Teresa M. Stoepler

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.

Hemocyte Density Increases with Developmental Stage in an Immune-Challenged Forest Caterpillar

The cellular arm of the insect immune response is mediated by the activity of hemocytes. While hemocytes have been well-characterized morphologically and functionally in model insects, few studies have characterized the hemocytes of non-model insects. Further, the role of ontogeny in mediating immune response is not well understood in non-model invertebrate systems. The goals of the current study were to (1) determine the effects of caterpillar size (and age) on hemocyte density in naïve caterpillars and caterpillars challenged with non-pathogenic bacteria, and (2) characterize the hemocyte activity and diversity of cell types present in two forest caterpillars: Euclea delphinii and Lithacodes fasciola (Limacodidae). We found that although early and late instar (small and large size, respectively) naïve caterpillars had similar constitutive hemocyte densities in both species, late instar Lithacodes caterpillars injected with non-pathogenic E. coli produced more than a twofold greater density of hemocytes than those in early instars. We also found that both caterpillar species contained plasmatocytes, granulocytes and oenocytoids, all of which are found in other lepidopteran species, but lacked spherulocytes. Granulocytes and plasmatocytes were found to be strongly phagocytic in both species, but granulocytes exhibited a higher phagocytic activity than plasmatocytes. Our results strongly suggest that for at least one measure of immunological response, the production of hemocytes in response to infection, response magnitudes can increase over ontogeny. While the underlying raison d’ être for this improvement remains unclear, these findings may be useful in explaining natural patterns of stage-dependent parasitism and pathogen infection.

Review of Parasitoid Wasps and Flies (Hymenoptera, Diptera) Associated with Limacodidae (Lepidoptera) in North America, with a Key to Genera

Abstract. Hymenopteran and dipteran parasitoids of slug moth caterpillars (Lepidoptera: Limacodidae) from North America are reviewed, and an illustrated key to 23 genera is presented. Limacodid surveys and rearing were conducted during the summer months of 2004–2009 as part of research on the ecology and natural history of Limacodidae in the mid-Atlantic region of the U.S.A. Parasitoid rearing involved a combination of collecting naturally occurring larvae in the field (at least 14 host species) and placing out large numbers of “sentinel” larvae derived from laboratory colonies of three host species. Species in the following families are documented from limacodids in North America as primary or secondary parasitoids (number of genera for each family in parentheses; number of genera included in key but not reared through this research in brackets): Chalcididae ([1]; Hymenoptera: Chalcidoidea), Eulophidae (3; Chalcidoidea), Pteromalidae ([1]; Chalcidoidea), Trichogrammatidae (1; Chalcidoidea), Braconidae (3 [1]; Hymenoptera: Ichneumonoidea), Ichneumonidae (7 [3]; Ichneumonoidea), Ceraphronidae (1; Hymenoptera: Ceraphronoidea), Trigonalidae (2; Hymenoptera: Trigonaloidea), Bombyliidae ([1]; Diptera: Asilioidea), and Tachinidae (3; Oestroidea). We recovered 20 of 28 genera known to attack limacodids in North America. Records discerned through rearing in the mid-Atlantic region are augmented with previously published host-parasitoid relationships for Limacodidae in North America north of Mexico. New records are reported for the following parasitoids (total new records in parentheses): Uramya limacodis (Walker) (1), U. pristis (Townsend) (5), Austrophorocera spp. (6), Ceraphron sp. (1), Alveoplectrus lilli Gates (1), Playplectrus americana (Girault) (10), Pediobius crassicornis (Thomson) (1), Trichogramma (1), Mesochorus discitergus (Say) (1), Hyposoter fugitivus (Say) (1), and Isdromas lycaenae (Howard) (5). The male of Platyplectrus americana (Hymenoptera: Eulophidae) is redescribed, and the female is described for the first time. Incidental and miscellaneous host-parasitoid associations are discussed, and it is concluded that most of these records are likely parasitoids of contaminants accidentally introduced during the limacodid rearing process. Triraphis eupoeyiae (Ashmead), new combination, is transferred from Rogas (Hymenoptera: Braconidae).

