Annual Review of Entomology - Volume 68, 2023

My research focuses on elucidating the chemical communication systems linking plants, herbivores, and natural enemies. My interests in integrating chemistry and agriculture led to my graduate studies in the emerging field of chemical ecology. My thesis research resulted in the identification, synthesis, and application of boll weevil sex pheromones. My research group subsequently developed chemical lures for more than 20 species of pest insects. I then shifted my focus to some of the first studies of the chemical signals produced by plants being attacked by herbivores. When insects feed, elicitors in the insects’ oral secretions, such as volicitin, a fatty acid–amino acid conjugate elicitor, stimulate plants to release volatile organic compounds. Parasitoid wasps learn to associate these species-specific volatiles with their herbivore hosts. These volatiles also prime nearby plants to activate a faster and higher defense response upon attack. Throughout my career, I have collaborated with scientists from diverse disciplines to tackle fundamental questions in chemical ecology and create innovative solutions for insect management. Our collaborative research has fundamentally changed and improved our understanding of the ongoing coevolution of plants, their herbivores, and the natural enemies that attack those herbivores.

Conservation biological control aims to enhance populations of natural enemies of insect pests in crop habitats, typically by intentional provision of flowering plants as food resources. Ideally, these flowering plants should be inherently attractive to natural enemies to ensure that they are frequently visited. We review the chemical ecology of floral resources in a conservation biological control context, with a focus on insect parasitoids. We highlight the role of floral volatiles as semiochemicals that attract parasitoids to the food resources. The discovery that nectar-inhabiting microbes can be hidden players in mediating parasitoid responses to flowering plants has highlighted the complexity of the interactions between plants and parasitoids. Furthermore, because food webs in agroecosystems do not generally stop at the third trophic level, we also consider responses of hyperparasitoids to floral resources. We thus provide an overview of floral compounds as semiochemicals from a multitrophic perspective, and we focus on the remaining questions that need to be addressed to move the field forward.

Genetically engineered corn and cotton that produce insecticidal toxins derived from the bacterium Bacillus thuringiensis (Bt) have been used to manage insect pests in the United States and elsewhere. In some cases, this has led to regional suppression of pest populations and pest eradication within the United States, and these outcomes were associated with reductions in conventional insecticides and increased profits for farmers. In other instances, pests evolved resistance to multiple Bt traits, compromising the capacity of Bt crops to manage pests and leading to increased feeding injury to crops in the field. Several aspects of pest biology and pest–crop interactions were associated with cases where pests remained susceptible versus instances where pests evolved resistance. The viability of future transgenic traits can be improved by learning from these past outcomes. In particular, efforts should be made to delay resistance by increasing the prevalence of refuges and using integrated pest management.

Iron is an essential micronutrient for all types of organisms; however, iron has chemical properties that can be harmful to cells. Because iron is both necessary and potentially damaging, insects have homeostatic processes that control the redox state, quantity, and location of iron in the body. These processes include uptake of iron from the diet, intracellular and extracellular iron transport, and iron storage. Early studies of iron-binding proteins in insects suggested that insects and mammals have surprisingly different mechanisms of iron homeostasis, including different primary mechanisms for exporting iron from cells and for transporting iron from one cell to another, and subsequent studies have continued to support this view. This review summarizes current knowledge about iron homeostasis in insects, compares insect and mammalian iron homeostasis mechanisms, and calls attention to key remaining knowledge gaps.

Mites are masters at attaching to larger animals, often insects, in a temporary symbiosis called phoresy that allows these tiny animals to exploit patchy resources. In this article, we examine phoresy in the Acari, including those that feed on their carriers in transit, from a broad perspective. From a phylogenetic perspective, phoresy has evolved several times from free-living ancestors but also has been lost frequently. Rotting logs appear to be the first patchy resource exploited by phoretic mites, but the evolution of rapid life cycles later permitted exploitation of short-lived resources. As phoresy is a temporary symbiosis, most species have off-host interactions with their carrier. These relationships can be highly complex and context dependent but often are exploitative of the carrier's resources or progeny. Transitions from phoresy to parasitism seem widespread, but evidence for transitions from obligate phoretic parasitism to permanent parasitism is weak.

Mating produces profound changes in the behavior of female flies, such as an increase in oviposition, reduction in sexual receptivity, increase in feeding, and even excretion. Many of these changes are produced by copulation, sperm, and accessory gland products that males transfer to females during mating. Our knowledge on the function of the male ejaculate and its effect on female insects is still incipient. In this article, we review peri- and postcopulatory behaviors in tephritid flies. We address the effects of male copulatory behavior; copula duration; and the male ejaculate, sperm, and accessory gland products on female remating behavior. Many species from these families are pests of economic importance; thus, understanding male mating effects on female behavior contributes to both developing more effective environmentally friendly control methods and furthering our understanding of evolutionary implications of intersexual competition and sexual conflict.

