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.

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.

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.

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.

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.

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.

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.

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.

Predicting Landscape Configuration Effects on Agricultural Pest Suppression.

Arthropod predators and parasitoids attack crop pests, providing a valuable ecosystem service. The amount of noncrop habitat surrounding crop fields influences pest suppression, but synthesis of new studies suggests that the spatial configuration of crops and other habitats is similarly important. Natural enemies are often more abundant in fine-grained agricultural landscapes comprising smaller patches and can increase or decrease with the connectivity of crop fields to other habitats. Partitioning organisms by traits has emerged as a promising way to predict the strength and direction of these effects. Furthermore, our ability to predict configurational effects will depend on understanding the potential for indirect effects among trophic levels and the relationship between arthropod dispersal capability and the spatial scale of underlying landscape structure.

Screening Drought-Tolerant Native Plants for Attractiveness to Arthropod Natural Enemies in the U.S. Great Lakes Region.

Arthropods provide a variety of critical ecosystem services in agricultural landscapes; however, agricultural intensification can reduce insect abundance and diversity. Designing and managing habitats to enhance beneficial insects requires the identification of effective insectary plants that attract natural enemies and provide floral resources. We tested the attractiveness of 54 plant species with tolerance to dry soils, contrasting perennial forbs and shrubs native to the Great Lakes region to selected non-native species in three common garden experiments in Michigan during 2015-2016. Overall, we found 32 species that attracted significantly more natural enemies than associated controls. Among these, Achillea millefolium and Solidago juncea were consistently among the most attractive plants at all three sites, followed by Solidago speciosa, Coreopsis tripteris, Solidago nemoralis, Pycnanthemum pilosum, and Symphyotrichum oolantangiense. Species which attracted significantly more natural enemies at two sites included: Asclepias syriaca, Asclepias tuberosa, Monarda fistulosa, Oligoneuron rigidum, Pycnanthemum virginianum, Dasiphora fruticosa, Ratibida pinnata, Asclepias verticillata, Monarda punctata, Echinacea purpurea, Helianthus occidentalis, Silphium integrifolium, Silphium terebinthinaceum, Helianthus strumosus, and Symphyotrichum sericeum. Two non-native species, Lotus corniculatus, and Centaurea stoebe, were also attractive at multiple sites but less so than co-blooming native species. Parasitic Hymenoptera were the most abundant natural enemies, followed by predatory Coleoptera and Hemiptera, while Hemiptera (Aphidae, Miridae, and Tingidae) were the most abundant herbivores. Collectively, these plant species can provide floral resources over the entire growing season and should be considered as potential insectary plants in future habitat management efforts.

A global synthesis reveals biodiversity-mediated benefits for crop production.

Human land use threatens global biodiversity and compromises multiple ecosystem functions critical to food production. Whether crop yield-related ecosystem services can be maintained by a few dominant species or rely on high richness remains unclear. Using a global database from 89 studies (with 1475 locations), we partition the relative importance of species richness, abundance, and dominance for pollination; biological pest control; and final yields in the context of ongoing land-use change. Pollinator and enemy richness directly supported ecosystem services in addition to and independent of abundance and dominance. Up to 50% of the negative effects of landscape simplification on ecosystem services was due to richness losses of service-providing organisms, with negative consequences for crop yields. Maintaining the biodiversity of ecosystem service providers is therefore vital to sustain the flow of key agroecosystem benefits to society.

Predators of monarch butterfly eggs and neonate larvae are more diverse than previously recognised.

Conserving threatened organisms requires knowledge of the factors impacting their populations. The Eastern monarch butterfly (Danaus plexippus L.) has declined by as much as 80% in the past two decades and conservation biologists are actively seeking to understand and reverse this decline. While it is well known that most monarchs die as eggs and young larvae, few studies have focused on identifying what arthropod taxa contribute to these losses. The aim of our study was to identify previously undocumented predators of immature monarchs in their summer breeding range in the United States. Using no-choice feeding assays augmented with field observations, we evaluated 75 arthropod taxa commonly found on the primary host plant for their propensity to consume immature monarchs. Here we report 36 previously unreported monarch predators, including representatives from 4 new orders (Orthoptera, Dermaptera, Lepidoptera and Opiliones) and 11 taxa (Acrididae, Gryllidae, Tettigoniidae, Forficulidae, Anthocoridae, Geocoridae, Lygaeidae, Miridae, Nabidae, Erebidae and Opilliones). Surprisingly, several putative herbivores were found to readily consume immature monarchs, both in a targeted fashion or incidentally as a result of herbivory. This work expands our understanding of the monarch predator community and highlights the importance of unrecognized predation on insects of conservation concern.

