Glucose- and disaccharide-containing baits impede secondary mortality in glucose-averse German cockroaches.

Glucose aversion in the German cockroach, Blattella germanica (L.), results in behavioral resistance to insecticidal baits. Glucose-averse (GA) cockroaches reject foods containing glucose, even in relatively low concentrations, which protects the cockroaches from ingesting lethal amounts of toxic baits. Horizontal transfer of baits and the resulting secondary mortality have been documented in German cockroaches, including in insecticide resistant strains. However, the effects of the GA trait on secondary mortality have not been investigated. We hypothesized that ingestion of insecticide baits that contain glucose or glucose-containing disaccharides would result in behaviorally relevant glucose levels in the feces, possibly deterring coprophagy by GA nymphs. We fed adult female cockroaches hydramethylnon baits rich in either glucose, fructose, sucrose, or maltose and compared secondary mortality of GA and wild-type (WT) nymphs via coprophagy. When adult females were fed baits containing glucose, sucrose, or maltose and their feces offered to nymphs, secondary mortality was significantly lower in GA nymphs than in WT nymphs. However, survival of GA and WT nymphs was similar on feces generated by adult females fed fructose bait. Analysis of feces indicated that disaccharides in baits were hydrolyzed into glucose, some of which was excreted in the feces of females that ingested the bait. Based on these results, we caution that baits containing glucose or glucose-containing oligosaccharides may impede cockroach interventions; while GA adults and large nymphs avoid ingesting such baits, first instars reject the glucose-containing feces of any WT cockroaches that consumed the bait.

Nutritional condition affects tergal gland secretion and courtship success of male cockroaches.

An integral part of the courtship sequence of the German cockroach (Blattella germanica) involves the male raising his wings to expose tergal glands on his dorsum. When a female cockroach feeds on the secretion of these glands, she is optimally positioned for mating. Core chemical components have been identified, but the effect of male diet on the quality of the tergal gland secretion remains unexplored. After validating the pivotal role of tergal feeding in mating, we starved or fed reproductively mature males for one week. We then paired each male with a sexually receptive female and observed their interactions through an infrared-sensitive camera. While starvation had no effect on male courtship behavior, it did influence the duration of female tergal feeding and mating outcomes. Females fed longer on the gland secretion of fed males, and fed males experienced greater mating success than starved males (73.9% vs. 48.3%, respectively). These results suggest that the quality of the tergal gland secretions, and by association mating success, are dependent on the nutritional condition of the male.

Rapid evolution of an adaptive taste polymorphism disrupts courtship behavior.

The evolution of adaptive behavior often requires changes in sensory systems. However, rapid adaptive changes in sensory traits can adversely affect other fitness-related behaviors. In the German cockroach, a gustatory polymorphism, 'glucose-aversion (GA)', supports greater survivorship under selection with glucose-containing insecticide baits and promotes the evolution of behavioral resistance. Yet, sugars are prominent components of the male's nuptial gift and play an essential role in courtship. Behavioral and chemical analyses revealed that the saliva of GA females rapidly degrades nuptial gift sugars into glucose, and the inversion of a tasty nuptial gift to an aversive stimulus often causes GA females to reject courting males. Thus, the rapid emergence of an adaptive change in the gustatory system supports foraging, but it interferes with courtship. The trade-off between natural and sexual selection under human-imposed selection can lead to directional selection on courtship behavior that favors the GA genotype.

Comparison of Diet Preferences of Laboratory-Reared and Apartment-Collected German Cockroaches.

The German cockroach, Blattella germanica (L.) (Blattodea: Ectobiidae), is a common pest of human-built structures worldwide. German cockroaches are generalist omnivores able to survive on a wide variety of foods. A number of studies have concluded that laboratory-reared B. germanica self-select diets with an approximate 1P:3C (protein-to-carbohydrate) ratio. We predicted that field-collected insects would exhibit more variable dietary preferences, related to the wide-ranging quality, quantity, and patchiness of foods available to them. We compared diet self-selection of B. germanica within apartments and in the laboratory by offering them a choice of two complementary diets with 1P:1C and 1P:11C ratios. We observed high variation in the population-level self-selection of these diets among individual apartment sites as well as among various life stages tested in laboratory-based assays. Significant differences between populations in various apartments as well as between populations maintained in the laboratory suggested that factors beyond temporary food scarcity influence diet choice. Nevertheless, we found significant correlations between the amounts of diets ingested by cockroaches in apartments and cockroaches from the same populations assayed in the laboratory, as well as between males, females, and nymphs from these populations. These findings suggest that females, males, and nymphs within apartments adapt to the local conditions and convergently prefer similar amounts of food of similar dietary protein content.

