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.

Assessing Anaerobic Soil Disinfestation as a Control Tactic for Delia radicum (Diptera: Anthomyiidae) in California Brussels Sprouts.

Fumigants are often the primary material used to manage plant disease agents, soil-borne arthropods, and weeds in California agriculture, particularly in the absence of crop rotation. However, some fumigants have come under increased regulatory scrutiny and are therefore no longer available for use. We tested two biologically based preplant crop-protection fumigant alternatives for their effectiveness in reducing populations of Delia radicum (L.), a soil-borne insect pest of cole crops. Laboratory and field tests compared pest survival in untreated control soil with survival under anaerobic soil disinfestation (ASD), which is induced by incorporating a carbon source (rice bran or grape pomace) and subsequently saturating the soil with water. We also measured and compared the effects of standard grower practices (fumigation), ASD and biofumigation (mustard seed meal incorporated before planting), and untreated control soils on fly abundance, pupal survival, and root damage in Brussels sprout fields. In both laboratory and field studies, D. radicum pupal survivorship was reduced in ASD-treated soils relative to control soils. Pupal survivorship of Musca domestica (L.) (Diptera: Muscidae), which was used as a proxy for D. radicum in some field experiments, was also reduced in ASD- and biofumigation-treated soils, when compared with untreated control soils. These results indicate that fumigant alternatives may provide useful insect pest management opportunities for compatible cropping systems.

A global synthesis of the effects of diversified farming systems on arthropod diversity within fields and across agricultural landscapes.

Agricultural intensification is a leading cause of global biodiversity loss, which can reduce the provisioning of ecosystem services in managed ecosystems. Organic farming and plant diversification are farm management schemes that may mitigate potential ecological harm by increasing species richness and boosting related ecosystem services to agroecosystems. What remains unclear is the extent to which farm management schemes affect biodiversity components other than species richness, and whether impacts differ across spatial scales and landscape contexts. Using a global metadataset, we quantified the effects of organic farming and plant diversification on abundance, local diversity (communities within fields), and regional diversity (communities across fields) of arthropod pollinators, predators, herbivores, and detritivores. Both organic farming and higher in-field plant diversity enhanced arthropod abundance, particularly for rare taxa. This resulted in increased richness but decreased evenness. While these responses were stronger at local relative to regional scales, richness and abundance increased at both scales, and richness on farms embedded in complex relative to simple landscapes. Overall, both organic farming and in-field plant diversification exerted the strongest effects on pollinators and predators, suggesting these management schemes can facilitate ecosystem service providers without augmenting herbivore (pest) populations. Our results suggest that organic farming and plant diversification promote diverse arthropod metacommunities that may provide temporal and spatial stability of ecosystem service provisioning. Conserving diverse plant and arthropod communities in farming systems therefore requires sustainable practices that operate both within fields and across landscapes.

Relative densities of natural enemy and pest insects within California hedgerows.

Research on hedgerow design for supporting communities of natural enemies for biological control lags behind farmer innovation in California, where assemblages of perennial plant species have been used on crop field margins in the last decade. We compared natural enemy to pest ratios between fields with hedgerows and fields with weedy margins by sampling beneficial insects and key pests of vegetables on sticky cards. We used biweekly vacuum samples to measure the distribution of key insect taxa among native perennial plant species with respect to the timing and intensity of bloom. Sticky cards indicated a trend that field margins with hedgerows support a higher ratio of natural enemies to pests compared with weedy borders. Hedgerow plant species hosted different relative densities of a generally overlapping insect community, and the timing and intensity of bloom only explained a small proportion of the variation in insect abundance at plant species and among hedgerows, with the exception of Orius spp. on Achillea millefolium L. and Baccharis pilularis De Candolle. Indicator Species Analysis showed an affinity of parasitic wasps, especially in the super-family Chalcidoidea, for B. pilularis whether or not it was in flower. A. millefolium was attractive to predatory and herbivorous homopterans; Heteromeles arbutifolia (Lindley) Roemer and B. pilularis to Diabrotica undecimpunctata undecimpunctata Mannerheim; and Rhamnus californica Eschsch to Hemerobiidae. Perennial hedgerows can be designed through species selection to support particular beneficial insect taxa, but plant resources beyond floral availability may be critical in providing structural refuges, alternative prey, and other attractive qualities that are often overlooked.

