Melittobia acasta (Hymenoptera: Eulophidae) female longevity and life stage-dependent parasitism using commercially managed Megachile rotundata (Hymenoptera: Megachilidae) as hosts.

Melittobia acasta Walker is one among other hymenopterous parasitoids of Megachile rotundata F. Commercial M. rotundata populations are employed to pollinate North American alfalfa for seed production. This wasp can be prolific when using M. rotundata as a host and can reduce or destroy bee stocks. Hundreds of M. acasta female offspring can develop in a single M. rotundata cell and disperse to infest other cells, producing thousands of more parasitoids. In this study, we determined (i) upon what bee life stages M. acasta females choose to lay eggs and if those eggs ultimately become adults and (ii) M. acasta female longevity when exposed to various resources within M. rotundata cells. We found that M. acasta females lay eggs on M. rotundata prepupae and pupae and that those eggs can hatch and survive to adulthood. Eggs are not laid on early instar bee larvae; eggs laid on adults do not survive. Average female life span is 5 days without feeding, 8-9 days if a pollen-nectar provision is available while the bee develops through larval stages, and 34 days if the wasp can feed on prepupal hemolymph. Wasp females can emerge from bee cells several days after trays of cells are taken to fields. Therefore, adult females could survive long enough for new bee offspring to become prepupae. Our findings support a better understanding of host life stage preference and the longevity of M. acasta females that can inform the timing of the implementation of possible control measures.

Captive Rearing Success and Critical Thermal Maxima of Bombus griseocollis (Hymenoptera: Apidae): A Candidate for Commercialization?

Commercialized bumble bees (Bombus) are primary pollinators of several crops within open field and greenhouse settings. However, the common eastern bumble bee (Bombus impatiens Cresson, 1863) is the only species widely available for purchase in North America. As an eastern species, concerns have been expressed over their transportation outside of their native range. Therefore, there is a need to identify regionally appropriate candidates for commercial crop pollination services, especially in the western U.S.A. In this study, we evaluated the commercialization potential of brown-belted bumble bees (Bombus griseocollis De Geer, 1773), a broadly distributed species throughout the U.S.A., by assessing nest initiation and establishment rates of colonies produced from wild-caught gynes, creating a timeline of colony development, and identifying lab-reared workers' critical thermal maxima (CTMax) and lethal temperature (ecological death). From 2019 to 2021, 70.6% of the wild-caught B. griseocollis gynes produced brood in a laboratory setting. Of these successfully initiated nests, 74.8% successfully established a nest (produced a worker), providing guidance for future rearing efforts. Additionally, lab-reared workers produced from wild-caught B. griseocollis gynes had an average CTMax of 43.5°C and an average lethal temperature of 46.4°C, suggesting B. griseocollis can withstand temperatures well above those commonly found in open field and greenhouse settings. Overall, B. griseocollis should continue to be evaluated for commercial purposes throughout the U.S.A.

Concerted cis and trans effects underpin heightened defense gene expression in multi-herbivore-resistant maize lines.

In maize (Zea mays ssp. mays), agriculturally damaging herbivores include lepidopteran insects, such as the European corn borer (Ostrinia nubilalis), and distantly related arthropods, like the two-spotted spider mite (Tetranychus urticae). A small number of maize lines, including B96 and B75, are highly resistant to both herbivores, and B96 is also resistant to thrips. Using T. urticae as a representative pest that causes significant leaf tissue damage, we examined the gene expression responses of these lines to herbivory in comparison with each other and with the susceptible line B73. Upon herbivory, the most resistant line, B96, showed the strongest gene expression response, with a dramatic upregulation of genes associated with jasmonic acid biosynthesis and signaling, as well as the biosynthesis of specialized herbivore deterrent compounds, such as death acids and benzoxazinoids. Extending this work with allele-specific expression analyses in F1 hybrids, we inferred that the concerted upregulation of many defense genes, including the majority of benzoxazinoid biosynthetic genes in B96, as compared with B73, for the herbivore treatment, resulted from an assemblage of trans control and multiple cis effects acting with similar directionality on gene expression. Further, at the level of individual and potentially rate limiting genes in several major defense pathways, cis and trans effects acted in a reinforcing manner to result in exceptionally high expression in B96. Our study provides a comprehensive resource of cis elements for maize lines important in breeding efforts for herbivore resistance, and reveals potential genetic underpinnings of the origins of multi-herbivore resistance in plant populations.

