Zi-Hua Zhao

The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology

The harlequin ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), is native to Asia but has been intentionally introduced to many countries as a biological control agent of pest insects. In numerous countries, however, it has been introduced unintentionally. The dramatic spread of H. axyridis within many countries has been met with considerable trepidation. It is a generalist top predator, able to thrive in many habitats and across wide climatic conditions. It poses a threat to biodiversity, particularly aphidophagous insects, through competition and predation, and in many countries adverse effects have been reported on other species, particularly coccinellids. However, the patterns are not consistent around the world and seem to be affected by many factors including landscape and climate. Research on H. axyridis has provided detailed insights into invasion biology from broad patterns and processes to approaches in surveillance and monitoring. An impressive number of studies on this alien species have provided mechanistic evidence alongside models explaining large-scale patterns and processes. The involvement of citizens in monitoring this species in a number of countries around the world is inspiring and has provided data on scales that would be otherwise unachievable. Harmonia axyridis has successfully been used as a model invasive alien species and has been the inspiration for global collaborations at various scales. There is considerable scope to expand the research and associated collaborations, particularly to increase the breadth of parallel studies conducted in the native and invaded regions. Indeed a qualitative comparison of biological traits across the native and invaded range suggests that there are differences which ultimately could influence the population dynamics of this invader. Here we provide an overview of the invasion history and ecology of H. axyridis globally with consideration of future research perspectives. We reflect broadly on the contributions of such research to our understanding of invasion biology while also informing policy and people.

Effects of agricultural intensification on ability of natural enemies to control aphids

Agricultural intensification through increasing fertilization input and cropland expansion has caused rapid loss of semi-natural habitats and the subsequent loss of natural enemies of agricultural pests. It is however extremely difficult to disentangle the effects of agricultural intensification on arthropod communities at multiple spatial scales. Based on a two-year study of seventeen 1500 m-radius sites, we analyzed the relative importance of nitrogen input and cropland expansion on cereal aphids and their natural enemies. Both the input of nitrogen fertilizer and cropland expansion benefited cereal aphids more than primary parasitoids and leaf-dwelling predators, while suppressing ground-dwelling predators, leading to an disturbance of the interspecific relationship. The responses of natural enemies to cropland expansion were asymmetric and species-specific, with an increase of primary parasitism but a decline of predator/pest ratio with the increasing nitrogen input. As such, agricultural intensification (increasing nitrogen fertilizer and cropland expansion) can destabilize the interspecific relationship and lead to biodiversity loss. To this end, sustainable pest management needs to balance the benefit and cost of agricultural intensification and restore biocontrol service through proliferating the role of natural enemies at multiple scales.

Weakening density dependence from climate change and agricultural intensification triggers pest outbreaks: a 37-year observation of cotton bollworms

Understanding drivers of population fluctuation, especially for agricultural pests, is central to the provision of agro-ecosystem services. Here, we examine the role of endogenous density dependence and exogenous factors of climate and human activity in regulating the 37-year population dynamics of an important agricultural insect pest, the cotton bollworm (Helicoverpa armigera), in North China from 1975 to 2011. Quantitative time-series analysis provided strong evidence explaining long-term population dynamics of the cotton bollworm and its driving factors. Rising temperature and declining rainfall exacerbated the effect of agricultural intensification on continuously weakening the negative density dependence in regulating the population dynamics of cotton bollworms. Consequently, ongoing climate change and agricultural intensification unleashed the tightly regulated pest population and triggered the regional outbreak of H. armigera in 1992. Although the negative density dependence can effectively regulate the population change rate to fluctuate around zero at stable equilibrium levels before and after outbreak in the 1992, the population equilibrium jumped to a higher density level with apparently larger amplitudes after the outbreak. The results highlight the possibility for exogenous factors to induce pest outbreaks and alter the population regulating mechanism of negative density dependence and, thus, the stable equilibrium of the pest population, often to a higher level, posing considerable risks to the provision of agro-ecosystem services and regional food security. Efficient and timely measures of pest management in the era of Anthropocene should target the strengthening and revival of weakening density dependence caused by climate change and human activities.

