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Dispersal of viable row-crop seeds of commercial agriculture by farmland birds: implication for genetically modified crops

Published online by Cambridge University Press:  16 December 2008

John L. Cummings
Affiliation:
U.S. Department of Agriculture, Animal and Plant Health Inspection Service, Wildlife Services, National Wildlife Research Center, 4101 LaPorte Avenue, Fort Collins, CO 80521, USA
Levis W. Handley
Affiliation:
U.S. Department of Agriculture, Animal and Plant Health Inspection Service, Biotechnology Regulatory Services, 4700 River Road, Riverdale, MD 20737, USA
Bruce Macbryde
Affiliation:
U.S. Department of Agriculture, Animal and Plant Health Inspection Service, Biotechnology Regulatory Services, 4700 River Road, Riverdale, MD 20737, USA
Shelagh K. Tupper
Affiliation:
U.S. Department of Agriculture, Animal and Plant Health Inspection Service, Wildlife Services, National Wildlife Research Center, 4101 LaPorte Avenue, Fort Collins, CO 80521, USA
Scott J. Werner
Affiliation:
U.S. Department of Agriculture, Animal and Plant Health Inspection Service, Wildlife Services, National Wildlife Research Center, 4101 LaPorte Avenue, Fort Collins, CO 80521, USA
Zachary J. Byram
Affiliation:
U.S. Department of Agriculture, Animal and Plant Health Inspection Service, Wildlife Services, National Wildlife Research Center, 4101 LaPorte Avenue, Fort Collins, CO 80521, USA

Abstract

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To address some concerns about the expansion of genetically engineered pharmaceutical and industrial crops to outdoor plantings and potential impacts on the human food supply, we determined whether commercial agriculture seeds of maize or corn Zea mays L., barley Hordeum vulgare L., safflower Carthamus tinctorius L. and rice Oryza sativa L. are digested or pass viably through the digestive tract, or are transported externally, by captive mallard ducks Anas platyrhynchos L., ring-necked pheasants Phasianus colchicus L., red-winged blackbirds Agelaius phoeniceus (L.) and rock pigeons Columba livia Gmelin (with the exception of whole maize seeds which were too large to feed to the blackbirds). These crop seeds, whether free-fed or force-fed, did not pass through the digestive tract of these bird species. The birds nonetheless did retain viable seeds in the esophagus/crop and gizzard for several hours. For example, after foraging for 6 h, mallards had retained an average of 228 ± 112 barley seeds and pheasants 192 ± 78 in the esophagus/crop, and their germination rates were 93 and 50%, respectively. Birds externally transported seeds away from the feeding location, but in only four instances were seeds found attached to their muddy feet or legs and in no case to feathers. Risk of such crop seeds germinating, establishing and reproducing off site after transport by a bird (externally or internally) or movement of a carcass by a predator, will depend greatly on the crop and bird species, location, environmental conditions (including soil characteristics), timing, and seed condition.

