Genetically modified crops for the bioeconomy: meeting public and regulatory expectations

As the United States moves toward a plant-based bioeconomy, a large research and development effort is focused on creating new feedstocks to meet biomass demand for biofuels, bioenergy, and specialized bioproducts, such as industrial compounds and biomaterial precursors. Most bioeconomy projections assume the widespread deployment of novel feedstocks developed through the use of modern molecular breeding techniques, but rarely consider the challenges involved with the use of genetically modified crops, which can include hurdles due to regulatory approvals, market adoption, and public acceptance. In this paper we consider the implications of various transgenic crops and traits under development for the bioeconomy that highlight these challenges. We believe that an awareness of the issues in crop and trait selection will allow developers to design crops with maximum stakeholder appeal and with the greatest potential for widespread adoption, while avoiding applications unlikely to meet regulatory approval or gain market and public acceptance. The views presented here are those of the authors and do not necessarily represent the views of the US government.     

New hope for dedicated genetically engineered bioenergy feedstocks?

The unique regulatory requirements and costs of genetic engineering (GE) are likely to inhibit commercialization of dedicated bioenergy crops due to the relatively small current market. Two recent regulatory approvals for GE plants, however, may signal a shift in policy and an opening of a door to a streamlined federal regulatory pathway for commercialization for non‐food plants. The change, however, may shift regulatory battles from the federal to the state and local level, as each state has independent authority to regulate plants under respective noxious weed/plant protection statutes. This previously dormant state regulatory power could result in even more complex barriers to commercialization of GE bioenergy crops‐‐replacing the regulatory delays embedded in the federal system with regulatory chaos at the state and local level.     

Mini-review: Assessing the drivers of ship biofouling management – aligning industry and biosecurity goals

Biofouling exerts a frictional and cost penalty on ships and is a direct cause of invasion by marine species. These negative consequences provide a unifying purpose for the maritime industry and biosecurity managers to prevent biofouling accumulation and transfer, but important gaps exist between these sectors. This mini-review examines the approach to assessments of ship biofouling among sectors (industry, biosecurity and marine science) and the implications for existing and emerging management of biofouling. The primary distinctions between industry and biosecurity in assessment of vessels biofouling revolve around the resolution of biological information collected and the specific wetted surface areas of primary concern to each sector. The morphological characteristics of biofouling and their effects on propulsion dynamics are of primary concern to industry, with an almost exclusive focus on the vertical sides and flat bottom of hulls and an emphasis on antifouling and operational performance. In contrast, the identity, biogeography, and ecology of translocated organisms is of highest concern to invasion researchers and biosecurity managers and policymakers, especially as it relates to species with known histories of invasion elsewhere. Current management practices often provide adequate, although not complete, provision for hull surfaces, but niche areas are well known to enhance biosecurity risk. As regulations to prevent invasions emerge in this arena, there is a growing opportunity for industry, biosecurity and academic stakeholders to collaborate and harmonize efforts to assess and manage biofouling of ships that should lead to more comprehensive biofouling solutions that promote industry goals while reducing biosecurity risk and greenhouse gas emissions.     

Projected gains and losses of wildlife habitat from bioenergy‐induced landscape change

Domestic and foreign renewable energy targets and financial incentives have increased demand for woody biomass and bioenergy in the southeastern United States. This demand is expected to be met through purpose‐grown agricultural bioenergy crops, short‐rotation tree plantations, thinning and harvest of planted and natural forests, and forest harvest residues. With results from a forest economics model, spatially explicit state‐and‐transition simulation models, and species–habitat models, we projected change in habitat amount for 16 wildlife species caused by meeting a renewable fuel target and expected demand for wood pellets in North Carolina, USA. We projected changes over 40 years under a baseline ‘business‐as‐usual’ scenario without bioenergy production and five scenarios with unique feedstock portfolios. Bioenergy demand had potential to influence trends in habitat availability for some species in our study area. We found variation in impacts among species, and no scenario was the ‘best’ or ‘worst’ across all species. Our models projected that shrub‐associated species would gain habitat under some scenarios because of increases in the amount of regenerating forests on the landscape, while species restricted to mature forests would lose habitat. Some forest species could also lose habitat from the conversion of forests on marginal soils to purpose‐grown feedstocks. The conversion of agricultural lands on marginal soils to purpose‐grown feedstocks increased habitat losses for one species with strong associations with pasture, which is being lost to urbanization in our study region. Our results indicate that landscape‐scale impacts on wildlife habitat will vary among species and depend upon the bioenergy feedstock portfolio. Therefore, decisions about bioenergy and wildlife will likely involve trade‐offs among wildlife species, and the choice of focal species is likely to affect the results of landscape‐scale assessments. We offer general principals to consider when crafting lists of focal species for bioenergy impact assessments at the landscape scale.     

