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Bt Proteins Exacerbate Negative Growth Effects in Juvenile Rusty (F. rusticus) Crayfish Fed Corn Diet

  • Molly E. J. West
  • Paul A. MooreEmail author
Article

Abstract

The adoption of genetically modified (GM) crops has occurred rapidly in the United States. The transfer of GM corn byproducts from agricultural fields to nearby streams after harvest is significant and occurs well into the post-harvest year. These corn leaves, stems, and cobs then become a detrital food source for organisms, such as shredders in the stream ecosystem. Considering that the nontarget effects of Bt corn have been observed in some terrestrial organisms, we assessed whether Bt toxins affect an important aquatic organism, juvenile F. rusticus crayfish. Juvenile crayfish were fed six distinct diet treatments: two varieties of Bt corn, two non-Bt controls of herbicide tolerant corn, and two controls: fish gelatin and river detritus. Juveniles were fed these diets while housed in flow-through artificial streams that received natural stream water from a local source. Specific growth rate and survivorship of the crayfish were measured throughout the study. Juveniles fed corn diets grew significantly less and had reduced survival compared with juveniles fed fish gelatin or river detritus diets. Furthermore, juveniles fed one Bt variety of corn (VT Triple Pro®) exhibited significantly less growth than those fed one of the herbicide tolerant varieties (Roundup Ready 2®). Our study shows that corn inputs to streams may be detrimental to the growth and survivorship of juvenile crayfish and that certain Bt varieties may exacerbate these negative effects. These effects on crayfish will have repercussions for the entire ecosystem, because crayfish are conduits of energy between many trophic levels.

Notes

Acknowledgements

The authors thank the members of the Laboratory for Sensory Ecology, Bowling Green State University, for their assistance in collection and care of specimens, as well as for reviewing the manuscript. They also thank the University of Michigan Biological Station for funding through the Mariam P. and David M. Gates Graduate Student Endowment Fund to M.E.J.W. and also for the use of facilities. Lastly, thanks to the Bowling Green State University Faculty Research Committee for a Building Strength Award and a Fulbright Fellowship to P.A.M. for help in funding this project.

