An exploratory analysis of the structure of tetranychid and phytoseiid assemblages in walnut orchards in California.

Spider mites were considered secondary pests of walnut production in California, under the control of phytoseiid predators. Due to increased importance as walnut pests in recent decades there is renewed interest in the structure and function of the associated phytoseiid assemblage. In this study we report the results from a 3 year survey of the tetranychid and phytoseiid assemblages in walnut orchards in the Central Valley of California. The survey was conducted to determine the range and dominance of web-spinning Tetranychus species present, to investigate the species richness and dominance of the phytoseiid species present, and to explore whether patterns of variation in the relative abundance of phytoseiid species could be explained by one or more explanatory variables. Tetranychus urticae was the dominant spider mite in all growing regions and years with T. pacificus and T. turkestani also present in orchards in the southern San Joaquin Valley. Phytoseiid species richness declined with latitude among the three walnut growing regions and of the 13 species found Amblyseius similoides, Euseius stipulatus, Galendromus occidentalis and Typhlodromus caudiglans were the most abundant and widespread species present. Mean proportional abundance significantly increased from early (mid May-July) to late (August-mid October) season and from southern to northern growing regions for Type II and IV predators, but significantly decreased from early to late season and from southern to northern growing regions for Type III predators. The mean proportional abundance of Type II predators, particularly G. occidentalis, significantly increased and that of Type III predators significantly decreased with mean Tetranychus density in individual orchards. The current survey provides a more in-depth analysis of mite assemblages in walnut orchards in California and can be used to better inform adaptive management strategies for integrated mite management in the future.

Suitability of the shrub-steppe habitat of Eastern Washington for Halyomorpha halys (Hemiptera: Pentatomidae).

The invasive brown marmorated stink bug, Halyomorpha halys Stål (Hemiptera: Pentatomidae), has spread throughout most of Washington (WA) State since its detection in 2012. While it has emerged as a major agricultural and nuisance pest in the Pacific Northwest (PNW) west of the Cascade Mountains, pest pressure in the major tree fruit-growing areas in semi-arid northern and central WA State remains low. The reasons for this are unclear, although both biotic and abiotic conditions may be contributing factors. We evaluated the suitability of a common shrub-steppe/riparian corridor plant assemblage for supporting H. halys development from egg to adult in summer and fall through controlled feeding studies. Nymphs successfully completed development on this diet of PNW native plants, though it generally resulted in lower survivorship and adult weight and longer developmental times than a modified colony diet or a diet of known hosts from the eastern United States. These developmental data were used to parameterize stage-structured matrix models to predict the impact of diet and extreme heat events on H. halys population growth. The predicted net reproductive rate (R0) of H. halys was consistently and substantially reduced by a diet of PNW native plants, and heat shock imposed further severe reductions in R0. Our results suggest that the combined population effects of suboptimal plant host quality and regional heat waves may explain the lack of landscape-level H. halys pest pressure in semi-arid regions of the PNW.

Reproductive attributes and functional response of Anastatus japonicus on eggs of Antheraea pernyi, a factitious host.

BACKGROUND: Anastatus japonicus Ashmead (Hymenoptera: Eupelmidae) is a solitary egg endoparasitoid that has been studied for inundative biological control of Halyomorpha halys Stål (Hemiptera: Pentatomidae) in China. In this study, we assessed the reproductive attributes and functional response of Anastatus japonicus on a factitious host, Antheraea pernyi (Guérin-Méneville) (Lepidoptera: Anthelidae) at 25 ± 1 °C, 70 ± 5% relative humidity and 16 h:8 h light/dark photoperiod. RESULTS: The mean lifetime fecundity of Anastatus japonicus females was 404.3 progeny produced over an average oviposition period of 42.3 days. The sex ratio of adult progeny was slightly male biased (51.2%), whereas more female progeny were produced before day 20 of a female's life. Single 1-day-old mated Anastatus japonicus females exhibited a type II functional response to increasing host densities (1-50 eggs), with an inverse host density-dependent pattern of percent parasitism. The upper limit to the daily attack rate was estimated as 7.6 Antheraea pernyi eggs. Furthermore, mutual interference among Anastatus japonicus females occurred when increasing densities of parasitoids (1, 2, 4, 8, 16) were exposed to 30 host eggs. CONCLUSION: Laboratory functional response result revealed that individual Anastatus japonicus might be unable to respond effectively to increasing host density in the field, which could be compensated by releasing larger numbers of wasps. Strong mutual interference among foraging Anastatus japonicus females should be considered in any future inundative biological control programs for the sustainable management of Halyomorpha halys or other host insect pests. © 2022 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Pesticide exposure of wild bees and honey bees foraging from field border flowers in intensively managed agriculture areas.

