Jules Silverman

Overview. The sensory systems of animals guide adaptive decisions about choice of food, habitat and potential mates. The gustatory system detects and discriminates among tastants that conveys information about the quality and nutritional value of food. Gustatory receptor neurons (GRNs) are housed within hair-like sensilla in insects that are broadly distributed on chemosensory appendages. GRNs can be defined by their modal taste specificity (e.g., sugar- or bitter-GRN) based on the gustatory receptors (GRs) they express. Each specific taste cell projects an axon directly to the central nervous system and guides acceptance and rejection of tastants. Taste polymorphisms are often described as changes in sensitivity of GRNs within a taste modality, with phenotypes ranging from highly sensitive to completely insensitive to a particular compound. The proposed project addresses a unique gain-of-function natural polymorphism that results in a highly adaptive behavior. In response to selection with baits, populations of the obligatorily commensal German cockroach Blattella germanica have developed behavioral deterrence to glucose and fructose, two universal phagostimulants. This trait is heritable, the rejection behavior is elicited by glucose or fructose alone, and the trait confers significant fitness advantage under selection pressure of glucose- or fructose-containing baits. This project will delineate mechanisms in the peripheral gustatory system responsible for this unusual phenotype with systematic electrophysiological, behavioral, morphological, genetic and molecular analyses. The project will test the hypotheses that (a) glucose and fructose are processed as deterrents by GRNs, (b) different taste organs differ in their GRN organization, contributing to effective processing of tastants as appetitive and aversive stimuli, and (c) that the molecular mechanism(s) that underlie this neuronal change involves either mis-expression of sugar-GRs on bitter GRNs or modifications of bitter-GRs on bitter-GRNs for affinity for glucose or fructose. Intellectual Merit. This research is significant to neuroethology and evolutionary biology because it will describe how persistent anthropogenic selection in an urban setting can result in rapid neuronal changes in gustatory function that support new behaviors and new food choices. The proposed research is the first in any animal to (i) characterize rapid changes in the gustatory system that have resulted in the emergence of a new adaptive behavior; (ii) describe in detail a novel system where a single stimulus at the same intensity mediates opposite appetitive and aversive responses by activating different neurons of the same sensory modality; and (iii) characterize the best understood case of behavioral resistance in animals. Finally, studies of the gustatory system in cockroaches, a primitive hemimetabolous lineage, will contribute to a broader understanding of insect gustation that so far has centered mainly on holometabolous and more highly advanced Diptera and Hymenoptera. Broader Impacts. Although behavioral resistance is often cited as a major impediment to efficacious pest control, especially of disease vectors, the mechanisms that underlie behavioral resistance are not known. Our recent Science paper and the proposed research represent the clearest delineation of sensory mechanisms that underlie the rapid emergence of a behavioral resistance trait in an animal population. We will recruit and train undergraduates through NCSU������������������s Honors, HHMI, Caldwell Scholars and Park Scholars programs. Graduate students will be recruited through listserves and local Historically Black Colleges and Universities. Cockroaches are excellent ���������������charismatic������������������ subjects for outreach and STEM activities. STEM outreach activities will include BugFest (35,000 participants annually in one day), Science Caf��������s, press releases, and the popular media. We have developed several modules on olfactory and gustatory responses of insects to sex pheromones and foods, and the interaction between human-imposed selection and rapid evolutionary adaptations, and we have presented outreach activities at local K-12 schools in disadvantaged communities. In collaboration with faculty at the NC School of Science and Math, we are developing hands-on integrated neurophysiology-behavior modules for NC high schools, and behavioral and electrophysiological assays of glucose-aversion have been incorporated into Insect Physiology and Insect Behavior courses. Our work is being incorporated into several textbooks and apps on Behavior and Evolution.

