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Biological control has been effectively exploited by mankind since 300 CE. By promoting the natural regulation of pests, weeds, and diseases, it produces societal benefits at the food-environment-health nexus. Here we scrutinize biological control endeavours and their social-ecological outcomes through a holistic 'One-Health' lens, recognizing that the health of humans, animals, plants, and the wider environment are linked and interdependent. Evidence shows that biological control generates desirable outcomes within all One Health dimensions, mitigating global change issues such as chemical pollution, biocide resistance, biodiversity loss, and habitat destruction. Yet, its cross-disciplinary achievements remain underappreciated. To remedy this, we advocate a systems-level, integrated approach to biological control research, policy, and practice. Framing biological control in a One Health context helps to unite medical and veterinary personnel, ecologists, conservationists and agricultural professionals in a joint quest for solutions to some of the most pressing issues in planetary health.

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The release of biological control agents has been an important means of controlling invasive species for over 150 years. While these releases have led to the sustainable control of over 250 invasive pest and weed species worldwide, a minority have caused environmental harm. A growing recognition of the risks of biological control led to a focus on risk assessment beginning in the 1990s along with a precipitous decline in releases. While this new focus greatly improved the safety of biological control, it came at the cost of lost opportunities to solve environmental problems associated with invasive species. A framework that incorporates benefits and risks of biological control is thus needed to understand the net environmental effects of biological control releases. We introduce such a framework, using native biodiversity as the common currency for both benefits and risks. The model is based on interactions among four categories of organisms: (1) the biological control agent, (2) the invasive species (pest or weed) targeted by the agent, (3) one or more native species that stand to benefit from the control of the target species, and (4) one or more native species that are at risk of being harmed by the released biological control agent. Conservation values of the potentially benefited and harmed native species are incorporated as well, and they are weighted according to three axes: vulnerability to extinction, the ecosystem services provided, and cultural significance. Further, we incorporate the potential for indirect risks to native species, which we consider will result mainly from the ecological process of agent enrichment that may occur if the agent exploits but does not control the target pest or weed. We illustrate the use of this framework by retrospectively analyzing the release of the vedalia beetle, Novius (= Rodolia) cardinalis, to control the cottony cushion scale, Icerya purchasi, in the Galapagos Islands. While the framework is particularly adaptable to biological control releases in natural areas, it can also be used in managed settings, where biological control protects native species through the reduction of pesticide use.

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The hymenopteran subfamily Charipinae (Cynipoidea: Figitidae) consist of a group of parasitic wasps that are exclusive hyperparasitoids of Hemipteran. The species boundaries in Charipinae have historically been unclear. While diagnostic morphological features have been established for the stepwise separation of species, it is recommended to confirm those limits using molecular data. Here, we focus on the genera Alloxysta Förster, 1869 and Phaenoglyphis Förster, 1869, both of which contain species that are hyperparasitoids of aphids. We sequenced three genes (mitochondrial COI and 16S rDNA, and nuclear ITS2 rDNA) from specimens that were identified as belonging to five species: Alloxysta brevis (Thomson, 1862), A. castanea (Hartig, 1841), A. ramulifera (Thomson, 1862), A. victrix (Westwood, 1833), and Phaenoglyphis villosa (Hartig, 1841). The phylogeny resulting from concatenating these genes supported the species status of the five morphologically identified taxa, with P. villosa nested within Alloxysta. Our study thus indicates that these molecular markers can successfully distinguish charipine species, and also indicates that the genera Alloxysta and Phaenoglyphis may be more closely related than previously hypothesized. We also present the first estimates of genetic distances for these species. Future studies that include more species, loci, and/or genomic data will complement our research and help determine species relationships within the Charipinae subfamily.

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Broad-spectrum insecticides are the main control measure of the invasive and economically damaging soybean aphid (Aphis glycines) in North America, although biological control by resident natural enemies can also greatly diminish population levels. One such natural enemy is the accidentally introduced Eurasian parasitoid Aphelinus certus (Hymenoptera: Aphelinidae), though its impact appears to be limited by low rates of parasitism early in the growing season. We tested the hypothesis that A. certus might experience high overwintering mortality. In the laboratory, we used thermocouple thermometry to measure the supercooling points of diapausing parasitoids and assessed parasitoid survival after exposure to ecologically relevant durations of low temperature. We found A. certus to be freeze-intolerant with a median supercooling point of -28°C. When exposed to temperatures of 0°C for up to 7 months, adults emerged only after exposures of at least 60 days and survival decreased with durations beyond 150 days. We also conducted in-field studies at sites from northern Minnesota to southern Iowa to determine if diapausing A. certus could overwinter above and below the snowpack. Survival was negatively correlated with increasing latitude and was greater for parasitoids placed on the ground than 1 meter off the ground, likely due to the warmer and stabler temperatures of the subnivean microclimate. Our results suggest that A. certus is capable of overwintering in the region inhabited by soybean aphid but may experience substantial mortality even under ideal conditions. Climate change is predicted to bring warmer, drier winters to the North American Midwest, with decreased depth and duration of snow cover, which may further reduce overwintering survival.

