Cross‐seasonal legacy effects of arthropod community on plant fitness in perennial plants

Abstract

In perennial plants, interactions with other community members during the vegetative growth phase may influence community assembly during subsequent reproductive years and may influence plant fitness. It is well‐known that plant responses to herbivory affect community assembly within a growing season, but whether plant–herbivore interactions result in legacy effects on community assembly across seasons has received little attention. Moreover, whether plant–herbivore interactions during the vegetative growing season are important in predicting plant fitness directly or indirectly through legacy effects is poorly understood. Here, we tested whether plant–arthropod interactions in the vegetative growing season of perennial wild cabbage plants, Brassica oleracea, result in legacy effects in arthropod community assembly in the subsequent reproductive season and whether legacy effects have plant fitness consequences. We monitored the arthropod community on plants that had been induced with either aphids, caterpillars or no herbivores in a full‐factorial design across 2 years. We quantified the plant traits ‘height’, ‘number of leaves’ and ‘number of flowers’ to understand mechanisms that may mediate legacy effects. We measured seed production in the second year to evaluate plant fitness consequences of legacy effects. Although we did not find community responses to the herbivory treatments, our data show that community composition in the first year leaves a legacy on community composition in a second year: predator community composition co‐varied across years. Structural equation modelling analyses indicated that herbivore communities in the vegetative year correlated with plant performance traits that may have caused a legacy effect on especially predator community assembly in the subsequent reproductive year. Interestingly, the legacy of the herbivore community in the vegetative year predicted plant fitness better than the herbivore community that directly interacted with plants in the reproductive year. Synthesis. Thus, legacy effects of plant–herbivore interactions affect community assembly on perennial plants across growth seasons and these processes may affect plant reproductive success. We argue that plant–herbivore interactions in the vegetative phase as well as in the cross‐seasonal legacy effects caused by plant responses to arthropod herbivory may be important in perennial plant trait evolution such as ontogenetic variation in growth and defence strategies.

Plant ontogeny determines strength and associated plant fitness consequences of plant‐mediated interactions between herbivores and flower visitors

“…Herbivory affects organisms that engage in interactions with the plant under attack soon after the event. Moreover, new interactions established over the rest of the life of the plant are affected until the plant dies (Stam et al, ; Stam, Kos, Dicke, & Poelman, ; Van Zandt & Agrawal, ). The ontogeny of the herbivores themselves likely influences the outcomes of the effects of plant ontogeny on flower‐visitor interactions and plant fitness (Barber, Adler, Theis, Hazzard, & Kiers, ; Pineda, Soler, Pastor, Li, & Dicke, ).…”

“…This can have consequences for plant‐mediated interactions (Chrétien et al, ; Soler et al, ; Stam, Chrétien, Dicke, & Poelman, ; Stam et al, ) and plant seed production (Stam et al, ). Ontogenetic variation in networks of indirect plant‐mediated interactions includes these complex interactive effects on plant fitness (Poelman & Kessler, ; Rusman et al, ; Soper Gorden & Adler, ; Stam et al, ). Taken together, variation in direct and indirect consequences of herbivory during plant ontogeny likely imposes selection pressures that drive the evolution of plant defence ontogenetic trajectories (Barton & Boege, ; Ochoa‐López et al, ).…”

“…Simultaneous herbivory can induce different plant responses as compared to induction by a single herbivore (Pierre, Jansen, et al, ; Ponzio, Papazian, Albrectsen, Dicke, & Gols, ). This can have consequences for plant‐mediated interactions (Chrétien et al, ; Soler et al, ; Stam, Chrétien, Dicke, & Poelman, ; Stam et al, ) and plant seed production (Stam et al, ). Ontogenetic variation in networks of indirect plant‐mediated interactions includes these complex interactive effects on plant fitness (Poelman & Kessler, ; Rusman et al, ; Soper Gorden & Adler, ; Stam et al, ).…”

Predictability of Biotic Stress Structures Plant Defence Evolution

“…Plant responses to an initial attacker can thus affect the likelihood of colonisation by subsequent herbivores [13,26]. These correlations among antagonists can be immediate such as found for the correlated attack for pathogens spread by insect vectors [27], or spanning over longer periods of time and even across seasons for perennial plants, such as found for the correlations between transient attack by herbivores and their legacy effects on future biotic stress [28]. Thus, by perceiving the current herbivore interaction as a cue for the type of future attack, plants may incorporate likely future stress in their response to the current attacker.…”

Plasticity in Induced Resistance to Sequential Attack by Multiple Herbivores in Brassica Nigra

“…Only a few studies have explored plant defences to sequential herbivory beyond dual attack. These studies show that the order, the identity and the species richness of the attackers in uences plant defence against a late arriving herbivore (Fernández de Bobadilla et al, 2021; Mathur et al, 2013;Stam et al, 2014Stam et al, , 2017Stam et al, , 2018Stam et al, , 2019. Nonetheless, in nature, herbivores often arrive sequentially, and studies including a realistic number of sequential attackers are lacking.…”