Bees are critical for food crop pollination, yet their populations are declining as agricultural practices intensify. Pollinator-attractive field border plantings (e.g. hedgerows and forb strips) can increase bee diversity and abundance in agricultural areas; however, recent studies suggest these plants may contain pesticides. Pesticide exposure for wild bees remains largely unknown; however, this information is needed to inform agricultural practices and pesticide regulations meant to protect bees. It is important to determine whether border plantings that attract and support pollinators may also deliver pesticides to them. In this study, we collected various samples for pesticide residue analysis, including: multiple species of wild bees, honey bees, flowers from four types of bee-attractive field border plants, and soil. Silicone bands were also utilized as passive aerial samplers of pesticide residues. The five pesticides detected most frequently across all samples were the insecticide bifenthrin, the herbicides thiobencarb, metolaclor, and propanil, and the fungicide fluopyram. We detected the greatest number of parent pesticides in bands (24), followed by soil (21). Pesticides were also detected in field border plant flowers (16), which do not receive direct pesticide applications, and included many products which were not applied to adjacent field crops. Pesticide concentrations were lower in bees than in flowers but higher in bees than in soils. Pesticide residue per bee (ng/bee) increased with increasing wild bee size, though pesticide concentration (ng/g) did not increase. While honey bees and wild bees contained a similar number and concentration of pesticides overall, pesticide mixtures varied by bee type, and included some mixtures known to cause sublethal effects. The results from this study highlight the benefits of measuring more sample types to capture the total exposome of bees, including a greater range of bee species, as well as the need to consider exposure to pesticides at the landscape level.

Review: classical biological control of invasive stink bugs with egg parasitoids - what does success look like?

Although the enemy release hypothesis forms the theoretical basis for classical (=importation) biological control of invasive pests, its core assumptions are not always examined. This could contribute to unrealistic expectations for some biological control programs. In this paper we examine the assumptions that: (i) enemy release has contributed to the invasive nature of four exotic pentatomids in North America; and (ii) classical biological control with egg parasitoids has been or will be successful in reducing populations of these pests below economically significant levels. First, we review the history of biological control programs against invasive stink bugs to highlight the variable and controversial levels of success of introducing egg parasitoids against stink bugs. Then, we use simple stage-structured matrix models to demonstrate that it may be easy to overestimate the contribution of egg parasitism alone to a reduction in stink bug population growth. Finally, we discuss what realistic expectations might be for success of biological control against invasive stink bugs using egg parasitoids in the context of integrated pest management programs. © 2020 Her Majesty the Queen in Right of Canada Pest Management Science © 2020 Society of Chemical Industry.

Sources of Variation in the Adult Flight of Walnut Husk Fly (Diptera: Tephritidae): A Phenology Model for California Walnut Orchards.