The implications of habitat management on the population viability of the endangered Ohlone tiger beetle (Cicindela ohlone) metapopulation.

Despite their role in providing ecosystem services, insects remain overlooked in conservation planning, and insect management approaches often lack a rigorous scientific basis. The endangered Ohlone tiger beetle (Cicindela ohlone) occurs in a 24-km(2) area in Santa Cruz County, California. The once larger metapopulation now consists of subpopulations inhabiting five patches of coastal prairie where it depends on bare ground for mating, foraging, and oviposition. Human activities have eliminated natural disturbances and spread invasive grasses, reducing C. ohlone's bare-ground habitat. Management actions to restore critical beetle habitat consist of cattle and horse grazing, maintaining slow bicycle speeds on occupied public trails, and artificial creation of bare-ground plots. Recreational biking trails help maintain bare ground, but can cause beetle mortality if left unregulated. We tracked C. ohlone survivorship and estimated fecundity for three years. We then constructed a stage-structured population projection matrix model to estimate population viability among the five patches, and to evaluate the success of management interventions. We demonstrate that habitat creation, regulation of bicycle speed, and migration between patches increase C. ohlone survival and population viability. Our results can be directly applied to management actions for conservation outcomes that will reduce species extinction risk and promote recolonization of extirpated patches.

What risk assessments of genetically modified organisms can learn from institutional analyses of public health risks.

The risks of genetically modified organisms (GMOs) are evaluated traditionally by combining hazard identification and exposure estimates to provide decision support for regulatory agencies. We question the utility of the classical risk paradigm and discuss its evolution in GMO risk assessment. First, we consider the problem of uncertainty, by comparing risk assessment for environmental toxins in the public health domain with genetically modified organisms in the environment; we use the specific comparison of an insecticide to a transgenic, insecticidal food crop. Next, we examine normal accident theory (NAT) as a heuristic to consider runaway effects of GMOs, such as negative community level consequences of gene flow from transgenic, insecticidal crops. These examples illustrate how risk assessments are made more complex and contentious by both their inherent uncertainty and the inevitability of failure beyond expectation in complex systems. We emphasize the value of conducting decision-support research, embracing uncertainty, increasing transparency, and building interdisciplinary institutions that can address the complex interactions between ecosystems and society. In particular, we argue against black boxing risk analysis, and for a program to educate policy makers about uncertainty and complexity, so that eventually, decision making is not the burden that falls upon scientists but is assumed by the public at large.

Avian conservation practices strengthen ecosystem services in California vineyards.

Insectivorous Western Bluebirds (Sialia mexicana) occupy vineyard nest boxes established by California winegrape growers who want to encourage avian conservation. Experimentally, the provision of available nest sites serves as an alternative to exclosure methods for isolating the potential ecosystem services provided by foraging birds. We compared the abundance and species richness of avian foragers and removal rates of sentinel prey in treatments with songbird nest boxes and controls without nest boxes. The average species richness of avian insectivores increased by over 50 percent compared to controls. Insectivorous bird density nearly quadrupled, primarily due to a tenfold increase in Western Bluebird abundance. In contrast, there was no significant difference in the abundance of omnivorous or granivorous bird species some of which opportunistically forage on grapes. In a sentinel prey experiment, 2.4 times more live beet armyworms (Spodoptera exigua) were removed in the nest box treatment than in the control. As an estimate of the maximum foraging services provided by insectivorous birds, we found that larval removal rates measured immediately below occupied boxes averaged 3.5 times greater than in the control. Consequently the presence of Western Bluebirds in vineyard nest boxes strengthened ecosystem services to winegrape growers, illustrating a benefit of agroecological conservation practices. Predator addition and sentinel prey experiments lack some disadvantages of predator exclusion experiments and were robust methodologies for detecting ecosystem services.

