Initial herbivory and exposure to herbivory-induced volatiles enhance arthropod species richness by diversifying community assemblages

Abstract

Plant ecological traits affect the species identity of plant-colonizing arthropods, which in turn induces species-specific trait changes in plants, forming feedback between plants and arthropods. Such feedback can amplify initial differences in species composition, leading to large variations (i.e., high β diversity). We hypothesized that the differences in plant initial conditions have sustained effects on arthropod community composition and species richness. To test this hypothesis, we monitored arthropod community assembly on a willow tree species, Salix eriocarpa, which was experimentally manipulated into three initial treatments: undamaged (in chamber 1); damaged by the specialist leaf beetle, Plagiodera versicolora (chamber 2); and “exposed” plants that were undamaged but were exposed to volatiles from damaged plants (in chamber 2). The arrival and population dynamics of the leaf beetle were affected by the plant’s initial condition (chamber 1 vs. 2), which could result from the microscale environmental heterogeneity between chambers (chamber effect) and/or from the herbivory-related impacts (direct herbivory and exposure to induced volatiles in chamber 2). The community composition on damaged and exposed plants became significantly different on day 32. In addition, the divergence in composition between plant individuals was significantly smaller in undamaged plants (chamber 1) than in damaged and exposed plants (chamber 2) on day 60. The compositional variations (β diversity) between chambers, between treatments, and between days, comprised a large proportion (two third) of the total species richness (γ diversity) in the whole community of arthropods. These results suggest that plant initial condition is a key driver of community assembly and the maintenance of species diversity.

Plant volatiles and priority effects interactively determined initial community assembly of arthropods on multiple willow species

“…In conclusion, our study found that both PVOCs and priority effects played a significant role in the short-term, initial stages of community assembly of arthropods on willow trees. Although our monitoring was limited to the initial stages, we predict that the effects of community divergence observed in our study was not transient but could persist in a longer timescale, at least for several months, based on previous studies (Stam et al, 2018;Yoneya et al, 2023) indicating such lasting effects. Our study indicated that riparian willow forests are an excellent model system for community assembly, along with recent studies focusing on the local co-occurrence of multiple willow species (Yoneya et al, 2012), its temporally dynamic characteristics (Nakamura et al, 2005), plant volatile-mediated food chains (Yoneya & Takabayashi, 2013), and high diversity of arthropods (Nakamura et al, 2006;Yoneya et al, 2023).…”

“…Our results suggest that both the priority effect and environmental filtering play significant roles in the observed community assembly processes. Linkage between the earliest and subsequent colonizer communities suggests the presence of priority effects caused by plant-arthropod feedback (Utsumi et al, 2010;Yoneya et al, 2023).…”

“…This results in arthropod community composition depending on the plant species and genotype identity (Hochwender & Fritz, 2004 ). At the same time, induced responses such as induced resistance and compensatory regrowth are herbivore‐species‐specific and deterministic (Kessler & Halitschke, 2007 ; Van Zandt & Agrawal, 2004a ), which in turn affect the subsequent community assembly (Stam et al, 2018 ; Van Zandt & Agrawal, 2004b ), forming feedback between plant traits and arthropods (i.e., plant–arthropod feedback, Utsumi et al, 2010 ; Yoneya et al, 2023 ). When such feedback is initiated by the earliest colonizers on a plant whose identity can vary stochastically (Bacca et al, 2021 ; Shinohara & Yoshida, 2021 ), it results in a priority effect (Chase, 2003 ; Fukami, 2015 ) because of the combination of stochastic and deterministic processes (Chase, 2010 ), which contribute to the divergence of community composition even within a plant population.…”

“…Nevertheless, very few studies (Zu et al, 2020 ) have investigated the linkage between PVOCs and diverse arthropod communities. At the same time, the divergence of arthropod communities between plant individuals due to priority effects has also received increasing attention (Stam et al, 2018 ; Utsumi, 2015 ; Van Zandt & Agrawal, 2004b ; Yoneya et al, 2023 ). Previous studies have addressed the role of initial stage communities in shaping later stages of community development by experimentally manipulating either the initial herbivore colonizers (Stam et al, 2018 ; Utsumi, 2015 ; Van Zandt & Agrawal, 2004b ) or the plant initial conditions, including exposure to herbivore‐induced PVOCs (Yoneya et al, 2023 ), while maintaining other environmental conditions homogeneous.…”

“…At the same time, the divergence of arthropod communities between plant individuals due to priority effects has also received increasing attention (Stam et al, 2018 ; Utsumi, 2015 ; Van Zandt & Agrawal, 2004b ; Yoneya et al, 2023 ). Previous studies have addressed the role of initial stage communities in shaping later stages of community development by experimentally manipulating either the initial herbivore colonizers (Stam et al, 2018 ; Utsumi, 2015 ; Van Zandt & Agrawal, 2004b ) or the plant initial conditions, including exposure to herbivore‐induced PVOCs (Yoneya et al, 2023 ), while maintaining other environmental conditions homogeneous. The manipulation of initial colonizers in a homogeneous environment has been widely applied to microbial (Dickie et al, 2012 ; Toju et al, 2018 ) and plant (Fukami et al, 2005 ) communities.…”