Restoring functional integrity of the global production ecosystem through biological control.

Human society is anchored in the global agroecosystem. For millennia, this system has provided humans with copious supplies of nutrient-rich food. Yet, through chemical intensification and simplification, vast shares of present-day farmland derive insufficient benefits from biodiversity and prove highly vulnerable to biotic stressors. Here, we argue that on-farm action centered on biological control can effectively defuse pest risk by bolstering foundational ecosystem services. By harnessing plant, animal and microbial biodiversity, biological control offers safe, efficacious and economically-sound plant health solutions and coevolved options for invasive species mitigation. In recent years, its scientific foundation has been fortified and solutions have been refined for myriad ecologically brittle systems. Yet, for biological control to be mainstreamed, it needs to be rebooted, intertwined with (on- and off-farm) agroecological tactics and refurbished - from research, policy and regulation, public-private partnerships up to modes of implementation. Misaligned incentives (for chemical pesticides) and adoption barriers further need to be removed, while its scientific underpinnings should become more interdisciplinary, policy-relevant, solution-oriented and linked with market demand. Thus, biological control could ensure human wellbeing in a nature-friendly manner and retain farmland ecological functioning under global change.

Biological control for One Health.

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.

Salinity stress alters plant-mediated interactions between above- and below-ground herbivores.

Below-ground herbivory impacts plant development and often induces systemic responses in plants that affect the performance and feeding behavior of above-ground herbivores. Meanwhile, pest-damaged root tissue can enhance a plant's susceptibility to abiotic stress such as salinity. Yet, the extent to which herbivore-induced plant defenses are modulated by such abiotic stress has rarely been studied. In this study, we examine whether root feeding by larvae of the turnip moth, Agrotis segetum (Lepidoptera: Noctuidae) affects the performance of the above-ground, sap-feeding aphid Aphis gossypii (Hemiptera: Aphididae) on cotton, and assess whether those interactions are modulated by salinity stress. In the absence of salinity stress, A. segetum root feeding does not affect A. gossypii development. On the other hand, under intense salinity stress (i.e., 600 mM NaCl), A. segetum root feeding decreases aphid development time by 16.1 % and enhances fecundity by 72.0 %. Transcriptome, metabolome and bioassay trials showed that root feeding and salinity stress jointly trigger the biosynthesis of amino acids in cotton leaves. Specifically, increased titers of valine in leaf tissue relate to an enhanced performance of A. gossypii. Taken together, salinity stress alters the interaction between above- and below-ground feeders by changing amino acid accumulation. Our findings advance our understanding of how plants cope with concurrent biotic and abiotic stressors, and may help tailor plant protection strategies to varying production contexts.

Biodiversity loss impacts top-down regulation of insect herbivores across ecosystem boundaries.

Biodiversity loss, as driven by anthropogenic global change, imperils biosphere intactness and integrity. Ecosystem services such as top-down regulation (or biological control; BC) are susceptible to loss of extinction-prone taxa at upper trophic levels and secondary 'support' species e.g., herbivores. Here, drawing upon curated open-access interaction data, we structurally analyze trophic networks centered on the fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae) and assess their robustness to species loss. Tri-partite networks link 80 BC organisms (invertebrate or microbial), 512 lepidopteran hosts and 1194 plants (including 147 cultivated crops) in the Neotropics. These comprise threatened herbaceous or woody plants and conservation flagships such as saturniid moths. Treating all interaction partners functionally equivalent, random herbivore loss exerts a respective 26 % or 108 % higher impact on top-down regulation in crop and non-crop settings than that of BC organisms (at 50 % loss). Equally, random loss of BC organisms affects herbivore regulation to a greater extent (13.8 % at 50 % loss) than herbivore loss mediates their preservation (11.4 %). Yet, under moderate biodiversity loss, (non-pest) herbivores prove highly susceptible to loss of BC organisms. Our topological approach spotlights how agriculturally-subsidized BC agents benefit vegetation restoration, while non-pest herbivores uphold biological control in on- and off-farm settings alike. Our work underlines how the on-farm usage of endemic biological control organisms can advance conservation, restoration, and agricultural sustainability imperatives. We discuss how integrative approaches and close interdisciplinary cooperation can spawn desirable outcomes for science, policy and practice.

