Skip to main content
SpringerLink
Log in

The interaction of two-spotted spider mites, Tetranychus urticae Koch, with Cry protein production and predation by Amblyseius andersoni (Chant) in Cry1Ac/Cry2Ab cotton and Cry1F maize

  • Original Paper
  • Published:
Transgenic Research Aims and scope Submit manuscript

Abstract

Crops producing insecticidal crystal (Cry) proteins from the bacterium, Bacillus thuringiensis (Bt), are an important tool for managing lepidopteran pests on cotton and maize. However, the effects of these Bt crops on non-target organisms, especially natural enemies that provide biological control services, are required to be addressed in an environmental risk assessment. Amblyseius andersoni (Acari: Phytoseiidae) is a cosmopolitan predator of the two-spotted spider mite, Tetranychus urticae (Acari: Tetranychidae), a significant pest of cotton and maize. Tri-trophic studies were conducted to assess the potential effects of Cry1Ac/Cry2Ab cotton and Cry1F maize on life history parameters (survival rate, development time, fecundity and egg hatching rate) of A. andersoni. We confirmed that these Bt crops have no effects on the biology of T. urticae and, in turn, that there were no differences in any of the life history parameters of A. andersoni when it fed on T. urticae feeding on Cry1Ac/Cry2Ab or non-Bt cotton and Cry1F or non-Bt maize. Use of a susceptible insect assay demonstrated that T. urticae contained biologically active Cry proteins. Cry proteins concentrations declined greatly as they moved from plants to herbivores to predators and protein concentration did not appear to be related to mite density. Free-choice experiments revealed that A. andersoni had no preference for Cry1Ac/Cry2Ab cotton or Cry1F maize-reared T. urticae compared with those reared on non-Bt cotton or maize. Collectively these results provide strong evidence that these crops can complement other integrated pest management tactics including biological control.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adamczyk JJ, Sumerford DV (2001) Potential factors impacting season-long expression of Cry1Ac in 13 commercial varieties of Bollgard cotton. J Insect Sci 1:13

    Article  PubMed Central  PubMed  Google Scholar 

  • Álvarez-Alfageme F, Ferry N, Castanera P, Ortego F, Gatehouse AMR (2008) Prey mediated effects of Bt maize on fitness and digestive physiology of the red spider mite predator Stethorus punctillum Weise (Coleoptera: Coccinellidae). Transgenic Res 17:943–954

    Article  PubMed  Google Scholar 

  • Álvarez-Alfageme F, Bigler F, Romeis J (2011) Laboratory toxicity studies demonstrate no adverse effects of Cry1Ab and Cry3Bb1 to larvae of Adalia bipunctata (Coleoptera: Coccinellidae): the importance of study design. Transgenic Res 20:467–479

    Article  PubMed Central  PubMed  Google Scholar 

  • Amano H, Chant DA (1977) Life-history and reproduction of 2 species of predacious mites, Phytoseiulus persimilis Athias-Henriot and Amblyseius andersoni (Chant) (Acarina: Phytoseiidae). Can J Zool 55:1978–1983

    Article  Google Scholar 

  • Amano H, Chant DA (1978) Some factors affecting reproduction and sex-ratios in 2 species of predacious mites, Phytoseiulus persimilis Athias-Henriot and Amblyseius andersoni (Chant) (Acarina: Phytoseiidae). Can J Zool 56:1593–1607

    Article  Google Scholar 

  • Archer TL, Bynum ED (1993) Yield loss to maize from feeding by the Banks grass mite and two-spotted spider mite (Acari: Tetranychidae). Exp Appl Acarol 17:895–903

    Article  Google Scholar 

  • Auger P, Migeon A, Ueckermann EA, Tiedt L, Navajas M (2013) Evidence for synonymy between Tetranychus urticae and Tetranychus cinnabarinus (Acari, Prostigmata, Tetranychidae): review and new data. Acarologia 53:383–415

