Insectivorous bats selectively source moths and eat mostly pest insects on dryland and irrigated cotton farms

Insectivorous bats are efficient predators of pest arthropods in agroecosystems. This pest control service has been estimated to be worth billions of dollars to agriculture globally. However, few studies have explicitly investigated the composition and abundance of dietary prey items consumed or assessed the ratio of pest and beneficial arthropods, making it difficult to evaluate the quality of the pest control service provided. In this study, we used metabarcoding to identify the prey items eaten by insectivorous bats over the cotton‐growing season in an intensive cropping region in northern New South Wales, Australia. We found that seven species of insectivorous bat (n = 58) consumed 728 prey species, 13 of which represented around 50% of total prey abundance consumed. Importantly, the identified prey items included major arthropod pests, comprising 65% of prey relative abundance and 13% of prey species recorded. Significant cotton pests such as Helicoverpa punctigera (Australian bollworm) and Achyra affinitalis (cotton webspinner) were detected in at least 76% of bat fecal samples, with Teleogryllus oceanicus (field crickets), Helicoverpa armigera (cotton bollworm), and Crocidosema plebejana (cotton tipworm) detected in 55% of bat fecal samples. Our results indicate that insectivorous bats are selective predators that exploit a narrow selection of preferred pest taxa and potentially play an important role in controlling lepidopteran pests on cotton farms. Our study provides crucial information for farmers to determine the service or disservice provided by insectivorous bats in relation to crops, for on‐farm decision making.     

Bird and bat predation services in tropical forests and agroforestry landscapes

Understanding distribution patterns and multitrophic interactions is critical for managing bat‐ and bird‐mediated ecosystem services such as the suppression of pest and non‐pest arthropods. Despite the ecological and economic importance of bats and birds in tropical forests, agroforestry systems, and agricultural systems mixed with natural forest, a systematic review of their impact is still missing. A growing number of bird and bat exclosure experiments has improved our knowledge allowing new conclusions regarding their roles in food webs and associated ecosystem services. Here, we review the distribution patterns of insectivorous birds and bats, their local and landscape drivers, and their effects on trophic cascades in tropical ecosystems. We report that for birds but not bats community composition and relative importance of functional groups changes conspicuously from forests to habitats including both agricultural areas and forests, here termed ‘forest‐agri’ habitats, with reduced representation of insectivores in the latter. In contrast to previous theory regarding trophic cascade strength, we find that birds and bats reduce the density and biomass of arthropods in the tropics with effect sizes similar to those in temperate and boreal communities. The relative importance of birds versus bats in regulating pest abundances varies with season, geography and management. Birds and bats may even suppress tropical arthropod outbreaks, although positive effects on plant growth are not always reported. As both bats and birds are major agents of pest suppression, a better understanding of the local and landscape factors driving the variability of their impact is needed.     

An appetite for pests: Synanthropic insectivorous bats exploit cotton pest irruptions and consume various deleterious arthropods

Conservation biological control (CBC) seeks to minimize the deleterious effects of agricultural pests by enhancing the efficiency of natural enemies. Despite the documented potential of insectivorous bats to consume pests, many synanthropic bat species are still underappreciated as beneficial species. We investigated the diet of Kuhl's pipistrelle (Pipistrellus kuhlii), a common synanthropic insectivorous bat that forages in urban and agricultural areas, to determine whether it may function as a natural enemy in CBC. Faecal samples of P. kuhlii were collected throughout the cotton‐growing season from five roost sites near cotton fields located in a Mediterranean agroecosystem, Israel, and analyzed using DNA metabarcoding. Additionally, data on estimated abundance of major cotton pests were collected. We found that the diet of P. kuhlii significantly varied according to sites and dates and comprised 27 species of agricultural pests that were found in 77.2% of the samples, including pests of key economic concern. The dominant prey was the widespread cotton pest, the pink bollworm, Pectinophora gossypiella, found in 31% of the samples and in all the roosts. Pink bollworm abundance was positively correlated with its occurrence in the bat diet. Furthermore, the bats’ dietary breadth narrowed, while temporal dietary overlap increased, in relation to increasing frequencies of pink bollworms in the diet. This suggests that P. kuhlii exploits pink bollworm irruptions by opportunistic feeding. We suggest that synanthropic bats provide important pest suppression services, may function as CBC agents of cotton pests and potentially contribute to suppress additional deleterious arthropods found in their diet in high frequencies.     

