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Adding Biodiversity to Agricultural Landscapes Through Ecology and Biotechnology

Summary and Keywords

Agriculture is practiced on 38% of the landmass on Earth, and having replaced natural ecosystems, it is the largest terrestrial biome on Earth. Agricultural biomes are typically focused on annual crops that are produced as a succession of genetically uniform monocultures. Compared to the ecosystems they replaced, agroecosystems provide fewer ecosystem functions and contain much less biodiversity. The large-scale conversion from natural lands to agriculture occurred centuries ago in the Old World (Africa, China, Europe, and India), but in many areas during the latter 20th and early 21st centuries, especially tropical areas with rich biodiversity, agriculture is an emerging industry. Here, displacement of natural ecosystems is also a late 20th-century occurrence, and much of it is ongoing. Regardless of where or when agriculture was established, biodiversity declined and ecosystem services were eroded.

Agricultural practices are the second largest contributor to biodiversity loss, due to the loss of habitat, competition for resources, and pesticide use. Most (~96%) of the land used to produce crops is farmed using conventional methods, while smaller percentages are under organic production (~2%) or are producing biotech crops (~4%). Regardless of how agriculture is practiced, it exacts a toll on biodiversity and ecosystem services. While organic agriculture embraces many ecological principals in producing food, it fails to recognize the value of biotechnology as a tool to reduce the environmental impact of agriculture. Herbicide- and/or insect-resistant crops are the most widely planted biotech crops worldwide. Biotech crops in general, but especially insect-resistant crops, reduce pesticide use and increase biodiversity. The widespread adoption of glyphosate-resistant crops increased the use of this herbicide, and resistance evolved in weeds. On the other hand, glyphosate has less environmental impacts than other herbicides. Because of the limited scale of biotech production, it will not have large impacts on mitigating the effects of agriculture on biodiversity and ecosystem services. To have any hope of reducing the environmental impact of agriculture, agro-ecology principals and biotechnology will need to be incorporated. Monetizing biodiversity and ecosystem services through incorporation into commodity prices will incentivize producers to be part of the biodiversity solution. A multi-level biodiversity certification is proposed that is a composite score of the biodiversity and ecosystem services of an individual farm and the growing region were the food is produced. Such a system would add value to the products from farms and ranches proportionate to the level by which their farm and region provides biodiversity and ecosystem services as the natural ecosystem it replaced.

Keywords: biodiversity, ecosystem services, GMOs, organic agriculture, conventional agriculture, agroecology, communicating science, monetizing biodiversity, biodiversity farming certification

Introduction

Agriculture is practiced on 38.4% of the landmass on Earth (FAOSTAT, 2019), and having replaced natural ecosystems, it is the largest terrestrial biome on Earth. While agriculture has largely been practiced using the same crops and cultural methods since plants were first domesticated, advances in science and technology have added a third phase, genetic engineering, to follow the first phase, domestication, and the second phase, breeding. Genetically modified organisms (GMOs), also known as genetically engineered (GE) crops, or biotech crops, have been commercially produced since 1994. Although widely accepted by scientific organizations across the life sciences, they are not accepted by large segments of the population, a worldwide phenomenon. Conversely, the scientific community, based on the accumulated evidence, has concluded these technologies are safe for the environment, humans, and the livestock animals that have been fed biotech crops. Crop production is usually classified as conventional, organic, or biotech depending on the cultural practices and whether a genetically modified crop is grown. Conventional crop production typically includes the use of hybrids, inbred lines, and in some cases open pollinated varieties. Biotech crop production uses hybrid varieties which have genetically engineered “trait events,” most often herbicide- or insect-resistant traits, or both. Organic production, on the other hand, can use hybrids, inbred varieties, or open pollinated varieties, but not a biotech variety. Conventional agriculture typically relies on synthetic chemical fertilizers and pesticides, whereas organic production does not allow synthetic chemicals. Instead, organic producers incorporate ecological principles to control weeds and insects and provide mineral nutrition to plants and typically utilize more complex crop rotation schemes than conventional agriculture (Pimentel, Hepperly, Hanson, Douds, & Seidel, 2005).

Regardless of how agriculture is practiced, it replaced land that supported plants and animals that together defined an ecosystem. Agriculture is a major driver in the overwhelming loss of biodiversity the world experienced during the 20th century, and the loss of biodiversity continues today (IPBES, 2019; Maxwell, Fuller, Brooks, & Watson, 2016). This is simply because agriculture contributes to the loss of habitat needed for the survival and evolution of the naturally occurring plants and animals. This can be further exacerbated when there is competition for limited resources or when pesticides and fertilizers have effects beyond their applied area. There is emerging evidence that where agriculture is practiced to maintain or enhance ecosystem services that agriculture production itself benefits from ecosystem services from robust naturally occurring ecosystems (Power, 2010). This article will address the history of humans as engineers that led naturally to genetic engineering, provide an overview of the consequences of practicing agriculture on a global and transformative scale, and discuss the need to innovate new approaches to use biotechnology and ecology to mitigate the impacts of agriculture. A mechanism is proposed by which to monetize biodiversity and ecosystem services in agriculture. A biodiversity certification program would be used to add value to the food produced by those that incorporate ecological practices that conserve or enhance biodiversity and ecosystem services.

The Innate Engineer

The arc of human evolution is in part defined by our increasing capacity to manipulate our environment. Evidence of human (i.e., genus Homo)-engineered tools date back 2.6 million years ago (MYA) (Semaw et al., 1997; Sileshi Semaw et al., 2003), and evidence of pre-hominin tools from 3.3 MYA (Harmand et al., 2015) indicate that our ability to use and make tools to manipulate the natural world for survival is a basal trait. Humans developed the capacity for higher-order thinking to observe, synthesize, and remark about their natural world through figurative art, leaving evidence some 40,000 to (Aubert et al., 2014; Aubert et al., 2018) 64,000 years ago (Hoffmann et al., 2018). Pottery, needed to securely store food and cooking, is known from 20,000 years ago (Wu et al., 2012), preceding the recognized boundaries of agriculture by several thousand years. Humans have responded to the persistent threats of food insecurity by manipulating their environment to favor agriculture, applying engineering and scientific knowledge to expand agriculture and make it a more efficient enterprise. Archaeological evidence including silt deposits (Jacobsen & Adams, 1958; Sandor, Eash, & NS, 1995), tax records (Jacobsen & Adams, 1958), and carbon isotope discrimination of grains grown in early agricultural centers (Ferrio, Araus, Buxó, Voltas, & Bort, 2005; Riehl, Pustovoytov, Weippert, Klett, & Hole, 2014) indicate that humans have manipulated water systems to irrigate crops for at least 10,000 years in present-day Middle East and since at least 6,700 years ago in South America (Dillehay, Eling, & Rossen, 2005). Even at the earliest stages of agriculture, manipulating the natural environment had consequences that required solutions. Diversion of water from natural ecosystems to agriculture resulted in increases in soil salinity that resulted in decreased crop yields (Helbaek, 2014; Jacobsen & Adams, 1958), and crops that were more tolerant to salinity had to be grown (Helbaek, 2014). Irrigation, however, conferred less exposure of crops and domesticated livestock to the vagaries of droughts, shifted some cultures to a sedentary lifestyle, and increased social interactions within communities. As agricultural practices evolved and new foods became more commonplace, alleles in the human genome that altered enzyme activity and metabolism became more common in certain populations (Laland, Odling-Smee, & Myles, 2010). Agriculture has thus transformed societies and altered our genomes, but because of the scale on which it is practiced today, made necessary because of expanding world population, it also has had profoundly negative effects on the natural world.

Agriculture developed independently on multiple continents, but evidence of the earliest agricultural beginnings, the domestication of cereals in the Middle East, occurred some 12,000 years ago (Diamond, 2002; Riehl, Zeidi, & Conard, 2013). Each crop and livestock animal that today provides our food existed in a natural (wild) state long before humans intervened. Each crop or livestock animal experienced a domestication path that lasted several hundred to thousands of years (Frantz et al., 2015; Hilbert et al., 2017; Kistler et al., 2018) and, by necessity, resulted in reduced genetic (allelic) diversity to reach its current state. Evidence of the domestication process has been provided through traditional archaeological methods, while DNA sequencing has been used to identify loci within plant and animal genomes that were the targets of human selection during the domestication process (Zhou et al., 2016). Evidence indicates that agriculture is practiced today largely as it was at the beginning and that the same challenges that faced humankind at that time have never been overcome. For example, archaeological evidence of early rice plantings ~5300 bce indicate rice was grown as a monoculture and that weeds were present in the production fields (Fuller et al., 2009), indicating that crops and weeds have always coexisted.

