Residence time determines invasiveness and performance of garlic mustard (Alliaria petiolata) in North America.

While biological invasions have the potential for large negative impacts on local communities and ecological interactions, increasing evidence suggests that species once considered major problems can decline over time. Declines often appear driven by natural enemies, diseases or evolutionary adaptations that selectively reduce populations of naturalised species and their impacts. Using permanent long-term monitoring locations, we document declines of Alliaria petiolata (garlic mustard) in eastern North America with distinct local and regional dynamics as a function of patch residence time. Projected site-specific population growth rates initially indicated expanding populations, but projected population growth rates significantly decreased over time and at the majority of sites fell below 1, indicating declining populations. Negative soil feedback provides a potential mechanism for the reported disappearance of ecological dominance of A. petiolata in eastern North America.

Predation risk differentially affects aphid morphotypes: impacts on prey behavior, fecundity and transgenerational dispersal morphology.

To avoid predation, prey initiate anti-predator defenses such as altered behavior, physiology and/or morphology. Prey trait changes in response to perceived predation risk can influence several aspects of prey biology that collectively contribute to individual success and thus population growth. However, studies often focus on single trait changes in a discrete life stage or morphotype. We assessed how predation risk by Harmonia axyridis affects several important traits in the aphid, Myzus persicae: host plant preference, fecundity and investment in dispersal. Importantly, we examined whether these traits changed in a similar way between winged (alate) and wingless (apterous) adult aphid morphotypes, which differ in morphology, but also in life-history characteristics important for reproduction and dispersal. Host plant preference was influenced by the presence of H.axyridis odors in choice tests; wingless aphids were deterred by the odor of plants with H.axyridis whereas winged aphids preferred plants with H.axyridis present. Wingless aphids reared in the presence of ladybeetle cues produced fewer offspring in the short-term, but significantly more when reared with exposure to predator cues for multiple generations. However, winged aphid fecundity was unaffected by H.axyridis cues. Lastly, transgenerational plasticity was demonstrated in response to predation risk via increased formation of winged aphid morphotypes in the offspring of predator cue-exposed wingless mothers. Importantly, we found that responses to risk differ across aphid polyphenism and that plasticity in aphid morphology occurs in response to predation risk. Together our results highlight the importance of considering how predation risk affects multiple life stages and morphotypes.

The effectiveness of flower strips and hedgerows on pest control, pollination services and crop yield: a quantitative synthesis.

Floral plantings are promoted to foster ecological intensification of agriculture through provisioning of ecosystem services. However, a comprehensive assessment of the effectiveness of different floral plantings, their characteristics and consequences for crop yield is lacking. Here we quantified the impacts of flower strips and hedgerows on pest control (18 studies) and pollination services (17 studies) in adjacent crops in North America, Europe and New Zealand. Flower strips, but not hedgerows, enhanced pest control services in adjacent fields by 16% on average. However, effects on crop pollination and yield were more variable. Our synthesis identifies several important drivers of variability in effectiveness of plantings: pollination services declined exponentially with distance from plantings, and perennial and older flower strips with higher flowering plant diversity enhanced pollination more effectively. These findings provide promising pathways to optimise floral plantings to more effectively contribute to ecosystem service delivery and ecological intensification of agriculture in the future.

Flower traits associated with the visitation patterns of bees.

Plant-pollinator interactions are partially driven by the expression of plant traits that signal and attract bees to the nutritional resources within flowers. Although multiple physical and chemical floral traits are known to influence the visitation patterns of bees, how distinct bee groups vary in their responses to floral traits has yet to be elucidated. In this study, we used a common garden experiment to test for morphological floral traits associated with pollen quantity at the plant species level, and examined how the visitation patterns of taxonomically and functionally distinct bee groups are related to flower trait characteristics of 39 wildflower species. We also determined how floral traits influence the structure of wild bee communities visiting plants and whether this varies among geographic localities. Our results suggest that floral area is the primary morphological floral trait related to bee visitation of several distinct bee groups, but that wild bee families and functionally distinct bee groups have unique responses to floral trait expression. The composition of the wild bee communities visiting different plants was most strongly associated with variability in floral area, flower height, and the quantity of pollen retained in flowers. Our results inform wildflower habitat management for bees by demonstrating that the visitation patterns of distinct bee taxa can be predicted by floral traits, and highlight that variability in these traits should be considered when selecting plants to support pollinators.