Type
Research Article
Copyright
© ISBR, EDP Sciences, 2008

References

APHIS/BRS (USDA Animal and Plant Health Inspection Service, Biotechnology Regulatory Services) (2007) Draft Guidance for APHIS Permits for Field Testing or Movement of Organisms with Pharmaceutical or Industrial Intent. USDA/APHIS/BRS, Riverdale, Maryland, 42 p, http://www.aphis.usda.gov/brs/pdf/Pharma_Guidance.pdf
Bellrose FC, Sieh JG (1960) Massed waterfowl flights in the Mississippi flyway, 1956 and 1957. Wilson Bull. 72: 29–59
Bent AC (1932/1963) Life Histories of North American Gallinaceous Birds. Smithsonian Institution, U.S. National Museum Bull. 162 / Dover Publications, New York, 490 p
Bent AC (1958/1965) Life Histories of North American Blackbirds, Orioles, Tanagers, and Allies. Smithsonian Institution, U.S. National Museum Bull. 211 / Dover Publications, New York, 549 p
Bernhardt GE, Van Allsburg L, Dolbeer RA (1987) Blackbird and starling feeding behavior on ripening corn ears. Ohio J. Sci. 87: 125–129
Brugger KE, Dolbeer RA (1990) Geographic origin of red-winged blackbirds relative to rice culture in southwestern and southcentral Louisiana. J. Field Ornithol. 61: 90–97
Chakauya E, Chikwamba R, Rybicki EP (2006) Riding the tide of biopharming in Africa: considerations for risk assessment. South African J. Sci. 102: 284–288
Charalambidou, I, Santamaría, L (2002) Waterbirds as endozoochorous dispersers of aquatic organisms: a review of experimental evidence. Acta Oecol. 23: 165176 CrossRef
Charalambidou I, Santamaría L, Langevoord O (2003) Effect of ingestion by five avian dispersers on the retention time, retrieval and germination of Ruppia maritima seeds. Functional Ecol. 17: 747–753
Charalambidou I, Santamaría L, Jansen C, Nolet BA (2005) Digestive plasticity in mallard ducks modulates dispersal probabilities of aquatic plants and crustaceans. Functional Ecol. 19: 513–519
Clark RG, Gentle GC (1990) Estimates of grain passage time in captive mallards. Canad. J. Zool. 68: 2275–2279
Clausen P, Nolet BA, Fox AD, Klaassen M (2002) Long-distance endozoochorous dispersal of submerged macrophyte seeds by migratory waterbirds in northern Europe – a critical review of possibilities and limitations. Acta Oecol. 23: 191–203
Cooke WW (1940) Bird Migration. U.S. Dept. Agric. Bull. 185: 1–47
Cummings JL, Shwiff SA, Tupper SK (2005) Economic impacts of blackbird damage to the rice industry. In Nolte DL and Fagerstone KA, eds, Proceedings of the 11th Wildlife Damage Management Conference, Wildlife Damage Management Working Group of The Wildlife Society, Fort Collins, Colorado, pp 317–322
Dalal M, Dani RG, Kumar PA (2006) Current trends in the genetic engineering of vegetable crops. Sci. Hort. 107: 215–225
Desai BB (2004) Seeds Handbook: Biology, Production, Processing, and Storage, 2nd edn, Marcel Dekker, New York, 787 p
DeVault, TL, Rhodes, OE Jr, Shivik, JA (2003) Scavenging by vertebrates: behavioral, ecological, and evolutionary perspectives on an important energy transfer pathway in terrestrial ecosystems. Oikos 102: 225234 CrossRef
Dill HH (1969) A Field Guide to Cannon Net Trapping. U.S. Department of the Interior, Bureau of Sport Fisheries and Wildlife, 18 p
Dolbeer, RA (1978) Movement and migration patterns of red-winged blackbirds: a continental overview. Bird-Banding 49: 1734 CrossRef
Einsiedel, EF, Medlock, J (2005) A public consultation on plant molecular farming. AgBioForum 8: 2632
Elbehri, A (2005) Biopharming and the food system: examining the potential benefits and risks. AgBioForum 8: 1825
EPA (United States Environmental Protection Agency) (1996) Ecological Effects Test Guidelines: OPPTS 850.4100 Terrestrial Plant Toxicity, Tier I (Seedling Emergence). EPA 712-C-96-153, 6 p
Figuerola J, Green AJ (2002a) Dispersal of aquatic organisms by waterbirds: a review of past research and priorities for future studies. Freshwater Biol. 47: 483–494
Figuerola J, Green AJ (2002b) How frequent is external transport of seeds and invertebrate eggs by waterbirds? A study in Doñana, SW Spain. Archiv. Hydrobiol. 155: 557–565