    Article  Google Scholar 

  • Bai YY, Jiang MX, Cheng JA, Wang D (2006) Effects of CrylAb toxin on Propylea japonica (Thunberg) (Coleoptera: Coccinellidae) through its prey, Nilaparvata lugens (Homoptera: Delphacidae), feeding on transgenic Bt rice. Environ Entomol 35:1130–1136

    Article  CAS  Google Scholar 

  • Benedict JH, Sachs ES, Altman DW, Deaton WR, Kohel RJ, Berberich SA (1996) Field performance of cottons expressing transgenic Cry1A insecticidal proteins for resistance to Heliothis virescens and Helicoverpa zea (Lepidoptera: Noctuidae). J Econ Entomol 89:230–238

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Boodley JW, Sheldrake RJ (1977) Cornell peat-lite mixes for commercial plant growing. Cornell Information Bulletin 43, Ithaca, New York

  • Chen M, Zhao JZ, Collins HL, Earle ED, Cao J, Shelton AM (2008) A critical assessment of the effects of Bt transgenic plants on parasitoids. PLoS One 3:e2284

    Article  PubMed Central  PubMed  Google Scholar 

  • Comas C, Lumbierres B, Pons X, Albajes R (2014) No effects of Bacillus thuringiensis maize on nontarget organisms in the field in southern Europe: a meta-analysis of 26 arthropod taxa. Transgenic Res 23:135–143

    Article  CAS  PubMed  Google Scholar 

  • Conner AJ, Glare TR, Nap JP (2003) The release of genetically modified crops into the environment. Part II: overview of ecological risk assessment. Plant J 33:19–46

    Article  PubMed  Google Scholar 

  • Dong HZ, Li WJ (2007) Variability of endotoxin expression in Bt transgenic cotton. J Agron Crop Sci 193:21–29

    Article  CAS  Google Scholar 

  • Dutton A, Klein H, Romeis J, Bigler F (2002) Uptake of Bt-toxin by herbivores feeding on transgenic maize and consequences for the predator Chrysoperla carnea. Ecol Entomol 27:441–447

    Article  Google Scholar 

  • Dutton A, Romeis J, Bigler F (2003) Assessing the risks of insect resistant transgenic plants on entomophagous arthropods: Bt-maize expressing Cry1Ab as a case study. Biocontrol 48:611–636

    Article  CAS  Google Scholar 

  • Esteves AB, de Oliveira JV, Torres JB, Gondim MGC (2010) Compared biology and behavior of Tetranychus urticae Koch (Acari: Tetranychidae) and Phytoseiulus macropilis (Banks) (Acari: Phytoseiidae) on BollGard (TM) and non-transgenic isoline cotton. Neotrop Entomol 39:338–344

    Article  Google Scholar 

  • Fernandez-Maizeejo J, Wechsler S, Livingston M, Mitchell L (2014) Genetically engineered crops in the United States. US Department of Agriculture Economic Research Service. http://www.ers.usda.gov/media/1282242/err162_summary.pdf

  • Ferry N, Mulligan EA, Stewart CN, Tabashnik BE, Port GR, Gatehouse AMR (2006) Prey-mediated effects of transgenic canola on a beneficial, non-target, carabid beetle. Transgenic Res 15:501–514

    Article  CAS  PubMed  Google Scholar 

  • García M, Ortego F, Castañera P, Farinós GP (2010) Effects of exposure to the toxin Cry1Ab through Bt maize fed-prey on the performance and digestive physiology of the predatory rove beetle Atheta coriaria. Biol Control 55:225–233

    Article  Google Scholar 

  • García M, Ortego F, Castañera P, Farinós GP (2012) Assessment of prey-mediated effects of the coleopteran-specific toxin Cry3Bb1 on the generalist predator Atheta coriaria (Coleoptera: Staphylinidae). Bull Entomol Res 102:293–302