Effects of Provision Type and Pesticide Exposure on the Larval Development of Osmia lignaria (Hymenoptera: Megachilidae).

Wild and managed bee populations are in decline, and one of many environmental causes is the impact of pesticides on developing bees. For solitary bees, delayed larval development could lead to asynchronous adult emergence, unhealthy and inefficient adult pollinators, and decreased brood production and survival. We examined a methodology for testing Osmia lignaria Say (Hymenoptera: Megachilidae) larval responses to pesticide exposure using a laboratory bioassay. We created two provision types: a homogenized blend of O. lignaria provisions from an apple orchard and homogenized almond pollen pellets collected by honey bees plus sugar water. Pesticides were administered to the provisions to compare toxic effects. We recorded larval developmental durations for second-fifth instar and for fifth instar to cocoon initiation for larvae fed provisions treated with water (control) or doses of three pesticides and a representative spray-tank mixture (acetamiprid, boscalid/pyraclostrobin, dimethoate, and acetamiprid plus boscalid/pyraclostrobin). All larvae survived to cocoon initiation when only water was added to provisions. Impacts of pesticide treatments significantly differed between the apple and almond homogenates. The greatest treatment effects occurred when the homogenized almond provision was mixed with acetamiprid alone and when combined with boscalid/pyraclostrobin. Optimizing bioassays through the use of appropriate larval food for exposing solitary bee larvae to agrochemicals is crucial for assessing risks for pollinators.

Seeking Alfalfa Resistance to a Rhizophagous Pest, the Clover Root Curculio (Sitona hispidulus F.).

Since the cancellation of broad-spectrum soil-active insecticides in alfalfa (Medicago sativa L.) production, clover root curculio (Sitona hispidulus F.) (CRC) larval root damage has increased. Current CRC management practices are limited in their ability to suppress larval feeding belowground. First, we field screened developmental alfalfa populations for CRC damage. Subsequently, we developed a soil-less arena to observe nodule feeding and development (head capsule width) of larvae in the lab. This method was used to evaluate five alfalfa populations (two CRC-susceptible (control) and three CRC-resistant populations) against larvae. Further, one CRC-resistant population paired with its genetically similar susceptible population were tested against adult leaf consumption and oviposition in the greenhouse. Field screening revealed that the alfalfa populations selected for little or no larval root feeding damage were more resistant to CRC larval feeding than their corresponding unselected cultivars and significantly more resistant than populations selected for susceptibility. The development of a soil-less arena provided a useful method for evaluation of root-larva interactions. Although larval development was similar across susceptible and resistant alfalfa populations, one CRC-resistant population (NY1713) displayed overall increased nodulation and, thus, had a significantly lower proportion of nodules consumed by larvae. Adult feeding and oviposition aboveground were similar across all populations tested. These results provide possible candidates and screening method for the development and evaluation of alfalfa cultivars that may reduce the impacts of larval feeding and that offer an additional option for CRC management.

Characterizing Billbug (Sphenophorus spp.) Seasonal Biology Using DNA Barcodes and a Simple Morphometric Analysis.

Billbugs (Sphenophorus spp.) are a complex of grass-feeding weevil species that reduce the aesthetic and functional qualities of turfgrass. Effective billbug monitoring and management programs rely on a clear understanding of their seasonal biology. However, our limited understanding of regional variation in the species compositions and seasonal biology of billbugs, stemming primarily from our inability to identify the damaging larval stage to species level, has hindered efforts to articulate efficient IPM strategies to growers. We used a combination of DNA barcoding methods and morphometric measures to begin filling critical gaps in our understanding of the seasonal biology of the billbug species complex across a broad geographic range. First, we developed a DNA barcoding reference library using cytochrome oxidase subunit 1 (COI) sequences from morphologically identified adult billbugs collected across Indiana, Missouri, Utah and Arizona. Next, we used our reference library for comparison and identification of unknown larval specimens collected across the growing season in Utah and Indiana. Finally, we combined our DNA barcoding approach with larval head capsule diameter, a proxy for developmental instar, to develop larval phenology charts. Adult COI sequences varied among billbug species, but variation was not influenced by geography, indicating that this locus alone was useful for resolving larval species identity. Overlaid with head capsule diameter data from specimens collected across the growing season, a better visualization of billbug species composition and seasonal biology emerged. This approach will provide researchers with the tools necessary to fill critical gaps in our understanding of billbug biology and facilitate the development of turfgrass pest management programs.