A phenology model of the walnut husk fly, Rhagoletis completa Cresson, was developed to more accurately predict the timing of the flight period and optimize management decisions. A data set of 153 orchard years in which adults were trapped throughout the season was used for the development and validation of this model. Data from California Irrigation Management Information System (CIMIS) weather stations were used to match orchard-year datasets with historical climatic data on degree-day (DD) accumulation, winter chill, and winter rainfall. A cumulative Weibull distribution was used to model the relationship between cumulative trap catch and DD accumulation for R. completa in California. The model was used to predict thermal requirements for the start (5% cumulative trap catch) and mid-point (50% cumulative trap catch) of the flight period, which were 1,670 and 2,179 DDs, respectively. The prediction for 50% cumulative trap catch of R. completa in California was much higher than the thermal requirement estimated in Oregon previously (1,751 DDs). Linear mixed effects models were used to evaluate other environmental and orchard-specific factors which could explain the large variation between predicted and observed thermal requirements for both the start and mid-point of the flight period. Latitude, walnut cultivar leaf-out time, orchard age and year, as a continuous variable, all contributed significantly to explain deviations from the predictions of the DD model for individual orchard years. Such factors can be used both to adjust predicted thermal requirements for these two specific and informative stages of the flight period, and to provide a basis for ecological and evolutionary hypotheses.

An Alternative Perspective for the Theory of Biological Control.

Importation biological control represents the planned introduction of a specialist natural enemy from the region of origin of an invasive pest or weed. For this study, the author considered why attempts to develop a predictive theory for biological control have been misguided and what future directions might be more promising and effective. Despite considerable interest in the theory of consumer⁻resource population dynamics, such theory has contributed little to improvements in the success of biological control due to a focus on persistence and equilibrium dynamics rather than establishment and impact. A broader consideration of invasion biology in addition to population ecology offers new opportunities for a more inclusive theory of biological control that incorporates the demographic and genetic processes that more specifically address the establishment and impact of introduced natural enemies. The importance of propagule size and genetic variance for successful establishment, and of contributions to host population growth, relative population growth rates, interaction strength, and coevolution for suppression of host abundance are discussed as promising future directions for a theory of biological control.

Could increased understanding of foraging behavior help to predict the success of biological control?

Importation biological control, the introduction of a specialist natural enemy from the region of origin of an invasive pest or weed, has been practiced for more than 100 years and has provided some iconic success stories, but also a number of failures. To improve both the success and safety of biological control in the future it is important to consider all opportunities that can help to transform biological control into a more predictive science. Once established, whether or not an imported natural enemy can reduce the abundance and distribution of an invasive host, likely depends on a suite of life history and behavioral traits that include phenological synchronization and foraging efficiency among many others. One key aspect of foraging efficiency is how individuals respond to the patchy distribution of hosts in a spatially fragmented environment when facing potential competition and predation risk. Another is what distributions of natural enemy foraging effort lead to the greatest temporal reduction in mean host density among patches. Here we explore the current theoretical framework for natural enemy foraging behavior and find some evidence that a weak resource dilution distribution of natural enemies among patches might be an important trait for improving the success of importation biological control.

Comparative genetics of invasive populations of walnut aphid, Chromaphis juglandicola, and its introduced parasitoid, Trioxys pallidus, in California.

Coevolution may be an important component of the sustainability of importation biological control, but how frequently introduced natural enemies coevolve with their target pests is unclear. Here we explore whether comparative population genetics of the invasive walnut aphid, Chromaphis juglandicola, and its introduced parasitoid, Trioxys pallidus, provide insights into the localized breakdown of biological control services in walnut orchards in California. We found that sampled populations of C. juglandicola exhibited higher estimates of genetic differentiation (FST) than co-occurring populations of T. pallidus. In contrast, estimates of both the inbreeding coefficient (GIS) and contemporary gene flow were higher for T. pallidus than for C. juglandicola. We also found evidence of reciprocal outlier loci in some locations, but none showed significant signatures of selection. Synthesis and applications. Understanding the importance of coevolutionary interactions for the sustainability of biological control remains an important and understudied component of biological control research. Given the observed differences in gene flow and genetic differentiation among populations of T. pallidus and C. juglandicola, we suspect that temporary local disruption of biological control services may occur more frequently than expected while remaining stable at broader regional scales. Further research that combines genomewide single nucleotide polymorphism genotyping with measurements of phenotypic traits is needed to provide more conclusive evidence of whether the occurrence of outlier loci that display significant signatures of selection can be interpreted as evidence of the presence of a geographic mosaic of coevolution in this system.

