Predicting and Controlling Spillover in Multispecies Disease Transmission Networks: Steady-State Analysis.

AbstractIn multispecies disease systems, pathogen spillover from a "reservoir community" can maintain disease in a "sink community" where it would otherwise die out. We develop and analyze models for spillover and disease spread in sink communities, focusing on questions of control: which species or transmission links are the most important to target to reduce the disease impact on a species of concern? Our analysis focuses on steady-state disease prevalence, assuming that the timescale of interest is long compared with that of disease introduction and establishment in the sink community. We identify three regimes as the sink community R0 scales from 0 to 1. Up to R0≈0.3, overall infection patterns are dominated by direct exogenous infections and one-step subsequent transmission. For R0≈1, infection patterns are characterized by dominant eigenvectors of a force-of-infection matrix. In between, additional network details can be important; we derive and apply general sensitivity formulas that identify particularly important links and species.

A Time for Every Purpose: Using Time-Dependent Sensitivity Analysis to Help Understand and Manage Dynamic Ecological Systems.

AbstractSensitivity analysis is often used to help understand and manage ecological systems by assessing how a constant change in vital rates or other model parameters might affect the management outcome. This allows the manager to identify the most favorable course of action. However, realistic changes are often localized in time-for example, a short period of culling leads to a temporary increase in the mortality rate over the period. Hence, knowing when to act may be just as important as knowing what to act on. In this article, we introduce the method of time-dependent sensitivity analysis (TDSA) that simultaneously addresses both questions. We illustrate TDSA using three case studies: transient dynamics in static disease transmission networks, disease dynamics in a reservoir species with seasonal life history events, and endogenously driven population cycles in herbivorous invertebrate forest pests. We demonstrate how TDSA often provides useful biological insights, which are understandable on hindsight but would not have been easily discovered without the help of TDSA. However, as a caution, we also show how TDSA can produce results that mainly reflect uncertain modeling choices and are therefore potentially misleading. We provide guidelines to help users maximize the utility of TDSA while avoiding pitfalls.

Pathogen transport amplifies or dilutes disease transmission depending on the host dose-response relationship.

Pathogen transport by biotic or abiotic processes (e.g. mechanical vectors, wind, rain) can increase disease transmission by creating more opportunities for host exposure. But transport without replication has an inherent trade-off, that creating new venues for exposure decreases the average pathogen abundance at each venue. The host dose-response relationship is therefore required to correctly assess infection risk. We model and analyse two examples-biotic mechanical vectors in plant-pollinator networks, and abiotic-facilitated long-distance pathogen dispersal-to illustrate how oversimplifying the dose-response relationship can lead to incorrect epidemiological predictions. When the minimum infective dose is high, mechanical vectors amplify disease transmission less than suggested by simple compartment models, and may even dilute transmission. When long-distance dispersal leads to infrequent large exposures, models that assume a linear force of infection can substantially under-predict the speed of epidemic spread. Our work highlights an important general interplay between dose-response relationships and pathogen transport.

Bumble bee (Bombus impatiens) survival, pollen usage, and reproduction are not affected by oxalate oxidase at realistic concentrations in American chestnut (Castanea dentata) pollen.

Transgenic American chestnut trees expressing a wheat gene for oxalate oxidase (OxO) can tolerate chestnut blight, but as with any new restoration material, they should be carefully evaluated before being released into the environment. Native pollinators such as bumble bees are of particular interest: Bombus impatiens use pollen for both a source of nutrition and a hive building material. Bees are regular visitors to American chestnut flowers and likely contribute to their pollination, so depending on transgene expression in chestnut pollen, they could be exposed to this novel source of OxO during potential restoration efforts. To evaluate the potential risk to bees from OxO exposure, queenless microcolonies of bumble bees were supplied with American chestnut pollen containing one of two concentrations of OxO, or a no-OxO control. Bees in microcolonies exposed to a conservatively estimated field-realistic concentration of OxO in pollen performed similarly to no-OxO controls; there were no significant differences in survival, bee size, pollen use, hive construction activity, or reproduction. A ten-fold increase in OxO concentration resulted in noticeable but non-significant decreases in some measures of pollen usage and reproduction compared to the no-OxO control. These effects are similar to what is often seen when naturally produced secondary metabolites are supplied to bees at unrealistically high concentrations. Along with the presence of OxO in many other environmental sources, these data collectively suggest that oxalate oxidase at field-realistic concentrations in American chestnut pollen is unlikely to present substantial risk to bumble bees.