The domestication of crops and livestock occurred without knowledge of genetic principles, yet these crops and animals performed reasonably well. For example, yields of maize grown by Native Americans were comparable to that of maize varieties utilized in breeding programs and sold by seed companies early in the 20th century (Hayes & Garber, 1927). Mendel’s work (1865) and rediscoveries of his paper in the early 20th century established the genetic foundations by which breeding schemes of crops and livestock were developed to increase yields by reducing losses to diseases and insects, altering morphology, and improving resistance to abiotic stresses. Maize has long been a model for genetics and many of the genetic principles and breeding schemes were developed using this crop. For example, maize varieties sold in the United States from 1860 to 1920 were open pollinated, and yields did not increase during that period. Double crosses were introduced and used from 1921 to 1960, and yield increased an average of 1.10 bu/acre/year. As genetic knowledge accumulated and combining abilities of the different varieties became known, single cross F1 hybrids were used and yields increased from 62.4 bu/ac/year in 1961 to 176.4 bu/ac/year in 2018 (Allard, 1999; USDA ERS, 2019).

The efficiency and the magnitude of improvement by which plants and animals can be modified is accomplished by identifying and understanding the genetic basis underlying the traits of interest. Early geneticists developed genetic maps to establish the linear order of genes and estimate how many genes control a given trait. The first genetic map was created to establish the number and order of genes affecting eye color in Drosophila (Sturtevant, 1913). Over the next 60 years, this method was used to deduce the location of genetic loci associated with easily discernible traits. For example, early genetic maps of tomato and maize contained 45 and 58 loci that were associated with various morphological traits (Butler, 1952; Emerson, 1932). Methods were developed that advanced understanding of DNA and RNA molecules, especially electrophoresis (Markham & Smith, 1952) and restriction enzymes (Linn & Arber, 1968), and they were quickly adopted by geneticists and breeders to develop genetic maps based on DNA markers and identify loci associated with simple qualitative traits (Botstein, White, Skolnick, & Davis, 1980; Lander & Botstein, 1986). The use of DNA-based markers led to the “Mendelization” of quantitative traits in which DNA markers were statistically associated with a phenotype to estimate the number of loci and the effect of those loci in the expression of the trait under study (Lander & Botstein, 1989; Paterson et al., 1988).

Further technological developments advanced the abilities and efficiency of breeders. The ability of biologists to harness enzymes that replicate and synthesize short stretches of DNA was made possible through the development of the polymerase chain reaction (PCR) and the apparatus that automated it, the PCR machine; these advances revolutionized biology. Sanger sequencing methods, followed by second- and third-generation sequencing technologies, lowered costs per read and led to long-length reads, respectively, allowing biologists insights into long-standing fundamental questions in biology, medicine, evolution, and ecology. These sequencing technologies applied to unstructured populations enabled genome wide association studies, or applied to sophisticated structured mapping populations (e.g., nested association populations), provided abilities to more precisely, accurately and efficiently improve traits in plants and animals through traditional breeding. The genomes of many crop plants and livestock animals have been sequenced and serve as reference sequences by which to identify candidate genes underlying a quantitative trait locus from a genetic map. Today, the current version of the tomato genome (version ITAG4.0) has identified 34,075 genes, of which 4,794 are novel. There are several maize genotypes serving as reference genomes; B73 (INSDC Assembly GCA_0000005005.6) identified 39,591 genes. Low-level genome sequencing of populations (e.g., genotyping-by-sequencing), sophisticated interrelated and large mapping populations (e.g., nested association populations), have provided information on the magnitude of allelic effects, epistasis, pleiotropy, and gene–environment interactions and have allowed breeders to maximize the genetic potential in maize (Buckler et al., 2009). Many important agronomic traits are genetically complex, and typically, many small-effect loci modulate the expression of the trait. Time to flowering in maize, for example, is controlled by 36 and 39 loci for male and female flowers, respectively (Buckler et al., 2009). Due to linkage and the inability to control or accurately predict crossover events, the ability to improve traits controlled by multiple, small-effect loci is limited. However, when genes, loci, and specific alleles are identified, this informs gene editing targets and, by reducing the number of backcrosses needed, can dramatically shorten the breeding cycle and the release of genetically uniform and stable varieties.

The use of these molecular and genetic tools yields information that improves the efficiency and capabilities of breeders, but the magnitude of improvement or adaptation is limited to that which exists in the sexually compatible gene pool of that crop. The same tools also provide information needed to engineer plants and animals and, as a process, yield much more predictable results than currently possible using traditional breeding approaches. Importantly, these tools enable traits to be improved or the introduction of traits for which natural variation does not exist. The tools used in current biotech crops, those used in gene/genome editing, and those being developed in systems biology allow greater and more precise control over genes and genomes than the tool used by domesticators over the millennia and breeders over the last century—selection and improvement based on phenotypic selection.

The Introduction and Rejection of GMOs

While breeders were early adopters of the molecular tools being developed to exploit natural variation available in gene pools, early practioneers of biotechnology envisioned altering traits beyond what breeders could accomplish or that which existed in nature. Because DNA is the basic building block of life, if a gene existed in nature, it had the potential to be expressed in a plant. A mood of “vibrant optimism” (Lyons, 1983) surrounded agriculture biotechnology, which promised a bounty that could feed billions more hungry people. The initial goals for crops produced through plant biotechnology and announced through the popular press were similar to the objectives of plant biologists and plant breeders. They included (Lyons, 1983):

  • Crops that will be less susceptible to diseases caused by viruses, bacteria, fungi, and worms.

  • A greater resistance to stresses brought on by drought, salinity, chill, and frost.

  • More efficient crops that will better absorb fertilizer.

  • Plants able to make their own nitrogen fertilizers.

  • An increase in plants’ photosynthetic efficiency through more effective trapping of light.

  • Genetic regulation of plant growth, for example, the development of dwarf fruit and nut trees easier to harvest with machines,

  • Control over the cellular architecture of a plant, making its fruit lower in water content and higher in solids.

Very few articles on agriculture biotechnology appeared in the popular press between 1980 and 1990. This, coupled with a lack of public understanding of the science of biotechnology, allowed public and industry scientists to work on projects that were scientifically interesting and would help establish the boundaries of technical feasibility. For industry, the technology promised new products and production efficiencies.

The first reports in the popular press of genetic engineering of plants indicated that the new technology was enthusiastically embraced by a wide variety of chemical, pharmaceutical, and oil companies that were at that time invested in agriculture (e.g., DuPont, Pfizer, Upjohn, Ciba-Giegy, Atlantic Richfield, Occidental Petroleum, and Monsanto—originally a chemical/pharmaceutical company that transitioned into agriculture) with predictions that the agricultural market would outperform the medical market (Crittenden, 1981). Early promises of the products that agriculture biotechnology would deliver were perhaps overstated and underdelivered. Articles in the popular press suggested there would be “perennial corn,” crops that can fix their own nitrogen, potatoes and tomatoes on the same vine, and “plants that tolerate high levels of salt in heavily irrigated soil.” Great profits were forecast in New York Times headlines from that period: “The gene machine hits the farm,” (Crittenden, 1981) which proclaimed that “Behind each vision lurks a multibillion dollar market.” At this stage of agricultural biotechnology, it was 20 years before the first plant genome was sequenced (Arabidopsis thaliana) whose complexity and number of genes surprised most scientists. While it revealed the complexity of plant genomes, it also provided the roadmap by which whole genome sequencing would deliver unparalleled insight into plant evolution, form, function, and metabolic pathways and lead to other complementary “omic” technologies.

The first commercialized GMO crop, the FLAVR SAVR tomato, was released in 1994 and caused an “enormous media stir,” much of it positive (Winerip, 2013). Prior to this release, 28% of the U.S. public said the potential risks of genetic engineering of foods outweighed the benefits (Shanahan, Scheufele, & Lee, 2001); by 2015, 57% of the U.S. public believed GM foods were unsafe (PEW Research Center 2015) and 47% of the surveyed public in China were not comfortable with GMO crops (Cui & Shoemaker, 2018). The European Union public has long rejected GMO crops (Bonny, 2003).