Temporal Patterns in the Abundance and Species Composition of Spiders on Host Plants of the Invasive Moth Epiphyas postvittana (Lepidoptera: Tortricidae).

Generalist predators such as spiders may help mitigate the spread and impact of exotic herbivores. The lack of prey specificity and long generation times of spiders may allow them to persist when pests are scarce, and to limit the growth of pest populations before they reach damaging levels. We examined whether resident spiders are likely to play a role in maintaining populations of the invasive light brown apple moth, Epiphyas postvittana (Walker) (Lepidoptera: Tortricidae), below outbreak levels in California. We surveyed the spider community on two E. postvittana host plants, the ornamental Australian tea tree, Leptospermum laevigatum, and the weed French broom, Genista monspessulana, to characterize spider and larval E. postvittana abundance and spider species composition throughout the year. Spider densities and species composition showed slight seasonal changes. Spiders were present during periods of high and low E. postvittana abundance. Anyphaenid hunting spiders, Anyphaena aperta Banks in Australian tea tree and Anyphaena pacifica Banks in French broom, dominated spider species composition at four of five sampled sites, and underwent only slight seasonal variation in abundance. Adult A. aperta were rare at all times of the year, suggesting that high mortality among juvenile A. aperta limits the potential of this species as a predator of E. postvittana. Nevertheless, the continued presence of spiders throughout the year indicates that the resident spider community is likely to play a key role in reducing E. postvittana populations in California.

Novel multitrophic interactions among an exotic, generalist herbivore, its host plants and resident enemies in California.

What happens when an exotic herbivore invades and encounters novel host plants and enemies? Here, we investigate the impacts of host plant quality and plant architecture on an exotic generalist herbivore, Epiphyas postvittana (Lepidoptera: Tortricidae) and its interactions with resident parasitoids in California. Using artificial diet and five plant species, we found significant effects of diet on the fitness of E. postvittana under laboratory conditions. In the field, based on a common garden experiment with host plants of nine species, we found that larval parasitism varied among plant species by a factor of 2.1 with a higher risk of parasitism on shorter than taller plants. Parasitism of egg masses varied by a factor of 4.7 among plant species with a higher risk of parasitism on taller than shorter plants. In the laboratory, the foraging time of a resident egg parasitoid on excised leaves varied among plant species, but did not correspond to observed egg parasitism rates on these same plants in the field. On leaves of Plantago lanceolata, the probability of egg parasitism decreased with trichome density. Overall, there was a significant effect of host plant on the intrinsic rate of increase of E. postvittana and on the extent of parasitism by resident parasitoids, but no correlation existed between these two effects. The recent decline of E. postvittana in California may be due to the low quality of some host plants and to the many resident enemies that readily attack it, perhaps due to its phylogenetic relatedness to resident tortricids.

Nitrogen-Mediated Interaction: A Walnut-Aphid-Parasitoid System.

The effects of plant quality on natural enemies are often overlooked in planning and executing biological control programs for insect pests in agriculture. Plant quality, however, could help to explain some of the observed variation in effectiveness of biological control, as it can indirectly influence natural enemy populations. In this study, we used the walnut aphid Chromaphis juglandicola (Kaltenbach) to address the effect of increased nitrogen availability to the host plant on parasitism by the specialist parasitoid Trioxys pallidus (Haliday). In laboratory experiments with walnut seedlings, a higher chlorophyll content index of the foliage in response to added nitrogen was correlated with a decrease in the number of mummies produced by female parasitoids over a 24-h period but an increase in the proportion and the size of female offspring. In field sampling of walnut orchards, there was no relationship between the percent parasitism of walnut aphids by T. pallidus and the chlorophyll content index of the trees. Nitrogen fertilizer and plant quality can clearly affect biological control and should be given greater consideration in integrated pest management.

Pathogenicity, morphology, and characterization of a Nosema fumiferanae isolate (Microsporidia: Nosematidae) from the light brown apple moth, Epiphyas postvittana (Lepidoptera: Tortricidae) in California.

