Phylogenetic relatedness of food plants reveals highest insect herbivore specialization at intermediate temperatures along a broad climatic gradient

Abstract

The composition and richness of herbivore and plant assemblages change along climatic gradients, but knowledge about associated shifts in specialization is scarce and lacks controlling for the abundance and phylogeny of interaction partners. Thus, we aimed to test whether the specialization of phytophagous insects in insect-plant interaction networks decreases toward cold habitats as predicted by the 'altitude niche-breadth hypothesis' to forecast possible consequences of interaction rewiring under climate change. We used a non-invasive, standardized metabarcoding approach to reconstruct dietary relationships of Orthoptera species as a major insect herbivore taxon along a broad temperature gradient (~12°C) in Southern Germany. Based on Orthoptera surveys, feeding observations, collection of fecal pellets from >3,000 individuals of 54 species, and parallel vegetation surveys on 41 grassland sites, we quantified plant resource availability and its use by herbivores. Herbivore assemblages were richer in species and individuals at sites with high summer temperatures, while plant richness peaked at intermediate temperatures.Corresponding interaction networks were most specialized in warm habitats. Considering phylogenetic relationships of plant resources, however, the specialization pattern was not linear but peaked at intermediate temperatures, mediated by herbivores feeding on a narrow range of phylogenetically related resources. Our study provides empirical evidence of resource specialization of insect herbivores along a climatic gradient, demonstrating that resource phylogeny, availability, and temperature interactively shape the specialization of herbivore assemblages. Instead of low specialization levels only in cold, harsh habitats, our results suggest increased generalist feeding due to intraspecific changes and compositional differences at both ends of the microclimatic gradient. We conclude that this nonlinear change of phylogeny-based resource specialization questions predictions derived from the 'altitude-niche breadth hypothesis' and highlights the currently limited understanding of how plant-herbivore interactions will change under future climatic conditions.

Micro‐ and macroclimate interactively shape diversity, niches and traits of Orthoptera communities along elevational gradients

“…We collected traits of the occurring Orthoptera species both empirically and from literature (Table S2). Ecological traits were the species' moisture preferences ranging between hygrophilic and xerophilic species based on classifications by Harz (1969), Harz (1975), Oschmann (1991), Ingrisch and Köhler (1998), Klaiber et al (2017), Thorn et al (2022) and Dvořák et al (2022), a diet breadth index, which specifies the range of used resource items with respect to evolutionary relationships (range between oligophagous species, mainly feeding on a narrow range of phylogenetically related resources, to polyphagous species which regularly use a broad range of resources) based on fieldrecorded feeding interactions, barcoding of faecal samples, feeding experiments and published literature (Descombes, Marchon, et al, 2017;Descombes et al, 2020;Fauna Info CSCF, 2022;Ibanez et al, 2013;Ingrisch & Köhler, 1998;König et al, 2022;Pitteloud et al, 2021), and the monthly triad marking the beginning of larval hatching as a phenological trait (own observations, Ingrisch & Köhler, 1998;Schlumprecht & Waeber, 2003;Zuna-Kratky & Landmann, 2017; Table S2).…”

“…Bray-Curtis dissimilarity, balanced variation or abundance gradients rates with temperature and microclimate (Descombes, Marchon, et al, 2017;König et al, 2022). Additionally, we tested the effect of elevational difference and microclimatic differences on compositional dissimilarities with permutational mantel tests based on Pearson product-moment correlation.…”

“…Additionally, the reduction of wing length independent of body size is a common adaptation in cold environments (Laiolo et al., 2023; Leihy & Chown, 2020; Tiede et al., 2018), as it may be advantageous to allocate resources to reproduction rather than wing development (energy trade‐off, Hodkinson, 2005; Laiolo et al., 2023; Tiede et al., 2018). Cold habitats may also require utilizing a broad range of food items, thus favouring less specialized species (König et al., 2022; Pitteloud et al., 2021; Rasmann et al., 2014). Despite the urge to understand the position of species' climatic niches to estimate potential threats for the systems in the context of climate change, it is largely neglected how microclimate interacts with macroclimate to form the climatic niches of species and how trait combinations promote or constrain the use of microclimatic refugia under a warmer macroclimate according to predictions.…”

Launching insectphylo.org; a new hub facilitating construction and use of synthesis molecular phylogenies of insects

“…The Tree of Life provides a unifying backbone across biological fields. Phylogenetic frameworks comprise diverse and nuanced information, which are regularly applicable to near‐term global challenges: Insect community composition under tree extinction undergoes phylogenetic structural changes more nuanced than revealed by species richness alone (Wang et al, 2019); Phylogenetic distance between pairs of insect species contributes to likelihood of their co‐occurrence (Wang et al, 2022); Traits defining ecological responses often show phylogenetic conservation and thus enhanced predictive capabilities are enabled where using phylogenetic instead of taxonomic groups (Carew et al, 2011); Evolutionary distinctive but species‐poor biodiversity components are likely to be missed where phylogeny is not taken into account in conservation (Nogueira et al, 2019), and phylogenetic structuring of resources impacts decisions such as specialization in interacting species (König et al, 2022). The public availability of species‐comprehensive phylogenies clearly facilitates such studies (Hernández‐Agüero et al, 2022; Tomczyk et al, 2022; Vancaester & Blaxter, 2022), though there can be difficulties in obtaining phylogenies for studies of regional insect species pools (Stork, 2018).…”

“…phylogenetic instead of taxonomic groups (Carew et al, 2011); Evolutionary distinctive but species-poor biodiversity components are likely to be missed where phylogeny is not taken into account in conservation (Nogueira et al, 2019), and phylogenetic structuring of resources impacts decisions such as specialization in interacting species (König et al, 2022). The public availability of species-comprehensive phylogenies clearly facilitates such studies (Hernández-Agüero et al, 2022;Tomczyk et al, 2022;Vancaester & Blaxter, 2022), though there can be difficulties in obtaining phylogenies for studies of regional insect species pools (Stork, 2018).…”