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Most social insect lineages contain socially parasitic cheater species that, rather than produce their own workers, infiltrate the nests of closely related social species and force the hosts to rear their offspring. These parasites have often lost social traits, like the ability to rear and produce workers, while retaining abilities for reproductive control and exhibiting novel parasitic innovations to capitalize on host resources. Given their close relationships with their hosts, social parasites are particularly informative to understand antagonistic coevolution and the essential components of sociality. Bumble bee social parasites are well suited to inform such evolutionary questions as they exhibit a gradation from facultative to obligate parasitism in their three independent origins of social parasitism, while also exhibiting a diverse obligately socially parasitic lineage, the subgenus Psithyrus Lepeletier, that varies across species in host use and invasion strategies. Despite the insights it can provide, cuckoo bumble bees, like most social parasites, are rare to encounter, and as such represent some of the most poorly understood bumble bee lineages. In this review, we bring together the state of our knowledge on the ecology and evolution of these rare cuckoo bees, to set a framework for further study, while also highlighting our current gaps in knowledge. In particular, we describe patterns of host breadth, geographic range, behavioral and morphological innovations, and social invasion strategies utilized across these bees to varying success. Considering their rarity, we highlight the pressing need to study these social parasites given conservation threats posed by host species declines.
Management of natural habitats is an important strategy for rare plant conservation. One common tool for managing natural habitats is the use of controlled fire. Rare plants in fire-dependent ecosystems often rely on frequent fires to increase nutrient availability, initiate germination, and limit cover from light competitors. Fire can also alter arthropod communities, including the pollinator communities upon which many flowering plants rely for sexual reproduction. However, it remains unclear how fire affects the pollination ecology of rare plants in fire-dependent ecosystems. Here we studied sites of varying burn history to examine the role of time since last fire on the morphology, flower visitor community, and degree of pollen limitation of seed production of Venus flytrap (Dionaea muscipula). The area occupied by blooming D. muscipula and number of traps per individual decreased with increasing time since burn. Though flower visitor richness and evenness were highest in sites of intermediate time post-burn, we found no differences in the composition of the flower visitor community in sites of different burn histories. Hand-pollinated flowers produced 8.3% more seeds per fruit than open-pollinated flowers, indicating that D. muscipula was pollen-limited, but burn history did not affect the magnitude of pollen limitation. Though we found no clear effect of burn history on the pollination ecology of D. muscipula, differences in blooming area and trap number suggest that burn history influences its distribution and growth, and affirms the benefits of frequent fires to its persistence.
Pollination by animals presents important advantages for plant reproduction. However, relying on biotic pollen dispersers also exposes plants to challenges, which include, for instance, the need to match the ecologies and phenologies of the pollinator species. Because of their ecological simplicity, specialized pollination systems are useful models to understand some of the variables that modulate how zoophilous pollination evolves, and whether or not species involved in pollination interactions respond jointly to evolutionary or ecological processes. In this study, we used a combination of field work, species distribution modeling (SDM), and geospatial analyses to investigate whether the number of floral visits by different pollinators in specialized zoophilous pollination interactions is correlated with the climatic suitability of the pollinator insects and, thus, to insect potential abundance. To do this, we investigated the pollination biology of four Calceolaria L. (Calceolariacea) species from central Chile, and we sampled across their whole ranges. Our results indicate that the four plant species are pollinated by different oil-bees of genera Centris Fabricius (Apidae: Centridini) and Chalepogenus Holmberg (Apidae: Tapinotaspidini), and that the number of floral visits varies at different localities. Our SDMs were accurate, successfully recovering the known ranges of the pollinators. Our analyses indicated that most plant species occur at localities in which insect climatic suitabilities are high. Furthermore, the number of pollinator visits at each locality was significantly and positively correlated with the insect suitability values, suggesting that matching high suitability areas can indeed increase the reproductive success of the plants.