Management swing potential for bioenergy crops

Bioenergy crops are often classified (and subsequently regulated) according to species that have been evaluated as environmentally beneficial or detrimental, but in practice, management decisions rather than species per se can determine the overall environmental impact of a bioenergy production system. Here, we review the greenhouse gas balance and ‘management swing potential’ of seven different bioenergy cropping systems in temperate and tropical regions. Prior land use, harvesting techniques, harvest timing, and fertilization are among the key management considerations that can swing the greenhouse gas balance of bioenergy from positive to negative or the reverse. Although the management swing potential is substantial for many cropping systems, there are some species (e.g., soybean) that have such low bioenergy yield potentials that the environmental impact is unlikely to be reversed by management. High‐yielding bioenergy crops (e.g., corn, sugarcane, Miscanthus, and fast‐growing tree species), however, can be managed for environmental benefits or losses, suggesting that the bioenergy sector would be better informed by incorporating management‐based evaluations into classifications of bioenergy feedstocks.     

Perennial Agroenergy Feedstocks as En Route Habitat for Spring Migratory Birds

Increased production of bioenergy crops in North America is projected to exacerbate already heavy demands upon existing agricultural landscapes with potential to impact biodiversity negatively. Grassland specialist birds are an imperilled avifauna for which perennial-based, next-generation agroenergy feedstocks may provide suitable habitat. We take a multi-scaled spatial approach to evaluate the ability of two candidate second-generation agroenergy feedstocks (switchgrass, Panicum virgatum, and mixed grass–forb plantings) to act as spring migratory stopover habitat for birds. In total, we detected 35 bird species in mixed grass–forb plantings and switchgrass plantings, including grassland specialists and species of state and national conservation concern (e.g., Henslow’s Sparrow, Ammodramus henslowii). Some evidence indicated that patches with higher arthropod food availability attracted a greater diversity of migrant bird species, but species richness, total bird abundance, and the abundance of grassland specialist species were similar in fields planted with either feedstock. Species richness per unit area (species density) was relatively higher in switchgrass fields. The percent land cover of forest in landscapes surrounding study fields was negatively associated with bird species richness and species density. Habitat patch size and within-patch vegetation structure were unimportant in predicting the diversity or abundance of spring en route bird assemblages. Our results demonstrate that both switchgrass and mixed grass–forb plantings can attract diverse assemblages of migrant birds. As such, industrialized production of these feedstocks as agroenergy crops has the potential to provide a source of en route habitat for birds, particularly where fields are located in relatively unforested landscapes. Because industrialization of cellulosic biomass production will favor as yet unknown harvest and management regimes, predicting the ultimate value of perennial-based biomass plantings for spring migrants remains difficult.     

Accelerating the development of a sustainable bioenergy portfolio through stable isotopes

Bioenergy could help limit global warming to 2°C above pre-industrial levels while supplying almost a fourth of the world's renewable energy needs by 2050. However, the deployment of bioenergy raises concerns that adoption at meaningful scales may lead to unintended negative environmental consequences. Meanwhile, the full consolidation of a bioenergy industry is currently challenged by a sufficient, resilient, and resource-efficient biomass supply and an effective conversion process. Here, we provide a comprehensive analysis of how stable isotope approaches have accelerated the development of a robust bioeconomy by advancing knowledge about environmental sustainability, feedstock development, and biological conversion. We show that advances in stable isotope research have generated crucial information to (1) gain mechanistic insight into the potential of bioenergy crops to mitigate climate change as well as their impact on water and nutrient cycling; (2) develop high-yielding, resilient feedstocks that produce high-value bioproducts in planta; and (3) engineer microbes to enhance feedstock conversion to bioenergy products. Further, we highlight knowledge gaps that could benefit from future research facilitated by stable isotope approaches. We conclude that advances in mechanistic knowledge and innovations within the field of stable isotopes in cross-disciplinary research actions will greatly contribute to breaking down the barriers to establishing a robust bioeconomy.     