Changes in the Peripheral Chemosensory System Drive Adaptive Shifts in Food Preferences in Insects.

A key challenge in understanding the evolution of animal behaviors is to identify cellular and molecular mechanisms that underlie the evolution of adaptive traits and behaviors in polymorphic populations under local selection pressures. Despite recent advances in fish, mice, and insects, there are still only a few compelling examples of major genes and cellular mechanisms associated with complex behavioral changes. Shifts in food or host preferences in insects, accompanied by changes in the peripheral chemosensory system, offer some of the best examples of adaptive behavioral evolution. A remarkable example is the German cockroach, Blattella germanica, a major indoor pest with a highly diverse omnivorous diet. Strong and persistent selection pressure with toxic-baits has induced rapid evolution of behavioral resistance in multiple cockroach populations. While typical cockroaches detect and accept the sugar glucose as a feeding-stimulant, behaviorally resistant cockroaches avoid eating glucose-containing toxic baits by sensing glucose as a deterrent. We review the peripheral gustatory neural mechanisms of glucose-aversion and discuss how the rapid emergence of taste polymorphisms can impede pest control efforts and affect foraging and mate-choice in adapted cockroach populations.

Persistence of a sugar-rejecting cockroach genotype under various dietary regimes.

Glucose-aversion is a heritable trait that evolved in a number of German cockroach (Blattella germanica L.) populations in response to strong selection with glucose-containing insecticide baits. However, in the absence of glucose-containing bait, glucose-averse (GA) cockroaches have lower performance than wild-type (WT) cockroaches in several fitness-determining traits. We allocated 48 caged populations initiated with homozygous GA and WT adults to four dietary treatments consisting of either pure rodent chow, rodent chow mixed to yield a content of either 20% glucose or 20% fructose, or a treatment consisting of choice between the 20% glucose- and the 20% fructose-containing food. After 6 months we found significantly higher frequency of WT individuals in populations restricted to the 20% glucose food, and after 12 months all dietary treatments contained significantly more WT individuals than expected. In accompanying experiments, we found lower survival and longer development time of GA nymphs restricted to glucose-containing food. We furthermore found evidence for assortative mating of females with males from their own genotype, with significant differences within WT cockroaches. Our study shows experimental evidence that within heterogeneous populations, WT German cockroaches will over time prevail in abundance over GA individuals, even when glucose is not a dietary component.

Effects of foraging distance on macronutrient balancing and performance in the German cockroach Blattella germanica.

The German cockroach (Blattella germanica) is an excellent model omnivore for studying the effect of foraging effort on nutrient balancing behavior and physiology, and its consequences for performance. We investigated the effect of foraging distance on individual German cockroaches by providing two foods differing in protein-to-carbohydrate ratio at opposite ends of long containers or adjacent to each other in short containers. Each food was nutritionally imbalanced, but the two foods were nutritionally complementary, allowing optimal foraging by selective feeding from both foods. We measured nutrient-specific consumption in fifth instar nymphs and newly eclosed females foraging at the two distances, hypothesizing that individuals foraging over longer distance would select more carbohydrate-biased diets to compensate for the energetic cost of locomotion. We then determined dry mass growth and lipid accumulation in the nymphs as well as mass gain and the length of basal oocytes in the adult females as an estimate of sexual maturation. Nymphs foraging over longer distance accumulated less lipid relative to total dry mass growth, but contrary to our predictions, their protein intake was higher and they accumulated more structural mass. In concordance, adult females foraging over longer distance gained more body mass and matured their oocytes faster. Our results show a positive effect of foraging distance on fitness-related parameters at two life stages, in both cases involving increased consumption of specific nutrients corresponding to requirements at the respective life stage.

