Current status and future perspectives on natural enemies for pest control in Taiwan

ABSTRACT

In Taiwan, the agricultural policy, ‘Reduce the consumption of pesticide to half in the next 10 years’, was launched in 2017. Pesticide application, which results in contamination of food by chemical residues, pest resistance, and other adverse ecological effects, is a growing public and environmental concern. Pest control by natural predators is, thus, the best alternative. Biological control methods implemented based on insights obtained from studies on pest behaviour, rearing, and various crop management modes, increase the possibility of controlling pests in modern organic agricultural systems. More than a decade has passed since the first introduction of a predatory insect in Taiwan for pest control (in the 1990s). Predatory and parasitic natural enemies, including lacewing, predatory stink bugs, Orius, and parasitic wasps, were initially used for controlling thrips, aphids, spider mites, whiteflies, and lepidopteran pests. At present, there exists a wide range of integrated pest management (IPM) methods incorporating other non-chemical, biological, and agricultural methods. However, recently, there has been an increase in research and development on the utilisation of natural enemies of insects and the associated food safety issues. Mass production and release, storage, and handling techniques of insect predators and parasitoids have been successful in recent years. The final goal of present day research is to develop natural enemy products and provide an IPM-based model to farmers for using natural enemies in agricultural production systems, thereby reducing pesticide application and ensuring food security.     

Group foraging in carnivorous plants: Carnivorous plant Drosera makinoi (Droseraceae) is more effective at trapping larger prey in large groups

Some predatory animals, represented by large carnivores, forage in groups and benefit from this behavior. We tested the hypothesis that carnivorous plants also benefit from group foraging to improve the efficiency of trapping large prey using Drosera makinoi (Droseraceae). As a result of our field observations, it was found that larger neighboring D. makinoi density yields a greater number of large preys (≥3 mm) and total prey biomass per plant. Results showed that a total of 43.4% of the events to trap large prey was achieved by two trap leaves belonging to two neighboring D. makinoi plants. Our results proved that group foraging in D. makinoi enables them to trap large prey.     

Modeling herbivore functional responses causing boom‐bust dynamics following predator removal

Native biodiversity is threatened by invasive species in many terrestrial and marine systems, and conservation managers have demonstrated successes by responding with eradication or control programs. Although invasive species are often the direct cause of threat to native species, ecosystems can react in unexpected ways to their removal or reduction. Here, we use theoretical models to predict boom‐bust dynamics, where the removal of predatory or competitive pressure from a native herbivore results in oscillatory population dynamics (boom‐bust), which can endanger the native species’ population in the short term. We simulate control activities, applied to multiple theoretical three‐species Lotka‐Volterra ecosystem models consisting of vegetation, a native herbivore, and an invasive predator. Based on these communities, we then develop a predictive tool that—based on relative parameter values—predicts whether control efforts directed at the invasive predator will lead to herbivore release followed by a crash. Further, by investigating the different functional responses, we show that model structure, as well as model parameters, are important determinants of conservation outcomes. Finally, control strategies that can mitigate these negative consequences are identified. Managers working in similar data‐poor ecosystems can use the predictive tool to assess the probability that their system will exhibit boom‐bust dynamics, without knowing exact community parameter values.     

Poor nutritional condition promotes high-risk behaviours: a systematic review and meta-analysis

