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Use of Biotechnology for Sustainable Agriculture!
Agricultural production systems have real resource limitations. There is limited land area suitable for agricultural production, which land resource scientists believe will see a net increase of 5% over the next century.
Other limitations include fossil fuels-most temperature zone crops require more fossil fuel for production than the plants capture as harvestable photosynthate. Based on current sources and rates of consumption, we also have limited supplies of phosphorous and potassium. A second, perhaps equally important concern is the instability of agricultural production environments.
Predictions of climatic change suggest that global mean temperatures could change by either plus or minus 2-4°C. While it is unlikely that we will experience such radical mean temperature changes over the next decade, it is realistic to expect some temperature and associated precipitation changes over the next 20 to 50 years.
Net changes in mean temperature over the next 50 years will probably reflect the balance between increasing greenhouse gases and changes in atmospheric particulates from volcanic activity and combustion. Desertification processes appear active in both Africa and Asia. Clearly, climate is unstable, and may have an impact on the stability of agricultural production over the next century.
If we examine total world agricultural production over the past 30 years, two dramatic changes are perceptible. First, agricultural production has increased dramatically (on par with population growth). Secondly, there is increasing annual variation in total production around that trend line. Variation has increased substantially in the past few decades, perhaps as a result of the natural interplay between variable climatic conditions and increasingly intense agricultural output.
A third major source of uncertainty is associated with variable economic and trade policies, including uncertainties associated with the implementation and effect of the recently concluded negotiations of the General Agreement on Tariffs and Trade (GATT). Mr. Arthur Dunkel, former Director General of GATT, proposed the process in the hope that GATT would eliminate agricultural production subsidies, and there will certainly be an impact, whether positive or negative. All three areas of uncertainty (resources, climatic change, and trade policy) will determine when-or if-the global agri-food system will be sustainable.
What impact can biotechnology have on agricultural sustainability or global food security? Biotechnology may help in global agricultural sustainability if it accelerates genetic advances in productivity. There has been much talk about biotechnology in a general way, in some very specific applications. Increases in productivity in the past 100 years-which have been huge and have accommodated a 400% increase in human population-have relied on two major components genetic advances and increases in resource inputs.
Many of our agricultural resources are limited, so in the long term it is very important to use resources wisely.
Future sustainability will probably also come about through genetic advance. The maize industry in North America and Europe has increased productivity at a rate of two bushels per acre per year in recent decades, mostly through improved hybrids. Similar relative gains through genetic advances have been made in cereals, soybeans and most other major grain crops. Gains in vegetable crop productivity have been somewhat slower over that period.
If biotechnology can help us advance the genetics of our food crops (greater output per unit of finite resource input), then it can contribute towards agricultural sustainability. If biotechnology can help preserve environmental resources, and both essential resources (air, water and nutrients) and also aesthetic resources (green space, parks, diversity, etc.), then biotechnology may help us move towards agricultural sustainability.
If biotechnology (and plant breeding and genetics) fails to help improve resource utilization efficiency, then agriculture will probably not be sustainable, and the size of the global community will decline as resources are exhausted. If biotechnology fails to help preserve aesthetic components of the environment, then there will also be a decline in the quality of life for the global population.
Environmental considerations are critical to sustainable agriculture, and biotechnology may contribute to enhancing or conserving environmental resources, if properly managed. If not properly managed, biotechnology could accelerate environmental degradation.
If biotechnology is really to have an impact on sustainability, real sustainability, then it has to be available to those who need it. Certainly, the pilot programmes of the International Service for the Acquisition of Agri-biotech Applications (ISAAA) are an effort towards that end. But there are many additional efforts that are required.
One area often ignored, in the context of technology transfer, is human resource development in those regions that can best benefit from biotechnology, in order to have the expertise available and apply it in the most appropriate ways to answer regional needs. Technology transfer is an essential requirement if biotechnology is going to have a real impact on global agricultural sustainability.
The real challenge has been an evolution of appropriate regulatory processes that ensure biotechnology impacts positively on the major factors related to agricultural sustainability, while protecting environmental resources and human health and welfare. If, through regulatory processes, we can move towards positive benefits from biotechnology, sustainability will be one step closer-that is, sustainability may become a real possibility, rather than the major uncertainty it is today.
