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

Abstract

1. Plants show ontogenetic variation in growth-defence strategies to maximize reproductive output within a community context. Most work on plant ontogenetic variation in growth-defence trade-offs has focussed on interactions with antagonistic insect herbivores. Plants respond to herbivore attack with phenotypic changes. Despite the knowledge that plant responses to herbivory affect plant mutualistic interactions with pollinators required for reproduction, indirect interactions between herbivores and pollinators have not been included in the evaluation of how ontogenetic growth-defence trajectories affect plant fitness. 2. In a common garden experiment with the annual Brassica nigra, we investigated whether exposure to various herbivore species on different plant ontogenetic stages (vegetative, bud or flowering stage) affects plant flowering traits, interactions with flower visitors and results in fitness consequences for the plant. 3. Effects of herbivory on flowering plant traits and interactions with flower visitors depended on plant ontogeny. Plant exposure in the vegetative stage to the caterpillar Pieris brassicae and aphid Brevicoryne brassicae led to reduced flowering time and flower production, and resulted in reduced pollinator attraction, pollen beetle colonization, total seed production and seed weight. When plants had buds, infestation by most herbivore species tested reduced flower production and pollen beetle colonization. Pollinator attraction was either increased or reduced. Plants infested in the flowering stage with P. brassicae or Lipaphis erysimi flowered longer, while infestation by any of the herbivore species tested increased the number of flower visits by pollinators. 4. Our results show that the outcome of herbivore-flower visitor interactions in B. nigra is specific for the combination of herbivore species and plant ontogenetic stage. Consequences of herbivory for flowering traits and reproductive output were strongest when plants were attacked early in life. Such differences in selection pressures imposed by herbivores to specific plant ontogenetic stages may drive the evolution of distinct ontogenetic trajectories in growth-defence-reproduction strategies and include indirect interactions between herbivores and flower visitors.This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Additional supporting information may be found online in theSupporting Information section. How to cite this article: Rusman Q, Lucas-Barbosa D, Hassan K, Poelman EH. Plant ontogeny determines strength and associated plant fitness consequences of plant-mediated interactions between herbivores and flower visitors. J Ecol.

Multiple Attack to Inflorescences of an Annual Plant Does Not Interfere with the Attraction of Parasitoids and Pollinators

“…The ontogenetic stage in which plants are infested can influence the effects of attack on plant seed set (Rusman et al, 2020 ). In our field experiments, plants were exposed to attackers at the onset of flowering, and although the initial attack may have been minor for the plant, the attackers that settle on the flowering plant may multiply or develop to more voracious developmental stages while altering patterns of plant phenotypic responses.…”

Seasonal abundance of Tuberolachnus salignus and its effect on flowering of host willows of varying susceptibility

“…Insect herbivory can change the plant resource allocation process, which leads to changes in floral traits, flowering time and flower production (Hoffmeister et al., 2016; Rusman et al., 2020). The extent to which herbivory affects flowering phenology appears to relate to the ability of the host plant to compensate for the damage (Freeman et al., 2003; Oesterheld & McNaughton, 1991).…”

Plant defence strategies to multi-herbivore attack

“…There is even modelling exercises made to assess the plant growth defence trade-off under conditions of herbivory and competition for light (de Vries et al, 2017(de Vries et al, , 2018(de Vries et al, , 2019. Second, the pollinator community of B. nigra plants, as well as the effects of single attack by different herbivores and the effects of dual attack on the pollinator community have also been explored (Chrétien et al, 2021;Rusman et al, 2018Rusman et al, , 2020. Third, there is information on how community complexity shapes selection on traits in B. nigra (Lankau & Strauss, 2008).…”

“…Important selective agents on plant traits are herbivores, natural enemies of the herbivores and pollinators. Herbivores can directly affect plant fi tness by consuming photosynthetic plant tissues, fl owers and/or seeds and indirectly by altering the attraction of other herbivores, natural enemies of the herbivores and by altering pollinator visitation (Grass et al, 2018;Rusman et al 2020). Natural enemies of the herbivores, such as parasitoids and predators, can have positive direct effects on plant fi tness by reducing herbivore pressure (Bustos-Segura et al, 2020) and indirect effects by altering herbivore, omnivore and pollinator behaviour.…”

“…phloem feeders, leaf chewers or a mix of both). Recent studies identifi ed that B. nigra plants respond differentially to attack by different herbivore feeding guilds as well as the number of species attacking the plant (Fernández de Bobadilla et al, 2021), and that indirect interactions due to herbivore-induced plant responses affect plant reproductive success (Pashalidou et al, 2015;Rusman et al, 2018Rusman et al, , 2020. We specifi cally studied how the composition of the introduced herbivore community affected a) plant colonisation by the herbivore Plutella xylostella, one of the most prevalent herbivores attacking B. nigra plants ; b) top-down control of this herbivore population by parasitoids; c) visitation of fl owers by pollinators; and d) how these interactions collectively affect plant fi tness in terms of seed production.…”