The first commercially released biotech crop promised to fix a problem in tomatoes that developed through decades of breeding. In addition to breeding for disease resistance and fruit qualities, breeders had been adapting tomatoes that would allow tomatoes to be mechanically harvested and shipped long distances. Because of genetic linkage, modern commercial cultivars lost their flavor during this process. The Imperial Chemical Industries P.L.C. of Britain and Calgene, Davis, CA, funded research aimed to change the flavor and rate of ripening of the tomato to extend its post-harvest shelf life and improve its taste (Feder, 1992). By slowing down the rate of polygulactoronase with antisense RNA, the fruit could be held on the plant longer to accumulate solids and improve flavor and still maintain firmness to allow shipping. The first genetically engineered product, the FLAVR SAVR tomato, was approved for deregulation by the USDA in July 1992 and finalized in October and was approved by the U.S. FDA for human consumption in May 1994. While sold in grocery stores and labeled as a genetically engineered tomato, it was accepted by consumers (Winerip, 2013). The product failed for reasons completely unrelated to its biotech properties.

Other crop-related early genetic engineering projects were not as well received (Tivnan, 1988). The first release of a genetically engineered organism into the environment occurred in 1985. Advanced Genetic Sciences of Oakland, CA, received approval by the U.S. Environmental Protection Agency (EPA) to release bacteria that were modified to prevent ice nucleation and protect, in this trial, strawberry plants against freeze damage. After approval by the EPA, a lawsuit led by Jeremy Rifkin was filed to stop the trials, claiming the risks to the natural world were too high. The company had plans to sell the bacteria, called Frostban. Although the trials worked and the bacteria helped prevent frost damage, the public was not receptive to releasing bioengineered organisms into the environment, portending the problems biotechnology would face as the potential environmental risks of biotech crops resonated with the public.

Monarch butterflies have long been a symbol of the potential environmental impacts of biotech crops. The popular press widely reported results of a laboratory experiment in which Monarch butterfly caterpillars fed pollen from transgenic Bacillus thuringiensis (Bt) maize grew slower and had higher mortality rates than those fed pollen from the non-transgenic maize variety (Losey, Rayor, & Carter, 1999; Yoon, 1999). Multiple field studies later showed mortality rates of Monarch butterflies were not different between fields growing transgenic maize or its non-transgenic counterpart (Oberhauser et al., 2001). Importantly, they concluded that rather than Bt maize being a threat to monarch butterflies, common agricultural practices such as weed control and foliar insecticide use could have large impacts on monarch populations. Indeed, widespread planting of herbicide-tolerant (HT) soybean and maize has resulted in the loss of milkweed, the only food source for Monarch butterfly caterpillars. The clean-field approach associated with HT crops has been blamed for the decline of the Monarch butterfly, known as the “milkweed limitation hypothesis.” Other factors have also contributed to the wild fluctuations observed in Monarch butterfly numbers that occur during the migration between the United States and Mexico. These include sublethal exposure to pesticides, road mortality, and increasing amounts of disease (Agrawal & Inamine, 2018). It is worth noting that monarch butterfly populations were in decline in California before the release of transgenic crops, suggesting other mitigating factors are involved.

The GMO–monarch butterfly story is illustrative of the problems at the interface of science and social media. The original monarch paper was not peer-reviewed, but its alarming conclusion, and others that reported similar harmful effects on the monarch, received widespread global coverage in the popular press. Careful, peer-reviewed studies that provided context and careful evaluation outlining the potential impacts and that concluded Bt maize pollen did not lead to higher monarch caterpillar mortality received scant public attention (Shelton & Sears, 2001). The fact that scientists can alter organisms beyond what occurred through domestication and breeding alarms the public and is perceived as not being natural. The environmental consequences, they argue, are unknown and potentially catastrophic. Evolution, however, uses the same four nucleotides as the instructional material for building organisms, regardless of the organism, and the use of these nucleotides is, by definition, natural. Thus, the objection by the public to GMO crops is the process by which they are made, not the product. Worldwide, agencies that oversee the safety of GE crops regulate the process, not the product, bypassing consumers to make market choices and pre-empting the development of new products, especially non-commodity specialty crops (Bradford, Van Deynze, Gutterson, Parrott, & Strauss, 2005; Miller & Bradford, 2010).

While some may be alarmed that science has developed the ability to bioengineer crop plants, humans, as engineers, have changed the natural world to an extent that every ecosystem on Earth has been altered. The degradation of ecosystems, not GMOs, is the much greater threat to the planet. Indeed, human activities in general degrade Earth’s ecosystems, but agriculture in particular is the second largest human activity driving the placement of taxa onto the International Union for the Conservation of Nature (IUCN) Red List of Threatened SpeciesTM, meaning their numbers are thought to be so low their survival is threatened or endangered. Much of the damage done to ecosystems occurred during the period coinciding with the Industrial Revolution and European expansion to new continents and islands, but it is ongoing. A recent Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES, 2019) concludes that given current practices, up to 1.175 million plants and animals will go extinct, with catastrophic consequences for the Earth’s biosystems and national economies. Changes in land and sea use, including for food production, is the largest driver of biodiversity loss (FAO, 2019). To the extent that biotechnology can be used to mitigate the effects of agriculture and human encroachment on wildlands, it should be utilized and its role in this regard recognized and promoted.

What Are the Facts of GMO Crops?

A biotech crop is one in which recombinant deoxyribonucleic acid (rDNA) methods have been used to insert a gene from another species to alter the expression of a trait (National Academies of Sciences, Engineering, & and Medicine, 2016). Biotech crops were grown on 190 M ha worldwide in 2017, equivalent to 3.9% of the total global crop acreage (FAOSTAT, 2019; ISAAA, 2017). Although biotech crops were grown in 24 countries, 5 countries accounted for 91% of the acreage planted globally, with the United States accounting for nearly 40% of the total. When a modification is made to alter a single trait, it is referred to as a single-event trait; several traits can be combined within the same plant through genetic engineering or conventional crossing of two plants, referred to as gene stacking or pyramiding. In the United States, 19 crops species have had 197 single-event traits approved, but only three crops—maize, cotton, and soybeans—comprised 96% of the global biotech crop acreage planted (ISAAA, 2017; USDA ERS, 2019). Despite the relatively small percentage of total global acreage planted in biotech crops, the impacts can be locally significant since a given biotech crop may dominate the agricultural plantings across that region. For example, in the United States, 10 biotech crops were planted across 75 million ha, with maize and soybeans accounting for ~91% of the total acreage (ISAAA, 2017; USDA ERS, 2019) . In the United States, 92% of the corn, 94% of the cotton, and 94% of the soybeans planted in 2018 contained at least one GE trait, predominantly herbicide tolerance or insect resistance (USDA ERS, 2019).

Overall, compared to conventional crops, the production of a biotech crop requires that less pesticides be applied. Relative to conventional crops, biotech crops did not require the use of 671 million kg of active ingredients between 1996 and 2016 (ISAAA, 2017). During the 2016 production year, 48.5 million kg of pesticides (active ingredients) were not applied to biotech crops (ISAAA, 2017), which represents ~1.9% of the total amount of pesticide active ingredient applied worldwide in 2016 (FAOSTAT, 2019). While the global reduction in pesticide use due to biotech crops is relatively small, in regions where biotech crops (herbicide-tolerant and/or insect-resistant) dominate production, how much and what pesticides are used can be significantly different depending on crop.

Herbicide tolerance is the dominant GE trait, covering 47% of the global biotech crop acreage (ISAAA, 2017) with glyphosate resistance as the most common engineered trait (Duke, 2018). The glyphosate resistance trait was first introduced in 1996 in soybean, and within 10 years, 90% of all GE soybean crops planted were resistant to glyphosate (Duke, 2018). In the United States, ~97% of the GE maize crop planted in 2017 was herbicide tolerant, either as a single herbicide-tolerant trait or a stacked trait with insect resistance plus herbicide tolerance (Duke, 2018; ISAAA, 2017). A 13-year study conducted between 1998 and 2011 found that growers of glyphosate-tolerant soybeans used 28% more herbicides than non-adopters, while maize growers used 1.2% less. Glyphosate use in soybeans and maize increased during this period but replaced herbicides that were more harmful to humans and the environment. The impact of pesticides is often measured by the environmental impact quotient (EIQ), and because glyphosate has a relatively low EIQ, the increased use of this herbicide had a similar impact as that used by soybean growers that used less herbicides but that were more environmentally harmful (Perry, Ciliberto, Hennessy, & Moschini, 2016). By the same comparison, growers of insect-resistant maize used 11.2% less insecticides than non-adopters (active ingredient basis), equivalent to a 10.4% reduction in the EIQ (Perry et al., 2016). These trends observed in the United States appear amenable to the generalization that less synthetic insecticides have been applied to fields growing Bt crops and, in some cases, non-Bt fields in proximity of Bt fields have seen a reduction in synthetic pesticides as well (reviewed in NAS, 2016).