Ecological and Evolutionary Problems in Transgenic Crops:
The genetic improvement of cultivated plants through the use of recombinant DNA techniques promises to enhance the quality of food and fiber, to increase yield through better protection from diseases and pests, and to reduce the need for chemical inputs-both toxins and fertilizers.
Because many of these advances allow more efficient use of land already in agricultural use, they promise not only to feed and clothe people but to help alleviate the pressure for conversion of wild lands into croplands and pastures. The development of improved tree varieties for reforestation of degraded tropical agricultural lands, through rDNA techniques, could provide a sustainable supply of forest products that would further relieve pressure on tropical forests.
What, then, are the conceivable ecological hazards associated with the testing and use of transgenic plants?
There are six categories of environmental concern:
1) The creation of new weeds;
2) The amplification of the effects of existing weeds;
3) Harm to non-target species;
4) Disruptive effects on biotic communities;
5) Adverse effects on ecosystem processes; and
6) Squandering of valuable biological resources.
Creation of New Weeds:
Many crops have been domesticated to such a degree that they are entirely dependent on human activities. Maize, wheat and bananas are good examples. Such crops, whatever the improvements made through biotechnology, are unlikely to become self-propagating weeds in any ecological context. Some other cultivated plants are weeds in some contexts and crops in others-certain kinds of millets (Pennisetum spp.) and sorghums (Sorghum spp.) fall into this category.
The introduction of a gene that increases plant fitness (such as resistance to disease or to pests) to a crop in this category might shift the balance toward weediness in areas where they are now safely grown as crops, or promote weediness in varieties now considered safe. Other crops have close weedy relatives-including sugarcane (Saccharum), rice (Oryza), potatoes (Solanum), sweet potato (Ipomoea), vegetable and oil seed (Brassica), sunflower (Helianthus), and oats (Avena).
For some of these crops, which still share many characteristics with their weedy ancestors, certain kinds of genetic alterations might create weed problems with the crop itself. For example, a transgenic, highly salt-tolerant variety of paddy rice might itself invade estuaries. Generally, however, the likelihood of most crops themselves becoming serious weeds is small.
Considerably more likely is the development of increased problems with already-weedy relatives, by the acquisition of fitness-conferring genes from a transgenic crop through hybridization and introgression. Ecologists consider this scenario to be the primary ecological risk from transgenic plants. It is often wrongly discounted, however, due to a common confusion between the concepts of introgression and hybridization.
Some pairs or groups of closely-related plant species (for example, orchids or cucurbits) hybridize freely in cultivation, free from the constraints of the co-evolved pollinator systems of their ancestral habitats. For other groups of plants, hybridization is infrequent, rare, or completely impossible. If formed, first-generation (50/50) hybrids may be fully fertile, but more often they have reduced fertility, or are completely sterile.
Introgression is the incorporation of genes from one species into the gene pool of another. The process must begin with hybridization, but it is more complex. Introgression in nature is precisely analogous to a common technique of plant varietal improvement. The plant breeder may start with a variety that has many desirable commercial characteristics, but is susceptible to some pathogen.
The breeder crosses this variety with a wild relative that lacks the commercial traits, but is resistant to the pathogen. Often, the first-generation hybrids that have the resistance trait will have lost many of the desirable commercial traits of the cultivated parent. These must be recaptured by repeated backcrossing and selection.
The process of hybridization plus backcrossing and selection is an exact parallel, under artificial selection, to the process of introgression under natural selection. Just as the breeder’s first generation hybrid lacks the combination of traits that makes it either a fit wild plant or a desirable cultivated plant, the first generation hybrid between a transgenic crop and a weedy wild relative at the edge of a test plot or a farmer’s field would likely be rejected both by the farmer and by nature-its fitness relative to the wild plant would be low.
But if it flowers and passes pollen to its wild cousins, the next generation will have % of the genes of the wild relative, the next 7/8, and so on: this is the process of introgression. If the hybrid included a transgenic trait that would, by itself, confer high fitness on the weedy relative such as disease or pest resistance-then natural selection will rapidly promote the reproductive success of these successively “wilder” genotypes, just as the plant breeder regains the commercial qualities of the new variety by backcrossing.