Crithidia bombi can infect two solitary bee species while host survivorship depends on diet.

Pathogens and lack of floral resources interactively impair global pollinator health. However, epidemiological and nutritional studies aimed at understanding bee declines have historically focused on social species, with limited evaluations of solitary bees. Here, we asked whether Crithidia bombi, a trypanosomatid gut pathogen known to infect bumble bees, could infect the solitary bees Osmia lignaria (females) and Megachile rotundata (males), and whether nutritional stress influenced infection patterns and bee survival. We found that C. bombi was able to infect both solitary bee species, with 59% of O. lignaria and 29% of M. rotundata bees experiencing pathogen replication 5­11 days following inoculation. Moreover, access to pollen resulted in O. lignaria living longer, although it did not influence M. rotundata survival. Access to pollen did not affect infection probability or resulting pathogen load in either species. Similarly, inoculating with the pathogen did not drive survival patterns in either species during the 5­11-day laboratory assays. Our results demonstrate that solitary bees can be hosts of a known bumble bee pathogen, and that access to pollen is an important contributing factor for bee survival, thus expanding our understanding of factors contributing to solitary bee health.

Landscape simplification shapes pathogen prevalence in plant-pollinator networks.

Species interaction networks, which play an important role in determining pathogen transmission and spread in ecological communities, can shift in response to agricultural landscape simplification. However, we know surprisingly little about how landscape simplification-driven changes in network structure impact epidemiological patterns. Here, we combine mathematical modelling and data from eleven bipartite plant-pollinator networks observed along a landscape simplification gradient to elucidate how changes in network structure shape disease dynamics. Our empirical data show that landscape simplification reduces pathogen prevalence in bee communities via increased diet breadth of the dominant species. Furthermore, our empirical data and theoretical model indicate that increased connectance reduces the likelihood of a disease outbreak and decreases variance in prevalence among bee species in the community, resulting in a dilution effect. Because infectious diseases are implicated in pollinator declines worldwide, a better understanding of how land use change impacts species interactions is therefore critical for conserving pollinator health.

Trait-Based Modeling of Multihost Pathogen Transmission: Plant-Pollinator Networks.

Epidemiological models for multihost pathogen systems often classify individuals taxonomically and use species-specific parameter values, but in species-rich communities that approach may require intractably many parameters. Trait-based epidemiological models offer a potential solution but have not accounted for within-species trait variation or between-species trait overlap. Here we propose and study trait-based models with host and vector communities represented as trait distributions without regard to species identity. To illustrate this approach, we develop susceptible-infectious-susceptible models for disease spread in plant-pollinator networks with continuous trait distributions. We model trait-dependent contact rates in two common scenarios: nested networks and specialized plant-pollinator interactions based on trait matching. We find that disease spread in plant-pollinator networks is impacted the most by selective pollinators, universally attractive flowers, and cospecialized plant-pollinator pairs. When extreme pollinator traits are rare, pollinators with common traits are most important for disease spread, whereas when extreme flower traits are rare, flowers with uncommon traits impact disease spread the most. Greater nestedness and specialization both typically promote disease persistence. Given recent pollinator declines caused in part by pathogens, we discuss how trait-based models could inform conservation strategies for wild and managed pollinators. Furthermore, while we have applied our model to pollinators and pathogens, its framework is general and can be transferred to any kind of species interactions in any community.

Bee pathogen transmission dynamics: deposition, persistence and acquisition on flowers.

Infectious diseases are a primary driver of bee decline worldwide, but limited understanding of how pathogens are transmitted hampers effective management. Flowers have been implicated as hubs of bee disease transmission, but we know little about how interspecific floral variation affects transmission dynamics. Using bumblebees ( Bombus impatiens), a trypanosomatid pathogen ( Crithidia bombi) and three plant species varying in floral morphology, we assessed how host infection and plant species affect pathogen deposition on flowers, and plant species and flower parts impact pathogen survival and acquisition at flowers. We found that host infection with Crithidia increased defaecation rates on flowers, and that bees deposited faeces onto bracts of Lobelia siphilitica and Lythrum salicaria more frequently than onto Monarda didyma bracts . Among flower parts, bracts were associated with the lowest pathogen survival but highest resulting infection intensity in bee hosts. Additionally, we found that Crithidia survival across flower parts was reduced with sun exposure. These results suggest that efficiency of pathogen transmission depends on where deposition occurs and the timing and place of acquisition, which varies among plant species and environmental conditions. This information could be used for development of wildflower mixes that maximize forage while minimizing disease spread.