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Identifying traits that are associated with success of introduced natural enemies in establishing and controlling pest insects has occupied researchers and biological control practitioners for decades. Unfortunately, consistent general relationships have been difficult to detect, preventing a priori ranking of candidate biological control agents based on their traits. We summarise previous efforts and propose a series of potential explanations for the lack of clear patterns. We argue that the quality of current datasets is insufficient to detect complex trait-efficacy relationships and suggest several measures by which current limitations may be overcome. We conclude that efforts to address this elusive issue have not yet been exhausted and that further explorations are likely to be worthwhile.

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In Integrated Pest Management programs, insecticides are applied to agricultural crops when pest densities exceed a predetermined economic threshold. Under conditions of high natural enemy density, however, the economic threshold can be increased, allowing for fewer insecticide applications. These adjustments, called 'dynamic thresholds', allow farmers to exploit existing biological control interactions without economic loss. Further, the ability of natural enemies to disperse from, and subsequently immigrate into, insecticide-sprayed areas can affect their biological control potential. We develop a theoretical approach to incorporate both pest and natural enemy movement across field borders into dynamic thresholds and explore how these affect insecticide applications and farmer incomes. Our model follows a pest and its specialist natural enemy over one growing season. An insecticide that targets the pest also induces mortality of the natural enemy, both via direct toxicity and reduced resource pest densities. Pest and natural enemy populations recover after spraying through within-field reproduction and by immigration from neighboring unsprayed areas. The number of insecticide applications and per-season farmer revenues are calculated for economic thresholds that are either fixed (ignoring natural enemy densities) or dynamic (incorporating them). The model predicts that using dynamic thresholds always leads to reduced insecticide application. The benefit of dynamic thresholds in reducing insecticide use is highest when natural enemies rapidly recolonize sprayed areas, and when insecticide efficacy is low. We discuss real-life situations in which monitoring of natural enemies would substantially reduce insecticide use and other scenarios where the presence of beneficial organisms may lead to threshold modifications.

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The performance (development and reproduction) of generalist predators can vary greatly among the prey species that they use, and these differences can influence the ability of predatory insects to suppress pest populations. The aim of this study was to compare the performance of larvae of the green lacewing Chrysoperla rufilabris (Burmeister, 1839) by offering 16 species of aphids and by assessing the effects of each species on the survival, larval development time, prey consumption, pupal mass and egg load of adult Chr. rufilabris females taking aphid phylogeny into account. Chrysoperla rufilabris larvae preyed on individuals from all 16 aphid species, but complete development, adult emergence and egg load production were achieved only in seven species. As a general pattern, the best levels of performance were achieved for an aphid clade that includes the soybean aphid, Aphis glycines (Matsumara, 1917), and for a milkweed-feeding species, Myzocallis asclepiadis (Monell, 1879). We found significant phylogenetic clustering for most of the performance traits indicating the aspects of specialization in the diet breadth of Chr. rufilabris despite the fact that this species is considered a generalist aphid predator. These findings can help us to understand the interactions of this species in agroecological food webs, where it is commonly found, and provide insights into why natural, conservation biological control or augmentative releases may succeed or fail.

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Many parasites of seasonally available hosts must persist through times of the year when hosts are unavailable. In tropical environments, host availability is often linked to rainfall, and adaptations of parasites to dry periods remain understudied. The bird-parasitic fly Philornis downsi has invaded the Galapagos Islands and is causing high mortality of Darwin's finches and other bird species, and the mechanisms by which it was able to invade the islands are of great interest to conservationists. In the dry lowlands, this fly persists over a seven-month cool season when availability of hosts is very limited. We tested the hypothesis that adult flies could survive from one bird-breeding season until the next by using a pterin-based age-grading method to estimate the age of P. downsi captured during and between bird-breeding seasons. This study showed that significantly older flies were present towards the end of the cool season, with ~ 5% of captured females exhibiting estimated ages greater than seven months. However, younger flies also occurred during the cool season suggesting that some fly reproduction occurs when host availability is low. We discuss the possible ecological mechanisms that could allow for such a mixed strategy.