Habitat Management to Suppress Pest Populations: Progress and Prospects.

Habitat management involving manipulation of farmland vegetation can exert direct suppressive effects on pests and promote natural enemies. Advances in theory and practical techniques have allowed habitat management to become an important subdiscipline of pest management. Improved understanding of biodiversity-ecosystem function relationships means that researchers now have a firmer theoretical foundation on which to design habitat management strategies for pest suppression in agricultural systems, including landscape-scale effects. Supporting natural enemies with shelter, nectar, alternative prey/hosts, and pollen (SNAP) has emerged as a major research topic and applied tactic with field tests and adoption often preceded by rigorous laboratory experimentation. As a result, the promise of habitat management is increasingly being realized in the form of practical worldwide implementation. Uptake is facilitated by farmer participation in research and is made more likely by the simultaneous delivery of ecosystem services other than pest suppression.

Perennial grasslands enhance biodiversity and multiple ecosystem services in bioenergy landscapes.

Agriculture is being challenged to provide food, and increasingly fuel, for an expanding global population. Producing bioenergy crops on marginal lands--farmland suboptimal for food crops--could help meet energy goals while minimizing competition with food production. However, the ecological costs and benefits of growing bioenergy feedstocks--primarily annual grain crops--on marginal lands have been questioned. Here we show that perennial bioenergy crops provide an alternative to annual grains that increases biodiversity of multiple taxa and sustain a variety of ecosystem functions, promoting the creation of multifunctional agricultural landscapes. We found that switchgrass and prairie plantings harbored significantly greater plant, methanotrophic bacteria, arthropod, and bird diversity than maize. Although biomass production was greater in maize, all other ecosystem services, including methane consumption, pest suppression, pollination, and conservation of grassland birds, were higher in perennial grasslands. Moreover, we found that the linkage between biodiversity and ecosystem services is dependent not only on the choice of bioenergy crop but also on its location relative to other habitats, with local landscape context as important as crop choice in determining provision of some services. Our study suggests that bioenergy policy that supports coordinated land use can diversify agricultural landscapes and sustain multiple critical ecosystem services.

Shifts in dynamic regime of an invasive lady beetle are linked to the invasion and insecticidal management of its prey.

The spread and impact of invasive species may vary over time in relation to changes in the species itself, the biological community of which it is part, or external controls on the system. We investigate whether there have been changes in dynamic regimes over the last 20 years of two invasive species in the midwestern United States, the multicolored Asian lady beetle Harmonia axyridis and the soybean aphid Aphis glycines. We show by model selection that after its 1993 invasion into the American Midwest, the year-to-year population dynamics of H. axyridis were initially governed by a logistic rule supporting gradual rise to a stable carrying capacity. After invasion of the soybean aphid in 2000, food resources at the landscape level became abundant, supporting a higher year-to-year growth rate and a higher but unstable carrying capacity, with two-year cycles in both aphid and lady beetle abundance as a consequence. During 2005-2007, farmers in the Midwest progressively increased their use of insecticides for managing A. glycines, combining prophylactic seed treatment with curative spraying based on thresholds. This human intervention dramatically reduced the soybean aphid as a major food resource for H. axyridis at landscape level and corresponded to a reverse shift towards the original logistic rule for year-to-year dynamics. Thus, we document a short episode of major predator-prey fluctuations in an important agricultural system resulting from two biological invasions that were apparently damped by widespread insecticide use. Recent advances in development of plant resistance to A. glycines in soybeans may mitigate the need for pesticidal control and achieve the same stabilization of pest and predator populations at lower cost and environmental burden.

Trophic cascades in agricultural landscapes: indirect effects of landscape composition on crop yield.

