One of the major public concerns about transgenic crops is their effect on non-target organisms. The results of a number of studies have demonstrated that the effects of transgenic crops on non-target organisms including natural enemies and other arthropods are likely to be much less severe than those of the broad-spectrum insecticides.
Effect # 1. Non-Target Insects:
Within any agricultural system, several non-target species are expected which are related to the target species and which may be susceptible to the Bt protein expressed in the Bt crops.
The first report on the adverse effects of transgenic crops on non-target insects appeared in 1999. It was reported that the caterpillars of monarch butterfly, Danais plexippus (Linnaeus), fed on the milkweed plants sprinkled with Bt maize pollen, grew slower and had higher death rates than caterpillars fed on leaves sprinkled with pollen from non-Bt maize.
On the basis of the laboratory data, the authors developed a scenario in which they hypothesized that there could be potentially profound implications for the conservation of monarch butterflies with the widespread use of Bt maize. This report was criticized for its inappropriate design, methodology and interpretation; the major criticism was the fact that pollen densities on milkweed leaves were not quantified.
In another study, mortality of larvae of monarch butterfly from Bt maize pollen was recorded but there were large discrepancies between the toxin levels in pollen that they measured and those from replicated measurements accepted by EPA. This discrepancy was due to the use of pollen samples containing 43 per cent plant debris.
This debris was known to cause significant mortality and reduced weight gain by more than 80 per cent. This debris (mostly other parts) was an artifact of the collection method and unrelated to the Bt maize pollen that may fall on milkweed plants. However, these reports have tremendous implications about how science is conducted and communicated.
In other studies, there was no relationship between pollen deposition from transgenic maize and mortality of the black swallowtail butterfly, Papilio polyxenes Fabricius, and the milkweed tiger moth, Euchatias egle Drury. There was no adverse effect on overall development of non-target herbivore, Mamestra brassicae (Linnaeus), when reared on Plutella xylostella (Linnaeus)-resistant Bt Chinese cabbage.
Effect # 2. Predators:
The effects of transgenic plants on the activity and abundance of predators vary across crops, insect species and the transgenes in question. Cry1Ac was detected in Chrysoperla carnea (Stephens) larvae fed on resistant Plutella xylostella (Linnaeus) larvae reared on Bt oilseed rape.
However, no Cry1Ac could be detected in C. carnea larvae when the lacewings were transferred to P. xylostella larvae reared on non-transgenic plants, indicating that C. carnea is able to metabolize plant-produced Cry1Ac. There was no effect on preimaginal development or mortality of C. carnea when reared on Rhopalosiphum padi (Linnaeus) fed on Bt-maize.
Similarly, survival, aphid consumption, development and reproduction of Hippodamia convergens (Guerin-Meneville) are not influenced when fed on Myzus persicae (Sulzer) reared on potatoes expressing δ-endotoxin. Feeding C. carnea on Tetranychus urticae Koch (which ingested Bt toxin from the transgenic plants) or R. padi (which did not ingest the Bt toxin) did not affect survival or development of the predator.
Field surveys have shown little impact of Bt maize on predator species numbers or densities. In tritrophic studies with the hemipteran predator, Orius insidiosus (Say), there was no effect when feeding on Bt-intoxicated European corn borers. In this case, the results were confirmed with direct feeding studies on Bt corn silks and observations of populations in Bt and non-Bt maize fields.
A significant increase in the mortality and delay in development of C. carnea was observed when fed on Spodoptera littoralis (Boisduval) and Ostrinia nubilalis (Hubner) which had ingested Bt toxins from transgenic corn. The mean total immature mortality for C. carnea raised on Bt-fed prey was 62 per cent, as compared with 37 per cent on Bt-free prey.
However, experimental design in this study did not make distinction between a direct effect due to the Bt protein on the predator and indirect effect of consuming a sub-optimal diet consisting of sick or dying prey that had succumbed to the Bt toxin. Thus, the effects observed appear to reflect the poor nutritional quality of Bt-susceptible prey rather than any toxic effect of the Bt protein on lacewings.
Effect # 3. Parasitoids:
In general, transgenic plants seem to have little or no effect on parasitoids of insect pests. In fact, increased levels of parasitism by Campoletis sonorensis (Cameron) on H. virescens have been observed on transgenic tobacco as compared to non-transgenic plants.
Physiological mechanism was put forth to support this phenomenon, i.e. toxic plants generally caused larvae to grow more slowly which may increase the duration of attack by natural enemies. In another study, activity of Cordiochiles nigriceps Viereck on H. virescens was not influenced by transgenic plants, which may be due to behavioural mechanism, i.e. toxic plant increased movement of larvae, which may alter their chances of encountering by parasitoids.
Similarly, transgenic corn was observed to have no adverse effects on the parasitization of O. nubilalis by Eriborus terebrans (Gravenhorst) and Macrocentrus grandii Goidanich. However, the larval development and mortality of the parasitoid, Parallorhogas pyralophagus (Marsh), was adversely affected, when reared on Bt-susceptible insects that had fed on Bt maize, but the fitness of the emerging adults was not impacted.
No adverse effect was found on diamondback moth parasitoid, Cotesia plutellae Kurdjumov by feeding on Cry1Ac-resistant larvae. No Cry1Ac protein was detected in newly emerged larvae of the parasitic wasp, Cotesia vestalis Haliday, fed on diamondback moth larvae, which had fed on Bt oilseed rape.
