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The regulation of genetically modified (GM) crops is a topical issue in agriculture and environment over the past 2 decades. The objective of this paper is to recount regulatory and adoption practices in some developing countries that have successfully adopted GM crops so that aspiring countries may draw useful lessons and best practices for their biosafatey regulatory regimes. The first 11 mega-GM crops growing countries each with an area of more than one million hectares in 2014 were examined. Only five out of the 11 countries had smooth and orderly adoption of these crops as per the regulatory requirement of each country. In the remaining 6 countries (all developing countries), GM crops were either introduced across borders without official authorization, released prior to regulatory approval or unapproved seeds were sold along with the approved ones in violation to the existing regulations. Rapid expansion of transgenic crops over the past 2 decades in the developing world was a result of an intense desire by farmers to adopt these crops irrespective of regulatory roadblocks. Lack of workable biosafety regulatory system and political will to support GM crops encouraged unauthorized access to GM crop varieties. In certain cases, unregulated access in turn appeared to result in the adoption of substandard or spurious technology which undermined performance and productivity. An optimal interaction among the national agricultural innovation systems, biosafety regulatory bodies, biotech companies and high level policy makers is vital in making a workable regulated progress in the adoption of GM crops. Factoring forgone opportunities to farmers to benefit from GM crops arising from overregulation into biosafety risk analysis and decision making is suggested. Building functional biosafety regulatory systems that balances the needs of farmers to access and utilize the GM technology with the regulatory imperatives to ensure adequate safety to the environment and human health is recommended.
Groundbreaking discoveries, inventions and innovations in molecular biology and biotechnology since the second half of the 20th century have brought new tools and techniques for the introduction or modification of traits of agronomic interest in crop varieties beyond what is possible in nature (Barton and Brill, 1983; Sun, 1986; Gasser and Fraley, 1989; Cressey, 2013; Voytas, 2013, 2015; Zhang et al., 2015). Crops developed through the new methods of modern biotechnology are called genetically modified (GM) or genetically engineered crops. The field of plant genetic engineering is evolving from gene discovery and introgression in the 1980s (Barton and Brill, 1983; Sun, 1986; Gasser and Fraley, 1989) to genome editing (Cressey, 2013; Voytas, 2013; Kanchiswamy et al., 2015; Zhang et al., 2015) and synthetic biology (Wusheng and Stewart, 2015) to date giving exciting opportunities for plant breeding and crop improvement programs but also more challenges related to regulation of crop varieties and hybrids developed through novel genetic approaches.
GM crops are the fastest adopted crop technology in history (James, 2012; Khush, 2012), growing from an area of 1.7 million hectares in 1996 to 181 million hectares in 2014 (James, 2014). The first generation of GM crops widely cultivated to date bear mainly input traits for insect and disease resistance and herbicide tolerance (James, 2014). Strong intellectual property (IP) protection made possible by patents on crop varieties bearing these traits offered attractive profits to biotechnology and seed companies while conferring the needed operational, yield and cost advantages to adopting farmers (Kathage and Qaim, 2012; Lusser et al., 2012). Patents protecting these GE traits have started expiring opening further opportunities for wider adoption of the technology uninhibited by intellectual property regimes, provided that appropriate and functional biosafety regulatory regimes are put in place (Hawker, 2013; Schonenberg, 2014). The objective of this paper is to present a brief adoption history and regulatory challenges that developing countries have experienced in the past 2 decades such that aspiring countries might find helpful guidance to make informed decision on their GM crops biosafety regulatory approach.
The advent of genetic engineering was marked by a parallel evolution of the regulation of the processes and products of genetic engineering spanning from the laboratory to the marketplace and end-use. Among the important landmarks in the regulation of genetic engineering are a reminder by scientists for biosafety guidelines in 1973 (Singer and Soil, 1973), a call for voluntary moratorium on certain aspects of recombinant DNA (rDNA) in 1974 (Berg et al., 1974), the Asilomar Conference on rDNA molecules in 1975 (Berg et al., 1975), the United Nations Convention on Biological Diversity (UN, 1992), the Cartagena Protocol on Biosafety to the Convention on Biological Diversity (CBD, 2000), and the Nagoya - Kuala Lumpur Supplementary Protocol on Liability and Redress to the Cartagena Protocol on Biosafety (CBD, 2011).