Does plant diversity benefit agroecosystems? A synthetic review.

Predictive theory on how plant diversity promotes herbivore suppression through movement patterns, host associations, and predation promises a potential alternative to pesticide-intensive monoculture crop production. We used meta-analysis on 552 experiments in 45 articles published over the last 10 years to test if plant diversification schemes reduce herbivores and/or increase the natural enemies of herbivores as predicted by associational resistance hypotheses, the enemies hypothesis, and attraction and repellency model applications in agriculture. We found extensive support for these models with intercropping schemes, inclusion of flowering plants, and use of plants that repel herbivores or attract them away from the crop. Overall, herbivore suppression, enemy enhancement, and crop damage suppression effects were significantly stronger on diversified crops than on crops with none or fewer associated plant species. However, a relatively small, but significantly negative, mean effect size for crop yield indicated that pest-suppressive diversification schemes interfered with production, in part because of reducing densities of the main crop by replacing it with intercrops or non-crop plants. This first use of meta-analysis to evaluate the effects of diversification schemes, a potentially more powerful tool than tallies of significant positive and negative outcomes (vote-counting), revealed stronger overall effects on all parameters measured compared to previous reviews. Our analysis of the same articles used in a recent review facilitates comparisons of vote-counting and meta-analysis, and shows that pronounced results of the meta-analysis are not well explained by a reduction in articles that met its stricter criteria. Rather, compared to outcome counts, effect sizes were rarely neutral (equal to zero), and a mean effect size value for mixed outcomes could be calculated. Problematic statistical properties of vote-counting were avoided with meta-analysis, thus providing a more precise test of the hypotheses. The unambiguous and encouraging results from this meta-analysis of previous research should motivate ecologists to conduct more mechanistic experiments to improve the odds of designing effective crop diversification schemes for improved pest regulation and enhanced crop yield.

Herbivores on a dominant understory shrub increase local plant diversity in rain forest communities.

Indirect effects of trophic interactions on biodiversity can be large and common, even in complex communities. Previous experiments with dominant understory Piper shrubs in a Costa Rican rain forest revealed that increases in herbivore densities on these shrubs caused widespread seedling mortality as a result of herbivores moving from Piper to seedlings of many different plant genera. We tested components of the Janzen-Connell hypothesis by conducting focused studies on the effects of specialist and generalist Piper herbivores on local seedling diversity. Whereas specialist herbivores are predicted to increase mortality to neighboring seedlings that are closely related to the source plant, true generalists moving from source plants may cause density-dependent mortality of many species, and possibly increase richness if new species replace abundant species that have been thinned by herbivores. Therefore, we hypothesized that seedling richness would be greater in understory control plots created in patches of Piper that had normal densities of generalist herbivores compared to plots from which we removed generalist herbivores manually from all Piper shrubs. After 15 months, generalist-herbivore-removal plots had > 40% fewer seedlings, > 40% fewer species, and 40% greater seedling evenness, on average, than control plots with generalist herbivores intact. Using a complementary approach in unmanipulated plots in four forests, we used path analysis to test for a positive association between seedling diversity and herbivore damage on Piper species. In unmanipulated plots, for both generalist and specialist herbivores, our data were significant fits to the causal model that Piper herbivores decrease evenness and increase plant species richness, corroborating the experimental results. Because herbivores changed how individuals were apportioned among the species and families present (lower evenness), one interpretation of these associations between herbivores on Piper shrubs and local seedling richness is that high seedling mortality in dominant families allowed the colonization or survival of less common species. If interspecific or apparent competition allowed for a relative increase in species richness, then the Janzen-Connell hypothesis may extend its predictions to generalist seedling predators. We speculate that apparent competition may explain some of the deviations from neutral model predictions, especially at small scales.

