Hostname: page-component-8448b6f56d-jr42d Total loading time: 0 Render date: 2024-04-23T21:21:23.146Z Has data issue: false hasContentIssue false

Effects of Bacillus thuringiensis on non-target herbivoreand natural enemy assemblages in tropical irrigated rice

Published online by Cambridge University Press:  15 November 2003

Kenneth G. Schoenly
Affiliation:
Department of Biological Sciences, California State University, Stanislaus, Turlock CA 95382, USA
Michael B. Cohen
Affiliation:
Entomology and Plant Pathology Division, International Rice Research Institute, DAPO Box 7777, Metro Manila, Philippines Current address: Department of Biological Sciences, CW405 Biological Sciences Building, University of Alberta, Edmonton AB T6G 2E9, Canada
Alberto T. Barrion
Affiliation:
Entomology and Plant Pathology Division, International Rice Research Institute, DAPO Box 7777, Metro Manila, Philippines Current address: Biosystematics Unit, International Centre of Insect Physiology and Ecology, PO Box 3072, Nairobi, Kenya
Wenjun Zhang
Affiliation:
Research Institute of Entomology and State Key Lab for Biological Control, Zhongshan University, Guangzhou 510275, P.R. China
Bradley Gaolach
Affiliation:
Washington State University Cooperative Extension, King County, 919 SW Grady Way, Suite 120, Renton WA 98055-2945, USA
Vicente D. Viajante
Affiliation:
Entomology and Plant Pathology Division, International Rice Research Institute, DAPO Box 7777, Metro Manila, Philippines

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Endotoxins from Bacillus thuringiensis (Bt) produced in transgenic pest-resistant Bt crops are generally not toxic to predatory and parasitic arthropods. However, elimination of Bt-susceptible prey and hosts in Bt crops could reduce predator and parasitoid abundance and thereby disrupt biological control of other herbivorous pests. Here we report results of a field study evaluating the effects of Bt sprays on non-target terrestrial herbivore and natural enemy assemblages from three rice (Oryza sativa L.) fields on Luzon Island, Philippines. Because of restrictions on field-testing of transgenic rice, Bt sprays were used to remove foliage-feeding lepidopteran larvae that would be targeted by Bt rice. Data from a 546-taxa Philippines-wide food web, matched abundance plots, species accumulation curves, time-series analysis, and ecostatistical tests for species richness and ranked abundance were used to compare different subsets of non-target herbivores, predators, and parasitoids in Bt sprayed and water-sprayed (control) plots. For whole communities of terrestrial predators and parasitoids, Bt sprays altered parasitoid richness in 3 of 3 sites and predator richness in 1 of 3 sites, as measured by rarefaction (in half of these cases, richness was greater in Bt plots), while Spearman tests on ranked abundances showed that correlations, although significantly positive between all treatment pairs, were stronger for predators than for parasitoids, suggesting that parasitoid complexes may have been more sensitive than predators to the effects of Bt sprays. Species accumulation curves and time-series analyses of population trends revealed no evidence that Bt sprays altered the overall buildup of predator or parasitoid communities or population trajectories of non-target herbivores (planthoppers and leafhoppers) nor was evidence found for bottom-up effects in total abundances of non-target species identified in the food web from the addition of spores in the Bt spray formulation. When the same methods were applied to natural enemies (predators and parasitoids) of foliage-feeding lepidopteran and non-lepidopteran (homopteran, hemipteran and dipteran) herbivores, significant differences between treatments were detected in 7 of 12 cases. However, no treatment differences were found in mean abundances of these natural enemies, either in time-series plots or in total (seasonal) abundance. Analysis of guild-level trajectories revealed population behavior and treatment differences that could not be predicted in whole-community studies of predators and parasitoids. A more conclusive test of the impact of Bt rice will require field experiments with transgenic plants, conducted in a range of Asian environments, and over multiple cropping seasons.