Hybridization need not be a common event for introgression to proceed, carrying a transgenic trait from crop to weedy relative. That a crop and a weedy relative are known to hybridize only “rarely” is sufficient for the escape of a transgenic trait into the population of a weedy relative. If the gene does as much for the weed as the genetic engineer hopes it will do for the crop, then, at the limit, hybridization need only occur once for escape; natural selection will take care of the spread of the gene. Likewise, even crops such as sugarcane (Saccharum officinarum) and sweet potato (Ipomoea batatas), which are generally considered infertile, occasionally produce normal pollen; if hybrids form, once may be enough.
The second point” is that hybrids need not be particularly fit in themselves, as long as they are competent to backcross with the weedy relative. Maize (Zea mays) and its wild relatives, the teosintes of Mexico and Guatemala, provide a good example. Teosintes include three wild subspecies of maize itself (Zea mays mexicana, Z. mays parviglumis, and Z. mays huehuetenangensis) and three closely related species of Zea (Z. dipolperennis, Z. perennis and Z. luxurians).
Some of these taxa are agricultural weeds and some are wild land species. Hybrids between teosintes and cultivars of maize are known for several of these taxa. Supposedly, some Mexican farmers even encourage some hybridization by allowing weedy teosintes to grow at the edge of their fields to make the maize “stronger,” but genes may flow from maize to teosinte in such cases, too.
In all cases, the hybrid is of low fitness, as evaluated by both natural selection (the seeds do not disperse easily) and artificial selection (to the farmer, the grain is inferior in quality and is not as easily harvested as maize, so is not kept for seed).
Nonetheless, introgression from cultivated maize into wild teosinte populations. Such introgression simply indicates that, however lows the fitness of first-generation hybrids, they are nonetheless competent to backcross with teosinte. Because of the low fitness of intermediates, maize and the teosintes have kept their distinctive identities; an evolutionary biologist might call it a case of disruptive selection.
Some cite the fact that maize and teosinte have coexisted for centuries without losing their identities as evidence against the danger of creating a seriously weedy teosinte through acquisition of a transgenic trait, and against the danger of genetic contamination of wild teosinte gene pools with novel genes of distant origin (such as the Bacillus thuringiensis gene-B.t.).
These reassurances, based on a misunderstanding of the nature of introgression, are entirely misguided. It is also well to remember that when low-probability events (or hazards) are multiplied by large exposures, they become virtually inevitable. Even if the outcrossing rate of a crop plant is only 0.1%, if there are a million flowers in field, then we must expect 10,000 outcrossing events.
The irrelevance of traditional plant quarantine regulations and practices, with respect to guarding against introgression of transgenic traits into wild or weedy relatives of cultivated plants. Because a gene is not a disease or a pest, quarantine is pointless. The danger point is the open field somewhere in the middle of the countryside, not a port of entry.
Unfortunately, small numbers of familiar local weeds that contain a newly acquired, high-fitness; transgenic traits are likely to go unnoticed, simply because they are familiar, until they become a significant problem. Thus, awareness of the potential for introgression and vigilance regarding potential recipients of such genes are called for not at the port of entry, but around test plots and, later, in the first commercial fields.
The exception would be the very difficult task of controlling, at ports of entry, the illegal importation of small quantities of transgenic seed by individuals, even well-meaning farmers or amateur gardeners. Again, as we know from countless cases of “informal” importation of weeds and other undesirable species by individuals, one mistake can be costly.
In the case of transgenic plants, the non-target species of concern include both animals and other plants. When genes producing compounds intended to deter or kill pest insects or mites are incorporated into crop plants, the ideal result is that only the target pests are affected. We know from decades of unhappy experience that this ideal result is all too often not the case with chemical pesticides. Of course, our great hope is that transgenic plants with highly specific secondary chemicals are the answer.
Precautions are needed, however. An insect-pollinated transgenic plant that has been engineered to make an insecticidal compound intended to deter leaf or root-eating pests had better not produce the same compound in its pollen or nectar. A fiber plant that produces an insect toxin in its leaves had better not poison the farmer’s cattle that wander into the field. A plant that produces a mite toxin would likely affect beneficial predatory mites as well as phytophagous miles.
Even B.t. toxin, of which some strains affect only Lepidoptera insects, could potentially harm beneficial-or at least desirable-butterflies and moths. For example, the striking red-, orange-, or yellow-and-black heliconine butterflies of tropical forests not only help attract many natural history tourists to tropical countries, but are considered to be “keystone species” in most natural communities in the New World tropics. The larvae of most of this diverse group of butterflies feed on wild species of Passiflora or passion-fruit vines (maracuya). Because certain Lepidopteran larvae are also pests of cultivated passion-fruit, incorporation of the B.t. gene would seem a natural approach to improving this crop.