Maize Inbred Line B96 Is the Source of Large-Effect Loci for Resistance to Generalist but Not Specialist Spider Mites.

Maize (Zea mays subsp. mays) yield loss from arthropod herbivory is substantial. While the basis of resistance to major insect herbivores has been comparatively well-studied in maize, less is known about resistance to spider mite herbivores, which are distantly related to insects and feed by a different mechanism. Two spider mites, the generalist Tetranychus urticae, and the grass-specialist Oligonychus pratensis, are notable pests of maize, especially during drought conditions. We assessed resistance (antibiosis) to both mites of 38 highly diverse maize lines, including several previously reported to be resistant to one or the other mite species. We found that line B96, as well as its derivatives B49 and B75, were highly resistant to T. urticae. In contrast, neither these three lines, nor any others included in our study, were notably resistant to the specialist O. pratensis. Quantitative trait locus (QTL) mapping with replicate populations from crosses of B49, B75, and B96 to susceptible B73 identified a QTL in the same genomic interval on chromosome 6 for T. urticae resistance in each of the three resistant lines, and an additional resistance QTL on chromosome 1 was unique to B96. Single-locus genotyping with a marker coincident with the chromosome 6 QTL in crosses of both B49 and B75 to B73 revealed that the respective QTL was large-effect; it explained ∼70% of the variance in resistance, and resistance alleles from B49 and B75 acted recessively as compared to B73. Finally, a genome-wide haplotype analysis using genome sequence data generated for B49, B75, and B96 identified an identical haplotype, likely of initial origin from B96, as the source of T. urticae resistance on chromosome 6 in each of the B49, B75, and B96 lines. Our findings uncover the relationship between intraspecific variation in maize defenses and resistance to its major generalist and specialist spider mite herbivores, and we identified loci for use in breeding programs and for genetic studies of resistance to T. urticae, the most widespread spider mite pest of maize.

Influence of adjuvants on the amount, specificity and functional activity of antibody response to human influenza vaccine in mice.

It's been almost a century since immunologists started using adjuvants as tools to develop more effective vaccines. Despite the rising number of adjuvanted vaccines in the last decades, we still lack knowledge of the adjuvants' effects on antibody response. This study was aimed to test the effect of immunizing mice with the human Inactivated Influenza vaccine (IIV), either alone or combined with different widely used adjuvants on the specific antibody response induced. Differential levels of IgM and IgG subclasses were found with the different adjuvants tested. Higher levels of antibodies did not always correspond with a higher efficacy to interfere with the virus infectivity. Differences in neutralization properties are possibly mediated by the specificity of the repertoire of antibodies induced. The repertoire was studied using a phage display 7-mer peptide library to screen for epitopes/mimotopes recognized by serum pools from vaccinated mice. The selected phage clones included peptides that corresponded to conformational mimotopes since they have no homology with lineal sequences of the Influenza strains' proteins. Five peptides were identified as recognized by sera from mice immunized with the IIV vaccine alone, including peptides from the hemagglutinin stalk domain, and by sera from mice immunized with the vaccine plus the different adjuvants employed. Adjuvants elicited a more diverse repertoire of epitope-recognizing antibodies that recognized epitopes of the HA recombinant globular head. Mimotopes were theoretically located at the neutralizing antigenic sites of the globular head of Influenza A H1N1pdm09, Influenza A H3N2, and Influenza B hemagglutinin. This study illustrates how different adjuvants can modify the extent and quality of humoral immunity against the IIV vaccine and the effectiveness of vaccination.

Banks Grass Mite (Acari: Tetranychidae) Suppression May Add to the Benefit of Drought-Tolerant Corn Hybrids Exposed to Water Stress.

Spider mite (Acari: Tetranychidae) outbreaks are common on corn grown in the arid West. Hot and dry conditions reduce mite development time, increase fecundity, and accelerate egg hatch. Climate change is predicted to increase drought incidents and produce more intense temperature patterns. Together, these environmental shifts may cause more frequent and severe spider mite infestations. Spider mite management is difficult as many commercially available acaricides are ineffective due to the development of resistance traits in field mite populations. Therefore, alternative approaches to suppress outbreaks are critically needed. Drought-tolerant plant hybrids alleviate the challenges of growing crops in water-limited environments; yet, it is unclear if drought-tolerant hybrids exposed to water stress affect mite outbreaks under these conditions. We conducted a greenhouse experiment to evaluate the effect of drought-tolerant corn hybrids on Banks grass mite [Oligonychus pratensis Banks (Acari: Tetranychidae)], a primary pest of corn, under optimal irrigation and water-stress irrigation. This was followed by a 2-yr field study investigating the effect of drought-tolerant corn hybrids exposed to the same irrigation treatments on Banks grass mite artificially infested on hybrids and resident spider mite populations. Results showed that water-stressed drought-tolerant hybrids had significantly lower Banks grass mite and resident spider mite populations than water-stressed drought-susceptible hybrids. Interestingly, water-stressed drought-tolerant hybrids had equal Banks grass mite populations to drought-susceptible and drought-tolerant hybrids under optimal irrigation. We posit that planting drought-tolerant hybrids may suppress spider mite outbreaks in water-challenged areas.