Agriculture is in a genetic race with organisms that, due to large population sizes and short generation times, can respond more quickly to selection pressure and develop resistance faster than breeders can develop resistance in crops. Herbicides and insecticides act as a selection pressure, and their overuse has long been recognized as accelerating the evolution of herbicide-resistant weeds and insecticide-resistant insect populations. The extensive use of glyphosate-tolerant biotech crops has resulted in sharp increases in the amounts of glyphosate used, and by 2019, tolerance had evolved in 43 weed species (Duke, 2018; Heap, 2019). Similarly, excessive exposure to Bt crops will result in insect tolerance or resistance. To reduce the evolution of resistant insect populations, Bt crops require refuges of non-Bt crops be interplanted, but over time, Bt-resistant insect populations have been reported and appear to be accelerating (Tabashnik & Carrière, 2017). While structured refuges have long been advocated to delay the evolution of resistance, serendipitous plantings over a 11-year period of a mixture of Bt to non-Bt seeds (3:1, respectively) conferred protection and resistance did not develop, suggesting perhaps a more effective strategy to limit evolution of resistance than structured refuges (Tabashnik & Carrière, 2017).

A possible unintended environmental effect of Bt crops is that they could also impact off-target organisms and reduce insect biodiversity. In maize, for example, Bt crops target lepidopteran larvae that feed on stalks, ears, or leaves and coleopteran larvae that feed on roots. Similarly, weed biodiversity could be decreased by the use of herbicide-tolerant GE crops. However, insect biodiversity has been higher in Bt crops when compared to the same non-Bt varieties planted, and weed biodiversity in herbicide-resistant maize and soybean crops had similar weed biodiversity of those fields planted with non-GE crops(National Academies of Sciences, Engineering, and Medicine, 2016). The U.S. National Academies concluded that the key to preserving biodiversity was to use GE crops in situations that promoted long-term economic and resource sustainability (National Academies of Sciences, Engineering, and Medicine, 2016). For example, planting stress-adapted GE crops into marginal natural lands that are not currently in production is not sustainable since it would replace natural lands with agriculture with negative impacts on biodiversity. Instead, GE crops that confer greater resistance or tolerance to abiotic stresses should be planted in areas currently under production to mitigate abiotic stresses that are predicted to increase in intensity and duration as global warming progresses (Lobell, Schlenker, & Costa-Roberts, 2011; Rosenzweig et al., 2014)

Characterizing soil biotic communities and understanding their role in agriculture and sustainability is a nascent but active field. A five-year study indicated that arthropods and microbial diversity of soils were similar between a transgenic poplar expressing Bt and its non-GE clone (Zuo et al., 2018). However, these conclusions were based only on bacteria that could be cultured, and since only a small fraction of soil bacteria can be cultured (Chaudhary, Khulan, & Kim, 2019; Stewart, 2012), the possible effects of the transgenic poplar on the full microbial community are not known. Other studies did not rely on the smaller subset of bacteria that can be cultured, but instead sequenced all the DNA that could be extracted from the soil; they concluded that with respect to diversity and abundance, bacterial communities were similar between transgenic Cry1Ac cotton and sugarcane and their same-variety non-transgenic controls (Li et al., 2018; Zhou et al., 2016).

Since the first commercial biotech crops were introduced in 1994, over 2.34 billion ha have been planted (ISAAA, 2017). A large body of primary literature exists regarding safety and risks of GE crops. Globally, over 280 scientific, professional organizations and institutions (e.g., AAAS, AMA, ASPB, Chinese Academy of Sciences, European Commission, European Food Safety Authority, FAO, OECD, Royal Science, U.S. National Academies of Science, and the WHO) have weighed the evidence and concluded, overall, that GE crops are safe for the environment, humans, and livestock animals (Norero, 2019). Of note, the U.S. National Academies considered the safety or negative effects of GE crops, sought “all credible views,” and did not selectively use sources to justify a preferred outcome. The U.S. National Academies concluded that GE crops did not contribute to environmental problems and that GE crops do not introduce an additional risk to human health, which is an expected outcome since the biochemical content between a GE crop and its non-GE counterpart is essentially the same (National Academies of Sciences, Engineering, and Medicine, 2016). Billions of livestock have been raised on GE feed with similar (or better) animal performance and health outcomes than those observed before GE feed was introduced and used (Van Eenennaam & Young, 2014). Regarding the social and economic consequences of biotech crops, compared to non-GE counterparts, profit is higher for GE crops regardless whether the crop is produced in developed or developing countries (ISAAA, 2017). While profitability depends on the crop, GE trait, and commodity prices, most growers of GE crops have benefited. Since 1996, farmers growing single and stacked GE traits in soybean, maize, cotton, canola, papaya, and sugar beets have accumulated an estimated $186 billion of benefits compared to conventional crops (ISAAA, 2017). Farmers benefited from using less labor, no-till technology associated with herbicide tolerance, and reduced use of insecticides.

The scientific evidence regarding the safety and risks of GMOs is based on the commercial production of biotech crops that, cumulatively, have been grown since 1994 on over 2.34 billion ha worldwide. While GMO technology is not without risk, these are generally well recognized by the scientific community and industry. Potential risks include deleterious effects on human and animal health including inducing allergic reactions; alterations of intestinal mucosa or microbiota from GE foods; unintended socioeconomic issues related to GE crops in developing countries; loss of biodiversity due to GE crops; and the development of herbicide- or insecticide-tolerant/resistant weeds and crops, respectively (National Academies of Sciences, Engineering, and Medicine, 2016). Current and future technologies and their products, however, should continue to be evaluated by independent entities rather than the companies developing them, and the peer-reviewed results communicated transparently to the public.

What Influences Attitudes, Beliefs, and Acceptance of GMOs and Science?

Acceptance and attitudes regarding GMOs has at least partly been driven by a public who distrust their government, the media, and, increasingly, higher education and science, but beliefs and receptiveness are tempered by religious and political views (Pew Research Center, 2015). It is important that scientists understand and learn how to communicate effectively with the public and policymakers. Data are the currency by which scientists develop, support, or refute hypotheses and by which other scientists can be persuaded to adopt or reject a theory. Data and facts, however, do not tend to change minds and opinions outside science fields. Perhaps as a consequence of the declining belief in experts, an increasing portion of the population believe that their opinion is as correct and equally valid as that of an expert (Nichols, 2017). Extreme opponents of GMOs in France, Germany, and the United States are less knowledgeable about science and genetics, yet think they know the most, when in fact, they know the least compared to others with less extreme views (Fernbach, Light, Scott, Inbar, & Rozin, 2019). People tend to discount evidence that contradicts their personally held beliefs, and as a person updates their beliefs, undesirable information is underweighed relative to desirable information (Sharot, 2017). A person is less likely to accept as true a set of facts that is counter to their strongly held belief and when faced with counterevidence remain resolute. Based on MRI imaging and fMRI data analyses, this phenomenon appears to be a neurologically based emotional response. Belief resistance showed increased response in the dorsomedial prefrontal cortex and decreased activity in the orbitofrontal cortex, which appears to be a protective mechanism against counterevidence ((Kaplan, Gimbel, & Harris, 2016). These results suggest that engaging with the public and policymakers to provide data-driven information in the early stages of technology development and the rollout of products is likely to promote a balanced and informed understanding of science issues.

The tendency for people to seek confirming evidence, as opposed to both confirming and disconfirming, is known as confirmation bias (Mynatt, Doherty, & Tweney, 1977; Nickerson, 1998; Wason, 1960). Social media and search engines have tremendous capacity to reinforce confirmation bias. Multiple studies have assessed various social media platforms, and the data clearly show that people rarely engage in discourse with others outside their set of values (Barberá, Jost, Nagler, Tucker, & Bonneau, 2015; Takikawa & Nagayoshi, 2017), but seeking broader views is also influenced by religious and political views (Pew Research Center, 2015). Unless search engines are used under an anonymous or incognito function, results are returned that are deemed more relevant to the geographic origin of the search and from the residual data collected from previous searches, which together are likely to reveal political and social tendencies of the searcher with high probabilities (Bao, Zheng, Wilkie, & Mokbel, 2015; Kliman-Silver, Hannak, Lazer, Wilson, & Mislove, 2015). Thus, individuals seeking information and opinions that may conflict with and challenge their beliefs must actively seek this information since search algorithms are designed to return results “relevant” to the user.