References

  1. Aimanova KG, Zhuang M, Gill SS (2006) Expression of Cry1Ac cadherin receptors in insect midgut and cell lines. J Invertebr Pathol 92:178–187Google Scholar
  2. Alcorlo P, Geiger W, Otero M (2008) Reproductive biology and life cycle of the invasive crayfish Procambarus clarkia (Crustacea: Decapoda) in diverse aquatic habitats of South-Western Spain: implications for population control. Found Appl Limnol 173(3):197–212Google Scholar
  3. Bøhn T, Primicerio K, Hessen DO, Traavik T (2008) Reduced fitness of Daphnia magna fed a Bt-transgenic maize variety. Arch Environ Contam Toxicol 55(4):584–592Google Scholar
  4. Bøhn T, Traavik T, Primicerio K (2010) Demographic responses of Daphnia magna fed transgenic Bt-maize. Ecotoxicology 19(2):419–430Google Scholar
  5. Broderick NA, Raffa KF, Handelsman J (2006) Midgut bacteria required for Bacillus thuringiensis insecticidal activity. PNAS 103(41):15196–15199Google Scholar
  6. Broderick NA, Robinson CJ, McMahon MD, Holt J, Handelsman J, Raffa KF (2009) Contributions of gut bacteria to Bacillus thuringiensis—induced mortality vary across a range of Lepidoptera. BMC Biol 7:11Google Scholar
  7. Carreira BM, Dias MP, Rebelo R (2014) How consumption and fragmentation of macrophytes by the invasive crayfish Procambarus clarkia shape the macrophyte communities of temporary ponds. Hydrobiologia 721(1):89–98Google Scholar
  8. Celada JD, Fuertes JB, Carral JM, Saez-Royuela M, Gonzalez-Rodriguez A (2013) Effects of vitamin A inclusion in practical diets on survival and growth of juvenile crayfish (Pacifastacus leniusculus Dana, Astacidae) from the onset of exogenous feeding. Aquac Nutr 20:213–218Google Scholar
  9. Chambers PA, Hanson JM, Burke JM, Prepas EE (1990) The impact of the crayfish Orconectes virilis on aquatic macrophytes. Freshw Biol 24(1):81–91Google Scholar
  10. Chambers CP, Whiles MR, Rosi-Marshall EJ, Tank JL, Royer TV, Griffiths NA, Evans-White MA, Stojak AR (2010) Responses of stream macroinvertebrates to Bt maize leaf detritus. Ecol Appl 20(7):1949–1960Google Scholar
  11. Creed RP Jr., (1994) Direct and indirect effects of crayfish grazing in a stream community. Ecology 75(7):2091–2103Google Scholar
  12. Creed RP Jr., Reed JM (2004) Ecosystem engineering by crayfish in a headwater stream community. J N Am Benthol Soc 23(2):224–236Google Scholar
  13. Crickmore N (2005) Using worms to better understand how Bacillus thuringiensis kills insects. Trends Microbiol 13:347–350Google Scholar
  14. Dalzell BJ, Filley TR, Harbor JM (2005) Flood pulse influences on terrestrial organic matter export from an agricultural watershed. J Geophys Res 110:G02011Google Scholar
  15. DiDonato GT, Lodge DM (1993) Species replacements among Orconectes crayfishes in Wisconsin lakes: the role of predation by fish. Can J Fish Aq Sci 50:1484–1488Google Scholar
  16. Dissanayake A, Galloway TS, Jones MB (2008) Physiological responses of juvenile and adult shore crabs Carcinus maenas (Crustacea: Decapoda) to pyrene exposure. Mar Environ Res 66(4):445–450Google Scholar
  17. Dorn NJ, Mittelbach GG (1999) More than predator and prey: a review of interactions between fish and crayfish. Vie Milieu 49:229–237Google Scholar
  18. Dorn NJ, Wojdak JM (2004) The role of omnivorous crayfish in littoral communities. Commun Ecol 140:150–159Google Scholar
  19. Dubois NR, Dean DH (1995) Synergism between Cry1A insecticidal crystal proteins and spores of Bacillus thuringiensis, other bacterial spores, and vegetative cells against Lymantria dispar (Lepidoptera: Lymantriidae) Larvae. Environ Entomol 24(6):1741–1747Google Scholar
  20. Elvira B, Nicola GG, Almodovar A (1996) Pike and red swamp crayfish: a new case on predator–prey relationship between aliens in central Spain. J Fish Biol 48:437–446Google Scholar
  21. Figueiredo MSRB, Anderson AJ (2003) Ontogenetic changes in digestive proteases and carbohydrases from the Australian freshwater crayfish, redclaw Cherax quadricarinatus (Crustacea, Decapoda, Parastacidae). Aquac Res 34(13):1235–1239Google Scholar
