Skip to main content

Bottom-up effects of breeding tomato genotypes on behavioural responses and performance of Tetranychus evansi population

Abstract

The tomato red spider mite, TRSM, Tetranychus evansi Baker & Pritchard (Acari: Tetranychidae), is an invasive tomato pest in several countries, with potential to reduce yield by up to 90% in Africa. Solanum habrochaites, access PI 134417 is a wild tomato genotype resistant to several arthropod pests, including TRSM. There is an interest in increasing the resistance of a tomato genotype (Solanum lycopersicum cv. TLCV15) widely cultivated by smallholder western African farmers to TRSM, through interspecific crossings with that wild genotype. For this purpose, after obtaining the F1 progeny and as well as F2 (SPJ-10–2017) and BC1 back-crossed (SPJ-05–2018) genotypes selected for high glandular trichome densities, we characterized their resistance level to TRSM. We quantified the types and densities of trichomes on the abaxial surface of their leaflets, and examined the subsequent bottom-up effects of these progeny plants attributes on behaviour and demographic parameters of the mite. Our results showed that the densities of glandular trichomes inherited from the resistant genotype (PI 134417) by the progenies were highly variable, with types I, IV and VI being the most prevalent. The progeny SPJ-10–2017 was classified as resistant, while the progenies F1 and SPJ-05–2018 were classified as partially resistant. These findings constitute one of the first steps towards advancing breeding programs in African countries to obtain tomato genotypes resistant to TRSM, targeting more sustainable production.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Data availability

All material will be made available on a repository.

Code availability

All codes will be made available upon request.

References

  1. Alba JM, Montserrat M, Fernandez-Munoz R (2008) Resistance to the two-spotted spider mite (Tetranychus urticae) by acylsucroses of wild tomato (Solanum pimpinellifolium) trichomes studied in a recombinant inbred line population. Exp Appl Acarol 47:35–47. https://doi.org/10.1007/s10493-008-9192-4

    Article  PubMed  Google Scholar 

  2. Al-Bayati AS (2019) Breeding for tomato resistance to spider mite Tetranychus urticae Koch (Acari: Tetranychidae), Theses, University of Kentucky

  3. Antonious GF, Snyder JC (2008) Tomato leaf crude extracts for insects and spider mite control. In: V. R. Preedy, Watson RR (eds) Tomatoes and tomato products: nutritional, medicinal and therapeutic properties. Science Publishers: Enfield, pp 269–297.

  4. Azandémè-Hounmalon YG, Affognon HD, Assogba KF, Tamo M, Fiaboe KKM, Kreiter S, Martin T (2015) Farmers control practices against the invasive red spider mite, Tetranychus evansi Baker & Pritchard in Benin. Crop Prot 76:53–58. https://doi.org/10.1016/j.cropro.2015.06.007

    Article  Google Scholar 

  5. Baker BP, Green TA, Loker AJ (2020) Biological control and integrated pest management in organic and conventional systems. Biol Control 140:1040952. https://doi.org/10.1016/j.biocontrol.2019.104095

    Article  Google Scholar 

  6. Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  7. Bleeker PM, Mirabella R, Diergaarde PJ, VanDoorn A, Tissier A Kant, MR Prins M, de Vos M, Haring MA, Schuurink RC (2012) Improved herbivore resistance in cultivated tomato with the sesquiterpene biosynthetic pathway from a wild relative. Proc Natl Acad Sci 49: 20124−20129. Doi: https://doi.org/10.1073/pnas.1208756109

  8. Bonato O (1999) The effect of temperature on life history parameters of Tetranychus evansi (Acari: Tetranychidae). Exp Appl Acarol 23:11–19

    Article  Google Scholar 

  9. Boubou A, Migeon A, Navajas RG, M, (2010) Recent emergence and worldwide spread of the red tomato spider mite, Tetranychus evansi: genetic variation and multiple cryptic invasions. Biol Invas 13:81–92

    Article  Google Scholar 

  10. Campos ML, de Almeida M, Rossi ML, Martinelli AP, Junior CGL, Figueira A, Rampelotti-Ferreira FT, Vendramim JD, Benedito VA, Peres LEP (2009) Brassinosteroids interact negatively with jasmonates in the formation of anti-herbivory traits in tomato. J Exp Bot 60:4347–4361. https://doi.org/10.1093/jxb/erp270

    Article  PubMed  Google Scholar 

  11. Chi H (2020a) TWOSEX-MSChart: a computer program for the age-stage, two-sex life table analysis. http://140.120.197.173/Ecology/prod02.htm. Accessed June 2020).