Parasitoid wasps are important components of insect food chains and have played a central role in biological control programs for over a century. Although the vast majority of parasitoids exploit insect herbivores as hosts, others parasitize predatory insects and arthropods, such as ladybird beetles, hoverflies, lacewings, ground beetles, and spiders, or are hyperparasitoids. Much of the research on the biology and ecology of parasitoids of predators has focused on ladybird beetles, whose parasitoids may interfere with the control of insect pests like aphids by reducing ladybird abundance. Alternatively, parasitoids of the invasive ladybird Harmonia axyridis may reduce its harmful impact on native ladybird populations. Different life stages of predatory insects and spiders are susceptible to parasitism to different degrees. Many parasitoids of predators exhibit intricate physiological interrelationships with their hosts, adaptively manipulating host behavior, biology, and ecology in ways that increase parasitoid survival and fitness.

Since the transition from water to land, maintaining water balance has been a key challenge for terrestrial arthropods. We explore factors that allow terrestrial arthropods to survive within a variably dry world and how they shape ecological interactions. Detection of water and hydration is critical for maintaining water content. Efficient regulation of internal water content is accomplished by excretory and osmoregulatory systems that balance water intake and loss. Biochemical and physiological responses are necessary as water content declines to prevent and repair the damage that occurs during dehydration. Desiccation avoidance can occur seasonally or daily via a move to more favorable areas. Dehydration and its avoidance have ecological impacts that extend beyond a single species to alter trophic interactions. As climate changes, evolutionary and ecological processes will be critical to species survival during drought.

Spotted lanternfly, Lycorma delicatula (White), invaded the eastern United States in 2014 and has since caused economic and ecological disruption. In particular, spotted lanternfly has shown itself to be a significant pest of vineyards and ornamental plants and is likely to continue to spread to new areas. Factors that have contributed to its success as an invader include its wide host range and high mobility, which allow it to infest a wide range of habitats, including agricultural, urban, suburban, and managed and natural forested areas. Management is dependent on chemical use, although no single currently available control measure alone will be sufficient.

Bed bugs (Hemiptera: Cimicidae) are an important group of obligate hematophagous urban insect pests. The global resurgence of bed bugs, involving the common bed bug, Cimex lectularius L., and the tropical bed bug, Cimex hemipterus (F.), over the past two decades is believed to be primarily due to the development of insecticide resistance, along with global travel and poor pest management, which have contributed to their spread. This review examines and synthesizes the literature on bed bug origins and their global spread and the literature on historical and contemporary control options. This includes bed bug prevention, detection and monitoring, nonchemical and chemical control methodologies (and their limitations), and potential future control options. Future research needs are highlighted, especially the factors behind the modern resurgence, the necessity of identifying differences between the two bed bug species relevant to control, and the need to improve insecticide test protocols and management strategies.

Communication by substrate-borne mechanical waves is widespread in insects. The specifics of vibrational communication are related to heterogeneous natural substrates that strongly influence signal transmission. Insects generate vibrational signals primarily by tremulation, drumming, stridulation, and tymbalation, most commonly during sexual behavior but also in agonistic, social, and mutualistic as well as defense interactions and as part of foraging strategies. Vibrational signals are often part of multimodal communication. Sensilla and organs detecting substrate vibration show great diversity and primarily occur in insect legs to optimize sensitivity and directionality. In the natural environment, signals from heterospecifics, as well as social and enemy interactions within vibrational communication networks, influence signaling and behavioral strategies. The exploitation of substrate-borne vibrational signaling offers a promising application for behavioral manipulation in pest control.

The economic and environmental threats posed by non-native forest insects are ever increasing with the continuing globalization of trade and travel; thus, the need for mitigation through effective biosecurity is greater than ever. However, despite decades of research and implementation of preborder, border, and postborder preventative measures, insect invasions continue to occur, with no evidence of saturation, and are even predicted to accelerate. In this article, we review biosecurity measures used to mitigate the arrival, establishment, spread, and impacts of non-native forest insects and possible impediments to the successful implementation of these measures. Biosecurity successes are likely under-recognized because they are difficult to detect and quantify, whereas failures are more evident in the continued establishment of additional non-native species. There are limitations in existing biosecurity systems at global and country scales (for example, inspecting all imports is impossible, no phytosanitary measures are perfect, knownunknowns cannot be regulated against, and noncompliance is an ongoing problem). Biosecurity should be a shared responsibility across countries, governments, stakeholders, and individuals.

Stingless bees form perennial colonies of honey-making insects. The >600 species of stingless bees, mainly Neotropical, live throughout tropical latitudes. Foragers influence floral biology, plant reproduction, microbe dispersal, and diverse ecosystem functions. As tropical forest residents since the upper Cretaceous, they have had a long evolutionary history without competition from honey bees. Most stingless bees are smaller than any Apis species and recruit nest mates to resources, while their defense strategies exclude stinging behavior but incorporate biting. Stingless bees have diversified ecologically; excel in nesting site selection and mutualisms with plants, arthropods, and microbes; and display opportunism, including co-opting plant defenses. As their biology becomes better known, applications to human endeavors are imposing selective pressures from exploitation and approaches to conservation that entail colony extraction from wildlands. Although some meliponines can adjust to new conditions, their populations shall require tropical diversity for survival and reproduction.

