Genetic underpinnings of arthropod community distributions in Populus trichocarpa.

Community genetics seeks to understand the mechanisms by which natural genetic variation in heritable host phenotypes can encompass assemblages of organisms such as bacteria, fungi, and many animals including arthropods. Prior studies that focused on plant genotypes have been unable to identify genes controlling community composition, a necessary step to predict ecosystem structure and function as underlying genes shift within plant populations. We surveyed arthropods within an association population of Populus trichocarpa in three common gardens to discover plant genes that contributed to arthropod community composition. We analyzed our surveys with traditional single-trait genome-wide association analysis (GWAS), multitrait GWAS, and functional networks built from a diverse set of plant phenotypes. Plant genotype was influential in structuring arthropod community composition among several garden sites. Candidate genes important for higher level organization of arthropod communities had broadly applicable functions, such as terpenoid biosynthesis and production of dsRNA binding proteins and protein kinases, which may be capable of targeting multiple arthropod species. We have demonstrated the ability to detect, in an uncontrolled environment, individual genes that are associated with the community assemblage of arthropods on a host plant, further enhancing our understanding of genetic mechanisms that impact ecosystem structure.

Succession of Fungal Communities and Their Functional Profiles in a Decaying Foundation Species.

Dead plant biomass from foundation plant species is fundamental for the survival of coastal salt marshes because dead biomass aids in the vertical accretion of the ecosystem. Fungi regulate the decomposition of dead biomass, and thus play an essential role for marsh survival. Despite their importance, little is known about the compositional and functional changes of fungal communities in plant matter throughout senescence and litter decomposition. Here, we analyzed how fungal communities and their functionality change in the foundation plant species Spartina patens, which builds vast amounts of dead plant biomass (thatch) on the soil surface. We analyzed the chemical and fungal properties of live biomass, standing dead biomass (dead biomass shortly after senescence), upper thatch (top layer of litter on the soil surface), and lower thatch (bottom layer of litter on the soil surface) during September and November of 2021. We found that the chemical and fungal properties of different S. patens biomass types followed a predictable litter decomposition pattern. Notably, live biomass, standing dead biomass, upper thatch, and lower thatch all hosted unique fungal communities and litter chemistry. Functional groups present in live biomass (pathogens, epiphytes, and mycoparasites) were lost during senescence and later replaced by diverse saprotrophs. The abundance of lignocellulose saprotrophs increased throughout decomposition, with the highest abundance occurring in lower thatch. These results suggest a predictable succession of fungal communities through the senescence and decomposition of the foundation species S. patens. Our study highlights the diversity of fungal communities in a disappearing foundation species.

Does artificial light at night alter moth community composition?

Ecological studies investigating the effects of artificial light at night (ALAN) have primarily focused on single or a few species, and seldom on community-level dynamics. As ALAN is a potential cause of insect and biodiversity declines, community-level perspectives are essential. We empirically tested the hypothesis that moth species differentially respond to ALAN and that these responses can cause shifts in community composition. We sampled moths from prairie fragments in Colorado, USA. We tested whether local light sources, sky glow, site area and/or vegetation affected moth community diversity. We found that increased sky glow decreased moth abundance and species richness and shifted community composition. Increased sky glow shifted moth community composition when light and bait traps were combined; notably this result appears to be driven entirely by moths sampled at bait traps, which is an unbiased sampling technique. Our results show that ALAN has significant effects on moth communities and that local light sources have contrasting effects on moth community composition compared to sky glow. It is imperative that we better understand the contrasting effects of types of ALAN to comprehend the overall impacts of light pollution on biodiversity declines. This article is part of the theme issue 'Light pollution in complex ecological systems'.

Species loss and nitrogen pollution alter litter decomposition dynamics in coastal salt marshes.

Litter decomposition is a central ecosystem function because dead plant biomass plays a critical role in carbon storage, the nitrogen (N) cycle, and as food/habitat for animals and microorganisms. In the face of global change, interactions between organisms that participate in litter decomposition are likely to change due to species loss and N pollution. To understand how these global change factors may interact to alter litter decomposition, we manipulated the detritivore community and N concentrations in a coastal salt marsh for 2 years. We chose to manipulate densities of a dominant, detritivorous snail (Melampus bidentatus) because its population size is expected to decline due to climate change, yet its impact on litter decomposition has not been tested in the field. We measured litter decomposition rates, detritivore densities, and the N concentrations of sediment and litter. We found that endogenous N enrichment (N added live plants before decomposition), exogenous N enrichment (N added to decomposing plants) and higher densities of Melampus increased litter decomposition rates. Linear mixed models further revealed that snails, other detritivores, and soil NH4+ were the best predictors of litter mass loss in the middle stages of decomposition. Notably, exogenous N added to litter already enriched with N further increased mass loss but did not increase litter %N. Our study reveals how global change in the form species loss and N pollution can have palpable impacts on carbon cycling and ecosystem function.