Type
Research Article
Copyright
© ISBR, EDP Sciences, 2003

References

Aguda, RM, Datta, K, Tu, J, Datta, SK, Cohen, MB (2001) Expression of Bt genes under control of different promoters in rice at vegetative and flowering stages. Int. Rice Res. Note. 26: 26-27
Alinia, FB, Ghareyazie, L, Rubia, E, Bennett, J, Cohen, MB (2000) Effect of plant age, larval age, and fertilizer treatment on resistance of a cry1Ab-transformed aromatic rice to lepidopterous stem borers and foliage feeders. J. Econ. Entomol. 93: 484-493. CrossRef
Bazzaz, FA (1975) Plant species diversity in old-field successional ecosystems in southern Illinois. Ecology 56: 485-488 CrossRef
Bender, EA, Case, TJ, Gilpin, ME (1984) Perturbation experiments in community ecology: theory and practice. Ecology 65: 1-13 CrossRef
Bernal, CC, Aguda, RM, Cohen, MB (2002) Effect of rice lines transformed with Bacillus thuringiensis toxin genes on the brown planthopper and its predator Cyrtorhinus lividipennis. Entomol. Exp. Appl. 102: 21-28 CrossRef
Bersier, L-F, Dixon, P, Sugihara, G (1999) Scale-invariant or scale-dependent behavior of the link density property in food webs: A matter of sampling effort? Am. Nat. 153: 676-682 CrossRef
Bottrell, DG, Barbosa, P, Gould, F (1998) Manipulating natural enemies by plant variety selection and modification: a realistic strategy? Annu. Rev. Entomol. 43: 347-367 CrossRef
Carpenter SR (1988) Complex interactions in lake communities. Springer-Verlag, New York
Carpenter, SR (1990) Large-scale perturbations: opportunities for innovation. Ecology 71: 2038-2043 CrossRef
Chow SC, Liu JP (1999) Design and Analysis of Bioavailability and Bioequivalence Studies, 2nd edn. Marcel Dekker, New York
Cohen, JE, Luczak, T (1992) Trophic levels in community food webs. Evol. Ecol. 6: 73-89 CrossRef
Cohen, JE, Schoenly, K, Heong, KL, Justo, HD, Arida, G, Barrion, AT, Litsinger, JA (1994) A food web approach to evaluating the effect of insecticide spraying on insect pest population dynamics in a Philippine irrigated rice ecosystem. J. Appl. Ecol. 31: 747-763 CrossRef
Cohen, MB, Romena, AM, Gould, F (2000) Dispersal by larvae of the stem borers Scirpophaga incertulas (Lepidoptera: Pyralidae) and Chilo suppressalis (Lepidoptera: Crambidae) in plots of transplanted rice. Environ. Entomol. 29: 958-971 CrossRef
Dale, PJ, Clarke, B, Fontes, EMG (2002) Potential for the environmental impact of transgenic crops. Nat. Biotechnol. 20: 567-574
Daniel WW (1990) Applied Nonparametric Statistics, 2nd edn. Houghton-Mifflin, Boston
De Datta SK (1981) Principles and Practices of Rice Production. John Wiley and Sons, New York
De Kraker, J, van Huis, A, Heong, KL, van Lenteren, JC, Rabbinge, R (1999) Population dynamics of rice leaffolders (Lepidoptera: Pyralidae) and their natural enemies in irrigated rice fields in the Philippines. Bull. Entomol. Res. 89: 411-421
Dixon PM, Garrett KA (1994) Statistical issues for field experimenters. In Kendall RJ, Lacher TE Jr, eds, Wildlife Toxicology and Population Modeling: Integrated Studies of Agroecosystems. Lewis Publishers, Boca Raton, pp 439-450
Domingo I, Schoenly K (1998) An improved suction apparatus for sampling invertebrate communities in flooded rice. Int. Rice Res. Note 23(2) 38-39
Feinsinger P (2001) Designing Field Studies for Biodiversity Conservation. The Nature Conservancy and Island Press, Washington
Fitt GP, Wilson LJ (2002) Non-target effects of Bt cotton: a case study from Australia. In Akhurst RJ, Beard CE, Hughes P, eds, Proceedings of the 4th Pacific Rim Conference on Bt and its Environmental Impact Canberra, Australia, October 2001. CSIRO, Canberra, pp 175-182
Gallagher KD, Kenmore PE, Sogawa K (1994) Judicious use of insecticides deter planthopper outbreaks and extend the life of resistant varieties in Southeast Asian rice. In Denno RF, Perfect JT, eds, Planthoppers: Their Ecology and Management. Chapman & Hall, New York, pp 599-614
Goldwasser, L, Roughgarden, J (1997) Sampling effects and the estimation of food-web properties. Ecology 78: 41-54 CrossRef