Land cover diversity increases predator aggregation and consumption of prey

A lower diversity of land cover types is purported to decrease arthropod diversity in agroecosystems and is dependent on patterns of land use and fragmentation. Ants, important providers of ecosystem services such as biological control, are susceptible to landscape‐level changes. We determined the relationships between land cover diversity and fragmentation on the within‐field spatial associations of ants to pests and resulting predation events by combining mapping and molecular tools. Increased land cover diversity and decreased fragmentation increased ant abundance, spatial association to pests and predation. Land cover diversity and fragmentation were more explanatory than land cover types. Even so, specific land cover types, such as deciduous forest, influenced ant and pest diversity more so than abundance. These results indicate that geospatial techniques and molecular gut content analysis can be combined to determine the role of land use in influencing predator–prey interactions and resulting predation events in agroecosystems.     

农田生态系统植物多样性对害虫种群数量的影响

着重分析植物多样性影响害虫发生为害及种群数量的生态学机制,综合评述了关于这种机制的两种主要假说,即天敌假说和资源集中假说．同时总结了植物多样性增大和减少对害虫控制的有利和不利因素．研究表明农田生态系统中植物多样性的增大在多数情况下能导致某些害虫种群数量的下降,但是目前很难就不同栖境中所有类型的害虫形成一般性的结论     

21世纪害虫管理的一些特征展望

分析了近年来国内外IPM研究的进展 ,认为未来的害虫管理是以作物的控害作用为中心 ,以农田生态系统或区域性生态系统为对象 ,以大量信息管理为基础 ,以发展新技术 (转基因作物和昆虫性信息素 )和农民参与为重点 ,以生态调控为手段 ,以持续发展为方向。从而使害虫管理提高到一个新的境界     

Bats and birds increase crop yield in tropical agroforestry landscapes

Human welfare is significantly linked to ecosystem services such as the suppression of pest insects by birds and bats. However, effects of biocontrol services on tropical cash crop yield are still largely unknown. For the first time, we manipulated the access of birds and bats in an exclosure experiment (day, night and full exclosures compared to open controls in Indonesian cacao agroforestry) and quantified the arthropod communities, the fruit development and the final yield over a long time period (15 months). We found that bat and bird exclusion increased insect herbivore abundance, despite the concurrent release of mesopredators such as ants and spiders, and negatively affected fruit development, with final crop yield decreasing by 31% across local (shade cover) and landscape (distance to primary forest) gradients. Our results highlight the tremendous economic impact of common insectivorous birds and bats, which need to become an essential part of sustainable landscape management.     

Interaction effects between local flower richness and distance to natural woodland on pest and beneficial insects in apple orchards

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Movement of insect pests in agricultural landscapes

Insect pests continue to exact a high toll on agricultural production, in spite of intense agrochemical input. The movement of insect pests from one place to another underlies their abundance and distribution in space and time, hence, ultimately, the extent of the inflicted crop damage. An improved understanding of dispersal mechanisms assists the deployment of sustainable pest management practices. Here, we review the latest advances in the study of the dispersal of herbivore insect pests in contemporary agro‐ecosystems. We address the factors triggering dispersal in typical agricultural landscapes, the contribution of agro‐ecosystem design and management to dispersal patterns, and the wider implications of natural and human‐mediated dispersal. Integrating practical knowledge with evolutionary theory holds the potential to improve predictions on how insect pests respond to present and future challenges imposed by changes of climate and land use.     

The impact of secondary pests on Bacillus thuringiensis (Bt) crops

The intensification of agriculture and the development of synthetic insecticides enabled worldwide grain production to more than double in the last third of the 20th century. However, the heavy dependence and, in some cases, overuse of insecticides has been responsible for negative environmental and ecological impacts across the globe, such as a reduction in biodiversity, insect resistance to insecticides, negative effects on nontarget species (e.g. natural enemies) and the development of secondary pests. The use of recombinant DNA technology to develop genetically engineered insect‐resistant crops could mitigate many of the negative side effects of insecticides. One such genetic alteration enables crops to express toxic crystalline (Cry) proteins from the soil bacteria Bacillus thuringiensis (Bt). Despite the widespread adoption of Bt crops, there are still a range of unanswered questions concerning longer term agro‐ecosystem interactions. For instance, insect species that are not susceptible to the expressed toxin can develop into secondary pests and cause significant damage to the crop. Here, we review the main causes surrounding secondary pest dynamics in Bt crops and the impact of such outbreaks. Regardless of the causes, if nonsusceptible secondary pest populations exceed economic thresholds, insecticide spraying could become the immediate solution at farmers’ disposal, and the sustainable use of this genetic modification technology may be in jeopardy. Based on the literature, recommendations for future research are outlined that will help to improve the knowledge of the possible long‐term ecological trophic interactions of employing this technology.     