The strength and prevalence of trophic cascades, defined as positive, indirect effects of natural enemies (predatory and parasitic arthropods) on plants, is highly variable in agroecosystems. This variation may in part be due to the spatial or landscape context in which hese trophic cascades occur. In 2011 and 2012, we conducted a natural enemy exclusion experiment in soybean fields along a gradient of landscape composition across southern Wisconsin and Michigan, USA. We used structural equation modeling to ask (1) whether natural enemies influence biocontrol of soybean aphids (SBA) and soybean yield and (2) whether landscape effects on natural enemies influence the strength of the trophic cascades. We found that natural enemies (NE) suppressed aphid populations in both years of our study, and, in 2011, the yield of soybean plants exposed to natural enemies was 37% higher than the yield of plants with aphid populations protected from natural enemies. The strength of the :rophic cascade was also influenced by landscape context. We found that landscapes with a higher proportion of soybean and higher diversity habitats resulted in more NE, fewer aphids, and, in some cases, a trend toward greater soybean yield. These results indicate that landscape context is important for understanding spatial variability in biocontrol and yield, but other factors, such as environmental variability and compensatory growth, might overwhelm the beneficial effects of biocontrol on crop yield.

Farming for Ecosystem Services: An Ecological Approach to Production Agriculture.

A balanced assessment of ecosystem services provided by agriculture requires a systems-level socioecological understanding of related management practices at local to landscape scales. The results from 25 years of observation and experimentation at the Kellogg Biological Station long-term ecological research site reveal services that could be provided by intensive row-crop ecosystems. In addition to high yields, farms could be readily managed to contribute clean water, biocontrol and other biodiversity benefits, climate stabilization, and long-term soil fertility, thereby helping meet society's need for agriculture that is economically and environmentally sustainable. Midwest farmers-especially those with large farms-appear willing to adopt practices that deliver these services in exchange for payments scaled to management complexity and farmstead benefit. Surveyed citizens appear willing to pay farmers for the delivery of specific services, such as cleaner lakes. A new farming for services paradigm in US agriculture seems feasible and could be environmentally significant.

Conservation genetics and the implication for recovery of the endangered Mitchell's satyr Butterfly, Neonympha mitchellii mitchellii.

The modern delineation of taxonomic groups is often aided by analyses of molecular data, which can also help inform conservation biology. Two subspecies of the butterfly Neonympha mitchellii are classified as federally endangered in the United States: Neonympha mitchellii mitchellii, the Mitchell's satyr, and Neonympha mitchellii francisi, the Saint Francis's satyr. The recent discovery of additional disjunct populations of N. mitchellii in the southeastern US could have important implications for both legal protection and management decisions. We elucidated the relationships among 48 individuals representing 5 N. mitchellii populations using 6 molecular markers (5 nuclear and 1 mitochondrial) under a variety of analytical frameworks. Phylogenetic analysis resulted in moderately supported clades that corresponded with the geographic region where samples originated. Clustering analyses identified 3 groups, wherein the 2 named subspecies formed separate clusters. Coalescent analyses indicated evolutionary divergence between N. m. mitchellii and all other populations but weakly supported divergence among N. m. francisi and the recently discovered populations. Hence, the 2 currently accepted subspecies were clearly different from one another, but the recently discovered populations could not be completely distinguished from N. m. francisi or each other. We propose that N. m. mitchellii and N. m. francisi continue to be managed as separate endangered species.

Agricultural landscape simplification and insecticide use in the Midwestern United States.

Agronomic intensification has transformed many agricultural landscapes into expansive monocultures with little natural habitat. A pervasive concern is that such landscape simplification results in an increase in insect pest pressure, and thus an increased need for insecticides. We tested this hypothesis across a range of cropping systems in the Midwestern United States, using remotely sensed land cover data, data from a national census of farm management practices, and data from a regional crop pest monitoring network. We found that, independent of several other factors, the proportion of harvested cropland treated with insecticides increased with the proportion and patch size of cropland and decreased with the proportion of seminatural habitat in a county. We also found a positive relationship between the proportion of harvested cropland treated with insecticides and crop pest abundance, and a positive relationship between crop pest abundance and the proportion cropland in a county. These results provide broad correlative support for the hypothesized link between landscape simplification, pest pressure, and insecticide use. Using regression coefficients from our analysis, we estimate that, across the seven-state region in 2007, landscape simplification was associated with insecticide application to 1.4 million hectares and an increase in direct costs totaling between $34 and $103 million. Both the direct and indirect environmental costs of landscape simplification should be considered in design of land use policy that balances multiple ecosystem goods and services.