Quantifying targets to manage invasion risk: light gradients dominate the early regeneration niche of naturalized and pre-commercial Miscanthus populations

Prospective bioenergy crops have caused concern about their invasive potential because they often share characteristics with known invasive species. Studies that examine the factors that limit regeneration of these crop species will be crucial for identifying vulnerable habitats and devising management strategies to reduce the likelihood of escape from cultivation. Using a response surface design, we investigated the influence of light availability, soil moisture, and litter cover on recruitment and establishment of a potential biofuel cultivar of Miscanthus as well as an invasive congener. Responses were similar for the two plant types. Light availability had a strong influence on seedling success at both stages, though light limitation prevented establishment only at the lowest light level. Although variation in recruitment rates was low within plant types, establishment varied extensively in response to different light conditions. Low variation in Miscanthus seedling recruitment that led to establishment of a seedling bank under a range of light intensities may facilitate a “sit and wait” situation that raises the likelihood of successful escapes. Therefore, management efforts that restrict seed movement and increase light competition for seedlings will be important for lowering invasion risk. As deliberate introductions of bioenergy crops increase, ecological studies that quantify conditions required for successful escapes will be key to helping agronomists and managers mitigate the risk of unintended invasions.     

Development and status of dedicated energy crops in the United States

The biofuel industry is rapidly growing because of increasing energy demand and diminishing petroleum reserves on a global scale. A multitude of biomass resources have been investigated, with high-yielding, perennial feedstocks showing the greatest potential for utilization as advanced biofuels. Government policy and economic drivers have promoted the development and commercialization of biofuel feedstocks, conversion technologies, and supply chain logistics. Research and regulations have focused on the environmental consequences of biofuels, greatly promoting systems that reduce greenhouse gas emissions and life-cycle impacts. Numerous biofuel refineries using lignocellulosic feedstocks and biomass-based triglycerides are either in production or pre-commercial development phases. Leading candidate energy crops have been identified, yet require additional efforts to realize their full potential. Advanced biofuels, complementing conventional biofuels and other renewable energy sources such as wind and solar, provide the means to substantially displace humanity’s reliance on petroleum-based energy.     

Biotechnology Towards Energy Crops

New crops are gradually establishing along with cultivation systems to reduce reliance on depleting fossil fuel reserves and sustain better adaptation to climate change. These biological assets could be efficiently exploited as bioenergy feedstocks. Bioenergy crops are versatile renewable sources with the potential to alternatively contribute on a daily basis towards the coverage of modern society’s energy demands. Biotechnology may facilitate the breeding of elite energy crop genotypes, better suited for bio-processing and subsequent use that will improve efficiency, further reduce costs, and enhance the environmental benefits of biofuels. Innovative molecular techniques may improve a broad range of important features including biomass yield, product quality and resistance to biotic factors like pests or microbial diseases or environmental cues such as drought, salinity, freezing injury or heat shock. The current review intends to assess the capacity of biotechnological applications to develop a beneficial bioenergy pipeline extending from feedstock development to sustainable biofuel production and provide examples of the current state of the art on future energy crops.     

Avian use of perennial biomass feedstocks as post-breeding and migratory stopover habitat

Increased production of biomass crops in North America will require new agricultural land, intensify the cultivation of land already under production and introduce new types of biomass crops. Assessing the potential biodiversity impacts of novel agricultural systems is fundamental to the maintenance of biodiversity in agricultural landscapes, yet the consequences of expanded biomass production remain unclear. We evaluate the ability of two candidate second generation biomass feedstocks (switchgrass, Panicum virgatum, and mixed-grass prairie) not currently managed as crops to act as post-breeding and fall migratory stopover habitat for birds. In total, we detected 41 bird species, including grassland specialists and species of state and national conservation concern (e.g. Henslow's Sparrow, Ammodramus henslowii). Avian species richness was generally comparable in switchgrass and prairie and increased with patch size in both patch types. Grassland specialists were less abundant and less likely to occur in patches within highly forested landscapes and were more common and likely to occur in larger patches, indicating that this group is also area-sensitive outside of the breeding season. Variation in the biomass and richness of arthropod food within patches was generally unrelated to richness and abundance metrics. Total bird abundance and that of grassland specialists was higher in patches with greater vegetation structural heterogeneity. Collectively, we find that perennial biomass feedstocks have potential to provide post-breeding and migratory stopover habitat for birds, but that the placement and management of crops will be critical factors in determining their suitability for species of conservation concern. Industrialization of cellulosic bioenergy production that results in reduced crop structural heterogeneity is likely to dramatically reduce the suitability of perennial biomass crops for birds.     

