Genetically Modified Organisms in Entomology

2008 Student Debate The Use of Genetically Modified Organisms in Entomology

Anne L. Nielsen and Roxanne G. Burrus

- ogy is an area of active research, but it remains a controversial In preparation for the debates, each student team was assigned one Ttopic.he use GMOsof genetically have numerous modified applications; organisms (GMOs) however, in entomol the ben- ofthe three accuracy topics of and current a pro evaluation or con position. procedures An introductory in the United team States. was also chosen for each topic to provide the audience with unbiased background information about the topic question and the issues efits may be outweighed by concerns and negative impacts. GMOs- utilize recombinant DNA technology to cut a small piece of DNA from prepare, but the majority of the work was done in the two months isone expressed. species (donor) The host and species introduce is now it a into GMO the and DNA has of acquired another traits spe precedingbeing addressed. the Annual The Meeting. teams had Each approximately team was asked five to months select noto ciesit could (host) not with have which obtained it cannot by conventional cross, but in breeding.which the donorSuch traits DNA more than 40 references, to which they must limit their argument. Reference materials and an abstract of each team’s position were are the genes most widely put to commercial use. Plants that are shared between sides prior to the debate. include herbicide resistance and insect tolerance/resistance, which During the ESA annual meeting, each debate team is invited to proteins derived from the soil-borne bacteria Bacillus thuringiensis modified for insect tolerance or resistance commonly express Cry1- of the topic is given, after which each team gives a seven-minute santo Corp. in 1996. Ten years after introduction, Bt cotton and Bt participatepresentation in on the their debate position. symposium. The debate A five-minute continues introductionfor a total of maize(Bt). These were grown crops wereon 162 first million made hectares commercially worldwide available (James by 2006). Mon Transgenic crops have reported reduced pesticide inputs, resulting of three judges for each debate topic who asked questions of both in decreased costs and ease of management. Yield increases have 20teams minutes after theafter debate the presentations. and determined In which 2008, team we included made the a betterpanel been minimal, if they occur at all (Kathuria et al. 2007). However, argument. Each debate team was given feedback from the judges pollen transfer and the impacts to non-target arthropods are of top that could be used in the preparation of the written arguments that ecological concern. follow. The written statements are limited to 600 words and 15 of the original 40 references. For the purposes of this debate, GMOs included herbicide-resistant plants and organisms that are altered GMOs, at least in research, also include genetically modified with Wolbachia, but did not include sterilized insects (Sterile Insect targetingdisease vectors the parasite, (GMVs). or GMVsmodifying are primarily the arthropod modified itself in via one sterile of two in- Technique). Sterilized insects were not considered GMOs because ways:sect technique genetically or modifying the release the of phenotypeindividuals of carrying the arthropod dominant vector lethal by the sterilization conferred on an insect does not proceed to the next genes (Alphey et al. 2002). For both agricultural and human health generation; the insects are incapable of reproducing the mutated

risks to human health, biodiversity, and the environment. transmission of pathogens is prevented, this is true only for the applications, there are downstream effects to consider: specifically,- currentgenome. sterilized Although generation. the genome is modified and successful vector dent debate at the annual Entomological Society of America (ESA) Are GMO crops and GMO disease vectors a viable option for the In 2008, the use of GMOs in entomology was the topic of the stu regarding the use of GMOs in agriculture and human health, including topic are presented by the student teams. meeting in Reno, NV. Three important questions were discussed U.S. and other nations? The introductions and positions for each 106 American Entomologist • Summer 2010 ▲Pro Position TOPIC Gladys K. Andino, Victoria A. Caceres, Gloria I. Giraldo-Calderón, Julia Genetically modified insect disease vectors should be incor- K. Prado, Kapil R. Raje, and Janice P. Van Zee porated into vector-borne disease control programs because they decrease disease transmission and spread to humans and livestock with fewer environmental risks than conven- Department of Entomology, Purdue University tional control methods. increaseVector-borne health diseases care costs, cause andan enormous decrease burden productivity, on human mostly health in worldwide. These diseases cause significant economic losses, Introduction pest control techniques alone have not provided adequate control, Jennifer E. Bergh and Kimberly M. Skyrm ascountries evidenced that by can over least one afford million this deaths (Jacobs-Lorena and 300 million 2006). cases Traditional annually for malaria alone (Boëte and Koella 2003). Other vector-borne OregonArthropod-transmitted State University diseases such as malaria, leishmaniasis, try- diseases are also expected to increase as climate change, rapid global transportation, and increased immigration spread exotic vectors have emerged as serious health risks, imposing an overwhelming bur- and diseases into new areas (Abraham et al. 2007). The two main panosomiasis, dengue fever, yellow fever, and West Nile encephalitis den on world populations. These emerging and resurgent vector-borne traditional chemical control tactics, application of pesticides and diseases cause millions of new infections and incidences of mortality - annually, particularly in developing countries (WHO 2004). ness, respectively due to resistant insects and parasites (Riehle et al. Historically, vector control programs have utilized an integrated administration2003). Despite decadesof pharmaceutical of intense research drugs, are on malariaof limited and effective dengue, approach with a combination of traditional control methods, preven- a third strategy, vaccination, is only available for yellow fever, and in Entomology tive measures and pharmaceutical regimes (Lacey et al. 2001). The even in this case the disease has not yet been eradicated. (Jacobs- limited success of