The Cartagena Protocol on Biosafety was adopted on 29 January 2000 and entered into force on 11 September 2003. The Protocol is based on the precautionary approach contained in Principle 15 of the Rio Declaration on Environment and Development. The Protocol is believed to have guided the development of biosafety laws, regulations and guidelines in many developing countries that are party to the Protocol. The Protocol is significant for the agricultural sector as it recognizes both the benefits and the potential risks arising from rDNA technology and hence it stresses the need to do a scientifically sound risk assessment to avoid any adverse effects on the environment and health.
However, different countries have interpreted and implemented the Precautionary approach differently. Some countries have taken precaution as decision making based on scientific risk assessment and have, therefore, put in place regulatory measures proportional to the perceived risks; opening doors for testing and commercialization of rDNA-based agricultural technologies. However, many developing countries have issued prohibitive and unworkable legislations, denying farmers access to a powerful technology to tackle production constraints and increase incomes while keeping to the minimum potential risks to human health and the environment.
Despite this, at present, there are 28 countries growing transgenic crops globally (James, 2014). Genetically modified crops have been a dominant feature of the agricultural landscape in the Americas while some countries in Asia such as India, China, Pakistan, Bangladesh and the Philippines have been selective of the GM crop they are cultivating, at the crop and traits level. In Africa, South Africa and Burkina Faso have gone far in GM crop based agriculture. Sudan has introduced Bt-cotton since 2012 while GM maize cultivation in Egypt appears to have stalled (James, 2014). This aside, there are a number of other African countries that have displayed interest in adopting these crops and are working on locally relevant food security crops such as cassava, maize, banana, cowpea, sweet potato, sorghum, rice, etc. Some countries in Africa are already conducting confined field trials (CFTs) with general release in a few countries in the horizon.
In 2014, 11 out of the 28 GM-growing countries had more than 1 million hectare of GM crops (James, 2014). These GM crop mega-countries have treaded different paths in terms of frameworks for regulation of these crops. Some countries have built new legislative frameworks, others have modified existing ones, while still others such as the USA have operated within prior existing regulatory frameworks.
Regulation and diffusion of genetically modified crops operate under a macrocosm of actors that include national regulatory body, multinational and national biotech corporations and a number of other diverse actors put together under a broad frame of the National Agricultural Innovation System (NAIS) (Fig. 1). The NAIS essentially consisted of farmers, seed producers and traders, and public and private agricultural research system that were instrumental in the regulated or unregulated introduction of GM crops in the respective developing country territories as will be recounted later. Ideally, in a system where the biosafety regulatory system is functional, the interaction among biosafety regulators, technology suppliers and local innovators is optimal and decisions are predictable. The ultimate result is often timely and regulated access to technology ensured by efficient and flexible regulatory approaches and implementation capacity, which result in sustainable, predictable and workable biosafety regulatory system. However, in reality, the process of GM crops adoption has proved to be inconsistent. In some countries, technology adoption preceded regulatory regimes. In some others, although a potentially workable regulatory system was put in place, the system would be held hostage because of submission to the demands of anti-GMO groups. Still in some others, decision is too protracted or the regulatory requirement is too cumbersome to work through.
All these above scenarios either deny access to technology by farmers or invite the temptation to access the technology without the necessary regulatory oversight. In such instances, technology introduction across borders was effected by actors in the NAIS without due consideration for biosafety requirements. These actors mostly were farmers through their cross-border networks. In addition, in some countries both private seed companies and public research centers were involved in breeding trait bearing genes into locally adapted varieties leading to the unauthorized cultivation from several thousand to millions of hectares of GM crop varieties. For instance, of the top 11 mega-biotech countries, more than 50% (Table 1) had a history of unregulated and unapproved access to GM crop varieties especially at the early stages of technology introduction as briefly detailed in the following section.