Habitat Type Influences Danaus plexippus (Lepidoptera: Nymphalidae) Oviposition and Egg Survival on Asclepias syriaca (Gentianales: Apocynaceae).

As agricultural practices intensify, species once common in agricultural landscapes are declining in abundance. One such species is the monarch butterfly (Danaus plexippus L.), whose eastern North American population has decreased approximately 80% during the past 20 yr. One hypothesis explaining the monarch's decline is reduced breeding habitat via loss of common milkweed (Asclepias syriaca L.) from agricultural landscapes in the north central United States due to the adoption of herbicide-tolerant row crops. Current efforts to enhance monarch breeding habitat primarily involve restoring milkweed in perennial grasslands. However, prior surveys found fewer monarch eggs on common milkweed in grassland versus crop habitats, indicating potential preference for oviposition in row crop habitats, or alternatively, greater egg loss to predation in grasslands. We tested these alternative mechanisms by measuring oviposition and egg predation on potted A. syriaca host plants. Our study revealed that habitat context influences both monarch oviposition preference and egg predation rates and that these patterns vary by year. We found higher monarch egg predation rates during the first 24 h after exposure and that much of the predation occurs at night. Overall, we documented up to 90% egg mortality over 72 h in perennial grasslands, while predation rates in corn were lower (10-30% mortality) and more consistent between years. These findings demonstrate that weekly monarch egg surveys are too infrequent to distinguish oviposition habitat preferences from losses due to egg predation and suggest that monarch restoration efforts need to provide both attractive and safe habitats for monarch reproduction.

Effect of Switchgrass Ecotype and Cultivar on Establishment, Feeding, and Development of Fall Armyworm (Lepidoptera: Noctuidae).

As interest in production of second-generation biofuels increases, dedicated biomass crops are likely to be called upon to help meet feedstock demands. Switchgrass (Panicum virgatum L.) is a North American native perennial grass that as a candidate biomass crop, combines high biomass yields with other desirable ecosystem services. At present, switchgrass is produced on limited acres in the United States and experiences relatively minor insect pest problems. However, as switchgrass undergoes breeding to increase biomass yield and quality, and is grown on more acres, insect pest pressure will probably increase. To investigate how currently available switchgrass ecotypes and cultivars may influence herbivory by generalist insect herbivores, we performed feeding trials using neonate and late-instar fall armyworm [Spodoptera frugiperda JE Smith (Lepidoptera: Noctuidae)]. No-choice feeding experiments were used to explore how switchgrass varieties influence larval establishment, consumption levels, and life-history traits in contrast to a preferred host, corn (Zea mays L.). Neonate S. frugiperda consumed greater amounts of corn than switchgrass and increased amounts of upland versus lowland ecotypes. Late-instar larvae, which do the majority of the larval feeding, exhibited lower consumption of lowland ecotypes, which led to increased development time and reduced pupal weights. The exception to these trends was the upland cultivar 'Trailblazer', which unexpectedly performed similarly to lowland cultivars. These results suggest that both switchgrass ecotype and cultivar can influence feeding damage by a common generalist herbivore. These findings can be used to help inform current switchgrass planting decisions as well as future breeding efforts.

Managing biological control services through multi-trophic trait interactions: review and guidelines for implementation at local and landscape scales.