Plant fitness assessment for wild relatives of insect resistant crops.

Risk assessments of new insect-resistant crops will need to estimate the potential for increased weediness of wild crop relatives as a consequence of gene flow. When field experiments are precluded by containment concerns, simulation experiments can identify hazards or measure expected differences between GMOs and parental plants. To measure plant fitness consequences of wild plant protection from Bt-susceptible herbivores, we used topical sprays of bacterial Bacillus thuringiensis larvacide (Bt) on Brassica rapa. Spontaneous crosses between B. rapa and Bt cole crops cannot be precluded, especially if adoption of Bt varieties leads to high exposure. We compared survivorship and seed output of B. rapa that were either protected from or exposed to Bt-susceptible Lepidoptera in the various conditions where hybrids are likely to occur: cultivated (disked) soil, uncultivated agricultural field margins, and nearby non-crop habitats (meadows and ruderal areas). The relative effect of herbivore protection varied among years, habitats, and populations of seedlings. In 2003-2004, Bt sprays did not result in lower herbivory on B. rapa, and plant fitness was not increased. However, in 2004-2006 B. rapa seedlings protected from Bt-susceptible herbivores lived 25% longer, on average, than those that were exposed to these herbivores. In addition, an average B. rapa seedling sprayed with Bt throughout its lifetime was twice as likely to produce siliques and had 251% of the seed output of a seedling exposed to herbivores. The fitness advantage of Bt-based plant protection was apparent in 2004-2005 in half the plants that experienced higher herbivory, and for 2005-2006, was more pronounced in agricultural habitats than in meadows with established, perennial vegetation and less disturbance. Positive effects of Bt-based plant protection and greater fitness in disturbed habitats suggest that crop-wild gene flow may benefit weed populations, and that field tests with herbivore exclusion/addition experiments are feasible alternatives when molecular containment of transgenes restricts field experiments with insect resistant crop-wild hybrids.

Bt crops: predicting effects of escaped transgenes on the fitness of wild plants and their herbivores.

One prominent concern about genetically modified crops is the possibility of environmental impacts from the movement of fitness-enhancing traits to wild plant populations. Decisions to deregulate Bt crops in the USA have relied strongly on arguments that these crops will not interbreed with wild relatives in the permitted growing regions. Limited attention therefore has been directed to analyses of the consequences of gene flow. To provide a transparent evaluation process for risks associated with insecticidal transgene escape, we crafted a series of questions designed to guide this aspect of the risk assessment. We then explored the current knowledge base available for answering such risk-related questions for three Bt crops (cotton, rapeseed, and rice). First, we generated a list of wild relatives of these crops. A definitive list of potential transgene recipients is not yet possible for some crops. Sufficient data are not available for some crops to eliminate certain related plant species from consideration of fertile hybrid formation, thus making lists for these crops subject to speculation. Second, we queried the HOSTS database (UK) to obtain a worldwide listing of lepidopteran species that feed on these crops and their wild relatives, and to determine the host range of the larvae. To our knowledge, this list of 502 lepidopteran species is the first such list published for these crops and wild crop relatives. Third, we used a data set maintained by the Canadian Forest Service to assess Bt toxin susceptibility for these lepidopterans. Only 3% of those species have been tested for susceptibility; and the literature suggests that generalizations about susceptibility among taxa are difficult due to the variability within families. Fourth, we consulted the literature to interpret what is known about the ability of lepidopterans to regulate plant fitness or invasiveness. We could not eliminate the possibility of ecological release due to plant resistance against lepidopterans. In fact, there is strong experimental evidence that lepidopteran herbivores do limit the distribution and/or abundances of at least some wild plant species. Neither could we eliminate the possibility that non-target lepidopterans might have important functions in the ecosystem as pollinators or alternate hosts to natural enemies of pest species. This study suggests that crucial data are lacking for the development of a credible scientific basis to confirm or deny environmental risks associated with the escape of Bt transgene constructs to wild relatives. Given the absence of information on the identity, level of susceptibility, and ecological roles of lepidopterans exploiting specific wild relatives of Bt crops, we suggest that new efforts be directed to assessing possible consequences of lepidopteran mortality on resistant wild relatives.