Pest Status, Bio-Ecology, and Area-Wide Management of Mirids in East Asia.

Mirids (Hemiptera: Heteroptera: Miridae) feed upon a wide variety of cultivated and wild plants and can be economically important crop pests. They have traditionally been perceived as innocuous herbivores in East Asia; however, population levels of various mirid species have dramatically increased over the past decades. High-profile pests such as Apolygus spp., Adelphocoris spp., and Lygus spp. are now widely distributed across the region, and their infestation pressure is associated with climate, agroecological conditions, and farming practices. This review outlines how an in-depth understanding of pest biology, a systems-level characterization of pest ecology, and a comprehensive evaluation of integrated pest management tactics have enabled sustainable management of mirids across crop boundaries and harvest cycles. This work underscores how more holistic, integrative research approaches can accelerate the implementation of area-wide management of generalist pests, effectively prevent pest population build-up and yield impact, and shrink the environmental footprint of agriculture. In addition to highlighting the merits of interdisciplinary systems approaches, we discuss prospects and challenges for the sustainable management of polyphagous mirid pests in landscape matrices.

Institutional Context of Pest Management Science in the Global South.

The natural sciences are receiving increasing attention in the Global South. This timely development may help mitigate global change and quicken an envisioned food system transformation. Yet in order to resolve complex issues such as agrochemical pollution, science ideally proceeds along suitable trajectories within appropriate institutional contexts. Here, we employ a systematic literature review to map the nature of inquiry and institutional context of pest management science in 65 low- and middle-income countries published from 2010 to 2020. Despite large inter-country variability, any given country generates an average of 5.9 publications per annum (range 0-45.9) and individual nations such as Brazil, Kenya, Benin, Vietnam, and Turkey engage extensively in regional cooperation. International development partners are prominent scientific actors in West Africa but are commonly outpaced by national institutions and foreign academia in other regions. Transnational institutions such as the CGIAR represent a 1.4-fold higher share of studies on host plant resistance but lag in public interest science disciplines such as biological control. Despite high levels of scientific abstraction, research conducted jointly with development partners shows real yet marginal improvements in incorporating the multiple (social-ecological) layers of the farming system. Added emphasis on integrative system-level approaches and agroecological or biodiversity-driven measures can extend the reach of science to unlock transformative change.

Generalist Predators Shape Biotic Resistance along a Tropical Island Chain.

Islands offer exclusive prisms for an experimental investigation of biodiversity x ecosystem function interplay. Given that species in upper trophic layers, e.g., arthropod predators, experience a comparative disadvantage on small, isolated islands, such settings can help to clarify how predation features within biotic resistance equations. Here, we use observational and manipulative studies on a chain of nine Indonesian islands to quantify predator-mediated biotic resistance against the cassava mealybug Phenacoccus manihoti (Homoptera: Pseudococcidae) and the fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae). Across island settings, a diverse set of generalist lacewing, spider and ladybeetle predators aggregates on P. manihoti infested plants, attaining max. (field-level) abundance levels of 1.0, 8.0 and 3.2 individuals per plant, respectively. Though biotic resistance-as imperfectly defined by a predator/prey ratio index-exhibits no inter-island differences, P. manihoti population regulation is primarily provided through an introduced monophagous parasitoid. Meanwhile, resident predators, such as soil-dwelling ants, inflict apparent mortality rates up to 100% for various S. frugiperda life stages, which translates into a 13- to 800-fold lower S. frugiperda survivorship on small versus large islands. While biotic resistance against S. frugiperda is ubiquitous along the island chain, its magnitude differs between island contexts, seasons and ecological realms, i.e., plant canopy vs. soil surface. Hence, under our experimental context, generalist predators determine biotic resistance and exert important levels of mortality even in biodiversity-poor settings. Given the rapid pace of biodiversity loss and alien species accumulation globally, their active conservation in farmland settings (e.g., through pesticide phasedown) is pivotal to ensuring the overall resilience of production ecosystems.