Generalist and Specialist Mite Herbivores Induce Similar Defense Responses in Maize and Barley but Differ in Susceptibility to Benzoxazinoids.

While substantial progress has been made in understanding defense responses of cereals to insect herbivores, comparatively little is known about responses to feeding by spider mites. Nevertheless, several spider mite species, including the generalist Tetranychus urticae and the grass specialist Oligonychus pratensis, cause damage on cereals such as maize and wheat, especially during drought stress. To understand defense responses of cereals to spider mites, we characterized the transcriptomic responses of maize and barley to herbivory by both mite species, and included a wounding control against which modulation of defenses could be tested. T. urticae and O. pratensis induced highly correlated changes in gene expression on both maize and barley. Within 2 h, hundreds of genes were upregulated, and thousands of genes were up- or downregulated after 24 h. In general, expression changes were similar to those induced by wounding, including for genes associated with jasmonic acid biosynthesis and signaling. Many genes encoding proteins involved in direct defenses, or those required for herbivore-induced plant volatiles, were strongly upregulated in response to mite herbivory. Further, biosynthesis genes for benzoxazinoids, which are specialized compounds of Poaceae with known roles in deterring insect herbivores, were induced in maize. Compared to chewing insects, spider mites are cell content feeders and cause grossly different patterns of tissue damage. Nonetheless, the gene expression responses of maize to both mite herbivores, including for phytohormone signaling pathways and for the synthesis of the benzoxazinoid 2-hydroxy-4,7-dimethoxy-1,4-benzoxazin-3-one glucoside, a known defensive metabolite against caterpillars, resembled those reported for a generalist chewing insect, Spodoptera exigua. On maize plants harboring mutations in several benzoxazinoid biosynthesis genes, T. urticae performance dramatically increased compared to wild-type plants. In contrast, no difference in performance was observed between mutant and wild-type plants for the specialist O. pratensis. Collectively, our data provide little evidence that maize and barley defense responses differentiate herbivory between T. urticae and O. pratensis. Further, our work suggests that the likely route to specialization for O. pratensis involved the evolution of a robust mechanism to cope with the benzoxazinoid defenses of its cereal hosts.

Combinations of plant water-stress and neonicotinoids can lead to secondary outbreaks of Banks grass mite (Oligonychus pratensis Banks).

Spider mites, a cosmopolitan pest of agricultural and landscape plants, thrive under hot and dry conditions, which could become more frequent and extreme due to climate change. Recent work has shown that neonicotinoids, a widely used class of systemic insecticides that have come under scrutiny for non-target effects, can elevate spider mite populations. Both water-stress and neonicotinoids independently alter plant resistance against herbivores. Yet, the interaction between these two factors on spider mites is unclear, particularly for Banks grass mite (Oligonychus pratensis; BGM). We conducted a field study to examine the effects of water-stress (optimal irrigation = 100% estimated evapotranspiration (ET) replacement, water stress = 25% of the water provided to optimally irrigated plants) and neonicotinoid seed treatments (control, clothianidin, thiamethoxam) on resident mite populations in corn (Zea mays, hybrid KSC7112). Our field study was followed by a manipulative field cage study and a parallel greenhouse study, where we tested the effects of water-stress and neonicotinoids on BGM and plant responses. We found that water-stress and clothianidin consistently increased BGM densities, while thiamethoxam-treated plants only had this effect when plants were mature. Water-stress and BGM herbivory had a greater effect on plant defenses than neonicotinoids alone, and the combination of BGM herbivory with the two abiotic factors increased the concentration of total soluble proteins. These results suggest that spider mite outbreaks by combinations of changes in plant defenses and protein concentration are triggered by water-stress and neonicotinoids, but the severity of the infestations varies depending on the insecticide active ingredient.