Relative strengths of top-down and bottom-up forces in a tropical forest community.

We tested integrative bottom-up and top-down trophic cascade hypotheses with manipulative experiments in a tropical wet forest, using the ant-plant Piper cenocladum and its associated arthropod community. We examined enhanced nutrients and light along with predator and herbivore exclusions as sources of variation in the relative biomass of plants, their herbivores (via rates of herbivory), and resident predaceous ants. The combined manipulations of secondary consumers, primary consumers, and plant resources allowed us to examine some of the direct and indirect effects on each trophic level and to determine the relative contributions of bottom-up and top-down cascades to the structure of the community. We found that enhanced plant resources (nutrients and light) had direct positive effects on plant biomass. However, we found no evidence of indirect (cascading through the herbivores) effects of plant biomass on predators or top predators. In contrast, ants had indirect effects on plant biomass by decreasing herbivory on the plants. This top-down cascade occurred whether or not plant resources were enriched, conditions which are expected to modify top-down forces.

Parasitism rates and sex ratios of a parasitoid wasp: effects of herbivore and plant quality.

We studied interactions among collards, Brassica oleracea var. acephala, the diamondback moth (DBM), Plutella xylostella (Lepidoptera: Yponomeutidae) and its parasitoid Diadegma insulare (Hymenoptera: Ichneumonidae) by manipulating plant nitrogen (N) concentrations in field and laboratory experiments. Parasitoid abundance strongly reflected DBM abundance and was related to total leaf N. Parasitism rates were high (70.7%) and density-independent. Wasp sex ratios varied markedly (3-93% female) in response to the herbivores, the plants, or both. Higher proportions of female wasps emerged from DBM larvae on plants with high leaf N than on unfertilized plants. More female wasps also emerged from larvae parasitized as larger instars. We suggest that wasps have the potential to control DBM populations through long-term numerical responses mediated by variable sex ratios.

The Enemies Hypothesis: Tritrophic Interactions and Vegetational Diversity in Tropical Agroecosystems.

The effects of vegetational diversity on the abundance of natural enemies of herbivores were studied in a traditional agroecosystem in tropical Mexico. Visitation patterns of parasitic Hymenoptera and densities of predators were compared between monocultures of squash and maize and mixed assemblages of maize, cowpea, and squash. The impact of parasitoid visitation was assessed by monitoring the percent parasitism of a target herbivore in the system: Diaphania hyalinata (L.) (Lepidoptera: Pyralidae), a cucurbit specialist. The "Enemies" hypothesis predicts a positive correlation between plant species richness and natural enemy abundance, which results in the regulation of herbivores at lower levels in diverse vegetation than in pure stands. The specific questions addressed in this study were: (1) are the major groups of natural enemies more abundant in patches of diverse vegetation than in monocultures?; (2) if so, does an increase in either abundance or diversity of natural enemies cause a concomitant increase in herbivore regulation?; (3) are the effects of vegetational diversity uniform over major enemy groups? The activity of hymenopteran parasitoids was affected by cropping pattern. Malaise trap captures of parasitoids in general, and of those species that attack D. hyalinata on squash, were consistently greater in tricultures than in squash monocultures, but were also greater in maize monocultures. Parasitism rates of eggs and larvae were higher on squash interplanted with maize and cowpea. These data partially support the "Enemies" hypothesis in explaining lower herbivore levels in diverse vegetation. However, the effects of diversity, per se, do not seem to be as important as the presence of maize in the system. The responses of natural enemies to vegetational diversity were not uniform. Most predators were not significantly influenced by cropping patterns, and some were more abundant in squash monocultures. The results of this study are discussed in terms of possible routes by which members of the third trophic level are influenced by plants in association.