  12. Chi H, You MS, Atlihan R, Smith CL, Kavousi A, Ozgokçe MS, Guncan A, Tuan SJ, Fu JW, Xu YY, Zheng FQ, Ye BH, Chu D, Yu Y, Gharekhani G, Saska P, Gotoh T, Schneider MI, Bussaman P, Gokçe A, Liu TX (2020) Age-stage, two-sex life table: an introduction to theory, data analysis, and application. Entomol Gen. https://doi.org/10.1127/entomologia/2020/0936

    Article  Google Scholar 

  13. de Moraes GJ, Flechtmann CHW (2008) Manual de acarologia: acarologia básica e ácaros de plantas cultivadas no Brasil. Ribeirão Preto: Holos.

  14. Demétrio CGB, Hinde J, Moral RA (2014) Models for overdispersed data in entomology. In: Ferreira CP, Godoy WAC (eds) Ecological modeling applied to entomology. Springer, Switzerland, pp 219–259

    Google Scholar 

  15. Efron B, Tibshirani RJ (1993) An introduction to the bootstrap. Chapman & Hall, New York

    Book  Google Scholar 

  16. Fathipour Y, Maleknia B, Bagheri A, Soufbaf M, Zalucki MP (2019) Spider mite host plant resistance traits improve the predatory performance of Phytoseiulus persimilis on cucumber, despite negative life history impacts. Biol Control 138:104064. https://doi.org/10.1016/j.biocontrol.2019.104064

    CAS  Article  Google Scholar 

  17. Furtado IP, de Moraes GJ, Kreiter S, Tixier MS, Knapp M (2007) Potential of a Brazilian population of the predatory mite Phytoseiulus longipes as a biological control agent of Tetranychus evansi (Acari: Phytoselidae: Tetranychidae). Biol Control 42:139–147

    Article  Google Scholar 

  18. Hair JF Jr, Black WC, Babin BJ, Anderson RE, Tatham RL (2006) Multivariate data analysis, 6th edn. Pearson Prentice Hall, New Jersey

    Google Scholar 

  19. Han P, Desneux N, Amiens-Desneux E, Le Bot J, Bearez P, Lavoir AV (2016) Does plant cultivar difference modify the bottom-up effects of resource limitation on plant–herbivorous insect interactions? J Chem Ecol 42:1293–1303

    CAS  Article  Google Scholar 

  20. Han P, Desneux N, Becker C, Larbat R, Le Bot J, Adamowicz S, Zhang J, Lavoir AV (2019) Bottom-up effects of irrigation, fertilization and plant resistance on Tuta absoluta: implication for Integrated Pest Management. J Pest Sci 92:1359–1370

    Article  Google Scholar 

  21. Handford CE, Elliott CT, Campbell K (2015) Review of the global pesticide legislation and the scale of challenge in reaching the global harmonization of food safety standards. Integr Environ Asses 11:525–536

    Article  Google Scholar 

  22. Heidari N, Sedaratian-Jahromi A, Ghane-Jahromi M, Zalucki MP (2020) How bottom-up effects of different tomato cultivars affect population responses of Tuta absoluta (Lep.: Gelechiidae): a case study on host plant resistance. Arthropod Plant Int 14:181–192

    Article  Google Scholar 

  23. Hufbauer RA, Torchin ME (2007) Integrating ecological and evolutionary theory of biological invasions. In: Nentwig W (ed) biological invasions. Springer, Berlin, pp 79–96

    Chapter  Google Scholar 

  24. Janssen A, Sabelis MW (1992) Phytoseiid life-histories, local predator-prey dynamics, and strategies for control of tetranychid mites. Exp Appl Acarol 14:233–250. https://doi.org/10.1007/bf01200566