  22. Firbank LG, Heard MS, Woiwod IP, Hawes C, Haughton A, Champion GT, Scott RJ, Hill MO, Dewar AM, Squire GR, May MJ, Brooks DR, Bohan D, Daniels RE, Osborne JL, Roy DB, Black H, Rothery P, Perry JN (2003) An introduction to the farm-scale evaluations of genetically modified herbicide-tolerant crops. J Appl Ecol 40:2–16Google Scholar
  23. Galeotti P, Rubolini D, Fea G, Ghia D, Nardi PA, Gherardi F, Fasola M (2006) Female freshwater crayfish adjust egg and clutch size in relation to multiple male traits. Proc Biol Sci 273(1590):1105–1110Google Scholar
  24. Goddard JS, Al-Yahyai DSS (2001) Chemical and nutritional characteristics of dried sardine silage. J Aquat Food Prod Technol 10(4):39–50Google Scholar
  25. Gómez I, Sánchez J, Muñoz-Garay C, Matus V, Gill SS, Soberón M, Bravo A (2014) Bacillus thuringiensis Cry1A toxins are versatile proteins with multiple modes of action: two distinct pre-pores are involved in toxicity. Biochem J 459:383–396Google Scholar
  26. Graça MAS (2001) The role of invertebrates on leaf litter decomposition in streams: a review. Int Rev Hydrobiol 86(4–5):383–393Google Scholar
  27. Graça MAS, Canhoto C (2006) Leaf litter processing in low order streams. Limnetica 25(1–2):1–10Google Scholar
  28. Griffiths NA, Tank JL, Royer TV, Rosi-Marshall EJ, Whiles MR, Chambers CP, Frauendorf TC, Evans-White MA (2009) Rapid decomposition of maize detritus in agricultural headwater streams. Ecol Appl 19(1):133–142Google Scholar
  29. Griffiths NA, Tank JL, Royer TV, Rosi EJ, Shogren AJ, Frauendorf TC, Whiles MR (2017) Occurrence, leaching, and degradation of Cry1Ab protein from transgenic maize detritus in agricultural streams. Sci Total Environ 592:97–105Google Scholar
  30. Harrington DP, Fleming TR (1982) A class of rank test procedures for censored survival data. Biometrika 69:553–566Google Scholar
  31. Hemphill TA, Banerjee S (2015) Mandatory food labeling for GMOs. Regulation 37(4):7–10Google Scholar
  32. Holdich DM (2002) Biology of freshwater crayfish. Blackwell Science Ltd., NottinghamGoogle Scholar
  33. Jensen PD, Dively GP, Swan CM, Lamp WO (2010) Exposure and nontarget effects of transgenic Bt corn debris in streams. Environ Entomol 39(2):707–714Google Scholar
  34. Jones CG, Lawton JH, Shackak M (1994) Organisms as ecosystem engineers. Oikos 69(3):373–386Google Scholar
  35. Jones JPG, Andriahajaina FB, Ranambinintsoa EH, Hockley NJ, Ravoahangimalala O (2006) The economic importance of freshwater crayfish harvesting in Madagascar and the potential of community-based conservation to improve management. Oryx 40(2):168–175Google Scholar
  36. Jurat-Fuentes JL, Adang MJ (2006) Cry toxin mode of action in susceptible and resistant Heliothis virescens larvae. J Invertebr Pathol 92:166–171Google Scholar
  37. Jurat-Fuentes J, Karumbaiah L, Jakka S, Ning C, Liu C, Wu K, Jackson J, Gould F, Blanco C, Portilla M, Perera O, Adang M (2011) Reduced levels of membrane-bound alkaline phosphatases are common to lepidopteran strains resistant to Cry toxins from Bacillus thuringiensis. PLoS ONE 6(3):1–8Google Scholar
  38. Kassambara A, Kosinski M, Biecek P, Fabian S (2018) Drawing survival curves using ‘ggplot2.’ R package version 0.4.3. https://cran.r-project.org/web/packages/survminer/survminer.pdf. Accessed 11 April 2019
  39. Klerck D, Sweeney JC (2007) The effect of knowledge types on consumer-perceived risk and adoption of genetically modified foods. Psychol Mark 24:171–193Google Scholar
  40. Klümper W, Qaim M (2014) A meta-analysis of the impacts of genetically modified crops. PLoS ONE 9(11):e111629Google Scholar
  41. Koppenhöfer AM, Kaya HK (1997) Additive and synergistic interaction between entomophatogenic nematodes and Bacillus thuringiensis for scarab grub control. Biol Control 8:131–137Google Scholar