Another emerging theory on how to change beliefs is by hearing information from a person or entity thought of as trustworthy. The public may not see a scientist as “warm” or “trustworthy,” and many believe their results are influenced by the need to obtain research money and/or please the food industry (Fiske & Dupree, 2014; Pew Research Center, 2016), thus driving down the degree of trust. Consumers largely do not trust corporations or industries to regulate themselves or assess risk, and indeed, food companies have fought mandatory GMO food labeling, arguing that by doing so, the label is implicitly making a claim that GMO foods are not safe for people or the environment, known as the labels-as-signals hypothesis (Costanigro & Lusk, 2014). For example, in the United States, the non-GMO Project campaign is used to make this claim and the campaign’s label appears on a wide variety of products. Interestingly, data show that mandatory GMO labeling appears to have the opposite effect. The state of Vermont mandates labeling of food that has been produced using genetically engineered methods. In surveys taken 6 and 12 months after mandatory labeling of GE foods, compared to a national control group, a 19% reduction in opposition to GE foods was observed in Vermont (Kolodinsky & Lusk, 2018). Labeling foods that have been produced using genetic engineering may provide consumers a sense of full disclosure, providing a sense of control over their purchases and an in increase in trust of the system. Beginning in 2022, the United States will mandate labeling GE foods as a “bioengineered food” but will exclude labeling foods that have been produced using gene editing or other technologies that could be achieved through conventional breeding. Utilizing new technologies to produce food that have the potential to preserve biodiversity and the environment will depend on the success that scientists have in gaining public trust through transparency and balanced communication of data.

Agriculture, the Two-Edged Sword

Despite unceasing pressure from disease, drought, floods, insects, and weeds, agriculture has repeatedly innovated to feed an expanding global population. In 1993, the worldwide food supply was 2,616 kcal/capita/day. By 2013, 2,884 kcal/capita/day were produced, an increase of 10.2%, while the amount of agricultural land decreased by 0.2% during this time frame (FAOSTAT, 2019). As the world population continues to expand, food production will need to be increased further, with estimates ranging from 25% up to 110% (Alexandratos & Bruinsma, 2012; Hunter, Smith, Schipanski, Atwood, & Mortensen, 2017; Tilman, Balzer, Hill, & Befort, 2011). Assuming that yield is required to be doubled and yield trends continue as they have, it is questionable this goal can be met. If the current yield trends of four crops (maize, rice, wheat, and soybean) that provide ~60% of the world’s calories are maintained, it will not be sufficient to meet global caloric demands (Ray, Mueller, West, & Foley, 2013) and up to 100 million ha of additional land would need to be added to production (Pastor et al., 2019). Doing so, however, will come at a cost of losing biodiversity.

Feeding the world’s expanding population is not simply a matter of producing more calories. Undernourishment, obesity, food waste, and food distribution are additional factors to be addressed, with many or all of these food problems present at the same time within a country. In 2017, an estimated 821 million people worldwide are undernourished while at the same time one in eight adults (~672 million) are obese (FAO, IFAD, UNICEF, WFP, & WHO, 2018). In the developing world, plant breeders are developing new varieties that are staples in developing countries. To address micronutrient malnutrition breeders are exploiting natural variation and conventional breeding techniques to create biofortified crops that are enriched in iron, zinc, and provitamin A (Pfeiffer & McClafferty, 2007). Developing more nutritious crops through biotechnology has long been a goal, and an early success was the development of golden rice to address vitamin A deficiency in developing world countries (Beyer et al., 2002; Paine et al., 2005) (Beyer et al., 2002). Many agronomic crops including barley, cassava, corn, potato, sorghum, and wheat have been biofortified through biotechnology to increase the concentration of ascorbate, β‎-carotene, folate, α‎- and γ‎-tocopherol, iron, zinc, and copper (De Steur et al., 2015). Similarly, in horticultural or specialty crops, by 2008, 49 papers were published that established proof of concept for improving the vitamin or nutritional quality through genetic engineering (Miller & Bradford, 2010). As of 2019, no bioengineered specialty crops or golden rice have been commercially produced due to the regulatory process and a perceived lack of consumer acceptance (De Steur et al., 2015; Miller & Bradford, 2010)

The Environmental Impact of Agriculture

Crop yields are influenced by the genetics of the variety, amount and quality of water, the amount and quality of nutrition available, soil health, and the degree by which abiotic and biotic stresses reduce yield. Depending on the ability to optimize each of these factors, yields vary considerably across the globe. For example, the worldwide average rice production during the 2017–2018 growing season was 4.5 metric tons/ha, with a range of 2.1 to a 8.4 metric tons/ha, for Nigeria and the United States, respectively. Similarly, world maize production averaged 5.6 metric tons/ha, with a range of 1.2 to 11 metric tons/ha for Zimbabwe and the United States, respectively (FAOSTAT, 2019).

On a global scale, without crop protection, pests, including pathogens, viruses, animals, and weeds, reduce crop yields. In wheat, pests typically reduce yields by about 50% and rice yields by 77% (Oerke, 2006). With few exceptions, over the last 26 years, increasing amounts of pesticides and fertilizers have been applied to maintain or increase yields. Between 1990 and 2016 (the last date for available data), worldwide pesticide use increased by 78% from 2.285, to 4.1 million tons active ingredient applied (FAOSTAT, 2019). In general, developed countries and regions did not apply markedly more pesticides and, in some cases, applied less. For example, between 1990 and 2016, pesticide use in the United States and Europe increased by 1.7% and decreased by 11.5% respectively. Conversely, in developing countries where agricultural has been recently intensified, pesticide use increased by 759% and 794% in Brazil and Argentina, respectively (FAOSTAT, 2019). Five countries account for 91% of the biotech acreage planted globally, but overall there is no relationship at a national level between the amount of pesticides applied and whether the country grows biotech crops. Weeds will continue to be a major agricultural problem requiring significant inputs of labor, money, and herbicides to mitigate weeds. Worldwide, almost 3.5 billion pounds of herbicides are applied annually, at a cost to farmers/producers of about $25 billion annually (Atwood & Paisley-Jones, 2017). In the United States, herbicide use between 2002 and 2016 increased by 24%, while in Brazil and Argentina, herbicide use increased by 1,023% and 1,108%, respectively (FAOSTAT, 2019).

These data indicate that while agriculture is practiced worldwide, there is tremendous variation in how agriculture is practiced and how yields and pesticide use are affected by the biotic and abiotic environment. There are limitations in the worldwide data that prevent collection of what type of pesticides are being applied. Detailed reporting on active ingredients is needed at a country level. However, while the modes of action of pesticides are largely known, there are limitations in knowledge of the broader ecological consequences of a single active ingredient, let alone the synergistic effects of mixtures that are often a reality in agricultural production.

Conventional Agricultural Impacts Ecosystems and Biodiversity

Of the approximately 13 billion ha of arable land area on Earth, ~38.4% is used for agricultural purposes (FAOSTAT, 2019). Agriculture production can be broadly classified as conventional, using synthetic fertilizers and pesticides, or organic. Conventional agriculture can include biotech crops, but organic agriculture does not. Organic agriculture seeks to reduce the environmental impact of agriculture through the implementation and practice of ecological production systems to enhance biodiversity, biological cycles, and soil biological activity (USDA National Organic Standards Board). Conventional agriculture can also utilize the ecological principles embraced by organic agriculture to enhance sustainability. Regardless of how it is practiced, agriculture has negative impacts on biodiversity through two actions. The first, and most consequential, is the loss of natural habitat associated with agricultural conversion, and the second is the use of what can broadly be referred to as inputs, the water, fertilizers, and pesticides applied to produce crops and raise livestock.