    Article  Google Scholar 

  25. Kaiser HF (1958) The varimax criterion for analytic rotation in factor analysis. Psychometrika 23:187–200

    Article  Google Scholar 

  26. Kennedy GG (2003) Tomato, pests, parasitoids, and predators: tritrophic interactions involving the genus Lycopersicon. Ann Rev Entomol 48:51–72. https://doi.org/10.1146/annurev.ento.48.091801.112733

    CAS  Article  Google Scholar 

  27. Keskin N, Kumral NA (2015) Screening tomato varietal resistance against the two-spotted spider mite [Tetranychus urticae (Koch)]. Int J Acarology 41:300–309. https://doi.org/10.1080/01647954.2015.1028440

    Article  Google Scholar 

  28. Khanamani M, Fathipour Y, Hajiqanbar H (2015) Assessing compatibility of the predatory mite Typhlodromus bagdasarjani (Acari: Phytoseiidae) and resistant eggplant cultivar in a tritrophic system. Ann Entomol Soc Am 108:501–512. https://doi.org/10.1093/aesa/sav032

    Article  Google Scholar 

  29. Lucini T, Faria MV, Rohde C, de Resende JTV (2015) Acylsugar and the role of trichomes in tomato genotypes resistance to Tetranychus urticae. Arthropod-Plant Int 9:45–53

    Article  Google Scholar 

  30. Luckwill LC (1943) The genus Lycopersicon: an historical, biological, and taxonomic survey of the wild and cultivated tomatoes. Aberdeen University Press, Aberdeen

    Google Scholar 

  31. Maciel GM, Marquez GR, Silva ECD, Andaló V, Belloti IF (2018) Tomato genotypes with determinate growth and high acylsugar content presenting resistance to spider mite. Crop Breed Appl Biotechnol 18:1–8

    CAS  Article  Google Scholar 

  32. Maluf WR, Campos GA, Cardoso MG (2001) Relationships between trichome types and spider mite (Tetranychus evansi) repellence in tomatoes with respect to foliar zingiberene contents. Euphytica 121:73–80

    Article  Google Scholar 

  33. Maluf WR, Maciel GM, Gomes LAA, Cardoso MG, Gonçalves LD, Silva EC, Knapp M (2010) Broad-spectrum arthropod resistance in hybrids between high- and low-acylsugar tomato lines. Crop Sci 50:439–450

    Article  Google Scholar 

  34. Meynard CN, Migeon A, Navajas M (2013) Uncertainties in predicting species distributions under climate change: a case study using Tetranychus evansi (Acari: Tetranychidae), a widespread agricultural pest. PLoS One 8:e66445

  35. Migeon A, Dorkeld F (2021) Spider Mites Web: a comprehensive database for the Tetranychidae. INRA, http://www.montpellier.inra.fr/CBGP/spmweb/

  36. Navajas M, Moraes GJ, Pigeon PAA (2012) Revision of the invasion of Tetranychus evansi, biology, colonization pathways, potential expansion and prospective for biological control. Exp Appl Acarol 59:43–65

    Article  Google Scholar 

  37. Nyoni BN, Gorman K, Mzilahowa T, Williamson MS, Navajas M, Field LM, Bass C (2011) Pyrethroid resistance in the tomato red spider mite, Tetranychus evansi, is associated with mutation of the para-type sodium channel. Pest Manag Sci 67:891–897. https://doi.org/10.1002/ps.2145

    CAS  Article  PubMed  Google Scholar 

  38. Oliveira JRF, Resende JTV, Filho RBL, Roberto SR, Silva PR, Rech C, Nardi C (2020) Tomato breeding for sustainable crop systems: high levels of zingiberene providing resistance to multiple arthropods. Horticulturae 6:34–48. https://doi.org/10.3390/horticulturae6020034

    CAS  Article  Google Scholar 

  39. Oliveira JRF, de Resende JTV, Maluf WR, Lucini T, de Lima Filho RBL, de Lima IP, Nardi C (2018) Trichomes and allelochemicals in tomato genotypes have antagonistic effects upon behaviour and biology of Tetranychus urticae. Front Plant Sci 9:1132. https://doi.org/10.3389/fpls.2018.01132