Insecticide resistance and nutrition interactively shape life-history parameters in German cockroaches.

Fitness-related costs of evolving insecticide resistance have been reported in a number of insect species, but the interplay between evolutionary adaptation to insecticide pressure and variable environmental conditions has received little attention. We provisioned nymphs from three German cockroach (Blattella germanica L.) populations, which differed in insecticide resistance, with either nutritionally rich or poor (diluted) diet throughout their development. One population was an insecticide-susceptible laboratory strain; the other two populations originated from a field-collected indoxacarb-resistant population, which upon collection was maintained either with or without further selection with indoxacarb. We then measured development time, survival to the adult stage, adult body size, and results of a challenge with indoxacarb. Our results show that indoxacarb resistance and poor nutritional condition increased development time and lowered adult body size, with reinforcing interactions. We also found lower survival to the adult stage in the indoxacarb-selected population, which was exacerbated by poor nutrition. In addition, nutrition imparted a highly significant effect on indoxacarb susceptibility. This study exemplifies how poor nutritional condition can aggravate the life-history costs of resistance and elevate the detrimental effects of insecticide exposure, demonstrating how environmental conditions and resistance may interactively impact individual fitness and insecticide efficacy.

Diet quality affects bait performance in German cockroaches (Dictyoptera: Blattellidae).

BACKGROUND: Bait formulations are widely used to control German cockroach (Blattella germanica) populations. To perform optimally, these formulations must compete favorably with non-toxic alternative foods present within the insect's habitat. We hypothesized that the nutritional history of cockroaches and their acceptance or avoidance of glucose would affect their food preference and thus bait efficacy. To test this hypothesis, we conducted a controlled laboratory experiment, first providing glucose-accepting and glucose-averse cockroaches nutritionally defined diets and then offering them identical diets containing the insecticide hydramethylnon as a bait proxy to evaluate the effect of diets of differing macronutrient composition on bait performance. RESULTS: The interaction between diet composition and bait composition affected the survival of adult males as well as first-instar nymphs exposed to excretions produced by these males. Survival analyses indicated different responses of glucose-averse and glucose-accepting insects, but generally any combination of diet and bait that resulted in high diet intake and low bait intake reduced secondary kill. CONCLUSIONS: This study represents a comprehensive examination of the effect of alternative foods on bait efficacy. We suggest that disparities between the nutritional quality of baits and the foods that are naturally available could profoundly impact the management of German cockroach infestations. © 2016 Society of Chemical Industry.

Insecticide resistance and diminished secondary kill performance of bait formulations against German cockroaches (Dictyoptera: Blattellidae).

BACKGROUND: Bait formulations are considered to be the most effective method for reducing German cockroach (Blattella germanica) infestations. An important property of some bait formulations is secondary kill, whereby active ingredient (AI) is translocated in insect-produced residues throughout the cockroach population, especially affecting relatively sedentary early-instar nymphs. RESULTS: B. germanica was collected from a location where baits containing hydramethylnon, fipronil or indoxacarb had become ineffective, and these AIs were topically applied to adult males. Results revealed the first evidence for hydramethylnon resistance, moderate resistance to fipronil and extremely high resistance to indoxacarb. Insecticide residues excreted by field-collected males that had ingested commercial baits effectively killed nymphs of an insecticide-susceptible laboratory strain of B. germanica but failed to kill most nymphs of the field-collected strain. CONCLUSIONS: We report three novel findings: (1) the first evidence for hydramethylnon resistance in any insect; (2) extremely high levels of indoxacarb resistance in a field population; (3) reduced secondary mortality in an insecticide-resistant field-collected strain of B. germanica. We suggest that, while secondary mortality is considered to be advantageous in cockroach interventions, the ingestion of sublethal doses of AI by nymphs may select for high insecticide resistance by increasing the frequency of AI resistance alleles within the population. © 2015 Society of Chemical Industry.

Suboptimal nutrient balancing despite dietary choice in glucose-averse German cockroaches, Blattella germanica.