Land Conversion = Loss of Habitat and Biodiversity

Before the Industrial Revolution (pre-1700) agriculture was widely practiced across Europe and Asia. By 1700, about half of the terrestrial biosphere was in a natural state, not being used for agriculture, pasturelands, or settlements (Ellis, Klein Goldewijk, Siebert, Lightman, & Ramankutty, 2010). As Europeans expanded to the New World, large transformations of natural lands to agriculture occurred between 1850 and 1950 in the United States, Australia, and South Africa. In the United States for example, the amount of agricultural land in production did not peak until 1954. During the 1980s and 1990s, the most rapid conversion to agricultural land was in tropical areas while at the same time developed countries either maintained or lost agricultural land (FAOSTAT, 2019; Gibbs et al., 2010; Song et al., 2018). Since 1700, over 70% of grasslands, 50% of the savanna, 45% of temperate forests, and 27% of tropical forests globally have been converted to agricultural lands (Foley et al., 2011; Gibbs et al., 2010; Ramankutty, Evan, Monfreda, & Foley, 2008; Ramankutty & Foley, 1999). In tropical areas, most of the new agricultural land added was from the conversion of forests to agricultural lands (Gibbs et al., 2010). Currently, about 70% of the remaining global forest cover is within 1 km of the forest’s edge, adding to further fragmentation and habitat loss and increasing the likelihood of conversion to agriculture (Haddad et al., 2015). In particular, the biodiversity losses and carbon sequestration associated with loss of tropical forests is disproportionately high compared to that of temperate forests, but it is the forests in extra-tropical forests that are expanding and only partly offset the loss in the tropics (Fargione et al., 2018; Song et al., 2018).

As the percentage of agricultural cover increases in an area, fewer species are present and the phylogenetic distance and shared evolutionary history between species is lower (Grab et al., 2019). These attributes of lower diversity and trait function lead to diminished ecosystem services (Grab et al., 2019). Although there are a few notable exceptions, the loss of natural habitat results in reduced numbers of individuals, populations, and, in some cases, entire species. Biotech crops are generally not planted into areas that have been recently converted into agricultural lands. From that perspective, biotech crops do not directly contribute to loss of natural lands or the loss of biodiversity associated with loss of habitat.

It is estimated that Earth has between 8.7 million and 20 million kinds of plants, animals, and fungi, but only 1.733 million have been described. The IUCN assesses taxa using defined criteria that includes current and projected population trends, population size, and geographic range. The 2016 IUCN Red List (Version 2016-1) evaluation of 82,454 species (~5.68% of the total described taxa) listed 8,688 species (10.5% of the evaluated taxa) as either “critically endangered,” “endangered,” “vulnerable,” or “near-threatened.” For each of the 8,688 listed species, six drivers of biodiversity decline were identified, including “over-exploitation,” “agricultural activity,” “urban development,” “invasion and disease,” “pollution,” “system modification,” and “climate change” (Maxwell et al., 2016). Maxwell and colleagues retained the “near-threatened” category but collectively referred to species listed as critically endangered, endangered, and those vulnerable as “threatened.” More than 80% of the threatened or near-threatened species were vulnerable to more than one of the six external threats. Climate change is likely to be an increasingly serious threat to biodiversity, but during the 2016 IUCN assessment, it is responsible for the declining numbers of only 19.4% (1,688 of 8,688) of the threatened or near-threatened species (Maxwell et al., 2016). Currently, the largest threat to biodiversity is over-exploitation (e.g., logging, hunting, fishing, gathering plants), which threatens the survival 6,241 of the 8,688 species (71.8%). The second-largest threat to biodiversity is agricultural activity, affecting 5,407 (62.2%) of the evaluated species. Agricultural activity is defined as crop or livestock farming, timber plantations, and aquaculture. Of the agricultural activities, crop farming was identified as a threat to 4,692 species, while livestock farming was responsible for harming 2,267 species (Maxwell et al., 2016). The most recent IUCN Red List (Version 2019-1) assessed 98,512 taxa, of which 27,159 (27.6%) are listed as threatened (IUCN, 2019). Of those for which sufficient data allowed estimates, 25% of the mammals, 14% of birds, 40% of the amphibians, and 40% of the gymnosperms are threatened with extinction (IUCN, 2019, Table 1a,).

A separate evaluation of 27,600 IUCN-listed vertebrate species found that 32% are decreasing in population size and range (Ceballos, Ehrlich, & Dirzo, 2017). Population decline is a harbinger of extirpation (locally extinct) and/or extinction and, not surprisingly, is especially prominent in tropical areas, which are typically species-rich. Between 1970 and 2014, population sizes of vertebrate species globally have declined by 60%, while in Central and South America the declines are estimated to be 89% (WWF, 2018). However, as a percentage of total species richness, population extinctions of vertebrates are highest in temperate regions, which typically exhibit low species diversity (Ceballos et al., 2017). The extirpation of local populations, entire species of animals, plants, and microorganisms, means that ecosystem functions are being lost, and this will have ecological and economic consequences for human interests and commerce. For the individual animals in populations that survive, genetic diversity is also lost, making those populations less equipped to evolve and survive in changing environments.

The loss of biodiversity extends to insects as well. In nature protection areas across Germany, a 76% decline in flying insect biomass was observed over a 27-year period between 1989 and 2016 (Hallmann et al., 2017). While no single cause of insect declines was identified, the nature protection areas were imbedded in human-dominated landscapes across a variety of habitats. In this study, higher insect biomass was observed in nutrient-rich habitats compared to habitats classified as nutrient-poor, but declines were proportionate across all habitats (Hallmann et al., 2017). Total flying insect biomass can be considered a broad indicator of ecosystem health and function. A loss of such magnitude suggests wholesale collapse in ecosystem functions and adds to the widespread reports of reduced populations in moths, butterflies, and bees that have been widely reported. Because Germany does not allow production of biotech crops, the wholesale loss of insects cannot be attributed to GMO production (Hallmann et al., 2017).

Bees are important pollinators for horticultural crops, and colony collapse has been observed globally (Goulson, Nicholls, Botías, & Rotheray, 2015). Multiple factors are thought to contribute to colony collapse (Goulson et al., 2015), and while single insecticides have been theorized to be responsible, bees are highly mobile and may be exposed to multiple pesticides to and from the hive. A single pesticide alone may exhibit low toxicity to honeybees, but tank-mixes may contain multiple fungicides or a combination of fungicides and insecticides, and these combinations may exhibit synergistic acute toxicity in honeybees (Wade, Lin, Kurkul, Regan, & Johnson, 2019). The results may be specific to a crop, the time of year, and the environmental regulations in region where the crop is located. For example, in almond crops grown in California, the toxic effect of the combination of insecticides and fungicides (especially sterol biosynthesis-inhibiting fungicides) are greater than that predicted by the individual components (Wade et al., 2019). Thus, the pesticides registered for each crop and each region indicate the complexity of protecting pollinators in conventionally grown crops. Insects are integral components of an ecosystem providing many services including pollination, herbivory, ordetritivory and as a food source for higher trophic animals, especially birds and bats. Preservation of insect biodiversity is a key component of preserving ecosystem services, in addition to the pollination services provided for agriculture.

Ecosystem declines include loss of biodiversity, environmental degradation, and increased conflict over resources among the dominant species. At some critical point, a state change may occur, resulting in a loss of the dominant species, development of alternative biological communities, or a collapse of the entire ecosystem (Vignieri & Fahrenkamp-Uppenbrink, 2017). As agricultural lands replace natural ecosystems, large increases in net primary productivity relative to a natural ecosystem (i.e., current prevailing vegetation) are observed in the crop land (Haberl et al., 2007). Conversion of natural land can also redirect ecological energy flows from relatively dispersed ecosystem food webs to more localized and concentrated areas (Haberl et al., 2007). These diversions in energy flows from established ecosystems are hallmarks of a loss in ecosystem function, and when diverted to agriculture it may lead to increased soil degradation, interruption and changing of biogeochemical cycles, and increased pesticide use if agricultural inputs cannot be held steady or reduced (Harberl et al., 2007). Short of preserving land and ecosystems, reducing or limiting inputs can be accomplished by using biotech crops that lower insecticide applications and reduce fertilizer applications and using no- or low-till methods.

Intact ecosystems provide ecosystem services, which can be simply defined as contributions of nature to human welfare (Boyd & Banzhaf, 2007; Costanza et al., 1997), and include, but are not limited to, carbon sequestration and storage, natural grasslands for livestock production, water for crop irrigation, livestock, industry and domestic water, flood protection, and recreational and aesthetic value (Farber, Costanza, & Wilson, 2002; Naidoo et al., 2008). A resilient ecosystem is able to resist an environmental perturbation and not switch to another state and, if disturbed, can recover relatively quickly from a disturbance (Hodgson, McDonald, & Hosken, 2015). Resilience and recovery from disturbance are complex, affected by both abiotic and biotic factors. At the community level, species richness appears to confer greater resilience to perturbation and less tendency to change state, perhaps because a there are more species to carry out ecosystem functions that were carried out by the species lost (Hisano, Searle, & Chen, 2018). At a continental level, however, species richness does not parallel resilience and appears to be more susceptible to climate variability (Hisano et al., 2018). While agricultural lands contribute to human welfare through contributing of food and fiber, comparatively they are biodiversity deserts that provide few ecosystem services. The open question is: Can agriculture be practiced on a scale that provides sufficient food while incorporating practices that provide ecosystem services across large geographic farming regions?

