Abstract
The carrot psyllid, Bactericera trigonica, is a vector of ‘Candidatus Liberibacter solanacearum’ which infects carrots and many of solanaceous plants. The psyllid was first reported in Spain, then it was rapidly spreading throughout the Mediterranean countries, where it causes considerable damages to carrot crops. To minimize the spread of psyllid species as well as the associated fastidious bacteria, field inspections have been carried out in order to seek for a natural enemies of B. trigonica. Field surveys revealed the presence of a new eulophid parasitoid for the first time in Tunisia attacking larvae of B. trigonica, the main responsible for the significant losses in carrot fields. In order to study the parasitism rate of this parasitoid, a weekly sampling of carrot plants carrying the psyllids and its parasitoids was performed in carrot fields. The parasitism rate and the preferential stage for this parasitoid were also determined under laboratory conditions. The result shows Tamarixia pronomus, preferred late (4th and 5th) instar larvae to early (2nd and 3rd) instar larvae of B. trigonica. There, the parasitism average of late instars was estimated to average 80% and approached 100%. It should be noted that parasitism rates varied by season, with the spring showing the highest averages. Further efforts are warranted to enhance the biological control of B. trigonica and thereby reduce psyllid populations and the spread of ‘Candidatus Liberibacter solanacearum’.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alfaro-Fernández A, Siverio F, Cebrián MC, Villaescusa FJ, Font MI (2012) Candidatus Liberibacter solanacearum’ associated with Bactericera trigonica-affected carrots in the Canary Islands. Plant Dis 96(4):581. https://doi.org/10.1094/pdis-10-11-0878-pdn
Antolínez CA, Fereres A, Moreno A (2017) Risk assessment of ‘Candidatus Liberibacter solanacearum’ transmission by the psyllids Bactericera trigonica and B. tremblayi from Apiaceae crops to potato. Sci Rep 7:45534. https://doi.org/10.1038/srep45534
Antolínez CA, Moreno A, Ontiveros I, Pla S, Plaza M, Sanjuan S, Fereres A (2019) Seasonal abundance of psyllid species on carrots and potato crops in Spain. Insects 10(9):287. https://doi.org/10.3390/insects10090287
Augier L, Gastaminza G, Lizondo M, Argañaraz M, Willink E (2006) Presencia de Diaphorina citri (Hemiptera: Psyllidae) en el noroeste argentino (noa). Rev Soc Entomol Arg65(3–4):67–68
Ben Othmen S, Morán FE, Navarro I, Barbé S, Martínez C, Marco-Noales E, López MM (2018) Candidatus Liberibacter solanacearum’ haplotypes D and E in carrot plants and seeds in Tunisia. J Plant Pathol 100(2):197–207. https://doi.org/10.1007/s42161-018-0045-7
Ben Othmen S, Abbes K, El Imem M, Ouvrard D, Rapisarda C, Chermiti B (2019) Bactericera trigonica and B. nigricornis (Hemiptera: Psylloidea) in Tunisia as potential vectors of ‘Candidatus Liberibacter. solanacearum’on Apiaceae Orient Insects 53(4):497–509. https://doi.org/10.1080/00305316.2018.1536003
Burckhardt D, Yefremova Z, Yegorenkova E (2015) The jumping plant louse Diaphorina teucria sp. nov. (Hemiptera, Liviidae) associated with Teucrium (Lamiaceae) and its parasitoid Tamarixia dorchinaesp.nov. (Hymenoptera: Eulophidae) from the Negev desert, Israel. Zootaxa 3920(3):463–470. https://doi.org/10.11646/zootaxa.3920.3.5
Cerón-González C, Lomeli-Flores JR, Rodríguez-Leyva E, Torres-Ruíz A (2014) Fertility and feeding of Tamarixia triozae (Hymenoptera: Eulophidae) on potato psyllid Bactericera cockerelli. Rev Mexi Cien Agríc 5(5):893–899. https://doi.org/10.29312/REMEXCA.V5I5.912
Chien CC, Chu YI, Ku SC (1991) Parasitic strategy, morphology, and life history of Tamarixia radiata (Hymenoptera: Eulophidae). Chinj Entomol 11(4):264–281
Chu YI, Chien CC (1991) Utilization of natural enemies to control of psyllid vectors transmitting citrus greening. Integrated control of plant virus diseases. Food and Fertilizer Technology Center for the Asian and Pacific region, Taipei, Taiwan,135–145