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Seed coating ('seed treatment') is the leading delivery method of neonicotinoid insecticides in major crops such as soybean, wheat, cotton and maize. However, this prophylactic use of neonicotinoids is widely discussed from the standpoint of environmental costs. Growing soybean plants from neonicotinoid-coated seeds in field, we demonstrate that soybean aphids (Aphis glycines) survived the treatment, and excreted honeydew containing neonicotinoids. Biochemical analyses demonstrated that honeydew excreted by the soybean aphid contained substantial concentrations of neonicotinoids even one month after sowing of the crop. Consuming this honeydew reduced the longevity of two biological control agents of the soybean aphid, the predatory midge Aphidoletes aphidimyza and the parasitic wasp Aphelinus certus. These results have important environmental and economic implications because honeydew is the main carbohydrate source for many beneficial insects in agricultural landscapes.

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Interactions that shape parasitoid host ranges occur within the context of both host and parasitoid phylogenetic history. While host-associated speciation of parasitoids can lead to increased host specificity, it can also lead to a broadening of host range through radiation onto a new group of host species. In both cases, sister-species of parasitoids may have widely divergent host ranges. But how should host range be estimated? Traditional views of host ranges as simple lists of species have given way to analyses that can detect host phylogenetic signal. Host relatedness can also be codified into useful indices that reflect the phylogenetic breadth of host range. All of these considerations have important implications for biological control, particularly in the realm of risk assessment.

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Parasitoids used as biological control agents often parasitize more than a single host species and these hosts tend to vary in suitability for offspring development. The population dynamics of parasitoids and hosts may be altered by these interactions, with outcomes dependent on the levels of suitability and acceptance of both host species. Parasitism of individuals of an unsuitable host species may indirectly increase populations of a suitable host species if eggs laid into unsuitable hosts do not develop into adult parasitoids. In this case, the unsuitable host is acting as an egg sink for parasitoids and this can reduce parasitism of suitable hosts under conditions of egg limitation. We studied parasitoid-mediated indirect interactions between two aphid hosts, Aphis glycines (the soybean aphid) and A. nerii (the milkweed, or oleander aphid), sharing the parasitoid Aphelinus certus. While both of these aphid species are accepted by A. certus, soybean aphid is a much more suitable host than milkweed aphid is. We observed a drastic reduction of parasitoid offspring production (45%) on the suitable host in the presence of the unsuitable host in microcosm assays. Aphelinus certus females laid eggs into the unsuitable hosts (Aphis nerii) in the presence of the suitable host leading to egg and/or time limitation and reduced fitness. The impact of these interactions on the equilibrium population sizes of the three interacting species was analyzed using a consumer-resource modeling approach. Both the results from the laboratory experiment and the modeling approaches identified apparent predation between soybean aphid and milkweed aphid, in which milkweed aphid acts as a sink for parasitoid eggs leading to an increase in the soybean aphid population. The presence of soybean aphids had the opposite effect on milkweed aphid populations as it supported increases in parasitoid abundance and thus reduced the fitness and abundance of this aphid species.

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Domestication disconnects an animal from its natural environment and diet, imposing changes in the attendant microbial community. We examine these changes in Philornis downsi (Muscidae), an invasive parasitic fly of land birds in the Galapagos Islands. Using a 16S rDNA profiling approach we studied the microbiome of larvae and adults of wild and laboratory-reared populations. These populations diverged in their microbiomes, significantly more so in larval than in adult flies. In field-collected second-instar larvae, Klebsiella (70.3%) was the most abundant taxon, while in the laboratory Ignatzschineria and Providencia made up 89.2% of the community. In adults, Gilliamella and Dysgonomonas were key members of the core microbiome of field-derived females and males but had no or very low representation in the laboratory. Adult flies harbour sex-specific microbial consortia in their gut, as male core microbiomes were significantly dominated by Klebsiella. Thus, P. downsi microbiomes are dynamic and shift correspondingly with life cycle and diet. Sex-specific foraging behaviour of adult flies and nest conditions, which are absent in the laboratory, may contribute to shaping distinct larval, and adult male and female microbiomes. We discuss these findings in the context of microbe-host co-evolution and the implications for control measures.