973项目“重大农业害虫猖獗危害的机制及可持续控制的基础研究”简介

2006年9月,国家重点基础研究发展计划(973)农业领域2006年度项目“重大农业害虫猖獗危害的机制及可持续控制的基础研究”经科技部批准正式立项启动。该项目以全系统管理思想为指导,在基因、个体、种群、生态系统等不同层次,阐明我国重大农业害虫种群分化与暴发的分子基础,解析害虫与寄主作物及天敌间的相互作用机制,建立害虫监测与预警系统,提出重大农业害虫可持续控制的新途径和新方法,为我国农业减灾、经济的可持续发展奠定科学基础。项目的主要研究内容包括:害虫生长发育与生殖调控的分子机制;害虫对环境胁迫的适应机制;杀虫药剂诱导害虫再猖獗的机制;害虫与寄主植物的协同进化;天敌与害虫的互作及控害机制;作物-害虫-天敌食物网关系及其调控机理;重大害虫区域性暴发监测与预警。项目的总体目标为:阐明害虫生长发育、种群分化的分子基础,揭示害虫种群调节的内在机制;解析作物、害虫及天敌间的互作机制,丰富和发展植物-害虫-天敌协同进化理论;阐明主要害虫区域性灾变机理,发展害虫预警新技术;发展与环境相容的、增强自然控害功能的新技术,提出重大农业害虫可持续控制的新途径和新方法;凝炼一支害虫控制基础研究的创新团队,丰富和发展我国害虫管理的科学理论与实践,提升我国有害生物防控的原始创新和集成创新能力,扩大国际影响。     

Relationships between biodiversity and biological control in agroecosystems: Current status and future challenges

Agricultural systems around the world are faced with the challenge of providing for the demands of a growing human population. To meet this demand, agricultural systems have intensified to produce more crops per unit area at the expense of greater inputs. Agricultural intensification, while yielding more crops, generally has detrimental impacts on biodiversity. However, intensified agricultural systems often have fewer pests than more “environmentally-friendly” systems, which is believed to be primarily due to extensive pesticide use on intensive farms. In turn, to be competitive, less-intensive agricultural systems must rely on biological control of pests. Biological pest control is a complex ecosystem service that is generally positively associated with biodiversity of natural enemy guilds. Yet, we still have a limited understanding of the relationships between biodiversity and biological control in agroecosystems, and the mechanisms underlying these relationships. Here, we review the effects of agricultural intensification on the diversity of natural enemy communities attacking arthropod pests and weeds. We next discuss how biodiversity of these communities impacts pest control, and the mechanisms underlying these effects. We focus in particular on novel conceptual issues such as relationships between richness, evenness, abundance, and pest control. Moreover, we discuss novel experimental approaches that can be used to explore the relationships between biodiversity and biological control in agroecosystems. In particular, we highlight new experimental frontiers regarding evenness, realistic manipulations of biodiversity, and functional and genetic diversity. Management shifts that aim to conserve diversity while suppressing both insect and weed pests will help growers to face future challenges. Moreover, a greater understanding of the interactions between diversity components, and the mechanisms underlying biodiversity effects, would improve efforts to strengthen biological control in agroecosystems.     

When bats go viral: negative framings in virological research imperil bat conservation

The recent upsurge in bat‐borne virus research has attracted substantial news coverage worldwide. A systematic review of virological literature revealed that bats were described as a major concern for public health in half of all studies (51%), and that their key role in delivering ecosystem services was disregarded in almost all studies (96%). Although research on zoonoses is of the utmost importance, biased framings of bats can undermine decades of conservation efforts. We urge researchers and science communicators to consider the conservation impacts of how research findings are presented to the public carefully, and, whenever possible, to highlight the ecological significance of bats, their dire conservation situation and their importance for human well‐being.     

Numerical and Functional Responses of Forest Bats to a Major Insect Pest in Pine Plantations

Global change is expected to modify the frequency and magnitude of defoliating insect outbreaks in forest ecosystems. Bats are increasingly acknowledged as effective biocontrol agents for pest insect populations. However, a better understanding is required of whether and how bat communities contribute to the resilience of forests to man- and climate-driven biotic disturbances. We studied the responses of forest insectivorous bats to a major pine defoliator, the pine processionary moth pityocampa, which is currently expanding its range in response to global warming. We used pheromone traps and ultrasound bat recorders to estimate the abundance and activity of moths and predatory bats along the edge of infested pine stands. We used synthetic pheromone to evaluate the effects of experimentally increased moth availability on bat foraging activity. We also evaluated the top-down regulation of moth population by estimating T. pityocampa larval colonies abundance on the same edges the following winter. We observed a close spatio-temporal matching between emergent moths and foraging bats, with bat activity significantly increasing with moth abundance. The foraging activity of some bat species was significantly higher near pheromone lures, i.e. in areas of expected increased prey availability. Furthermore moth reproductive success significantly decreased with increasing bat activity during the flight period of adult moths. These findings suggest that bats, at least in condition of low prey density, exhibit numerical and functional responses to a specific and abundant prey, which may ultimately result in an effective top-down regulation of the population of the prey. These observations are consistent with bats being useful agents for the biocontrol of insect pest populations in plantation forests.     

