Major Host Research Articles

Review and Comparative Assessment of Biacetabulum macrocephalum McCrae, 1962 (Cestoda: Caryophyllidae) from Catostomus commersoni (Lacépède) in Wisconsin, USA

Specimens of Biacetabulum macrocephalum McCrae, 1962 (Cestoda: Caryophyllidae) were first described from the white sucker, Catostomus commersoni (Lacépède) in Colorado. The white sucker appears to be its major host species in a few other states often in the Mississippi River basin. We have collected and examined this uncommon cestode, also from C. commersoni in Tichigan Lake, a tributary of the Mississippi River and from the Root River in SE Wisconsin. We update our first and only 1986 account of our Wisconsin population, with new observations and measurements, and compare with those in the original and other descriptions. The morphology of B. macrocephalum is revisited using light microscopy revealing new features. Emphasis is placed on the morphological variability of its scolex and reproductive structures especially its ovarian arms and pre- and post-ovarian vitellaria. Measurements of 10 specimens from the Root River provided an opportunity to review the taxonomy and description of the species, distinguish locality differences, and correct and update other statements and concepts by other observers. The disconnected distribution of worms from the same host species in separate waters of various states is described.

Field Infestation and Seasonality Range of Bactrocera dorsalis (Hendle) in Major Host Mango Cultivars of Sindh, Pakistan

Field Infestation and Seasonality Range of Bactrocera dorsalis (Hendle) in Major Host Mango Cultivars of Sindh, Pakistan

FIRST RECORD OF HOYA MELIFLUA (BLANCO) MERR. (APOCYNACEAE, ASCLEPIADOIDEAE) IN THE NATURAL ECOSYSTEMS OF BATANGAS IN LUZON ISLAND, PHILIPPINES, WITH NOTES ON ASSOCIATED FLORA

The Philippine islands host a significantly high concentration of native and endemic Hoya species. However, there are no previous records of this genus in the natural ecosystems within the province of Batangas, Luzon Island. The present study pioneered the exploration of Hoya plants and their associated communities in Batangas. A route-walk method was employed within the forests of Lobo, Batangas, to document Hoya species. Morphological characteristics, habitat, host plants, substrates, and associated flora were also recorded. Only one species was identified, Hoya meliflua (Blanco) Merr., with material deposited in the Batangas State University – The National Engineering University Lobo Campus Herbarium (Reg. #: Pasado 001). The morphology and other plant references and databases confirmed its identity. The study found that the individuals of H. meliflua in Lobo inhabit the secondary riverine forests along ecotourism sites, with Schizostachyum textorium (Blanco) Merr., Ficus balete Merr., Tectona philippinensis Benth. & Hook.f. ex Merr. and Pterospermum diversifolium Blume as the major host plants. The assessment of the associated flora revealed 46 species, of which 100% were natives, 13% were Philippine endemics, and 14% were threatened nationally and internationally. The conservation of H. meliflua in Batangas can be improved by mainstreaming its importance as an ornamental plant and a key biodiversity species within ecotourism sites. Further studies can help in revealing the presence of other Hoya spp. on the island.

In vitro Methodology to Assess Quantitative Resistance in Plant-fungus Pathosystems

Background: Quantitative resistance (QR) to fungal pathogens remains a primary focus of all major host breeding programs. Field screenings for resistant plants, although accurate and effective, demand significant time and a sizable workforce to accomplish. Moreover, weather conditions in the field may not always be favorable for uniform disease spread, which eventually may lead to the failure of the overall experiment. The development of a more efficient and reliable bioassay to screen for resistance to fungal pathogens would be advantageous for any breeding program working on disease resistance; however, only if it correlates with field screening trials. Objective: The objective of this review is to combine novel findings related to rapid screening methods to evaluate QR, which are needed to accelerate the progress in developing fungal disease resistance in cultivars. Insights into the in vitro quantitative components of the host-pathogen interaction, factors affecting in vitro evaluation in young plant materials, as well as molecular pathways for the association between the in vitro and adult plant responses to fungal infection are also reviewed. Conclusion: An in vitro method was found to be efficient and successful in terms of inoculum volume, plant samples, and working space. The main advantage of this method is its predictive ability for adult plant disease. In addition, it provides reproducible results and is found to be a simple and reliable method. The in vitro assay allows rapid and early determination of resistance/susceptibility to fungal pathogens, which can be incorporated into a breeding program for identifying resistant plants.