Disease where you dine: plant species and floral traits associated with pathogen transmission in bumble bees.

Hotspots of disease transmission can strongly influence pathogen spread. Bee pathogens may be transmitted via shared floral use, but the role of plant species and floral trait variation in shaping transmission dynamics is almost entirely unexplored. Given the importance of pathogens for the decline of several bee species, understanding whether and how plant species and floral traits affect transmission could give us important tools for predicting which plant species may be hotspots for disease spread. We assessed variation in transmission via susceptibility (probability of infection) and mean intensity (cell count of infected bees) of the trypanosomatid gut pathogen Crithidia bombi to uninfected Bombus impatiens workers foraging on 14 plant species, and assessed the role of floral traits, bee size and foraging behavior on transmission. We also conducted a manipulative experiment to determine how the number of open flowers affected transmission on three plant species, Penstemon digitalis, Monarda didyma, and Lythrum salicaria. Plant species differed fourfold in the overall mean abundance of Crithidia in foraging bumble bees (mean including infected and uninfected bees). Across plant species, bee susceptibility and mean intensity increased with the number of reproductive structures per inflorescence (buds, flowers and fruits); smaller bees and those that foraged longer were also more susceptible. Trait-based models were as good or better than species-based models at predicting susceptibility and mean intensity based on AIC values. Surprisingly, floral size and morphology did not significantly predict transmission across species. In the manipulative experiment, more open flowers increased mean pathogen abundance fourfold in Monarda, but had no effect in the other two plant species. Our results suggest that variation among plant species, through their influence on pathogen transmission, may shape bee disease dynamics. Given widespread investment in pollinator-friendly plantings to support pollinators, understanding how plant species affect disease transmission is important for recommending plant species that optimize pollinator health.

Landscape predictors of pathogen prevalence and range contractions in US bumblebees.

Several species of bumblebees have recently experienced range contractions and possible extinctions. While threats to bees are numerous, few analyses have attempted to understand the relative importance of multiple stressors. Such analyses are critical for prioritizing conservation strategies. Here, we describe a landscape analysis of factors predicted to cause bumblebee declines in the USA. We quantified 24 habitat, land-use and pesticide usage variables across 284 sampling locations, assessing which variables predicted pathogen prevalence and range contractions via machine learning model selection techniques. We found that greater usage of the fungicide chlorothalonil was the best predictor of pathogen (Nosema bombi) prevalence in four declining species of bumblebees. Nosema bombi has previously been found in greater prevalence in some declining US bumblebee species compared to stable species. Greater usage of total fungicides was the strongest predictor of range contractions in declining species, with bumblebees in the northern USA experiencing greater likelihood of loss from previously occupied areas. These results extend several recent laboratory and semi-field studies that have found surprising links between fungicide exposure and bee health. Specifically, our data suggest landscape-scale connections between fungicide usage, pathogen prevalence and declines of threatened and endangered bumblebees.

Compensatory mechanisms for ameliorating the fundamental trade-off between predator avoidance and foraging.

Most organisms face the problem of foraging and maintaining growth while avoiding predators. Typical animal responses to predator exposure include reduced feeding, elevated metabolism, and altered development rate, all of which can be beneficial in the presence of predators but detrimental in their absence. How then do animals balance growth and predator avoidance? In a series of field and greenhouse experiments, we document that the tobacco hornworm caterpillar, Manduca sexta, reduced feeding by 30-40% owing to the risk of predation by stink bugs, but developed more rapidly and gained the same mass as unthreatened caterpillars. Assimilation efficiency, extraction of nitrogen from food, and percent body lipid content all increased during the initial phase (1-3 d) of predation risk, indicating that enhanced nutritional physiology allows caterpillars to compensate when threatened. However, we report physiological costs of predation risk, including altered body composition (decreased glycogen) and reductions in assimilation efficiency later in development. Our findings indicate that hornworm caterpillars use temporally dynamic compensatory mechanisms that ameliorate the trade-off between predator avoidance and growth in the short term, deferring costs to a period when they are less vulnerable to predation.