Insects have evolved fine-tuned gustatory and post-ingestive physiological mechanisms that enable them to self-select an optimal composition of macronutrients. Their ability to forage optimally among multiple food sources and maximize fitness parameters depends on their ability not only to taste and perceive the nutritional value of potential foods but also to avoid deleterious components; the strength of such avoidance should reflect the severity of the perceived hazard. In German cockroaches (Blattella germanica), glucose aversion has evolved in some populations in response to anthropogenic selection with glucose-containing insecticidal baits. In four feeding treatments, we gave newly eclosed glucose-averse female cockroaches free choice to feed from two artificial, nutritionally complementary foods varying in protein and carbohydrate composition, with glucose or fructose as the sole carbohydrate source in either food. After 6days of feeding, we measured diet consumption and the length of basal oocytes as an estimate of sexual maturation. The females did not compromise on their aversion to glucose in order to balance their protein and carbohydrate intake, and experienced lower sexual maturation rates as a consequence. Nutrient specific hunger via feedback mechanisms, and adjustments to gustatory sensitivity thus do not override the deterrence of glucose, likely due to strong selection against ingesting even small amounts of toxin associated with glucose in baits. In the absence of baits, glucose aversion would be expected to incur a fitness cost compared to wild-type individuals due to lower overall food availability but also to larger difficulty in attaining a nutritionally balanced diet.

Changes in taste neurons support the emergence of an adaptive behavior in cockroaches.

In response to the anthropogenic assault of toxic baits, populations of the German cockroach have rapidly evolved an adaptive behavioral aversion to glucose (a phagostimulant component of baits). We hypothesized that changes in the peripheral gustatory system are responsible for glucose aversion. In both wild-type and glucose-averse (GA) cockroaches, D-fructose and D-glucose stimulated sugar-gustatory receptor neurons (GRNs), whereas the deterrent caffeine stimulated bitter-GRNs. In contrast, in GA cockroaches, D-glucose also stimulated bitter-GRNs and suppressed the responses of sugar-GRNs. Thus, D-glucose is processed as both a phagostimulant and deterrent in GA cockroaches, and this newly acquired peripheral taste sensitivity underlies glucose aversion in multiple GA populations. The rapid emergence of this highly adaptive behavior underscores the plasticity of the sensory system to adapt to rapid environmental change.

Propagule pressure and climate contribute to the displacement of Linepithema humile by Pachycondyla chinensis.

Identifying mechanisms governing the establishment and spread of invasive species is a fundamental challenge in invasion biology. Because species invasions are frequently observed only after the species presents an environmental threat, research identifying the contributing agents to dispersal and subsequent spread are confined to retrograde observations. Here, we use a combination of seasonal surveys and experimental approaches to test the relative importance of behavioral and abiotic factors in determining the local co-occurrence of two invasive ant species, the established Argentine ant (Linepithema humile Mayr) and the newly invasive Asian needle ant (Pachycondyla chinensis Emery). We show that the broader climatic envelope of P. chinensis enables it to establish earlier in the year than L. humile. We also demonstrate that increased P. chinensis propagule pressure during periods of L. humile scarcity contributes to successful P. chinensis early season establishment. Furthermore, we show that, although L. humile is the numerically superior and behaviorally dominant species at baits, P. chinensis is currently displacing L. humile across the invaded landscape. By identifying the features promoting the displacement of one invasive ant by another we can better understand both early determinants in the invasion process and factors limiting colony expansion and survival.

Effect of scattered and discrete hydramethylnon bait placement on the Asian needle ant.

The Asian needle ant (Pachycondyla chinensis Emery) is invading natural and disturbed habitats across the eastern United States. While recent studies document the impact of P. chinensis on native ecosystems and human health, effective control measures remain unknown. Thus, we evaluated the field performance of a hydramethylnon granular bait, Maxforce Complete Granular Insect Bait, dispersed in clumps or scattered against P. chinensis. We also measured the effect of this bait on P. chinensis outside of the treatment zone. Surprisingly, unlike reports for other ant species, we achieved nearly complete P. chinensis population reductions 1 d after treatments were applied. Significant ant reductions were achieved until the end of our study at 28 d. No difference was recorded between clumped and scattered application methods. We found no overall difference in ant reductions from the edge out to 5 m beyond the treatment zone. Other local ant species appeared to be unaffected by the bait and foraging activity increased slightly after P. chinensis removal from treated areas. We suggest that Maxforce Complete Granular Insect Bait can be effective in an Asian needle ant treatment program.