  42. Kreps TA, Baldridge AK, Lodge DM (2012) The impact of an invasive predator (Orconectes rusticus) on freshwater snail communities: insights on habitat-specific effects from a multilake long-term study. Can J Fish Aquat Sci 69(7):1164–1173Google Scholar
  43. Krogh PH, Griffiths B, Demšar D, Bohanec M, Debeljak M, Andersen MN, Sausse C, Birch ANE, Caul S, Holmstrup M, Heckmann LH (2007) Responses by earthworms to reduced tillage in herbicide tolerant maize and Bt maize cropping systems. Pedobiologia 51(3):219–227Google Scholar
  44. Lahman SE, Moore PA (2015) Olfactory sampling recovery following sublethal copper exposure in the rusty crayfish, Orconectes rusticus. Bull Environ Contam Toxicol 95(4):441–446Google Scholar
  45. Li Y-L, Du J, Fang Z-X, You J (2013) Dissipation of insecticidal Cry1Ac protein and its toxicity to nontarget aquatic organisms. J Agric Food Chem 61:10864–10871Google Scholar
  46. Linn MD, Moore PA (2014) The effects of Bt corn on rusty crayfish growth and survival. Arch Environ Contam Toxicol 67(3):436–443Google Scholar
  47. Lodge DM, Kershner MW, Aloi JE (1994) Effects of an omnivorous crayfish (Orconectes rusticus) on a freshwater littoral food web. Ecology 75(5):1265–1281Google Scholar
  48. Maguire I, Klobucar G, Erben R (2005) The relationship between female size and egg size in the freshwater crayfish Austropotamobius torrentium. Bull Fr Pêche Piscic 376–377:777–785Google Scholar
  49. Meyer KM, Gimpel K, Brandl R (2007) Viability analysis of endangered crayfish populations. J Zool 273:364–371Google Scholar
  50. Momot WT (1995) Redefining the role of crayfish in aquatic ecosystems. Rev Fish Sci 3:33–63Google Scholar
  51. Moore JW (2006) Animal ecosystem engineers in streams. Bioscience 56(3):237–246Google Scholar
  52. Mossé J (1990) Nitrogen to protein conversion factor for ten cereals and six legumes or oilseeds. A reappraisal of its definition and determination. Variation according to species and to seed protein content. J Agric Food Chem 38:18–24Google Scholar
  53. Nagamatsu N, Koike T, Sasaka K, Yoshimoto A, Furukawa Y (1999) The cadherin-like protein is essential to specificity determination and cytotoxic action of the Bacillus thuringiensis insecticidal CryIAa toxin. FEBS Lett 460(2):385–390Google Scholar
  54. Office of Prevention, Pesticides and Toxic Substances (2011, November) Pesticide fact sheet. US EPAGoogle Scholar
  55. Peters JA, Kreps T, Lodge DM (2008) Assessing the impacts of rusty crayfish (Orconectes rusticus) on submergent macrophytes in a north-temperate U.S. lake using electric fences. Am Midl Nat 159(2):287–297Google Scholar
  56. Prihoda KR, Coats JR (2008) Aquatic fate and effects of Bacillus thuringiensis Cry3Bb1 protein: toward risk assessment. Environ Toxicol Chem 27:793–798Google Scholar
  57. Que Q, Chilton M, de Fontes C, He C, Nuccio M, Zhu T, Wu Y, Chen J, Shi L (2010) Trait stacking in transgenic crops: challenges and opportunities. GM Crops 1(4):220–229Google Scholar
  58. Reynolds J, Souty-Grosset C, Richardson A (2013) Ecological roles of crayfish in freshwater and terrestrial habitats. Freshw Crayfish 19(2):197–218Google Scholar
  59. Roessink I, Gylstra R, Heuts P, Specken B, Ottburg F (2017) Impact of invasive crayfish on water quality and aquatic macrophytes in the Netherlands. Aquat Invasions 12(3):397–404Google Scholar
  60. Rosi-Marshall EJ, Tank JL, Royer TV, Whiles MR, Evans-White M, Chambers C, Stephen ML (2007) Toxins in transgenic crop byproducts may affect headwater stream ecosystems. Proc Natl Acad Sci USA 104(41):16204–16208Google Scholar
  61. Roth BM, Tetzlaff JC, Alexander ML, Kitchell JF (2007) Reciprocal relationships between exotic rusty crayfish, macrophytes, and Lepomis species in northern Wisconsin lakes. Ecosystems 10(1):75–86Google Scholar
  62. Shah TR, Prasad K, Kumar P (2016) Maize: a potential source of human nutrition and health: a review. Cogent Food Agric 2(1):1–9Google Scholar
  63. Sharma HC, Sharma JH, Crouch KK (2004) Genetic transformation of crops for insect resistance: potential and limitations. Crit Rev Plant Sci 23:47–72Google Scholar