these approaches combined with developing resis- Lorena 2006). Because these methods of control are only partially tance has brought about an interest in the use of alternative control be incorporated into disease control programs. effective,Germ-line we arguetransformation that genetically in insects modified of medical vectors importance(GMVs) should is methods, as stated by Knols and Bossin (2006): “The continued threat already feasible in Aedes, Anopheles, Culex, Rhodnius, and Glossina of vector-borne diseases calls for both reactive and proactive efforts At a 1991 meeting of the World Health Organization’s Special spp. (Jacobs-Lorena 2006, Beard et al. 2001, Aksoy et al. 2001). The to mitigate the significant morbidity and mortality they cause.” Programme on Research and Training in Tropical Diseases and most promising strategy to date is paratransgenesis, in which an the MacArthur Foundation, researchers evaluated current disease - control strategies and formulated a plan to evaluate promising site, altering the arthropod host’s ability to transmit the pathogen - arthropod’s(Beard et al. symbiotic 2001). Paratransgenesis bacteria is genetically could modifiedbe used to to controlkill the para both African and American forms of trypanosomiasis (sleeping sickness alternatives (Christophides 2005). Genetically modified disease vec for inclusion within comprehensive control programs (Beaty 2000, and Chagas disease) (Beard et al. 2001, Aksoy et al. 2001). Labora- tors (GMV) are currently being considered as one such alternative Christophides 2005). tory and greenhouse experiments have been successfully conducted for one of the principal vectors of Chagas disease, R. prolixus, and for vectors to transmit pathogens (Christophides 2005, Curtis 2006). Trypanosoma cruzi The goal of GMV programs is to perturb the ability of insect - creating GM vectors that are refractory to disease transmission by , using a synthetic material called CRUZIGARD that In reaching this goal, researchers have explored two approaches: ascontains the next transgenic step (Beard bacteria et al. 2001).(Beard The et al. initial 2001). steps Due for to thethe effectivetransfor- development (Riehle et al. 2003, James 2005, Jacobs-Lorena 2006). nessmation of CRUZIGARD of malaria mosquitoes as a driving mechanism,(Anopheles spp.) field trialshave arealready warranted led to Methodsaltering their utilized physiology in these and/or approaches behavior, include or by thedisrupting use of dominant pathogen lethal genes, the use of bacterial symbionts that disrupt pathogen- testedidentification for Plasmodium of the promoters, species thateffectors, cause malariaand reporter in humans genes affecting(Riehle interfere with pathogen development. etmalaria al. 2003). in mice. The drivingThe effectiveness systems being of these investigated transgenes for mosquitoes needs to be esis or transmission, and the use of effector genes, whose products - include genetic phenomena (e.g., competitive displacement, reduced sideration of all potential complications and issues before release Evaluation of GMV agents as a control strategy requires con - systems based on exploitation of infectious and infectious-like agents genesis, and disease transmission must be amenable to the use of (extracellularheterozygous fitness,and intracellular under-dominance, symbiotic and microorganisms, meiotic drive) and viruses, other within control programs. Vector and pathogen life cycles, patho genetically manipulated refractory vectors (Marrelli et al. 2007, and transposons) (James 2005). Researchers are optimistic that these strategies can be further improved (Moreira et al. 2004). social, and ethical concerns must be carefully considered (Macer Although there is speculation about possible problems associated 2005,Lambrechts Knols and et al. Bossin 2008). 2006, Ecological, Lacey 2001). epidemiological, Additional issues economic, include these risks have not been supported by lab trials (Rodriguez 2006). and the burden of cost on developing nations (Lacey et al. 2001). with GMVs (e.g., the creation of a super-parasite), the estimates of the effects of biotic and abiotic parameters, environmental impacts, Because of the highly mobile nature of insect vectors, international free. Even pharmaceutical drugs and pesticides have risks associated collaboration is critical, as is education of stakeholders (Kapuscinski Unfortunately,with their use (Atkinsonno control andmethod Handler or strategy 2005). can be considered risk- 2002, Macer 2005). Given the potential impacts and the range of these issues, there is considerable controversy surrounding the incorporation of geneti- Ongoing field studies of insect behavior and ecology in potential release sites afford an unprecedented opportunity to develop novel vector control strategies that incorporate GMVs (Knols and Bossin callyAmerican modified Entomologist organisms • into disease control programs. 2006, Willem and Boëte 2003). Furthermore, the use of GMVs has107 Volume 56, Number 2 the potential to reduce the negative environmental impact of insecticides (Abraham 2007). can promote virulence evolution. Educational programs that integrate local communities and naïve mice. These findings suggest that resistant hosts, like GMVs, scientists are crucial; this process needs to be completely open to which greatly enhances the ecological dynamics of vector species and all involved (Macer 2005). Ethical, social, and legal implications Unlike genetically modified plants, GMVs are incredibly mobile,- should be resolved to ensure public acceptance and successful theminterferes within with sovereign the dynamics political of borders. released It GMV. is also Given unethical the uncontrol to release scientists, it is incumbent upon us to continue searching for new lable and unpredictable nature of GMVs, it is impossible to contain- implementationways to mitigate ofthe GMVs devastating (Toure andimpact Manga of these 2006). diseases. As responsible The use fected countries and individuals (Macer 2005). It is our position that GMVs without acquiring informed consent from all potentially af human life is precious. with traditional control methodologies (e.g. insecticides, bed nets, of GMVs is one avenue that we must explore; after all, every single tacticalhabitat implementationreduction) (Spielman of GMV 1994). for disease Because control indigenous is incompatible vector Acknowledgements populations have experienced selective pressure due to traditional preparation for the debate and for his comments and suggestions for Wethis