Plant volatiles mediate Aphis gossypii settling but not predator foraging in intercropped cotton.

BACKGROUND: The cotton aphid, Aphis gossypii Glover (Hemiptera: Aphididae) is an important pest of cotton and horticultural crops globally. In China, smallholder farmers regularly intercrop cotton with garlic or onion. Aside from higher farm-level revenue, cotton intercrops are typified by lower Aphis gossypii abundance than monocrops. So far, the mechanistic basis of this lowered pest pressure has not been empirically assessed. RESULTS: Field trials showed that Aphis gossypii abundance is lower and (relative) abundance of aphid predators higher in early-season cotton intercrops than in monocrops. Cage trials and Y-tube olfactometer tests further indicated that garlic and onion volatiles repel Aphis gossypii alates. Electrophysiological bioassays and gas chromatography-mass spectrometry (GC-MS) identified two physiologically active volatiles, that is, diallyl disulfide and propyl disulfide from garlic and onion respectively. Next, behavioral tests confirmed that both sulfur compounds exert a repellent effect on alate Aphis gossypii. CONCLUSION: Garlic and onion volatiles interfere with Aphis gossypii settling, but do not affect its main (ladybird) predators. Meanwhile, early-season cotton/onion intercrops bear higher numbers of Aphis gossypii predators and fewer aphids. By thus unveiling the ecological underpinnings of aphid biological control in diversified cropping systems, our work advances non-chemical management of a globally-important crop pest. © 2023 Society of Chemical Industry.

Hoverflies provide pollination and biological pest control in greenhouse-grown horticultural crops.

Beneficial insects provide pollination and biological control in natural and man-made settings. Those ecosystem services (ES) are especially important for high-value fruits and vegetables, including those grown under greenhouse conditions. The hoverfly Eupeodes corollae (Diptera: Syrphidae) delivers both ES, given that its larvae prey upon aphid pests and its adults pollinate crops. In this study, we investigated this dual role of E. corollae in three insect-pollinated and aphid-affected horticultural crops i.e., tomato, melon and strawberry within greenhouses in Hebei province (China). Augmentative releases of E. corollae increased fruit set and fruit weight of all three crops, and affected population dynamics of the cotton aphid Aphis gossypii (Hemiptera: Aphididae). On melon and strawberry, E. corollae suppressed A. gossypii populations by 54-99% and 50-70% respectively. In tomato, weekly releases of 240 E. corollae individuals/100 m2led to 95% fruit set. Meanwhile, releases of 160 hoverfly individuals per 100 m2led to 100% fruit set in melon. Also, at hoverfly/aphid release rates of 1:500 in spring and 1:150 in autumn, aphid populations were reduced by more than 95% on melon. Lastly, on strawberry, optimum levels of pollination and aphid biological control were attained at E. corollae release rates of 640 individuals/100 m2. Overall, our work shows how augmentative releases of laboratory-reared hoverflies E. corollae can enhance yields of multiple horticultural crops while securing effective, non-chemical control of resident aphid pests.

Ecology, invasion history and biodiversity-driven management of the coconut black-headed caterpillar Opisina arenosella in Asia.

The coconut black-headed caterpillar (BHC), Opisina arenosella Walker (Lepidoptera: Xyloryctidae) is an important herbivore of palm trees that originates in South Asia. Over the past decades, O. arenosella has spread to several countries in Eastern and Southeast Asia. BHC larval feeding can cause severe defoliation and occasional plant death, resulting in direct production losses (e.g., for coconut) while degrading the aesthetic value of urban and rural landscapes. In this review paper, we systematically cover taxonomy, bio-ecology, invasion history and current management of O. arenosella throughout Asia. Given that O. arenosella is routinely controlled with insecticides, we equally explore options for more sustainable management through agroecological and biodiversity-based tactics e.g., cultural control or biological control. Also, recent advances in chemical ecology have unlocked lucrative opportunities for volatile-mediated monitoring, mating disruption and mass-trapping. Substantial progress has been made in augmentation biological control, with scheduled releases of laboratory-reared parasitoids lowering BHC infestation pressure up to 95%. Equally, resident ants provide 75-98% mortality of BHC egg masses within the palm canopy. Biological control has been effectively paired with sanitary measures and good agronomy (i.e., proper fertilization, irrigation), and promoted through participatory farmer training programs. Our comprehensive listing of non-chemical preventative and curative tactics offer bright prospects for a more environmentally-sound, biodiversity-driven mitigation of a palm pest of regional allure.

