Alejandro C. Costamagna

PREDATORS EXERT TOP‐DOWN CONTROL OF SOYBEAN APHID ACROSS A GRADIENT OF AGRICULTURAL MANAGEMENT SYSTEMS

The discovery of soybean aphid, Aphis glycines Matusumura, in North America in 2000 provided the opportunity to investigate the relative strength of top-down and bottom-up forces in regulating populations of this new invasive herbivore. At the Kellogg Biological Station Long Term Ecological Research site in agroecology, we contrasted A. glycines establishment and population growth under three agricultural production systems that differed markedly in disturbance and fertility regimes. Agricultural treatments consisted of a conventional-tillage high-input system, a no-tillage high-input system, and a zero-chemical-input system under conventional tillage. By selectively restricting or allowing predator access we simultaneously determined aphid response to top-down and bottom-up influences. Irrespective of predator exclusion, our agricultural manipulations did not result in bottom-up control of A. glycines intrinsic rate of increase or realized population growth. In contrast, we observed strong evidence for top-down control of A. glycines establishment and overall population growth in all production systems. Abundant predators, including Harmonia axyridis, Coccinella septempunctata, Orius insidiosus, and various predaceous fly larvae, significantly reduced A. glycines establishment and population increase in all trials. In contrast to other systems in which bottom-up forces control herbivore populations, we conclude that A. glycines is primarily controlled via top-down influences of generalist predators under a wide range of agricultural management systems. Understanding the role of top-down and bottom-up forces in this context allows agricultural managers to focus on effective strategies for control of this invasive pest.

Manipulating plant resources to enhance beneficial arthropods in agricultural landscapes

Abstract Annual crop fields typically are simple habitats dominated by a few plant species where pesticides play a major role in managing weed and insect infestations. Recently, there has been significant interest in the potential to reduce reliance on pesticides by manipulating plant species and communities to benefit natural enemies of insects and weeds. Such efforts aim to enhance natural enemy impact by providing appropriate food, shelter, and hosts, and efforts typically are accomplished by manipulation of plant species, populations, or communities. Habitat management is generally viewed as an important factor in maintaining stable insect and natural enemy populations in agricultural systems and may have a similar function in increasing weed seed predation. Crop and noncrop habitats provide resources to natural enemies either directly through floral nectar and pollen, indirectly by increased host or prey availability, or through emergent properties of the habitat such as by moderating the microclimate. These critical resources for natural enemies can be provided in agricultural ecosystems at several scales: within fields, at field margins, or as a component of the larger landscape. Because individual natural enemy species may require quite specific resources at different times and spatial scales, not all attempts to manipulate habitat diversity are equally effective. We review the role of plant resources, including weeds, in supporting natural enemy communities and provide case studies of how varying plant diversity at different spatial scales can influence the effectiveness of biological control in agricultural landscapes.

Suppression of soybean aphid by generalist predators results in a trophic cascade in soybeans

Top-down regulation of herbivores in terrestrial ecosystems is pervasive and can lead to trophic cascades that release plants from herbivory. Due to their relatively simplified food webs, agroecosystems may be particularly prone to trophic cascades, a rationale that underlies biological control. However, theoretical and empirical studies show that, within multiple enemy assemblages, intraguild predation (IGP) may lead to a disruption of top-down control by predators. We conducted a factorial field study to test the separate and combined effects of predators and parasitoids in a system with asymmetric IGP. Specifically we combined ambient levels of generalist predators (mainly Coccinellidae) of the soybean aphid, Aphis glycines Matsumura, with controlled releases of the native parasitoid Lysiphlebus testaceipes (Cresson) and measured their impact on aphid population growth and soybean biomass and yield. We found that generalist predators provided strong, season-long aphid suppression, which resulted in a trophic cascade that doubled soybean biomass and yield. However, contrary to our expectations, L. testaceipes provided minor aphid suppression and only when predators were excluded, which resulted in nonadditive effects when both groups were combined. We found direct and indirect evidence of IGP, but because percentage parasitism did not differ between predator exclusion and ambient predator treatments, we concluded that IGP did not disrupt parasitism during this study. Our results support theoretical predictions that intraguild predators which also provide strong herbivore suppression do not disrupt top-down control of herbivores.

Probability of Cost-Effective Management of Soybean Aphid (Hemiptera: Aphididae) in North America

ABSTRACT Soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is one of the most damaging pests of soybean, Glycine max (L.) Merrill, in the midwestern United States and Canada. We compared three soybean aphid management techniques in three midwestern states (Iowa, Michigan, and Minnesota) for a 3-yr period (2005–2007). Management techniques included an untreated control, an insecticidal seed treatment, an insecticide fungicide tank-mix applied at flowering (i.e., a prophylactic treatment), and an integrated pest management (IPM) treatment (i.e., an insecticide applied based on a weekly scouting and an economic threshold). In 2005 and 2007, multiple locations experienced aphid population levels that exceeded the economic threshold, resulting in the application of the IPM treatment. Regardless of the timing of the application, all insecticide treatments reduced aphid populations compared with the untreated, and all treatments protected yield as compared with the untreated. Treatment efficacy and cost data were combined to compute the probability of a positive economic return. The IPM treatment had the highest probability of cost effectiveness, compared with the prophylactic tank-mix of fungicide and insecticide. The probability of surpassing the gain threshold was highest in the IPM treatment, regardless of the scouting cost assigned to the treatment (ranging from

Temporal variation in the response of parasitoids to agricultural landscape structure

0.00 to

Performance and prospects of Rag genes for management of soybean aphid

19.76/ha). Our study further confirms that a single insecticide application can enhance the profitability of soybean production at risk of a soybean aphid outbreak if used within an IPM based system.