thank manuscript. Dr. Jeffrey Holland for his time and guidance during our control methods for extended periods, GMVs are more likely to be severelyvector-borne affected. disease control. They cannot be controlled by the safety ▼Con Position In summary, we cannot support the incorporation of GMVs into Robert D. Anderson, Amanda C. Bachmann, Thomas G. Bentley, Beth - A. Irwin, and Daniel R. Schmehl andtrollable, management unsustainable, practices and legally potentially mandated unsafe for genetically to humans modified and the environment.organisms. The Existing release vector-borne of GMVs is inherently disease control unpredictable, programs uncon “fail” primarily in areas that lack the adequate infrastructure to maintain Department of Entomology, The Pennsylvania State University incorporated into vector-borne disease control programs. In addi- Genetically modified insect disease vectors (GMV) should not be will not be solved by compromising the ecology of a region and the ethicsthem. Vector-borneof science. disease control is a humanitarian problem that there are epidemiological, ecological, and ethical reasons why this istion a poor to low approach expectations to vector-borne regarding thedisease efficacy control. of the GMV strategy, Acknowledgements - We would like to thank Michael Saunders and the Department GMVs are less fit than their wild type (WT) counterparts (Ras of Entomology at Penn State for their contributions. gon 2008); therefore, genetic drivers are necessary to increase the inproportion a population of GMV (Christophides in the population et al 2006).(James Rearing 2005). Itand is estimated releasing that a 10:1 ratio of GMV to WT is needed to establish GMV traits- TOPIC Genetically modified organisms (GMOs) should be incorpo- cally improbable. rated into management programs for insect crop pests to GMVs into a population in such numbers is expensive and logisti- reduce insecticide use while providing acceptable levels of age is necessary to successfully drive desired traits into a population damage against all pests and improve crop yield. (ChristophidesEven if it were 2005). possible Because to release the driver GMVs and at these gene arelevels, mutagenic gene link in Introduction linkage breaks down between them. If the driver becomes associated David R. Coyle withnature, a non-target unpredictable gene, effects it could in result GMV in populationsundesirable phenotypescould arise if and the failure of the proposed control method. Most importantly, the gene drive system is irreversible once released. DepartmentThe world’s ofpopulation Entomology, is approachingUniversity of Wisconsin7 billion people, yet the proportion of cultivatable land continues to decline. Biotechnol-

James (2005) and Rasgon (2008) independently created models time.that predict Furthermore, that a 100% disease refractory vector interactions GMV population are complicated is required forby ofogy, global both agriculture. urban and rural,As such, is aGMOs significant are a very part contentious of our culture, issue and in diseasethe fact control,that diseases meaning can that be vectored100% efficacy by multiple is required species 100% and of one the bothgenetically-modified agriculture and ecology.organisms Are (GMOs) GMOs safe are ato significant both humans component and the environment? Is it feasible to use them as tools in food production? lead to acquisition of a new vector. For example, Chikungunya virus wasspecies introduced can vector to multipleMauritius, diseases. where it Novel acquired ecological a new situations vector (Aedes can albopictus) in the absence of its native vector (Aedes aegypti) (de Arearchitecture they effective can be in changedcontrolling to createpests and dwarf increasing varieties yield? that show elevatedVarious productivity traits can be(Sakamoto altered during and Matsuoka the creation 2004). of InGMOs. the case Plant of - wheat and rice, for example, increased nitrogen fertilization via soil Lamballeriecessful disease et al.control. 2008). These factors make it difficult to saturate amendments not only results in increased seed production, but also an environment with the 100% refractory GMV necessary for suc in stem elongation. However, dwarf varieties will convert nitrogen (Snow et al. 2005). Potential shifts in co-evolved vector-pathogen into additional seeds instead of vegetative growth, thus increasing relationshipsRelease of couldGMVs drive may changesalso select in diseasefor more virulence. virulent Mackinnonpathogens productivity. Plant defense can be enhanced, as in the case of the et al. (2004) reared several generations of malaria-immunized and many crop cultivars using Bacillus thuringiensis (Bt) as a manage- non-immunized mice and found that the immune-experienced ma- have been altered with Bt, including crops such as corn, rice, pota- ment tool (Romeis et al. 2006). At least 52 different plant species laria108 lines were significantly more virulent to both immunized and American Entomologist • Summer 2010 toes, canola, soybean, and cotton (Dunwell 2000). Plant physiology Crop losses caused by insect pests represent one of the great- can also be altered, and GMOs that show increased photosynthesis est limiting factors to crop production (Sharma et al. 2003). This rates, improved foliar sugar and starch ratios, altered senescence, potential for loss is one of the reasons crop producers are eager for and tolerance to environmental stress have been tested (Dunwell new technologies that can reduce the loss caused by pests. One of usage would be both assumed and accepted as an integral part of - global2000). food With production. all the potential However, benefits there of GMOs,is considerable one might controversy think their thesecticide potential use canbenefits be attributed of GMO usage to pest-resistant is the reduction genes in incorporated the amount inof manyinsecticides GMO products, applied (James which 2007,provide USDA insect 2008). control Reduction and alleviate in in From an agronomic perspective, GMOs are an integral part of the need to apply insecticides (James 2007). surrounding the use and benefits of GMOs. andglobal the food farmer. and Carpenter fiber production, et al. (2001) and reported when properly a reduction used, of ~1.2they reportedAnother a 260 potential million-pound benefit of GMOsincrease is the in increasecotton yield in crop when yields, using in requiremillion kgreduced of insecticides pesticide per inputs, year inbenefiting cotton alone. both However,the environment insects, part due to lower