We recently discovered infections by a microsporidium closely related to Nosema fumiferanae in field populations of the light brown apple moth, Epiphyas postvittana (Walker) (Lepidoptera: Tortricidae), in the San Francisco region of California. E. postvittana originates from Australia and was first detected in California in 2006; therefore, our aim was to identify and determine the origin of the Nosema isolate. We characterized the pathogenicity, transmission pathways, and ultrastructure of this new Nosema isolate. In addition, we sequenced fragments of commonly used genetic markers (ITS, SSU, and RPB1), and examined the phylogenetic relationships between the Nosema isolate and other microsporidian species commonly found in lepidopteran hosts. The pathogenicity of the Nosema isolate was investigated by infecting second instar larvae of E. postvittana. Larval and pupal survivorship were reduced by 7% and 13% respectively, and pupation occurred 1-2d later in infected individuals than in healthy individuals. Emerging infected females died 5d earlier than healthy females, and daily fecundity was 22% lower. Hatch rate also was 22% lower for eggs oviposited by infected females. Vertical transmission was confirmed; spores were present in 68% of egg masses and 100% of the surviving larvae from infected females. Ultrastructure images, together with sequences from selected genetic markers, confirmed the Nosema isolate to be a member of the Nosema fumiferanae species complex (Nosema fumiferanae postvittana subsp. n.). The association of this pathogen with E. postvittana contributes further to the biotic resistance that E. postvittana has experienced since its introduction to California.

Pathogenicity, prevalence and intensity of a microsporidian infection by Nosema fumiferanae postvittana in the light brown apple moth, Epiphyas postvittana, in California.

While biological invasions are increasing, in some cases exotic species exhibit an initial phase of population growth and spread, followed by a subsequent phase of natural decline. The light brown apple moth, Epiphyas postvittana (Walker) (Lepidoptera: Tortricidae), provides a unique opportunity to examine potential mechanisms for the natural suppression of an exotic insect species that has become established in coastal California. We recently discovered a microsporidian pathogen, Nosema fumiferanae postvittana, from E. postvittana in its novel range. In the laboratory, we examined the pathogenicity and latent period of this microsporidium, and in the field we determined its prevalence and intensity in five locations using quantitative real-time PCR (qPCR). In the laboratory, when comparing healthy larvae to larvae infected with up to 10(5) spores, we found a reduction in juvenile survivorship (from 100% to 26%), a prolongation of juvenile development time (of up to 9-10 days), a reduction in viable lifetime fecundity (from 788 to 1) and a reduction in the intrinsic rate of increase (from 0.18 to 0.008). The median lethal dose (LD50) was estimated to be 1.8 × 10(4) spores, and the mean latent period for infections with 10(3) spores was 12.67 days. Our field sampling revealed that E. postvittana populations have further declined from previously reported densities in San Francisco and Santa Cruz. We detected N. fumiferanae postvittana in all five locations with an overall prevalence of 5%, which did not appear to be influenced consistently by either host density or season. Mean microsporidian intensity in field-infected individuals was 226 spores. Although the laboratory results demonstrated the potential for host suppression, the field sampling indicated that the prevalence and intensity of microsporidian infection were too low to account for the continued decline in population densities of E. postvittana in coastal California.

iMSAT: a novel approach to the development of microsatellite loci using barcoded Illumina libraries.

BACKGROUND: Illumina sequencing with its high number of reads and low per base pair cost is an attractive technology for development of molecular resources for non-model organisms. While many software packages have been developed to identify short tandem repeats (STRs) from next-generation sequencing data, these methods do not inform the investigator as to whether or not candidate loci are polymorphic in their target populations. RESULTS: We provide a python program iMSAT that uses the polymorphism data obtained from mapping individual Illumina sequence reads onto a reference genome to identify polymorphic STRs. Using this approach, we identified 9,119 candidate polymorphic STRs for use with the parasitoid wasp Trioxys pallidus and 2,378 candidate polymorphic STRs for use with the aphid Chromaphis juglandicola. For both organisms we selected 20 candidate tri-nucleotide STRs for validation. Using fluorescent-labeled oligonucleotide primers, we genotyped 91 female T. pallidus collected in nine localities and 46 female C. juglandicola collected in 4 localities and found 15 of the examined markers to be polymorphic for T. pallidus and 12 of the examined markers to be polymorphic for C. juglandicola. CONCLUSIONS: We present a novel approach that uses standard Illumina barcoding primers and a single Illumina HiSeq run to target polymorphic STR fragments to develop and test STR markers. We validate this approach using the parasitoid wasp T. pallidus and its aphid host C. juglandicola. This approach, which would also be compatible with 454 Sequencing, allowed us to quickly identify markers with known variability. Accordingly, our method constitutes a significant improvement over existing STR identification software packages.