Characterization of Salix nigra floral insect community and activity of three native Andrena bees.

Salix nigra (black willow) is a widespread tree that hosts many species of polylectic hymenopterans and oligolectic bees of the genus Andrena. The early flowering of S. nigra makes it an important nutritive resource for arthropods emerging from hibernation. However, since S. nigra is dioecious, not all insect visits will lead to successful pollination. Using both visual observation and pan-trapping, we characterized the community of arthropods that visited S. nigra flowers and assessed differences among male and female trees as well as the chemical and visual drivers that influenced community composition across 3 years. We found that male trees consistently supported higher diversity of insects than female trees and only three insect species, all Andrena spp., consistently visited both sexes. Additionally, Andrena nigrae, which was the only insect that occurred more on female than male flowers, correlated strongly to volatile cues. This suggests that cross-pollinators cue into specific aspects of floral scent, but diversity of floral visitors is driven strongly by visual cues of yellow male pollen. Through time, the floral activity of two Andrena species remained stable, but A. nigrae visited less in 2017 when flowers bloomed earlier than other years. When native bee emergence does not synchronize with bloom, activity appears to be diminished which could threaten species that subsist on a single host. Despite the community diversity of S. nigra flowers, its productivity depends on a small fraction of species that are not threatened by competition, but rather rapidly changing conditions that lead to host-insect asynchrony.

Global change in marine coastal habitats impacts insect populations and communities.

Salt marsh and mangrove coastal ecosystems provide critical ecosystem services, but are being lost at an alarming rate. Insect communities in these ecosystems are threatened by human impacts, including sea level rise, habitat loss, external inputs including nutrients, metals, and hydrocarbons, as well as weather events, such as hurricanes. While some disturbances are felt throughout the food web (e.g. hurricanes), others are mediated by impacts on the dominant plants (e.g. nutrient subsidies). The impacts of these disturbances on insects/spiders and their rate of recovery is dependent on trophic level, life history, and diet breadth. While we understand impacts of single disturbances relatively well, we have very little understanding of how multiple disturbances interact to affect insect communities.

Prey identity but not prey quality affects spider performance.

Increasing host plant quality affects higher trophic level predators, but whether such changes are simply a result of prey density or are also affected by changes in prey quality remain uncertain. Moreover, whether changes in prey quality affect measures of predator performance is understudied. Using a combination of field and greenhouse mesocosm experiments, we demonstrate that the survival and body size of a hunting spider (Pardosa littoralis Araneae: Lycosidae) is affected more by prey species identity than the trophic level of the prey. Furthermore, increasing host plant quality does not necessarily propagate through the food web by altering prey quality. While changes in plant quality affected spider body mass, they did so in opposite ways for spiders feeding on Prokelisia (Hemiptera: Delphacodes) herbivores relative to Tytthus (Hemiptera: Miridae) egg predators, and had no impact on spider body mass for two additional species of intraguild prey. These changes in body mass were important because greater body mass increased spider egg production. To examine the generality of this pattern, we reviewed the literature and found a consistent positive relationship between female body size and egg production for Pardosa species, indicating that body size is a reliable proxy for fitness. While many studies emphasize the importance of nitrogen to arthropod diets, this focus may be driven largely by our understanding of herbivore diets rather than predator diets. Thus, the positive impact of host plant quality on higher trophic level predators appears to be driven more by altering prey composition, density, and availability rather than simply providing predators with more nutritious prey.

Predator population size structure alters consumption of prey from epigeic and grazing food webs.

Numerous studies have found that predators can suppress prey densities and thereby impact important ecosystem processes such as plant productivity and decomposition. However, prey suppression by spiders can be highly variable. Unlike predators that feed on prey within a single energy channel, spiders often consume prey from asynchronous energy channels, such as grazing (live plant) and epigeic (soil surface) channels. Spiders undergo few life cycle changes and thus appear to be ideally suited to link energy channels, but ontogenetic diet shifts in spiders have received little attention. For example, spider use of different food channels may be highly specialized in different life stages and thus a species may be a multichannel omnivore only when we consider all life stages. Using stable isotopes, we investigated whether wolf spider (Pardosa littoralis, henceforth Pardosa) prey consumption is driven by changes in spider size. Small spiders obtained > 80% of their prey from the epigeic channel, whereas larger spiders used grazing and epigeic prey almost equally. Changes in prey consumption were not driven by changes in prey density, but by changes in prey use by different spider size classes. Thus, because the population size structure of Pardosa changes dramatically over the growing season, changes in spider size may have important implications for the strength of trophic cascades. Our research demonstrates that life history can be an important component of predator diet, which may in turn affect community- and ecosystem-level processes.

