Skip to main content
SpringerLink
Log in

Does the scion or rootstock of Citrus sp. affect the feeding and biology of Diaphorina citri Kuwayama (Hemiptera: Liviidae)?

  • Original Paper
  • Published:
Arthropod-Plant Interactions Aims and scope Submit manuscript

Abstract

The Asian citrus psyllid (ACP) Diaphorina citri is the main vector of the bacteria associated with Huanglongbing, and can exploit more than 50 species of the family Rutaceae as hosts. The number of possible hosts is even higher if plant varieties are included. This study evaluated the influence of different combinations of scion and rootstock citrus varieties on the development and feeding of ACP. Survival rates for the egg stage were highest on the Valencia and Sicilian varieties, both grafted on Sunki mandarin, with means of 87.99 and 87.98%, respectively; and lowest (67.63%) on Hamlin × Rangpur lime. The lowest levels of both nymphal and total viability (egg-adult) were obtained on Hamlin, regardless of the rootstock used. The total development time (egg-adult) ranged from 17.92 to 19.33 days for the Pêra × Sunki and Hamlin × Swingle combinations, respectively. Cluster analysis separated the hosts into two groups, the first consisting of the combinations of the Hamlin variety, and the second group formed by the other varieties. The highest food value (assessed by the area of honeydew produced) was observed for the orange scion varieties, and among these, the highest value was observed on Valencia (0.902 cm2); the smallest honeydew area was obtained on Ponkan (0.269 cm2). The rootstocks did not affect the feeding behavior of D. citri. The results of this study could aid in the development of management techniques, mainly in providing information for the installation of new citrus groves and assistance in crop-improvement research.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alves GR, Diniz AJF, Parra JRP (2014) Biology of the huanglongbing vector Diaphorina citri (Hemiptera: Liviidae) on different host plants. J Econ Entomol 107:691–696

    Article  CAS  PubMed  Google Scholar 

  • Ammar E, Hall DG, Shatters RG Jr (2013) Stylet morphometrics and citrus leaf vein structure in relation to feeding behavior of the Asian citrus psyllid Diaphorina citri, vector of citrus huanglongbing bacterium. PLoS ONE 8(3):e59914. doi:10.1371/journal.pone.005991

    Article  CAS  PubMed Central  Google Scholar 

  • Ammar ED, Richardson ML, Abdo Z, Hall DG, Shatters RG Jr (2014) Differences in stylet sheath occurrence and the fibrous ring (Sclerenchyma) between xCitroncirus plants relatively resistant or susceptible to adults of the Asian citrus psyllid Diaphorina citri (Hemiptera: Liviidae). PLoS ONE 9(10):e110919. doi:10.1371/journal.pone.0110919

    Article  PubMed Central  Google Scholar 

  • Aubert B (1987) Trioza erytreae Del Guercio and Diaphorina citri Kuwayama (Homoptera: Psyllidae), the two vectors of citrus greening disease: biological aspects and possible control strategies. Fruits 42:149–162

    Google Scholar 

  • Awmack CS, Leather SR (2002) Host plant quality and fecundity in herbivorous insects. Annu Rev Entomol 47:817–844

    Article  CAS  PubMed  Google Scholar 

  • Belasque J Jr, Yamamoto PT, Miranda MP, Bassanesi RB, Ayres AJ, Bové JM (2009) Controle do huanglongbing no estado de São Paulo, Brasil. Citrus Res Technol 31:53–64

    Google Scholar 

  • Borgoni PC, Vendramim JD, Lourenção AL, Machado MA (2014) Resistance of Citrus and Related Genera to Diaphorina citri Kuwayama (Hemiptera: Liviidae). Neotrop Entomol 43:465–469. doi:10.1007/s13744-014-0230-0

    Article  CAS  PubMed  Google Scholar 

  • Brodbeck BV, Mizell RF III, French WJ, Andersen PC, Aldrich JH (1990) Amino acids as determinants of host preference for the xylem feeding leafhopper, Homalodisca coagulata (Homoptera: Cicadellidae). Oecologia 83:338–345

    Article  PubMed  Google Scholar 

  • Cano A, Bermejo A (2011) Influence of rootstock and cultivar on bioactive compounds in citrus peels. J Sci Food Agric 91:1702–1711. doi:10.1002/jsfa.4375

    Article  CAS  PubMed  Google Scholar 

  • García-Pérez F, Ortega-Arenas LD, López-Arroyo JI, González-Hernández A, Lomeli-Flores JR, Romero-Nápoles J (2013) Morphometry of Diaphorina citri (Hemiptera: Liviidae) on six Rutaceae from Veracruz, Mexico. Fla Entomol 96:529–537. doi:10.1653/024.096.0218

    Article  Google Scholar 

  • George J, Ammar E, Hall DG, Lapointe SL (2017) Sclerenchymatous ring as a barrier to phloem feeding by Asian citrus psyllid: evidence from electrical penetration graph and visualization of stylet pathways. PLoS ONE 12(3):e0173520. doi:10.1371/journal.pone.0173520