    Article  PubMed  PubMed Central  Google Scholar 

  40. R Development Core Team (2019) R: A Language and Environment for Statistical Computing. Vienna.

  41. Resende JTD, de Maluf WR, Cardoso MG, Faria MV, Gonçalves LD, Nascimento IR (2008) Resistance of tomato genotypes with high level of acyl sugars to Tetranychus evansi Baker & Pritchard. Sci Agric 65:31–35

    Article  Google Scholar 

  42. Sarr I, Knapp M, Ogol CKP, Baumgärtner J (2002) Impact of predators on Tetranychus evansi Baker and Pritchard populations and damage on tomatoes (Lycopersicon esculentum Mill.) in Kenya. Abstract retrieved from Abstract Abstract book of the 11th International Congress of Acarology, Merida, Mexico (No 271).

  43. Savi PJ, de Moraes GJ, Boiça Junior AL, Melville CC, Carvalho RF, Lourenção AL, Andrade DJ (2019a) Impact of leaflet trichomes on settlement and oviposition of Tetranychus evansi (Acari: Tetranychidae) in African and South American tomatoes. Syst Appl Acarol 24: 2559–2576. Doi: https://doi.org/10.11158/saa.24.12.19

  44. Savi PJ, de Moraes GJ, Melville CC, Andrade DJ (2019b) Population performance of Tetranychus evansi (Acari: Tetranychidae) on African tomato varieties and wild tomato genotypes. Exp Appl Acarol 77:555–570

    CAS  Article  Google Scholar 

  45. Savi PJ, de Moraes GJ, Andrade DJ (2021) Effect of tomato genotypes with varying levels of susceptibility to Tetranychus evansi on performance and predation capacity of Phytoseiulus longipes. Biocontrol. https://doi.org/10.1007/s10526-021-10096-5

    Article  Google Scholar 

  46. Schoonhoven LM, van Loon JJA, Dicke M (2005) Insect-plant biology. Oxford University Press, Oxford

    Google Scholar 

  47. Sharma HC, Ortiz R (2002) Host plant resistance to insects: an eco-friendly approach for pest management and environment conservation. J Environ Biol 23:111–135

    CAS  PubMed  Google Scholar 

  48. Silva P (1954) Um novo ácaro nocivo ao tomateiro na Bahia. Bol Inst Biol Bahia 1:1–20

    Google Scholar 

  49. Simmons AT, Gurr GM (2005) Trichomes of Lycopersicon species and their hybrids: effects on pests and natural enemies. J for Res 7:265–276. https://doi.org/10.1111/j.1461-9563.2006.00271.x

    Article  Google Scholar 

  50. Statsoft I (2012) STATISTICA (Data Analysis Software System); Version 11; Science Open: Berlin, German

  51. Van der Putten WH, Vet LEM, Harvey JA, Wäckers FL (2001) Linking above—and belowground multitrophic interactions of plants, herbivores, pathogens, and their antagonists. Trends Ecol Evol 16:547–554

    Article  Google Scholar 

  52. Ximénez-Embún MG, Ortego F, Castañera P (2016) Drought stressed tomato plants triggers bottom-up effects on the invasive Tetranychus evansi. PLoS One 11:e0145275.

Download references

Acknowledgements

To Coordination for the Improvement of Higher Education Personnel (CAPES), Brazil – Finance Code 001, for granting scholarships to PJS and the National Council for Scientific and Technological Development (CNPq) for granting the research productivity scholarship-Case No. 301492 / 2018-2 to DJA. We also thank Prof. Dr. Wesley Augusto Conde Godoy and Dr. José Bruno Malaquias (Insect Ecology Laboratory, Department of Entomology and Acarology, University of São Paulo) (ESALQ/USP), Piracicaba, São Paulo, Brazil for providing and assisting in the video tracking on EthoVision XT software.

Funding

The authors have no funding to report.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Patrice Jacob Savi.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Consent to publish

All authors read and approved the manuscript.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Communicated by Peng Han.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Savi, P.J., de Moraes, G.J., Carvalho, R.F. et al. Bottom-up effects of breeding tomato genotypes on behavioural responses and performance of Tetranychus evansi population. J Pest Sci (2021). https://doi.org/10.1007/s10340-021-01437-5

Download citation

Keywords

  • Life table parameters
  • Trichomes
  • Resistant genotype
  • Tomato red spider mite
  • Sustainable production