Tandem carrying, a new foraging strategy in ants: description, function, and adaptive significance relative to other described foraging strategies.

An important aspect of social insect biology lies in the expression of collective foraging strategies developed to exploit food. In ants, four main types of foraging strategies are typically recognized based on the intensity of recruitment and the importance of chemical communication. Here, we describe a new type of foraging strategy, "tandem carrying", which is also one of the most simple recruitment strategies, observed in the Ponerinae species Pachycondyla chinensis. Within this strategy, workers are directly carried individually and then released on the food resource by a successful scout. We demonstrate that this recruitment is context dependent and based on the type of food discovered and can be quickly adjusted as food quality changes. We did not detect trail marking by tandem-carrying workers. We conclude by discussing the importance of tandem carrying in an evolutionary context relative to other modes of recruitment in foraging and nest emigration.

Differential inputs from chemosensory appendages mediate feeding responses to glucose in wild-type and glucose-averse German cockroaches, Blattella germanica.

Glucose is a universal phagostimulant in many animal species, including the cockroach Blattella germanica. However, some natural populations of B. germanica have been found that are behaviorally deterred from eating glucose. In dose-response studies, glucose was a powerful phagostimulant for wild-type cockroaches, but it strongly deterred feeding in a glucose-averse strain. Both strains, however, exhibited identical dose-response curves to other phagostimulants and deterrents. As a lead to electrophysiological and molecular genetics studies to investigate the mechanisms that underlie glucose-aversion, we used 2 assay paradigms to delineate which chemosensory appendages on the head contribute to the reception of various phagostimulatory and deterrent chemicals. Both simultaneous dual stimulation of the antenna and mouthparts of the insects and 2-choice preference tests in surgically manipulated insects showed that the glucose-averse behavior could be elicited through the gustatory systems of the antennae and mouthparts. The paraglossae alone were sufficient for maximum sensitivity to both phagostimulants and deterrents, including glucose as a deterrent in the glucose-averse strain. In addition to the paraglossae, the labial palps were more important than the maxillary palps in the reception of deterrents (caffeine in both strains and glucose in the glucose-averse strain). The maxillary palps, on the other hand, played a more important role in the reception of phagostimulants (fructose in both strains and glucose in the wild-type strain). Our results suggest that distinct inputs from the chemosensory system mediate opposite feeding responses to glucose in the wild-type and glucose-averse strains.

The Argentine ant persists through unfavorable winters via a mutualism facilitated by a native tree.

Mutualisms and facilitations can fundamentally change the relationship between an organism's realized and fundamental niche. Invasive species may prove particularly suitable models for investigating this relationship as many are dependent on finding new partners for successful establishment. We conducted field-based experiments testing whether a native tree facilitates the successful survival of the invasive Argentine ant, Linepithema humile (Mayr), through unfavorable winter conditions in the southeastern United States. We found Argentine ant nests aggregated around the native loblolly pine, Pinus taeda L., during the winter months. The bark of this tree absorbed enough radiant solar energy to reach temperatures suitable for Argentine ant foraging even when ambient temperatures should have curtailed all foraging. Conversely, foraging ceased when the trunk was shaded. The sun-warmed bark of this tree gave the Argentine ant access to a stable honeydew resource. Argentine ants were not found on or near deciduous trees even though bark temperatures were warm enough to permit Argentine ant foraging on cold winter days. Augmenting deciduous trees with sucrose water through the winter months lead to Argentine ant nests remaining at their base and Argentine ants foraging on the tree. The Argentine ant requires both foraging opportunity and a reliable winter food source to survive through unfavorable winter conditions in the southeastern United States. The loblolly pine provided both of these requirements extending the realized niche of Argentine ants beyond its fundamental niche.

Is it easy to be urban? Convergent success in urban habitats among lineages of a widespread native ant.