Animal behaviour can lead to varying levels of risk, and an individual's physical condition can alter the potential costs and benefits of undertaking risky behaviours. How risk-taking behaviour depends on condition is subject to contrasting hypotheses. The asset protection principle proposes that individuals in better condition should be more risk averse, as they have higher future reproductive potential (i.e. more to lose). The state-dependent safety hypothesis proposes that high-condition individuals that are more likely to survive and maximise the benefits of risky situations may make apparently riskier choices, as their individual risk is in fact lower. We systematically searched for studies that experimentally manipulated animals’ nutritional or energetic condition through diet treatments, and subsequently measured risk-taking behaviour in contexts relating to predation, novelty and exploration. Our meta-analysis quantified condition effects on risk-taking behaviour at both the mean and variance level. We preregistered our methods and hypotheses prior to conducting the study. Phylogenetic multilevel meta-analysis revealed that the lower-nutritional-condition individuals showed on average ca. 26% greater tendency towards risk than high-condition individuals (95% confidence interval: 15–38%; N = 126 studies, 1297 effect sizes). Meta-regressions revealed several factors influencing the overall effect, such as the experimental context used to measure risk-taking behaviour, and the life stage when condition was manipulated. Meta-analysis of variance revealed no clear overall effect of condition on behavioural variance (on average ca. 3% decrease in variance in low- versus high-condition groups; 95% confidence interval: −8 to 3%; N = 119 studies, 1235 effect sizes), however, the experimental context was an important factor influencing the strength and direction of the variance effect. Our comprehensive systematic review and meta-analysis provide insights into the roles of state dependency and plasticity in intraspecific behavioural variation. While heterogeneity among effect sizes was high, our results show that poor nutritional state on average increases risk taking in ecological contexts involving predation, novelty and exploration.     

Breaking down shell strength: inferences from experimental compression and future directions enabled by 3D printing

Mollusc and brachiopod shells have served as biological armour for hundreds of millions of years. Studying shell strength in compression experiments can provide insights into macroevolution, predator–prey dynamics, and anthropogenic impacts on aquatic ecosystems. These studies have been conducted across fields including palaeontology, ecology, conservation biology and engineering using a range of techniques for a variety of purposes. Using this approach, studies have demonstrated that predators can cause changes in prey shell morphology in the laboratory over both short timescales and over longer evolutionary timescales. Similarly, environmental factors such as nutrient concentration and ocean acidification have been shown to influence shell strength. Experimental compression tests have been used to study the functional morphology of shell-crushing predators and to test how the taphonomic state of shells (e.g. presence of drill holes, degree of shell degradation) may influence their likelihood of being preserved in the fossil record. This review covers the basic principles and experimental design of compression tests used to infer shell strength. Although many investigations have used this methodology, few provide a detailed explanation of how meaningfully to interpret data generated using compression experiments for those unfamiliar with this method. Furthermore, this review provides a compilation of the findings of studies that have employed these experimental methods to address specific themes: taphonomy, morphology, predation, environmental variables, and climate change. Many authors have used experimental compression tests, however, disparities among methodologies (e.g. in experimental design, taxa, specimen preservation, etc.) limit the applicability of findings from taxon-specific studies to broader eco-evolutionary questions. The review highlights confounding factors, such as shell thickness, size, damage, microstructure, and taphonomic state, and address how they can be mitigated using three-dimensional (3D)-printed model shells. 3D prints have been demonstrated as valuable proxies for understanding aspects of shell morphology that cannot otherwise be experimentally isolated. Using 3D printed models allows simplification of complex biological systems for idealized experimental studies. Such studies can isolate specific aspects of shell morphology to establish fundamental relationships between form and function. Establishing standardized methods of testing shell strength in this way will not only permit comparison across studies but also will enable investigators systematically to add complexity to their models.     

Heritability of anti‐predatory traits: vigilance and locomotor performance in marmots