Fluvial Deposition and Land Use Change Control Selenium Occurrence in Mollisols of Cold Region Agroecosystems.

Mollisols support the most productive agroecosystems in the world. Despite their critical links to food quality and human health, the varying distributions of selenium (Se) species and factors governing Se mobility in the mollisol vadose zone remain elusive. This research reveals that, in northern mollisol agroecosystems, Se hotspots (≥0.32 mg/kg) prevail along the regional river systems draining the Lesser Khingan Mountains, where piedmont Se-rich oil shales are the most probable source of regional Se. While selenate and selenite dominate Se species in the water-soluble and absorbed pools, mollisol organic matter is the major host for Se. Poorly crystalline and crystalline Fe oxides are subordinate in Se retention, hosting inorganic and organic Se at levels comparable to those in the adsorbed pool. The depth-dependent distributions of mollisol Se species for the non-cropland and cropland sites imply a predominance of reduced forms of Se under the mildly acidic and reducing conditions that, in turn, are variably impacted by agricultural land use. These findings therefore highlight that fluvial deposition and land use change together are the main drivers of the spatial variability and speciation of mollisol Se.

When Do States Repatriate Refugees? Evidence from the Middle East

AbstractWhich conditions affect whether a state will choose to repatriate forcibly displaced populations residing within its borders? One of the most pressing issues related to the protracted Syrian refugee situation concerns the future of over 5 million Syrians who sought shelter in neighboring states. With host countries pursuing disparate strategies on Syrians’ return, the existing literature has yet to provide a framework that is able to account for variation on host states’ policies toward refugee repatriation. In this paper, we expand upon the concept of the refugee rentier state to theorize inductively upon the conditions shaping states’ policymaking on repatriation. We draw upon multi-sited fieldwork across the three major refugee host states in the Eastern Mediterranean (Jordan, Lebanon, and Turkey) to establish that a refugee rentier state's strategy is driven by domestic political economy costs related to the hosting of refugee populations as well as its geostrategic interests vis-à-vis these refugees’ country of origin. Using a comparative case study approach, we note how a state is more likely to pursue a blackmailing strategy based on threats if it faces high domestic political economy costs and adopts an interventionist policy vis-à-vis the sending state, as in the case of Turkey. Otherwise, it is more likely to pursue a backscratching strategy based on bargains, as in the case of Lebanon and Jordan. We conclude with a discussion on how this framework sheds light on refugee host states’ repatriation policies on a global scale.

Modeling of historical and current distributions of lone star tick, Amblyomma americanum (Acari: Ixodidae), is consistent with ancestral range recovery.

The lone star tick, Amblyomma americanum L., is a three-host hard tick notorious for aggressive feeding behavior. In the early to mid-20th century, this species' range was mostly limited to the southern USA. Since the 1950s, A. americanum has been detected in many new localities in the western, northcentral, and northeastern regions of the country. To examine the influence of climate on this apparent expansion, we used historical (1748-1950) lone star locations from the literature and museum records to model areas suitable for this species based on past environmental conditions in the late 1800s - early 1900s. We then projected this model forward using present (2011-2020) climatic conditions and compared the two for evidence of climate-associated distributional shifts. A maximum entropy distribution or Maxent model was generated by using a priori selected climatic variables including temperature, precipitation, and vapor pressure deficit. Temperature and vapor pressure deficit were selected as the most important factors in creating a sensitive and specific model (success rate = 82.6 ± 6.1%) that had a good fit to the existing data and was significantly better than a random model [partial ROC (receiver operating characteristic) to AUC (area under the ROC curve) ratio = 1.97 ± 0.07, P < 0.001]. The present projected model was tested with an independent dataset of curated museum records (1952-2020) and found to be 95.6% accurate. Comparison of past and present models revealed > 98% A. americanum niche overlap. The model suggests that some areas along the western fringe are becoming less suitable for A. americanum, whereas areas in some Great Lakes and coastal northeastern regions are becoming more suitable, results that are compatible with possible effects of climate change. However, these changes are minor, and overall climate in North America does not appear to have changed in ways significant to A. americanum's distribution. These findings are consistent with an alternative hypothesis that recent changes in A. americanum's distribution are a result of this species re-occupying its historical range, driven predominantly by factors other than climate, such as shifts in land use and population densities of major hosts.

