Parasitoid-host interaction behaviors in relation to host stages in the Tamarixia triozae (Hymenoptera: Eulophidae)-Bactericera cockerelli (Hemiptera: Triozidae) system.

Females of host-feeding parasitic wasps often partition hosts of different stages for feeding and parasitization, but the underlying behavioral mechanisms are largely unknown, making it difficult to evaluate parasitoid-host interactions and their effects on biological control success. Tamarixia triozae (Burks) is an ectoparasitoid of tomato-potato psyllid Bactericera cockerelli (Sulc), which utilizes nymphs and kills them both by parasitization and host feeding. In this study, we exposed female wasps to 1st- to 5th-instar psyllid nymphs simultaneously and made 13-h continuous video recording of parasitoid-host interactions. We then quantified host stage-dependent handling time for feeding and oviposition and behaviors of parasitoid attacks and host defenses from encountering to successful feeding and oviposition. Female wasps were more likely to encounter and evaluate older hosts. However, the encounter and evaluation did not necessarily result in the success of feeding and oviposition. Our findings suggest that (i) T. triozae continues to assess the host using its ovipositor after the evaluation phase, (ii) females prefer the mid-aged hosts for feeding piercing and feeding and the later instars for oviposition probing and oviposition, (iii) the combination of stage-specific host nutrition value, integument thickness and defense behavior determines the success of feeding attacks, and (iv) the optimal host resource for parasitoid offspring fitness defines host stage selection for oviposition. This study contributes to our understanding of parasitoid-host interactions and mechanisms behind host stage selections.

Trypanosomatids Associated in the Alimentary Canal of Bagrada hilaris (Hemiptera: Pentatomidae).

Bagrada hilaris (Burmeister) is an invasive pest of economically important crops in the United States. During physiological investigations of B. hilaris, a flagellated protozoan was discovered in the alimentary canal of many specimens. This manuscript characterizes the morphology and molecular identification of the trypanosomatid, which appears similar to trypanosomatids identified in other stink bug species. It has been identified as a species in the Blastocrithidia genus based on morphological characteristics and molecular analyses.

Ovigeny strategy of the parasitic wasp Cosmocomoidea annulicornis (Hymenoptera: Mymaridae): effect of female age, feeding and host availability on reproductive traits.

The reproductive traits of the mymarid wasp Cosmocomoidea annulicornis (Ogloblin) (Hymenoptera: Mymaridae) attacking eggs of the sharpshooter Tapajosa rubromarginata (Signoret) (Hemiptera: Cicadellidae) were evaluated under laboratory conditions. Bioassays were carried out to estimate the realized fecundity and egg load of females. The ovigeny index was calculated and different biological traits, such as body size, oöcyte length, gaster length and wing length, were analysed to assess significant associations between these traits and the species fitness. In addition, the effect of host availability and feeding on longevity and potential fecundity throughout life and the effect of female age on egg maturation dynamics were assessed. The results showed that C. annulicornis is a strongly synovigenic species. A positive correlation was found between fecundity and longevity of the females and between body size and oöcyte length. Contrary to expected, body size was not related to fecundity and longevity. Females lived significantly longer in the presence of hosts and honey than when they were host-deprived and honey-fed or both host and honey deprived. Host availability had a significant effect on the amount of eggs laid by C. annulicornis females. Female age was negatively associated with oöcyte length. Furthermore, females were able to mature additional eggs as they aged, nevertheless, when host-deprived, senescent females presented significantly less mature eggs than younger ones, suggesting a possible egg oosorption. These results might contribute to a better understanding of the reproductive potential of this species as a biocontrol agent.

Parasitoid vectors a plant pathogen, potentially diminishing the benefits it confers as a biological control agent.

Huanglongbing (HLB) is a destructive disease of citrus primarily transmitted by the Asian citrus psyllid (ACP). Biocontrol of ACP is an environmentally sustainable alternative to chemicals. However, the risk of parasitoid rational application in ACP biocontrol has never been evaluated. Here we show, the dominant parasitoid of ACP, Tamarixia radiata, can acquire the HLB pathogen Candidatus Liberibacter asiaticus (CLas) and transmit it horizontally when probing ACP nymphs. If these ACP nymphs survive the probing, develop to adults and move to healthy plants, CLas can be transmitted to citrus leaves during feeding. We illustrate the formerly unrecognized risk that a parasitoid can potentially serve as a phoretic vector of the pathogen transmitted by its host, thus potentially diminishing some of the benefits it confers via biocontrol. Our findings present a significant caution to the strategy of using parasitoids in orchards with different infection status of insect-vectored pathogens.