Regulating innovative crop technologies in Canada: the case of regulating genetically modified crops

The advent of genetically modified crops in the late 1980s triggered a regulatory response to the relatively new field of plant genetic engineering. Over a 7-year period, a new regulatory framework was created, based on scientific principles that focused on risk mitigation. The process was transparent and deliberately sought the input of those involved in crop development from non-governmental organizations, industry, academia and federal research laboratories. The resulting regulations have now been in place for over a decade, and the resilience of the risk-mitigating regulations is evident as there has been no documented case of damage to either environment or human health.     

Pest-Suppression Potential of Midwestern Landscapes under Contrasting Bioenergy Scenarios

Biomass crops grown on marginal soils are expected to fuel an emerging bioenergy industry in the United States. Bioenergy crop choice and position in the landscape could have important impacts on a range of ecosystem services, including natural pest-suppression (biocontrol services) provided by predatory arthropods. In this study we use predation rates of three sentinel crop pests to develop a biocontrol index (BCI) summarizing pest-suppression potential in corn and perennial grass-based bioenergy crops in southern Wisconsin, lower Michigan, and northern Illinois. We show that BCI is higher in perennial grasslands than in corn, and increases with the amount of perennial grassland in the surrounding landscape. We develop an empirical model for predicting BCI from information on energy crop and landscape characteristics, and use the model in a qualitative assessment of changes in biocontrol services for annual croplands on prime agricultural soils under two contrasting bioenergy scenarios. Our analysis suggests that the expansion of annual energy crops onto 1.2 million ha of existing perennial grasslands on marginal soils could reduce BCI between -10 and -64% for nearly half of the annual cropland in the region. In contrast, replacement of the 1.1 million ha of existing annual crops on marginal land with perennial energy crops could increase BCI by 13 to 205% on over half of the annual cropland in the region. Through comparisons with other independent studies, we find that our biocontrol index is negatively related to insecticide use across the Midwest, suggesting that strategically positioned, perennial bioenergy crops could reduce insect damage and insecticide use on neighboring food and forage crops. We suggest that properly validated environmental indices can be used in decision support systems to facilitate integrated assessments of the environmental and economic impacts of different bioenergy policies.     

Setaria viridis and Setaria italica, model genetic systems for the Panicoid grasses

Setaria italica and its wild ancestor Setaria viridis are diploid C(4) grasses with small genomes of ～515 Mb. Both species have attributes that make them attractive as model systems. Setaria italica is a grain crop widely grown in Northern China and India that is closely related to the major food and feed crops maize and sorghum. A large collection of S. italica accessions are available and thus opportunities exist for association mapping and allele mining for novel variants that will have direct application in agriculture. Setaria viridis is the weedy relative of S. italica with many attributes suitable for genetic analyses including a small stature, rapid life cycle, and prolific seed production. Setaria sp. are morphologically similar to most of the Panicoideae grasses, including major biofuel feedstocks, switchgrass (Panicum virgatum) and Miscanthus (Miscanthus giganteus). They are broadly distributed geographically and occupy diverse ecological niches. The cross-compatibility of S. italica and S. viridis also suggests that gene flow is likely between wild and domesticated accessions. In addition to serving as excellent models for C(4) photosynthesis, these grasses provide novel opportunities to study abiotic stress tolerance and as models for bioenergy feedstocks.     

Has Selection for Improved Agronomic Traits Made Reed Canarygrass Invasive?

