Shannon M. Murphy

Enemy-free space maintains swallowtail butterfly host shift

Natural enemies can be significant sources of mortality for herbivorous insects and therefore important agents of natural selection. One might expect selection to favor herbivores that escape from their natural enemies into enemy-free space. Although this is an appealing idea, it has received little empirical support, and no studies have documented enemy-free space as part of a nonagricultural, nonartificial host shift. The Alaskan swallowtail butterfly, Papilio machaon aliaska, uses as host plants a species in the family Apiaceae (Cnidium cnidiifolium) along with two Asteraceae species (Artemisia arctica and Petasites frigidus). I analyzed growth and survival of P. m. aliaska larvae in the field on the three host plants in treatments that either exposed or protected them from predators. I found that, in the presence of predators, larval survival is greater on the novel hosts (Asteraceae) than on the ancestral host (Apiaceae), but that in the absence of predators survival and growth are greater on the ancestral host. These results are a demonstration of enemy-free space as a mechanism for maintaining a naturally occurring host shift.

CHEMICAL FACILITATION OF A NATURALLY OCCURRING HOST SHIFT BY PAPILIO MACHAON BUTTERFLIES (PAPILIONIDAE)

Host shifts by herbivorous insects have contributed substantially to current patterns of association between insects and plants. Despite their evolutionary and agricultural interest, however, the plant traits that predispose insects to colonize some plants instead of others are poorly understood. To examine whether ancestral and novel hosts share similar chemical oviposition stimulants that would facilitate a host shift, we investigated a well-substantiated host shift within the Papilio machaon group of swallowtail butterflies. Papilio machaon aliaska uses three plant species as host plants. Cnidium cnidiifolium belongs to the family Apiaceae, the ancestral host-plant family of the P. machaon group. Artemisia arctica and Petasites frigidus, by contrast, belong to the family Asteraceae and were colonized relatively recently by this group of butterflies. Papilio machaon oregonius, a close relative of P. m. aliaska, feeds and oviposits exclusively on Artemisia dracunculus, also in the Asteraceae. We made polar and nonpolar extracts of all four host plants, conducted bioassays with P. m. aliaska and P. m. oregonius females to test for oviposition stimulants, and found that the polar extracts were the most active. Using high-performance liquid chromatography, we separated the polar extracts into three fractions and again conducted bioassays with P. m. aliaska and P. m. oregonius females. The fraction containing hydroxycinnamic acid (HCA) derivatives was the only active fraction for all plant species. We further separated the HCA fraction and found two sub-fractions that were active in all of the host-plant species. Co-chromatography indicated that several major constituents of the active fractions are shared between ancestral and novel hosts. In a secondary series of experiments, we investigated chemical fractions of a non-host plant, Artemisia frigida, and identified fractions of the A. frigida extract that contained oviposition deterrents and a fraction that contained oviposition stimulants for P. m. aliaska females. We conclude that the similarity of stimulant profiles in ancestral and novel host plants is consistent with the hypothesis that plant chemistry has played a role in the establishment of this host shift.

Increased primary production shifts the structure and composition of a terrestrial arthropod community

Numerous studies have examined relationships between primary production and biodiversity at higher trophic levels. However, altered production in plant communities is often tightly linked with concomitant shifts in diversity and composition, and most studies have not disentangled the direct effects of production on consumers. Furthermore, when studies do examine the effects of plant production on animals in terrestrial systems, they are primarily confined to a subset of taxonomic or functional groups instead of investigating the responses of the entire community. Using natural monocultures of the salt marsh cordgrass Spartina alterniflora, we were able to examine the impacts of increased plant production, independent of changes in plant composition and/or diversity, on the trophic structure, composition, and diversity of the entire arthropod community. If arthropod species richness increased with greater plant production, we predicted that it would be driven by: (1) an increase in the number of rare species, and/or (2) an increase in arthropod abundance. Our results largely supported our predictions: species richness of herbivores, detritivores, predators, and parasitoids increased monotonically with increasing levels of plant production, and the diversity of rare species also increased with plant production. However, rare species that accounted for this difference were predators, parasitoids, and detritivores, not herbivores. Herbivore species richness could be simply explained by the relationship between abundance and diversity. Using nonmetric multidimensional scaling (NMDS) and analysis of similarity (ANOSIM), we also found significant changes in arthropod species composition with increasing levels of production. Our findings have important implications in the intertidal salt marsh, where human activities have increased nitrogen runoff into the marsh, and demonstrate that such nitrogen inputs cascade to affect community structure, diversity, and abundance in higher trophic levels.

Cascading effects of host size and host plant species on parasitoid resource allocation

1. The bottom‐up factors that determine parasitoid host use are an important area of research in insect ecology. Host size is likely to be a primary cue for foraging parasitoids due to its potential influence on offspring development time, the risk of multiparasitism, and host immunocompetence. Host size is mediated in part by host‐plant traits that influence herbivore growth and potentially affect a herbivores quality as a host for parasitoids.