Recovery plans for rare and endangered insects most commonly focus on identifying critical abiotic habitat requirements for focal species, and then using these criteria in developing species management portfolios. Biotic interaction data are rarely available, and when produced are seldom integrated into management plans due to their complexity of interpretation. Here we examine advances in our understanding of biotic factors that regulate behavior and life history in two rare insect species of conservation focus: the carrion-breeding American burying beetle, Nicrophorus americanus (Olivier) and the lek mating Gryllotalpa major (Saussure). Current recovery and conservation plans for both species are heavily weighted by abiotic habitat considerations, despite the likely regulation of populations by critical biotic interactions such as interspecies competition, symbioses, predation, and behavioral variation. Examples presented here support a more cohesive approach to constructing conservation management plans to prioritize the integration of ecological interaction data, and to incentivize related research leading to more effective species recovery outcomes.
Dioecy is rare among flowering plants, and is associated with a high frequency of threatened species. Dioecious plants are often pollinated by wind or insects, but are susceptible to pollination failure should male and female plants become spatially separated, or should pollinator abundance decline. Here we characterize the plant–pollinator interactions of Rhus michauxii Sarg (Sapindales: Anacardiaceae), an endangered dioecious shrub endemic to the southeastern United States. Working in the sandhills region of North Carolina, we detected a diverse community of arthropods visiting R. michauxii flowers, including 55 species or morphospecies, with moderate niche overlap between male and female flowers. Although most visitors acquired pollen from male flowers, pollen loads were greatly reduced or diluted on visitors to female flowers; conspecific pollen was completely absent at all-female sites. Bees in the genus Megachile appear to be the most important pollen vectors in this system because of their abundance and pollen load composition. We constructed a regional pollen transport network involving 73 arthropod species and 46 pollen species/morphotypes, in which R. michauxii participated in 10% of links and attracted 38% of individual visitors, suggesting that it competes successfully with other plants for visitation. Finally, time-lapse videography revealed that female inflorescences were visited about six times less often than male inflorescences, but at similar times of day. Despite overall high rates of bee visitation, pollen movement from male to female plants was uncommon, and restoration of sexual reproduction in this species may require hand pollination or translocation of suitable mates to single-sex sites.
Special Collection: Tools of the Behavior and Biocontrol Trade
Dispersal is a key component in the population ecology and dynamics of insects and remains one of the most difficult and intractable ecological processes to study in the field. As a consequence, many researchers have looked to laboratory methods for investigating the myriad factors that govern and impact an insect's ability to move within its environment. A key tool in this effort since at least the early 1950s has been the insect flight mill. Nearly 260 studies have been published using flight mills covering 214 species in 61 families and 9 orders.This review explores the methodology and technology of tethered flight in insects using flight mills. The goal is to provide the reader with a historical context of the approach, an understanding of the available tools and technology, background on how best to apply these tools through a comparative lens, and to summarize the wide breadth of factors that have been explored to further our knowledge of insect flight behavior. Overall, it is hoped that the interested reader will understand the limits and benefits of flight mills and will know where to find the resources, and perhaps collaborators, to pursue this line of study.
Having an effective method to track movement of arthropods in nature is essential for any mark-release-recapture (MRR) or mark-capture (MC) type experiment. A simple protein immunomarking technique (PIT) was described over a quarter of a century ago that has since been proven to be a highly useful and versatile tool for tracking arthropod dispersal patterns. The PIT consists of tagging arthropods with a specific protein. In turn, recaptured arthropods are examined for the presence of the protein tag by a highly sensitive and specific enzyme-linked immunosorbent assay. In this article, I review the progression of the PIT procedure, provide guidelines for conducting a successful PIT (MRR or MC) dispersal study, and highlight some of the ways this procedure has been adapted to study the dispersal patterns of a wide variety of arthropod species. My goal is that this information will provide researchers with the motivation to develop even more creative uses for the PIT.