In China, the first biosafety regulation was issued by the Ministry of Science and Technology (MoST) in 1993 (Huang and Yang, 2011; Lagos and Jie, 2012). Thereafter, the Ministry of Agriculture (MoA) issued implementation measures in 1996 under the MoST's regulation of 1993. In 2001, the Chinese State Council issued a decree to regulate agricultural GMO replacing the 1996 regulation of the MoA. Subsequently, the MoA issued several regulations in 2002 in order to implement the 2001 decree by the State Council (Huang and Yang, 2011; Lagos and Jie, 2012).
In China, the MoA is the primary body governing GM crops (Lagos and Bugang, 2011). The Ministry for Environmental Protection is the national focal point for the negotiation and implementation of the Biosafety Protocol (Lagos and Bugang, 2011; Lagos and Jie, 2012). The MoA approves GM crops after assessment by the National Biosafety Committee for import and domestic production. Importing GM crops into China requires a certification that the GM product is fully tested and approved in the exporting country (Lagos and Bugang, 2011). In China, although familiar technologies like Bt cotton are deregulated at the technical level within the MoA, decision involving sensitive crops such as GM rice is left to the highest policy makers (Huang et al., 2005). China established its national GMO Biosafety Committee in 1997, the same year that the first commercial use of Bt cotton was approved. In this first year of Bt cotton release, 4 varieties developed by the public institutions were released along with one Bt cotton variety from Monsanto Company. Following this, a sharp rise in demand for the Bt cotton seed resulted in the proliferation of unapproved Bt cotton varieties, which were disseminated through the conventional seed system without the necessary regulatory oversight. In fact, the number of unauthorized Bt-cotton varieties exceeded the number of authorized Bt-cotton varieties after only several years of commercialization. As a result, nearly all of newly approved varieties were the varieties that were already being planted in farmers' fields, indicating that the regulatory system lagged behind the innovation system (Huang et al., 2005).
In China, unauthorized Bt-cotton market promoted the diffusion of good as well as bad Bt-cotton varieties. However, Bt cotton varieties approved by the biosafety committee performed better than unapproved ones, decreasing pesticide use and increasing seed cotton yields. Hence, in China farmers benefited much more from authorized Bt-cotton varieties that have gone through the regulatory system (Huang et al., 2005).
The Government of Pakistan constituted its National Biosafety Expert Committee (NBEC) in 1998 to develop a regulatory framework for the biosafety evaluation and release of GM crops (Nazli et al., 2012). However, it was only in 2005 that the Pakistan Biosafety Rules and the National Biosafety Guidelines were approved. In the interim period and afterwards until 2010, Bt cotton continued to spread from field to field without regulatory authorization (Nazli et al., 2012).
In Pakistan, exotic Bt cotton first reached farmers' fields in 2002 through the informal sector (Nazli et al., 2012). These varieties were not well adapted to the Pakistani growing conditions. Later on, both the public research institutions and seed companies bred the Bt gene into local varieties and successfully marketed without a formal regulatory approval. In 2012, Pakistan grew 2.8 million ha of Bt-cotton (James, 2012). Pakistan officially approved the adoption of Bt cotton only in 2010. However, such a delay in approval appeared to have encouraged an unauthorized adoption of Bt cotton in the country. In addition to biosafety concerns, lack of regulatory oversight means that the seed quality was compromised and support for farmers on ways of managing the technology and product stewardship was at best inadequate (Nazli et al., 2012).
In India, the Genetic Engineering Appraisal Committee (GEAC) is tasked with the assessment and technical recommendation of agricultural GMOs for environmental release (Jayaraman, 2004, 2010). The committee is accountable to the Ministry of Environment, Forestry and Climate Change (MoEFCC). The responsibility for final approval of GM crops for environmental release rests with the minister of the MoEFCC. By 2012, India grew 10.8 million ha of Bt-cotton. India provides a prime example of the benefits of Bt-cotton to smallholder farmers. A recent economic analysis of Bt cotton data collected between 2002 and 2008 indicated a 24% increase in cotton yield and a 50% gain in cotton profit for Bt-cotton adopting smallholder farmers. (Kathage and Qaim, 2012). Despite such a success, the introduction of Bt-cotton in India was not without challenges.