Long-term insect censuses capture progressive loss of ecosystem functioning in East Asia.

Insects provide critical ecosystem services such as biological pest control, in which natural enemies (NE) regulate the populations of crop-feeding herbivores (H). While H-NE dynamics are routinely studied at small spatiotemporal scales, multiyear assessments over entire agrolandscapes are rare. Here, we draw on 18-year radar and searchlight trapping datasets (2003-2020) from eastern Asia to (i) assess temporal population trends of 98 airborne insect species and (ii) characterize the associated H-NE interplay. Although NE consistently constrain interseasonal H population growth, their summer abundance declined by 19.3% over time and prominent agricultural pests abandoned their equilibrium state. Within food webs composed of 124 bitrophic couplets, NE abundance annually fell by 0.7% and network connectance dropped markedly. Our research unveils how a progressive decline in insect numbers debilitates H trophic regulation and ecosystem stability at a macroscale, carrying implications for food security and (agro)ecological resilience during times of global environmental change.

Bt maize can provide non-chemical pest control and enhance food safety in China.

China is the world's second-largest maize producer and consumer. In recent years, the invasive fall armyworm Spodoptera frugiperda (J.E. Smith) has adversely affected maize productivity and compromised food security. To mitigate pest-inflicted food shortages, China's Government issued biosafety certificates for two genetically modified (GM) Bt maize hybrids, Bt-Cry1Ab DBN9936 and Bt-Cry1Ab/Cry2Aj Ruifeng 125, in 2019. Here, we quantitatively assess the impact of both Bt maize hybrids on pest feeding damage, crop yield and food safety throughout China's maize belt. Without a need to resort to synthetic insecticides, Bt maize could mitigate lepidopteran pest pressure by 61.9-97.3%, avoid yield loss by 16.4-21.3% (range -11.9-99.2%) and lower mycotoxin contamination by 85.5-95.5% as compared to the prevailing non-Bt hybrids. Yield loss avoidance varied considerably between experimental sites and years, as mediated by on-site infestation pressure and pest identity. For either seed mixtures or block refuge arrangements, pest pressure was kept below established thresholds at 90% Bt maize coverage in Yunnan (where S. frugiperda was the dominant species) and 70% Bt maize coverage in other sites dominated by Helicoverpa armigera (Hübner) and Ostrinia furnacalis (Guenée). Drawing on experiences from other crop/pest systems, Bt maize in se can provide area-wide pest management and thus, contribute to a progressive phase-down of chemical pesticide use. Hence, when consciously paired with agroecological and biodiversity-based measures, GM insecticidal crops can ensure food and nutrition security, contribute to the sustainable intensification of China's agriculture and reduce food systems' environmental footprint.

Licorice strips enhance predator-mediated biological control in China's cotton crop.

BACKGROUND: Habitat management such as field- or farm-level diversification can conserve arthropod natural enemies, enhance biological pest control and lower (or suspend) insecticide use in agricultural crops. These approaches however have been underexploited to manage the aphid Aphis gossypii in cotton cropping systems of Xinjiang, China. In this study, we investigated whether the presence of licorice (Glycyrrhiza uralensis) at the field edge benefits generalist predator abundance and aphid biological control in local cotton crops. RESULTS: Field trials during 2020 and 2021 showed that licorice strips enhanced the in-field abundance of generalist predators (primarily ladybeetles) 2.2-4.3 fold during early season, i.e. initial growth before A. gossypii peak infestation pressure. During peak outbreak conditions in July, treatment fields with licorice strips experienced a respective 17.5-61.2% lowered aphid density and 12.3-14.6-fold higher predator-to-aphid abundance ratio (PAR) than control fields. In late season (aphid decline phase) of either year, cotton fields with licorice strips also attained a respective 4.7-9.9 fold higher PAR. Exclusion cage assays quantitatively assessed predator-mediated A. gossypii biological control and the relative contribution of licorice strips. The biocontrol services index (BSI) was 2.8 times (2020) and 1.4 times (2021) higher at 5 m distances from the licorice strip as compared to control fields. CONCLUSION: Licorice strips in the immediate vicinity of cotton fields benefit generalist arthropod predators and improve aphid biological control throughout the cotton cropping season. These findings help to integrate habitat management within integrated pest management (IPM) frameworks in the biggest cotton production region of China. © 2022 Society of Chemical Industry.

