Alison G. Power

Ecosystem services and agriculture: tradeoffs and synergies

Agricultural ecosystems provide humans with food, forage, bioenergy and pharmaceuticals and are essential to human wellbeing. These systems rely on ecosystem services provided by natural ecosystems, including pollination, biological pest control, maintenance of soil structure and fertility, nutrient cycling and hydrological services. Preliminary assessments indicate that the value of these ecosystem services to agriculture is enormous and often underappreciated. Agroecosystems also produce a variety of ecosystem services, such as regulation of soil and water quality, carbon sequestration, support for biodiversity and cultural services. Depending on management practices, agriculture can also be the source of numerous disservices, including loss of wildlife habitat, nutrient runoff, sedimentation of waterways, greenhouse gas emissions, and pesticide poisoning of humans and non-target species. The tradeoffs that may occur between provisioning services and other ecosystem services and disservices should be evaluated in terms of spatial scale, temporal scale and reversibility. As more effective methods for valuing ecosystem services become available, the potential for ‘win–win’ scenarios increases. Under all scenarios, appropriate agricultural management practices are critical to realizing the benefits of ecosystem services and reducing disservices from agricultural activities.

GENETICALLY ENGINEERED ORGANISMS AND THE ENVIRONMENT: CURRENT STATUS AND RECOMMENDATIONS1

The Ecological Society of America has evaluated the ecological effects of current and potential uses of field-released genetically engineered organisms (GEOs), as described in this Position Paper. Some GEOs could play a positive role in sustainable agriculture, forestry, aquaculture, bioremediation, and environmental management, both in developed and developing countries. However, deliberate or inadvertent releases of GEOs into the environment could have negative ecological effects under certain circumstances. Possible risks of GEOs could include: (1) creating new or more vigorous pests and pathogens; (2) exacerbating the effects of existing pests through hybridization with related transgenic organisms; (3) harm to nontarget species, such as soil organisms, non-pest insects, birds, and other animals; (4) disruption of biotic communities, including agroecosystems; and (5) irreparable loss or changes in species diversity or genetic diversity within species. Many potential applications of genetic engineering extend beyond traditional breeding, encompassing viruses, bacteria, algae, fungi, grasses, trees, insects, fish, and shellfish. GEOs that present novel traits will need special scrutiny with regard to their environmental effects. The Ecological Society of America supports the following recommendations. (1) GEOs should be designed to reduce environmental risks. (2) More extensive studies of the environmental benefits and risks associated with GEOs are needed. (3) These effects should be evaluated relative to appropriate baseline scenarios. (4) Environmental release of GEOs should be prevented if scientific knowledge about possible risks is clearly inadequate. (5) In some cases, post-release monitoring will be needed to identify, manage, and mitigate environmental risks. (6) Science-based regulation should subject all transgenic organisms to a similar risk assessment framework and should incorporate a cautious approach, recognizing that many environmental effects are GEO- and site-specific. (7) Ecologists, agricultural scientists, molecular biologists, and others need broader training and wider collaboration to address these recommendations. In summary, GEOs should be evaluated and used within the context of a scientifically based regulatory policy that encourages innovation without compromising sound environmental management. The Ecological Society of America is committed to providing scientific expertise for evaluating and predicting the ecological effects of field-released transgenic organisms.

Pathogen Spillover in Disease Epidemics

In field experiments manipulating generalist pathogens and host community composition, the presence of a highly susceptible reservoir species drove disease dynamics in multiple nonreservoir species, sometimes decreasing their abundance through apparent competition. The dynamics of generalist pathogens in multispecies host communities remain a major frontier for disease ecology. Of particular interest are how host community structure controls pathogen transmission and how disease spread feeds back to influence the host community. Pathogen spillover occurs when epidemics in a host population are driven not by transmission within that population but by transmission from a reservoir population. Here we review examples of spillover in pathogens infecting humans, domesticated animals, and crops, noting that most empirical evidence for spillover results from nonmanipulative, observational studies. We then present results from two field experiments utilizing an experimentally tractable model system of annual wild grasses and a generalist virus, the barley yellow dwarf virus. In these experiments, the presence of a highly susceptible reservoir species, Avena fatua (wild oats), greatly increased pathogen prevalence in several other species. This result demonstrates pathogen spillover and illustrates the crucial role of host community structure in controlling the dynamics of generalist pathogens. Further, pathogen spillover from A. fatua decreased the abundance of two other host species through pathogen‐mediated apparent competition. Thus, our results provide experimental support for theoretical predictions of strong feedbacks between host community structure and generalist disease dynamics.