Tri-trophic interactions: bridging species, communities and ecosystems.

A vast body of research demonstrates that many ecological and evolutionary processes can only be understood from a tri-trophic viewpoint, that is, one that moves beyond the pairwise interactions of neighbouring trophic levels to consider the emergent features of interactions among multiple trophic levels. Despite its unifying potential, tri-trophic research has been fragmented, following two distinct paths. One has focused on the population biology and evolutionary ecology of simple food chains of interacting species. The other has focused on bottom-up and top-down controls over the distribution of biomass across trophic levels and other ecosystem-level variables. Here, we propose pathways to bridge these two long-standing perspectives. We argue that an expanded theory of tri-trophic interactions (TTIs) can unify our understanding of biological processes across scales and levels of organisation, ranging from species evolution and pairwise interactions to community structure and ecosystem function. To do so requires addressing how community structure and ecosystem function arise as emergent properties of component TTIs, and, in turn, how species traits and TTIs are shaped by the ecosystem processes and the abiotic environment in which they are embedded. We conclude that novel insights will come from applying tri-trophic theory systematically across all levels of biological organisation.

Putting the genes into community genetics.

As part of the long-term fusion of evolutionary biology and ecology (Ford, 1964), the field of community genetics has made tremendous progress in describing the impacts of plant genetic variation on community and ecosystem processes. In the "genes-to-ecosystems" framework (Whitham et al., 2003), genetically based traits of plant species have ecological consequences, but previous studies have not identified specific plant genes responsible for community phenotypes. The study by Barker et al. (2019) in this issue of Molecular Ecology uses an impressive common garden experiment of trembling aspen (Figure 1) to test for the genetic basis of tree traits that shape the insect community composition. Using a Genome-Wide Association Study (GWAS), they found that genomic regions associated with phytochemical traits best explain variation in herbivore community composition, and identified specific genes associated with different types of leaf-modifying herbivores and ants. This is one of the first studies to identify candidate genes underlying the heritable plant traits that explain patterns of insect biodiversity.

Habitat edge responses of generalist predators are predicted by prey and structural resources.

Generalist predators are thought to be less vulnerable to habitat fragmentation because they use diverse resources across larger spatial scales than specialist predators. Thus, it has been suggested that generalist predators may respond positively to habitat edges or demonstrate no edge response, because they can potentially use prey resources equally well on both sides of the habitat edge. However, most predictions about generalist predator responses to the habitat edge are based solely on prey resources, without consideration of other potential drivers. For instance, structural resources are essential for some species to build webs to capture prey or to avoid intraguild predation and cannibalism. In this study, we used both prey and structural resources to predict the response of four predator functional groups (hunting spiders, web-building spiders, aerial predators, and epigeic predators that feed on the detrital/algal food web) to a habitat edge between two salt-marsh grasses (Spartina alterniflora and Spartina patens). We found that generalist predators largely demonstrated negative responses to the habitat edge and had distinct habitat associations. Positive edge responses were only observed in one functional group (hunting spiders), and this pattern was driven by the two most abundant species. Negative responses to the habitat edge were more common among taxa and were better explained by structural resources rather than prey resources in the two habitats. Although it is generally acknowledged that specialists decline in fragmented habitats, generalists are thought to be more resilient. However, our research demonstrates that even generalists have habitat structural or food resource requirements that may limit their resilience to habitat loss and fragmentation.

Arthropod communities on hybrid and parental cottonwoods are phylogenetically structured by tree type: Implications for conservation of biodiversity in plant hybrid zones.