levels of crop damage. United States cotton growers with their short generation times and voracious appetites, often withgenetically the use modified of Bacillus Bollgard® thuringiensis cotton (Bt) (Singh maize et (Singh al. 2006). et al. Also,2006). a to continually develop new pest management tactics (Carvalho 3.5 billion-pound increase in corn yields was reported by the NCFAP 2006).find a wayYield to increases circumvent have GMO been technologies, shown in some forcing but certainly companies not margin for the individual producer. all crops. Research in rice, for example, has generated many prom- Ultimately,One of the these major higher concerns crop associatedyields translate with the into use a ofhigher GMO profitprod- ising technologies; however, none of these have translated into real ucts is the development of resistance to Bt. The Bt resistance gene in insects is typically recessive, which allows for the use of a refuge increases in other grain crops (Kathuria et al. 2007). strategy to manage resistance (Gujar et al. 2007). Additionally, a yieldFrom increases. an ecological In contrast, perspective, there have GMOs been are safesome only significant in certain yield cir- - cumstances. In such cases, they have been shown to be detrimental tive at reducing survivorship (Cerda et al. 2006). Employing either of to non-target species while not always reducing pesticide inputs high-dose refuge strategy can be utilized and resistance has shown development to be effec into the environment. For example, green lacewing (Chrysoperla in crop systems. carnea) larvae showed increased mortality when fed prey reared on theseThe strategies initial cost is effectivefor GMO seeds at combating is higher Btthan that of conventional Bt corn, and in choice tests preferred prey that had not fed on Bt corn seeds; however, this will be balanced by reduced costs associated (Hilbeck 2001). GMO plant residue takes longer to decompose, and contaminates soil with toxicological properties even after breaking GMOs will outweigh the increase in startup costs. While some cases down (Flores et al. 2005). GMOs are unnatural, yet to date have not with pest management. The long-term economic benefits from using been shown to be unhealthy (Peterson et al. 2000), nor have they were still problems with pests, these instances do not appear to be been proven to be ecologically damaging. They have, however, not thehave standard. shown that The crop use yield of GMOs did not in increasepest management significantly programs or that there can been proven to actually be healthy or ecologically undamaging. This be a powerful tool in the battle against pests. Given current evidence of reduction in insecticide use, successful pest damage control, and - increased crop yield, we maintain that GMOs should be incorporated reflects the current state of science in that we simply do not yet know into management programs. enoughThe perfect about the GMO long-term crop would effects show of increased GMOs to yield,make informed require fewer deci sions (Wolfenbarger and Phifer 2008). Acknowledgments food chain, and disappear at the conclusion of the growing season. We would like to thank our faculty advisor Dr. Craig Coates, and pesticide inputs and applications, have zero effect on the ecological continue. Unfortunately, no such GMO exists, and until it does, the debate will ▼theCon Texas Position A&M University Department of Entomology. ▲Pro Position Ashfaq A. Sial, Nikolai G. Wiman, Jeremy L. Buchman, Aubrey M. Colvin, Therese A. Catanach, Jordan M. Coburn, and Andrew and Bonnie Ohler W. Boswell

DepartmentAlthough insecticidal of Entomology, GM crops Washington have been State promoted University under the DepartmentPesticide management of Entomology, is a Texaspriority A&M in Universityagriculture as it relates to premise of reducing pesticide use and increasing yields, we contend both maintaining pest damage at or below acceptable levels and to the relatively recent push for more environmentally friendly crop • reliance on GMOs for pest management is inconsistent with the prin- that: expectation that these approaches will provide suitable levels of pest • most comparisons in insecticide use have failed to note that Bt control.production. The New advent management of new technologies techniques provides are implemented an opportunity with the to ciples of ecologically based IPM as defined by Kogan (1998); therefore GM crops represent substitution of one pesticide for - anotheritself is classified (Hurley 2005); and regulated as a pesticide (EPA 1998), and refine management programs in an attempt to further reduce pest - damage. Genetically modified organisms (GMOs) are a pest manage tional economic outlays are taken into account (Raney 2006); thement integration tool that hasof GMOs seen ainto significant management increase programs in usage will during result the in • increasescurrent regulations in yield do for not the represent safe deployment economic of benefit GM crops when are addi in- last decade (James 2007, Fernandez-Cornejo 2008). We assert that damage, and increase crop yield. plants; and reduced insecticide use, provide sufficient protection against pest sufficient to prevent flow of transgenes to other crops and wild American Entomologist • 109

Volume 56, Number 2 • the regulations are voluntary and unenforceable. TOPIC In contrast to IPM, in which insecticides are applied according Current evaluation procedures of GMOs are adequate to to pest density relative to injury threshold, genetically incorporated determine their long-term impacts on the environment and toxins are expressed persistently and independently of pest popula- human health. tions (Jayaraman 2005). This prophylactic use of insecticides results in stronger selection pressure for resistant pest genotypes, increased Introduction Cheri M. Abraham pest complexes, and environmental contamination (Hurley 2005). risksFor example, of non-target successful effects suppression leading to ofsecondary Helicoverpa pest armigera outbreaks, (Hüb new- ner) with Bt cotton in China has reduced organophosphate use (Wu MississippiSince the application State University of Bacillus thuringiensis as an insecticide in 1961 et al. 2008), but has been accompanied by the emergence of mirid humanity(Milner 1994) have and fostered the availability a highly polarized of genetically debate modified worldwide. organisms Cur- bugs (Hemiptera: Miridae) as a new cotton pest complex (Lu et al. (GMOs) for cultivation, the effects of GMOs on the environment and 2008).to allay Bt resistance