India did a large scale field evaluation of Bt-cotton varieties from 1998–2001. A local seed company in partnership with Monsanto applied for release of Bt cotton varieties in 2001, but was requested to do more field trials for another year. However, in the same year it was found out that the Bt gene had gotten out into the hands of a local seed company without the needed license and regulatory authorization. The local company, because of a weak regulatory system, was able to distribute Bt-gene bearing cotton varieties for the planting of ~11,000 ha of unauthorized Bt cotton worth ~$30 million (Jayaraman, 2001). Fortunately, the incident proved that the Bt technology was effective in resulting in higher yields and reduced pesticides use. Following this, in 2002, the Indian government approved and allowed farmers to cultivate Bt cotton. However, even after this, emergence of many spurious varieties labeled as Bt cotton was common. In fact, by 2004, it was argued that more than half of the area under Bt cotton was planted to unapproved seeds (Jayaraman, 2004). Even today, there is a concern that withholding the approval of Bt eggplant would promote clandestine growing of the crop in the country (Jayaraman, 2010).
By 2012, Brazil grew about 36.6 million ha of genetically modified crops most of which was herbicide tolerant soybean (James, 2012). Brazil established the National Technical Biosafety Commission (CTNBio) in 1996. Although the CTNBio authorized transgenic soybean release in 1998, commercialization was delayed because of lawsuits that followed this authorization (Jepson, 2002; Cardoso et al., 2005). However, farmers had long planted herbicide tolerant soybean seeds commercialized by Monsanto Company brought in from Argentina without authorization. Brazil was caught between 2 strong forces of influence that made arriving at decisions hugely difficult. On one side were the anti-GMO activists and politicians who saw biotechnology as an unwelcome imposition on Brazil by multinational companies. On the other side was the powerful agri-business lobby, which took biotech as a competitive tool (The Economist, 2003).
At the beginning, Brazilian authorities banned commercial planting of GM crops, but allowed GM experiments and GM material in labeled consumer products (Jepson, 2002). However, after facts were created on the ground, Brazil officially approved the planting of herbicide tolerant soybean initially for a one year period in 2003 under the threat of “civil disobedience.” GM crops have been grown in the country legally ever since. Brazil enacted its biosafety law in 2005.
The government of Bolivia is said to have a strong anti-GMO stand (Smale et al., 2012). The only genetically modified crop that has been approved for production in Bolivia is herbicide tolerant soybean. The first approved crop was planted in 2005, but farmers had already introduced roundup ready soybeans from Brazil through informal networks. It is believed that the first herbicide tolerant seed was introduced from nearby Argentina and/or Brazil and tested initially by farmers near the end of the 1990s. The regulatory approval process for Monsanto's herbicide tolerant soybean began in 1998. Monsanto presented field trial results for herbicide tolerant soybean in February of that year, and in October, obligatory field trials were initiated. In November 2004, Bolivian authorities detected 400 ha of herbicide tolerant soybean and announced sanctions on commercial production. In 2005, the government of Bolivia authorized the production of herbicide tolerant soybean (Smale et al., 2012).
In 2014, Paraguay grew about 3.9 million ha of genetically modified crops (James, 2014). Up until the 2004/2005 season, the country did not allow the use of GM seeds. However, there had been unauthorized cultivation of herbicide tolerant soybeans since 1997 probably introduced from Argentina and/or Brazil. By 2003, run out of options, the government had displayed the intention to authorize GM crops already widely cultivated despite a legal ban. In 2004, Paraguay authorized the cultivation of GM soybean, in reaction to a situation where an estimated 80% of soybean planted was genetically modified. By the year 2010, Paraguay appears to have not yet passed and implemented a biosafety law (USDA Foreign Agricultural Service, 2010).
In Africa, while 3 countries (South Africa, Burkina Faso and the Sudan) are growing GM crops commercially, there are some 11 countries that are officially conducting confined field trials of GM crops. Apparently, countries that share borders with GM crop growing countries are at an increased risk of non-compliance of biosafety regulations because of porous borders that are easily prone to unauthorized movement of GM crop seeds. For instance, in a couple of workshops that the African Biosafety Network of Expertise (ABNE) project held in Ethiopia in 2015, participants reported that farmers along the border were already growing cotton strains resistant to bollworms through unauthorized introduction from the Sudan. Similar scenarios may happen in west African countries that grow cotton and share borders with Burkina Faso. These countries include Mali, Ghana, Ivory Coast, Togo, Benin and Niger. In southern Africa, South Africa is an early adopter of GM crop varieties and there is a likelihood that seeds containing GM traits may filter across the border without regulatory approval and official notice.
