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Larval house flies, Musca domestica (L.), nutritionally require live bacteria; therefore, all stadia are associated with microbe-rich environments. Larvae live among and ingest bacteria, which are digested via the combined activity of digestive enzymes, lysozyme, and antimicrobial effectors. Some bacteria resist digestion and subsequent proteolytic processes that occur during metamorphosis, and are carried trans-stadially. Adult house flies ingest bacteria directly from septic substrates or indirectly via self-grooming. Ingested bacteria also face digestion in adults; nonetheless, some microbes not only survive, but proliferate and exchange genetic material. The interaction between adult flies and bacteria is critical in determining vector potential. If the fly is ineffective at eliminating ingested microbes, they can be disseminated in excreta. Unlike larvae, adult house flies are highly mobile, synanthropic, and gregarious, moving indiscriminately between septic environments and domestic locations. Flies can travel miles between sites, dispersing pathogens and their antibiotic-resistance and virulence genes. Considered together, these aspects of adult fly biology underlie their role in the epidemiology and ecology of infectious diseases. Studies of house fly biology have fortuitously revealed interesting adaptations to their septic lifestyle that can be exploited in future approaches to fly control and human health. Larval dependence on microbes can be integrated in novel control strategies, which alter habitat microflora. In contrast, larvae can be utilized beneficially to clear manure of pathogens before being used as fertilizer. In addition, house fly defense effectors such as antimicrobial peptides serve as an untapped resource with the potential to generate novel classes of microbicidal therapeutics.
Blow flies are commonly associated with decomposing material. In most cases, the larvae are found feeding on decomposing vertebrate remains; however, some species have specialized to feed on living tissue or can survive on other alternate resources like feces. Because of their affiliation with such septic environments, these insects have close associations with microbes. Historically, a tremendous amount of research focused on these insects due to their veterinary importance. Within the past 40 yr, efforts have expanded this research to include areas such as systems ecology, forensics, and even wound debridement (maggot) therapy. Initial research efforts examining the relationship between microbes and these insects were hampered by the technology available. However, with the advent of high-throughput sequencing and modern molecular techniques, new avenues of research examining these interactions have opened up. The purpose of this article is to highlight the research exploring the interactions between microbes and blow flies with regards to blow fly biology, the application of such information to benefit humanity, and potential future pathways of research.
House flies, Musca domestica L., develop within and feed upon microbe-rich substrates such as manure, acquiring and potentially disseminating pathogenic bacteria. Because adult female flies frequent manure due to oviposition or nutrition requirements, we hypothesized females would consume more manure than males even in the presence of additional food sources (e.g. sugar), resulting in measurable differences in bacterial load between sexes. House fly acquisition of bacteria from manure inoculated with GFP-expressing E. coli or Salmonella sp. was examined for both sexes over 24 h in assays where 1) inoculated manure was the only food source and 2) both inoculated manure and sugar water were provided. We conducted assays with mated male and female flies separately to determine sex-specific effects on bacterial acquisition. Over 24 h, bacterial abundance increased in manure inoculated with S. Typhimurium, but not E. coli. In flies, bacterial abundance increased within sex only in S. Typhimurium assays. Overall, female flies harbored more bacteria than males; however, differences in abundance were only significant at early time points. In the E. coli manure–sugar assays, male and female colony-forming units (CFU) abundance differed at 4 and 12 h, while CFU abundance differed at 4 and 12 h in all S. Typhimurium assays. Fly digestive tract observations from manure–sugar assays supported these initial differences especially at 4 h where females contained manure and fly food, while males contained only sugar water. Identifying sex-specific effects on house fly acquisition and carriage of bacteria from manure facilitates risk assessment of pathogen transmission on farms.