Where have all the grouse ticks gone? Apparent decline in collections of Haemaphysalis chordeilis Packard.

Haemaphysalis chordeilis Packard, also known as the grouse or bird tick, is a three-host tick native to North America. Literature from the early 20th century reported a widespread distribution of this tick across the US and Canada. As its name implies, ground-dwelling birds such as grouse and quail were frequent hosts, and occasionally large infestations were reported in domestic flocks making it a pest of economic importance. However, after the mid-1900's records of this species appear scarce, and a number of more recent studies of ticks on birds (including ostensibly favored host species) did not detect it. To confirm this perception with data, we conducted a literature search for collection records of this species and compared the records across two eras (pre-1965 and post-1965), finding very few records of H. chordeilis in recent years, despite increased attention brought to this genus by the detection of exotic Haemaphysalis longicornis Neumann populations in the eastern US. We also compiled a list of studies after 1965 that examined appropriate hosts for ectoparasites but failed to find H. chordeilis. We interpret the apparent decline of ticks in the context of documented population declines in several major host species over the same time frame and discuss whether ectoparasite populations should be subject to the same conservation consideration as their hosts.

Horizontal Transfer and Evolutionary Profiles of Two Tc1/DD34E Transposons (ZB and SB) in Vertebrates.

Both ZeBrafish (ZB), a recently identified DNA transposon in the zebrafish genome, and SB, a reconstructed transposon originally discovered in several fish species, are known to exhibit high transposition activity in vertebrate cells. Although a similar structural organization was observed for ZB and SB transposons, the evolutionary profiles of their homologs in various species remain unknown. In the present study, we compared their taxonomic ranges, structural arrangements, sequence identities, evolution dynamics, and horizontal transfer occurrences in vertebrates. In total, 629 ZB and 366 SB homologs were obtained and classified into four distinct clades, named ZB, ZB-like, SB, and SB-like. They displayed narrow taxonomic distributions in eukaryotes, and were mostly found in vertebrates, Actinopterygii in particular tended to be the major reservoir hosts of these transposons. Similar structural features and high sequence identities were observed for transposons and transposase, notably homologous to the SB and ZB elements. The genomic sequences that flank the ZB and SB transposons in the genomes revealed highly conserved integration profiles with strong preferential integration into AT repeats. Both SB and ZB transposons experienced horizontal transfer (HT) events, which were most common in Actinopterygii. Our current study helps to increase our understanding of the evolutionary properties and histories of SB and ZB transposon families in animals.

Artificial induction of chromosome aneuploidy in CHO cells alters their function as host cells.

Chinese hamster ovary (CHO) cells are major host cells for biopharmaceuticals. During culture, the chromosome number of CHO cells alters spontaneously. Here, we investigated the effects of artificial changes in the chromosome number on productivity. When cell fusion between antibody-producing CHO-K1-derived cells was induced, we observed a wide range of aneuploidy that was not detected in controls. In particular, antibody productivities were high in clone-derived cell populations that retained a diverse chromosome number distribution. We also induced aneuploid cells using 3-aminobenzamide that causes chromosome non-disjunction. After induction of aneuploidy by 3-aminobenzamide, cells with an increased chromosome number were isolated, but cells with a decreased chromosome number could not be isolated. When antibody expression vectors were introduced into these isolated clones, productivity tended to increase in cells with an increased chromosome number. Further analysis was carried out by focusing on clone 5E8 with an average chromosome number of 37. When 5E8 cells were used as host, the productivity of multiple antibodies, including difficult-to-express antibodies, was improved compared with CHO-K1 cells. The copies of exogenous genes integrated into the genome were significantly increased in 5E8 cells. These findings expand the possibilities for host cell selection and contribute to the efficient construction of cell lines for recombinant protein production.

Deployment of a Reservoir-Targeted Vaccine Against Borrelia burgdorferi Reduces the Prevalence of Babesia microti Coinfection in Ixodes scapularis Ticks.