The Anagyrus (Hymenoptera: Encyrtidae) parasitoids of the obscure mealybug Pseudococcus viburni (Hemiptera: Pseudococcidae) in Spain, with description of a new species.

The presence of three species of the genus Anagyrus Howard (Hymenoptera: Encyrtidae) parasitizing the obscure mealybug Pseudococcus viburni (Signoret) (Hemiptera: Pseudococcidae) in agricultural ecosystems of citrus, persimmon and ornamental plants from Eastern Spain is recorded. Anagyrus aligarhensis Agarwal Alam is recorded for the first time as parasitoid on this mealybug. Anagyrus fusciventris (Girault) is a new record for Spain. Anagyrus borrianensis sp. nov., reared as a specific primary parasitoid of this mealybug, is described and illustrated. The joint presence of Anagyrus pseudococci (Girault) and Anagyrus vladimiri Triapitsyn on citrus crops is confirmed. A key to species of Anagyrus parasitoids of Planococcus and Pseudococcus mealybugs in Eastern Spain is provided.

Integrative Techniques Confirms the Presence of Bemisia tabaci Parasitoids: Encarsia formosa, Encarsia porteri and Eretmocerus mundus (Hymenoptera: Aphelinidae) on Soybean and Tomatoes in South Brazil.

Parasitoid wasps from the Aphelinidae family (Hymenoptera) are important control agents of Bemisia tabaci (Gennadius, 1889) cryptic species, both through reproduction and feeding processes. Identifying native parasitoid species within agricultural systems affected by Bemisia whitefly species is the first step to developing guidelines for the creation and release of biological control agents aiming at this highly damaging pest species complex. Taxonomic and phylogenetic analyses based on morphological and molecular characters, respectively, confirmed the occurrence of Encarsia formosa (Gahan, 1924) in greenhouse tomatoes from Santa Maria, Encarsia porteri (Mercet, 1928) in open-field soybean from Santa Maria, and Eretmocerus mundus Mercet, 1931 in greenhouse tomatoes from São José do Hortêncio, all within Rio Grande do Sul state (South Brazil). This is the first report of En. formosa, En. porteri and Er. mundus parasitising B. tabaci in South Brazil, and the first En. porteri partial mtCOI gene sequence being reported and characterised. The high temperature inside the tomato greenhouses can be a possible cause for the predominance of Er. mundus in São José do Hortêncio, and sex ratios in the surveyed populations point to female and male prevalence within Encarsia and Eretmocerus genera, respectively. The combined use of taxonomic and molecular characterisation highlights the importance of combining both morphological and molecular approaches in the assessment of previously unidentified whitefly parasitoids.

Courtship, Mating Behavior, and Ovary Histology of the Nymph Parasitoid Psyllaephagus bliteus (Hymenoptera: Encyrtidae).

The potential of the parasitoid Psyllaephagus bliteus Riek for the biological control of the eucalyptus pest Glycaspis brimblecombei Moore (Hemiptera: Aphalaridae) nymphs is high. This research sought to analyze the courtship, male competition, and mating behavior of P. bliteus at the proportions of 1:1 and 2:1 males to female in a Petri dish (5 cm diameter), and to describe the ovary histology of virgin and mated females of this parasitoid. At 1:1, males touch the antennae and thorax-abdomen of females during courtship, but females avoid mate attempts before they are 48 h old. At 2:1, the competition between male parasitoids inhibits mating. The histology of ovaries of virgin and mated P. bliteus females is similar, with two well-defined germarium and vitellarium regions, with oocytes at different developmental stages, including mature ones rich in yolk and with eggshell. A clearer understanding of the reproductive behavior and histology of P. bliteus aids in the use of this parasitoid for the biological control of G. brimblecombei.

Contrasting drivers of diversity in hosts and parasites across the tropical Andes.