Plant breeders have played an essential role in improving agricultural crops, and their efforts will be critical to meet the increasing demand for cellulosic bioenergy feedstocks. However, a major concern is the potential development of novel invasive species that result from breeders' efforts to improve agronomic traits in a crop. We use reed canarygrass as a case study to evaluate the potential of plant breeding to give rise to invasive species. Reed canarygrass has been improved by breeders for use as a forage crop, but it is unclear whether breeding efforts have given rise to more vigorous populations of the species. We evaluated cultivars, European wild, and North American invader populations in upland and wetland environments to identify differences in vigor between the groups of populations. While cultivars were among the most vigorous populations in an agricultural environment (upland soils with nitrogen addition), there were no differences in above- or below-ground production between any populations in wetland environments. These results suggest that breeding has only marginally increased vigor in upland environments and that these gains are not maintained in wetland environments. Breeding focuses on selection for improvements of a specific target population of environments, and stability across a wide range of environments has proved elusive for even the most intensively bred crops. We conclude that breeding efforts are not responsible for wetland invasion by reed canarygrass and offer guidelines that will help reduce the possibility of breeding programs releasing cultivars that will become invasive.     

Biorefinery Developments for Advanced Biofuels from a Sustainable Array of Biomass Feedstocks: Survey of Recent Biomass Conversion Research from Agricultural Research Service

When the USA passed the Renewable Fuel Standards (RFS) of 2007 into law, it mandated that, by the year 2022, 36 billion gallons of biofuels be produced annually in the USA to displace petroleum. This targeted quota, which required that at least half of domestic transportation fuel be “advanced biofuels” either produced from lignocellulosic feedstocks or be a sustainable liquid fuel other than corn ethanol or biodiesel from vegetable oils, will not likely be met due to the difficulty in commercializing alternative biofuels. The number one cost to a biorefinery is the biomass feedstock cost. Thus, it is important that research into biorefinery strategies be closely coupled to advances in crop science that account for crop yield and crop quality. To reach the RFS targets, stepwise progress in biorefinery technology is needed, as the industry moves from corn ethanol toward utilizing a wider array of lignocellulose-based biomass feedstocks. In 2010, the US Department of Agriculture created five Regional Biomass Research Centers to optimize production, collection, and conversion of crops to bioenergy, thus building a network that fosters collaboration among researchers to improve the biorefinery industry. An important component of the five Regional Biomass Research Centers is the four USDA Agricultural Research Service (ARS) regional utilization laboratories located across the country. These USDA ARS labs were originally set up by their commodities, whereby, in broad terms, the Northern Lab, now NCAUR, focused on corn and soy; the Eastern Lab on oils, leather, dairy, and meats; the Southern Lab on cotton, sugars, and fibers; and the Western Lab on other grains, including wheat and specialty crops. Each lab’s traditional expertise in these respective core commodity crops has been maintained as biofuel research came to the fore, but with the addition of new crops and biotechnological expertise, these labs often collaborate with each other, as will be revealed below. This review outlines some of the recent advances from the ARS labs in developing new bioprocessing strategies required to develop bioenergy from new crop sources.     

Dedicated Energy Crops and Crop Residues for Bioenergy Feedstocks in the Central and Eastern USA

Dedicated energy crops and crop residues will meet herbaceous feedstock demands for the new bioeconomy in the Central and Eastern USA. Perennial warm-season grasses and corn stover are well-suited to the eastern half of the USA and provide opportunities for expanding agricultural operations in the region. A suite of warm-season grasses and associated management practices have been developed by researchers from the Agricultural Research Service of the US Department of Agriculture (USDA) and collaborators associated with USDA Regional Biomass Research Centers. Second generation biofuel feedstocks provide an opportunity to increase the production of transportation fuels from recently fixed plant carbon rather than from fossil fuels. Although there is no “one-size-fits-all” bioenergy feedstock, crop residues like corn (Zea mays L.) stover are the most readily available bioenergy feedstocks. However, on marginally productive cropland, perennial grasses provide a feedstock supply while enhancing ecosystem services. Twenty-five years of research has demonstrated that perennial grasses like switchgrass (Panicum virgatum L.) are profitable and environmentally sustainable on marginally productive cropland in the western Corn Belt and Southeastern USA.     