    Article  PubMed  PubMed Central  Google Scholar 

  • Halbert SE, Manjunath KL (2004) Asian citrus psyllids (Sternorrhyncha: Psyllidae) and greening disease of citrus: a literature review and assessment of risk in Florida. Fla Entomol 87:330–353

    Article  Google Scholar 

  • Haynes KJ, Cronin JT (2006) Interpatch movement and edge effects: the role of behavioral responses to the landscape matrix. Oikos 113:43–54

    Article  Google Scholar 

  • Hodkinson ID (2009) Life cycle variation and adaptation in jumping plant lice (Insecta: Hemiptera: Psylloidea): a global synthesis. J Nat Hist 43:65–179

    Article  Google Scholar 

  • Koepke T, Dhingra A (2013) Rootstock scion somatogenetic interactions in perennial composite plants. Plant Cell Rep 32:1321–1337. doi:10.1007/s00299-013-1471-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu B, Coy M, Wang J, Stelinski LL (2015) The effect of host plant species on the detoxifying enzymes of the Asian citrus psyllid, Diaphorina citri (Hemiptera: Liviidae). Fla Entomol 98:997–999

    Article  Google Scholar 

  • Malinga GM, Valtonen A, Nyeko P, Vesterinen EJ, Roininen H (2014) Bottom-up impact on the cecidomyiid leaf galler and its parasitism in a tropical rainforest. Oecologia 176:511–520. doi:10.1007/s00442-014-3024-5

    Article  PubMed  Google Scholar 

  • Mayhew PJ (2001) Herbivore host choice and optimal bad motherhood. Trends Ecol Evol 16:165–167

    Article  PubMed  Google Scholar 

  • Muñoz ST, García AH, Pérez MJ, Boyero JR, Vela JM, Martínez-Ferri E (2008) Effects of rootstock and flushing on the incidence of three insects on ‘Clementine de Nules’ citrus trees. Environ Entomol 37:1531–1537. doi:10.1603/0046-225X-37.6.1531

    Article  PubMed  Google Scholar 

  • Nava DE, Gomez-Torres ML, Rodrigues MDL, Bento JMS, Parra JRP (2007) Biology of Diaphorina citri (Hem., Psyllidae) on different hosts and different temperatures. J Appl Entomol 131:709–715

    Article  Google Scholar 

  • Nehru RK, Bhagat KC, Koul VK (2004) Influence of citrus species on the development of Diaphorina citri. Ann Pl Protec Sci 12:436–438

    Google Scholar 

  • Parra JRP, Alves GR, Diniz AJF, Vieira JM (2016) Tamarixia radiata (Hymenoptera: Eulophidae) Diaphorina citri (Hemiptera: Liviidae): mass rearing and potential use of the parasitoid in Brazil. J Int Pest Manag 7:5–11

    Article  Google Scholar 

  • R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  • Ribeiro AB, Abdelnur PV, Garcia CF, Belini A, Severino VGP, da Silva MFGF, Fernandes JB, Vieira PC, Carvalho AS, Souza AA, Machado MA (2008) Chemical Characterization of Citrus sinensis grafted on C. limonia and the effect of some isolated compounds on the growth of Xylella fastidiosa. J Agric Food Chem 56:7815–7822

    Article  CAS  PubMed  Google Scholar 

  • Richardson ML, Hall DG (2013) Resistance of Poncirus and Citrus × Poncirus germplasm to the Asian citrus psyllid. Crop Sci 53:183–188

    Article  Google Scholar 

  • Saha D, Mukhopadhyay A, Bahadur M (2012) Effect of host plants on fitness traits and detoxifying enzymes activity of Helopeltis theivora, a major sucking insect pest of tea. Phytoparasitica 40:433–444. doi:10.1007/s12600-012-0244-2

    Article  CAS  Google Scholar 

  • Sétamou M, Bartels DW (2015) Living on the edges: spatial niche occupation of Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae), citrus groves. PLoS ONE 10(7):e0131917. doi:10.1371/journal.pone.0131917

    Article  PubMed  PubMed Central  Google Scholar 

  • Sétamou M, Schulthess F, Bosque-Pérez NA, Poehling H-M, Borgemeister C (1999) Bionomics of Mussidia nigrivenella (Lepidoptera: Pyralidae) on three host plants. Bull Entomol Res 89:465–471. doi:10.1017/S0007485399000607

    Article  Google Scholar 

  • Sétamou M, da Graça JV, Sandoval JL II (2016) Suitability of native North American Rutaceae to serve as host plants for the Asian citrus psyllid (Hemiptera: Liviidae). J Appl Entomol. doi:10.1111/jen.12300

    Google Scholar 

  • Simon JC, d’Alençon E, Guy E, Jacquin-Joly E, Jaquiéry J, Nouhaud P, Peccoud J, Sugio A, Streiff R (2015) Genomics of adaptation to host-plants in herbivorous insects. Brief Funct Genomics 14:413–423. doi:10.1093/bfgp/elv015