has been supported (Onstad et al. 2001) under canola, and corn, which have increased in worldwide cultivation The effectiveness of high-dose/refuge strategy deployed by EPA rentlyfor at leastthere 12 are years two groups (Brookes of GMOs: and Barfoot plants 2006);such as and soybean, insects cotton, such are rare, b) resistance alleles are recessive, c) random mating occurs theamong following individuals potentially in Bt crops false assumptions:and refuges, and a) resistant d) a high individualsdose of the as honey bee, silkworm, mosquitoes, pink bollworm, and med fly, biotechnologyamong others, 2004).which areEmpowering awaiting field plants trials against and herbicides,future release insect for frequencytoxin is expressed of 0.16 forin Bt Bt crops resistance (EPA 1998).alleles inHowever, some populations exceptions toof pests,commercial and pathogens and beneficial sounds purposespromising, (Pew but the initiative possibility on of food ecologi and- Pectinophorathese assumptions gossypiella have (Saunders) been found was in unexpectedthe field. The and mean considered initial cal disaster causes alarm. GMO proponents argue that GMO crops comparatively high (Tabashnik et al. 2000). Resistance to Bt toxins in a lab-selected strain of Ostrinia nubilalis (Hubner) was inherited the other hand, GMO food crops foster fear in the general public (Ando as an incompletely dominant autosomal gene (Huang et al. 1999). andresult Khanna in healthier 2000). foods, Allegations higher havefarm income,been made and that greater humanity profits. may On Random mating may not occur because Bt delays the development somehow receive some mutation through consumption of GMOs due of insects such as Leptinotarsa decemlineata (Say), leading to unsyn- to horizontal or vertical gene transfer or the creation of “genetic mon- chronized emergence times between populations from Bt and refuge sters” made under the guise of good intentions (Ando and Khanna 2000). As a result, stricter measures have been suggested to make sure that these fears are alleviated (Ando and Khanna 2000). andcrops they (Nault decline et al. over 2000). time The (Karanthi levels ofet al.the 2005). Bt toxin Recently can vary observed among Current evaluation techniques, standardized by the World Health increasesdifferent inBt the varieties frequency and ofwithin resistance different alleles parts in some of individual populations plants, of Organization and Food and Agricultural Organization and imple- Helicoverpa zea (Boddie) suggest the potential for failure of existing mented by the Environmental Protection Agency, the Food and Drug

With the current transgenic crop technology, transgenes cannot be resistance management strategies (Tabashnik et al. 2008). marketAdministration, (FDA 1992). and These the United regulations, States which Department were formulated of Agriculture, prior threatens identity preservation for various cultivars of conventional toscreen the technological GMOs for possible advancements adverse that effects we are before now poisedproducts to achieve,come to containedand organic in cropsfields whereand their the introgression crops are grown. cannot The beflow easily of transgenes reversed are constantly being reviewed. So far, there have been no reported (Mercer and Wainwright 2007). Current EPA containment strate- environmental catastrophes related to GMOs. The pre-market safety

safeguard to prevent the release of a harmful GMO (FDA 1992). In gies (buffers) are ineffective in preventing pollen-mediated gene thereview twelve Section years 402 of GMO (a) (1) crop of theproduction, act (21 USC higher 342 farm (a) (1))incomes acts asand a theflow, risk particularly of pollen-mediated with regards gene to transmission insect-pollinated cannot crops be eliminated. (Pasquet positive environmental impacts have been reported, as measured by et al. 2008). Although chloroplast modification offers future hope, environment impact quotients (Brookes and Barfoot 2006). However, other stakeholders, which is another break from the mandate of IPM The inability to restrict flow of transgenes violates the interests of is further complicated by cultural practices such as seed trading, the National Research Council Committee has recently concluded that (Koganwhich is 1998). a critical In developingcomponent countries, of rural farming. containment In summary, of transgenes all of “the effects on the environment were considered to have the greatest topotential their mobility for long-term (Pew initiativeimpact” and on identifiedfood and biotechnology aquatic organisms 2004). and are incompatible with the principles of IPM that enjoins the use of insects to be of the highest concern for negative effects of GMOs due allthe the potential resources effects of ecology of currently to manage registered pests Bt whilecrops doingdescribed less harmherein to the environment. measuresWith increasing by national technology and international and genetically regulatory modified bodies insectsbefore waiting for field releases, many questions arise. Do we need stricter Acknowledgments evidence regarding the inadequacy of existing measures before we The authors wish to thank Dr. Allan S. Felsot for his guidance revampreleasing them? a GMO Although into the the market? current standardsShould we have wait been for successful scientific and support as faculty advisor and editor in preparing, presenting, in preventing the release of GMOs that would cause increased damage to the environment, are they still adequate or should standards and policies be increased? Are we clear on the jurisdiction with our theirand writing feedback. for this debate, and the faculty, staff, and students in the Department of Entomology at Washington State University for 110 regulatory bodies as GM insectsAmerican are awaiting Entomologist field •trials? Summer Are 2010 the assessment, and risk characterization adequate, and do they justify more predictable and controllable than those in conventionally bred policies for hazard identification, hazard characterization, exposure plantsIn general, that have DNA been alterations used for centuries. by recombinant However, technology GMO evaluation are far evaluation procedures? As with any new technology, are we just procedures are more rigorous than the accepted and established thereluctant stand toof theembrace United this States boon that of scienceGMOs are in safespite with of our their success current to procedures used to evaluate pesticides and products of conven- date in preventing any negative impact on the environment?

