Skip to main content
Log in

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

  • Published:
Archives of Environmental Contamination and Toxicology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aimanova KG, Zhuang M, Gill SS (2006) Expression of Cry1Ac cadherin receptors in insect midgut and cell lines. J Invertebr Pathol 92:178–187

    Article  CAS  Google Scholar 

  • 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):197–212

    Article  Google Scholar 

  • 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):584–592

    Article  CAS  Google Scholar 

  • Bøhn T, Traavik T, Primicerio K (2010) Demographic responses of Daphnia magna fed transgenic Bt-maize. Ecotoxicology 19(2):419–430

    Article  CAS  Google Scholar 

  • Broderick NA, Raffa KF, Handelsman J (2006) Midgut bacteria required for Bacillus thuringiensis insecticidal activity. PNAS 103(41):15196–15199

    Article  CAS  Google Scholar 

  • 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 7:11

    Article  CAS  Google Scholar 

  • 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):89–98

    Article  CAS  Google Scholar 

  • 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 20:213–218

    Google Scholar 

  • Chambers PA, Hanson JM, Burke JM, Prepas EE (1990) The impact of the crayfish Orconectes virilis on aquatic macrophytes. Freshw Biol 24(1):81–91

    Article  Google Scholar 

  • 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):1949–1960

    Article  Google Scholar 

  • Creed RP Jr., (1994) Direct and indirect effects of crayfish grazing in a stream community. Ecology 75(7):2091–2103

    Article  Google Scholar 

  • Creed RP Jr., Reed JM (2004) Ecosystem engineering by crayfish in a headwater stream community. J N Am Benthol Soc 23(2):224–236

    Article  Google Scholar 

  • Crickmore N (2005) Using worms to better understand how Bacillus thuringiensis kills insects. Trends Microbiol 13:347–350

    Article  CAS  Google Scholar 

  • Dalzell BJ, Filley TR, Harbor JM (2005) Flood pulse influences on terrestrial organic matter export from an agricultural watershed. J Geophys Res 110:G02011

    Article  CAS  Google Scholar 

  • DiDonato GT, Lodge DM (1993) Species replacements among Orconectes crayfishes in Wisconsin lakes: the role of predation by fish. Can J Fish Aq Sci 50:1484–1488

    Article  Google Scholar 

  • 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):445–450

    Article  CAS  Google Scholar 

  • Dorn NJ, Mittelbach GG (1999) More than predator and prey: a review of interactions between fish and crayfish. Vie Milieu 49:229–237

    Google Scholar 

  • Dorn NJ, Wojdak JM (2004) The role of omnivorous crayfish in littoral communities. Commun Ecol 140:150–159

    Google Scholar 

  • 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):1741–1747

    Article  Google Scholar 

  • 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 48:437–446

    Google Scholar 

  • 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):1235–1239

    Article  CAS  Google Scholar 

  • 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 40:2–16

    Article  Google Scholar 

  • 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):1105–1110

    Article  Google Scholar 

  • Goddard JS, Al-Yahyai DSS (2001) Chemical and nutritional characteristics of dried sardine silage. J Aquat Food Prod Technol 10(4):39–50

    Article  Google Scholar 

  • 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 459:383–396

    Article  CAS  Google Scholar 

  • Graça MAS (2001) The role of invertebrates on leaf litter decomposition in streams: a review. Int Rev Hydrobiol 86(4–5):383–393

    Article  Google Scholar 

  • Graça MAS, Canhoto C (2006) Leaf litter processing in low order streams. Limnetica 25(1–2):1–10

    Google Scholar 

  • 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):133–142

    Article  Google Scholar 

  • 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 592:97–105

    Article  CAS  Google Scholar 

  • Harrington DP, Fleming TR (1982) A class of rank test procedures for censored survival data. Biometrika 69:553–566

    Article  Google Scholar 

  • Hemphill TA, Banerjee S (2015) Mandatory food labeling for GMOs. Regulation 37(4):7–10

    Google Scholar 

  • Holdich DM (2002) Biology of freshwater crayfish. Blackwell Science Ltd., Nottingham

    Google Scholar 

  • Jensen PD, Dively GP, Swan CM, Lamp WO (2010) Exposure and nontarget effects of transgenic Bt corn debris in streams. Environ Entomol 39(2):707–714

    Article  CAS  Google Scholar 

  • Jones CG, Lawton JH, Shackak M (1994) Organisms as ecosystem engineers. Oikos 69(3):373–386

    Article  Google Scholar 

  • 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):168–175

    Article  Google Scholar 

  • Jurat-Fuentes JL, Adang MJ (2006) Cry toxin mode of action in susceptible and resistant Heliothis virescens larvae. J Invertebr Pathol 92:166–171

    Article  CAS  Google Scholar 

  • 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):1–8

    Article  CAS  Google Scholar 

  • 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

  • Klerck D, Sweeney JC (2007) The effect of knowledge types on consumer-perceived risk and adoption of genetically modified foods. Psychol Mark 24:171–193

    Article  Google Scholar 

  • Klümper W, Qaim M (2014) A meta-analysis of the impacts of genetically modified crops. PLoS ONE 9(11):e111629

