Claudio Gratton

A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems

Bees provide essential pollination services that are potentially affected both by local farm management and the surrounding landscape. To better understand these different factors, we modelled the relative effects of landscape composition (nesting and floral resources within foraging distances), landscape configuration (patch shape, interpatch connectivity and habitat aggregation) and farm management (organic vs. conventional and local-scale field diversity), and their interactions, on wild bee abundance and richness for 39 crop systems globally. Bee abundance and richness were higher in diversified and organic fields and in landscapes comprising more high-quality habitats; bee richness on conventional fields with low diversity benefited most from high-quality surrounding land cover. Landscape configuration effects were weak. Bee responses varied slightly by biome. Our synthesis reveals that pollinator persistence will depend on both the maintenance of high-quality habitats around farms and on local management practices that may offset impacts of intensive monoculture agriculture.

Landscape diversity enhances biological control of an introduced crop pest in the north-central USA

Arthropod predators and parasitoids provide valuable ecosystem services in agricultural crops by suppressing populations of insect herbivores. Many natural enemies are influenced by non-crop habitat surrounding agricultural fields, and understanding if, and at what scales, land use patterns influence natural enemies is essential to predicting how landscape alters biological control services. Here we focus on biological control of soybean aphid, Aphis glycines Matumura, a specialist crop pest recently introduced to the north-central United States. We measured the amount of biological control service supplied to soybean in 26 replicate fields across Michigan, Wisconsin, Iowa, and Minnesota across two years (2005-2006). We measured the impact of natural enemies by experimentally excluding or allowing access to soybean aphid infested plants and comparing aphid population growth over 14 days. We also monitored aphid and natural enemy populations at large in each field. Predators, principally coccinellid beetles, dominated the natural enemy community of soybean in both years. In the absence of aphid predators, A. glycines increased significantly, with 5.3-fold higher aphid populations on plants in exclusion cages vs. the open field after 14 days. We calculated a biological control services index (BSI) based on relative suppression of aphid populations and related it to landscape diversity and composition at multiple spatial scales surrounding each site. We found that BSI values increased with landscape diversity, measured as Simpsons D. Landscapes dominated by corn and soybean fields provided less biocontrol service to soybean compared with landscapes with an abundance of crop and non-crop habitats. The abundance of Coccinellidae was related to landscape composition, with beetles being more abundant in landscapes with an abundance of forest and grassland compared with landscapes dominated by agricultural crops. Landscape diversity and composition at a scale of 1.5 km surrounding the focal field explained the greatest proportion of the variation in BSI and Coccinellidae abundance. This study indicates that natural enemies provide a regionally important ecosystem service by suppressing a key soybean pest, reducing the need for insecticide applications. Furthermore, it suggests that management to maintain or enhance landscape diversity has the potential to stabilize or increase biocontrol services.