A Simple Protocol for Extracting Hemocytes from Wild Caterpillars

Insect hemocytes (equivalent to mammalian white blood cells) play an important role in several physiological processes throughout an insects life cycle. In larval stages of insects belonging to the orders of Lepidoptera (moths and butterflies) and Diptera (true flies), hemocytes are formed from the lymph gland (a specialized hematopoietic organ) or embryonic cells and can be carried through to the adult stage. Embryonic hemocytes are involved in cell migration during development and chemotaxis regulation during inflammation. They also take part in cell apoptosis and are essential for embryogenesis. Hemocytes mediate the cellular arm of the insect innate immune response that includes several functions, such as cell spreading, cell aggregation, formation of nodules, phagocytosis and encapsulation of foreign invaders. They are also responsible for orchestrating specific insect humoral defenses during infection, such as the production of antimicrobial peptides and other effector molecules. Hemocyte morphology and function have mainly been studied in genetic or physiological insect models, including the fruit fly, Drosophila melanogaster, the mosquitoes Aedes aegypti and Anopheles gambiae and the tobacco hornworm, Manduca sexta. However, little information currently exists about the diversity, classification, morphology and function of hemocytes in non-model insect species, especially those collected from the wild. Here we describe a simple and efficient protocol for extracting hemocytes from wild caterpillars. We use penultimate instar Lithacodes fasciola (yellow-shouldered slug moth) (Figure 1) and Euclea delphinii (spiny oak slug) caterpillars (Lepidoptera: Limacodidae) and show that sufficient volumes of hemolymph (insect blood) can be isolated and hemocyte numbers counted from individual larvae. This method can be used to efficiently study hemocyte types in these species as well as in other related lepidopteran caterpillars harvested from the field, or it can be readily combined with immunological assays designed to investigate hemocyte function following infection with microbial or parasitic organisms.

Host ontogeny determines parasitoid use of a forest caterpillar

For most organisms, patterns of natural enemy‐mediated mortality change over the course of development. Shifts in enemy pressure are particularly relevant for organisms that exhibit exponential growth during development, such as juvenile insects that increase their mass by several orders of magnitude. As one of the dominant groups of insect herbivores in most terrestrial plant communities, larval lepidopterans (caterpillars) are host to a diverse array of parasitoids. Previous research has described how the frequency of herbivore parasitism varies among host plants or habitats, but much less is known about how parasitism pressure changes during host development. To test whether the two major parasitoid taxa, wasps and flies, differentially attack shared hosts based on host developmental stage, we simultaneously exposed early‐ and late‐instar Euclea delphinii Boisduval (Lepidoptera: Limacodidae) caterpillars to parasitism in the field. We found strong evidence that parasitoids partition hosts by size; adult female wasps preferentially parasitized small caterpillars, whereas adult female flies preferred to attack large caterpillars. Our results demonstrate that host ontogeny is a major determinant of parasitoid host selection. Documenting how shifts in enemy pressure vary with development is important to understanding both the population biology and evolutionary ecology of prey species and their enemies.

Intraplant Movement of Generalist Slug Caterpillars (Limacodidae: Lepidoptera) : Effects of Host Plant and Light Environment

ABSTRACT Insect herbivores frequently move about on their host plants to obtain food, avoid enemies and competitors, and cope with changing environmental conditions. Although numerous plant traits influence the movement of specialist herbivores, few studies have examined movement responses of generalist herbivores to the variable ecological conditions associated with feeding and living on an array of host plants. We tested whether the movement patterns of two generalist caterpillars (Euclea delphinii Boisduval and Acharia stimulea Clemens, Limacodidae) differed on six different host tree species over 10 d. Because these tree species vary in the range of light environments in which they commonly grow, we also compared the movement responses of E. delphinii caterpillars to two contrasting light environments, sun and shade. For both caterpillar species, multiple measures of movement varied significantly among host tree species. In early censuses, movement rates and distances were highest on red oak and black cherry and lowest on white oak. Site fidelity was greatest on white oak and lowest on black cherry. Movement of both caterpillar species varied inversely with mean predator density on five of the six host trees. Other ecological predictors (e.g., leaf size and the density of other herbivores) were unrelated to movement. Light environment altered behavior such that caterpillars in the shade moved and fed more often, and moved greater distances, than caterpillars in the sun. Although the mechanism(s) promoting or inhibiting movement under these different conditions requires further study, the consequences of increased movement for caterpillar development and mortality from natural enemies are discussed.