GMOs rests in whether or not the current evaluation methods are consumerstional plant morebreeding wary (EPA and 2008b).skeptical A about lack of such knowledge products. about how adequateUntil these to protect questions the environment are more clearly and answered, consumers. the debate over recombinantIndustries DNAhave technologya tremendous works incentive or how to itensure is evaluated that there makes are no unacceptable long-term impacts of their products. Consequently, Acknowledgements I would like to thank Dr. Held for reading my earlier drafts and by various regulatory agencies. In fact, it is our contention that risk providing suggestions and corrections. additionalassessments internal for most evaluations GMOs tend build to be upon excessive, the requirements going well definedbeyond the data required, which amounts to “overkill.” Such redundancies ▲Pro Position in regulatory frameworks mainly arise because of case-by-case Jaime Fuest, Shakunthala Nair, Krishnareddy Bayyareddy, and Shimat V. Joseph Jamie Fuest, J., Nair, S., Bayyareddy, K., Joseph, S.V., and L.P. system, but it comes at a cost. When additional data are demanded, Guillebeau evaluationit neither increases of GM products. available Some information redundancy about benefits the safetythe regulatory of a GM

Thus, we argue that GMO regulation is dynamic; its procedures University of Georgia product nor improves public confidence (McHughen 2007). Following their commercialization in 1995, 308.75 million acres growing knowledge and experience (Conner et al. 2003). Stringent worldwide (James 2007). Such widespread adoption of this revo- vary spatially and temporally on a case-by-case basis and reflect (39.34% of global total crop acreage) of GM crops have been planted evaluations with numerous components and integration of extensive lutionary technology reflects a high degree of conviction about the term protection of human health and the environment. - efforts by multiple agencies and industries assure adequate long- benefits and safety of GM products. There have been no scientifically documented cases of adverse effects on human health or the environ Acknowledgements ment from any product of recombinant DNA technology approved by We would like to thank our faculty advisor Paul Guillebeau for his United States regulatory procedures (McHughen and Smyth 2008). time, valuable inputs, and dedication in preparing for this debate. TheInsect-resistant successes and associatedGM plants benefitsare derived of GM primarily crops are from a result Bacillus of rigorous and effective evaluation. Athens for funding our participation in the debate. thuringiensis (Bt)-based technology. Bt is a naturally occurring and We also thank the Department of Entomology, University of Georgia, ▼Con Position pesticide application on food crops since 1961 (Milner 1994). Since Jonathan D. Willis, Anais Castagnola, Paul Rhoades, Kristen Abney, ubiquitousits discovery soil in 1901bacterium and the and utilization its δ-endotoxin of its insecticidal has been properties,labeled for and Carl Jones the environmental and human health aspects of Bt have been widely

UniversityCurrently, toof Tennesseedeliberate atoptimum Knoxville mechanisms for evaluating the investigated.(Sayre and Seidler Over 1002005). years of scientific evidence suggest that the - efficacyThe most and non-target publicized incidenteffects ofrelated Bt products to negative are highly consequences predictable of man health and the environment, we address the procedures of the GMOs was the release of StarlinkTM corn into the human food market long-term impact of genetically modified organisms (GMOs) on hu when it had been approved only for animal consumption. Although Agriculture, the Food and Drug Administration, and other countries’ negative media coverage generated widespread public concern, no Environmental Protection Agency, the United States Department of - 2002). This event spurred improvements in evaluation and enforce- counterpartvate industry, agencies the farming and community, international and organizations national and international influencing adverse quantifiable health consequences were documented (Chassy homelandregulatory practices.bodies as theyContinuous contribute efficacy to the review development of universities, of GMOs pri for Evaluation procedures are designed not only to illuminate the de- the global market is as crucial a priority action as ever. The conse- mentsirable procedures aspects of GM in the crops, United but areStates. also intended to look for potential negative characteristics. When negative characteristics are excluded on suburban, urban, rural, wilderness, and aquatic environments from the marketplace, the evaluation process has served its purpose. worldwide.quences of recombinant Revolutionizing DNA the technology pesticide have industry, an ecological GMOs became impact For instance, voluntary cancellations of products undergoing evaluation a part of an arsenal of tools available to integrated pest manage- are common, and conditional or time-limited registrations indicate that products are still under an additional level of control or scrutiny. These types of registration ensure that evaluation is ongoing and facilitate increasingment systems part intended of daily diets.to enhance We reviewed food and the fiber existing yields. regulatory Globally, active observations that address product quality and safety at regular proceduresfood crops modifiedwhich inadequately through recombinant take into account methods various comprise biological an time intervals. The fact that very few pesticides are under time-limited risk factors and concluded that the current evaluation procedures are registration indicates the elevated level of scrutiny for GM products, demonstrating that they are not indiscriminately approved (EPA of GMOs on human health and the environment. notSubstantial sufficiently equivalenceextensive enough is the to current appropriately standard assess to measure the impact the safety of GMOs. This methodology persists as a standard measure- 2008a). Exclusion of some products with undesirable characteristics shouldAmerican not Entomologist condemn all • recombinant DNA technology. 