    Article  PubMed  Google Scholar 

  • Garcia-Alonso M, Jacobs E, Raybould A, Nickson TE, Sowig P, Willekens H, Van der Kouwe P, Layton R, Amijee F, Fuentes AM, Tencalla F (2006) A tiered system for assessing the risk of genetically modified plants to non-target organisms. Environ Biosaf Res 5:57–65

    Article  Google Scholar 

  • Hellmich RL, Albajes R, Bergvinson D, Prasifka JR, Wang Z-Y, Weiss MJ (2008) The present and future role of insect-resistant genetically modified maize in IPM. In: Romeis J, Shelton AM, Kennedy GG (eds) Integration of insect-resistant, genetically modified crops within IPM programs. Springer, New York, pp 119–158

    Chapter  Google Scholar 

  • Jalali SK, Yadavalli L, Ojha R, Kumar P, Sulaikhabeevi SB, Sharma R, Nair R, Kadanur RC, Kamath SP, Komarlingam MS (2014) Baseline sensitivity of maize borers in India to the Bacillus thuringiensis insecticidal proteins Cry1A.105 and Cry2Ab2. Pest Manag Sci. doi:10.1002/ps.3888

    PubMed  Google Scholar 

  • James C (2014) Global status of commercialized biotech/GM crops: 2014 ISAAA Brief No. 49. ISAAA, Ithaca, NY

  • Kennedy GG (2008) Integration of insect-resistant genetically modified crops within IPM programs. In: Romeis J, Shelton AM, Kennedy GG (eds) Integration of insect-resistant, genetically modified crops within IPM Programs. Springer, New York, pp 1–26

    Chapter  Google Scholar 

  • Lawo NC, Wäckers FL, Romeis J (2010) Characterizing indirect prey-quality mediated effects of a Bt crop on predatory larvae of the green lacewing, Chrysoperla carnea. J Insect Physiol 56:1702–1710

    Article  CAS  PubMed  Google Scholar 

  • Li YH, Romeis J (2010) Bt maize expressing Cry3Bb1 does not harm the spider mite, Tetranychus urticae, or its ladybird beetle predator, Stethorus punctillum. Biol Control 53:337–344

    Article  CAS  Google Scholar 

  • Li YH, Romeis J, Wang P, Peng YF, Shelton AM (2011) A comprehensive assessment of the effects of Bt cotton on Coleomegilla maculata demonstrates no detrimental effects by Cry1Ac and Cry2Ab. PLoS One 6:e22185

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Liu XX, Chen M, Collins HL, Onstad DW, Roush RT, Zhang Q, Earle ED, Shelton AM (2014) Natural enemies delay insect resistance to Bt crops. PLoS One 9:e90366

    Article  PubMed Central  PubMed  Google Scholar 

  • Lövei GL, Andow DA, Arpaia S (2009) Transgenic insecticidal crops and natural enemies: a detailed review of laboratory studies. Environ Entomol 38:293–306

    Article  PubMed  Google Scholar 

  • Lu YH, Wu KM, Jiang YY, Guo YY, Desneux N (2012) Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 487:362–365

    Article  CAS  PubMed  Google Scholar 

  • Luo Z, Dong HH, Li WJ, Ming Z, Zhu YQ (2008) Individual and combined effects of salinity and waterlogging on Cry1Ac expression and insecticidal efficacy of Bt cotton. Crop Prot 27:1485–1490

    Article  CAS  Google Scholar 

  • McMurtry J (1982) The use of phytoseiids for biological control: progress and future prospects. Recent advances in knowledge of the Phytoseiidae. University of California, Berkeley, pp 23–48

    Google Scholar 

  • Meissle M, Romeis J (2009a) The web-building spider Theridion impressum (Araneae: Theridiidae) is not adversely affected by Bt maize resistant to corn rootworms. Plant Biotechnol J 7:645–656

    Article  CAS  Google Scholar 

  • Meissle M, Romeis J (2009b) Insecticidal activity of Cry3Bb1 expressed in Bt maize on larvae of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Entomol Exp Appl 131:308–319