Similarly, no significant changes were observed in the parasitization rate, larval period, pupal period, cocoon weight or adult emergence rate when the parasitoid, Microplitis mediator (Haliday), was reared on the M. brassicae larvae fed with Bt transgenic Chinese cabbage. Studies on the impact of Bt broccoli plants on Pteromalus puparum (Linnaeus), an endoparasitoid of Pieris rapae (Linnaeus), indicated that there was adverse effect on parasitism rate, developmental time, total number and longevity of P. puparum.
However, no Cry1C toxin was detected in newly emerged P. puparum adults developing in Bt-fed hosts. Moreover, no negative effect was found on the progeny of P. puparum developing from the Bt plant-fed host when subsequently supplied with a healthy host (P. rapae pupae). The negative impact of Bt broccoli on P. puparum resulted from poor quality of the host rather than direct effects of the Bt toxin.
Effect # 4. Pollinators:
Pollination is another factor that must be considered in terms of possible effects of transgene products on beneficial insects. Some reports indicate that transgenic plants seem to have low or no harmful effects on the lifespan and behaviour of honey bees.
Trypsine inhibitor, wheat germ agglutinin, serine protease inhibitor from soybean, cysteine protease inhibitor from rice, chicken egg white cystatin, and Bowman-Birk type SBTI do not produce harmful effects on honey bees at the concentrations expressed in transgenic plants.
The chitinase transgene in genetically modified oilseed rape did not affect learning performance of honey bees; beta-1, 3-glucanase affected the level of conditioned responses (the extinction process occurring more rapidly as the concentration increased), and CpTi induced marked effects in both conditioning and test phases, especially at high concentrations. Thus, it can be assumed that transgenic crops do not pose a major threat to the activity and abundance of pollinators.
Effect # 5. Secondary Insect Pests:
The large-scale cultivation of transgenic crops with resistance to certain insect pests may result in secondary insect pest problems becoming a serious constraint in crop production. It may, therefore, become necessary to resort to spraying in order to control the secondary insect pests, which would adversely affect the natural enemies.
The Bt toxins may be ineffective against certain insect pests, e.g. leafnoppers, mirid bugs, root feeders, etc. and this may offset some of the advantages of the insect-resistant transgenic crops. The transgenic Bt cotton, which is resistant to bollworms, is susceptible to sucking pests like the jassid, Amrasca biguttula biguttula (Ishida); whitefly, Bemisia tabaci (Gennadius); mealybug, Phenacoccus solenopsis Tinsley, and less effective against Spodoptera litura (Fabricius).
There are also no differences in the susceptibility of transgenic and non-transgenic cotton varieties to boll weevil and aphids. Effective and timely control measures should be adopted for the control of secondary pests on transgenic crops. There is a need to deploy protease inhibitor and lectin genes that are effective against sucking pests, along with the Bt genes, to make genetically modified plants to be more effective against insect pests for sustainable crop protection.
Effect # 6. Wild Relatives of Crops:
One of the concerns of deploying transgenic crops is the possibility of vertical and horizontal gene flow. Gene flow can be defined as movement of a gene, via pollen or seed, followed by gene establishment in a new population. Gene movement via pollen occurs in space and time, and can result in gene flow to wild relatives, to other crops (including other genetically modified crops, i.e. gene stacking) and to feral populations.
Conversely, gene survival via seeds occurs in time (i.e., seed persistence) leading to genetically modified volunteers emerging in later years. There is evidence of hybridization to wild relatives in majority of the world’s principal crops, including banana, cassava, cotton, maize, millet, oats, potato, oilseed rape, rice, soybean and wheat. Unintended lateral transfer of a transgene between related and unrelated species is a potentially worrisome aspect of transgenic technology.
It is feared that the escape of a transgene to its related species or weeds growing near the transgenic crop may occur by pollen dispersal, thereby creating ‘super weeds’, endowed with, for instance insect resistance, which may eventually invade new habitats. While introgression of transgenes resulting in enhanced weediness is unlikely to happen in many cases, especially the gene flow between different species, it is theoretically possible.
The report of a possible gene flow between maize and teosinte in Mexico is of great concern. The report recommends that quantitative studies be carried out on the potential gene flow to the genus Zea before liberating transgenic maize varieties, and that experimentation with transgenic crops take place under the strictest security measures to prevent gene flow. The introgression events are relatively common in maize, and the transgenic DNA constructs are maintained in the population from one generation to the next.
Therefore, there is a need to study the impact of gene flow from commercial hybrids to the traditional land races in the centers of origin in order to know the period for which the integrity of transgene construct is retained and the increase and/or decrease in the abundance of the transgene construct over time.
Once large-scale cultivation of transgenics is undertaken, the possibility of genetic exchange between land races and transgenic material cannot be summarily ignored and it is essential to secure germplasm in the gene banks globally.
Effect # 7. Soil Biota:
The levels of Bt proteins found in the soil of Bt crop fields will be low even after several consecutive years of growing Bt crops. Even if substantial amounts of Bt protein were to persist and accumulate in soil, no activity is expected against the invertebrate species that are important to soil processes.
It has been demonstrated that two species of Collembola are not susceptible to a variety of Cry1, Cry2 and Cry3 Bt proteins. Similarly, it has been found that representative species of earthworms, nematodes, protozoa, bacteria and fungi were not impacted by the Cry1Ab protein found in most commonly used Bt corn products.
Several of the non-target field studies on Bt rice, Bt corn, Bt cotton and Bt potatoes have included sampling of either ground dwelling insects and/ or pit fall trapping, and no adverse impacts on ground-dwelling or soil-dwelling taxa have been detected.
Transgenic cotton leaves had no significant acute toxicity on the earthworm, Eisenia fetida (Savigny), from oral exposure to the transgenic line, GK19. No significant differences were observed between Bt and non-Bt rice variety in either decomposition dynamics or in the soil microbial communities associated with residue decay.