Necrophagous insect studies have shown that decomposing vertebrate remains are an important ephemeral resource within an ecosystem. However, the microbes (e.g., bacteria and archaea) that were a part of the once living organism and the exogenous taxa that colonize this postmortem resource remain largely underexplored. Also, it is not well understood how these two kingdoms interact to recycle decaying biomass, an important mechanistic question for ecosystem function ecology. To better understand microbial community dynamics throughout decomposition, we used swine carcasses (N = 6) as models for mammalian postmortem decomposition to characterize epinecrotic microbial communities from: the abdominal skin of replicate carcasses; the internal microbiome of individual necrophagous dipteran larvae (maggots); and the microbiome of dipteran larval masses that had colonized the carcasses. Sampling occurred every 12 h for the duration of the decomposition process. We characterized these microbial communities over time using high-throughput 16S amplicon sequencing. The relative abundance of microbial taxa changed over decomposition as well as across sampling locations, suggesting significant interactions between the environment, microbes, and insect larvae. Maggot masses were represented by multiple blow fly species in each mass: Phormia regina (Meigen), Lucilia coeruleiviridis (Macquart), and Cochliomyia macellaria(F.). Relative abundance of these species within the mass also changed as decomposition progressed, suggesting the presence of certain Calliphoridae species within a mass may be associated with temporal shifts of the microbial communities. These results provide new insight into the community ecology of carrion decomposition by providing new data on interactions of microbes and dipteran larvae over time.
Strains of Salmonella enterica can be subdivided into clades that differ in their genetic composition, influencing microbial ecology and bacterial transmission. Salmonella serovar Montevideo strains 1110 and 304, representatives of two different clades, were used to evaluate interactions with the various stages of horn fly development. Sterilized cattle dung was inoculated with Salmonella monocultures, and horn fly larvae were exposed to 103, 105, and 107 colony-forming units (CFU)/g per strain. Salmonella supported horn fly development, and concentration-dependent differences in pupal survival suggested that Salmonella Montevideo 304 impacts adult emergence when larvae are reared in a high concentration. Viable bacteria of each strain were quantified from larvae, pupae, and newly emerged adults. Both strains were cultured from larvae at a mean ~105, regardless of concentration, and both strains survived pupation. Quantities of Salmonella 1110 were stationary through the midpupal stage, after which quantities declined in pupae reared in 105 and increased twofold in pupae reared in 107 CFU/g. Quantities of Salmonella 304 remained stationary throughout pupal development when reared in 105, yet increased 29-fold when reared in 107 CFU/g. At high densities, properties of Salmonella 304 may influence its interaction with horn fly larvae, enabling the bacteria to evade degradation during larval gut histolysis and to subsequently proliferate during the late stages of pupal development. This may account for the observed effect on adult emergence. The Salmonella strains were rarely cultured from newly emerged adults, indicating that transstadial carriage to the adult stage is inefficient.
Bacteria are essential for stable fly (Stomoxys calcitrans (L.)) larval survival and development, but little is known about the innate microbial communities of stable flies, and it is not known if their varied dietary substrates influence their gut microbial communities. This investigation utilized 454 sequencing of 16S and 18S amplicons to characterize and compare the bacterial and eukaryotic microbial communities in stable fly larvae and their developmental substrates. The microbial community of the third-instar stable fly larvae is unambiguously distinct from the microbial community of the supporting substrate, with bacterial communities from larvae reared on different substrates more similar to each other than to the communities from their individual supporting substrates. Bacterial genera that were more abundant proportionally in larvae compared to their substrates were Erysipelothrix, Dysgonomonas, Ignatzschineria (Gammaproteobacteria), and Campylobacter (Epsilonprotobacteria). The alphaproteobacteria Devosia, Brevundimonas, Sphingopyxix, and Paracoccus were more abundant proportionally in field substrates compared to their larvae. The main genera responsible for differences between the positive and negative field substrates were Dysgonomonas and Proteiniphilum. In contrast to Dysgonomonas, Proteiniphilum was more abundant in substrate than in the larvae. A large number of sequences were assigned to an unclassified protest of the superphylum Alveolata in larvae and their substrate. Microscopy validated these findings and a previously undescribed gregarine (phylum Apicomplexa, class Conoidasida) was identified in stable fly larvae and adults.
