control plants. However, regrowth following simulated grazing resulted in a significant delay in flowering with the consequence that the seed yield of fertile plants was reduced by 55% as compared to the control plants. These results suggest that in resource-rich garden conditions P. saxifraga may immediately repair injuries caused by flower herbivory, but repairs more extensive shoot injury less successfully. Delayed phenology decreases the benefits of immediate repair. In resource-poor conditions, the benefits of regrowth can be negligible. Accordingly, in our field population, the plants postponed their reproduction until the following year in response to simulated grazing and frequently in response to flower removal. When the plants gain very little from regrowth, the costs of reproduction would select for postponed reproduction in response to injury.

Environmental context determines within- and potential between-generation consequences of herbivory

“…A previous study similarly showed that snipping apical meristems in potted C. americanum resulted in delayed Xowering (L. Guarinello, unpublished data). Later Xowering of damaged plants is not surprising as most Xowers were produced on side branches that grew after the loss of the apical meristem, and indeed is found in a number of species (e.g., Lennartsson et al 1998;TiYn 2000;Freeman et al 2003;Huhta et al 2009). However, because understory plants Xower on average 11 days after light-gap plants (see also Galloway and Etterson 2009), this delay resulted in deer-browsed plants in light gaps initiating Xowering slightly after uneaten plants in the understory.…”

“…Consequently, by inXuencing Xowering time, the maternal light environment promotes the production of annual oVspring in light-gap habitats and biennials in the shaded understory (Galloway 2002(Galloway , 2005. Browsing has been shown to alter phenology in other plant species (Lennartsson et al 1998;TiYn 2000;Freeman et al 2003;Huhta et al 2009). If deer herbivory likewise aVects the temporal components of Xowering in C. americanum, browsed plants may be biased towards the production of either annual or biennial oVspring.…”

Ontogenetic changes in tolerance to herbivory in Arabidopsis

“…At pre-reproductive stages, the production of more vegetative tissue should have high priority (Harper 1977), but protecting the existing tissue through resistance is also important. Therefore, plants should invest in resistance only if the shunting of resources to resistance does not slow down vegetative growth to the extent that fitness decreases more than it would from the loss of vegetative tissue to herbivores (Huhta et al 2003(Huhta et al , 2009Avila-Sakar and Laarakker, in preparation). In order to quantify this fitness cost of herbivory, the rate of loss of fitness as a function of the amount of tissue removed by herbivores, i.e., tolerance, must be determined.…”

Additive and non-additive effects of simulated leaf and inflorescence damage on survival, growth and reproduction of the perennial herb Arabidopsis lyrata

“…Loss of leaf tissue can lead to the mobilisation of stored resources from root to shoot (Danckwerts 1993), but can also modify photosynthetic rates in remaining leaf tissue (Retuerto et al 2006) and leaf longevity (Mabry and Wayne 1997). Loss of inXorescences can, among other things, lead to maturation of fruits in a greater proportion of open Xowers (Wise et al 2008), but can also increase resource storage in root (Huhta et al 2009), which is opposite to the expected response to leaf damage. Further work is required to identify the mechanisms giving rise to the non-additive eVects documented in the present study.…”

“…If a plant suppresses any further reproduction following inXorescence damage and remains vegetative, resources that would have been otherwise invested in reproduction may be stored below-ground and invested in reproduction in the following year (Venecz and Aarssen 1998). On the other hand, when the damaged plants immediately re-Xower, this investment may reduce their future reproductive potential (Huhta et al 2009). From considerations of resource allocation and lifehistories, simultaneous damage to vegetative and reproductive structures clearly has the potential to aVect Wtness nonadditively, yet interactions between Xoral and leaf herbivory have remained relatively unexplored (McCall 2007).…”