Legacy effects of herbivory enhance performance and resistance of progeny plants

Abstract

Herbivory‐induced changes in plant resistance and tolerance traits can mediate the interaction between spatially and temporally separated above‐ and below‐ground herbivores. However, it is unknown how long the impact of transient herbivory events last or if legacy effects can be detected systemically in the plant and across plant generations. Here, we studied the impact of transient above‐ground herbivory by the specialist caterpillar Manduca sexta on the plant traits of wild tobacco Nicotiana attenuata and the consequences for below‐ground root‐knot nematodes Meloidogyne incognita in short‐term, long‐term, and transgenerational experiments. In the short‐ and long‐term experiments, above‐ and below‐ground herbivory had significant, albeit independent, impacts on key plant traits such as plant biomass, nutrient content, and secondary metabolites. In addition, herbivory influenced fitness parameters such as seed yield and quality. In the long‐term and transgenerational experiments, transient above‐ground herbivory had facilitating effects on nematodes, irrespective of any treatments of the parental plants. We found evidence for transgenerational legacy effects of both above‐ and below‐ground herbivory on the resistance of progeny plants against above‐ground herbivores. Additionally, below‐ground herbivory in the parental generation increased the root biomass of progeny plants. Synthesis. Our results suggest that herbivory may have a long‐term impact on plant fitness by improving the performance of progeny plants challenged by above‐ and below‐ground herbivory.

Trait‐mediated indirect interactions: Moose browsing increases sawfly fecundity through plant‐induced responses

“…Studies have shown that the effect on the second herbivore is often larger when herbivores are separated in time, since the plant has had more time to respond (Denno et al, ; Erb, Robert, Hibbard, & Turlings, ). In addition, many responses diminish over time, and persistence of the response differs, both between responses and systems (Björkman, Dalin, & Ahrné, ; Kafle & Wurst, ). The effect of initial damage on the receiving herbivore might increase at first but over time decrease, creating a hump‐shaped relationship between time since initial damage and effect on the second herbivore.…”

Overgrazing-induced legacy effects may permit Leymus chinensis to cope with herbivory

“…Therefore, clarifying the overgrazing-induced legacy effects in plant defense strategies is critical for understanding processes occurring in grazing ecosystems. However, most previous studies on herbivory-induced legacy effects on plant defense strategies have focused on short-term insect herbivory, in contrast, studies examining long-term livestock grazing have received less attention by comparison (Holeski, Jander & Agrawal, 2012;Kafle & Wurst, 2019).…”

“…Environmental disturbances (e.g., drought, herbivory) can have persistent effects on ecological attributes (e.g., ecological processes, community structure, population dynamics, and plant and soil characteristics) long after they occur (i.e., the legacy effect) ( Fox et al, 2015 ; Kafle & Wurst, 2019 ). Legacy effects are ubiquitous phenomena in nature and have been extensively studied in the context of plant succession, herbivory, invasive plants, ecosystem engineering, and human land use ( Cuddington, 2011 ; Kostenko et al, 2012 ; Wurst & Ohgushi, 2015 ).…”

Legacy effects of historical grazing alter leaf stomatal characteristics in progeny plants

“…However, little is known about transgenerational effects induced by overgrazing in forage grass. According to a recent study by Kafle, Wurst & Dam (2019), single herbivory in the parental generation did not prime the transgenerational response, only sequential above-and below-ground herbivory did. Therefore, it can be speculated that transgenerational responses require a certain threshold of environmental stress.…”