Direct and Interactive Effects of Enemies and Mutualists on Plant Performance: a Meta-Analysis

Plants engage in multiple, simultaneous interactions with other species; some (enemies) reduce and others (mutualists) enhance plant performance. Moreover, effects of different species may not be independent of one another; for example, enemies may compete, reducing their negative impact on a plant. The magnitudes of positive and negative effects, as well as the frequency of interactive effects and whether they tend to enhance or depress plant performance, have never been comprehensively assessed across the many published studies on plant-enemy and plant-mutualist interactions. We performed a meta-analysis of experiments in which two enemies, two mutualists, or an enemy and a mutualist were manipulated factorially. Specifically, we performed a factorial meta-analysis using the log response ratio. We found that the magnitude of (negative) enemy effects was greater than that of (positive) mutualist effects in isolation, but in the presence of other species, the two effects were of comparable magnitude. Hence studies evaluating single-species effects of mutualists may underestimate the true effects found in natural settings, where multiple interactions are the norm and indirect effects are possible. Enemies did not on average influence the effects on plant performance of other enemies, nor did mutualists influence the effects of mutualists. However, these averages mask significant and large, but positive or negative, interactions in individual studies. In contrast, mutualists ameliorated the negative effects of enemies in a manner that benefited plants; this overall effect was driven by interactions between pathogens and belowground mutualists (bacteria and mycorrhizal fungi). The high frequency of significant interactive effects suggests a widespread potential for diffuse rather than pairwise coevolutionary interactions between plants and their enemies and mutualists. Pollinators and mycorrhizal fungi enhanced plant performance more than did bacterial mutualists. In the greenhouse (but not the field), pathogens reduced plant performance more than did herbivores, pathogens were more damaging to herbaceous than to woody plants, and herbivores were more damaging to crop than to non-crop plants (suggesting evolutionary change in plants or herbivores following crop domestication). We discuss how observed differences in effect size might be confounded with methodological differences among studies.

Vector preference and disease dynamics: a study of barley yellow dwarf virus

Using simple analytical models of the probability of disease transmission and a spatially explicit computer simulation of the spread of the aphid-transmitted barley yellow dwarf virus, we examined the effect of vector preference for diseased or healthy hosts on the spread of an economically important plant pathogen. Our analytical models indicate that the effect of vector preference for diseased plants on the probability of disease spread depends on the frequency of diseased plants in the population. In a non-spatial environment with a high frequency of diseased plants, disease spread is favored by vectors preferring healthy plants. With a low frequency of diseased plants, disease spread is favored by vectors preferring diseased plants. The effect of vector preference depends on the amount of persistence exhibited by the disease. For persistently transmitted diseases, the vector remains infective for a long period after visiting a diseased host. Persistence increases the rate of spread for a vector preferring healthy hosts more than it increases the rate of spread for a vector preferring diseased hosts. Using a Markov chain model of disease transmission, we have shown that an increase in the spatial patchiness of the disease can lead to a decrease in the rate of disease spread by a vector capable of moving only limited distances. The effect of spatial disease structure depends on the preference behavior exhibited by the vector. Our spatially explicit computer simulation explored the effect of frequency, persistence, and spatial structure in a dynamic model. All of these factors were shown to be important in describing the impact of vector disease preference on epidemiology. Many of our results contrast with the assumption found in the agricultural literature that a preference for diseased plants leads to an increase in disease spread. These results may have implications for the evolution of pathogen-modified vector behavior and/or host attractiveness. Explicit knowledge of the interaction between spatial dynamics and vector preference will improve our ability to model epidemics and predict the spread of infectious diseases.

Insect transmission of plant viruses: a constraint on virus variability.

Genetic diversity in viruses is shaped by high rates of recombination and is constrained by host defenses and the requirements of transmission. Recent studies of insect-transmitted plant viruses demonstrate highly conserved molecular motifs in viral genomes that regulate the specificity of insect transmission. In contrast, advances in our understanding of host plant response to virus infection reveal some generalized patterns of host defense to a diversity of viruses.

Plant Community Diversity, Herbivore Movement, and an Insect-Transmitted Disease of Maize