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The Avian Vampire Fly, Philornis downsi, has invaded the Galapagos Islands, where it causes high mortality of endemic and native landbird species, including most species of Darwin's finches. Control methods are under development, but key information is missing about the reproductive biology of P. downsi and the behavior of flies in and near nests of their hosts. We used external and internal nest cameras to record the behavior of P. downsi adults within and outside nests of the Galapagos Flycatcher, Myiarchus magnirostris, throughout all stages of the nesting cycle. These recordings showed that P. downsi visited flycatcher nests throughout the day with higher fly activity during the nestling phase during vespertine hours. The observations also revealed that multiple P. downsi individuals can visit nests concurrently, and that there are some interactions among these flies within the nest. Fly visitation to nests occurred significantly more often while parent birds were away from the nest than in the nest, and this timing appears to be a strategy to avoid predation by parent birds. We report fly mating behavior outside the nest but not in the nest cavity. We discuss the relevance of these findings for the adaptive forces shaping P. downsi life history strategies as well as rearing and control measures. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s10905-021-09789-7.

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Permethrin is increasingly used for parasite control in bird nests, including nests of threatened passerines. We present the first formal evaluation of the effects of continued permethrin exposure on the reproductive success and liver function of a passerine, the zebra finch (Taeniopygia guttata), for two generations. We experimentally treated all nest material with a 1% permethrin solution or a water control and provided the material to breeding finches for nest building. The success of two consecutive clutches produced by the parental generation and one clutch produced by first-generation birds were tracked. Finches in the first generation were able to reproduce and fledge offspring after permethrin exposure, ruling out infertility. Permethrin treatment had no statistically significant effect on the number of eggs laid, number of days from clutch initiation to hatching, egg hatch rate, fledgling mass or nestling sex ratio in either generation. However, treating nest material with permethrin significantly increased the number of hatchlings in the first generation and decreased fledgling success in the second generation. Body mass for hatchlings exposed to permethrin was lower than for control hatchlings in both generations, but only statistically significant for the second generation. For both generations, an interaction between permethrin treatment and age significantly affected nestling growth. Permethrin treatment had no effect on liver function for any generation. Permethrin was detected inside 6 of 21 exposed, non-embryonated eggs (28.5% incidence; range: 693-4781 ng of permethrin per gram of dry egg mass). Overall, results from exposing adults, eggs and nestlings across generations to permethrin-treated nest material suggest negative effects on finch breeding success, but not on liver function. For threatened bird conservation, the judicious application of this insecticide to control parasites in nests can result in lower nestling mortality compared to when no treatment is applied. Thus, permethrin treatment benefits may outweigh its sub-lethal effects.

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Parasitoid lifespan is influenced by nutrient availability, thus the lifespan of parasitoids that rely on their hosts for nutritional resources (either via host feeding or by consuming honeydew) should vary with host density. We assessed the survival and reproduction of one such species, Aphelinus certus-a parasitoid of the soybean aphid, Aphis glycines-over a range of host densities using a laboratory assay. We found a positive, asymptotic relationship between host density and the lifespan and fecundity of A. certus that was supported by a traditional survivorship analysis as well as a logistic model. Parasitoids from this assay were also used to develop a wing wear index relating setae damage to parasitoid age. This index was used to estimate the life expectancy of field-collected parasitoids, which was shorter than the life expectancy of laboratory-reared female parasitoids. Finally, host-density-dependent parasitoid lifespan was incorporated into a coupled-equations matrix population model that revealed that decreasing the degree of host density dependence leads to higher equilibrium host densities and changes in the quality of equilibrium (e.g. stable limit cycles). These results detail the relatively unstudied phenomenon of host-density-dependent parasitoid lifespan and suggest that differences between laboratory- and field-determined parasitoid life expectancy have important implications for population dynamics and the biological control of insects.

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Interspecific competition for limited resources can drive ecological specialization and trait expression. Organisms released from intense competition may exploit a broader range of resources, but if reunited with stronger competitors, survivorship may depend on foraging behaviors that reduce competition. We compared the host selection behavior of the parasitoid Cotesia glomerata from two North American populations that differ in their association with Cotesia rubecula, a superior competitor. Both parasitoids originate from Europe and attack the imported cabbageworm (a.k.a. small cabbage white) Pieris rapae, but C. glomerata was introduced into North America almost a century before C. rubecula. After re-association in North America, C. rubecula has displaced C. glomerata in several regions, but not in other regions. Host selection was measured in female C. glomerata from Maryland (MD) where it coexists with C. rubecula, and in conspecifics from Colorado (CO) where C. rubecula is absent. Unparasitized and C. rubecula-parasitized P. rapae hosts were used in choice tests to examine whether C. glomerata host selection behavior differed based on the population's association history with C. rubecula. We found that C. glomerata from MD had a higher likelihood of avoiding hosts parasitized by C. rubecula (and thus avoiding competition) than did wasps from CO. The ability of C. glomerata to avoid hosts parasitized by C. rubecula may facilitate coexistence in MD; whereas, the lack of discrimination in CO populations of C. glomerata naïve to C. rubecula could contribute to the displacement of C. glomerata were C. rubecula to enter the same habitat.