BOTTOM-UP FORCES MEDIATE NATURAL-ENEMY IMPACT IN A PHYTOPHAGOUS INSECT COMMUNITY

We employed a combination of factorial experiments in the field and labo- ratory to investigate the relative magnitude and degree of interaction of bottom-up factors (two levels each of host-plant nutrition and vegetation complexity) and top-down forces (two levels of wolf-spider predation) on the population growth of Prokelisia planthoppers (P. dolus and P. marginata), the dominant insect herbivores on Spartina cordgrass through- out the intertidal marshes of North America. Treatments were designed to mimic combi- nations of plant characteristics and predator densities that occur naturally across habitats in the field. There were complex interactive effects between plant resources and spider predation on the population growth of planthoppers. The degree that spiders suppressed planthoppers depended on both plant nutrition and vegetation complexity, an interaction that was dem- onstrated both in the field and laboratory. Laboratory results showed that spiders checked planthopper populations most effectively on poor-quality Spartina with an associated matrix of thatch, all characteristics of high-marsh meadow habitats. It was also this combination of plant resources in concert with spiders that promoted the smallest populations of planthop- pers in our field experiment. Planthopper populations were most likely to escape the sup- pressing effects of predation on nutritious plants without thatch, a combination of factors associated with observed planthopper outbreaks in low-marsh habitats in the field. Thus, there is important spatial variation in the relative strength of forces with bottom-up factors dominating under low-marsh conditions and top-down forces increasing in strength at higher elevations on the marsh. Enhancing host-plant biomass and nutrition did not strengthen top-down effects on planthoppers, even though nitrogen-rich plants supported higher densities of wolf spiders and other invertebrate predators in the field. Rather, planthopper populations, particularly those of Prokelisia marginata, escaped predator restraint on high-quality plants, a result we attribute to its mobile life history, enhanced colonizing ability, and rapid growth rate. Thus, our results for Prokelisia planthoppers suggest that the life history strategy of a species is an important mediator of top-down and bottom-up impacts. In laboratory mesocosms, enhancing plant biomass and nutrition resulted in increased spider reproduction, a cascading effect associated with planthopper increases on high- quality plants. Although the adverse effects of spider predation on planthoppers cascaded down and fostered increased plant biomass in laboratory mesocosms, this result did not occur in the field where top-down effects attenuated. We attributed this outcome in part to the intraguild predation of other planthopper predators by wolf spiders. Overall, the general paradigm in this system is for bottom-up forces to dominate, and when predators do exert a significant suppressing effect on planthoppers, their impact is generally legislated by vegetation characteristics.

Perennial grasslands enhance biodiversity and multiple ecosystem services in bioenergy landscapes

Significance Science-based polices are needed to inform sustainable bioenergy landscape design. Our key finding is 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. The implication is that careful design of bioenergy landscapes has the potential to enhance multiple services in food and energy crops, leading to important synergies that have not yet informed the ongoing bioenergy debate. This study is especially timely as high commodity prices are driving conversion of marginal lands to annual crop production, reducing future flexibility. 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.

Feeding-induced changes in plant quality mediate interspecific competition between sap-feeding herbivores.

Feeding-induced plant resistance is a well-documented phenomenon for leaf- chewing insects. Furthermore, feeding-induced resistance provides the mechanistic basis for many cases of delayed interspecific competition, whereby previous feeding by one species diminishes the performance of other herbivores which attack the same plant later in the season. This phenomenon, however, has been very poorly investigated for sap-feeding insects. The results we present here for salt marsh-inhabiting planthoppers ( Prokelisia dolus and P. marginata) provide one of the few known examples of delayed, plant-mediated interspecific competition between two sap-feeding insects. Three lines of experimental evidence from the laboratory, field cages, and open field plots provide support for the detrimental effects of previous feeding by one planthopper species on the subsequent survival and performance of the other. Laboratory experiments showed that prior feeding on cordgrass by one congener resulted in reduced performance of the other in the following generation. However, the effect was asymmetric. Prior feeding by P. dolus resulted in prolonged development and reduced body size (a correlate of fecundity) in P. marginata, whereas only development was protracted in P. dolus when plants were previously exposed to P. marginata. Consequently, P. dolus appears to be the superior competitor in the context of delayed, plant-mediated interactions. The negative effects of previous feeding by P. dolus on the development time, body size, and survival of P. marginata obtained in the laboratory were confirmed both in cages and on cage-free islets of cordgrass in the field. Feeding-induced reductions in host-plant quality by P. dolus may provide additional impetus for P. marginata to migrate from shared habitats on the high marsh to nutritionally superior plants in the low marsh rarely occupied by P. dolus. The mechanism underlying the delayed competitive effects between Prokelisia plan- thoppers is most likely diminished plant nutrition, because feeding by P. dolus significantly reduces the concentration of essential amino acids in cordgrass. The asymmetry of plant- mediated competition between the Prokelisia species may be due to the ability of P. dolus to better tolerate feeding-depleted levels of plant nitrogen via compensatory feeding. Even though these two planthoppers do not suffer significant fitness reductions during contemporaneous interactions, they compete severely in the context of feeding-induced plant resistance which is expressed later in the season. This result, coupled with the fact that most studies of interspecific interaction between herbivorous insects are contempo- raneous, indicates that interspecific competition may be profoundly underestimated as a structuring force in phytophagous insect communities.

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

Seasonal shift from bottom-up to top-down impact in phytophagous insect populations

34 and

Flux of aquatic insect productivity to land: comparison of lentic and lotic ecosystems

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.