Within-Plant Distribution of Soybean Aphid (Hemiptera: Aphididae) and Development of Node-Based Sample Units for Estimating Whole-Plant Densities in Soybean

Temporal variations in the relationship between agricultural landscape complexity and parasitoid abundance were assessed in Ingham County, MI. The study site consisted of a 3. 2k m× 13.9 km area including a complex and a simplified agricultural landscape. Landscape structure was quantified using black and white aerial photographs and digital land-use data. A heterogeneous mixture of crop and non-crop habitats characterized the complex landscape (40.6% of non-crop habitat), while the simple landscape was more uniform and contained less non-crop habitat (28.6%). In the complex landscape fields were 75% smaller, had 63% more perimeter of wooded field edge per hectare of field area, and 81% more field edge in wide hedgerow than in the simple landscape. In June–July 1993, 1996, 1998, 2000, and 2001, a total of 15,786 armyworm (Pseudaletia unipuncta) larvae were released into maize fields. A total of 3752 larvae were recovered and reared in the laboratory with 1410 individuals parasitized by 15 identified species of parasitoids. Two species, Glyptapanteles militaris and Meteorus communis, represented 96.3% of the parasitoids recovered. Agricultural landscape structure influenced the temporal dynamics of P. unipunctaparasitism. While G. militaris was equally present in the simple (48.8% of total recovery) and complex landscape (51.2%), M. communiswas found mostly in the complex landscape (78.9%). Overall, percentage parasitism differed between landscapes and among years with different trends in the simple and complex landscapes. These results indicate that effects of landscape structure on parasitism are not adequately characterized by short-term studies.

An exponential growth model with decreasing r captures bottom-up effects on the population growth of Aphis glycines Matsumura (Hemiptera: Aphididae)

The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is an invasive insect pest of soybean [Glycine max (L.) Merr. (Fabaceae)] in North America, and it has led to extensive insecticide use in northern soybean‐growing regions there. Host plant resistance is one potential alternative strategy for managing soybean aphid. Several Rag genes that show antibiosis and antixenosis to soybean aphid have been recently identified in soybean, and field‐testing and commercial release of resistant soybean lines have followed. In this article, we review results of field tests with soybean lines containing Rag genes in North America, then present results from a coordinated regional test across several field sites in the north‐central USA, and finally discuss prospects for use of Rag genes to manage soybean aphids. Field tests conducted independently at multiple sites showed that soybean aphid populations peaked in late summer on lines with Rag1 or Rag2 and reached economically injurious levels on susceptible lines, whereas lines with a pyramid of Rag1 + Rag2 held soybean aphid populations below economic levels. In the regional test, aphid populations were generally suppressed by lines containing one of the Rag genes. Aphids reached putative economic levels on Rag1 lines for some site years, but yield loss was moderated, indicating that Rag1 may confer tolerance to soybean aphid in addition to antibiosis and antixenosis. Moreover, no yield penalty has been found for lines with Rag1, Rag2, or pyramids. Results suggest that use of aphid‐resistant soybean lines with Rag genes may be viable for managing soybean aphids. However, virulent biotypes of soybean aphid were identified before release of aphid‐resistant soybean, and thus a strategy for optimal deployment of aphid‐resistant soybean is needed to ensure sustainability of this technology.

Effect of food resources on adult Glyptapanteles militaris and Meteorus communis (Hymenoptera: Braconidae), parasitoids of Pseudaletia unipuncta (Lepidoptera: Noctuidae)

Abstract The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is capable of reducing soybean, Glycine max (L.) Merr., yield up to 40% during severe outbreaks. Frequent sampling, which can be costly and time-consuming, is essential to making informed management decisions. However, one way to decrease sampling effort is to use a reduced sample unit when possible. The objectives of this study were to describe the vertical distribution of soybean aphid within soybean over time and to define node-based sample units of varying sizes by testing the ability of selected units to accurately estimate whole-plant aphid density. Within-plant distribution of soybean aphid changed significantly with time. However, the average nodal position where soybean aphids were found on soybean remained within the top half of the plant at all three locations studied across all sample dates. Consequently, selecting the node with the highest aphid density multiplied by the total number of infested nodes (NMAX′) was the best predictor of aphids on remaining soybean components in both the original (r2 = 0.855) and validation (r2 = 0.824) data sets. For sample units that included more than a single node to estimate densities, a weighted formula, which incorporated changes observed in the within-plant aphid distribution, improved model performance (higher r2 values) and reduced variability around parameter estimates compared with a node-averaged formula. Our results suggest that smaller sample units provide reliable estimations of whole-plant aphid density throughout the growing season for differently maturing soybean, which is essential to their use in pest management decisions and development of future sampling plans.

Landscape-scale pest suppression is mediated by timing of predator arrival

1 There is ample evidence that the life history and population dynamics of aphids are closely linked to plant phenology. Based on life table studies, it has been proposed that the growth of aphid populations could be modeled with an exponential growth model, with r decreasing linearly with time. This model has never been tested under field conditions.