Geographic turnover in community composition is created and maintained by eco-evolutionary forces that limit the ranges of species. One such force may be antagonistic interactions among hosts and parasites, but its general importance is unknown. Understanding the processes that underpin turnover requires distinguishing the contributions of key abiotic and biotic drivers over a range of spatial and temporal scales. Here, we address these challenges using flexible, nonlinear models to identify the factors that underlie richness (alpha diversity) and turnover (beta diversity) patterns of interacting host and parasite communities in a global biodiversity hot spot. We sampled 18 communities in the Peruvian Andes, encompassing ∼1,350 bird species and ∼400 hemosporidian parasite lineages, and spanning broad ranges of elevation, climate, primary productivity, and species richness. Turnover in both parasite and host communities was most strongly predicted by variation in precipitation, but secondary predictors differed between parasites and hosts, and between contemporary and phylogenetic timescales. Host communities shaped parasite diversity patterns, but there was little evidence for reciprocal effects. The results for parasite communities contradicted the prevailing view that biotic interactions filter communities at local scales while environmental filtering and dispersal barriers shape regional communities. Rather, subtle differences in precipitation had strong, fine-scale effects on parasite turnover while host-community effects only manifested at broad scales. We used these models to map bird and parasite turnover onto the ecological gradients of the Andean landscape, illustrating beta-diversity hot spots and their mechanistic underpinnings.

Parasitoids (Hymenoptera) of Mealybug Pests (Hemiptera: Pseudococcidae) from Southern Brazil: Molecular and Morphological Characterization.

Parasitoids of three mealybug pests (Hemiptera: Pseudococcidae), Planococcus ficus (Signoret), Pseudococcus sociabilis Hambleton, and Pseudococcus viburni (Signoret) have been identified for the first time in Brazil. Mealybugs were collected in fruit-growing areas along southern Brazil during 2013-2016. An integrative approach, combining morphological and molecular methods, was used to identify the Brazilian parasitoids to the species level. Fifteen species were recorded, including 14 primary parasitoids belonging to Encyrtidae and Platygastridae and a single secondary parasitoid species belonging to Signiphoridae. The encyrtid parasitoids Acerophagus flavidulus (Brèthes), Anagyrus calyxtoi Noyes and Zaplatycerus sp., and the signiphorid secondary parasitoid Chartocerus axillaris De Santis are reported for the first time in Brazil.

Determining the Minimum Temperature for Storage of Tamarixia radiata (Hymenoptera: Eulophidae) Adults for Biological Control of Asian Citrus Psyllid.

In order to control the spread of the huanglongbing (HLB) disease in citrus plants, one of the main approaches is management of its vector, the Asian citrus psyllid, Diaphorina citri Kuwayama. The intensive use of chemicals to control the psyllid has caused concern due to the damage to the environment and human health, and biological control has been a more sustainable and environmentally safe strategy. For D. citri, the parasitoid wasp Tamarixia radiata Waterston has been used successfully in the state of São Paulo, Brazil, reducing populations of D. citri nymphs by up 80% in some municipalities. Mass rearing of wasps is required to provide efficient control, which implies that quality control is required, especially in storage and transportation. In most cases, the insects are not used on the same day of emergence, which makes it necessary to develop strategies to delay development without negatively affecting the wasps. Here, we evaluated the survival of T. radiata adults over eight different exposure times (2, 4, 6, 8, 10, 12, 14, and 16 days) in three different temperatures (7, 9, and 11°C). After these periods, they were transferred to climate chambers at 25°C and their survival curves over 30 days were analyzed. We concluded that adults can be maintained at 9°C for up to 6 days without significant damage to their survival during and after the exposure period, functioning well for D. citri IPM implementation.

The Role of Trialeurodes vaporariorum-Infested Tomato Plant Volatiles in the Attraction of Encarsia formosa (Hymenoptera: Aphelinidae).