Bird communities in future bioenergy landscapes of the Upper Midwest.

Although many studies now examine how multiple factors influence the dynamics of herbivore populations, few studies explicitly attempt to document where and when each is important and how they vary and interact. In fact, how temporal variation in top-down (natural enemies) and bottom-up (host plant resources) factors affect herbivore dynamics has been suggested as a particularly important yet poorly understood feature of terrestrial food webs. In this study we examined how temporal changes in predator density (wolf spiders, sheet-web builders, and mirid egg predators) and host-plant resources (plant quality and structural complexity) influence the population dynamics of the dominant phytophagous insects on Atlantic-coast salt marshes, namely Prokelisia planthoppers (Homoptera: Delphacidae). We designed a factorial experiment in meadows of Spartina alterniflora to mimic natural variation in vegetation quality and structure by establishing two levels of plant nutrition (leaf nitrogen content) by fertilization, and two levels of habitat complexity by adding leaf litter (thatch). We then assessed seasonal changes in the strength of bottom-up (plant quality) and top-down (predator) impacts on planthopper populations. Planthopper populations responded positively to increased plant quality treatments in late summer. Despite the greater number of planthopper adults colonizing fertilized Spartina plots compared to unfertilized controls, the offspring of these colonists were much less abundant at the end of the season in fertilized plots, particularly those with thatch. The initial colonization effect was later erased because arthropod predators selectively accumulated in fertilized plots where they inflicted significant mortality on all stages of planthoppers. Predators rapidly colonized fertilized plots and reached high densities well in advance of planthopper colonization, a response we attribute to their rapid aggregation in complex-structured habitats with readily available alternative prey. Our results suggest that plant resources not only mediate the strength of predator impacts on herbivore populations, but they also promote the coupling of predator and prey populations and thus influence when enemy impacts are realized.

DOES "ENEMY-FREE SPACE" EXIST? EXPERIMENTAL HOST SHIFTS OF AN HERBIVOROUS FLY

Recently, food web studies have started exploring how resources from one habitat or ecosystem influence trophic interactions in a recipient ecosystem. Benthic production in lakes and streams can be exported to terrestrial habitats via emerging aquatic insects and can therefore link aquatic and terrestrial ecosystems. In this study, we develop a general conceptual model that highlights zoobenthic production, insect emergence, and ecosystem geometry (driven principally by area-to-edge ratio) as important factors modulating the flux of aquatic production across the ecosystem boundary. Emerging insect flux, defined as total insect production emerging per meter of shoreline (g C x m(-1) x yr(-1)) is then distributed inland using decay functions and is used to estimate insect deposition rate to terrestrial habitats (g C x m(-2) x yr(-1)). Using empirical data from the literature, we simulate insect fluxes across the water-land ecosystem boundary to estimate the distribution of fluxes and insect deposition inland for lakes and streams. In general, zoobenthos in streams are more productive than in lakes (6.67 vs. 1.46 g C x m(-2) x yr(-1)) but have lower insect emergence to aquatic production ratios (0.19 vs. 0.30). However, as stream width is on average smaller than lake radius, this results in flux (F) estimates 2 1/2 times greater for lakes than for streams. Ultimately, insect deposition onto land (within 100 m of shore) adjacent to average-sized lakes (10-ha lakes, 0.021 g C x m(-2) x yr(-1)) is greater than for average-sized streams (4 m width, 0.002 g C x m(-2) x yr(-1)) used in our comparisons. For the average lake (both in size and productivity), insect deposition rate approaches estimates of terrestrial secondary production in low-productivity ecosystems (e.g., deserts and tundra, approximately 0.07 g C x m(-2) x yr(-1)). However, larger lakes (1300 ha) and streams (16 m) can have average insect deposition rates (approximately 0.01-2.4 g C x m(-2) x yr(-1)) comparable to estimates of secondary production of more productive ecosystems such as grasslands. Because of the potentially large inputs of emerging aquatic insects into terrestrial habitats, ecosystem processes and terrestrial consumers can be influenced by insect inputs. The relative contribution of lakes and streams to this flux will vary among landscapes depending on the number and size of these ecosystems types on the landscape.