Arranging the bouquet of disease: floral traits and the transmission of plant and animal pathogens.

Several floral microbes are known to be pathogenic to plants or floral visitors such as pollinators. Despite the ecological and economic importance of pathogens deposited in flowers, we often lack a basic understanding of how floral traits influence disease transmission. Here, we provide the first systematic review regarding how floral traits attract vectors (for plant pathogens) or hosts (for animal pathogens), mediate disease establishment and evolve under complex interactions with plant mutualists that can be vectors for microbial antagonists. Attraction of floral visitors is influenced by numerous phenological, morphological and chemical traits, and several plant pathogens manipulate floral traits to attract vectors. There is rapidly growing interest in how floral secondary compounds and antimicrobial enzymes influence disease establishment in plant hosts. Similarly, new research suggests that consumption of floral secondary compounds can reduce pathogen loads in animal pollinators. Given recent concerns about pollinator declines caused in part by pathogens, the role of floral traits in mediating pathogen transmission is a key area for further research. We conclude by discussing important implications of floral transmission of pathogens for agriculture, conservation and human health, suggesting promising avenues for future research in both basic and applied biology.

High pesticide exposure and risk to bees in pollinator plantings adjacent to conventionally managed blueberry fields.

Wildflower plantings adjacent to agricultural fields provide diverse floral resources and nesting sites for wild bees. However, their proximity to pest control activities in the crop may result in pesticide exposure if pesticides drift into pollinator plantings. To quantify pesticide residues in pollinator plantings, we sampled flowers and soil from pollinator plantings and compared them to samples from unenhanced field margins and crop row middles. At conventionally managed farms, flowers from pollinator plantings had similar exposure profiles to those from unenhanced field margins or crop row middles, with multiple pesticides and high and similar risk quotient (RQ) values (with pollinator planting RQ: 3.9; without pollinator planting RQ: 4.0). Whereas samples from unsprayed sites had significantly lower risk (RQ: 0.005). Soil samples had overall low risk to bees. Additionally, we placed bumble bee colonies (Bombus impatiens) in field margins of crop fields with and without pollinator plantings and measured residues in bee-collected pollen. Pesticide exposure was similar in pollen from sites with or without pollinator plantings, and risk was generally high (with pollinator planting RQ: 0.5; without pollinator planting RQ: 1.1) and not significant between the two field types. Risk was lower at sites where there was no pesticide activity (RQ: 0.3), but again there was no significant difference between management types. The insecticide phosmet, which is used on blueberry farms for control of Drosophila suzukii, accounted for the majority of elevated risk. Additionally, analysis of pollen collected by bumble bees found no significant difference in floral species richness between sites with or without pollinator plantings. Our results suggest that pollinator plantings do not reduce pesticide risk and do not increase pollen diversity collected by B. impatiens, further highlighting the need to reduce exposure through enhanced IPM adoption, drift mitigation, and removal of attractive flowering weeds prior to insecticide applications.

Field agrochemical exposure impacts locomotor activity in wild bumblebees.

Agricultural intensification has been identified as one of the key causes of global insect biodiversity losses. These losses have been further linked to the widespread use of agrochemicals associated with modern agricultural practices. Many of these chemicals are known to have negative sublethal effects on commercial pollinators, such as managed honeybees and bumblebees, but less is known about the impacts on wild bees. Laboratory-based studies with commercial pollinators have consistently shown that pesticide exposure can impact bee behavior, with cascading effects on foraging performance, reproductive success, and pollination services. However, these studies typically assess only one chemical, neglecting the complexity of real-world exposure to multiple agrochemicals and other stressors. In the summer of 2020, we collected wild-foraging workers of the common eastern bumblebee, Bombus impatiens, from five squash (Cucurbita) agricultural sites (organic and conventional farms), selected to represent a range of agrochemical, including neonicotinoid insecticide, use. For each bee, we measured two behaviors relevant to foraging success and previously shown to be impacted by pesticide exposure: sucrose responsiveness and locomotor activity. Following behavioral testing, we used liquid chromatography-tandem mass spectrometry (LC-MS/MS) chemical analysis to detect and quantify the presence of 92 agrochemicals in each bumblebee. Bees collected from our sites did not vary in pesticide exposure as expected. While we found a limited occurrence of neonicotinoids, two fungicides (azoxystrobin and difenoconazole) were detected at all sites, and the pesticide synergist piperonyl butoxide (PBO) was present in all 123 bees. We found that bumblebees that contained higher levels of PBO were less active, and this effect was stronger for larger bumblebee workers. While PBO is unlikely to be the direct cause of the reduction in bee activity, it could be an indicator of exposure to pyrethroids and/or other insecticides that we were unable to directly quantify, but which PBO is frequently tank-mixed with during pesticide applications on crops. We did not find a relationship between agrochemical exposure and bumblebee sucrose responsiveness. To our knowledge, this is the first evidence of a sublethal behavioral impact of agrochemical exposure on wild-foraging bees.