Figuerola J, Green AJ, Santamaría L (2002) Comparative dispersal effectiveness of wigeongrass seeds by waterfowl wintering in south-west Spain: quantitative and qualitative aspects. J. Ecol. 90: 989–1001
Figuerola J, Green AJ, Santamaría L (2003) Passive internal transport of aquatic organisms by waterfowl in Doñana, south-west Spain. Global Ecol. Biogeogr. 12: 427–436
Fischer R, Stoger E, Schillberg S, Christou P, Twyman RM (2004) Plant-based production of biopharmaceuticals. Current Opinion Plant Biol. 7: 152–158
Floss DM, Falkenburg D, Conrad U (2007) Production of vaccines and therapeutic antibodies for veterinary applications in transgenic plants: an overview. Transgenic Res. 16: 315–332
Freese B, Hansen M, Gurian-Sherman D (2004) Pharmaceutical Rice in California: Potential Risks to Consumers, the Environment and the California Rice Industry. Friends of the Earth (FOE), Center for Food Safety, Consumers Union, and Environment California, FOE, Washington, DC, 19 p
Gepts P (2004) Crop domestication as a long-term selection experiment. Plant Breed. Rev. 24: 1–44
Goldstein DA, Thomas JA (2004) Biopharmaceuticals derived from genetically modified plants. QJM: Internat. J. Med. 97: 705–716
Green, AJ, Figuerola, J, Sánchez, MI (2002) Implications of waterbird ecology for the dispersal of aquatic organisms. Acta Oecol. 23: 177189 CrossRef
Gressel J, ed (2005) Crop Ferality and Volunteerism. CRC Press, Boca Raton, Florida, USA, 422 p
Han, M, Su, T, Zu, Y-G, An, Z-G (2006) Research advances on transgenic plant vaccines. Acta Genetica Sinica 33: 285293 CrossRef
Herdt RW (2006) Biotechnology in agriculture. Annual Rev. Environ. Resour. 31: 265–295
Holland JM, Hutchison MAS, Smith B, Aebischer NJ (2006) A review of invertebrates and seed-bearing plants as food for farmland birds in Europe. Annals Appl. Biol. 148: 49–71
Howard JA, Hood EE (2007) Methods for growing nonfood products in transgenic plants. Crop Sci. 47: 1255–1262
Knittle CE, Linz GM, Johns BE, Cummings JL, Davis JE, Jaeger MM (1987) Dispersal of male red-winged blackbirds from two spring roosts in central North America. J. Field Ornithol. 58: 490–498
Ma JK-C, Chikwamba R, Sparrow P, Fischer R, Mahoney R, Twyman RM (2005) Plant-derived pharmaceuticals – the road forward. Trends Plant Sci. 10: 580–585
Malone CR (1965) Dispersal of plankton: rate of food passage in mallard ducks. J. Wildl. Managem. 29: 529–533
Manley SW, Kaminski RM, Reinecke KJ, Gerard PD (2004) Waterbird foods in winter-managed ricefields in Mississippi. J. Wildl. Managem. 68: 74–83
Martin AC, Zim HS, Nelson AL (1951/1961) American Wildlife and Plants: A Guide to Wildlife Food Habits. McGraw-Hill Book Co., New York/Dover Publications, New York, 500 p
Mascia PN, Flavell RB (2004) Safe and acceptable strategies for producing foreign molecules in plants. Current Opinion Plant Biol. 7: 189–195
McAtee, WL (1947) Distribution of seeds by birds. Amer. Midland Naturalist 38: 214223 CrossRef
Mewett O, Johnson H, Holtzapffel R (2007) Plant Molecular Farming in Australia and Overseas. Bureau of Rural Sciences, Australian Government, Canberra, xvi + 47 p
Moschini GC (2006) Pharmaceutical and industrial traits in genetically modified crops: coexistence with conventional agriculture. Amer. J. Agric. Econ. 88: 1184–1192
Mueller, MH, van der Valk, AG (2002) The potential role of ducks in wetland seed dispersal. Wetlands 22: 170178 CrossRef
Murphy DJ (2007) Improving containment strategies in biopharming. Plant Biotech. J. 5: 555–569 + Tables S1–S3 (17 p)
Nathan R, Muller-Landau HC (2000) Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends Ecol. Evol. 15: 278–285
Nelms CO, Twedt DJ (1996) Seed deterioration in flooded agricultural fields during winter. Wildl. Soc. Bull. 24: 85–88
Nogales, M, Medina, FM, Valido, A (1996) Indirect seed dispersal by the feral cats Felis catus in island ecosystems (Canary Islands). Ecography 19: 36 CrossRef
Nogales M, Quilis V, Medina FM, Mora JL, Trigo LS (2002) Are predatory birds effective secondary seed dispersers? Biol. J. Linnean Soc. 75: 345–352