111 Volume 56, Number 2 ment despite improper evaluation of unexpected downstream gene patterns of pesticide use. Science 292 expression events (Levidow et al. 2007). Microarray data testing Carvalho, F.P. 2006. Agriculture, pesticides, food security and food safety. : 637-638. Cerda, H., A. H. Sayyed, D. J. Wright. 2006. Diamondback moth resistance toEnviron. Bacillus Sci. thuringiensis Policy 9: 685-92. eachexpression other thanlevels other of MON810 non-trans insertion gene lines events used of toCry1Ab compare Bt toxingene demonstrated that transgenic modified lines were more similar to Chandler, S. and J.M. Dunwell. transgenic 2008. canola: evaluation of refugia size with thenon-recessive environmental resistant release insects. of transgenic J. Appl. Entomol. plants. 130: Crit. 421-5. Rev. Plant Sci. Gene flow, risk assessment and newexpression technologies (Coll et createsal 2008). the Substantial need for equivalencenew evaluation as an procedures evaluation parameter allowed the GMO industry to flourish, but the advent of Chassy, B. M. 2002. Food safety evaluation of crops produced through (Domingo 2007). 27:25-49. - Christophides, G. K. 2005. Transgenic mosquitoes and malaria transmis- biotechnology. J. Am. Coll. Nutr. 21: 166S-173S. Unintentional gene expression events do occur, creating diges Christophides, G. K., L. C. Gouagna, M. Jacobs-Lorena, A. A. James, and K. Olson.sion. Cell. 2006. Microbiol. 7: 325-333. isolines,tive and themorphological Bt lines were consequences. found to be higher In the in case lignin of content,corn modified which What are relevant assays for refractoriness? pp. 165-170. tocan produce lead to decreased Bt Cry1Ab digestibility in three different (Deepak insertion and Stotzky events 2001). vs. non-BtFeed- ing trials with Roundup-ready soybean performed on Wistar rats In B.G.J. Knols and C. Louis (eds.) Bridging laboratory and field research resulted in a higher rate of stillbirths and lower birth weights. These Coll,for A., genetic A. Nadal, control M. of Palaudelmas, disease vectors. J. Messeguer,Wageningen URE. Mele, Frontis P. Series.Puig- domenech,Springer. Dordrecht, M. Pla. 2008.Netherlands. testes (Moch 2006). Another study using Snowdrop lectin, a protein Lack of repeatable differential expression mice also showed cellular modifications to the liver, pancreas, and with insecticidal capabilities engineered into potato, caused growth Conner,patterns A. J., between T. R. Glare, MON810 and J. and P. Nap. comparable 2003. The commercial release of varietiesgenetically of stunting and damage to the kidney, thymus, intestine, and immune maize. Plant Mol. Bio. 68:105-117. system. Such studies illustrate the need to reevaluate the current modified crops into the environment. Part II. Overview of ecological evaluation procedures. Curtis, C. F. 2006. Review of previous applications of genetics to vector risk assessment. PlantIn J. 33: 19-46. Another concern raised by the presence of GMOs in the environ- control. pp. 33-44. B.G.J. Knols and C. Louis (eds.), Bridging laboratory ment is transgene crossover to wild relatives of GMOs. A case of gene de Lamballerie,and field research X., E. forLeroy, genetic R. N. control Charrel, of K.disease Ttsetsarkin, vectors. S. Wageningen Higgs, and E.UR A. Frontis Gould. Series. 2008. Springer. Chikungunya Dordrecht, virus Netherlands. adapts to tiger mosquito via herbivorydrift occurred by insects in a Bt (Snow strain et from al. 2003). a cultivated Spread sunflower of Bt genes line to wildto a wild sunflower strain, which led to increased fecundity and reduced Deepak, S. and G. Stotzky. 2001. Bt corn has higher lignin content than relatives would reduce natural refuge areas that limit increase of evolutionary convergence: a sign of things to come? Virology J. 5:33. resistance emergence in insect pest populations. Domingo, J.L. 2007. GMOs have risen to the forefront of international agriculture, and non-Bt corn. Am. J. Bot. 88: 1704–1706. as important commodities, they require safe utilization to preserve Dunwell, J.M. 2000 .Toxicity Transgenic studies approaches of genetically to crop modified improvement. plants: a review J. Exp. of the published literature. Crit. Rev. Food Sci. Nutr. 47:721-733. market share and human health and to protect non-target organisms (EPA) Environmental Protection Agency. 1998. interacting in a shared ecosystem. The arrival of new genetic moni- The Environmental ProtectionBot. 51: 487-496. Agency’s white paper on Bt plant-pesticide resistance man- toring techniques provides the opportunity to continually increase our safety standards. The aforementioned cases illustrate the need Pollution Prevention Division, Washington, DC. to modify the evaluation procedures to adequately measure the long- (EPA)agement Environmental (EPA Publication Protection 739-S-98-001). Agency. 2008a. U.S. EPA, Current Biopesticides & Previously and 7 Registered Section 3 PIP Registrations. 