Apparently, the expansion or restriction of GM crop cultivation in different parts of the world is a function of the prevailing policy environment maneuvered by actors such as farmers, consumers and anti-GMO activists (Fig. 2). For instance, in Europe strong anti-GMO policies appear to have been shaped by a negative reaction about the technology from vocal consumers and environmentalists. In Latin America, GMO policies were largely influenced by enlightened and powerful farmers who saw agronomic and economic benefits from the first generation of GM crop traits. These large farmers were able to muster quite a lot of political clout to flaunt government regulations and to establish unauthorized facts on the ground and thereby necessitate the creation of a GMO friendly regulatory environment in the respective jurisdictions. In developing Asia, entrepreneurial farmers and seed producers were instrumental in diffusing the technology often also in breach of regulatory requirements. In South Africa, where technology-proficient large scale farmers are common, GM crop testing and diffusion took place early in the process in compliance with existing regulations. In Burkina Faso and Sudan political will was cardinal for the delayed but orderly introduction of the technology. In the rest of Sub-Saharan Africa, the dominant smallholder farmers are even scarcely aware of the existence of the technology and the regulatory issues, leaving policy driving space for elites to conduct endless workshops and arguments in conference halls across the sub-region.
Although the introduction of GM crops into the farming systems of developing countries is rife with regulatory non-compliance, experiences to date indicate little liability and redress issues arising because of such non-compliance. However, high profile cases such as the lawsuits on GMO rice in the USA which was settled for $750 million (Harris and Beasley, 2011) indicate the need to put workable biosafety regulatory systems that ensures predictability, compliance and properly regulated GM seed access by farmers. In developing countries, liability and redress concerns and the required safeguards should be considered on a case-by-case basis depending on the nature of the commodity, its use and the demands of export markets.
Genetically modified crop agriculture has rapidly become part of the cropping systems of the world. The introduction of these crops into a wide range of agro-ecologies where commodity crops such as soybean, cotton, maize and canola grow have lessened crop losses due to weeds and insect pests, lowered pesticide use and increased incomes. In addition, use of zero tillage and weed control by glyphosate in standing glyphosate-tolerant crops has enhanced soil conservation, reduced costs and eased crop management, in the end promoting sustainable agriculture.
In Latin American countries where land is in relative abundance, the introduction of glyphosate tolerant soybean has brought the cultivation of large land area under this crop, attracted large investment, increased aggregate production and stimulated export-oriented economic growth. In India and China, GM crop cultivation, largely centered on Bt cotton, has visibly benefited smallholder farmers by increasing incomes and consumption expenditure (Kathage and Qaim, 2012), enhanced supply of raw materials to local industry and export market, generated employment and overall stimulated the national economy. However, the introduction of these crops in many countries continues to face resistance because of precaution related to biosafety and socio-economic considerations.
The fact that these crops have been in use for nearly 2 decades without any incidence of harm leaves no room for questioning their safety. Nonetheless, the issue of socio-economic consideration is a Pandora's Box amenable for many interpretations. So far, there is little evidence that GM crops pose serious socio-economic problems that are different from other known agricultural technologies. Rather, major GM crop traits currently available in the market such as glyphosate tolerant soybean and insect tolerant cotton are agronomic traits that confer advantages for the farmers. In the absence of convincing threat and existence of these apparent advantages, obviously farmers are the bearers of the cost of overregulation.
The unauthorized access to GM crop seeds presented above detailed the natural reaction by farmers as a counter balance to unsound regulatory measures in individual countries, indicating difficulty of limiting access to an agricultural technology when the affected part of the society, in this case farmers, weighs on the opportunity cost of not adopting an otherwise useful technology.
