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

Abstract

Induced responses in plants, initiated by herbivory, create potential for trait‐mediated indirect interactions among herbivores. Responses to an initial herbivore may change a number of plant traits that subsequently alter ecological processes with additional herbivores. Although common, indirect interactions between taxonomically distant herbivores, such as mammals and insects, are less studied than between taxonomically related species (i.e., insect–insect). In terms of mammal–insect interactions, effects on insect numbers (e.g., density) are relatively well studied, whereas effects on performance (e.g., fecundity) are rarely explored. Moreover, few studies have explored mammal–insect interactions on coniferous plants. The aim of this study was to investigate the effect of mammalian induced responses on insect performance. We specifically investigated the effect of moose (Alces alces) browsing on Scots pine (Pinus sylvestris) and subsequent effects on sawfly (Neodiprion sertifer) performance. Sawfly larvae were reared on browsed, clipped, and unbrowsed control pine trees in a controlled field experiment. Afterward, cocoon weight was measured. Needle C:N ratio and di‐terpene content were measured in response to browsing. Sawfly performance was enhanced on trees browsed by moose. Cocoon weight (proxy for fecundity) was 9 and 13% higher on browsed and clipped trees compared to unbrowsed trees. Cocoon weight was weakly related to needle C:N ratio, and browsed trees had lower a C:N ratio compared to unbrowsed trees. Needle di‐terpene content, known to affect sawfly performance, was neither affected by the browsing treatments nor did it correlate with sawfly weight. We conclude that mammalian herbivory can affect insect herbivore performance, with potential consequences for ecological communities and with particular importance for insect population dynamics. The measured plant variables could not fully explain the effect on sawfly performance providing a starting point for the consideration of additional plant responses induced by mammalian browsing affecting insect performance.

Effect of forest stand type on host plant quality and direct and indirect effects on pine sawfly performance

“…The female cocoons were weighed with a microbalance (Mettler Toledo MX5) approximately two to three weeks after collection and prior to adult emergence. We weighed only female cocoons as a proxy for fecundity, because a strong correlation between egg load and cocoon weight has been established (Nordkvist et al ., 2019). To calculate predation mortality, we used the larvae from the predation treatment by summing up the number of predated and parasitized larvae and divided that number by the initial number of larvae in the group.…”

“…For each experimental pine, we collected 20 needles of the previous year from the branch that hosted the sheltered groups after the sawfly larvae had spun cocoons. The collected needles reflect the food quality that the larvae experienced as the response of pine to sawfly defoliation has not been found to induce an immediate or delayed induced response (Niemelä et al ., 1991; Lyytikäinen, 1994; McMillin & Wagner, 1997; Lyytikäinen‐Saarenmaa, 1999; Nordkvist et al ., 2019). The collected needles were immediately folded in aluminium foil and placed in a plastic box containing dry ice to avoid any resin acid degradation.…”

Plant Mediated Interactions: Lower Sawfly Survival on Pines Previously Browsed by Moose

“…Sawflies are subjected to predation in their larval stage by various generalists, mainly ants (Olofsson, 1992;Lindstedt et al, 2006;Kaitaniemi et al, 2007) and spiders (Juutinen, 1967;Kaitaniemi et al, 2007). Sawfly performance is commonly related to pine needle nitrogen (Björkman et al, 1991(Björkman et al, , 1997 and diterpene content (Larsson et al, 1986;Björkman et al, 1997), but moose browsing has previously been shown not to influence sawfly bottomup survival (Nordkvist et al, 2019). Predation of sawfly larvae is commonly related to pine needle diterpene content, due to sequestering and related anti-predator behavior by sawfly larvae (Lindstedt et al, 2006;Kollberg et al, 2015), but moose browsing has previously been shown not to affect diterpene content of pine needles (Nordkvist et al, 2019).…”

Host Availability, Repulsive Companion Planting, and Predation Interact and Shape How a Parthenogenetic Aphid Population Responds to a Stratified Ecological Challenge

“…d) interference of the companion's non-volatiles (e.g., saponins) with the ingestion of the imbibed phloem (Koul 2008;Ben-Issa et al 2017). e) aerial and below-ground communication between the plant neighbours (host [hospitable] and companion [hostile]) which alters the aphid-embedding context making it more uncertain and/or disturbing (Law and Regnier 1971;Ninkovic et al 2013;Ben-Issa et al 2017;Elhakeem et al 2018;Kalske et al 2019); this can be envisioned to occur in a trait-mediated fashion appertaining to the interaction between the metabolites and the microbiomes of both plants, as the companion plant might lead to quality changes in the shared microhabitat and in the accompanied crop (Wu et al 2016;Ben-Issa et al 2017;Khudr et al 2018;Nordkvist et al 2019).…”