The analysis of arthropod feeding activity is often determined by using species-specific postmortem gut content polymerase chain reaction and enzyme-linked immunosorbent assays (ELISA). Such mono-specific assays require time, resources, and technical expertise to develop for the food item (usually a pest insect species) that is the target of the investigation. A generic predator gut analysis method was described over a quarter of a century ago that does not require the development of a species-specific gut assay. This generic method remained in relative obscurity until about a decade ago. Recently, it has been used to study a wide range of arthropod feeding activities, such as carnivory, herbivory, scavenging, and other feeding interactions. For this review, I have coined this method as the universal food immunomarking technique (UFIT). The UFIT consists of tagging food items (i.e., prey, foliage, carrion, etc.) with a specific protein. In turn, the gut contents of foraging arthropods are examined for the presence of protein-marked food items by a standardized protein-specific sandwich ELISA. In this article, I give examples of the benefits of the UFIT gut assay approach over prey-specific gut assay approaches and tips on conducting a successful UFIT experiment, and provide examples of how it has been adapted to study a wide variety of arthropod feeding behaviors. My goal is to make researchers aware of another valuable tool in the gut analysis toolbox.
Lipids and carbohydrates have long been measured in organisms with various techniques. The microseparation and calorimetric method for quantifying lipids with a vanillin reagent, and glycogen and sugars with an anthrone reagent in mosquitoes described by Van Handel have been adapted widely for many insect species. Given the common use of this technique and variety of applications, a review is warranted. First, the procedure and adaptations are described, followed by other procedures available for quantifying energetic reserves. Next, practical logistics for running assays are discussed for new users. Previously, these assays have been reviewed for studying the sugar feeding behavior of biting flies and parasitoids. This review will survey a wider variety of applications from 85 papers with an emphasis on publications since 2004. For example, nutrient assays have been applied to establish the baseline energetic reserves of insects under various conditions, evaluating habitat manipulation programs, to better understand maternal allocation, overwintering and mating behavior, and flight energetics.
New or improved technologies can enable entomologists to address previously intractable questions, especially in the area of insect behavior. In this review, we describe the basic elements of applied computer vision for entomologists: image capture, data extraction, and analysis. We describe some of the currently available options in imaging hardware and cameras, lighting, software, as well as some basic data collection scenarios, and give detailed examples from our own experience. We suggest that the study of insect behavior is increasingly based on quantification of behavioral phenomena, that use of computer vision techniques for quantification will increase, and that the application of these tools and approaches will bring new insight and answers to questions in entomology. We hope this review can serve as a starting point for those interested in delving deeper into how computer vision can be applied to their research.
Studying the feeding, host damage, and transmission (i.e., acquisition, retention, and inoculation) of pathogens (plant and animal) by piercing-sucking arthropods is challenging. The piercing mouthparts are probed into opaque host tissues, precluding direct observation. This challenge was overcome by the invention of electropenetrography, or electrical penetration graph (both abbreviated EPG), the most rigorous method to identify arthropod feeding behaviors. However, until recently, most EPG research was restricted to studies of hemipteran plant pests, especially aphids and leafhoppers. Recent advances in EPG technology via the third-generation, alternating current–direct current (AC–DC) monitor (electropenetrograph) are opening new doors to expand the science into all types of arthropod feeding and oviposition. EPG can be used in three ways for the development of novel integrated pest management (IPM) tactics. First, in cases where the fundamental mechanisms of feeding/oviposition effects or pathogen transmission are unknown, EPG is instrumental in identifying mechanisms. Second, once the causes of damage or transmission are understood, EPG can be used to demonstrate the effects of insecticides, antifeedants, repellents, or other chemicals on specific feeding behaviors responsible for damage or transmission.Third, EPG can similarly identify the effects of resistant versus susceptible varieties of crop plants and animals, including transgenic organisms genetically engineered to express biopesticides or other genes. The purpose of this paper is to encourage new research avenues by 1) thoroughly reviewing history and electronic principles of EPG, culminating in the AC–DC electropenetrograph, 2) reviewing principles underlying biological meanings of waveforms, and 3) presenting a few examples of waveforms from new arthropod taxa.