First Host Records for the Nearctic Species Triraphis discoideus (Hymenoptera: Braconidae: Rogadinae)

ABSTRACT: Limacodid larvae were collected from 2004 – 2007 on leaves of the following host plants in the District of Columbia and Maryland: Carya glabra, pignut hickory; Quercus alba, white oak; Quercus rubra, northern red oak; Nyssa sylvatica, black gum; Prunus serotina, black cherry; and Fagus grandifolia, American beech. Field-collected larvae were brought to the laboratory where they were kept in isolation for the purpose of rearing parasitoids. The rogadine braconid Triraphis discoideus (Cresson) was reared from the following host-host plant combinations: Acharia stimulea (Clemens), Adoneta spinuloides (Herrich-Schäffer), Lithacodes fasciola (Herrich-Schäffer), and Parasa chloris (Moore) on red oak; Euclea delphinii (Boisduval) on black gum and red oak; Isa textula (Herrich-Schäffer) on American beech, red oak, and white oak; Natada nasoni (Grote) on American beech, black gum, red oak, and white oak; Prolimacodes badia Hübner on black cherry and red oak; and an undetermined species of Tortricidia Packard on American beech. Host use was previously unknown for T. discoideus. Host use and phenology are discussed for Triraphis harrisinae (Ashmead), the only other described species of Triraphis in the Nearctic Region.

Facilitative Effects of Group Feeding on Performance of the Saddleback Caterpillar (Lepidoptera: Limacodidae)

ABSTRACT Gregarious feeding by insect herbivores is a widely observed, yet poorly understood, behavioral adaptation. Previous research has tested the importance of group feeding for predator deterrence, noting the ubiquity of aposematism among group-feeding insects, but few studies have examined the role of feeding facilitation for aggregates of insect herbivores. We tested the hypothesis that group feeding has facilitative effects on performance of the saddleback caterpillar, Acharia stimulea Clemens, a generalist herbivore of deciduous trees. In an understory forest setting, we reared caterpillars alone or in groups on two different host plants, white oak (Quereus alba L.) and American beech (Fagus grandifolia Ehrlich), and recorded multiple measures of insect performance during regular field censuses. As predicted, A. stimulea caterpillars feeding in groups on white oak had increased relative growth rates compared with caterpillars feeding alone, and the magnitude of this facilitative effect varied among censuses, conferring benefits both early and late in development. By contrast, no facilitative effects of group feeding were detected on beech, suggesting that the benefits of facilitative feeding may be host specific. On both hosts, caterpillar development time was slightly faster for group-feeding cohorts compared with their solitary counterparts. Because early instar caterpillars are particularly vulnerable to predation and parasitism, even modest increases in growth rates and reductions in development time may decrease exposure time to enemies during these vulnerable stages. On both hosts, group feeding also reduced the trade-off between individual development time and cocoon mass, suggesting that feeding efficiency is improved in group feeders relative to solitary caterpillars.

A New Species of Alveoplectrus Wijesekara and Schauff (Hymenoptera: Chalcidoidea: Eulophidae) Parasitic on Limacodidae (Lepidoptera)

Abstract Alveoplectrus lilli Gates, new species, (Hymenoptera: Chalcidoidea: Eulophidae) is described and illustrated. This species was reared from five species of field-collected slug caterpillars (Lepidoptera: Limacodidae). It is differentiated from similar species of Alveoplectrus.

LIGHT ENVIRONMENT GENERATES ECOLOGICAL TRADE‐OFFS IN HERBIVORES

Photo 1. White oak (Quercus alba) saplings were grown in (A) full sun or (B) full shade (under 90% light reduction shade cloth) on the roof of Bell Hall, a four-story building located at George Washington University in Washington, D.C. Saplings were kept under these light conditions for three months (30 March–30 June 2010), which encompassed the entire developmental process from pre-bud break through full leaf expansion and hardening, to induce saplings to produce (C) sun and (D) shade leaves, respectively. White oak shade-grown saplings produced fewer leaves than sun-grown saplings, but individual shade leaves were 78% larger, resulting in greater total leaf area compared to sun-grown saplings. Shade leaves were 27% lower in toughness, 14% lower in carbon:nitrogen ratio, 42% and 77% lower in hydrolyzable and condensed tannins, respectively, 12% higher in nitrogen, and 8% higher in water content relative to sun leaves. LIGHT ENVIRONMENT GENERATES ECOLOGICAL TRADE-OFFS IN HERBIVORES Teresa M. Stoepler and John T. Lill All photographs by Teresa M. Stoepler