Gotelli NJ, Graves GR (1996) Null Models in Ecology. Smithsonian University Press, Washington, D.C.
Heong, KL, Aquino, GB, Barrion, AT (1991) Arthropod community structures of rice ecosystems in the Philippines. Bull. Entomol. Res. 81: 407-416 CrossRef
Heong, KL, Aquino, GB, Barrion, AT (1992) Population dynamics of plant- and leafhoppers and their natural enemies in rice ecosystems in the Philippines. Crop Protect. 11: 371-379 CrossRef
Heong, KL, Escalada, MM, Huan, NH, Mai, V (1998) Use of communication media in changing rice farmers' pest management in the Mekong Delta, Vietnam. Crop Protect. 17: 413-425 CrossRef
Heong KL, Schoenly KG (1998) Impact of insecticides on herbivore-natural enemy communities in tropical rice ecosystems. In Haskell PT, McEwen P, eds, Ecotoxicology. Pesticides and Beneficial Organisms. Kluwer Academic Publishers, Boston, pp 381-403
Hilbeck A. (2002) Transgenic host plant resistance and non-target effects. In Letourneau DK, Burrows BE, eds, Genetically Engineered Organisms. Assessing Environmental and Human Health Effects. CRC Press, Boca Raton, pp 167-185
Hurlbert, SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol. Monogr. 54: 187-211 CrossRef
IRRI (1979) IRRI Annual Report for 1979. Manila, Philippines
IRRI (1994) World rice statistics. Manila, Philippines
James FC, Rathbun S (1981) Rarefaction, relative abundance, and diversity of avian communities. Auk 98: 785-800
Khush GS (1989) Multiple disease and insect resistance for increased yield stability in rice. In Progress in Irrigated Rice Research. International Rice Research Institute. Manila Philippines, pp 79-92
Letourneau DK, Burrows BE (2002) Genetically Engineered Organisms. Assessing Environmental and Human Health Effects. CRC, Boca Raton
Likens, GE (1985) An experimental approach for the study of ecosystems. J. Ecol. 73: 381-396 CrossRef
Liu, ZC, Ye, GY, Cui, H, Tu, JM, Datta, K, Datta, SK (2002) Effect of transgenic Bacillus thuringiensis rice on population dynamics of main non-target insect pests and superior species of spiders in the field. Acta Phytophylacica Sinica 29: 138-144 (in Chinese)
Longino, JT, Colwell, RK (1997) Biodiversity assessment using structured inventory: capturing the ant fauna of a tropical rain forest. Ecol. Appl. 7: 1263-1277 CrossRef
Losey JE, Obrycki JJ, Hufbauer RA (2002) Impacts of genetically engineered crops on non-target herbivores: Bt-corn and monarch butterflies as a case study. In Letourneau DK, Burrows BE, eds, Genetically Engineered Organisms. Assessing Environmental and Human Health Effects. CRC Press, Boca Raton, pp 143-165
Martinez, ND, Hawkins, BA, Dawah, HA, Feifarek, BP (1999) Effects of sampling effort on characterization of food-web structure. Ecology 80: 1044-1055
Morin PJ (1999) Community Ecology. Blackwell Science, Oxford
Petras, SF, Casida, LE (1985) Survival of Bacillus thuringiensis spores in soil. Appl. Environ. Microbiol. 50: 1496-1501
Pinnock, DE, Brand, RJ, Milstead, JE (1971) The field persistence of Bacillus thuringiensis spores. J. Invert. Path. 18: 405-411 CrossRef
Reissig WH, Heinrichs EA, Litsinger JA, Moody K, Fiedler L, Mew TW, Barrion AT (1986) Illustrated Guide to Integrated Pest Management in Rice in Tropical Asia. International Rice Research Institute, Los Banos
Savary, S, Willocquet, L, Elazegui, FS, Castilla, NP, Teng, PS (2000) Rice pest constraints in tropical Asia: quantification of yield losses due to rice pests in a range of production situations. Plant Dis. 84: 357-369 CrossRef
Schindler DW (1987) Detecting ecosystem response to anthropogenic stress. Can. J. Fish. Aquat. Sci. 44 (supplement): 6-25
Schindler, DW (1998) Replication versus realism: the need for ecosystem-scale experiments. Ecosystems 1: 323-334 CrossRef
Schoenly, K, Cohen, JE (1991) Temporal variation in food web structure: 16 empirical cases. Ecol. Monogr. 61: 267-298 CrossRef
Schoenly K, Zhang W. (1999a) IRRI Biodiversity Software Series. I. LUMP, LINK, and JOIN: utility programs for biodiversity research. IRRI Technical Bulletin No. 1. Manila (Philippines), International Rice Research Institute, Los Banos