Ecological studies are increasingly moving towards trait-based approaches, as the evidence mounts that functions, as opposed to taxonomy, drive ecosystem service delivery. Among ecosystem services, biological control has been somewhat overlooked in functional ecological studies. This is surprising given that, over recent decades, much of biological control research has been focused on identifying the multiple characteristics (traits) of species that influence trophic interactions. These traits are especially well developed for interactions between arthropods and flowers - important for biological control, as floral resources can provide natural enemies with nutritional supplements, which can dramatically increase biological control efficiency. Traits that underpin the biological control potential of a community and that drive the response of arthropods to environmental filters, from local to landscape-level conditions, are also emerging from recent empirical studies. We present an overview of the traits that have been identified to (i) drive trophic interactions, especially between plants and biological control agents through determining access to floral resources and enhancing longevity and fecundity of natural enemies, (ii) affect the biological control services provided by arthropods, and (iii) limit the response of arthropods to environmental filters, ranging from local management practices to landscape-level simplification. We use this review as a platform to outline opportunities and guidelines for future trait-based studies focused on the enhancement of biological control services.

Cellulosic biofuel contributions to a sustainable energy future: Choices and outcomes.

Cellulosic crops are projected to provide a large fraction of transportation energy needs by mid-century. However, the anticipated land requirements are substantial, which creates a potential for environmental harm if trade-offs are not sufficiently well understood to create appropriately prescriptive policy. Recent empirical findings show that cellulosic bioenergy concerns related to climate mitigation, biodiversity, reactive nitrogen loss, and crop water use can be addressed with appropriate crop, placement, and management choices. In particular, growing native perennial species on marginal lands not currently farmed provides substantial potential for climate mitigation and other benefits.

Scaling up our understanding of non-consumptive effects in insect systems.

Non-consumptive effects (NCEs) of predators on prey is an important topic in insect ecology with potential applications for pest management. NCEs are changes in prey behavior and physiology that aid in predation avoidance. While NCEs can have positive outcomes for prey survival there may also be negative consequences including increased stress and reduced growth. These effects can cascade through trophic systems influencing ecosystem function. Most NCEs have been studied at small spatial and temporal scales. However, recent studies show promise for the potential to manipulate NCEs for pest management. We suggest the next frontier for NCE studies includes manipulating the landscape of fear to improve pest control, which requires scaling-up to field and landscape levels, over ecologically relevant time frames.

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.

Predicting plant attractiveness to pollinators with passive crowdsourcing.

Global concern regarding pollinator decline has intensified interest in enhancing pollinator resources in managed landscapes. These efforts frequently emphasize restoration or planting of flowering plants to provide pollen and nectar resources that are highly attractive to the desired pollinators. However, determining exactly which plant species should be used to enhance a landscape is difficult. Empirical screening of plants for such purposes is logistically daunting, but could be streamlined by crowdsourcing data to create lists of plants most probable to attract the desired pollinator taxa. People frequently photograph plants in bloom and the Internet has become a vast repository of such images. A proportion of these images also capture floral visitation by arthropods. Here, we test the hypothesis that the abundance of floral images containing identifiable pollinator and other beneficial insects is positively associated with the observed attractiveness of the same species in controlled field trials from previously published studies. We used Google Image searches to determine the correlation of pollinator visitation captured by photographs on the Internet relative to the attractiveness of the same species in common-garden field trials for 43 plant species. From the first 30 photographs, which successfully identified the plant, we recorded the number of Apis (managed honeybees), non-Apis (exclusively wild bees) and the number of bee-mimicking syrphid flies. We used these observations from search hits as well as bloom period (BP) as predictor variables in Generalized Linear Models (GLMs) for field-observed abundances of each of these groups. We found that non-Apis bees observed in controlled field trials were positively associated with observations of these taxa in Google Image searches (pseudo-R (2) of 0.668). Syrphid fly observations in the field were also associated with the frequency they were observed in images, but this relationship was weak. Apis bee observations were not associated with Internet images, but were slightly associated with BP. Our results suggest that passively crowdsourced image data can potentially be a useful screening tool to identify candidate plants for pollinator habitat restoration efforts directed at wild bee conservation. Increasing our understanding of the attractiveness of a greater diversity of plants increases the potential for more rapid and efficient research in creating pollinator-supportive landscapes.