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.

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.

Comparative morphology of the gastrointestinal tract in the feeding specialist Sciurus aberti and several generalist congeners

Aberts squirrel (Sciurus aberti) is a highly specialized mammal dependent upon ponderosa pine (Pinus ponderosa) for a significant part of its yearly diet. For up to six months of the year, these squirrels only eat ponderosa pine phloem, which is a high-fiber, low-quality diet. We compared gross morphologies of the gastrointestinal tract in specialized Aberts squirrels to those of generalist fox squirrels (S. niger) and found that Aberts squirrels have significantly longer gastrointestinal tracts with greater tissue surface area and weight than do fox squirrels. Published data describing the eastern gray squirrel (S. carolinensis) and the western gray squirrel (S. griseus) indicate that these generalist species have body weights and a gut morphology very similar to that of the fox squirrel. We conclude that the morphology of the digestive tract of Aberts squirrel has become adapted to its low-quality diet.

Life History Traits and Rearing Techniques for Fall Webworms (Hyphantria cunea Drury) in Colorado

ABSTRACT. The fall webworm (Hyphantria cunea Drury) is a moth species native to North America and an invasive pest in Europe and Asia. Hyphantria cunea larvae are noted generalists, and have been recorded feeding on dozens of plant families worldwide. There appear to be at least two forms of H. cunea that are distinguished by the larval head capsule color: black or red. Most previous accounts of H. cunea in the literature focus on the black-headed form. The three goals of the research we present here are to 1) detail successful rearing techniques for the red-headed form of H. cunea, 2) describe life history traits of red-headed H. cunea in Colorado and 3) test whether female pupal mass predicts potential fecundity for H. cunea as well as other lepidopteran species. Our data are compiled from two years of rearing experiments in the lab. In addition, we compare measures of life history traits from our research with those of other collections of H. cunea from Asia, Europe, Canada, and other regions of the United States to enable a better comparison between the black-headed and red-headed forms of H. cunea.

The effect of host plant on larval survivorship of the Alaskan swallowtail butterfly (Papilio machaon aliaska)

The Alaskan swallowtail butterfly, Papilio machaon aliaska (Lepidoptera: Papilionidae), uses three plant species as host plants. Cnidium cnidiifolium (Turcz.) Schischk. belongs to the family Apiaceae, the ancestral host‐plant family of the P. machaon group. Artemisia arctica Less. and Petasites frigidus (L.) Franch, in contrast, belong to the distantly related Asteraceae family and were colonized relatively recently by this group of butterflies. Previous work has shown that larval survival is highest on the novel host plants when natural enemies are present in the field. Here I examine whether P. m. aliaska fitness varied when individuals were reared on the three host plants in a common environment, free of environmental and ecological complications such as predation. I collected 12 P. m. aliaska females and measured their reproductive success when their progeny were reared on each of the three host plants. I assessed larval fitness on each of the hosts by recording the percentage pupation and percentage emergence as well as by measuring pupal mass. I found that larvae reared on the ancestral host plant, C. cnidiifolium, had higher fitness than did larvae reared on either of the novel host plants, A. arctica or P. frigidus. Larvae reared on C. cnidiifolium were more likely to pupate, achieved a greater pupal mass, and had higher emergence rates than larvae reared on the novel hosts. I interpret these results to mean that, in the absence of predation, the ancestral host plant is a better host for P. m. aliaska larvae than either novel host and I contend that this result does not appear to support the hypothesis that P. m. aliaska populations in central Alaska are divided into host races.

Enemy-Free Space for Parasitoids

ABSTRACT Natural enemies often cause significant levels of mortality for their prey and thus can be important agents of natural selection. It follows, then, that selection should favor traits that enable organisms to escape from their natural enemies into “enemy-free space” (EFS). Natural selection for EFS was originally proposed as a general force in structuring ecological communities, but more recently has become conceptually narrow and is typically only invoked when studying the evolutionary ecology of host plant use by specialized insect herbivores. By confining the application of EFS to specialist herbivores, its potential value to community and evolutionary ecology has been marginalized. As a first step toward exploring the potential explanatory power of EFS in structuring ecological niches of higher trophic-level organisms, we consider host use by parasitoids. Here, we present three distinct mechanisms from our studies of caterpillar host—parasitoid interactions suggesting that parasitoids may be under selection to exploit traits of their hosts and the plants on which those hosts feed to garner EFS for their developing offspring. The neglect of EFS as a top—down selective force on host use by parasitoids may be a serious limitation to basic and applied ecology, given the great diversity of parasitoids and their significance in controlling herbivore populations in both natural and managed ecosystems. Parasitoids and other mesopredators represent excellent candidates for further developments of EFS theory and testing of its broader importance.