Animals must allocate some proportion of their time to detecting predators. In birds and mammals, such anti‐predator vigilance has been well studied, and we know that it may be influenced by a variety of intrinsic and extrinsic factors. Despite hundreds of studies focusing on vigilance and suggestions that there are individual differences in vigilance, there have been no prior studies examining its heritability in the field. Here, we present one of the first reports of (additive) genetic variation in vigilance. Using a restricted maximum likelihood procedure, we found that, in yellow‐bellied marmots (Marmota flaviventris), the heritability of locomotor ability (h² = 0.21), and especially vigilance (h² = 0.08), is low. These modest heritability estimates suggest great environmental variation or a history of directional selection eliminating genetic variation in these traits. We also found a significant phenotypic (r_P = ?0.09 ± 0.04, P = 0.024) and a substantial, but not significant, genetic correlation (r_A = ?0.57 ± 0.28, P = 0.082) between the two traits (slower animals are less vigilant while foraging). We found no evidence of differential survival or longevity associated with particular phenotypes of either trait. The genetic correlation may persist because of environmental heterogeneity and genotype‐by‐environment interactions maintaining the correlation, or because there are two ways to solve the problem of foraging in exposed areas: be very vigilant and rely on early detection coupled with speed to escape, or reduce vigilance to minimize time spent in an exposed location. Both strategies seem to be equally successful, and this ‘locomotor ability‐wariness’ syndrome may therefore allow slow animals to compensate behaviourally for their impaired locomotor ability.     

Timing and intensity of bush cricket predation on egg batches of pine processionary moth: no evidence of population control

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Temporal activity of spiders and earwigs during winter in apple trees under a Mediterranean climate

It is well known that spiders are present in high numbers in orchards and may contribute to biocontrol. Some recent studies in central Europe further showed that some spiders are active year-round and consume pests even in winter. Using cardboard traps laid every two weeks, we carried out a survey to determine which spider and earwig species are active from September to May in an experimental, pesticide-free, apple orchard under a Mediterranean climate. We observed that spider activity was never completely absent. The structure of the spider communities showed a marked seasonality in three periods (so-called ‘autumn’, ‘winter’ and ‘spring’). Only two spider genera, Philodromus and Trachelas, were highly active in winter (percentage of catches during this season above 40%) and six others (Lathys, Clubiona, Gnaphosa, Theridion, Phrurolithus) had moderate activity (between 20 and 40%). The two earwig species had different patterns of winter activity with Forficula auricularia almost absent whereas F. pubescens was moderately active on trees. Spider community abundance, diversity and evenness significantly decreased between autumn and winter and remained low in the following spring probably because the attractiveness of the traps is much lower at this time of year due to mild temperatures and the presence of leaves on the trees. Winter-active spiders could contribute to pest biocontrol during the cold season and we advocate that the use of broad-spectrum pesticides at the end of winter, as classically applied in orchards, may be counter-productive for pest control.     

Perils of ingesting harmful prey by advanced snakes

The advanced snakes (Alethinophidia) include the extant snakes with a highly evolved head morphology providing increased gape and jaw flexibility. Along with other physiological and morphological adaptations, this allows them to immobilize, ingest, and transport prey that may be disproportionately large or presents danger to the predator from bites, teeth, horns, or spines. Reported incidents of snakes failing to consume prey and being injured or killed during feeding mostly reflect information in the form of natural-history notes. Here we provide the first extensive review of such incidents, including 101 publications describing at least 143 cases of mortality (including six of ‘multiple individuals’) caused by ingestion or attempted consumption of injurious prey. We also report on 15 previously unpublished injurious feeding incidents from the USA, Austria, and Bulgaria, including mortality of five juvenile piscivorous dice snakes (Natrix tessellata) from a single location. Occurrences are spread across taxa, with mortality documented for at least 73 species from eight families and 45 genera. Incidents were generally well represented within each of three major categories: oversized prey (40.6%), potentially harmful prey (40.6%), and predator's behavioural/mechanical errors (18.9%). Reptile (33%) and fish (26%) prey caused disproportionately high mortality compared to mammals (16%). Feeding can be dangerous throughout a snake's life, with the later stages of feeding likely being more perilous. The number of reports has increased over time, and the data seem biased towards localities with a higher number of field-working herpetologists. We propose a standardized framework, comprising a set of basic information that should ideally be collected and published, and which could be useful as a template for future data collection, reporting, and analyses. We conclude that incidents of mortality during feeding are likely to be more common than previously assumed, and this hypothesis has implications for the ecology of persistence where populations are impacted by changing trophic environments.