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Integrating elements from life tables into population models within a matrix framework has been an underutilized method of describing host-parasitoid population dynamics. This type of modeling is useful in describing demographically-structured populations and in identifying points in the host developmental timeline susceptible to parasitic attack. We apply this approach to investigate the effect of parasitism by the Asian parasitoid Aphelinus certus on its host, the soybean aphid (Aphis glycines). We present a matrix population model with coupled equations that are analogous to a Nicholson-Bailey model. To parameterize the model, we conducted several bioassays outlining host and parasitoid life history and supplemented these studies with data obtained from the literature. Analysis of the model suggests that, at a parasitism rate of 0.21 d-1, A. certus is capable of maintaining aphid densities below economically damaging levels in 31.0% of simulations. Several parameters-parasitoid lifespan, colonization timeline, host developmental stage, and mean daily temperature-were also shown to markedly influence the overall dynamics of the system. These results suggest that A. certus might provide a valuable service in agroecosystems by suppressing soybean aphid populations at relatively low levels of parasitism. Our results also support the use of A. certus within a dynamic action threshold framework in order to maximize the value of biological control in pest management programs.

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Parasitic wasps are among the most species-rich groups on Earth. A major cause of this diversity may be local adaptation to host species. However, little is known about variation in host specificity among populations within parasitoid species. Not only is such knowledge important for understanding host-driven speciation, but because parasitoids often control pest insects and narrow host ranges are critical for the safety of biological control introductions, understanding variation in specificity and how it arises are crucial applications in evolutionary biology. Here, we report experiments on variation in host specificity among 16 populations of an aphid parasitoid, Aphelinus certus. We addressed several questions about local adaptation: Do parasitoid populations differ in host ranges or in levels of parasitism of aphid species within their host range? Are differences in parasitism among parasitoid populations related to geographical distance, suggesting clinal variation in abundances of aphid species? Or do nearby parasitoid populations differ in host use, as would be expected if differences in aphid abundances, and thus selection, were mosaic? Are differences in parasitism among parasitoid populations related to genetic distances among them? To answer these questions, we measured parasitism of a taxonomically diverse group of aphid species in laboratory experiments. Host range was the same for all the parasitoid populations, but levels of parasitism varied among aphid species, suggesting adaptation to locally abundant aphids. Differences in host specificity did not correlate with geographical distances among parasitoid populations, suggesting that local adaption is mosaic rather than clinal, with a spatial scale of less than 50 kilometers. We sequenced and assembled the genome of A. certus, made reduced-representation libraries for each population, analyzed for single nucleotide polymorphisms, and used these polymorphisms to estimate genetic differentiation among populations. Differences in host specificity correlated with genetic distances among the parasitoid populations.

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Biological control, a globally-important ecosystem service, can provide long-term and broad-scale suppression of invasive pests, weeds and pathogens in natural, urban and agricultural environments. Following (few) historic cases that led to sizeable environmental up-sets, the discipline of arthropod biological control has-over the past decades-evolved and matured. Now, by deliberately taking into account the ecological risks associated with the planned introduction of insect natural enemies, immense environmental and societal benefits can be gained. In this study, we document and analyze a successful case of biological control against the cassava mealybug, Phenacoccus manihoti (Hemiptera: Pseudococcidae) which invaded Southeast Asia in 2008, where it caused substantial crop losses and triggered two- to three-fold surges in agricultural commodity prices. In 2009, the host-specific parasitoid Anagyrus lopezi (Hymenoptera: Encyrtidae) was released in Thailand and subsequently introduced into neighboring Asian countries. Drawing upon continental-scale insect surveys, multi-year population studies and (field-level) experimental assays, we show how A. lopezi attained intermediate to high parasitism rates across diverse agro-ecological contexts. Driving mealybug populations below non-damaging levels over a broad geographical area, A. lopezi allowed yield recoveries up to 10.0 t/ha and provided biological control services worth several hundred dollars per ha (at local farm-gate prices) in Asia's four-million ha cassava crop. Our work provides lessons to invasion science and crop protection worldwide. Furthermore, it accentuates the importance of scientifically-guided biological control for insect pest management, and highlights its potentially large socio-economic benefits to agricultural sustainability in the face of a debilitating invasive pest. In times of unrelenting insect invasions, surging pesticide use and accelerating biodiversity loss across the globe, this study demonstrates how biological control-as a pure public good endeavor-constitutes a powerful, cost-effective and environmentally-responsible solution for invasive species mitigation.

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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.

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