Organic Production and Biotech Crops as Tools to Promote Biodiversity

In general, meta-analyses indicate that organic agriculture is associated with greater species biodiversity, especially in intensively farmed regions (Bengtsson, Ahnström, & Weibull, 2005; Tuck et al., 2014). The results, however, depend on the crop, and consistent effects on taxa are not observed, with greater biodiversity observed in intensively farmed regions (Tuck et al., 2014). Crop rotations can be used to manage soil water and nutrition, weeds, diseases, and insects but are also used simply to respond to markets. Crop rotations are valuable because they can also add biodiversity. Because synthetic fertilizers and pesticides cannot be used in organic production, crop rotation is often a strategy used to partially replace some of the functions of fertilizers and pesticides. Worldwide, in 2017 almost 70 million ha were managed organically, representing ~1.4% of the total land in agriculture (BiBL, 2019; FAOSTAT, 2019). Thus, although organic production methods are favorable to long-term sustainability of agriculture and generally increase biodiversity, their overall impact is limited by the scale of practice. While the organic community uses hybrids with improved resistance to diseases or greater tolerance to abiotic stresses, they have taken a position not to use bioengineered plant varieties. By precluding the use of technologies that help promote biodiversity and land stewardship, the overall impact of organic agriculture is further limited.

Integrating Agriculture, Technology, and Ecology to Preserve Biodiversity and Ecosystems

With the world population predicted to increase to 9.1 billion by 2050, food production must be increased to ensure food security. Can agriculture be sustainably intensified (Hunter et al., 2017) in a manner that leads to increased food production without further environmental degradation and an increased loss of biodiversity? Despite a long history of practicing agriculture, only recently have agronomists and ecologists recognized the broader potential of an agroecosystem to benefit society beyond an immediate need to produce crops and livestock (Power, 2010).

Can Future Biotech Crops That Increase Productivity Be Ignored?

Two long-sought-after goals of plant genetic engineering—increasing photosynthetic efficiency and biological nitrogen fixation—if realized, will be transformative. Crop yields depend on adequate light, nitrogen, and water and limiting the effects of biotic stresses (weeds, insects, and diseases). Not surprisingly, increasing photosynthetic efficiency is not straightforward. Photosynthetic efficiency is affected by canopy light interception, canopy leaf nitrogen, and crop water status and the various feedback mechanisms that serve to limit water loss (Wu, Hammer, Doherty, von Caemmerer, & Farquhar, 2019). Thus increasing efficiency by addressing crop and physiological dynamics is daunting. However, because photorespiration lowers photosynthetic efficiency in C3 plants by 20–50%, it may be more tractable through metabolic pathways. Photorespiration is the process by which RuBisCO oxygenates instead of carboxylates RuBP, leaving byproducts that require energy to detoxify. A synthetic biology approach was used to re-engineer photorespiratory pathways that resulted in a 25% increase in biomass in experimental plants; with the addition of RNAi to suppress the native photorespiratory pathway, the biomass of the experimental plants increased by 40% (South, Cavanagh, Liu, & Ort, 2019). Nitrogen deficiencies limit photosynthesis and therefore biomass and yield. Synthetic fertilizers are often used to ensure adequate N, and worldwide, 110.2 metric tons of nitrogen fertilizers were used in 2016, a 33% increase from 2002 (FAOSTAT, 2019). The carbon impact of using nitrogen fertilizers is appreciable, estimated at 1–2% of total global energy. In addition to the energy required to synthesize nitrogen fertilizers, once applied to fields, nitrous oxides are released to the atmosphere. On a per molecule basis, N2O is a potent greenhouse gas having 300 times the heating capacity of CO2 (Stein & Yung, 2003), and agriculture, by far, is the largest anthropogenic source of nitrous oxides released to the atmosphere (Park et al., 2012). Cereal crops, planted on 731.4 M ha worldwide, are the largest users of nitrogen fertilizers, and it has long been a goal to engineer biological nitrogen fixation in these crops (Hardy & Havelka, 1975; Shanmugam & Valentine, 1975). Transferring prokaryotic nitrogen fixation (nif) genes into chloroplasts, mitochondria, or root plastids of cereals and other crops would allow non-legume plants to fix atmospheric nitrogen and reduce the use of synthetic fertilizers. The strict requirement to maintain a balanced expression of the encoded proteins in the transferred nif pathway has made this largely an intractable problem. Using synthetic biology, nitrogen fixing (nif) genes were grouped together based on similar expression levels, and the various assemblies were tested to identify the optimum combination of stoichiometrically balanced polyproteins, tailing tolerance, and nitrogenase activity (Yang et al., 2018). The optimum combination of 14 essential nif genes were assembled into five “giant genes” that enabled growth on dinitrogen. This synthetic biology engineering approach mimics a naturally occurring post-translational modification observed in RNA viruses in which a polyprotein is cleaved by a viral protease to form functional components of consistent stoichiometry.

Both photosynthetic efficiency and biological nitrogen fixation have been demonstrated to be technically feasible, and the next step will be to transfer these systems to crop plants and conduct field evaluations. These systems represent a much greater degree of engineering than any biotech crop released to date. They also promise to do much more to lessen the impact of agriculture than any biotech crop released to date; their reception by the general public, organic agriculture, and groups generally opposed to GMO technology will be interesting.

When possible, natural variation can and should be exploited to improve the performance of crops. Most crops grown today can be crossed to their wild progenitors, and useful alleles can be transferred to crops to confer resistance to disease and abiotic stresses (Argyris, Dahal, Hayashi, Still, & Bradford, 2008; Tanksley & McCouch, 1997). Biological nitrogen fixation was demonstrated in an indigenous land race of maize, which fixed nitrogen at rates between 29% and 82%, apparently through the mucilage associated with the aerial roots of the landrace (Van Deynze et al., 2018). The genes responsible for biological nitrogen fixation in the primitive landrace are yet to be identified, and extensive crossing would need occur since the landrace is not adapted to modern agronomic practices. While using wild germplasm is useful, after crossing an elite domesticated variety to its wild progenitor, the resulting progeny resemble weeds, and the breeder must perform several crosses back to the domesticated elite cultivar to eliminate most of the genome from the wild species. Crossing, however, is unpredictable, and the resulting progeny contain many unwanted genes and traits, a process called genetic linkage or linkage drag. Genome editing techniques, like CRISPR (clustered regularly interspaced short palindromic repeats), eliminate linkage drag and replace the need for successive crosses by efficiently altering the precise allele in the target gene, thus eliminating several generations of backcrossing (Zhang, Malzahn, Sretenovic, & Qi, 2019). Since CRISPR technology accomplishes what can be done through traditional breeding, the United States will not regulate CRISPR technology as a GMO (USDA, 2018). On the other hand, the European Union will treat crop varieties developed using CRISPR technology as a GMO, thus subjecting them to a long and expensive regulatory process to bring a crop to market (Callaway, 2018).