Tritrophic defenses as a central pivot of low-emission, pest-suppressive farming systems.

The ongoing COVID-19 pandemic has spotlighted the intricate connections between human and planetary health. Given that pesticide-centered crop protection degrades ecological resilience and (in-)directly harms human health, the adoption of ecologically sound, biodiversity-driven alternatives is imperative. In this Synthesis paper, we illuminate how ecological forces can be manipulated to bolster 'tritrophic defenses' against crop pests, pathogens, and weeds. Three distinct, yet mutually compatible approaches (habitat-mediated, breeding-dependent, and epigenetic tactics) can be deployed at different organizational levels, that is, from an individual seed to entire farming landscapes. Biodiversity can be harnessed for crop protection through ecological infrastructures, diversification tactics, and reconstituted soil health. Crop diversification is ideally guided by interorganismal interplay and plant-soil feedbacks, entailing resistant cultivars, rotation schemes, or multicrop arrangements. Rewarding opportunities also exist to prime plants for enhanced immunity or indirect defenses. As tritrophic defenses spawn multiple societal cobenefits, they could become core features of healthy, climate-resilient, and low-carbon food systems.

Perennial Flowering Plants Sustain Natural Enemy Populations in Gobi Desert Oases of Southern Xinjiang, China.

Natural habitats play crucial roles in biodiversity conservation and shape the delivery of ecosystem services in farming landscapes. By providing diverse resources to foraging natural enemies, they can equally enhance biological pest control. In this study, we described the plant community and foliage-dwelling invertebrate predators within non-crop habitats of the Gobi Desert oases in southern Xinjiang, China. We assessed whether plant-related variables (i.e., species identity, flowering status) and herbivore abundance affect natural enemy identity and abundance. A total of 18 plant species belonging to 18 genera and 10 families were commonly encountered, with Apocynum pictum (Apocynaceae), Phragmites communis (Poaceae), Karelinia caspia (Asteraceae), and Tamarix ramosissima (Tamaricaceae) as the dominant species. Certain plant species (P. communis) primarily provide shelter, while others offer (floral, non-floral) food resources or alternative prey. Predatory ladybeetles and spiders were routinely associated with these plants and foraged extensively within adjacent field crops. Plant traits and herbivore abundance explained up to 44% (3%-44%) variation in natural enemy community and exhibited consistent, year-round effects. Among all plant species, A. pictum consistently had a significantly higher abundance of resident natural enemies, except for August 2019. Our study underlines how perennial flowering plants, such as A. pictum, are essential to sustain natural enemy communities and related ecosystem services in arid settings. This work not only informs sustainable pest management initiatives but also shows how non-crop habitats at the periphery of agricultural fields underpin ecological resilience under adverse climatic conditions.

Windborne migration amplifies insect-mediated pollination services.

Worldwide, hoverflies (Syrphidae: Diptera) provide crucial ecosystem services such as pollination and biological pest control. Although many hoverfly species exhibit migratory behavior, the spatiotemporal facets of these movement dynamics, and their ecosystem services implications are poorly understood. In this study, we use long-term (16-year) trapping records, trajectory analysis, and intrinsic (i.e., isotope, genetic, pollen) markers to describe migration patterns of the hoverfly Episyrphus balteatus in northern China. Our work reveals how E. balteatus migrate northward during spring-summer and exhibits return (long-range) migration during autumn. The extensive genetic mixing and high genetic diversity of E. balteatus populations underscore its adaptive capacity to environmental disturbances, for example, climate change. Pollen markers and molecular gut analysis further illuminate how E. balteatus visits min. 1012 flowering plant species (39 orders) over space and time. By thus delineating E. balteatus transregional movements and pollination networks, we advance our understanding of its migration ecology and facilitate the design of targeted strategies to conserve and enhance its ecosystem services.