Deciphering mechanisms that regulate succession on ephemeral resources is critical for elucidating food web dynamics and nutrient recycling. Blow fly (Diptera: Calliphoridae) colonization and utilization of vertebrate carrion serve as a model for such studies, as they are the primary invertebrates that recycle this ephemeral resource. Initial colonization by blow flies often results in heightened attraction and colonization by competing conspecifics and heterospecifics, thereby regulating associated arthropod succession patterns. We examined the response of Cochliomyia macellaria (F.) and Chrysomya rufifacies (Macquart) to conspecific and heterospecific eggs. Because Ch. rufifacies is facultatively predacious and cannabalistic, we hypothesized that adults would recognize the presence of conspecific and heterospecific eggs, thus avoiding potential predation and competition. Using a Y-tube olfactometer, we measured the residence time response of C. macellaria and Ch. rufifacies to conspecific and heterospecific eggs of three different age classes (fresh to 9-h-old). Fly responses to surface-sterilized eggs and to an aqueous solution containing egg-associated microbes were then examined. High-throughput sequencing was used to survey egg-associated bacteria from both species. We report that C. macellaria and Ch. rufifacies exhibit differential responses to eggs of conspecifics and heterospecifics, which appear to be a result of microbial volatile-related odors. These behaviors likely influence predator–prey interactions between species. Preliminary high-throughput sequencing revealed Ch. rufifacies had a similar egg-associated fauna as C. macellaria, which may serve as a form of camouflage, allowing it to colonize and thereby attract C. macellaria, a common prey for its larvae.
Filth flies have been implicated in the dispersal of human disease pathogens; however, the epidemiological parameters of the transmission of human pathogens from flies to plants are largely undescribed. The capacity of the black blow fly, Phormia regina Meigen, to acquire and subsequently deposit bacteria onto baby lettuce leaves was compared with that of the house fly, Musca domestica (L.). Adult P. regina and M. domestica were exposed to green fluorescent protein-tagged Escherichia coli O157:H7- or Salmonella enterica-inoculated manure and then allowed access to the lettuce plants. Bacteria on the plants and flies were assessed by plating and polymerase chain reaction. Although blow flies acquired significantly more E. coli O157:H7 than house flies, there was no significant difference between the deposition of bacteria on lettuce by the two fly species. In contrast, there was no significant difference in the acquisition of S. enterica by the two fly species. However, blow flies deposited more S. enterica onto lettuce than house flies. To more accurately assess transmission parameters, flies were given timed exposure and inoculation periods of 10 and 30 s. Blow flies acquired more E. coli O157:H7 than S. enterica in the both time periods. Flies exposed to manure for 30 s were then tested for deposition by forcing the flies to walk on lettuce leaves. Blow flies deposited comparable amounts of E. coli O157:H7 and S. enterica. Although house flies have historically been implicated in the transmission of human pathogens to food, the data presented suggest that blow flies are more efficient vectors of E. coli O157:H7 and S. enterica to leafy greens than house flies.
Agricultural intensification has brought obvious increases in the extent and intensity of agricultural activities, which simultaneously led to rapid changes in landscape patterns. However, the relationship between agricultural intensification and pest damage was poorly known at the landscape scale, especially in China. We conducted an analysis to examine the relationship between agricultural intensification and pest damage of six pest species by using statistical data from1987 to 2012 in China. Results showed that high crop diversity could significantly suppress damage of oligophagous pests such as cereal aphids, rice stem borers, and corn borers while having no effects on polyphagous pests such as cotton bollworms and armyworms except for cotton aphids. Landscape simplification has no significant effects on pest damage except cotton bollworms, and there was no interaction between crop diversity and landscape simplification. Moreover, the relationship between crop diversity and crop yields per hectare was significantly negative. The canonical correspondence analysis ordination diagram showed that pest species responded to the crop species differently. These results suggest that crop diversity have potential for sustainable pest management with complete prevention of pest damage on crops, and it is environment friendly.