David R. Horton, Navneet Kaur, W. Rodney Cooper, Eugene Miliczky, Ismael E. Badillo-Vargas, Gabriella Esparza-Díaz, Arash Rashed, Timothy D. Waters, Carrie H. Wohleb, Daniel L. Johnson, Lawrence Kawchuk, Andy S. Jensen
Arrival and spread of nonnative plant species can lead to changes in structure and function of the native insect fauna that include shifts in host use by native insect herbivores. Well-documented examples showing that these host shifts also lead to range expansion of native herbivores are, however, surprisingly rare. Evidence for range expansion requires an understanding of the insect's distribution preceding arrival of exotic species. These data often are lacking. The North American psyllid Bactericera maculipennis (Crawford) (Hemiptera: Triozidae), a specialist herbivore on plants in the Convolvulaceae, has been hypothesized to have expanded its geographic range after colonizing the exotic field bindweed (Convolvulus arvensis L.; Convolvulaceae). Efforts to test this idea run into the same retrospective problems typical of these analyses, in that the psyllid's host plant and its geographic distribution preceding arrival of C. arvensis are uncertain. We used the psyllid's current association with C. arvensis to help identify its natal (pre-bindweed) host, reasoning that a host shift by this specialist herbivore would be more likely if natal and exotic species are closely related. Phylogenetic analyses of plants, rearing trials, and field records led us to target species of Calystegia R. Brown (hedge and false bindweeds; Convolvulaceae) as natal hosts of B. maculipennis.The current presence of B. maculipennis in regions lacking Calystegia but where C. arvensis is common supported the hypothesis that arrival of the exotic weed C. arvensis has indeed led to range expansion by this host-specialized psyllid.
The association between Bemisia tabaci mitotypes and cotton leaf curl outbreaks in Pakistan was investigated using the mitochondria cytochrome oxidase I gene (COI) as a molecular marker. The 3′-651 base fragment has been used to resolve B. tabaci phylogenies. However, the 5′-618 base fragment was nearly unexplored. Phylogenetic analysis for 829 whiteflies from 11 districts in two provinces of Pakistan, indicated all haplotypes grouped on the Asia II major clade, with Asia II-1 mitotype predominating, at 84%, compared to Asia II-5 and II-7, at ∼16%, combined. The 3′- and 5′-fragment tree topologies were similar, while the concatenated topology was unique in some respects. Comparisons of segregating sites within the 3′- and 5′-loci, at third codon positions, 71 and 47, and of transitions to transversions (Ti/Tv) ratio of 2.93 and 5.9, respectively, showed the 3′-locus was most informative, while nucleotide diversity (π) was highest for the 5′-end, indicating both fragments contributed to concatenated tree structure. The extent of haplotype diversity, measured by Tajima's D, R2, and Fu's F analyses, revealed significant demographic expansion for Asia II-1 and II-7 mitotypes. The bottleneck that preceded the expansions was evident in the temporal changes in mtCOI polymorphisms beginning in ∼1990s, a timeframe known to have coincided with the adoption of a high-yield whitefly-susceptible cultivar in 1988, followed by pesticide overuse. These two cooperating phenomena appear to have exerted selection on the cotton leaf curl disease (CLCuD)-whitefly complex, resulting in the emergence of a resistance-breaking begomovirus as the polyphagous Asia II-1 mitotype underwent a genetic expansion that led to ‘a perfect storm’.
Eight exotic species of Cicadellidae apparently recently established in Hawaii are newly recorded. Four species belonging to subfamily Typhlocybinae, tribe Dikraneurini: Idona minuenda (Ball), native to Mexico and the Caribbean; Typhlocybella minima Baker, native to the Caribbean Basin from the southeastern United States to northern South America; Dikraneura absenta DeLong & Caldwell, is widespread in temperate North America west of the Rocky Mountains where it is reported to injure grasses, clover, and alfalfa; and Parallaxis yeeae n. sp. (Dikraneurini), representing the first record of the genus from Hawaii. Other new Hawaiian genus and species records are: Eupteryx decemnotata Rey (Typhlocybinae:Typhlocybini), native to Europe but recently established in Florida and California, which feeds on various species of Lamiaceae including several economically important herbs; Empoasca fabalis DeLong (Typhlocybinae: Empoascini), a pest of sweet potato and various legumes (Fabaceae) with a native range extending from the southern continental United States to Argentina but also established in Madeira and the Canary Islands; Anoscopus albifrons albifrons (L.) (Aphrodinae: Aphrodini), native to Europe but also established on the east and west coasts of temperate continental North America; and Ollarianus strictus (Ball) (Deltocephalinae: Athysanini), native to the southwestern United States and Mexico but recently introduced into Florida.
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