Natural enemies locate their herbivorous host and prey through kairomones emitted by host plants and herbivores. These kairomones could be exploited to attract and retain natural enemies in crop fields for insect pest control. The parasitoid Encarsia formosa preferentially parasitises its whitefly host, Trialeurodes vaporariorum, a major pest of tomato Solanum lycopersicum, thus offering an effective way to improve whitefly control. However, little is known about the chemical interactions that occur in E. formosa-T. vaporariorum-S. lycopersicum tritrophic system. Using behavioural assays and chemical analyses, we investigated the kairomones mediating attraction of the parasitoid to host-infested tomato plants. In Y-tube olfactometer bioassays, unlike volatiles of healthy tomato plants, those of T. vaporariorum-infested tomato plants attracted E. formosa, and this response varied with host infestation density. Coupled gas chromatography/mass spectrometric analyses revealed that host infestation densities induced varying qualitative and quantitative differences in volatile compositions between healthy and T. vaporariorum adult-infested tomato plants. Bioassays using synthetic chemicals revealed the attractiveness of 3-carene, ß-ocimene, ß-myrcene and α-phellandrene to the parasitoid, and the blend of the four compounds elicited the greatest attraction. Our results suggest that these terpenes could be used as an attractant lure to recruit the parasitoid E. formosa for the control of whiteflies in tomato crop fields.

Bioecology of Anagyrus saccharicola (Hymenoptera: Encyrtidae), a parasitoid of the pink sugarcane mealybug Saccharicoccus sacchari (Hemiptera: Pseudococcidae).

Parasitoids can be used as biological agents of pest control. Anagyrus saccharicola Timberlake (Hymenoptera: Encyrtidae) is a parasitoid of the pink sugarcane mealybug Saccharicoccus sacchari (Cockerell) (Hemiptera: Pseudococcidae). Although this mealybug is present in all sugarcane-producing countries, there is limited information regarding this pest and its parasitoid. Aiming to elucidate information on bioecological parameters of A. saccharicola, were evaluated the survival of parasitoid females and males at three temperatures, the host preference of the parasitoid, and the fecundity and longevity of the host. In addition, the parasitism rate of A. saccharicola was estimated based on three factors, feeding, mating, and time. Survival was evaluated at 20, 25, and 30°C. Host preference was conducted on 15-, 20-, and 30-day-old mealybugs. And the parasitism rate was evaluated in fed and unfed, mated and unmated parasitoids and with 24 h and newly emerged. The temperature of 20°C was the most favorable for parasitoid survival. Parasitism occurred at all evaluated ages of the mealybug; however, the preference was for those that were 30-days-old. The parasitized mealybugs longevity was approximately 8 additional days after parasitization, and non-parasitized mealybugs lived for an additional 20 days for mealybugs aged 30 and 20 days at the outset of the tests, and a further 13 days for the 15 days. Feeding and mating after 24 h of emergence resulted in a higher parasitism rate. These findings can contribute to more efficient rearing of A. saccharicola and in the planning of the biological control of S. sacchari in the integrated pest management programs.

Culture-free genome-wide locus sequence typing (GLST) provides new perspectives on Trypanosoma cruzi dispersal and infection complexity.

Analysis of genetic polymorphism is a powerful tool for epidemiological surveillance and research. Powerful inference from pathogen genetic variation, however, is often restrained by limited access to representative target DNA, especially in the study of obligate parasitic species for which ex vivo culture is resource-intensive or bias-prone. Modern sequence capture methods enable pathogen genetic variation to be analyzed directly from host/vector material but are often too complex and expensive for resource-poor settings where infectious diseases prevail. This study proposes a simple, cost-effective 'genome-wide locus sequence typing' (GLST) tool based on massive parallel amplification of information hotspots throughout the target pathogen genome. The multiplexed polymerase chain reaction amplifies hundreds of different, user-defined genetic targets in a single reaction tube, and subsequent agarose gel-based clean-up and barcoding completes library preparation at under 4 USD per sample. Our study generates a flexible GLST primer panel design workflow for Trypanosoma cruzi, the parasitic agent of Chagas disease. We successfully apply our 203-target GLST panel to direct, culture-free metagenomic extracts from triatomine vectors containing a minimum of 3.69 pg/µl T. cruzi DNA and further elaborate on method performance by sequencing GLST libraries from T. cruzi reference clones representing discrete typing units (DTUs) TcI, TcIII, TcIV, TcV and TcVI. The 780 SNP sites we identify in the sample set repeatably distinguish parasites infecting sympatric vectors and detect correlations between genetic and geographic distances at regional (< 150 km) as well as continental scales. The markers also clearly separate TcI, TcIII, TcIV and TcV + TcVI and appear to distinguish multiclonal infections within TcI. We discuss the advantages, limitations and prospects of our method across a spectrum of epidemiological research.