Field experiments were carried out in Nicaragua to examine the influence of plant community diversity, plant density, and host plant quality on the spread of an insect-transmitted plant pathogen. Population levels of the corn leafhopper Dalbulus maidis, which transmits the corn stunt spiroplasma to maize, were monitored in four experimental communities; low-density maize monoculture, high-density maize monoculture, two-species (maize/bean) polyculture, and multispecies (maize/weeds) polyculture. Leafhopper abundance per plant and the incidence of corn stunt were lower in high-density maize monocultures than in low-density monocultures. Increasing plant diversity by intercropping with nonhost species such as beans or weeds also led to lower leafhooper abundance and decreased disease incidence, but the effect was not enhanced as additional nonhost species were added to the community. Manipulating host plant quality by increasing nitrogen fertilization resulted in higher leafhopper densities at higher nitrogen levels. To explore the role of vector movement in disease spread, leafhopper movement rates and emigration were estimated by observing changes in the spatial gradients of leafhopper densities over time. This method of movement analysis requires neither marking the insects nor releasing them at a single point, and thus reduces the extreme disturbance caused by traditional mark-release techniques. The analysis indicated that leafhopper movement rates were lowest in the polycultures. In particular, across-row movement was strikingly inhibited in the bean polyculture. This polyculture also had the highest rates of emigration. These results indicate that plant quality, density, and diversity significantly affect the spread of corn stunt through their effects on the abundance and movement behavior of the corn leafhopper. These factors could be manipulated in a program of cultural control for corn stunt in maize fields in tropical America.

VIRUS SPREAD AND VECTOR DYNAMICS IN GENETICALLY DIVERSE PLANT POPULATIONS

Little is known about the influence of genetic diversity in plant populations on the dynamics of plant viruses, particularly those transmitted by insects. For these viruses, plant genetic diversity may affect virus incidence through impacts on the population dy- namics of the vector insects or through impacts on vector feeding behavior, which deter- mines transmission of the virus. This study was designed to explore the influence of plant genetic diversity on virus dispersal by aphid vectors and to examine the biological mech- anisms responsible for that influence. In a set of field experiments using the aphid-transmitted barley yellow dwarf virus, I examined the influence of genetic diversity in oat (Avena sativa L.) populations on the spread of the virus and on the population dynamics and movement behavior of aphid vectors of the virus. Only at relatively high aphid abundance were the densities of aphid vectors influenced by plant genetic diversity. In one year out of three, densities of the oat- bird cherry aphid, Rhopalosiphum padi (L.), were significantly lower in the genetically diverse stand than in the genetically homogeneous stands. In no year were densities of the English grain aphid, Sitobion avenae (F.), influenced by the host-plant population. Despite these weak or absent effects on vector abundance, the incidence of the virus was consistently lower in the genetically diverse oat populations. Disease reduction in the diverse populations appears to depend upon changes in aphid movement behavior that affect the efficiency of virus transmission. Mark-release experi- ments with S. avenae demonstrated that movement rates were significantly higher and plant tenure times were significantly lower in the genetically diverse oat populations. Be- cause the barley yellow dwarf virus requires several hours of aphid feeding for effective transmission, these reduced tenure times and increased travel time among plants led to a reduction of virus transmission. While plant genotype can clearly influence herbivorous insects dramatically, this study suggests that the effects on insects of genetic diversity per se in the host-plant population are likely to be subtle and not easily detected using standard field sampling techniques, except at high insect densities. Yet even at low vector densities, behavioral responses to plant genetic diversity can lead to significant effects on the spread of pathogens.

From limits to growth to global change. Constraints and contradictions in the evolution of environmental science and ideology.

Abstract The notions of ‘limits to growth’ and ‘global change’ have a number of similarities. Both are neo-Malthusian, are based on quantitative scientific research, and have gained prominence as global rationales for wide-ranging environmentalist agendas. Most importantly, both notions have served simultaneously as scientific concepts and as environmental movement ideologies. However, the favourable political reception accorded ‘global change’ is markedly different from the hostile reception of the ‘limits to growth’ Weltanschauung of the early 1970s. The two formulations are compared and contrasted, and possible explanations and implications are discussed. The relatively high degree of consensus on global change that currently prevails may mask contradictions that will lead to major conflicts over environmental policy.

Competition between Viruses in a Complex Plant‐‐Pathogen System

Interactions among viruses, vectors, and host plants may influence the spread and success of plant viruses. Major factors include direct competition within host plants, direct competition within vectors, differences in transmission rates, and virus influences on vector behavior and population dynamics. The aphid-transmitted barley yellow dwarf viruses (BYDVs), which infect a broad range of grasses worldwide, represent a model system for addressing questions about the outcome of direct and indirect competition be- tween viruses. Historical shifts in the relative prevalence of BYDV strains document the apparent displacement of one virus strain (PAV) by another (MAV) over 20 yr. In the barley yellow dwarf system, transmission rate appears to play an important role in determining the outcome of competition between viruses. Moreover, the interaction between transmission rate and vector behavior may be particularly important. PAV is the stronger competitor within hosts, where double infections occur more often than in insect vectors. PAV also has significant advantages due to higher overall transmission rates than MAV. In addition, vector aphids show a strong nonpreference for PAV that may lead to greater rates of virus spread.