Contrasting effects of bioenergy crops on biodiversity.

Agriculture is driving biodiversity loss, and future bioenergy cropping systems have the potential to ameliorate or exacerbate these effects. Using a long-term experimental array of 10 bioenergy cropping systems, we quantified diversity of plants, invertebrates, vertebrates, and microbes in each crop. For many taxonomic groups, alternative annual cropping systems provided no biodiversity benefits when compared to corn (the business-as-usual bioenergy crop in the United States), and simple perennial grass-based systems provided only modest gains. In contrast, for most animal groups, richness in plant-diverse perennial systems was much higher than in annual crops or simple perennial systems. Microbial richness patterns were more eclectic, although some groups responded positively to plant diversity. Future agricultural landscapes incorporating plant-diverse perennial bioenergy cropping systems could be of high conservation value. However, increased use of annual crops will continue to have negative effects, and simple perennial grass systems may provide little improvement over annual crops.

Landscape structure influences natural pest suppression in a rice agroecosystem.

Agricultural landscapes are constantly changing as farmers adopt new production practices and respond to changing environmental conditions. Some of these changes alter landscape structure with impacts on natural pest control, pesticide use, and conservation of biodiversity. In rice agroecosystems the effect of landscape structure on natural enemies and pest suppression is often poorly understood. Here we investigate the effect of landscape composition and configuration on a key pest of rice, the brown planthopper (Nilaparvata lugens). Using N. lugens as sentinel prey coupled with predator exclusions, we investigated landscape effects on herbivore suppression and rice grain yield at multiple spatial scales in two regions of Bangladesh. Ladybird beetles and spiders were the most abundant natural enemies of N. lugens with landscape effects observed at all scales on ladybird beetles. Specifically, ladybird beetles were positively influenced by road edges, and fallow land, while spiders were strongly influenced only by rice phenology. Predator exclusion cages showed that N. lugens abundance significantly increased in caged plots, reducing rice gain yield. We also used an estimated biocontrol service index that showed a significant positive relationship with landscape diversity and a significant negative impact on pest density and yield loss. These results suggest that promoting fallow lands and fragmented patches between rice fields could lead to more sustainable insect pest management in rice agroecosystems, potentially reducing the practice of prophylactic insecticide use.

Coexistence between similar invaders: The case of two cosmopolitan exotic insects.

Biological invasions are usually examined in the context of their impacts on native species. However, few studies have examined the dynamics between invaders when multiple exotic species successfully coexist in a novel environment. Yet, long-term coexistence of now established exotic species has been observed in North American lady beetle communities. Exotic lady beetles Harmonia axyridis and Coccinella septempunctata were introduced for biological control in agricultural systems and have since become dominant species within these communities. In this study, we investigated coexistence via spatial and temporal niche partitioning among H. axyridis and C. septempunctata using a 31-year data set from southwestern Michigan, USA. We found evidence of long-term coexistence through a combination of small-scale environmental, habitat, and seasonal mechanisms. Across years, H. axyridis and C. septempunctata experienced patterns of cyclical dominance likely related to yearly variation in temperature and precipitation. Within years, populations of C. septempunctata peaked early in the growing season at 550 degree days, while H. axyridis populations grew in the season until 1250 degree days and continued to have high activity after this point. C. septempunctata was generally most abundant in herbaceous crops, whereas H. axyridis did not display strong habitat preferences. These findings suggest that within this region H. axyridis has broader habitat and abiotic environmental preferences, whereas C. septempunctata thrives under more specific ecological conditions. These ecological differences have contributed to the continued coexistence of these two invaders. Understanding the mechanisms that allow for the coexistence of dominant exotic species contributes to native biodiversity conservation management of invaded ecosystems.

The importance of space, time, and stochasticity to the demography and management of Alliaria petiolata.