    Article  CAS  Google Scholar 

  • Mészáros A, Beuzelin JM, Stout MJ, Bommireddy PL, Riggio RM, Leonard RB (2011) Jasmonic acid-induced resistance to the fall armyworm, Spodoptera frugiperda, in conventional and transgenic cottons expressing Bacillus thuringiensis insecticidal proteins. Entomol Exp Appl 144:226–237

    Article  Google Scholar 

  • Naranjo SE (2009) Impacts of Bt crops on non-target invertebrates and insecticide use patterns. CAB Rev Perspect Agric Vet Sci Nutrit Nat Resour 4(011):1–23

    Google Scholar 

  • Naranjo SE, Ruberson JR, Sharma HC, Wilson L, Wu KM (2008) The present and future role of insect-resistant GM cotton in IPM. In: Romeis J, Shelton AM, Kennedy GG (eds) Integration of insect-resistant, genetically modified crops within IPM programs. Springer, New York, pp 159–194

    Chapter  Google Scholar 

  • Naranjo SE, Ellsworth PC, Frisvold GB (2015) Economics of biological control in integrated pest management of managed plant systems. Annu Rev Entomol 60:621–645

    Article  CAS  PubMed  Google Scholar 

  • Nguyen HT, Jehle JA (2007) Quantitative analysis of the seasonal and tissue-specific expression of Cry1Ab in transgenic maize Mon810. J Plant Dis Prot 114:82–87

    CAS  Google Scholar 

  • Niu Y, Meagher RL Jr, Yang F, Huang F (2013) Susceptibility of field populations of the fall armyworm (Lepidoptera: Noctuidae) from Florida and Puerto Rico to purified Cry1F protein and corn leaf tissue containing single and pyramided Bt genes. Florida Entomol 96:701–713

    Article  CAS  Google Scholar 

  • Obrist LB, Dutton A, Albajes R, Bigler F (2006a) Exposure of arthropod predators to Cry1Ab toxin in Bt maize fields. Ecol Entomol 31:143–154

    Article  Google Scholar 

  • Obrist LB, Dutton A, Romeis J, Bigler F (2006b) Biological activity of Cry1Ab toxin expressed by Bt maize following ingestion by herbivorous arthropods and exposure of the predator Chrysoperla carnea. Biocontrol 51:31–48

    Article  CAS  Google Scholar 

  • Olsen KM, Daly JC, Finnegan EJ, Mahon RJ (2005) Changes in Cry1Ac Bt transgenic cotton in response to environmental factors: temperature and insect damage. J Econ Entomol 98:1382–1390

    Google Scholar 

  • Onstad DW, Liu XX, Chen M, Roush R, Shelton AM (2013) Modeling the integration of parasitoid, insecticide and transgenic insecticidal crops for the long-term control of an insect pest. J Econ Entomol 106:1103–1111

    Article  CAS  PubMed  Google Scholar 

  • Prager SM, Martini X, Guvvala H, Nansen C, Lundgren J (2014) Spider mite infestations reduce Bacillus thuringiensis toxin concentration in corn leaves and predators avoid spider mites that have fed on Bacillus thuringiensis corn. Ann Appl Biol 165:108–116

    Article  CAS  Google Scholar 

  • Reddall A, Sadras VO, Wilson LJ, Gregg PC (2004) Physiological responses of cotton to two-spotted spider mite damage. Crop Sci 44:835–846

    Article  Google Scholar 

  • Romeis J, Meissle M, Bigler F (2006) Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nat Biotechnol 24:63–71

    Article  CAS  PubMed  Google Scholar 

  • Romeis J, van Driesche RG, Barratt BIP, Bigler F (2008a) Insect-resistant transgenic crops and biological control. In: Romeis J, Shelton AM, Kennedy GG (eds) Integration of insect-resistant, genetically modified crops within IPM programs. Springer, Nwe York, pp 87–117