You are what you eat: fatty acid profiles as a method to track the habitat movement of an insect.

Tracking the movement of small organisms is of tremendous importance to understanding the ecology of populations, communities, and ecosystems. However, it remains one of the most difficult challenges facing the field of movement ecology. We developed an intrinsic marking technique for tracking small organisms using dietary fatty acid profiles as a biomarker as well as for clarifying source-sink dynamics between populations on a landscape level. Navel orangeworm moths (NOW), Amyelois transitella (Walker) (Lepidoptera: Pyralidae), raised on two different host plants with significantly different fatty acid profiles, were used to develop a model that distinguishes NOW based on their larval host plant. Wild NOW from both known and unknown host plants were used to validate the model. NOW fatty acid profiles showed striking similarities to the fatty acid profile of their host plant demonstrating that fatty acids can act as an intrinsic marking technique for quantifying the movement of small organisms. We anticipate that given sufficient spatial variation in dietary fatty acids, this technique will be useful in studying the movement of arthropods and other invertebrates particularly when addressing questions of source-sink dynamics.

The importance of individual developmental variation in stage-structured population models.

Population stage structure is fundamental to ecology, and models of this structure have proven useful in many different systems. Many ecological variables other than stage, such as habitat type, site occupancy and metapopulation status are also modelled using transitions among discrete states. Transitions among life stages can be characterised by the distribution of time spent in each stage, including the mean and variance of each stage duration and within-individual correlations among multiple stage durations. Three modelling traditions represent stage durations differently. Matrix models can be derived as a long-run approximation from any distribution of stage durations, but they are often interpreted directly as a Markov model for stage transitions. Statistical stage-duration distribution models accommodate the variation typical of cohort development data, but such realism has rarely been incorporated in population theory or statistical population models. Delay-differential equation models include lags but no variation, except in limited cases. We synthesise these models in one framework and illustrate how individual variation and correlations in development can impact population growth. Furthermore, different development models can yield the same long-term matrix transition rates but different sensitivities and elasticities. Finally, we discuss future directions for estimating realistic stage duration models from data.

Small-scale intraspecific life history variation in herbivorous spider mites (Tetranychus pacificus) is associated with host plant cultivar.

Life history variation is a general feature of arthropod systems, but is rarely included in models of field or laboratory data. Most studies assume that local processes occur identically across individuals, ignoring any genetic or phenotypic variation in life history traits. In this study, we tested whether field populations of Pacific spider mites (Tetranychus pacificus) on grapevines (Vitis vinifera) display significant intraspecific life history variation associated with host plant cultivar. To address this question we collected individuals from sympatric vineyard populations where either Zinfandel or Chardonnay were grown. We then conducted a "common garden experiment" of mites on bean plants (Phaseolus lunatus) in the laboratory. Assay populations were sampled non-destructively with digital photography to quantify development times, survival, and reproductive rates. Two classes of models were fit to the data: standard generalized linear mixed models and a time-to-event model, common in survival analysis, that allowed for interval-censored data and hierarchical random effects. We found a significant effect of cultivar on development time in both GLMM and time-to-event analyses, a slight cultivar effect on juvenile survival, and no effect on reproductive rate. There were shorter development times and a trend towards higher juvenile survival in populations from Zinfandel vineyards compared to those from Chardonnay vineyards. Lines of the same species, originating from field populations on different host plant cultivars, expressed different development times and slightly different survival rates when reared on a common host plant in a common environment.