Fang Ouyang

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.

Effects of transgenic Bt cotton on overwintering characteristics and survival of Helicoverpa armigera.

The effects of transgenic Bt cotton on the overwintering generation of the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae), are unknown. We hypothesized that a Bt cotton diet may adversely affect fitness of this generation and examined fresh weight, lipids, glycogens, low-molecular-weight sugars and SCPs (supercooling points) of pupae, as well as survival of larvae, diapausing pupae and adult emergence in comparison with controls. Field and laboratory experiments showed that larvae fed on Bt cotton had a decreased pupation rate, and fewer entered diapause and emerged as adults compared with larvae fed non-Bt cotton. Furthermore, larvae fed Bt cotton had reduced pupal weight, glycogen content and trehalose levels both in diapausing and in non-diapausing pupae, and only diapausing pupae had an increased SCP compared to controls. The SCPs of diapausing pupae reared on Bt cotton were significantly higher than those reared on non-Bt cotton. The trehalose levels of diapausing pupae reared on Bt cotton were significantly lower than those of larvae reared on non-Bt cotton. Thus, these results suggest that a Bt cotton diet weakens the preparedness of cotton bollworm for overwintering and reduces survival of the overwintering generation, which will in turn reduce the density of the first generation in the following year. Effects of transgenic Bt cotton on the overwintering generation of cotton bollworm appear to have significantly contributed to the suppression of cotton bollworm observed throughout northern China in the past decade.

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.

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.

Intra-Species Mixture Alters Pest and Disease Severity in Cotton

ABSTRACT Widespread planting of crops genetically modified to express Bacillus thuringiensis (Bt) toxins for pest control may potentially affect nontarget pests and soil-borne disease. In this study, a field trial was conducted to explore the effects of habitat diversification, specifically an intraspecies mixture of genetically distinct cotton lines, on nontarget pests and soil-borne disease. It was hypothesized that the mixture would suppress disease severity and would alter pest and predator abundances. Results confirmed that a row-mixture of 75% insect-resistant cotton and 25% disease-resistant cotton suppressed Fusarium wilt and controlled cotton aphids. However, intercropping at the genotypic level increased mirid bug and sweetpotato whitefly densities in cotton. Moreover, the effect of the mixture on predator abundance ranged from neutral to positive and was highly variable among species and years. Species-specific pest responses to the crop mixture provide new insights for optimally sized and configured refuge construction in the future.

Cascade effects of crop species richness on the diversity of pest insects and their natural enemies

Understanding how plant species richness influences the diversity of herbivorous and predatory/parasitic arthropods is central to community ecology. We explore the effects of crop species richness on the diversity of pest insects and their natural enemies. Using data from a four-year experiment with five levels of crop species richness, we found that crop species richness significantly affected the pest species richness, but there were no significant effects on richness of the pests’ natural enemies. In contrast, the species richness of pest insects significantly affected their natural enemies. These findings suggest a cascade effect where trophic interactions are strong between adjacent trophic levels, while the interactions between connected but nonadjacent trophic levels are weakened by the intermediate trophic level. High crop species richness resulted in a more stable arthropod community compared with communities in monoculture crops. Our results highlight the complicated cross-trophic interactions and the crucial role of crop diversity in the food webs of agro-ecosystems.

The seesaw effect of winter temperature change on the recruitment of cotton bollworms Helicoverpa armigera through mismatched phenology.

Abstract Knowing how climate change affects the population dynamics of insect pests is critical for the future of integrated pest management. Rising winter temperatures from global warming can drive increases in outbreaks of some agricultural pests. In contrast, here we propose an alternative hypothesis that both extremely cold and warm winters can mismatch the timing between the eclosion of overwintering pests and the flowering of key host plants. As host plants normally need higher effective cumulative temperatures for flowering than insects need for eclosion, changes in flowering time will be less dramatic than changes in eclosion time, leading to a mismatch of phenology on either side of the optimal winter temperature. We term this the “seesaw effect.” Using a long‐term dataset of the Old World cotton bollworm Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) in northern China, we tested this seesaw hypothesis by running a generalized additive model for the effects of the third generation moth in the preceding year, the winter air temperature, the number of winter days below a critical temperature and cumulative precipitation during winter on the demography of the overwintering moth. Results confirmed the existence of the seesaw effect of winter temperature change on overwintering populations. Pest management should therefore consider the indirect effect of changing crop phenology (whether due to greenhouse cultivation or to climate change) on pest outbreaks. As arthropods from mid‐ and high latitudes are actually living in a cooler thermal environment than their physiological optimum in contrast to species from lower latitudes, the effects of rising winter temperatures on the population dynamics of arthropods in the different latitudinal zones should be considered separately. The seesaw effect makes it more difficult to predict the average long‐term population dynamics of insect pests at high latitudes due to the potential sharp changes in annual growth rates from fluctuating minimum winter temperatures.

Orientation behavior of Propylaea japonica toward visual and olfactory cues from its prey–host plant combination

The lady beetle Propylaea japonica (Thunberg) (Coleoptera: Coccinellidae) is an important predator of aphids in agroecosystems. The inundative release of coccinellid beetles can be an effective biological control strategy. An understanding of how biological control agents perceive and use stimuli from host plants is the key to successfully implement commercially produced predators. Here, we studied the relative role of visual and volatile cues. Dual‐choice assays using foraging‐naïve and foraging‐experienced P. japonica adults were conducted using cotton plants [Gossypium hirsutum L. (Malvaceae)] with or without infestation by the cotton aphid, Aphis gossypii (Glover) (Hemiptera: Aphididae). Overall, experienced beetles were more attracted than naïve beetles toward cues associated with aphid‐infested plants. Experienced beetles were also more responsive to olfactory cues compared with naïve beetles. Both foraging‐naïve and ‐experienced lady beetles integrate olfactory and visual cues from plants infested with aphids, with an apparently greater reliance on olfactory cues. The results suggest that foraging experience may increase prey location in P. japonica.