    Chapter  Google Scholar 

  • Romeis J, Bartsch D, Bigler F, Candolfi MP, Gielkins MC, Hartley SE, Hellmich RL, Huesing JE, Jepson PC, Layton R, Quemada H, Raybould A, Rose RI, Schiemann J, Sears MK, Shelton AM, Sweet J, Vaituzis Z, Wolt JD (2008b) Assessment of risk of insect-resistant transgenic crops to nontarget arthropods. Nat Biotechnol 26:203–208

    Article  CAS  PubMed  Google Scholar 

  • Romeis J, McLean MA, Shelton AM (2013) When bad science makes good headlines: the case of Bt crops. Nat Biotechnol 37:386–387

    Article  Google Scholar 

  • Shelton AM, Cooley RJ, Kroening MK, Wilsey WT, Eigenbrode SD (1991) Comparative analysis of two rearing procedures for diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae). J Entomol Sci 26:17–26

    Google Scholar 

  • Shelton AM, Naranjo SE, Romeis J, Hellmich RL, Wolt JD, Federici BA, Albajes R, Bigler F, Burgess EPJ, Dively GP, Gatehouse AMR, Malone LA, Roush RT, Sears MK, Sehnal F (2009a) Setting the record straight: a rebuttal to an erroneous analysis on transgenic insecticidal crops and natural enemies. Transgenic Res 18:317–322

    Article  CAS  PubMed  Google Scholar 

  • Shelton AM, Naranjo SE, Romeis J, Hellmich RL, Wolt JD, Federici BA, Albajes R, Bigler F, Burgess EPJ, Dively GP, Gatehouse AMR, Malone LA, Roush RT, Sears MK, Sehnal F, Ferry N, Bell HA et al (2009b) Appropriate analytical methods are necessary to assess nontarget effects of insecticidal proteins in GM crops through meta-analysis (Response to Andow et al. 2009). Environ Entomol 38:1533–1538

    Article  CAS  PubMed  Google Scholar 

  • Shelton AM, Naranjo SE, Romeis J, Hellmich RL (2012) Errors in logic and statistics plague a meta-analysis (response to Andow and Lovei 2012). Environ Entomol 41:1047–1049

    PubMed  Google Scholar 

  • SPSS (1988) SPSS user’s guide. SPSS Inc, Chicago

    Google Scholar 

  • Su HH, Tian JC, Naranjo SE, Romeis J, Hellmich RL, Shelton AM (2015) Bacillus thuringiensis plants expressing Cry1Ac, Cry2Ab and Cry1F are not toxic to the assassin bug, Zelus renardii. J Appl Entomol 139:23–30

    Article  CAS  Google Scholar 

  • Tian JC, Collins HL, Romeis J, Naranjo SE, Hellmich RL, Shelton AM (2012) Using field-evolved resistance to Cry1F maize in a lepidopteran pest to demonstrate no adverse effects of Cry1F on one of its major predators. Transgenic Res 21:1303–1310

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tian JC, Wang XP, Long LP, Romeis J, Naranjo SE, Hellmich RL, Wang P, Earle ED, Shelton AM (2013) Bt crops producing Cry1Ac, Cry2Ab and Cry1F do not harm the green lacewing, Chrysoperla rufilabris. PLoS One 8:e60125

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tian JC, Long LP, Wang XP, Naranjo SE, Romeis J, Hellmich RL, Wang P, Shelton AM (2014a) Using resistant prey demonstrates that Bt plants producing Cry1Ac, Cry2Ab, and Cry1F have no negative effects on Geocoris punctipes and Orius insidiosus. Environ Entomol 43:242–251

    Article  CAS  PubMed  Google Scholar 

  • Tian JC, Wang XP, Long LP, Romeis J, Naranjo SE, Hellmich RL, Shelton AM (2014b) Eliminating host-mediated effects demonstrates Bt maize producing Cry1F has no adverse effects on the parasitoid Cotesia marginiventris. Transgenic Res 23:257–264

