Environmental Risk Assessment of Transgenic Plants Using

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honey bees 18 21 as has behavioural disturbances 20 21 Acute toxicity is seldom. seen in insects 3 and not in honey bees 22 By 1998 at least 14 different PI genes had. successfully been introduced into crop plants 3 One of these the Kunitz Soybean. Trypsin Inhibitor SBTI a serine proteinase inhibitor is reported engineered into potato. and tobacco 23 Honey bees have serine proteinases as digestive enzymes 24 SBTI. may therefore have an impact on honey bee protein digestion and thus especially on. larval development,II Materials and methods, Expression levels of transgenes in GM plants vary according to plant tissue and. species 3 We chose 0 1 and 1 0 SBTI as realistic low and high expression levels. respectively 4 and investigated the juvenile development mortality and adult body mass. with larval diets containing 0 1 or 1 0 w w SBTI of total protein A control group was. fed with a larval diet containing 1 0 w w Bovine Serum Albumin BSA We did not. include the fact that nectar is dehydrated when it is converted into honey in the bee hive. and that this process increase the protein content in the honey that is fed to the larvae in. situ compared to the protein content in secreted nectar. The larvae were reared using the method by Br dsgaard et al 13 with the. modifications that the larvae were reared in sterile tissue culture multi wells 16 2 mm. and grafted daily to new wells with food Handling was hereby reduced to one time per day. with no additional feeding 25 Pure SBTI and BSA were obtained from Sigma St Louis. USA and mixed into the standard food 26 in concentrations of 0 1 and 1 0 w w of. total protein content in the food The larvae and pupae were monitored once daily until. adult emergence Larval and pupal stage as well as survival were noted Larval. development time was calculated at the LS stage 27 the larvae stop feeding and. defecate in this stage to begin pupation and at adult emergence The newly emerged. adults were weighed to investigate differences in body mass. III Results and discussion, Comparison of the present study with previous experiments 13 and unpublished. results suggests that the addition of BSA to the standard food does not change bee. development time or mortality Our experiments suggest that larval development will be. affected in several ways if the larval food contain SBTI Table 1 Significantly slower. juvenile development was observed if the food contained 1 0 SBTI The increased. development time was evident both in the feeding stages until LS and the non feeding. stages LS to adult Development times were not significantly influenced by 0 1 SBTI. Juvenile mortality was significantly increased when larvae were fed 1 0 SBTI compared. to the control fed 1 0 BSA A dose response relationship of SBTI has also been reported. for adult longevity of both honey bees 17 20 and bumble bees 28 The wet body mass. of newly emerged adults was significantly lower when the larvae were fed 1 0 SBTI. whereas 0 1 SBTI in the larval food did not have an effect on adult mass Reduction of. mass gain due to PIs in the food is also reported for other insect herbivores 15 29 The. consequences of smaller adult bees will probably be that these surviving bees will have. reduced performance as adults regardless of their food intake as adults. IV Conclusion, Adult worker honey bees mainly eat pollen as nurse bees with a peak in pollen. intake at day nine after emerging The pollen intake and thus amount and type of. digested protein is correlated to the developmental status of the hypopharyngeal glands. 30 31 The secretions of these glands are important components of the larval food It is. therefore likely that nurse bees that ingest PIs will be poorer producers of larval food both. in terms of quantity and quality Hence not only will the longevity and learning ability of. adult bees be reduced 17 20 affecting their performance as forager bees if they are. influenced by a SBTI containing pollen or nectar source they will probably also be sub. optimal tenders of larvae as nurse bees A crop expressing SBTI in a 1 0 concentration. in pollen or nectar will therefore have both a direct impact on honey bee larvae through. digestive inhibition resulting in increased development time increased juvenile mortality. and individuals surviving to adulthood being smaller and an indirect impact through. nourishment depletion through affected nurse bees The in vitro rearing technique. presented here makes it possible to monitor individual larval development and we suggest. that this should be included in an environmental risk assessment procedure before. releasing transgenic plants for field planting,V Acknowledgments. We thank Lene H Andersen P Asger Marthin and Ulla Sandberg for technical. assistance,REFERENCES, 1 T H Schuler G M Poppy B R Kerry I Denholm Trends Biotechnol 17 210 1999.