Although it is generally more adaptive for insects to produce additional generations than to have longer life cycles, some insects produce one or fewer generations per year (univoltine or semivoltine life cycles, respectively). Some insects with the potential to produce multiple generations per year produce a univoltine life cycle in response to environmental conditions. Obligatory univoltine insects have a single long diapause or multiple diapauses in different seasons. Semivoltine insects have multiple diapauses in different years, a prolonged diapause for more than a year, or diapause controlled by a circannual rhythm. Diapause in these insects greatly varies among species both in the physiological mechanism and in the evolutionary background, and there is no general rule defining it. In this review, we survey the physiological control of univoltine and semivoltine insects’ diapause and discuss the adaptive significance of the long life cycles. Although constraints such as slow development are sometimes responsible for these life cycles, the benefits of these life cycles can be explained by bet-hedging in many cases. We also discuss the effect of climate warming on these life cycles as a future area of research.

Wood-boring pests (WBPs) pose an enormous threat to global forest ecosystems because their early stage infestations show no visible symptoms and can result in rapid and widespread infestations at later stages, leading to large-scale tree death. Therefore, early-stage WBP detection is crucial for prompt management response. Early detection of WBPs requires advanced and effective methods like remote sensing. This review summarizes the applications of various remote sensing sensors, platforms, and detection methods for monitoring WBP infestations. The current capabilities, gaps in capabilities, and future potential for the accurate and rapid detection of WBPs are highlighted.

The fall armyworm (FAW), Spodoptera frugiperda (Lepidoptera, Noctuidae), is a well-known agricultural pest in its native range, North and South America, and has become a major invasive pest around the globe in the past decade. In this review, we provide an overview to update what is known about S. frugiperda in its native geographic ranges. This is followed by discussion of studies from the invaded areas to gain insights into S. frugiperda's ecology, specifically its reproductive biology, host plant use, status of insecticide resistance alleles, and biocontrol methods in native and invasive regions. We show that reference to host strains is uninformative in the invasive populations because multidirectional introduction events likely underpinned its recent rapid spread. Given that recent genomic analyses show that FAW is much more diverse than was previously assumed, and natural selection forces likely differ geographically, region-specific approaches will be needed to control this global pest.

Winter provides many challenges for insects, including direct injury to tissues and energy drain due to low food availability. As a result, the geographic distribution of many species is tightly coupled to their ability to survive winter. In this review, we summarize molecular processes associated with winter survival, with a particular focus on coping with cold injury and energetic challenges. Anticipatory processes such as cold acclimation and diapause cause wholesale transcriptional reorganization that increases cold resistance and promotes cryoprotectant production and energy storage. Molecular responses to low temperature are also dynamic and include signaling events during and after a cold stressor to prevent and repair cold injury. In addition, we highlight mechanisms that are subject to selection as insects evolve to variable winter conditions. Based on current knowledge, despite common threads, molecular mechanisms of winter survival vary considerably across species, and taxonomic biases must be addressed to fully appreciate the mechanistic basis of winter survival across the insect phylogeny.

The use of the functional feeding group–damage type system for analyzing arthropod and pathogen interactions with plants has transformed our understanding of herbivory in fossil plant assemblages by providing data, analyses, and interpretation of the local, regional, and global patterns of a 420-Myr history. The early fossil record can be used to answer major questions about the oldest evidence for herbivory, the early emergence of herbivore associations on land plants, and later expansion on seed plants. The subsequent effects of the Permian–Triassic ecological crisis on herbivore diversity, the resulting formation of biologically diverse herbivore communities on gymnosperms, and major shifts in herbivory ensuing from initial angiosperm diversification are additional issues that need to be addressed. Studies ofherbivory resulting from more recent transient spikes and longer-term climate trends provide important data that are applied to current global change and include herbivore community responses to latitude, altitude, and habitat. Ongoing paleoecological themes remaining to be addressed include the antiquity of modern interactions, differential herbivory between ferns and angiosperms, and origins of modern tropical forests. The expansion of databases that include a multitude of specimens; improvements in sampling strategies; development of new analytical methods; and, importantly, the ability to address conceptually stimulating ecological and evolutionary questions have provided new impetus in this rapidly advancing field.

There is growing awareness of pollinator declines worldwide. Conservation efforts have mainly focused on finding the direct causes, while paying less attention to building a systemic understanding of the fragility of these communities of pollinators. To fill this gap, we need operational measures of network resilience that integrate two different approaches in theoretical ecology. First, we should consider the range of conditions compatible with the stable coexistence of all of the species in a community. Second, we should address the rate and shape of network collapse once this safe operational space is exited. In this review, we describe this integrative approach and consider several mechanisms that may enhance the resilience of pollinator communities, chiefly rewiring the network of interactions, increasing heterogeneity, allowing variance, and enhancing coevolution. The most pressing need is to develop ways to reduce the gap between these theoretical recommendations and practical applications. This perspective shifts the emphasis from traditional approaches focusing on the equilibrium states to strategies that allow pollination networks to cope with global environmental change.