Laboratory and field efficacy of entomopathogenic fungi for the management of the sweetpotato weevil, Cylas formicarius (Coleoptera: Brentidae)

The sweetpotato weevil, Cylas formicarius (F.) (Coleoptera: Brentidae), is one of the most important pests of sweet potatoes in the world. With free trade between the United States and the U.S.-controlled Mariana Islands, C. formicarius has spread along with this commodity. Because of the cryptic nature of the larvae and nocturnal activity of the adults, and the cancellation of long-residual pesticides, this pest has become increasingly difficult to control. Therefore, the present study sought to explore and to compare the effectiveness of Metarhizium brunneum F52 (90ml a.i./ha), Beauveria bassiana GHA (40ml a.i./ha), spinosad (90g a.i./ha), azadirachtin (1484ml a.i./ha), B. bassiana+M. brunneum (20ml a.i./ha+45ml a.i./ha), B. bassiana+azadirachtin (20ml a.i./ha+742ml a.i./ha), B. bassiana+spinosad (20ml a.i./ha+45ml a.i./ha), M. brunneum+azadirachtin (45ml a.i./ha+742ml a.i./ha) and M. brunneum+spinosad (45ml a.i./ha+45 grams a.i./ha) in controlling this pest in both the laboratory and the field. The treatment with B. bassiana+M. brunneum was the most effective in reducing tuber damage by C. formicarius, producing the highest yields. The most adult cadavers were found in plots treated with the combination of two fungi. This combined fungal formulation appears to be appropriate for the practical control of C. formicarius on sweet potatoes.

Responses of Cereal Aphids and Their Parasitic Wasps to Landscape Complexity

ABSTRACT The intensification of agriculture has caused a decline in the complexity of agricultural landscapes because of the expansion of arable lands and the removal of natural habitats. These landscape changes, which have substantial effects on natural enemies (e.g., parasitoids) and on biological control services, have received considerable attention recently. In the current study, we analyzed the effects of landscape complexity on cereal aphids and their parasitic wasps in 24 sites during a period of 3 yr. In total, 11 primary parasitoid species and 6 hyperparasitoid species, comprising 5,220 individuals, were collected in our experiments. With the exception of two primary parasitic wasps (Trioxys asiaticus Telenga and Toxares sp.) and one hyperparasitic wasp (Dendrocerus carpenteri [Curtis]), most species were sensitive to landscape complexity after ≥1 yr. Species diversity, primary parasitism, and hyperparasitism increased with increasing landscape complexity. However, the relationship between the population density of active primary parasitoids (effective primary parasitoids) and landscape complexity was indicated by a quadratic function, not a linear function. The effective population density of primary parasitoids was maximal (2.04 individuals per 100 wheat stems) if the percentage of noncrop habitat was 38%. The hypothesis that landscape complexity may enhance the activity or higher diversity of primary parasitoids and hyperparasitoids was well-supported by our study. However, the hyperparasitoids had a more sensitive response to landscape complexity than the primary parasitoids. Further studies should aim to enhance the biological pest control of primary parasitoids and suppress hyperparasitoids by habitat manipulation. This technique could be used effectively for pest management in mosaic landscapes through habitat rearrangement and reorganization.

Solving the pitfalls of pitfall trapping: a two‐circle method for density estimation of ground‐dwelling arthropods

Summary Pitfall traps are widely used for investigating ground-dwelling arthropods, but have been heavily criticized due to their species-, habitat- and attractant-specific trapping radius which produces unreliable estimation of species diversity and density. We developed a two-circle method (TCM) for simultaneously estimating densities of ground-dwelling arthropods and the effective trapping radius. Multiple pairs of traps are located different distances apart, and the intersection of trapping areas can be calculated using the inverse trigonometric function. The density and effective trapping radius can be estimated from a nonlinear regression of the change in the total number of individuals caught with the distance between the paired pitfall traps. We compared the performance of TCM with the estimator based on the nested-cross array (NCA) for arranging pitfall traps, by comparing predicted densities from these two methods with the real density obtained from the suction sampling method (SSM). Simulations with known arthropod densities and effective trapping radius suggested that TCM produced accurate density estimation, while NCA significantly underestimated the known density. Pitfall trapping of ground-dwelling arthropods on two habitats (crop field and desert steppe) confirmed this conclusion when comparing estimation from TCM and NCA with densities obtained from the SSM. TCM is a promising technique for the density estimation of ground-dwelling arthropods, especially for traps with liquid attractant and areas with relatively homogenous habitat and away from habitat edges.

Maize benefits the predatory beetle, Propylea japonica (Thunberg), to provide potential to enhance biological control for aphids in cotton.

