skip to main content


Title: Plant phylogeny drives arboreal caterpillar assemblages across the Holarctic
Abstract

Assemblages of insect herbivores are structured by plant traits such as nutrient content, secondary metabolites, physical traits, and phenology. Many of these traits are phylogenetically conserved, implying a decrease in trait similarity with increasing phylogenetic distance of the host plant taxa. Thus, a metric of phylogenetic distances and relationships can be considered a proxy for phylogenetically conserved plant traits and used to predict variation in herbivorous insect assemblages among co‐occurring plant species.

Using a Holarctic dataset of exposed‐feeding and shelter‐building caterpillars, we aimed at showing how phylogenetic relationships among host plants explain compositional changes and characteristics of herbivore assemblages.

Our plant–caterpillar network data derived from plot‐based samplings at three different continents included >28,000 individual caterpillar–plant interactions. We tested whether increasing phylogenetic distance of the host plants leads to a decrease in caterpillar assemblage overlap. We further investigated to what degree phylogenetic isolation of a host tree species within the local community explains abundance, density, richness, and mean specialization of its associated caterpillar assemblage.

The overlap of caterpillar assemblages decreased with increasing phylogenetic distance among the host tree species. Phylogenetic isolation of a host plant within the local plant community was correlated with lower richness and mean specialization of the associated caterpillar assemblages. Phylogenetic isolation had no effect on caterpillar abundance or density. The effects of plant phylogeny were consistent across exposed‐feeding and shelter‐building caterpillars.

Our study reveals that distance metrics obtained from host plant phylogeny are useful predictors to explain compositional turnover among hosts and host‐specific variations in richness and mean specialization of associated insect herbivore assemblages in temperate broadleaf forests. As phylogenetic information of plant communities is becoming increasingly available, further large‐scale studies are needed to investigate to what degree plant phylogeny structures herbivore assemblages in other biomes and ecosystems.

 
more » « less
NSF-PAR ID:
10451036
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Ecology and Evolution
Volume:
10
Issue:
24
ISSN:
2045-7758
Page Range / eLocation ID:
p. 14137-14151
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Species interactions are expected to change in myriad ways as the frequency and magnitude of extreme temperature events increase with anthropogenic climate change.

    The relationships between endosymbionts, parasites and their hosts are particularly sensitive to thermal stress, which can have cascading effects on other trophic levels.

    We investigate the interactive effects of heat stress and parasitism on a terrestrial tritrophic system consisting of two host plants (one common, high‐quality plant and one novel, low‐quality plant), a caterpillar herbivore and a specialist parasitoid wasp.

    We used a fully factorial experiment to determine the bottom‐up effects of the novel host plant on both the caterpillars' life history traits and the wasps' survival, and the top‐down effects of parasitism and heat shock on caterpillar developmental outcomes and herbivory levels.

    Host plant identity interacted with thermal stress to affect wasp success, with wasps performing better on the low‐quality host plant under constant temperatures but worse under heat‐shock conditions.

    Surprisingly, caterpillars consumed less leaf material from the low‐quality host plant to reach the same final mass across developmental outcomes.

    In parasitized caterpillars, heat shock reduced parasitoid survival and increased both caterpillar final mass and development time on both host plants.

    These findings highlight the importance of studying community‐level responses to climate change from a holistic and integrative perspective and provide insight into potential substantial interactions between thermal stress and diet quality in plant–insect systems.

    Read the freePlain Language Summaryfor this article on the Journal blog.

     
    more » « less
  2. Abstract

    Plants face many environmental stresses that can impact their survival, development and fitness. Insects are the most diverse, abundant and threatening herbivores in nature. As a consequence, plants produce direct chemical and physical defences to reduce herbivory. They also release volatiles to recruit natural enemies that indirectly protect them from herbivory. The recruitment of parasitic wasps can benefit plant fitness because they ultimately kill their insect hosts.

    Recently, studies showed that parasitoids can indirectly mediate plant defences by modulating herbivore oral secretions. In addition to the direct benefits of parasitoids in terms of reducing herbivore survival, we tested if the reduction in induced defences by parasitized caterpillars compared to non‐parasitized caterpillars may reduce the costs associated with defence expression.

    We provide evidence that tomato plants treated with saliva from parasitized caterpillars have significantly higher fitness parameters including increased flower numbers (16.3%) and heavier fruit weight (13.5%), compared to plants treated with saliva from non‐parasitized caterpillars. Since plants were grown without actual herbivores, the higher values for these fitness parameters were due to lower costs of induced defences and not due to reduced herbivory by parasitized caterpillars. Furthermore, the resulting seed germination time was shorter and the germination rate was higher when the maternal plants were previously exposed to parasitized herbivore treatment compared to control (non‐treated) plants.

    Overall, application of saliva did not result in transgenerational priming of offspring defence responses. However, offspring of parents exposed to caterpillar saliva had lower constitutive levels and higher induced levels of trypsin inhibitor than offspring from unexposed parents.

    This study shows that the saliva of parasitized caterpillars can modulate plant defences and further demonstrates that the lower induction of plant defences is associated with elevated plant fitness in the absence of herbivore feeding, suggesting that induced plant defences are costly.