In the Northeast and upper Midwest of the United States, Babesia microti and Borrelia burgdorferi use Ixodes scapularis ticks as vector and Peromyscus leucopus mice as major reservoir host. We previously established, in a 5-year field trial, that a reservoir-targeted outer surface protein A vaccine reduces the prevalence of B. burgdorferi-infected ticks. We accessed ticks and mouse blood samples collected during the trial, extracted total DNA, and amplified the B. microti 18S rRNA gene. Vaccine deployment reduced the prevalence of ticks coinfected with B. microti and that of mice infected with B. microti. Breaking the enzootic cycle of B. burgdorferi may reduce the incidence of babesiosis.

Superhydrous aluminous silica phases as major water hosts in high-temperature lower mantle

Water transported by subducted oceanic plates changes mineral and rock properties at high pressures and temperatures, affecting the dynamics and evolution of the Earth's interior. Although geochemical observations imply that water should be stored in the lower mantle, the limited amounts of water incorporation in pyrolitic lower-mantle minerals suggest that water in the lower mantle may be stored in the basaltic fragments of subducted slabs. Here, we performed multianvil experiments to investigate the stability and water solubility of aluminous stishovite and CaCl2-structured silica, referred to as poststishovite, in the SiO2-Al2O3-H2O systems at 24 to 28 GPa and 1,000 to 2,000 °C, representing the pressure-temperature conditions of cold subducting slabs to hot upwelling plumes in the top lower mantle. The results indicate that both alumina and water contents in these silica minerals increase with increasing temperature under hydrous conditions due to the strong Al3+-H+ charge coupling substitution, resulting in the storage of water up to 1.1 wt %. The increase of water solubility in these hydrous aluminous silica phases at high temperatures is opposite of that of other nominally anhydrous minerals and of the stability of the hydrous minerals. This feature prevents the releasing of water from the subducting slabs and enhances the transport water into the deep lower mantle, allowing significant amounts of water storage in the high-temperature lower mantle and circulating water between the upper mantle and the lower mantle through subduction and plume upwelling. The shallower depths of midmantle seismic scatterers than expected from the pure SiO2 stishovite-poststishovite transition pressure support this scenario.

Phylogeography and Biological Characterizations of H12 Influenza A Viruses.

Influenza A virus (IAV) is widespread in wild bird reservoirs. Sixteen hemagglutinin subtypes are associated with wild waterfowl hosts; some subtypes are isolated infrequently, one of which is H12 IAV. In this study, we detected three H12 IAVs from Anas crecca and Anas formosa in Poyang Lake, China, in 2018, one of which was isolated. Phylogenetic analysis revealed that the genome sequences of the three H12 viruses belonged to the Eurasian lineage, except for PA genes and one NP gene, which belonged to the North American lineage. The growth kinetics showed that the H12 isolate grew better in A549 than MDCK cells. Moreover, although the H12 isolate cannot efficiently replicate in BALB/c mice, it can bind to both α-2,6 sialic acid (SA) and α-2,SA-linked receptors. In addition, we examined the phylodynamics of H12 viruses by Bayesian phylogeographic analysis. The results show that two major transmission routes of H12 IAVs were from Asia to Oceania and from Europe to South America, and Anas and Arenaria genera were the major hosts of the viral transmission. Our findings help us better understand the evolution of H12 IAV and highlight the need for the continued surveillance of IAVs circulating in wild birds.

Animal Models of Trypanosoma cruzi Congenital Transmission.

Chagas disease, initiated by the etiological agent Trypanosoma cruzi, is an endemic infection in the American continent. Although vectorial transmission of T. cruzi is recognized as the main mode of infection, other routes such as congenital and blood transfusion are also documented as important methods of transmission. T. cruzi maternal–fetal transmission has been recorded in humans and examined by some investigators in naturally and experimentally infected mammals. Dogs are recognized as the major reservoir host in maintaining the domestic transmission of T. cruzi; however, the importance of congenital transmission in preserving the infection cycle in dogs has not been studied in detail. In this article, we reviewed the current knowledge of congenital transmission of T. cruzi in humans and compared the placental architecture of humans and different animals with particular attention to rodents, dogs, and non-human primates that have been used as experimental models of T. cruzi infection, congenital transmission, and Chagas disease pathogenesis. The placentas of humans and animals have some similar and dissimilar characteristics that should inform the study design and interpretation of results when evaluating the efficacy of new anti-parasite drugs and therapies against congenital infection.

Non-targeted metabonomics and transcriptomics revealed the mechanism of mulberry branch extracts promoting the growth of Sanghuangporus vaninii mycelium.