    Article  CAS  Google Scholar 

  • Koppenhöfer AM, Kaya HK (1997) Additive and synergistic interaction between entomophatogenic nematodes and Bacillus thuringiensis for scarab grub control. Biol Control 8:131–137

    Article  Google Scholar 

  • 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):1164–1173

    Article  Google Scholar 

  • 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):219–227

    Article  CAS  Google Scholar 

  • Lahman SE, Moore PA (2015) Olfactory sampling recovery following sublethal copper exposure in the rusty crayfish, Orconectes rusticus. Bull Environ Contam Toxicol 95(4):441–446

    Article  CAS  Google Scholar 

  • 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 61:10864–10871

    Article  CAS  Google Scholar 

  • Linn MD, Moore PA (2014) The effects of Bt corn on rusty crayfish growth and survival. Arch Environ Contam Toxicol 67(3):436–443

    Article  CAS  Google Scholar 

  • Lodge DM, Kershner MW, Aloi JE (1994) Effects of an omnivorous crayfish (Orconectes rusticus) on a freshwater littoral food web. Ecology 75(5):1265–1281

    Article  Google Scholar 

  • 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 376–377:777–785

    Article  Google Scholar 

  • Meyer KM, Gimpel K, Brandl R (2007) Viability analysis of endangered crayfish populations. J Zool 273:364–371

    Article  Google Scholar 

  • Momot WT (1995) Redefining the role of crayfish in aquatic ecosystems. Rev Fish Sci 3:33–63

    Article  Google Scholar 

  • Moore JW (2006) Animal ecosystem engineers in streams. Bioscience 56(3):237–246

    Article  Google Scholar 

  • 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 38:18–24

    Article  Google Scholar 

  • 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):385–390

    Article  CAS  Google Scholar 

  • Office of Prevention, Pesticides and Toxic Substances (2011, November) Pesticide fact sheet. US EPA

  • 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):287–297

    Article  Google Scholar 

  • Prihoda KR, Coats JR (2008) Aquatic fate and effects of Bacillus thuringiensis Cry3Bb1 protein: toward risk assessment. Environ Toxicol Chem 27:793–798

    Article  CAS  Google Scholar 

  • 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):220–229

    Article  Google Scholar 

  • Reynolds J, Souty-Grosset C, Richardson A (2013) Ecological roles of crayfish in freshwater and terrestrial habitats. Freshw Crayfish 19(2):197–218

    Google Scholar 

  • 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):397–404

    Article  Google Scholar 

  • 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):16204–16208

    Article  CAS  Google Scholar 

  • 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):75–86

    Article  Google Scholar 

  • Shah TR, Prasad K, Kumar P (2016) Maize: a potential source of human nutrition and health: a review. Cogent Food Agric 2(1):1–9

    Google Scholar 

  • Sharma HC, Sharma JH, Crouch KK (2004) Genetic transformation of crops for insect resistance: potential and limitations. Crit Rev Plant Sci 23:47–72

    Article  CAS  Google Scholar 

  • 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):1640–1642

    Article  CAS  Google Scholar 

  • 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):147–163

    Article  Google Scholar 

  • 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 5:15107

    Article  CAS  Google Scholar 

  • 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):1230–1238

    Article  Google Scholar 

  • 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):17645–17650

    Article  CAS  Google Scholar 

  • Taugbøl T, Skurdal J (1992) Growth, mortality and moulting rate of noble crayfish, Astacus astacus L., juveniles in aquaculture experiments. Aquat Res 23(4):411–420

    Article  Google Scholar 

  • 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):197–218

    Article  CAS  Google Scholar 

  • 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

  • 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 32:883–890

    Article  Google Scholar 

  • 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

  • Usio N, Townsend C (2004) Roles of crayfish: consequences of predation and bioturbation for stream invertebrates. Ecology 85(3):807–822

    Article  Google Scholar 

  • 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):1480–1490

    Article  Google Scholar 

  • 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 111:1–12

    Article  CAS  Google Scholar 

  • Viktorov AG (2011) Transfer of Bt corn byproducts from terrestrial to stream ecosystems. Russ J Plant Phys 58(4):543–548

    Article  CAS  Google Scholar 

  • 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 54:2555–2563

    Article  Google Scholar 

  • Wilson SK (2000) Trophic status and feeding selectivity of blennies (Blenniidae: Salariini). Mar Biol 136(3):431–437

    Article  Google Scholar 

  • Wolf MC, Voigt R, Moore PA (2004) Spatial arrangement of odor sources modifies the temporal aspects of crayfish search strategies. J Chem Ecol 30:501–517

    Article  CAS  Google Scholar 

  • 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):20

    Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paul A. Moore.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

West, M.E.J., Moore, P.A. Bt Proteins Exacerbate Negative Growth Effects in Juvenile Rusty (F. rusticus) Crayfish Fed Corn Diet. Arch Environ Contam Toxicol 77, 452–460 (2019). https://doi.org/10.1007/s00244-019-00664-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00244-019-00664-3

Navigation