Our analysis of situations in Latin America depicted a case where few relatively large scale farmers muster a high degree of political clout to take the law into their hands and create facts on the ground to force governments into submission to allow cultivation of GM crops. The experiences of China and India where smallholder farmers are the majority indicate the tenacity for introducing and copying a technology without regulatory approval by the national innovation systems including public research centers and seed companies. The India and China Bt cotton biosafety non-compliance cases also indicate the difficulty of ensuring GM crop biosafety regulatory compliance in an environment where non-compliance with intellectual property rights is rife. This, obviously, is because of the fact that formal biosafety clearance would raise proprietary rights issues on the trait for which the biosafety approval was sought.
By and large, our analysis defies the usual presumption that regulatory inflexibility would deter access to GM crop technology. Rather, regulatory indecision and/or regulatory encumbrances appeared to pose a threat to unregulated environmental release of GM crops. Hence for traits that are farmer-friendly and farmers are a politically strong group or the innovation system is strong at copying technology, putting a functional and workable biosafety system is not an option but a critical necessity to avoid the prospect of an unregulated adoption.
With the currently available GM crop technologies, it is apparent that farmers are the global drivers of the adoption of genetically modified crops especially in the developing world. Because of cross-border linkages and relationships among local communities, it was obvious that GM crop technologies infiltrated into several countries without regulatory oversight. These indicate the importance of regional reconnaissance of the state of GM crops and the need for building functional biosafety systems in individual countries. Not least important is the need to consider regional approach to biosafety with the ultimate goal of harmonization of regional biosafety and biotechnology policies.
Africa is characterized by a rapidly growing population and a relatively large expanse of potentially cultivable land. The continent needs to enhance agricultural productivity through harnessing its land and labor resources to bring about food security and sustainability. Besides area expansion, raising productivity on the already cultivated land is cardinal in order to prevent the ill effects of agriculture on nature reserves. To this end, the rapid adoption of conventional and new technologies such as GM crops is required to raise productivity so as to ensure food and nutritional security, income growth and poverty reduction.
In Africa, while many more GM crop traits of relevance are in the pipeline, the 2 most widely commercialized traits—the herbicide glyphosate tolerance and insect resistance traits—have big potential to attract investment, reduce crop and yield losses, and enhance farm incomes and economic growth. While the relevance of Bt cotton in dry and hot African agro-ecologies is undisputed, the fact that the continent has a substantial warm semi-humid to humid lands suitable for herbicide tolerant soybean production should not be overlooked. Moreover, the potential advantage the Bt trait confers to protect the continentally important crops such as maize from insect damage and the ease of weed control in an array of standing crops under conservation tillage enabled by the herbicide resistance trait cannot be discounted.
However, making use of these opportunities requires the adoption of biosafety regulation that is workable, responsive and flexible. Apparently, many African countries are experimenting with GM crops, with several countries expected to progress toward commercialization and general release. In such a scenario, the foregoing conclusion is that there will be cross-border leakage of GM crop varieties from one country to the next without regulatory approval. This calls for the need to anticipate things beforehand and putting the necessary regulatory frameworks in place. From the lessons in Asia and Latin America, such frameworks need to consider practicality and functionality of the system in order to avoid unregulated release into the environment of GM crops. More importantly, given the potential for cross-border movement through informal seed exchange networks, the need for harmonization of GMO policies under regional blocks is of prime importance.
Since 1996, GM crops have become a common feature of the agricultural landscape in many countries of the world. Our review of literature indicated the expansion of these crops in many developing countries circumventing biosafety regulatory requirements. We found that unencumbered, efficient and flexible approach to biosafety regulation is key to the regulated adoption of safe and useful GM crop technologies. Lack of workable and functional biosafety regulatory system not only stifled access to technology and innovation but also encouraged unregulated and unauthorized access to the same technology the system wanted to limit access to. Such unauthorized access led to the adoption of substandard or spurious varieties which undermined performance, productivity and economic return for farmers. Regulatory intransigence was not sufficient to hold out from farmers a technology that worked well and is beneficial for them. We suggest that a flexible and workable biosafety system that considers regional dynamics would help promote biosafety regulatory compliance and minimize the prospect of unauthorized adoption of GM crops.
No potential conflicts of interest were disclosed.