Sanghuangprous vaninii is a wood-inhabiting fungus, and its mycelium and fruiting body show excellent medicinal values. Mulberry is one of the major hosts of S. vaninii, however, the mechanism of mulberry affecting the growth of S. vaninii has not been reported. In the present study, a mulberry-inhabiting strain of S. vaninii was selected to explore the effects of mulberry branch extracts (MBE) on the growth of the strain. Results showed that MBE could significantly promote the growth of S. vaninii mycelium at the concentration of 0.2 g/l. After 16 days of liquid culture, the dry weight of mycelium in 0.2 g/l MBE medium was higher by three times compared with that in the control. The non-targeted metabonomic analysis of the culture medium at different culture times and concentrations was conducted to find the key components in MBE that promoted the growth of S. vaninii mycelium. Under the different concentrations of MBE culture for 10 and 16 days, 22 shared differential metabolites were identified. Next, in accordance with the peak value trend of these metabolites, HPLC–MS and liquid culture validation, four components derived from MBE (i.e., scopoletin, kynurenic acid, 3,5-dihydroxybenzoic acid and 2,4-dihydroxybenzoic acid) could significantly increase the growth rate of mycelium at the concentration of 2 mg/l. Transcriptomic and qRT-PCR analyzes showed that MBE could upregulate hydrolase-related genes, such as serine–glycine–asparaginate–histidine (SGNH) hydrolase, alpha-amylase, poly-beta-hydroxybutyrate (PHB) depolymerase, glycosyl hydrolase family 61, cerato-platanin protein and Fet3, which might enhance the nutrient absorption ability of S. vaninii. Importantly, MBE could significantly increase the content of harmine, androstenedione and vesamicol, which have been reported to possess various medicinal effects. Results suggested that MBE could be an excellent additive for liquid culture of S. vaninii mycelium, and these hydrolase-related genes also provided candidate genes for improving the nutrient absorption capacity of S. vaninii.

Selective IgA Deficiency in Spontaneously Hypertensive Rats With Gut Dysbiosis.

The spontaneously hypertensive rat (SHR) is extensively used to study hypertension. Gut microbiota dysbiosis is a notable feature in SHR for reasons unknown. Immunoglobulin A (IgA) is a major host factor required for gut microbiota homeostasis. We hypothesized that inadequate IgA contributes to gut microbiota dysbiosis in SHR. IgA was measured in feces, cecum, serum, liver, gut-associated lymphoid tissue, and milk from SHR and Wistar Kyoto rats. IgA regulatory factors like IgM, IgG, and pIgR (polymeric immunoglobulin receptor) were analyzed. IgA and IgG antibodies and blood pressure (BP) were measured before and after administrating a bacterial antigen (ie, flagellin). Compared with Wistar Kyoto rats, SHR displayed remarkably near-deficient IgA levels accompanied by compensatory increases in serum IgM and IgG and gut-liver pIgR expression. Inadequate milk IgA in SHR emphasized this immune defect stemmed from the neonatal stage. Reduced IgA+ B cells in circulation and Peyer patches indicated a possible reason for the lower IgA in SHR. Noteworthy, a genetic insufficiency was unlikely because administering flagellin to SHR induced anti-flagellin IgA antibodies. This immune response surprisingly accelerated hypertension development in SHR, suggesting IgA quiescence may help maintain lower BP. This study is the first to reveal IgA deficiency in SHR as one host factor associated with gut microbiota dysbiosis and invigorates future research to determine the pathophysiological role of IgA in hypertension.

A manually curated compendium of expression profiles for the microbial cell factory Corynebacterium glutamicum

Corynebacterium glutamicum is the major host for the industrial production of amino acids and has become one of the best studied model organisms in microbial biotechnology. Rational strain construction has led to an improvement of producer strains and to a variety of novel producer strains with a broad substrate and product spectrum. A key factor for the success of these approaches is detailed knowledge of transcriptional regulation in C. glutamicum. Here, we present a large compendium of 927 manually curated microarray-based transcriptional profiles for wild-type and engineered strains detecting genome-wide expression changes of the 3,047 annotated genes in response to various environmental conditions or in response to genetic modifications. The replicates within the 927 experiments were combined to 304 microarray sets ordered into six categories that were used for differential gene expression analysis. Hierarchical clustering confirmed that no outliers were present in the sets. The compendium provides a valuable resource for future fundamental and applied research with C. glutamicum and contributes to a systemic understanding of this microbial cell factory.Measurement(s)Gene Expression AnalysisTechnology Type(s)Two Color MicroarrayFactor Type(s)WT condition A vs. WT condition B • Plasmid-based gene overexpression in parental strain vs. parental strain with empty vector control • Deletion mutant vs. parental strainSample Characteristic - OrganismCorynebacterium glutamicumSample Characteristic - Environmentlaboratory environmentSample Characteristic - LocationGermany

Importance of Host Abundance and Microhabitat in Tick Abundance.