As population modeling is increasingly called upon to guide policy and management, it is important that we understand not only the central tendencies of our study systems, but the consequences of their variation in space and time as well. The invasive plant Alliaria petiolata (garlic mustard) is actively managed in the United States and is the focus of a developing biological control program. Two weevils (Coleoptera: Curculionidae: Ceutorhynchus) that reduce fecundity (C. alliariae) and rosette survival plus fecundity (C. scrobicollis) are under consideration for release pending host specificity testing. We used a demographic modeling approach to (1) quantify variability in A. petiolata growth and vital rates and (2) assess the potential for single- or multiple-agent biocontrol to suppress growth of 12 A. petiolata populations in Illinois and Michigan studied over three plant generations. We used perturbation analyses and simulation models with stochastic environments to estimate stochastic growth rates (lambda(S)) and predict the probability of successful management using either a single biocontrol agent or two agent species together. Not all populations exhibited invasive dynamics. Estimates of lambda(S) ranged from 0.78 to 2.21 across sites, while annual, deterministic growth (lambda) varied up to sevenfold within individual sites. Given our knowledge of the biocontrol agents, this analysis suggests that C. scrobicollis alone may control A. petiolata at up to 63% of our study sites where lambda >1, with the combination of both agents predicted to succeed at 88% of sites. Across sites and years, the elasticity rankings were dependent on lambda. Reductions of rosette survival, fecundity, or germination of new seeds are predicted to cause the greatest reduction of lambda in growing populations. In declining populations, transitions affecting seed bank survival have the greatest effect on lambda. This contrasts with past analyses that varied parameters individually in an otherwise constant matrix, which may yield unrealistic predictions by decoupling natural parameter covariances. Overall, comparisons of stochastic and deterministic growth rates illustrate how analyses of individual populations or years could misguide management or fail to characterize complex traits such as invasiveness that emerge as attributes of populations rather than species.

Ecology and management of the soybean aphid in North America.

The soybean aphid, Aphis glycines Matsumura, has become the single most important arthropod pest of soybeans in North America. Native to Asia, this invasive species was first discovered in North America in July 2000 and has rapidly spread throughout the northcentral United States, much of southeastern Canada, and the northeastern United States. In response, important elements of the ecology of the soybean aphid in North America have been elucidated, with economic thresholds, sampling plans, and chemical control recommendations widely adopted. Aphid-resistant soybean varieties were available to growers in 2010. The preexisting community of aphid natural enemies has been highly effective in suppressing aphid populations in many situations, and classical biological control efforts have focused on the addition of parasitoids of Asian origin. The keys to sustainable management of this pest include understanding linkages between the soybean aphid and other introduced and native species in a landscape context along with continued development of aphid-resistant varieties.

Does the Presence of the Biological Control Agent, Hypena opulenta (Lepidoptera: Erebidae) on Swallow-Worts Deter Monarch Oviposition?

Invasive black and pale swallow-worts (Vincetoxicum nigrum (L.) Moench, and Vincetoxicum rossicum Kelopow), which are related to milkweeds, can act as ecological traps for monarch butterflies (Danaus plexippus L. (Lepidoptera: Nymphalidae)) as they lay eggs on them that fail to develop. A recently approved biological control agent against swallow-worts, Hypena opulenta Christoph, occupies the same feeding guild on swallow-worts as monarch larvae and could be perceived as a competitor to monarchs. We tested how the presence of this defoliating moth on swallow-worts may influence monarch host selection. In a two-year field experiment, we placed pale swallow-wort plants that were either infested with H. opulenta or noninfested as well as common milkweed (Asclepias syriaca L.), into monarch habitats to assess oviposition rates. In the laboratory, monarchs were either given a choice or not between milkweeds and black swallow-worts with or without H. opulenta. While monarchs strongly preferred common milkweed in the field, up to 25% of the eggs we observed were laid on pale swallow-wort, without preference for swallow-wort with (10.7%) or without (14.3%) H. opulenta. In laboratory choice and no-choice tests, monarchs did not lay any eggs on black swallow-wort, likely because of the long-term laboratory rearing on common milkweeds. Our results confirm that pale swallow-wort may act as an oviposition sink to monarchs in Michigan as well. Since the biological control program is still in its infancy, the nature of interactions between monarchs and H. opulenta may change as the biocontrol agent becomes more widespread.

Increasing corn for biofuel production reduces biocontrol services in agricultural landscapes.