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American Entomologist • Volume 56, Number 2 113 Special thanks are extended to Dr. Thomas E. Reagan at Louisiana Jordan M. Coburn is a Masters student in the laboratory of Dr. Pete State University for his continued dedication and guidance of the Teel; the primary focus of his research is medical entomology. student debates. He has contributed greatly to the organization of the Andrew W. Boswell is a Masters student in Dr. Spence Behmer’s labo- debates and to manuscript preparation over the past 12 years. ratory, focusing on insect nutritional ecology and physiology. The three separate judge panels, each comprised of three profes- sional scientists, all independently determined that the con position Washington State University for each topic made the better argument. We would like to thank Ashfaq A. Sial Wenatchee WA, where he is studying toxicodynamics and toxico- kinetics of reduced-risk is a Ph.D. student insecticides in Dr. Jay with F. novelBrunner’s modes program of action in Hogsette, Marc Fisher, Ulrich Bernier, Thomas Reagan, Nina Alphey, our judges Dina Fonseca, George Hamilton, Edwin Lewis, Jerome on obliquebanded leafroller. Nik Wiman and Eileen Cullen for volunteering their time and efforts. WSU Tree Fruit Research and Extension Center, where he works Oregon State University on Tachinidae is a Ph.D. as natural student enemies in Dr. Vincent of leafroller P. Jones spp. laboratory at the Kimberly M. Skyrm is a Ph.D. student working with Sujaya Rao Jeremy L. Buchman on the foraging behavior of native bumble bees in agricultural laboratory at USDA Yakima Agricultural Research Laboratory ecosystems. Wapato, WA, where is hean worksM.S. student on viruses in Dr. vectored Joseph E. by Munyaneza’s insect pests Jennifer E. Bergh is an M.S. student studying native bee ecology in of potato. wetland and agricultural ecosystems with Sujaya Rao. Bonnie Ohler is an M.S. student in Dr. Peter Landolt’s laboratory at USDA Yakima Agricultural Research Laboratory, Wapato WA, Purdue University where she studies chemical ecology of insect pests of tree fruits. Gladys K. Andino is a Ph.D. student in Greg Hunt’s lab, where she studies the genetics of honey bees. Mississippi State University Victoria Caceres is a Ph.D. student in Doug Richmond’s lab, where Cheri Abraham completed his M.S. at Mississippi State University working with Dr. David Held on Larra bicolor, the parasitoid on and sulfur on trophic interactions in turfgrass ecosystems. Scapteriscus mole crickets. He is currently at the University of Gloriashe I.studies Giraldo-Calderón the effect of isvarying a Ph.D. ratios student of innitrogen, Dr. Catherine phosphorus Hill’s Georgia studying in Dr. Kris Braman’s lab. lab, working on mosquito vision. Julia Prado is a Ph.D. student in Cliff Sadof´s lab, where she University of Georgia develops an integrated approach to managing red maples to avoid Jaime Fuest is a Ph.D. student working under the direction of D. Horton on the ecology and management of peach tree borers outbreaks of secondary pests. (Sesiidae) in peach systems. Kapil Raje Shakunthala Nair is a Ph.D. student working with S. Kristine Braman Virginia Ferris’ labs, where he works in molecular phylogenetics is a Ph.D. student in both Dr. Jeffrey Holland and Dr. on the pest status of lace bugs on ornamental plants. of Cerambicidae. Krishna Bayyareddy is a Ph.D. student in M. Adang’s lab and stud- Janice Van Zee is a Ph.D. student in Dr. Catherine Hill’s lab, working ies the Bt toxin receptors in the mosquito midgut that determine with tick cytogenetics and genomics. Shimat V. Joseph is pursuing a Ph.D. and his research focuses on Pennsylvania State University managementmosquitocidal strategies specificity. to reduce hemlock woolly adelgid, Adelges Dan Schmehl tsugae (Adelgidae) damage under the direction of S. K. Braman

Beth Irwin is is a a Ph.D. Ph.D. student inin Jim Consuelo Frazier’s De lab, Moraes where heand studies Mark theMescher’s sublethal laboratory, effects ofwhere pesticides she studieson the plant-symbiontEuropean Honeybee. inter- Universityand J. L. ofHanula. Tennessee at Knoxville actions. Jonathan Willis Tom Bentley is a Ph.D. student in Mark Mescher’s lab, where he identifying novel cellulolytic enzymes from insects. studies interactions between plant viruses, host plants, and Anais Castagnola is an M.S. student in Dr. Juan-Luis Jurat-Fuentes lab, insect vectors. physiology lab. Her project’s focus is insect midgut epithelial cell Rob Anderson is a Ph.D. candidate in Matt Thomas’ lab, where interactions and isthe an discovery M.S. student of novel in Dr.growth Jurat-Fuentes factors. insect Paul Rhoades is an M.S. student studying the pollination biology of competence of medically important insects. Amandahe studies Bachmann the effects is aof Ph.D. entomopathogenic candidate working fungi withon the Shelby vector and Bob Trigiano. Kristinthe flowering Abney is dogwoodan M.S. student with Drs. in Dean John Kopsell’sSkinner, Bill lab, Klingeman, where she studies secondary plant metabolites and phytonutrients. UniversityFleischer of on Wisconsin field crop pest population movement. David Coyle studies the ecology and impact of invasive root-feeding weevils Dr. Anne L. Nielsen is a postdoctoral researcher in Edwin Lewis’ lab at UC is a Ph.D. student with Dr. Kenneth Raffa, where he Davis, where her research focuses on abiotic factors impacting entomopathogenic nematodes used for biological control in greenhouses. She completed her Ph.D. in 2008 at Rutgers University on the population ecology of an on forest composition and fine root dynamics. Texas A&M University invasive stink bug species. Lt. Roxanne G. Burrus is a Ph.D. candidate at Aubrey M. Colvin is a Masters student in the laboratory of Dr. Robert the University of Florida, where her research focuses on isolating Escherichia Wharton. The focus of her research is the phylogenetic systemat- coli ics of Metopius (Hymenoptera: Ichneumonidae). Therese A. Catanach These O157:H7 two factors human will pathogenic be considered bacteria together from houseto estimate flies at the dairy potential farms, roleand Woolley; the focus of her research is the phylogenetic systematics determining the dispersal distances of house flies from dairies into town. of Xyphon (Hemiptera: is a masters Cicadellidae). student in that laboratory of Dr. Jim proximities to dairies. that house flies have in transmitting this disease to humans that live in close 114 American Entomologist • Summer 2010