    Article  CAS  PubMed  Google Scholar 

  • Torres JB, Ruberson JR (2008) Interactions of Bacillus thuringiensis Cry1Ac toxin in genetically engineered cotton with predatory heteropterans. Transgenic Res 17:345–354

    Article  CAS  PubMed  Google Scholar 

  • Tsolakis H, Ragusa di Chiara S (1994) Biological and life table parameters of Amblyseius andersoni (Chant) (Parasitiformes, Phytoseiidae) on different kinds of food substances. Phytophaga (Palermo) 5:21–28

    Google Scholar 

  • van der Linden A (2004) Amblyseius andersoni Chant (Acari: Phytoseiidae), a successful predatory mite on Rosa spp. Commun Agric Appl Biol Sci 69:157–163

    PubMed  Google Scholar 

  • Wilson LJ (1993) Spider mites (Acari: Tetranychidae) affect yield and fiber quality of cotton. J Econ Entomol 86:566–585

    Article  Google Scholar 

  • Wolfenbarger LL, Naranjo SE, Lundgren JG, Bitzer RJ, Watrud LS (2008) Bt crop effects on functional guilds of non-target arthropods: a meta-analysis. PLoS One 3:e2118

    Article  PubMed Central  PubMed  Google Scholar 

  • Zemková Rovensaká G, Zemek R, Schmidet JEU, Hilbeck A (2005) Altered host plant preference of Tetranychus urticae and prey preference of its predator Phytoseiulus persimilis (Acari: Tetranychidae, Phytoseiidae) on transgenic Cry3Bb-eggplants. Biol Control 33:293–300

    Article  Google Scholar 

  • Zhou GS, Zhou FC, Xie YM, Feng CN, Yang YZ (2009) Effects of temperature stress on Bt insecticidal protein expression in Bt transgenic cotton leaves and death rate of cotton bollworm. Cotton Sci 21:302–306

    Google Scholar 

Download references

Acknowledgments

This project was supported by the China Scholarship Council and the Biotechnology Risk Assessment Program Competitive Grant No. 2010-33522-21772 from the USDA, National Institute of Food and Agriculture. We thank H. Collins, M. Cheung and D. Olmstead for technical assistance and J. Nyrop and K. Wentworth for advice and supplying the initial colony of T. urticae.

Author information

Authors and Affiliations

  1. Department of Entomology, Cornell University, New York State Agricultural Experiment Station (NYSAES), Geneva, NY, USA

    Yan-Yan Guo & Anthony M. Shelton

  2. Department of Entomology, China Agricultural University, Beijing, China

    Yan-Yan Guo & Wang-Peng Shi

  3. State Key Laboratory Breeding Base for Zhejiang Sustainable Pest and Disease Control, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang, China

    Jun-Ce Tian

  4. Department of Agriculture Science, China Agricultural University, Beijing, China

    Xue-Hui Dong

  5. Agroscope, Institute for Sustainability Sciences ISS, Zurich, Switzerland

    Jörg Romeis

  6. Arid-Land Agricultural Research Center, USDA-ARS, Maricopa, AZ, 85138, USA

    Steven E. Naranjo

  7. Corn Insects and Crop Genetics Research Unit, USDA-ARS, Ames, IA, 50011, USA

    Richard L. Hellmich

  8. Department of Entomology, Iowa State University, Ames, IA, 50011, USA

    Richard L. Hellmich

Authors
  1. Yan-Yan Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jun-Ce Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wang-Peng Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xue-Hui Dong
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jörg Romeis
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Steven E. Naranjo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Richard L. Hellmich
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Anthony M. Shelton
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anthony M. Shelton.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 319 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guo, YY., Tian, JC., Shi, WP. et al. The interaction of two-spotted spider mites, Tetranychus urticae Koch, with Cry protein production and predation by Amblyseius andersoni (Chant) in Cry1Ac/Cry2Ab cotton and Cry1F maize. Transgenic Res 25, 33–44 (2016). https://doi.org/10.1007/s11248-015-9917-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11248-015-9917-1

Keywords

Search

Navigation