中国蝙蝠生物学研究进展及其保护对策

自2019年末,新冠肺炎的全球大流行使蝙蝠（翼手目动物）倍受关注,甚至人们“谈蝠色变”。蝙蝠在生态和分类上多样性极高,占哺乳动物种类的20%左右。蝙蝠不仅在害虫控制、种子传播、植物授粉等方面具有重要的生态作用和经济价值,也在健康长寿、生物仿生和语言进化等方面具有重要的科研价值。中国是全世界蝙蝠物种多样性最丰富的国家之一,已知的物种超过了140种。近几十年来,中国学者在蝙蝠分类学、生态学、行为学、进化生物学、神经生物学和病毒病源学等研究领域取得了丰硕的成果,然而涉及蝙蝠的生态系统服务和资源保护的相关研究比较少。由于生境退化、过度捕杀、栖息地破坏、城市化、杀虫剂使用、气候变化等原因,中国蝙蝠受到极大的威胁,约51%的物种位于近危等级之上。为了有效地保护中国蝙蝠物种的多样性,建议加强基础研究,建立中国蝙蝠多样性监测网络,加强蝙蝠栖息地保护,完善相关法律法规,加强蝙蝠公众教育,以促进中国蝙蝠生物学研究和保护。     

农田非作物生境调控与害虫综合治理

就害虫综合治理的研究而言,农田生态系统可以区分出作物生境和邻近作物的非作物生境。昆虫从作物生境迁移到非作物生境,与作物生境缺乏食物或受人类栽培活动干扰而引起的自然迁移、转换寄主和寻求庇护场所有关。许多研究表明,与特定作物田块相联系的植被类型和结构可影响害虫及其天敌迁居的种类、数量和时间。因此,我们可以通过改变大田周围非作物生境的植被组成及特征来调控农业生态系统中害虫与天敌的相互关系,提高天敌对害虫的控制效能。由于景观的空间格局对节肢动物的生物学特性有直接或间接的影响,所以,以景观为单元要比以同类作物的田块为单元更加适于害虫综合治理的研究和实施。在现代农业景观区域内重新引入和相嵌一些非栽培植物或廊道,可为众多有益节肢动物的繁殖、取食和避害提供多种类型的非作物栖境。     

Ecosystem services provided by aculeate wasps

The aculeate wasps are one of the most diverse and speciose insect taxa; they are omnipresent across ecosystems and exhibit diverse co-evolutionary and exploitative associations with other organisms. There is widespread conjecture that aculeate wasps are likely to perform essential ecological and economic services of importance to the health, well-being and nutritional needs of our planet. However, the scope and nature of the ecosystem services they provide are not well understood relative to other insect groups (e.g. bees, butterflies, beetles); an appreciation of their value is further tarnished by their public reputation as pointless pests. Here, we conduct the first comprehensive review of how aculeate wasps contribute to the four main areas of ecosystem services: regulatory, provisioning, supporting and cultural services. Uniting data from a large but previously disconnected literature on solitary and social aculeate wasps, we provide a synthesis on how these insects perform important ecosystem services as parasites, predators, biological indicators, pollinators, decomposers and seed dispersers; and their additional services as a sustainable alternative to meat for human consumption, and medicinal potential as sources of research leads for anti-microbials and cancer treatments. We highlight how aculeate wasps offer substantial, but largely overlooked, economic benefits through their roles in natural pest management and biological control programs. Accordingly, we provide data-driven arguments for reasons to consider the ecosystem service value of aculeate wasps on a par with other ‘useful’ insects (e.g. bees). Finally, we provide a research roadmap identifying the key areas of research required to capitalise better on the services provided by these important insects.     