Background Biological control provided by natural enemies play an important role in integrated pest management. Generalist insect predators provide an important biological service in the regulation of agricultural insect pests. Our goal is to understand the explicit process of oviposition preference, habitat selection and feeding behavior of predators in farmland ecosystem consisting of multiple crops, which is central to devising and delivering an integrated pest management program. Methodology The hypotheses was that maize can serve as habitat for natural enemies and benefits predators to provide potential to enhance biological control for pest insects in cotton. This explicit process of a predatory beetle, Propylea japonica, in agricultural ecosystem composed of cotton and maize were examined by field investigation and stable carbon isotope analysis during 2008–2010. Principal Finding Field investigation showed that P. japonica adults will search host plants for high prey abundance before laying eggs, indicating indirectly that P. japonica adults prefer to inhabit maize plants and travel to cotton plants to actively prey on aphids. The δ13C values of adult P. japonica in a dietary shift experiment found that individual beetles were shifting from a C3- to a C4-based diet of aphids reared on maize or cotton, respectively, and began to reflect the isotope ratio of their new C4 resources within one week. Approximately 80–100% of the diet of P. japonica adults in maize originated from a C3-based resource in June, July and August, while approximately 80% of the diet originated from a C4-based resource in September. Conclusion/Significance Results suggest that maize can serve as a habitat or refuge source for the predatory beetle, P. japonica, and benefits predators to provide potential to enhance biological control for insect pests in cotton.

Regulation of circadian locomotor rhythm by neuropeptide Y-like system in Drosophila melanogaster.

Circadian rhythms in behaviour and physiology exist widely in animals, plants, fungi and cyanobacteria. Although much work has been carried out to characterize the endogenous clock circuit, the output signals coupling the circadian pacemaker to behaviour and physiology remain elusive. Here, we show that neuropeptide F (NPF), a homologue of mammalian neuropeptide Y, and its G protein‐coupled receptor NPFR1 regulate the locomotor rhythm in Drosophila melanogaster. Flies with loss of function in NPF or NPFR1 were unable to ramp up their activity before lights off under light : dark (LD) cycles, and oscillations in npf/NPF and npfr1/NPFR1 were found to correlate temporally with the locomotor rhythm. Furthermore, NPF is expressed in clock neurones including dorsolateral neurones (LNds) and ventrolateral neurones (LNvs), whereas NPFR1 is expressed in dorsal neurone 1 (DN1) and LNds. These results show that NPF signalling is involved in the circadian locomotor rhythm in LD cycles.

Effects of crop species richness on pest-natural enemy systems based on an experimental model system using a microlandscape.

The relationship between crop richness and predator-prey interactions as they relate to pest-natural enemy systems is a very important topic in ecology and greatly affects biological control services. The effects of crop arrangement on predator-prey interactions have received much attention as the basis for pest population management. To explore the internal mechanisms and factors driving the relationship between crop richness and pest population management, we designed an experimental model system of a microlandscape that included 50 plots and five treatments. Each treatment had 10 repetitions in each year from 2007 to 2010. The results showed that the biomass of pests and their natural enemies increased with increasing crop biomass and decreased with decreasing crop biomass; however, the effects of plant biomass on the pest and natural enemy biomass were not significant. The relationship between adjacent trophic levels was significant (such as pests and their natural enemies or crops and pests), whereas non-adjacent trophic levels (crops and natural enemies) did not significantly interact with each other. The ratio of natural enemy/pest biomass was the highest in the areas of four crop species that had the best biological control service. Having either low or high crop species richness did not enhance the pest population management service and lead to loss of biological control. Although the resource concentration hypothesis was not well supported by our results, high crop species richness could suppress the pest population, indicating that crop species richness could enhance biological control services. These results could be applied in habitat management aimed at biological control, provide the theoretical basis for agricultural landscape design, and also suggest new methods for integrated pest management.

The cloning and expression of α‐tubulin in Monochamus alternatus

The Japanese pine sawyer Monochamus alternatus is one of the major forest pests. It damages pine directly and transfers the nematode Bursaphelenchus xylophilus to pine wood; resulting in serious economic losses around the world every year. α‐tubulin is one of most important proteins in most species. We cloned a ubiquitously expressed M. alternatusα‐tubulin gene and analysed its nucleotides and protein structure; its sequence characters are consistent with what have been reported in other insects. The alignment of proteins showed that there is high homology of α‐tubulin between M. alternatus and other species. Western blot and immunocytochemistry analyses suggested a common epitope of α‐tubulin between M. alternatus and Strongylcentrotus purpuratus. We also expressed the protein in Escherichia coli for further functional studies.