  64. Soberón M, Pardo-López L, López I, Gómez I, Tabashnik BE, Bravo A (2007) Engineering modified Bt toxins to counter insect resistance. Science 318(5856):1640–1642Google Scholar
  65. Statzner B, Peltret O, Tomanova S (2003) Crayfish as geomorphic agents and ecosystem engineers: effect of a biomass gradient on baseflow and flood-induced transport of gravel and sand in experimental streams. Freshw Biol 48(1):147–163Google Scholar
  66. Tabashnik BE, Zhang M, Fabrick JA, Wu Y, Gao M, Huang F, Wei J, Zhang J, Yelich A, Unnithan GC (2015) Dual mode of action of Bt proteins: protoxin efficacy against resistant insects. Sci Rep 5:15107Google Scholar
  67. Tablado Z, Tella JL, Sanchez-Zapata JA, Hiraldo F (2010) The paradox of the long-term positive effects of a North American crayfish on a European community of predators. Conserv Biol 24(5):1230–1238Google Scholar
  68. Tank JL, Rosi-Marshall EJ, Royer TV, Whiles MR, Griffiths NA, Frauendorf TC, Treering DJ (2010) Occurrence of maize detritus and a transgenic insecticidal protein (Cry1Ab) within the stream network of an agricultural landscape. Proc Natl Acad Sci USA 107(41):17645–17650Google Scholar
  69. Taugbøl T, Skurdal J (1992) Growth, mortality and moulting rate of noble crayfish, Astacus astacus L., juveniles in aquaculture experiments. Aquat Res 23(4):411–420Google Scholar
  70. Taverniers I, Papazova N, Bertheau Y, De Loose M, Holst-Jensen A (2008) Gene stacking in transgenic plants: towards compliance between definitions, terminology, and detection within the EU regulatory framework. Environ Biosaf Res 7(4):197–218Google Scholar
  71. Therneau TM (2018) Survival Analysis. R package version 2.43-3. https://cran.r-project.org/web/packages/survival/survival.pdf. Accessed 11 April 2019
  72. Tropea C, Arias M, Calvo NS, Greco LSL (2012) Influence of female size on offspring quality of the freshwater crayfish Cherax quadricarinatus (Parastacidae: Decapoda). J Crust Biol 32:883–890Google Scholar
  73. USDA Economic Research Service (2018) Adoption of genetically engineered crops in the U.S. https://www.ers.usda.gov/data-products/adoption-of-genetically-engineered-crops-in-the-us.aspx. Accessed 11 April 2019
  74. Usio N, Townsend C (2004) Roles of crayfish: consequences of predation and bioturbation for stream invertebrates. Ecology 85(3):807–822Google Scholar
  75. Usio N, Kamiyama R, Saji A, Takamura N (2009) Size-dependent impacts of invasive alien crayfish on a littoral marsh community. Biol Conserv 142(7):1480–1490Google Scholar
  76. Vachon V, Laprade R, Schwartz J-L (2012) Current models of the mode of action of Bacillus thuringiensis insecticidal crystal proteins: a critical review. J Invertebr Pathol 111:1–12Google Scholar
  77. Viktorov AG (2011) Transfer of Bt corn byproducts from terrestrial to stream ecosystems. Russ J Plant Phys 58(4):543–548Google Scholar
  78. Whitledge GW, Rabeni CF (1997) Energy sources and ecological role of crayfishes in an Ozark stream: insights from stable isotopes and gut analysis. Can J Fish Aquat Sci 54:2555–2563Google Scholar
  79. Wilson SK (2000) Trophic status and feeding selectivity of blennies (Blenniidae: Salariini). Mar Biol 136(3):431–437Google Scholar
  80. Wolf MC, Voigt R, Moore PA (2004) Spatial arrangement of odor sources modifies the temporal aspects of crayfish search strategies. J Chem Ecol 30:501–517Google Scholar
  81. Zwahlen C, Hilbeck A, Gugerli P, Nentwig W (2003) Degradation of the Cry1Ab protein within transgenic Bacillus thuringiensis corn tissue in the field. Mol Ecol 12(765–775):20Google Scholar

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Authors and Affiliations

  1. 1.Laboratory for Sensory Ecology, Department of Biological SciencesBowling Green State UniversityBowling GreenUSA
  2. 2.University of Michigan Biological StationPellstonUSA

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