The German cockroach, Blattella germanica, is a significant pest within human-built structures and continues to be an important target of the pest control industry. This cockroach is a prime source of antigens that trigger asthma and other allergic reactions, a vector of human pathogens and a general nuisance thereby necessitating intervention by pest management professionals (PMPs). Currently, chemical insecticides are utilized in attempts to control German cockroaches, with baits being the favored product form for the past 30 years. Baits are largely effective because they do not require precise targeting of locations harboring cockroaches. Nearly 20 years ago the industry was alerted to failures in cockroach control with baits due to an unusual form of resistance now widely recognized as bait aversion (behavioral resistance). Bait aversion develops when initially a very small fraction of B. germanica within a population reject a component of the bait matrix. Over time, as non-bait averse individuals are eliminated, bait-averse individuals proliferate and represent most of the population. Like behavioral resistance, insecticides can lose their effectiveness when cockroaches susceptible to the active ingredient are selected against (physiological resistance). Cockroach populations displaying both behavioral and physiological resistance are presumed very rare. Yet, we have recently discovered B. germanica populations from apartments where baits became ineffective, which fit this dual resistance profile. We contend that this is a serious emerging problem for the pest management industry whereby bait products, the mainstay of German cockroach control, are gradually rendered ineffective. The overall goal of this project is to provide the pest management industry with a profile of this dual-resistant cockroach and recommend possible alternative control measures. Specifically, we aim to conduct behavioral and physiological resistance studies with bait active ingredients (AIs) (hydramethylnon, fipronil, indoxacarb) and the sugars used as feeding stimulants in baits (glucose, fructose, sucrose), assessing AI x sugar interactions and their potential to accelerate bait product failures. We predict that behavioral and physiological resistance are linked with bait averse individuals consuming sublethal doses of insecticide, thus facilitating catabolism, sequestration and/or excretion of AI. We will test our hypothesis in 1) laboratory experiments with recently collected strains of B. germanica from apartments where bait products failed and 2) field collections provided by PMPs. We will also explore alternative control measures for this emerging pest variant.

The German cockroach, Blattella germanica, is a significant pest within human-built structures throughout the southeastern U.S. and continues to be an important target of the pest control industry. This cockroach is a prime source of allergens that trigger asthma and other allergic reactions, a vector of human pathogens and a general nuisance thereby necessitating intervention by pest management professionals (PMPs). Currently, chemical insecticides are utilized in attempts to control German cockroach infestations, with baits increasingly becoming the favored formulation over the past 30 years. Baits are largely effective because they do not require precise targeting of locations harboring cockroaches and they readily deliver lethal doses of pesticides. Nearly 20 years ago the industry was alerted to failures in cockroach control with baits due to an unusual form of behavioral resistance now widely recognized as bait aversion. Bait aversion develops when initially a very small fraction of B. germanica within a population reject a component of the bait matrix. Over time, as non-bait averse individuals are eliminated, bait-averse individuals proliferate and represent most of the population. Physiological resistance, where the active ingredient loses its effectiveness as insecticide-susceptible cockroaches are eliminated, is much more common in various insects. Cockroach populations displaying both behavioral and physiological resistance are presumed very rare and have never been described behaviorally and physiologically. Yet, we have recently discovered B. germanica populations from apartments where baits became ineffective, which fit this dual resistance profile. These populations represent a serious emerging problem for the pest management industry whereby bait products, the mainstay of German cockroach control, are gradually rendered ineffective. Our overall project goal is to establish a profile of this dual-resistant cockroach, determine the scope of the problem and recommend possible alternative control measures. This project is related to the USDA?s national integrated pest management (IPM) roadmap that calls for increasing the use of IPM systems to reduce potential human health risks and minimize adverse environmental effects from pest and related management strategies in residential and public areas. Specifically, we aim to conduct behavioral and physiological resistance studies with bait active ingredients (AIs) (hydramethylnon, fipronil, indoxacarb) and the sugars used as feeding stimulants in baits (glucose, fructose, sucrose), assessing AI x sugar interactions and their potential to accelerate bait product failures. We suggest that behavioral and physiological resistance traits are functionally linked, with bait averse individuals consuming sublethal doses of insecticide, thus facilitating slower absorption, and greater catabolism, sequestration and/or excretion of AI. We will test our hypothesis in 1) laboratory experiments with recently collected strains of B. germanica from apartments where bait products failed and 2) field collected strains provided by PMPs. We will also explore alternative control measures for this emerging pest variant. Because the German cockroach is found throughout the southeastern U.S., our project developed here, in North Carolina, will apply equally well to other regions of the U.S. Federal and local regulations have dictated the implementation of IPM programs in and around municipalities (offices, hospitals, schools, recreation areas). The initial phase of any IPM program requires assessing pest abundance and distribution. Thus, our efforts to determine the scope of the insecticide-resistant bait-averse cockroach threat will provide a key component necessary for establishing effective management programs.