Although hybridization in plants has been recognized as an important pathway in plant speciation, it may also affect the ecology and evolution of associated communities. Cottonwood species (Populus angustifolia and P. fremontii) and their naturally occurring hybrids are known to support different plant, animal, and microbial communities, but no studies have examined community structure within the context of phylogenetic history. Using a community composed of 199 arthropod species, we tested for differences in arthropod phylogenetic patterns within and among hybrid and parental tree types in a common garden. Three major patterns emerged. (1) Phylogenetic diversity (PD) was significantly different between arthropod communities on hybrids and Fremont cottonwood when pooled by tree type. (2) Mean phylogenetic distance (MPD) and net relatedness index (NRI) indicated that communities on hybrid trees were significantly more phylogenetically overdispersed than communities on either parental tree type. (3) Community distance (Dpw) indicated that communities on hybrids were significantly different than parental species. Our results show that arthropod communities on parental and hybrid cottonwoods exhibit significantly different patterns of phylogenetic structure. This suggests that arthropod community assembly is driven, in part, by plant-arthropod interactions at the level of cottonwood tree type. We discuss potential hypotheses to explain the effect of plant genetic dissimilarity on arthropod phylogenetic community structure, including the role of competition and environmental filtering. Our findings suggest that cottonwood species and their hybrids function as evolutionarily significant units (ESUs) that affect the assembly and composition of associated arthropod communities and deserve high priority for conservation.

Complex community and evolutionary responses to habitat fragmentation and habitat edges: what can we learn from insect science?

Habitat fragmentation is the primary factor leading to species extinction worldwide and understanding how species respond to habitat edges is critical for understanding the effects of fragmentation on insect diversity in both natural and managed landscapes. Most studies on insect responses to the habitat edge focus on bottom-up changes in resources. Only a few recent studies have examined multi-trophic responses to habitat edges; the results of these studies highlight the problem that we lack a conceptual framework to understand the complex results observed when a single species' response to an edge 'cascades' throughout the food web in ways that are currently not predictable. Recent research from insect systems suggests that habitat edge responses cascade both up and down multi-trophic foodwebs and these altered species interactions may affect evolutionary processes. Future studies that investigate the effects of habitat edges on both ecological and evolutionary dynamics can help to fill these knowledge gaps and we suggest that insects, with short generation times, present an ideal opportunity to do so.

Plant production and alternate prey channels impact the abundance of top predators.

While numerous studies have examined the effects of increased primary production on higher trophic levels, most studies have focused primarily on the grazing food web and have not considered the importance of alternate prey channels. This has happened despite the fact that fertilization not only increases grazing herbivore abundance, but other types of consumers such as detritivores that serve as alternate prey for generalist predators. Alternate prey channels can sustain generalist predators at times when prey abundance in the grazing food web is low, thus increasing predator densities and the potential for trophic cascades. Using arthropod data from a fertilization experiment, we constructed a hierarchical Bayesian model to examine the direct and indirect effects of plant production and alternate prey channels on predators in a salt marsh. We found that increased plant production positively affected the density of top predators via effects on lower trophic level herbivores and mesopredators. Additionally, while the abundance of algivores and detritivores positively affected mesopredators and top predators, respectively, the effects of alternate prey were relatively weak. Because previous studies in the same system have found that mesopredators and top predators rely on alternate prey such as algivores and detritivores, future studies should examine whether fertilization shifts patterns of prey use by predators from alternate channels to the grazing channel. Finally, the hierarchical Bayesian model used in this study provided a useful method for exploring trophic relationships in the salt marsh food web, especially where causal relationships among trophic groups were unknown.

Predator hunting mode influences patterns of prey use from grazing and epigeic food webs.

Multichannel omnivory by generalist predators, especially the use of both grazing and epigeic prey, has the potential to increase predator abundance and decrease herbivore populations. However, predator use of the epigeic web (soil surface detritus/microbe/algae consumers) varies considerably for reasons that are poorly understood. We therefore used a stable isotope approach to determine whether prey availability and predator hunting style (active hunting vs. passive web-building) impacted the degree of multichannel omnivory by the two most abundant predators on an intertidal salt marsh, both spiders. We found that carbon isotopic values of herbivores remained constant during the growing season, while values for epigeic feeders became dramatically more enriched such that values for the two webs converged in August. Carbon isotopic values for both spider species remained midway between the two webs as values for epigeic feeders shifted, indicating substantial use of prey from both food webs by both spider species. As the season progressed, prey abundance in the grazing food web increased while prey abundance in the epigeic web remained constant or declined. In response, prey consumption by the web-building spider shifted toward the grazing web to a much greater extent than did consumption by the hunting spider, possibly because passive web-capture is more responsive to changes in prey availability. Although both generalist predator species engaged in multichannel omnivory, hunting mode influenced the extent to which these predators used prey from the grazing and epigeic food webs, and could thereby influence the strength of trophic cascades in both food webs.