    Article  PubMed  Google Scholar 

  • Soares MS, da Silva DF, Forim MR, da Silva MFGF, Fernandes VB, Vieira PC, Silva DB, Lopes NP, Carvalho AS, de Souza AA, Machado MA (2015) Quantification and localization of hesperidin and rutin in Citrus sinensis grafted on C. limonia after Xylella fastidiosa infection by HPLC-UV and MALDI imaging mass spectrometry. Phytochemistry 115:161–170. doi:10.1016/j.phytochem.2015.02.011

    Article  CAS  PubMed  Google Scholar 

  • Souza TR, Villas-Boas RL, Quaggio JA, Salomão LC (2012) Nutrientes na seiva de plantas cítricas fertirrigadas. Rev Bras Frutic 34:482–492

    Article  Google Scholar 

  • Steinbauer MJ (2013) Shoot feeding as a nutrient acquisition strategy in free-living psylloids. PLoS ONE 8(10):e77990. doi:10.1371/journal.pone.0077990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Teck SLC, Fatimah A, Beattie A, Heng RQJ, King WS (2011) Influence of host plant species and flush growth stage on the Asian citrus psyllid, Diaphorina citri Kuwayama. Am J Agric Biol Sci 6:536–543

    Article  Google Scholar 

  • Tsagkarakis AE, Rogers ME (2010) Suitability of ‘Cleopatra’ mandarin as a host plant for Diaphorina citri (Hemiptera: Psyllidae). Fla Entomol 93:451–453. doi:10.1653/024.093.0322

    Article  Google Scholar 

  • Tsai JH, Liu YH (2000) Biology of Diaphorina citri (Homoptera: Psyllidae) on four host plants. J Econ Entomol 93:1721–1725

    Article  CAS  PubMed  Google Scholar 

  • Vale FXR, Fernandes-Filho E, Liberato JR (2003) A software plant disease severity assessment. In: Proceedings of the international congress of plant pathology, Plant Pathology Society, Christchurch, Aug 2003 p 105

  • Vendramim JD, Guzzo EC (2012) Plant resistance and insect bioecology and nutrition. In: Panizzi AR, Parra JRP (eds) Insect bioecology and nutrition for integrated pest management. CRC, Boca Raton, pp 657–686

    Chapter  Google Scholar 

  • Westbrook CJ, Hall DG, stover E, Duan YP, Lee RF (2011) Colonization of citrus and citrus-related germplasm by Diaphorina citri (Hemiptera: Psyllidae). HortScience 46:997–1005

    Google Scholar 

  • Wilson H, Miles AF, Daane KM, Altieri MA (2015) Landscape diversity and crop vigor influence biological control of the Western grape leafhopper (E. elegantula Osborn) in Vineyards. PLoS ONE 10(11):e0141752. doi:10.1371/journal.pone.0141752

    Article  PubMed  PubMed Central  Google Scholar 

  • Wise MJ, Partelow JM, Everson KJ, Anselmo MK, Abrahamson WG (2008) Good mothers, bad mothers, and the nature of resistance to herbivory in Solidago altissima. Oecologia 155:257–266

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank the Sylvio Moreira Citriculture Center for helping with the seedling production, and the São Paulo State Foundation for Research Aid (FAPESP—Process 2013/04291-0) for financial support.

Funding

This study was funded by the São Paulo State Foundation for Research Aid (FAPESP—Process 2013/04291-0).

Author information

Authors and Affiliations

  1. College of Agriculture Luiz de Queiroz (ESALQ), University of São Paulo, 9, Pádua Dias Avenue, Piracicaba, SP, Brazil

    Gustavo Rodrigues Alves, Vitor Hugo Beloti, Kenya Martins Faggioni-Floriano, Rafael de Andrade Moral, Clarice Garcia Borges Demétrio, José Roberto Postali Parra & Pedro Takao Yamamoto

  2. Center of Citriculture Sylvio Moreira (IAC-APTA), Cordeirópolis, SP, Brazil

    Sérgio Alves de Carvalho

Authors
  1. Gustavo Rodrigues Alves
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vitor Hugo Beloti
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kenya Martins Faggioni-Floriano
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sérgio Alves de Carvalho
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rafael de Andrade Moral
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Clarice Garcia Borges Demétrio
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. José Roberto Postali Parra
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Pedro Takao Yamamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gustavo Rodrigues Alves.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Handling Editor: Rupesh Kariyat.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alves, G.R., Beloti, V.H., Faggioni-Floriano, K.M. et al. Does the scion or rootstock of Citrus sp. affect the feeding and biology of Diaphorina citri Kuwayama (Hemiptera: Liviidae)?. Arthropod-Plant Interactions 12, 77–84 (2018). https://doi.org/10.1007/s11829-017-9555-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11829-017-9555-z

Keywords

Search

Navigation