Interaction complexity matters: disentangling services and disservices of ant communities driving yield in tropical agroecosystems

Owing to complex direct and indirect effects, impacts of higher trophic levels on plants is poorly understood. In tropical agroecosystems, ants interact with crop mutualists and antagonists, but little is known about how this integrates into the final ecosystem service, crop yield. We combined ant exclusion and introduction of invasive and native-dominant species in cacao agroecosystems to test whether (i) ant exclusion reduces yield, (ii) dominant species maximize certain intermediate ecosystem services (e.g. control of specific pests) rather than yield, which depends on several, cascading intermediate services and (iii) even, species-rich ant communities result in highest yields. Ants provided services, including reduced leaf herbivory and fruit pest damage and indirect pollination facilitation, but also disservices, such as increased mealybug density, phytopathogen dissemination and indirect pest damage enhancement. Yields were highest with unmanipulated, species-rich, even communities, whereas ant exclusion decreased yield by 27%. Introduction of an invasive-dominant ant decreased species density and evenness and resulted in 34% lower yields, whereas introduction of a non-invasive-dominant species resulted in similar species density and yields as in the unmanipulated control. Species traits and ant community structure affect services and disservices for agriculture in surprisingly complex ways, with species-rich and even communities promoting highest yield.     

Comparison of pollinators and natural enemies: a meta‐analysis of landscape and local effects on abundance and richness in crops

To manage agroecosystems for multiple ecosystem services, we need to know whether the management of one service has positive, negative, or no effects on other services. We do not yet have data on the interactions between pollination and pest‐control services. However, we do have data on the distributions of pollinators and natural enemies in agroecosystems. Therefore, we compared these two groups of ecosystem service providers, to see if the management of farms and agricultural landscapes might have similar effects on the abundance and richness of both. In a meta‐analysis, we compared 46 studies that sampled bees, predatory beetles, parasitic wasps, and spiders in fields, orchards, or vineyards of food crops. These studies used the proximity or proportion of non‐crop or natural habitats in the landscapes surrounding these crops (a measure of landscape complexity), or the proximity or diversity of non‐crop plants in the margins of these crops (a measure of local complexity), to explain the abundance or richness of these beneficial arthropods. Compositional complexity at both landscape and local scales had positive effects on both pollinators and natural enemies, but different effects on different taxa. Effects on bees and spiders were significantly positive, but effects on parasitoids and predatory beetles (mostly Carabidae and Staphylinidae) were inconclusive. Landscape complexity had significantly stronger effects on bees than it did on predatory beetles and significantly stronger effects in non‐woody rather than in woody crops. Effects on richness were significantly stronger than effects on abundance, but possibly only for spiders. This abundance‐richness difference might be caused by differences between generalists and specialists, or between arthropods that depend on non‐crop habitats (ecotone species and dispersers) and those that do not (cultural species). We call this the ‘specialist‐generalist’ or ‘cultural difference’ mechanism. If complexity has stronger effects on richness than abundance, it might have stronger effects on the stability than the magnitude of these arthropod‐mediated ecosystem services. We conclude that some pollinators and natural enemies seem to have compatible responses to complexity, and it might be possible to manage agroecosystems for the benefit of both. However, too few studies have compared the two, and so we cannot yet conclude that there are no negative interactions between pollinators and natural enemies, and no trade‐offs between pollination and pest‐control services. Therefore, we suggest a framework for future research to bridge these gaps in our knowledge.     

Insect declines and agroecosystems: does light pollution matter?

Drastic declines in insect populations, ‘Ecological Armageddon’, have recently gained increased attention in the scientific community, and are commonly considered to be the consequence of large‐scale factors such as land‐use changes, use of pesticides, climate change and habitat fragmentation. Artificial light at night (ALAN), a pervasive global change that strongly impacts insects, remains, however, infrequently recognised as a potential contributor to the observed declines. Here, we provide a summary of recent evidence of impacts of ALAN on insects and discuss how these impacts can drive declines in insect populations in light‐polluted areas. ALAN can increase overall environmental pressure on insect populations, and this is particularly important in agroecosystems where insect communities provide important ecosystem services (such as natural pest control, pollination, conservation of soil structure and fertility and nutrient cycling), and are already under considerable environmental pressure. We discuss how changes in insect populations driven by ALAN and ALAN itself may hinder these services to influence crop production and biodiversity in agricultural landscapes. Understanding the contribution of ALAN and other factors to the decline of insects is an important step towards mitigation and the recovery of the insect fauna in our landscapes. In future studies, the role of increased nocturnal illumination also needs to be examined as a possible causal factor of insect declines in the ongoing ‘Ecological Armageddon’, along with the more commonly examined factors. Given the large scale of agricultural land use and the potential of ALAN to indirectly and directly impact crop production and biodiversity, a better understanding of effects of ALAN in agroecosystems is urgently needed.