Caterpillar-induced rice volatiles provide enemy-free space for the offspring of the brown planthopper.

Plants typically release large quantities of volatiles in response to herbivory by insects. This benefits the plants by, for instance, attracting the natural enemies of the herbivores. We show that the brown planthopper (BPH) has cleverly turned this around by exploiting herbivore-induced plant volatiles (HIPVs) that provide safe havens for its offspring. BPH females preferentially oviposit on rice plants already infested by the rice striped stem borer (SSB), which are avoided by the egg parasitoid Anagrus nilaparvatae, the most important natural enemy of BPH. Using synthetic versions of volatiles identified from plants infested by BPH and/or SSB, we demonstrate the role of HIPVs in these interactions. Moreover, greenhouse and field cage experiments confirm the adaptiveness of the BPH oviposition strategy, resulting in 80% lower parasitism rates of its eggs. Besides revealing a novel exploitation of HIPVs, these findings may lead to novel control strategies against an exceedingly important rice pest.

Unsung heroes: fixing multifaceted sustainability challenges through insect biological control.

Insects are indispensable actors within global agri-food systems and ensure the delivery of myriad ecosystem services. A progressive decline in insect numbers - as inflicted by habitat loss, pollution or intensive agriculture - can jeopardize a sustained provisioning of those services. Though we routinely disregard how insects help meet multiple sustainable development challenges, a gradual insect decline can have grave, long-lasting consequences. Here, we describe how insect-mediated biological control not only defuses invasive pests and can reconstitute crop productivity, but equally delivers other positive social-ecological outcomes. Drawing upon the pan-tropical invasion of the cassava mealybug and its ensuing suppression by the monophagous parasitoid Anagyrus lopezi, we illuminate how biological control contributes to food security, poverty alleviation, human wellbeing and environmental preservation. Trans-disciplinary research and 'systems thinking' are needed to maximize the potential of these biodiversity-driven interventions, and thus reap the net positive spin-offs insects provide for farmers, the environment and human society.

Biological characteristics of Trissolcus urichi (Crawford) (Hymenoptera: Scelionidae) on Euschistus heros (Fabricius) and Dichelops melacanthus (Dallas) (Hemiptera: Pentatomidae) Eggs.

Species of the genus Trissolcus are effective as egg parasitoids of Euschistus heros and can potentially be used in a multispecies pest management approach. However, in order to successfully use those biocontrol agents in the field, previous detailed knowledge about their life history are necessary. Therefore, we evaluate some biological characteristics of Trissolcus urichi on Euschistus heros and Dichelops melacanthus eggs. Three independent experiments were performed: (1) T. urichi host preference between E. heros and D. melacanthus eggs. (2) T. urichi eggs-adult period (days), number of parasitized eggs in 24 h, emergence rate (%) and sex ratio of the parasitoid in E. heros and D. melacanthus eggs. (3) Morphometric characteristics of T. urichi grown on E. heros and D. melacanthus eggs. Trissolcus urichi preferred to parasitize E. heros eggs, exhibiting a higher number of parasitized eggs, higher rate of emergence (%) and faster development, as well as producing progeny of larger size than the parasitoids emerged from eggs of D. melacanthus in relation to body length, wing length and width. Thus, it can be concluded that T. urichi had better performance on E. heros eggs, although the parasitoid had also acceptable parasitism capacity and development in D. melacanthus eggs.

New species of Laboulbenia (Laboulbeniales, Ascomycota) on Gerridae (Hemiptera, Insecta), a new host family.

Four new species of Laboulbenia (Laboulbeniales, Ascomycota) occurring on Gerridae (Hemiptera, Insecta), a new host family, are described from six Central and South American countries: Bolivia, Brazil, Ecuador, Panama, Peru, and Venezuela. The new species are Laboulbenia brachymetrae, L. cylindrostethi, L. neogerris, and L. tachygerris.