    A freePlain Language Summarycan be found within the Supporting Information of this article.

     
    more » « less
  3. Abstract

    Crop diversification offers a promising solution to meet expanding global food demands while maintaining ecosystem services. Diversification strategies that use mixed planting to reduce pest damage (e.g. intercropping), termed ‘associational effects’ (AE) in the ecological literature, can decrease (associational resistance) or increase (associational susceptibility) herbivore abundance on a focal plant. While application of AE to agroecosystems typically reduces pest abundance, the range of outcomes varies widely.

    We conducted a meta‐analysis using 272 estimates of insect herbivore abundance on crops neighbored by a conspecific or heterospecific from 44 studies undertaken on six continents. We focus on four agricultural crops well represented from sites across the globe to test hypotheses related to understanding how herbivore traits (diet breadth, feeding guild, origin), plant traits (crop type, phylogenetic distance to neighbour) and environmental context (climate, experimental design) contribute to variation in the outcomes of AE.

    Overall, bicultures provided a strong reduction of insect abundance on the focal crop. Climate and interactions between herbivore traits, particularly diet breadth and origin, and plant traits or environmental context mediated the strength of AE.

    Bicultures provided the strongest reductions in insect abundance at low latitudes, and this effect decreased at higher latitudes but only for insects with certain traits. Abundance of generalist herbivores and globally distributed pests tended to be most strongly negatively affected by bicultures, under certain contexts, whereas specialist herbivores and native pests were less affected by neighbours.

    Synthesis and application. This meta‐analysis highlights that crop diversification schemes have an overall strongly beneficial effect of reducing pest abundance. However, there was also variability in the outcomes that is determined in part by the interactive effects of herbivore traits and environmental context. The results provide guidance for incorporating beneficial ecological interactions into integrated pest management strategies.

     
    more » « less
  4. Abstract

    Understanding factors that facilitate interspecific pathogen transmission is a central issue for conservation, agriculture, and human health. Past work showed that host phylogenetic relatedness and geographical proximity can increase cross‐species transmission, but further work is needed to examine the importance of host traits, and species interactions such as predation, in determining the degree to which parasites are shared between hosts.

    Here we consider the factors that predict patterns of parasite sharing across a diverse assemblage of 116 wild ungulates (i.e., hoofed mammals in the Artiodactyla and Perissodactyla) and nearly 900 species of micro‐ and macroparasites, controlling for differences in total parasite richness and host sampling effort. We also consider the effects of trophic links on parasite sharing between ungulates and carnivores.

    We tested for the relative influence of range overlap, phylogenetic distance, body mass, and ecological dissimilarity (i.e., the distance separating species in a Euclidean distance matrix based on standardized traits) on parasite sharing. We also tested for the effects of variation in study effort as a potential source of bias in our data, and tested whether carnivores reported to feed on ungulates have more ungulate parasites than those that use other resources.

    As in other groups, geographical range overlap and phylogenetic similarity predicted greater parasite community similarity in ungulates. Ecological dissimilarity showed a weak negative relationship with parasite sharing. Counter to our expectations, differences, not similarity, in host body mass predicted greater parasite sharing between pairs of ungulate hosts. Pairs of well‐studied host species showed higher overlap than poorly studied species, although including sampling effort did not reduce the importance of biological traits in our models. Finally, carnivores that feed on ungulates harboured a greater richness of ungulate helminths.

    Overall, we show that the factors that predict parasite sharing in wild ungulates are similar to those known for other mammal groups, and demonstrate the importance of controlling for heterogeneity in host sampling effort in future analyses of parasite sharing. We also show that ecological interactions, in this case trophic links via predation, can allow sharing of some parasite species among distantly related host species.

     
    more » « less
  5. Abstract

    Ecological research has increasingly highlighted the importance of intraspecific variation in shaping the structure and function of communities and ecosystems. Indeed, the effects of intraspecific variation can match or exceed those of interspecific variation. Previous reviews of intraspecific variation in plant traits across heterogeneous environments have focused primarily onmeanphenotypic effects. We propose that a richer and fuller understanding of the ecological causes and consequences of intraspecific variation would be provided by partitioning traitvarianceinto its subcomponents (genetic, environment, genotype by environment interaction).

    We used a meta‐analysis of 352 sets of genetic, environment and genotype by environment (G×E) variation estimates from 72 studies of Salicaceae to compare these sources of variation across plant traits (growth, foliar nitrogen, defence compounds), insect herbivore performance metrics (e.g., survival, growth, fecundity) and environmental conditions (e.g., soil nutrients, water, defoliation).

    Our findings revealed that variation in levels of defence compounds (both condensed tannins and salicinoids) and insect herbivore performance were primarily genetically determined, while variation in plant growth and foliar nitrogen was more environmentally determined.

    Plasticity in plant growth, foliar nitrogen levels and insect herbivore performance varied substantially across different sites (year × location), and nutrient, water and carbon dioxide environments. Plasticity was lowest for chemical defence traits and all traits in contrasting ozone and defoliation environments.

    Our quantitative review also revealed several gaps in the literature, including a need for surveying more mature plants, a wider variety of insect herbivore species (e.g., leaf‐galling insects, specialist insects) and underrepresented environmental treatments (e.g., competition, defoliation, disease, light and water availability).

    Findings from this analysis highlight the importance of, and patterns within, intraspecific variation with respect to shaping the evolvability and plasticity of traits and governing the interactions of plants and insects.

    Aplain language summaryis available for this article.

     
    more » « less