NRC (Committee on Environmental Impacts Associated with Commercialization of Transgenic Plants, Board on Agriculture and Natural Resources, National Research Council) (2002) Environmental Effects of Transgenic Plants: The Scope and Adequacy of Regulation. National Academies Press, Washington, DC, 342 p
Peterson CA, Lee SL, Elliott JE (2001) Scavenging of waterfowl carcasses by birds in agricultural fields of British Columbia. J. Field Ornithol. 72: 150–159 CrossRef
Peterson RKD, Arntzen CJ (2004) On risk and plant-based biopharmaceuticals. Trends Biotech. 22: 64–66
Pierson TA, Cobb RG, Scanlon PF (1976) Crop contents of rock doves in Virginia. Wilson Bull. 88: 489–490
Pinowski J, Summers-Smith JD, eds (1990) Granivorous Birds in the Agricultural Landscape. Polish Scientific Publishers, Warsaw, 360 p
Pollux BJA, Santamaría L, Ouborg NJ (2005) Differences in endozoochorous dispersal between aquatic plant species, with reference to plant population persistence in rivers. Freshwater Biol. 50: 232–242
Powers KD, Noble RE, Chabreck RH (1978) Seed distribution by waterfowl in southwestern Louisiana. J. Wildl. Managem. 42: 598–605
Proctor, VW (1964) Viability of crustacean eggs recovered from ducks. Ecology 45: 656658 CrossRef
Proctor, VW (1966) Dispersal of desmids by waterbirds. Phycologia 5: 227232 CrossRef
Prosser, P, Hart, ADM (2005) Assessing potential exposure of birds to pesticide-treated seeds. Ecotoxicology 14: 679691 CrossRef
Ridley HN (1930) The Dispersal of Plants Throughout the World. L. Reeve & Company, Ashford, Kent, Great Britain, 744 p
Rose E, Nagel P, Haag-Wackernagel D (2006) Spatio-temporal use of the urban habitat by feral pigeons (Columba livia). Behav. Ecol. Sociobiol. 60: 242–254 + S1 (1 p)
Santamaría L, Charalambidou I, Figuerola J, Green AJ (2002) Effect of passage through duck gut on germination of fennel pondweed seeds. Archiv. Hydrobiol. 156: 11–22 CrossRef
Scheller J, Conrad U (2005) Plant-based material, protein and biodegradable plastic. Current Opinion Plant Biol. 8: 188–196
Sibbald IR (1979) Passage of feed through the adult rooster. Poultry Sci. 58: 446–459 CrossRef
Smallwood M (2006) The impact of genomics on crops for industry. J. Sci. Food Agric. 86: 1747–1754
Sorensen AE (1986) Seed dispersal by adhesion. Annual Rev. Ecol. System. 17: 443–463
Spök A (2007) Molecular farming on the rise – GMO regulators still walking a tightrope. Trends Biotech. 25: 74–82
Stafford JD, Kaminski RM, Reinecke KJ, Manley SW (2006) Waste rice for waterfowl in the Mississippi Alluvial Valley. J. Wildl. Managem. 70: 61–69
Swank WG (1944) Germination of seeds after ingestion by pheasants. J. Wildl. Managem. 8: 223–231
Teli NP, Timko MP (2004) Recent developments in the use of transgenic plants for the production of human therapeutics and biopharmaceuticals. Plant Cell Tissue Organ Cult. 79: 125–145
Traveset A (1998) Effect of seed passage through vertebrate frugivores' guts on germination: a review. Perspectives Plant Ecol. Evol. System. 1: 151–190
Turcek FJ, Kelso L (1968) Ecological aspects of food transportation and storage in the Corvidae. Commun. Behav. Biol., Part A 1: 277–297
UCS (Union of Concerned Scientists) (2006) Position Paper: Pharmaceutical and Industrial Crops. Union of Concerned Scientists, Washington, DC, 23 p
van der Pijl L (1982) Principles of Dispersal in Higher Plants, 3rd edn, Springer-Verlag, Berlin and New York, 215 p
Vander Wall SB (1990) Food Hoarding in Animals. University of Chicago Press, Chicago, 453 p
Wang BC, Smith TB (2002) Closing the seed dispersal loop. Trends Ecol. Evol. 17: 379–385
Warwick SI, Stewart Jr CN (2005) Crops come from wild plants – how domestication, transgenes, and linkage together shape ferality. In Gressel J, ed, Crop Ferality and Volunteerism, CRC Press, Boca Raton, Florida, USA, pp 9–30
Yusibov, V, Rabindran, S, Commandeur, U, Twyman, RM, Fischer, R (2006) The potential of plant virus vectors for vaccine production. Drugs R. D. 7: 203217 CrossRef