Impact of Heat Stress on the Predatory Ladybugs Hippodamia variegata and Propylaea quatuordecimpunctata.

In cotton-growing regions of northwestern China, Hippodamia variegata (Goeze) and Propylaea quatuordecimpunctata (Linnaeus) (Coleoptera: Coccinellidae) are key natural enemies of hemipteran pests. As only H. variegata can be encountered in hot, arid production areas, the thermal responses and climatic adaptability of both species likely differ substantially. In this study, we assessed the survival, longevity, fecundity, prey consumption rate, and antioxidant capacity of both species under laboratory conditions at 32-38 °C. The (negative) impacts of elevated temperatures (i.e., 35 and 38 °C) on adult survival and reproduction were more pronounced for P. quatuordecimpunctata than for H. variegata. Similarly, high temperatures exhibited the strongest negative impacts on the prey consumption rates of P. quatuordecimpunctata. At elevated temperatures, superoxide dismutase and catalase activity increased, while glutathione-S-transferases activity decreased for both species. However, for P. quatuordecimpunctata, peroxidase activity and total antioxidant capacity progressively declined. Antioxidant responses thus constitute a key physiological adaptation of ladybugs to heat stress, reflecting a superior thermal tolerance of H. variegata. Our work emphasizes how laboratory assays can explain spatiotemporal distribution patterns of individual ladybugs and inform strategies to bolster their ensuing biological control under conditions of global warming or extreme weather events.

Agro-ecology science relates to economic development but not global pesticide pollution.

Synthetic pesticides are core features of input-intensive agriculture and act as major pollutants driving environmental change. Agroecological science has unveiled the benefits of biodiversity for pest control, but research implementation at the farm-level is still difficult. Here we address this implementation gap by using a bibliometric approach, quantifying how countries' scientific progress in agro-ecology relates to pesticide application regimes. Among 153 countries, economic development does spur scientific innovation but irregularly bears reductions in pesticide use. Some emerging economies bend the Environmental Kuznets curve (EKC) - the observed environmental pollution by a country's wealth - for pesticides and few high-income countries exhibit a weak agro-ecology 'technique effect'. Our findings support recent calls for large-scale investments in nature-positive agriculture, underlining how agro-ecology can mend the ecological resilience, carbon footprint, and human health impacts of intensive agriculture. Yet, in order to effectively translate science into practice, scientific progress needs to be paralleled by policy-change, farmer education and broader awareness-raising.

Population genetics unveils large-scale migration dynamics and population turnover of Spodoptera exigua.

BACKGROUND: Migration is a widespread phenomenon among many insect species, including herbivorous crop pests. At present, scant information exists on the long-range migration of the polyphagous armyworm, Spodoptera exigua and its underlying climatic determinants (i.e. East Asian or South Asian monsoon circulation). In this study, we employed a population genetics approach to delineate S. exigua migration patterns across multiple Asian countries. RESULTS: Using mitochondrial cytochrome I (COI) and microsatellite markers, low-to-moderate levels of genetic diversity were detected among 101 S. exigua populations collected across China, Pakistan and Vietnam. Haplotype diversity and nucleotide diversity did not differ between years. Two spatially explicit genetic clusters were detected, an eastern and a western clade, with the former comprising populations in the East Asia monsoon area. No genetic differentiation was recorded among armyworm populations in the year-round breeding area, nor among those of the overwintering and nonoverwintering areas. Five of the most widespread mitochondrial haplotypes reflected the extensive gene flow across at a large spatial scale. CONCLUSION: Low-to-moderate levels of genetic diversity were observed, and evidence was found for genetic clustering in certain geographical areas. Accordingly, our unique insights into S. exigua population genetics and spatiotemporal migration dynamics help to guide applied ecological studies, ecological intensification schemes or (area-wide) pest management campaigns in China and abroad. © 2021 Society of Chemical Industry.