Landscape surroundings and local habitat management affect patterns of insect biodiversity. Knowing which landscape and local factors are more important for insect species diversity informs landscape and local scale land management, yet can be challenging to disentangle. We sought to identify 1) which landscape factors surrounding, and 2) which local habitat factors within urban community gardens influence patterns in lady beetle (Coccinellidae) abundance and species richness. We assessed lady beetle abundance and taxonomic diversity, garden habitat characteristics, and the surrounding landscape composition in 19 gardens over two consecutive years. We found that the amount of natural area surrounding gardens at 3 km was the strongest correlate of abundance and species richness. Specifically, gardens surrounded by less natural area (gardens embedded in more urban landscapes) had higher lady beetle abundance and richness. In gardens embedded in landscapes with more amounts of natural land, local habitat features such as ornamental abundance and crop diversity may become more important for maintaining lady beetle abundance and richness. Our results suggest that within more urban landscapes, lady beetles may aggregate and accumulate in relatively resource-rich habitats like gardens. Thus, urban landscape quality and local habitat management may all interact to shape lady beetle communities within gardens.
The genus Tervureniagen. nov. is designated as new and its single species T. eloumdenispec. nov. is described from western and central Africa (Afrotropical region). The genus is separable from its closely related genera by the simultaneous occurrence in males of pectinate antenna, extremely reduced, lobate hindwings, and the tuft of elongate scales on the tip of the abdomen. The systematic position of the new genus within the tribe Syntomini is discussed on the basis of morphological characters. A key for the identification of the genera of African Thyretina bearing a pointed abdominal tuft is also provided. Wing pattern and male genitalia of the new species are depicted and a hypothesis about the function of the pointed abdomen with elongated hair-like setae is discussed.
There are many descriptive statistical models describing the temperature-dependent developmental rates of insects without derivation of biophysical processes; thus, it is difficult to explain how temperature affects development from the thermodynamic mechanisms. Fortunately, two mathematical models (the Sharpe–Schoolfield–Ikemoto [SSI] model and Ratkowsky–Olley–Ross [ROR] model) based on thermodynamics have been built to explain temperature-dependent reaction rates. Despite their differences in construction, both models produce similar functions when used to describe the effect of temperature on the probability of a theoretical rate-controlling enzyme that is in its active state. However, the previous fitting method of the SSI model was unable to achieve global optimization of parameter estimates; that of the ROR model usually underestimates the maximal probability of the rate-controlling enzyme that is in its active state, as found in some empirical data sets. In the present study we improved the fitting methods for these two models. We then used these two models to fit 10 data sets from published references. We found the models based on the improved fitting methods agree with the empirical data well and predict that the maximal probabilities of the rate-controlling enzyme that is in its active state are close to 1. The SSI model produces a slightly better goodness-of-fit value for the model than the ROR model, whereas the latter predicts a more symmetrical curve for the probability of the rate-controlling enzyme that is in its active state. If thermodynamic parameters of two or more different species are to be compared, we recommend that researchers use one or the other of these two models and follow the same fitting methods for all species.
The lettuce aphid, Nasonovia ribisnigri (Mosley), is an economically important pest of lettuce worldwide. Recently, the entomopathogenic fungus, Beauveria bassiana strain GHA, and the aphelinid parasitoid, Aphelinus abdominalis Dalman, have been reported to be potential biological control candidates for use against N. ribisnigri. However, no information is available on the interaction between B. bassiana and A. abdominalis when both are applied. This study therefore examined the compatibility of B. bassiana and A. abdominalis in laboratory experiments. Specifically, we assessed the susceptibility of two A. abdominalis developmental stages (larvae and pupae) to two spore concentrations of B. bassiana (high: 1 × 109 and low: 1 × 104 conidia/ml) and a control of 0.01% Tween 80. We found parasitoid larvae to be highly susceptible to infection at the high spore concentration of B. bassiana, as measured by rates of mummy formation (mean ± SE: 14% ± 2.23) and adult emergence (mean ± SE: 10% ± 5.56) compared with the control treatment (mummification: mean ± SE: 79% ± 3.22; adult emergence: mean ± SE: 87% ± 4.40). In contrast, B. bassiana had no effects on parasitoid development when parasitoid larvae were treated with the lower spore concentration or parasitoid pupae were treated with either high or low spore concentrations. This study suggests that it might be possible to combine B. bassiana and A. abdominalis for integrated pest management of N. ribisnigri. As such, the application of B. bassiana should be timed to coincide with the presence of advanced developmental stages of A. abdominalis to protect the parasitoid. Another option would be to delay the release of A. abdominalis after B. bassiana application, when A. abdominalis is no longer susceptible to fungal infection.
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