To reduce the risk of zoonoses, it is necessary to understand the infection process, including the ecology of animals and vectors (i.e., the 'One Health' approach). In temperate climates, ticks are the major vectors of zoonoses, so factors determining their abundance, such as host mammal abundance and microhabitat conditions, should be clarified. Sika deer (Cervus nippon) are a major tick host and are rapidly expanding their distribution in Japan. We established 12 plots along a gradient of sika deer abundance in Tochigi Prefecture, Japan. We monitored the occurrence of mammal species with camera traps and sampled questing ticks on a monthly basis by flagging along three transects (center of a trail, forest edge, and forest interior) at each site from April to November 2018. The camera traps recorded 12 mammal species, predominantly sika deer. Five Haemaphysalis species and three Ixodes species were sampled. The numbers of ticks sampled were explained by the photographic frequency of sika deer, and partly by that of other mammal species, depending on tick species and their developmental stages. The numbers of sampled adult and nymphal ticks were the highest at the forest edge, where vegetation cover was greatest. Thus, vegetation management in tick habitats and the control of sika deer populations may reduce tick abundance.

Host and gut bacteria share metabolic pathways for anti-cancer drug metabolism.

Pharmaceuticals have extensive reciprocal interactions with the microbiome, but whether bacterial drug sensitivity and metabolism is driven by pathways conserved in host cells remains unclear. Here we show that anti-cancer fluoropyrimidine drugs inhibit the growth of gut bacterial strains from 6 phyla. In both Escherichia coli and mammalian cells, fluoropyrimidines disrupt pyrimidine metabolism. Proteobacteria and Firmicutes metabolized 5-fluorouracil to its inactive metabolite dihydrofluorouracil, mimicking the major host mechanism for drug clearance. The preTA operon was necessary and sufficient for 5-fluorouracil inactivation by E. coli, exhibited high catalytic efficiency for the reductive reaction, decreased the bioavailability and efficacy of oral fluoropyrimidine treatment in mice and was prevalent in the gut microbiomes of colorectal cancer patients. The conservation of both the targets and enzymes for metabolism of therapeutics across domains highlights the need to distinguish the relative contributions of human and microbial cells to drug efficacy and side-effect profiles.

Investigating bracovirus chromosomal integration and inheritance in lepidopteran host and nontarget species.

Bracoviruses (BVs) are domesticated viruses found in braconid parasitoid wasp genomes. They are composed of domesticated genes from a nudivrius, coding viral particles in which wasp DNA circles are packaged. BVs are viewed as possible vectors of horizontal transfer of genetic material (HT) from wasp to their hosts because they are injected, together with wasp eggs, by female wasps into their host larvae, and because they undergo massive chromosomal integration in multiple host tissues. Here, we show that chromosomal integrations of the Cotesia typhae BV (CtBV) persist up to the adult stage in individuals of its natural host, Sesamia nonagrioides, that survived parasitism. However, while reproducing host adults can bear an average of nearly two CtBV integrations per haploid genome, we were unable to retrieve any of these integrations in 500 of their offspring using Illumina sequencing. This suggests either that host gametes are less targeted by CtBVs than somatic cells or that gametes bearing BV integrations are nonfunctional. We further show that CtBV can massively integrate into the chromosomes of other lepidopteran species that are not normally targeted by the wasp in the wild, including one which is divergent by at least 100 million years from the natural host. Cell entry and chromosomal integration of BVs are thus unlikely to be major factors shaping wasp host range. Together, our results shed new light on the conditions under which BV-mediated wasp-to-host HT may occur and provide information that may be helpful to evaluate the potential risks of uncontrolled HT associated with the use of parasitoid wasps as biocontrol agents.