Global climate niche estimates for bioenergy crops and invasive species of agronomic origin: potential problems and opportunities

The global push towards a more biomass-based energy sector is ramping up efforts to adopt regionally appropriate high-yielding crops. As potential bioenergy crops are being moved around the world an assessment of the climatic suitability would be a prudent first step in identifying suitable areas of productivity and risk. Additionally, this assessment also provides a necessary step in evaluating the invasive potential of bioenergy crops, which present a possible negative externality to the bioeconomy. Therefore, we provide the first global climate niche assessment for the major graminaceous (9), herbaceous (3), and woody (4) bioenergy crops. Additionally, we contrast these with climate niche assessments for North American invasive species that were originally introduced for agronomic purposes as examples of well-intentioned introductions gone awry. With few exceptions (e.g., Saccharum officinarum, Pennisetum purpureum), the bioenergy crops exhibit broad climatic tolerance, which allows tremendous flexibility in choosing crops, especially in areas with high summer rainfall and long growing seasons (e.g., southeastern US, Amazon Basin, eastern Australia). Unsurprisingly, the invasive species of agronomic origin have very similar global climate niche profiles as the proposed bioenergy crops, also demonstrating broad climatic tolerance. The ecoregional evaluation of bioenergy crops and known invasive species demonstrates tremendous overlap at both high (EI≥30) and moderate (EI≥20) climate suitability. The southern and western US ecoregions support the greatest number of invasive species of agronomic origin, especially the Southeastern USA Plains, Mixed Woods Plains, and Mediterranean California. Many regions of the world have a suitable climate for several bioenergy crops allowing selection of agro-ecoregionally appropriate crops. This model knowingly ignores the complex biotic interactions and edaphic conditions, but provides a robust assessment of the climate niche, which is valuable for agronomists, crop developers, and regulators seeking to choose agro-ecoregionally appropriate crops while minimizing the risk of invasive species.     

Fuzzy GIS‐based multi‐criteria evaluation for US Agave production as a bioenergy feedstock

In the United States, renewable energy mandates calling for increased production of cellulosic biofuels will require a diversity of bioenergy feedstocks to meet growing demands. Within the suite of potential energy crops, plants within the genus Agave promise to be a productive feedstock in hot and arid regions. The potential distributions of Agave tequilana and Agave deserti in the United States were evaluated based on plant growth parameters identified in an extensive literature review. A geospatial suitability model rooted in fuzzy logic was developed that utilized a suite of biophysical criteria to optimize ideal geographic locations for this new crop, and several suitability scenarios were tested for each species. The results of this spatially explicit suitability model suggest that there is potential for Agave to be grown as an energy feedstock in the southwestern region of the United States – particularly in Arizona, California, and Texas – and a significant portion of these areas are proximate to existing transportation infrastructure. Both Agave species showed the highest state‐level renewable energy benefit in Arizona, where agave plants have the potential to contribute 4.8–9.6% of the states' ethanol consumption, and 2.5–4.9% of its electricity consumption, for A. deserti and A. tequilana, respectively. This analysis supports the feasibility of Agave as a complementary bioenergy feedstock that can be grown in areas too harsh for conventional energy feedstocks.     

Farmers’ Willingness to Produce Alternative Cellulosic Biofuel Feedstocks Under Contract in Kansas Using Stated Choice Experiments

Many studies have assessed the technical feasibility of producing bioenergy crops on agricultural lands. However, while it is possible to produce large quantities of agricultural biomass for bioenergy from lignocellulosic feedstocks, very few of these studies have assessed farmers’ willingness to produce these crops under different contracting arrangements. The purpose of this paper is to examine farmers’ willingness to produce alternative cellulosic biofuel feedstocks under different contractual, market, and harvesting arrangements. This is accomplished by using enumerated field surveys in Kansas with stated choice experiments eliciting farmers’ willingness to produce corn stover, sweet sorghum, and switchgrass under different contractual conditions. Using a random utility framework to model the farmers’ decisions, the paper examines the contractual attributes that will most likely increase the likelihood of feedstock enterprise adoption. Results indicate that net returns above the next best alternative use of the land, contract length, cost share, financial incentives, insurance, and custom harvest options are all important contract attributes. Farmers’ willingness to adopt and their willingness-to-pay for alternative contract attributes vary by region and choice of feedstock.