Testing for phytochemical synergism: arthropod community responses to induced plant volatile blends across crops.

Using herbivore-induced plant volatiles (HIPVs) to attract specific natural enemies in the field has proven challenging, partly because of a poor understanding of: (i) which compound(s) to manipulate to attract specific taxa, and (ii) the ecological conditions over which HIPVs are effective. To address these issues, we quantified the response of a complex arthropod community to three common HIPVs (methyl salicylate, cis-3-hexen-1-ol, and phenylethyl alcohol) as individual compounds and equal part blends in corn and soybean fields. Of 119 arthropod taxa surveyed, we found significant responses by four species in corn fields (2 parasitoids, 1 herbivore, and 1 detritivore) and 16 in soybean fields (8 parasitoids, 3 predators, 4 herbivores, and 1 detritivore), with both attractive and repellent effects of the HIPVs observed. For example, tachinid flies were highly attracted to cis-3-hexen-1-ol (ca. 3-fold increase), but repelled by methyl salicylate (ca. 60 % decrease). Surprisingly, we found very few cases in which HIPVs acted synergistically; only two arthropod groups (ichneumonid wasps and phorid flies) were more attracted by a blend of the HIPVs than by the individual compounds composing the blend. Crop type, however, had a strong impact on the strength of arthropod responses to HIPVs. A few arthropod species were broadly affected across both crops (i.e., the herbivore Halticus bractatus was repelled by most of our treatments, regardless of crop background), but overall more arthropod groups responded to HIPVs released in soybean fields compared with corn. This was true despite the fact that taxa responding to HIPVs were present and abundant in both systems, suggesting that crop-based outcomes were likely driven by the plant matrix rather than mere differences in taxonomic composition of the arthropod community in corn vs. soybean fields. As a whole, these results suggest that: (i) repellent effects of HIPVs on natural enemies of herbivorous insects can be observed as frequently as attractive effects; (ii) odor blends may be no more effective than single-compound lures for some taxa; and (iii) crop background alters the magnitude of attraction to HIPVs, depending on the species being targeted.

Nutrient presses and pulses differentially impact plants, herbivores, detritivores and their natural enemies.

Anthropogenic nutrient inputs into native ecosystems cause fluctuations in resources that normally limit plant growth, which has important consequences for associated food webs. Such inputs from agricultural and urban habitats into nearby natural systems are increasing globally and can be highly variable, spanning the range from sporadic to continuous. Despite the global increase in anthropogenically-derived nutrient inputs into native ecosystems, the consequences of variation in subsidy duration on native plants and their associated food webs are poorly known. Specifically, while some studies have examined the effects of nutrient subsidies on native ecosystems for a single year (a nutrient pulse), repeated introductions of nutrients across multiple years (a nutrient press) better reflect the persistent nature of anthropogenic nutrient enrichment. We therefore contrasted the effects of a one-year nutrient pulse with a four-year nutrient press on arthropod consumers in two salt marshes. Salt marshes represent an ideal system to address the differential impacts of nutrient pulses and presses on ecosystem and community dynamics because human development and other anthropogenic activities lead to recurrent introductions of nutrients into these natural systems. We found that plant biomass and %N as well as arthropod density fell after the nutrient pulse ended but remained elevated throughout the nutrient press. Notably, higher trophic levels responded more strongly than lower trophic levels to fertilization, and the predator/prey ratio increased each year of the nutrient press, demonstrating that food web responses to anthropogenic nutrient enrichment can take years to fully manifest themselves. Vegetation at the two marshes also exhibited an apparent tradeoff between increasing %N and biomass in response to fertilization. Our research emphasizes the need for long-term, spatially diverse studies of nutrient enrichment in order to understand how variation in the duration of anthropogenic nutrient subsidies affects native ecosystems.

Do edge responses cascade up or down a multi-trophic food web?

Despite nearly 100 years of edge studies, there has been little effort to document how edge responses 'cascade' to impact multi-trophic food webs. We examined changes within two, four-tiered food webs located on opposite sides of a habitat edge. Based on a 'bottom-up' resource-based model, we predicted plant resources would decline near edges, causing similar declines in specialist herbivores and their associated predators, while a generalist predator was predicted to increase due to complementary resource use. As predicted, we found declines in both specialist herbivores and predators near edges, but, contrary to expectations, this was not driven by gradients in plant resources. Instead, the increase in generalist predators near edges offers one alternative explanation for the observed declines. Furthermore, our results suggest how recent advances in food web theory could improve resource-based edge models, and vice versa.