The Need to Monetize Ecosystem Services and Biodiversity in Agriculture

To a farmer or rancher, biodiversity and ecosystem benefits of agriculture may be an abstract concept if the more fundamental and pressing needs are economic and/or food security. Unless biodiversity and ecosystem services can be monetized or shown to improve yield or product quality, managing a farm to provide ecosystem services is not likely to be adopted to regionally impactful levels. Ecosystem services are not included in estimates of gross domestic product (GDP), but this idea has been proposed (Boyd & Banzhaf, 2007) and its value estimated at U.S. $16–54 trillion annually (Costanza et al., 1997). The signatories to the Convention of Biological Diversity adopted a strategic plan in 2020 that includes implementation of the EU nature legislation to better protect ecosystems and the services they provide, and all EU members are committed to delineate ecosystems and quantify their conditions and the services they supply (Maes et al., 2016). Virtually all nations are focused on their GDP. Growth of a nation’s GDP depends, in part, on investments of capital, innovation, and new technologies. Another contributor to the GDP is agricultural production, including goods and services. Agricultural innovation will be required to sustainably produce more food on a finite amount of arable land, but this comes at a time when public investment in agricultural research has been diminishing. For example, between 1948 and 2015, U.S. farm output grew by 170%, or an average of 1.38% per year. Over the last 40 years, the total factor productivity (TFP = aggregate output—aggregate input) in the United States steadily decreased so that between 2007 and 2015, the TFP of 0.53 was about one-quarter of its peak performance, observed during 1981 and 1990 (TFP = 2.11). When the amount of agricultural land remains constant or decreases, increased productivity will be dependent on advances in science and technology. Investments in public and private agricultural research, needed to drive innovation and new knowledge, has been stagnant in the United States since the 1980s and, in inflation-adjusted terms, has decreased since 2009 (Wang, Nehring, & Mosheim, 2018). Innovation is not necessarily restricted to technology. Agriculture has largely been practiced the same way throughout its entire history, as an insular endeavor, with fields isolated from the surrounding natural environment and fields containing a very narrow slice of biodiversity. To prevent further degradation of the environment and loss of biodiversity, this will have to change.

Organic production methods are favorable to long-term sustainability of agriculture and generally increase biodiversity, but their overall impact is limited by scale and failure to use technologies that limit pesticides and are consistent with their stated goals of sustainability. While applying synthetic pesticides and fertilizers is prohibited, the organic production philosophy of not allowing GE crops (e.g., insect-resistant GE crops) appears misguided based on the scientific evidence available. Similarly, future biotech crops are likely to improve the long-term sustainability of agriculture and generally increase biodiversity, but the overall impact will be limited by the scale of practice and the general lack of adopting agroecological practices, many of which are included in organic production. While organic agricultural production is effective in utilizing ecological principals to minimize environmental impacts of growing crops, it has not been particularly transformative or innovative, and given these trends, its contribution to solving the agriculture/biodiversity problem will be limited.

If biodiversity and ecosystem functions are to be incorporated into agricultural practices, they must be monetized. One approach is to develop a sustainability index by which farms, ranches, and food production regions would be rated and certified. A food labeled with the sustainability seal and rating would demand a premium price, proportionate to its rating. Consumers of organic foods are willing to pay a premium because they value health and nutrition and believe organic foods are better, have better taste than conventionally grown food, and are better for the environment (Hughner, McDonagh, Prothero, Shultz II, & Stanton, 2007). Thus, consumers who value sustainable agriculture as measured by biodiversity indices would likely be willing to pay a premium for those products. The sustainability index would be based on measures of biodiversity and ecosystem function incorporated during the production of that food product. The farm or ranch would receive a rating in which its biodiversity and contribution to ecosystem services are compared to a nearby and ecologically relevant functioning ecosystem. Whether the food is produced through “conventional” or organic methods or if it is a biotech crop (GMO, gene edited, etc.) would not be relevant. Ecologists are well equipped to measure biodiversity and ecosystem functioning and would work with agronomists to improve ratings by incorporating ecological practices into their farming and ranching operations.

Producing food in a sustainable method by conserving and promoting biodiversity and ecosystem services would require a “certified sustainable” program with labels denoting different levels of achievement toward this goal. This is a dramatic departure from how agriculture is practiced today. Food production is first a business; food producers are largely focused on a harvest that maximizes yield and product quality and must make a profit. A certified sustainable program, however, would require a producer to think beyond the borders of their farm or ranch. Instead, they become a collective of food producers, each contributing to a regional agroecosystem. Producing food for the sustainable market will require the land (or water) used during the production of the food to be a component of the regional agroecosystem. It would require conservation of habitat to promote native biodiversity and provide for habitat for corridors that would promote gene flow and access to additional habitat. For terrestrial food systems, the individual farm or ranch would receive a sustainability score that integrates the biodiversity of their unit’s contribution to the greater ecosystem function of their agroecosystem, reflecting a regional approach to food production.

This approach would require a degree of regional planning similar to that in place for municipalities and metro regions globally. But it would also require agronomists, ecologists, economists, and regional planners to work together to develop the rating index and to assign value to the individual farms and farming region. The individual farm will get a rating while agroecosystem regions will be defined and receive a sustainability rating as well. Thus the value-added component to the food produced will be an index that incorporates the level of biodiversity and ecosystem services of an individual farm and then region. Under this scenario, premium prices are paid for individual units (farms/ranches) that are highly rated, and an additional premium is derived when enough producers have collectively contributed to a highly functioning agroecosystem.

Conclusion

The loss of biodiversity is a worldwide problem and a direct result of human activities. The contribution of genetically engineered crops to the loss of biodiversity and the degradation of ecosystem services is no greater and often less than that of conventional agriculture. Given the catastrophic losses in biodiversity we are currently witnessing, the perceived threats of GMOs to the environment and human health are misplaced. Instead, governments and the public should recognize the threat that all agriculture faces on the planet and work toward solutions that allow increased yields to sustain the Earth’s population, but preserve the lands that provide habitat for plants and animals and provide ecosystem services. Organic agriculture, because it fails to embrace genetic technologies that minimize environmental degradation and the relatively small percentage of the total agricultural landscape, will not attain its potential impact. At the same time, the traits present in current biotech crops, the degree to which growers do not embrace agroecological practices, and the limited global scale these crops are produced on will also not solve biodiversity problems given this configuration. Future technologies, such as systems approaches, gene editing, and others that will follow, promise to have much greater impacts. Increased photosynthetic efficiencies in crops, biological nitrogen fixation in non-legume species, for example, should help minimize or eliminate habitat loss due to crop production. In our present economic model, growth in GDP consistently results in reductions in biodiversity and ecosystem services (Marques et al., 2019). Because agricultural production is the second largest driver of biodiversity loss, agriculture will be required to be part of the solution to preserve biodiversity and ecosystem services. Monetizing biodiversity and ecosystem services by including these in commodity prices is likely the only method by which agriculture can be incentivized to be part of the biodiversity solution.

Further Reading

Agrawal, A. A., & Inamine, H. (2018). Mechanisms behind the monarch’s decline. Science, 360(6395), 1294–1296.Find this resource:

    Alexandratos, N., & Bruinsma, J. (2012). World agriculture toward 2030/2050. The 2012 revision. ESA Working Paper No. 12–03. Food and Agriculture Organization of the United Nations.Find this resource:

      Bengtsson, J., Ahnström, J., & Weibull, A. C. (2005). The effects of organic agriculture on biodiversity and abundance: A meta-analysis. Journal of Applied Ecology, 42(2), 261–269.Find this resource:

        Diamond, J. (2002). Evolution, consequences and future of plant and animal domestication. Nature, 418(6898), 700–707.Find this resource:

          Fiske, S. T., & Dupree, C. (2014). Gaining trust as well as respect in communicating to motivated audiences about science topics. Proceedings of the National Academy of Sciences of the United States of America, 111 (Suppl. 4), 13593–13597.Find this resource:

            Foley, J. A., Ramankutty, N., Brauman, K. A., Cassidy, E. S., Gerber, J. S., Johnston, M., . . . Zaks, D. P. M. (2011). Solutions for a cultivated planet. Nature, 478, 337.Find this resource:

              National Academies of Sciences, Engineering, and Medicine. (2016). Genetically engineered crops: Experiences and prospects.Find this resource:

                Pew Research Center. (2015). Public and scientists’ views on science and society. Washington, D.C.: Pew Research Center.Find this resource:

                  Sharot, T. (2017). The influential mind: What the brain reveals about our power to change others. New York: Henry Holt.Find this resource:

                    South, P. F., Cavanagh, A. P., Liu, H. W., & Ort, D. R. (2019). Synthetic glycolate metabolism pathways stimulate crop growth and productivity in the field. Science, 363(6422), eaat9077.Find this resource:

                      Tabashnik, B. E., & Carrière, Y. (2017). Surge in insect resistance to transgenic crops and prospects for sustainability. Nature Biotechnology, 35, 926.Find this resource:

                        Tilman, D., Balzer, C., Hill, J., & Befort, B. L. (2011). Global food demand and the sustainable intensification of agriculture. Proceedings of the National Academy of Sciences, 108(50), 20260–20264.Find this resource:

                          Tuck, S. L., Winqvist, C., Mota, F., Ahnström, J., Turnbull, L. A., & Bengtsson, J. (2014). Land-use intensity and the effects of organic farming on biodiversity: A hierarchical meta-analysis. Journal of Applied Ecology, 51(3), 746–755.Find this resource:

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