Schoenly K, Zhang W (1999b) IRRI Biodiversity Software Series. V. RARE, SPPDISS, and SPPRANK: programs for detecting between-sample differences in community structure. IRRI Technical Bulletin No. 5. Manila (Philippines), International Rice Research Institute, Los Banos
Schoenly, K, Cohen, JE, Heong, KL, Litsinger, JA, Aquino, GB, Barrion, AT, Arida, G (1996a) Food web dynamics of irrigated rice fields at five elevations in Luzon, Philippines. Bull. Entomol. Res. 86: 451-466 CrossRef
Schoenly K, Cohen JE, Heong KL, Arida GS, Barrion AT, Litsinger JA (1996b) Quantifying the impact of insecticides on food web structure of rice-arthropod populations in a Philippine farmer's irrigated field: a case study. In G. Polis, K. Winemiller, eds, Food Webs: Integration of Patterns and Dynamics. Chapman and Hall, New York, pp 343-351
Schoenly, KG, Justo, HD Jr, Barrion, AT, Harris, MK, Bottrell, DG (1998) Analysis of invertebrate biodiversity in a Philippine farmer's irrigated rice field. Environ. Entomol. 27: 1125-1136 CrossRef
Settele J, Martin K, Achilles T (1993) Philippine rice terraces - investigations into the fauna of a traditional agroecosystem and the effects of agricultural change. In Barthlott W, Naumann CM, Schmidt-Loske K, Schuchmann KL, eds, Animal-Plant Interactions in Tropical Environments. Zoologisches Forschungsinstitut und Museum Alexander Koenig, pp 219-227
Settle, WH, Ariawan, H, Astuti, ET, Cahyana, W, Hakim, AL, Hindayana, D, Lestari, AS, Pajarningsih (1996) Managing tropical rice pests through conservation of generalist natural enemies and alternative prey. Ecology 77: 1975-1988 CrossRef
Shelton, AM, Zhao, JZ, Roush, RT (2002) Economic, ecological, food safety, and social consequences of the deployment of Bt transgenic plants. Annu. Rev. Entomol. 47: 845-881 CrossRef
Simberloff, D (1972) Properties of the rarefaction diversity measurements. Am. Nat. 196: 414-418 CrossRef
Simpson, IC, Roger, PA, Oficial, R, Grant, IF (1993a) Impacts of agricultural practices on aquatic oligochaete populations in ricefields. Biol. Fert. Soils 16: 27-33 CrossRef
Simpson, IC, Roger, PA, Oficial, R, Grant, IF (1993b) Density and composition of aquatic oligochaete populations in different farmers ricefields. Biol. Fert. Soils 16: 34-40 CrossRef
Simpson, IC, Roger, PA, Oficial, R, Grant, IF (1994a) Effects of nitrogen fertilizer and pesticide management on flood-water ecology in a wetland ricefield. II. Dynamics of microcrustaceans and dipteran larvae. Biol. Fert. Soils 17: 138-146 CrossRef
Simpson, IC, Roger, PA, Oficial, R, Grant, IF (1994b) Effects of nitrogen fertilizer and pesticide management on floodwater ecology in a wetland ricefield. III. Dynamics of benthic mollusks. Biol. Fert. Soils 18: 219-227 CrossRef
Spearman, C (1904) The proof and measurement of association between two things. Am. J. Psychol. 15: 72-101 CrossRef
Steidl RJ and Thomas L (2001) Power analysis and experimental design. In Scheiner SM, Gurevitch J, eds, Design and Analysis of Ecological Experiments, 2nd edn. Oxford University Press, Oxford, pp 14-36.
Tu, J, Zhang, G, Datta, K, Xu, C, He, Y, Zhang, Q, Khush, GS, Datta, SK (2000) Field performance of transgenic elite commercial hybrid rice expressing Bacillus thuringiensis $\delta$ -endotoxin. Nat. Biotechnol. 18: 1101-1104
Way MO, Grigarick AA, Litsinger JA, Palis F, Pingali PL (1991) Economic thresholds and injury levels for insect pests of rice. In Heinrichs EA, Miller TA, eds, Rice Insects: Management Strategies. Springer-Verlag, New York, pp. 67-105
West, AW, Burges, HD (1985) Persistence of Bacillus thuringiensis and Bacillus cereus in soil supplemented with grass or manure. Plant Soil 83: 389 CrossRef
Ye, G, Shu, Q, Yao, H, Cui, H, Cheng, X, Hu, C, Xia, Y, Gao, M, Altosaar, I (2001) Field evaluation of resistance of transgenic rice containing a synthetic cry1Ab gene from Bacillus thuringiensis Berliner to two stem borers. J. Econ. Entomol. 94: 271-276 CrossRef
Zar JH (1984) Biostatistical Analysis, 2nd edn. Prentice-Hall, New York