The most rapidly expanding habitat globally is the urban habitat, yet the origin and life histories of the populations of native species that inhabit this habitat remain poorly understood. We use DNA barcoding of the COI gene in the widespread native pest ant Tapinoma sessile to test two hypotheses regarding the origin of urban populations and traits associated with their success. First, we determine if urban samples of T. sessile have a single origin from natural populations by looking at patterns of haplotype clustering from across their range. Second, we examine whether polygynous colony structure--a trait associated with invasion success--is correlated with urban environments, by studying the lineage dependence of colony structure. Our phylogenetic analysis of 49 samples identified four well supported geographic clades. Within clades, Kimura-2 parameter pairwise genetic distances revealed <2.3% variation; however, between clade genetic distances were 7.5-10.0%, suggesting the possibility of the presence of cryptic species. Our results indicate that T. sessile has successfully colonized urban environments multiple times. Additionally, polygynous colony structure is a highly plastic trait across habitat, clade, and haplotype. In short, T. sessile has colonized urban habitats repeatedly and appears to do so using life history strategies already present in more natural populations. Whether similar results hold for other species found in urban habitats has scarcely begun to be considered.

Argentine ant invasion associated with loblolly pines in the southeastern United States: minimal impacts but seasonally sustained.

Invasive ants are notorious for directly displacing native ant species. Although such impacts are associated with Argentine ant invasions (Linepithema humile) worldwide, impacts within natural habitat are less widely reported, particularly those affecting arboreal ant communities. Argentine ants were detected in North Carolina mixed pine-hardwood forest for the first time but were localized on and around loblolly pines (Pinus taeda), probably because of association with honeydew-producing Hemiptera. We explored the potential impacts of L. humile on arboreal and ground-foraging native ant species by comparing interspersed loblolly pines invaded and uninvaded by Argentine ants. Impacts on native ants were assessed monthly over 1 yr by counting ants in foraging trails on pine trunks and in surrounding plots using a concentric arrangement of pitfall traps at 1, 2, and 3 m from the base of each tree. Of floristics and habitat variables, higher soil moisture in invaded plots was the only difference between plot types, increasing confidence that any ant community differences were caused by Argentine ants. Overall patterns of impact were weak. Composition differed significantly between Argentine ant invaded and uninvaded trunks and pitfalls but was driven only by the presence of Argentine ants rather than any resulting compositional change in native ant species. Native ant abundance and richness were similarly unaffected by L. humile. However, the abundance of individual ant species was more variable. Although numbers of the arboreal Crematogaster ashmeadi (Myrmicinae) declined on and around invaded pines, epigeic Aphaenogaster rudis (Myrmicinae) remained the most abundant species in all plots. Argentine ant densities peaked in late summer and fall, therefore overlapping with most native ants. Unexpected was their continued presence during even the coldest months. We provide evidence that Argentine ants can invade and persist in native North Carolina forests, probably mediated by pine-associated resources. However, their localized distribution and minimal impact on the native ant fauna relative to previously described invasions requires further resolution.

Population growth of Aphis gossypii and Myzus persicae (Hemiptera: Aphididae) in the presence of Linepithema humile and Tapinoma sessile (Hymenoptera: Formicidae).

Invasive ant species can have dramatic impacts on native ants, through direct predation and by usurping common resources. Most invasive ants and many native ants use honeydew, produced by phloem-sucking hemipterans. Because colonies of invasive ants can become very large after establishment, these ants may facilitate greater hemipteran trophobiont population growth compared with their sympatric native ant counterparts. We examined the population growth of an aphid mutualist, Aphis gossypii, and a nonmutualist, Myzus persicae, exposed to two Dolichoderine ants, Linepithema humile, a globally widespread invasive species, and Tapinoma sessile, a widespread co-occurring native ant, in North America in an enemy-free laboratory study. L. humile worker foraging activity was at least twice that of T. sessile, and populations of the myrmecophile, A. gossypii, were greater when exposed to L. humile than T. sessile, possibly caused, in part, by more frequent encounters with L. humile. L. humile ignored M. persicae when A. gossypii was absent, whereas T. sessile preyed on it. Both ant species preyed on M. persicae when A. gossypii was also present. This suggested that both ants may assess nutritional gains from aphid species (i.e., honeydew versus body tissue), eliminating less productive aphids competing for host plant space. Through their impact on populations of hemipteran mutualists, we suggest that colonies of L. humile and perhaps other invasive ants may acquire more honeydew than native ants, thereby fueling colony growth that leads to numerical dominance and widespread success in introduced environments.