Acute toxicity of the fungicide captan to honey bees and mixed evidence for synergism with the insecticide thiamethoxam.

Honey bees are commonly co-exposed to pesticides during crop pollination, including the fungicide captan and neonicotinoid insecticide thiamethoxam. We assessed the impact of exposure to these two pesticides individually and in combination, at a range of field-realistic doses. In laboratory assays, mortality of larvae treated with captan was 80-90% greater than controls, dose-independent, and similar to mortality from the lowest dose of thiamethoxam. There was evidence of synergism (i.e., a non-additive response) from captan-thiamethoxam co-exposure at the highest dose of thiamethoxam, but not at lower doses. In the field, we exposed whole colonies to the lowest doses used in the laboratory. Exposure to captan and thiamethoxam individually and in combination resulted in minimal impacts on population growth or colony mortality, and there was no evidence of synergism or antagonism. These results suggest captan and thiamethoxam are each acutely toxic to immature honey bees, but whole colonies can potentially compensate for detrimental effects, at least at the low doses used in our field trial, or that methodological differences of the field experiment impacted results (e.g., dilution of treatments with natural pollen). If compensation occurred, further work is needed to assess how it occurred, potentially via increased queen egg laying, and whether short-term compensation leads to long-term costs. Further work is also needed for other crop pollinators that lack the social detoxification capabilities of honey bee colonies and may be less resilient to pesticides.

Plant genotypic diversity reduces the rate of consumer resource utilization.

While plant species diversity can reduce herbivore densities and herbivory, little is known regarding how plant genotypic diversity alters resource utilization by herbivores. Here, we show that an invasive folivore--the Japanese beetle (Popillia japonica)--increases 28 per cent in abundance, but consumes 24 per cent less foliage in genotypic polycultures compared with monocultures of the common evening primrose (Oenothera biennis). We found strong complementarity for reduced herbivore damage among plant genotypes growing in polycultures and a weak dominance effect of particularly resistant genotypes. Sequential feeding by P. japonica on different genotypes from polycultures resulted in reduced consumption compared with feeding on different plants of the same genotype from monocultures. Thus, diet mixing among plant genotypes reduced herbivore consumption efficiency. Despite positive complementarity driving an increase in fruit production in polycultures, we observed a trade-off between complementarity for increased plant productivity and resistance to herbivory, suggesting costs in the complementary use of resources by plant genotypes may manifest across trophic levels. These results elucidate mechanisms for how plant genotypic diversity simultaneously alters resource utilization by both producers and consumers, and show that population genotypic diversity can increase the resistance of a native plant to an invasive herbivore.

Pesticide contamination of beeswax from managed honey bee colonies in New York State.

The New York State (NYS) beekeeping industry generated >$11M worth of honey in 2020 and >$300M in pollination services to agriculture annually. Bees are frequently exposed to pesticides through foraging and husbandry practices. Lipophilic pesticides can remain in beeswax for extended periods. We analyzed for pesticides in wax comb samples collected from NYS apiaries at the end of the growing season, comparing residue numbers and concentrations among beekeepers of different operation scales: commercial beekeepers (>300 colonies), sideliners (50-299 colonies), and hobbyists (<50 colonies). We analyzed samples collected from 72 managed honey bee colonies for 92 insecticides, herbicides, and fungicides by liquid chromatography-tandem mass spectrometry. Pesticides were detected in all samples and included 34 fungicides, 33 insecticides, and 22 herbicides. Each wax sample contained 7-35 different residues (x¯ = 17.8 residues). Wax from colonies managed by commercial beekeepers contained the most residues (x¯ = 21.9 residues), hobbyists were second (x¯ = 16.3 residues), and sideliners had the fewest (x¯ = 11.7 residues). Nearly all wax samples (98.6%) contained the pesticide synergist piperonyl butoxide, most samples (86%) contained common varroacides used to control honey bee parasites, including coumaphos and amitraz breakdown products, and 93.1% contained the fungicide difenoconazole. We detected 34 fungicides, 7 of which were found in 50% or more of the samples. We detected 22 herbicides. We found pesticide contamination of beeswax to be common, with commercial beekeepers experiencing the greatest contamination.