Increased demand for corn grain as an ethanol feedstock is altering U.S. agricultural landscapes and the ecosystem services they provide. From 2006 to 2007, corn acreage increased 19% nationally, resulting in reduced crop diversity in many areas. Biological control of insects is an ecosystem service that is strongly influenced by local landscape structure. Here, we estimate the value of natural biological control of the soybean aphid, a major pest in agricultural landscapes, and the economic impacts of reduced biocontrol caused by increased corn production in 4 U.S. states (Iowa, Michigan, Minnesota, and Wisconsin). For producers who use an integrated pest management strategy including insecticides as needed, natural suppression of soybean aphid in soybean is worth an average of $33 ha(-1). At 2007-2008 prices these services are worth at least $239 million y(-1) in these 4 states. Recent biofuel-driven growth in corn planting results in lower landscape diversity, altering the supply of aphid natural enemies to soybean fields and reducing biocontrol services by 24%. This loss of biocontrol services cost soybean producers in these states an estimated $58 million y(-1) in reduced yield and increased pesticide use. For producers who rely solely on biological control, the value of lost services is much greater. These findings from a single pest in 1 crop suggest that the value of biocontrol services to the U.S. economy may be underestimated. Furthermore, we suggest that development of cellulosic ethanol production processes that use a variety of feedstocks could foster increased diversity in agricultural landscapes and enhance arthropod-mediated ecosystem services.

Salinity Influences Plant-Pest-Predator Tritrophic Interactions.

Climate change-induced salinity intrusion into agricultural soils is known to negatively impact crop production and food security. However, the effects of salinity increase on plant-herbivore-natural enemy systems and repercussions for pest suppression services are largely unknown. Here, we examine the effects of increased salinity on communities of rice (Oryza sativa), brown planthopper (BPH), Nilaparvata lugens, and green mirid bug (GMB), Cyrtorhinus lividipennis, under greenhouse conditions. We found that elevated salinity significantly suppressed the growth of two rice cultivars. Meanwhile, BPH population size also generally decreased due to poor host plant quality induced by elevated salinity. The highest BPH density occurred at 2.0 dS/m salinity and declined thereafter with increasing salinity, irrespective of rice cultivar. The highest population density of GMB also occurred under control conditions and decreased significantly with increasing salinity. Higher salinity directly affected the rice crop by reducing plant quality measured with reference to biomass production and plant height, whereas inducing population developmental asynchrony between BPH and GMB observed at 2 dS/m salinity and potentially uncoupling prey-predator dynamics. Our results suggest that increased salinity has harmful effects on plants, herbivores, natural enemies, as well as plant-pest-predator interactions. The effects measured here suggest that the bottom-up effects of predatory insects on rice pests will likely decline in rice produced in coastal areas where salinity intrusion is common. Our findings indicate that elevated salinity influences tritrophic interactions in rice production landscapes, and further research should address resilient rice insect pest management combining multipests and predators in a changing environment.

Development and validation of node-based sample units for estimating soybean aphid (Hemiptera: Aphididae) densities in field cage experiments.

The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is currently the most important insect threat to soybean, Clycine max (L.) Merr., production in the North Central United States. Field cage studies are a key tool in investigating the potential of natural enemies and host plant resistance to control this pest. However, a major constraint in the use of cage studies is the limited number of treatments and replicates that can be used as aphid densities frequently become so large as to limit the number of experimental units that can be quantified. One way to overcome this limitation is to develop methods that estimate whole-plant aphid densities based on a reduced sampling plan. Here, we extend an existing method, node-sampling, used for estimating aphid populations in open field conditions and apply it to caged populations. We show that parameters calculated under open field conditions are inappropriate to estimate caged populations. In contrast, using four independent data sets of caged populations and a cross-validation technique, we demonstrate that a three-node sampling unit and a weighted formula provide accurate and robust estimates of whole-plant aphid density. This method reduced the number of aphids counted per plant by and average of 60%, with greater reductions at higher aphid densities. We further demonstrate that nearly identical statistical results were obtained when whole-plant or node-sampling estimates were used in the analysis of two case studies. The reduced sample unit method developed here saves time without sacrificing efficiency so that more plants, replications, or studies can be conducted that will lead to improved soybean aphid management.