2 L L Wolfenbarger P R Phifer Science 290 2088 2000. 3 T H Schuler G M Poppy B R Kerry I Denholm Trends Biotechnol 16 168 1998. 4 L Jouanin et al Plant Science 131 1 1998, 5 A H Hilder D Boulter Crop Protection 18 177 1999. 6 EU Official Journal L 117 08 05 1990 15 1990,7 USDA APHIS Technical Bulletin 1783 1991. 8 J B Free Insect pollination of crops Academic Press London 1993. 9 S E McGregor Insect pollination of cultivated plants Agriculture Handbook no 496. Agricultural Res Serv USDA 1976, 10 P C Jepson B C Croft G E Pratt Mol Ecol 3 81 1994. 11 EPPO EPPO Standards Guideline for the efficacy evaluation of plant products 1 161 1999. 12 C J Br dsgaard H Hansen W Ritter J Apicult Res 39 19 2000. 13 C J Br dsgaard W Ritter H Hansen Apidolologie 29 569 1998. 14 C A Ryan Annu Rev Phytopathol 28 939 1990, 15 R M Broadway S S Duffy J Insect Physiol 32 827 1986. 16 G L Orr J A Strickland T A Walsh J Insect Physiol 40 893 1994. 17 E P J Burgess L A Malone J T Christeller J Insect Physiol 42 823 1996. 18 L A Malone H A Giacon E P J Burgess J Z Maxwell J T Christeller W A Laing J. Econ Entomol 88 46 1995, 19 L A Malone E P J Burgess J T Christeller H S Gatehouse J Insect Physiol 44.
20 M H Pham Del gue et al Entomol Exp Appl 95 21 2000. 21 C Girard et al Transgenic Research 7 239 1998, 22 L P Belzunces Lenfant S D Pasquale M E Colin Comp Biochem Physiol 109B 63. 23 S Marchetti A Giordana A M Oliviere C Fogher M Delledonne Potato Res 37 450. 24 B B Moritz K Crailsheim J Insect Physiol 33 923 1987. 25 Y S C Peng E Mussen A Fong M A Montague T Tyler J Invert Pathol 60 127 1992. 26 H Rembold B Lackner J Apic Res 20 165 1981,27 H Rembold J P Kremer Apidologie 11 29 1980. 28 L A Malone E P J Burgess D Stefanovic H S Gatehouse Apidologie 31 25 2000. 29 E P J Burgess P S Stevens G K Keen W A Laing J T Christeller Entomol Exp Appl. 61 123 1991, 30 L N Standifer R H MacDonald M D Levin Ann Ent Soc Am 63 909 1970. 31 K Crailsheim et al J Insect Physiol 38 409 1992. Table 1 Development time from egg to LS stage and egg to adult adult body mass and. juvenile mortality of Apis mellifera ligustica L reared in vitro on diets with different. proteinase inhibitor content, Diet Development time Development time Adult body mass Juvenile excessive. to LS stage to adult g SE n mortality N,days SE n days SE n.
Standard 1 0 BSA 9 62a 0 06 188 21 05a 0 16 99 0 138a 0 003 99 4. Standard 0 1 SBTI 9 79a 0 03 312 20 73a 0 17 121 0 139a 0 003 120 11 76 ns 4. Standard 1 0 SBTI 10 29b 0 03 258 22 06b 0 13 74 0 109b 0 002 74 26 39 4. Larval stages L1 to LS are feeding 29, Means not followed by the same letter are significantly different pair wise T tests P 0 0001. Number of individuals, Significant difference from the control group pair wise T tests on arcsine transformed data P 0 05 ns not significant. Number of repetitions,Standard in vitro feed 26,ENVIRONMENTAL RISK ASSESSMENT OF TRANSGENIC. PLANTS USING HONEY BEE LARVAE, Henrik F Br dsgaard Camilla J Br dsgaard Henrik Hansen and G bor L L vei. Research Group Entomology Danish Institute of Agricultural Sciences. Research Centre Flakkebjerg DK 4200 Slagelse Denmark. Fax 45 58 11 33 01 email hfb bigfoot com,Curriculum Vitae.
Name Camilla J Br dsgaard, Education M Sc in Biology Ph D in Honeybee Pathology. Present Employment Senior Scientist at Danish Institute of Agricultural Science Department of. Crop Protection Research Group Entomology,Years with Institution 10 years. Key Qualifications, My research experience is focused on the biology of Paenibacillus larvae larvae causing AFB and. the ectoparasitic mite Varroa destructor drug free control of bee diseases and pollination research. management and planning During my Ph D study I developed a laboratory method for testing of. larval and adult bee resistance towards AFB The method is now used for testing different Danish. bee strains resistance levels to AFB and possible impacts of GMOs on larval development. Furthermore I have assisted in administration of the statutory control of bee diseases and bee. disease diagnosis I have participated in training of beekeepers in bee diseases and teaching. beekeeping advisors and students,For further information please cf my homepage at. ENVIRONMENTAL RISK ASSESSMENT OF TRANSGENIC PLANTS USING HONEY BEE LARVAE Henrik F Br dsgaard Camilla J Br dsgaard Henrik Hansen and G bor L L vei Research Group Entomology Danish Institute of Agricultural Sciences Research Centre Flakkebjerg DK 4200 Slagelse Denmark Fax 45 58 11 33 01 email hfb bigfoot com Abstract An environmental concern regarding the cultivation of

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