The wild land butterfly species would be severely affected, however, by the acquisition of the B.t. gene by these wild plants through introgression with a cultivated transgenic passion-fruit carrying the gene. Thus, unless hybridization can be prevented, it would seem dangerous to field test or commercialize passion-fruit cultivars with the B.t. gene anywhere near wild Passiflora spp. Harm to other plants caused by transgenic crops includes several potential problems, all of them consequences of the acquisition of transgenic traits by wild relatives through introgression.
Effects on Biotic Communities and Ecosystem Processes:
The composition and relative abundance of species, and the spatial structure of natural plant communities, depends upon a complex balance between plant-plant competition, the effects of herbivores and seed predators, and interaction with pollinators, seed dispersers, and soil mutualists. The acquisition of a high-fitness trait, such as protection against herbivorous insects, by a wild land plant species through introgression with a related transgenic crop could have several disruptive consequences.
We know from agricultural experience that pests are capable of causing massive reductions in crop reproductive fitness and yield. Experiments in natural communities and the record of successful biological control of weeds by imported insects and pathogens testify to the importance of reproductive control of plants by enemies in both agricultural and natural communities.
A wild land plant species, released from significant natural control, would become a better competitor, likely to reduce the density of competing plant species. Secondary effects could include declines in animal populations dependent on these species, and even changes in vegetation structure.
Ecologists have expressed concern about the effects of transgenic plants, or wild plants that acquire transgenic traits through introgression, on the functioning of ecosystems. Of course, transgenic trees used in reforestation projects may have very beneficial effects on ecosystem processes by increasing the per-area carbon fixation rate, by stabilizing or enriching soil, and by buffering climate.
But some caution is called for regarding transgenic (or other) plants that significantly affect soil nutrient balance. For example, if and when nitrogen fixation gene complexes are successfully introduced to forest trees, careful testing should precede widespread introduction in order to determine the effects on the supply and demand for other soil nutrients, particularly phosphorus.
Squandering of Valuable Biological Resources:
The principle biological resources that may be at risk from the testing and use of transgenic plants are plant genetic resources-in this case, not so much the genetic diversity of land races and cultivars, but diversity of the gene pools of wild species. Once again, the principal risk arises from introgression of cultivated crops with wild plants.
Some, such as African oil palm and cacao, are important components of the Costa Rican agricultural economy. In the case, at least, of oil palm, Costa Rican wild relatives have already been the source of genetic variation for past crop improvement.
Indeed, an ethical argument can be made against allowing introduction of genes from unrelated organisms to wild organisms of any species. For example, we know that genes from cultivated maize have entered the gene pools of wild teosintes.
This can be considered a natural process that is part of the evolution of crops from wild relatives. But the introduction of, for example, a gene from bacteria (B.t. toxin), or from a distantly related plant group, seems to some of us to be a different matter-a process referred to as the “conduit effect” (Figure 1).
There is no adverse ecological effect such genetic contamination devalues the genetic resource and evolutionary integrity of wild species. This ethical argument, of course, rests on the distinction between domesticated species, which have long evolved within the evolutionary domain of humans, and wild species, which have historically been comparatively free from our influence. Such congeneric matches are simply the most likely suspects for introgression-suspects that a wise regulatory policy should insist on knowing more about before granting permission for even an initial field trial, in my opinion.
One final resource that transgenic plants may threaten, if used unwisely, is the very small library of highly specific genes for the control of insect pests; the most obvious example is B.t. As for any other pesticide, resistance can evolve quickly if pest populations are continuously exposed to it over large areas, eliminating the pockets of susceptible genotypes whose resurgence is the key to continued effectiveness.
At present, a special cooperative effort between ecologists, evolutionary biologists and molecular biologists is underway, funded by the biotechnology industry, to find ways to prolong the useful life of the B.t. gene by minimizing exposure and pinpointing expression to vulnerable tissues, instead of relying on constitutive expression of the trait. This cooperative project is a fitting example to end with, showing the potential role that collaboration between ecologists and evolutionary biologists may play in the safe and effective implementation of biotechnology.