Developing a Degree-Day Model to Predict Billbug (Coleoptera: Curculionidae) Seasonal Activity in Utah and Idaho Turfgrass.

Billbugs are native pests of turfgrass throughout North America, primarily managed with preventive, calendar-based insecticide applications. An existing degree-day model (lower development threshold of 10°C, biofix 1 March) developed in the eastern United States for bluegrass billbug, Sphenophorus parvulus (Gyllenhal; Coleoptera: Curculionidae), may not accurately predict adult billbug activity in the western United States, where billbugs occur as a species complex. The objectives of this study were 1) to track billbug phenology and species composition in managed Utah and Idaho turfgrass and 2) to evaluate model parameters that best predict billbug activity, including those of the existing bluegrass billbug model. Tracking billbugs with linear pitfall traps at two sites each in Utah and Idaho, we confirmed a complex of three univoltine species damaging turfgrass consisting of (in descending order of abundance) bluegrass billbug, hunting billbug (Sphenophorus venatus vestitus Chittenden; Coleoptera: Curculionidae), and Rocky Mountain billbug (Sphenophorus cicatristriatus Fabraeus; Coleoptera: Curculionidae). This complex was active from February through mid-October, with peak activity in mid-June. Based on linear regression analysis, we found that the existing bluegrass billbug model was not robust in predicting billbug activity in Utah and Idaho. Instead, the model that best predicts adult activity of the billbug complex accumulates degree-days above 3°C after 13 January. This model predicts adult activity levels important for management within 11 d of observed activity at 77% of sites. In conjunction with outreach and cooperative networking, this predictive degree-day model may assist end users to better time monitoring efforts and insecticide applications against billbug pests in Utah and Idaho by predicting adult activity.

Pheromone Lure and Trap Color Affects Bycatch in Agricultural Landscapes of Utah.

Aerial traps, using combinations of color and attractive lures, are a critical tool for detecting and managing insect pest populations. Yet, despite improvements in trap efficacy, collection of nontarget species ("bycatch") plagues many insect pest surveys. Bycatch can influence survey effectiveness by reducing the available space for target species and increasing trap screening time, especially in areas where thousands of insects are captured as bycatch in a given season. Additionally, bycatch may negatively impact local nontarget insect populations, including beneficial predators and pollinators. Here, we tested the effect of pheromone lures on bycatch rates of Coccinellidae (Coleoptera), Apoidea (Hymenoptera), and nontarget Lepidoptera. Multicolored (primarily yellow and white) bucket traps containing a pheromone lure for capturing one of three survey target species, Spodoptera litura (F.), S. littoralis (Boisduval), or Helicoverpa armigera (Hübner), were placed in alfalfa and corn fields, and compared to multicolored traps without a pheromone lure. All-green traps with and without H. armigera lures were employed in a parallel study investigating the effect of lure and trap color on bycatch. Over 2,600 Coccinellidae representing seven species, nearly 6,400 bees in 57 species, and >9,000 nontarget moths in 17 genera were captured across 180 traps and seven temporal sampling events. Significant effects of lure and color were observed for multiple taxa. In general, nontarget insects were attracted to the H. armigera lure and multicolored trap, but further studies of trap color and pheromone lure specificity are needed to better understand these interactions and to minimize nontarget captures.

Biology and Management of Billbugs (Coleoptera: Curculionidae) in Turfgrass.

Billbugs (Coleoptera: Curculionidae: Sphenophorus spp.) are a complex of weevil pests affecting turfgrass throughout the United States. Billbug larvae cause damage by feeding in stems, on roots, and on the crowns of turf, causing severe discoloration and eventual plant death. Monitoring efforts have focused on nondestructive pitfall sampling of ground-active billbug adults and on destructive sampling using soil cores for larval stages in the soil. Given the cryptic nature of the susceptible larval stages, billbugs are typically managed by preventive applications of long-residual, systemic insecticides, including neonicotinoids and anthranilic diamides. Despite knowledge of effective management practices including pest-resistant turf varieties, irrigation management, and microbial controls that contribute to an IPM approach, billbug management continues to rely heavily on prophylactic synthetic insecticides. This review will summarize the identification and biology of billbugs and strategies for their management.

Distribution and Habitat of Ixodes pacificus (Acari: Ixodidae) and Prevalence of Borrelia burgdorferi in Utah.