The Southeastern US is now infested with the Argentine ant, Linepithema humile. This introduced invasive species is a serious urban and agricultural pest throughout California and may repeat it's negative impact in the southeast with several established populations already in this state. North Carolina still maintains an important agricultural based economy with burgeoning urbanization. Recent NC Dept Agriculture. statistics value the NC green industry at $8.6 billion and USDA ranks NC 7th in agricultural cash receipts. Management of Argentine ant populations is constrained by many factors, including the ant?s ready access to a relatively abundant and consistent food source; honeydew from aphids, soft scales and mealybugs. Currently, only chemical insecticides are utilized in attempts to control Argentine ants and these are frequently misapplied, overused, and are generally ineffective because the large, diffuse colony structure of Argentine ants makes nests difficult to locate and treat. Delivery of one insecticide form, bait, does not require precise location of the nest and has minimal effects on non-target organisms; however, baits often fail because they are rejected in favor of Sternorrhyncha honeydew. The overall goal of this project is to develop an alternative pest management system for Argentine ants and is related to the USDA?s national integrated pest management (IPM) roadmap that calls for increasing the use of IPM systems to reduce potential human health risks and minimize adverse environmental effects from pest and related management strategies in residential and public areas. Specifically, we aim to develop a novel management approach whereby Argentine ants are simultaneously prevented from accessing their preferred food source and provided insecticidal bait. We predict that while Sternorrhyncha reductions alone will negatively impact Argentine ant populations, insecticidal baits will further depress ant numbers, being consumed when honeydew is scarce. We will test our hypothesis in two separate urban settings (1) commercial business park (2) residential neighborhood, where Sternorrhyncha populations on ornamental and shade trees are reduced with a winter dormant oil application or a soil-injected systemic treatment, which is followed by ant baiting. We will also evaluate a low nontarget risk treatment whereby Argentine ants are prevented from reaching Sternorrhyncha in the canopy through the placement of sticky barriers around tree trunks, in conjunction with baiting. In addition to assessing the technical merit of this approach, we will conduct surveys of homeowner/enduser perceptions of performance, and extend the results of this research to stakeholders through workshops and Cooperative Extension Service mailings. Because the Argentine ant is found throughout much of the southeastern U.S. and California, the pest management program developed here, in North Carolina, will apply equally well to other regions of the U.S. Moreover, federal and local regulations have dictated the implementation of IPM programs in and around municipalities (offices, hospitals, schools, recreation areas) and results obtained from research and implementation of this proposal around private residences will be applicable to other peridomestic environments.

The odorous house ant (OHA), Tapinoma sessile, is the most widespread pest ant in the United States and has been a common structural pest for over 100 years (1, 2). Unlike most pest ants, the OHA is a true urban pest with both exterior and interior infestations (1, 3). Similar to the German cockroach, Blattella germanica, the OHA lives opportunistically throughout human habitation including under carpet and in wall voids (1, 4). This nesting behavior causes subsequent damage to improperly stored food and potential negative impacts on human health (3). Unlike the German cockroach however, the OHA is not confined to human structures, but is also found in large populations in natural areas within the urban landscape. These populations may potentially act as the source for invasions of human dwellings (3, 5). Infestation can result either from a single large colony, or from numerous smaller discontinuous colonies, however the impacts on humans are the same. These two infestation types can be difficult to visually discriminate, which often results in ineffective control due to the requirement for alternative management strategies based on colony type. Our long term goal is the development of the most efficacious control strategy for OHA infestations, which we will accomplish by understanding: (1) genetic differences that may exist within the species currently recognized as the OHA; (2) the colony structure and size of this invasive within the urban environment; and (3) the efficacy of standard control practices between different colony types. Our ultimate goal is to generate and apply information on the basic population biology and genetic processes involved in the establishment and spread of the OHA in order to develop more effective means of preventing infestation and for managing existing infestations. The proposed research is a timely extension of the PI?s research program on the management of other structural pests. We propose to address the following three specific objectives: 1. Accurately determine through molecular phylogenetic methods, the true identify of invasive ants currently recognize as the OHA. 2. Examine colony structure and size within four regions, representative of the current range of this pest ?species?. 3. Investigate the efficacy of standard treatment practices using laboratory manipulations of different colony types of pest populations identified in Objectives 1 & 2.

The goal of the Clayton Sustainability Initiative is to provide a one point survey at Bayer?s Clayton Research Farm addressing biodiversity of plants, insects, and macroinvertebrates, and water quality, and to subsequently make recommendations for enhanced sustainability practices.