A time for every purpose: using time-dependent sensitivity analysis to help understand and manage dynamic ecological systems.

Sensitivity analysis is often used to help understand and manage ecological systems, by assessing how a constant change in vital rates or other model parameters might affect the management outcome. This allows the manager to identify the most favorable course of action. However, realistic changes are often localized in time-for example, a short period of culling leads to a temporary increase in the mortality rate over the period. Hence, knowing when to act may be just as important as knowing what to act upon. In this article, we introduce the method of time-dependent sensitivity analysis (TDSA) that simultaneously addresses both questions. We illustrate TDSA using three case studies: transient dynamics in static disease transmission networks, disease dynamics in a reservoir species with seasonal life-history events, and endogenously-driven population cycles in herbivorous invertebrate forest pests. We demonstrate how TDSA often provides useful biological insights, which are understandable on hindsight but would not have been easily discovered without the help of TDSA. However, as a caution, we also show how TDSA can produce results that mainly reflect uncertain modeling choices and are therefore potentially misleading. We provide guidelines to help users maximize the utility of TDSA while avoiding pitfalls.

Wild bees are exposed to low levels of pesticides in urban grasslands and community gardens.

Globally documented wild bee declines threaten sustainable food production and natural ecosystem functioning. Urban environments are often florally abundant, and consequently can contain high levels of pollinator diversity compared with agricultural environments. This has led to the suggestion that urban environments are an increasingly important habitat for pollinators. However, pesticides, such as commercial bug sprays, have a range of lethal and sub-lethal impacts on bees and are widely available for public use, with past work indicating that managed bees (honeybees and bumblebees) are exposed to a range of pesticides in urban environments. Despite this, we still have a poor understanding of (i) whether wild bees foraging in urban environments are exposed to pesticides and (ii) if exposure differs between genera. Here we assessed pesticide exposure in 8 bee genera foraging across multiple urban landscapes. We detected 13 different pesticides, some at concentrations known to have sub-lethal impacts on pollinators. Both the likelihood of pesticides being detected, and the concentrations observed, were higher for larger bees, likely due to their greater foraging ranges. Our results suggest that restricting agrochemical use in urban environments, where the economic benefits are limited, is a simple way to reduce anthropogenic stress on wild bees.

Relationships between arthropod richness, evenness, and diversity are altered by complementarity among plant genotypes.

Biodiversity is quantified via richness (e.g., the number of species), evenness (the relative abundance distribution of those species), or proportional diversity (a combination of richness and evenness, such as the Shannon index, H'). While empirical studies show no consistent relationship between these aspects of biodiversity within communities, the mechanisms leading to inconsistent relationships have received little attention. Here, using common evening primrose (Oenothera biennis) and its associated arthropod community, we show that relationships between arthropod richness, evenness, and proportional diversity are altered by plant genotypic richness. Arthropod richness increased with O. biennis genotypic richness due to an abundance-driven accumulation of species in response to greater plant biomass. Arthropod evenness and proportional diversity decreased with plant genotypic richness due to a nonadditive increase in abundance of a dominant arthropod, the generalist florivore/omnivore Plagiognathas politus (Miridae). The greater quantity of flowers and buds produced in polycultures-which resulted from positive complementarity among O. biennis genotypes-increased the abundance of this dominant insect. Using choice bioassays, we show that floral quality did not change in plant genotypic mixtures. These results elucidate mechanisms for how plant genotypic richness can modify relationships between arthropod richness, evenness, and proportional diversity. More broadly, our results suggest that trophic interactions may be a previously underappreciated factor controlling relationships between these different aspects of biodiversity.