Knowledge about the distribution and abundance of the western black-legged tick, Ixodes pacificus Cooley and Kohls, in Utah is limited. Recent concerns over tick-borne diseases in Utah, primarily Lyme disease, have reinvigorated the need to understand the distribution and habitats favored by this tick species. We surveyed 157 sites throughout Utah to examine the distribution, abundance, and habitat of I. pacificus. In total, 343 adult ticks were collected from 2011 to 2013. Specifically, 119 I. pacificus, 217 Dermacentor andersoni Stiles, six D. albipictus Packard, and one D. hunteri Bishopp were collected. Overall, tick abundance was relatively low in the areas evaluated in Utah. I. pacificus collections were limited to sites above 1700 m. Ninety-two percent of I. pacificus were captured in the Sheeprock Mountains in Tooele County. I. pacificus positive collection sites were characterized by Gambel oak (Quercus gambelii Nuttall), juniper (Juniperus spp. L.), big sagebrush (Artemisia tridentata Nuttall) and black sagebrush (A. nova Nelson), and mixed grass habitat. All I. pacificus ticks were tested for the presence of Borrelia burgdorferi (Johnson, Schmid, Hyde, Steigerwalt, and Brenner, sensu stricto) using real-time PCR. All ticks tested negative for B. burgdorferi. The likelihood of encountering I. pacificus and acquiring Lyme disease in the areas evaluated in Utah is considerably low due to low tick abundance and limited distribution, as well as low prevalence (or absence) of B. burgdorferi in Utah.

Stem nematode counteracts plant resistance of aphids in alfalfa, Medicago sativa.

Plants are exploited by a diverse community of insect herbivores and phytopathogens that interact indirectly through plant-mediated interactions. Generally, plants are thought to respond to insects and pathogens through different defensive signaling pathways. As plants are selected for resistance to one phytophagous organism type (insect vs. pathogen) in managed systems, it is not clear how this selection may affect community interactions. This study examined the effect of nematode-resistant varieties on aphid (Acyrthosiphon pisum) suppression, and then determined how infection by the stem nematode, Ditylenchus dipsaci, mediated ecological effects on aphids and on plant defense proteins. Four alfalfa (Medicago sativa) varieties were selected with resistance to nematodes only (+,-), aphids only (-,+), nematodes and aphids (+,+), and susceptibility to nematodes and aphids (-,-). Field and greenhouse experiments were conducted to isolate the effect of nematode infection and aphid abundance on each variety. We found that varieties resistant to nematode, regardless of aphid resistance, had the lowest aphid counts, suggesting possible cross-resistance. Aphid abundance, however, increased when plants were exposed to nematodes. Resistant varieties were associated with elevated saponins but these compounds were not affected by insect or pathogen feeding. Concentrations of peroxidases and trypsin inhibitors, however, were increased in nematode resistant varieties when exposed to nematodes and aphids, respectively. The patterns of plant defense were variable, and a combination of resistance traits and changes in nutrient availability may drive positive interactions between nematodes and aphids aboveground.

Scared sick? Predator-pathogen facilitation enhances exploitation of a shared resource.

Resource use generally increases with greater consumer diversity, an effect often attributed to resource partitioning. Pathogens and predators are two classes of consumer that exhibit differences in ecologically important traits (e.g., size, resource acquisition strategy, foraging location) that could lead to complementary effects on shared prey/hosts. To examine this possibility, we manipulated diversity among a community of predators and pathogens that together attack an herbivorous beetle, Leptinotarsa decemlineata, and measured resulting effects on herbivore suppression and resulting plant damage. We found that herbivore mortality increased, and plant damage decreased, when more natural enemy species were present. However, closer examination revealed that it was the pairing of predator with pathogen species, rather than greater biodiversity per se, that strengthened herbivore suppression. In this community, predators occur aboveground, attacking herbivore juvenile stages feeding on plant foliage, whereas pathogens occur belowground and attack herbivores pupating in the soil. In a subsequent field experiment, we tracked the emergence of predator-pathogen complementarity throughout the course of beetle development. We found that herbivores exposed to predators aboveground were more susceptible to subsequent pathogen infection belowground, consistent with our observation in the laboratory that predator exposure weakens beetles' immune response. Thus, predators facilitated resource capture by pathogens, perhaps reflecting an inherent conflict for the herbivore in allocating energetic resources toward anti-predator vs. anti-pathogen defenses. Our results suggest that predator-pathogen combinations were particularly taxing not because the consumer species partitioned resources among themselves, but instead because they enforced the partitioning of resources internal to prey/host individuals.