De León JH, Setameou M (2010) Molecular evidence suggests that populations of the asian citrus psyllid parasitoid Tamarixia radiata (Hymenoptera: Eulophidae) from Texas, Florida, and Mexico represent a single species. Ann Entomo Soc Am 103(1):100–110. https://doi.org/10.1603/008.103.0113
Étienne J, Quilici S, Marival D, Franck A (2001) Biological control of Diaphorina citri (Hemiptera: Psyllidae) in Guadeloupe by imported Tamarixia radiata (Hymenoptera: Eulophidae). Fruits 56(5):307–315. https://doi.org/10.1051/fruits:2001131
Gómez-Torres ML, Nava DE, Parra RP (2012) Life table of Tamarixia radiata (Hymenoptera: Eulophidae) on Diaphorina citri (Hemiptera: Psyllidae) at different temperatures. J Eco Entomo 105:338–343. https://doi.org/10.1603/EC11280
Johnson TE (1971) Effectiveness of Tetrastichus triozae Burks (Hymenoptera: Eulophidae) as a biological control agent of Paratrioza cockerelli (Sulc.) (Homoptera: Psyllidae) in north central Colorado, The (Doctoral dissertation, Colorado State University). https://hdl.handle.net/10217/233862
McFarland CD, and., Hoy MA (2001) Survival of Diaphorina citri (Homoptera: Psyllidae), and its two Parasitoids, Tamarixia radiata (Hymenoptera: Eulophidae) and Diaphorencyrtus aligarhensis (Hymenoptera: Encyrtidae), under different relative humidities and temperature regimes. Fla Entomol 84:227–233. https://doi.org/10.2307/3496171
Medić Pap S, Gvozdanović Varga J, Červenski J, Stepanović J, Rekanović E, Stepanović M, Duduk B (2018) First report of ‘Candidatus Phytoplasma solani’infecting parsnip in Serbia. P Dis 102(5):1026–1026. https://doi.org/10.1094/PDIS-02-17-0197-PDN
Munyaneza JE, Fisher TW, Sengoda VG, Garczynski SF, Nissinen A, Lemmetty A (2010) First Report of” Candidatus Liberibacter solanacearum” Associated with psyllid-affected carrots in Europe. Plant Dis 94(5):639
Pena-Carrillo KI, Gonzales-Hernandez A, Lopez-Arroyo JS, Mercado-Hernandez R, Favela-Lara S (2015) Morphological and genetic variation in Mexican wild populations of Tamarixia radiata Fla Entomol 98(4): 1093–1100. https://www.jstor.org/stable/24587619
Pluke RW, Qureshi JA, Stansly PA (2008) Citrus flushing patterns, Diaphorina citri (Hemiptera: Psyllidae) populations and parasitism by Tamarixia radiata (Hymenoptera: Eulophidae) in Puerto Rico. Fla Entomol 91(1):36–42. https://doi.org/10.1653/0015-4040(2008)091[0036:CFPDCH]2.0.CO;2
Rakhshani E, Saeedifar A (2013) Seasonal fluctuations, spatial distribution and natural enemies of asian citrus psyllid Diaphorina citri Kuwayama (Hemiptera: Psyllidae) in Iran. Entomol Sci 16(1):17–25. https://doi.org/10.1111/j.1479-8298.2012.00531.x
Teresani GR, Bertolini E, Alfaro-Fernandez A, Martinez C, Tanaka FA, Kitajima EW, Rosello M, Sanjuan S, Ferrandiz JC, Lopez MM et al (2014) Association of ‘Candidatus Liberibacter solanacearum’ with a vegetative disorder of celery in Spain and development of a real-time PCR method for its detection. Phytopathology 104(8):804–811
Teresani GR, Hernández E, Bertolini E, de la Rosa FS, Lozano AM, Castiel AF, Alvarez MC (2017) Transmission of ‘Candidatus Liberibacter solanacearum’ by Bactericera trigonica Hodkinson to vegetable hosts. Span Agri Resea 15(4):1–11. https://doi.org/10.5424/sjar/2017154-10762
Torres MLG, Nava DE, Gravena S, Costa VA, Parra JR (2006) First report of Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae) on Diaphorina citri Kuwayama (Hemiptera: Psyllidae) in Brazil.Rev de Agricul. (Piracicaba) 81(1):112–117
Zuparko RL, De Queiroz DL, La Salle J (2011) Two new species of Tamarixia (hymenoptera: Eulophidae) from Chile and Australia, established as biological control agents of invasive psyllids (hemiptera: Calophyidae, triozidae) in California. Zootaxa 2921:13–27
Acknowledgements
The authors acknowledge with thanks l’Union Tunisienne de l’Agriculture et de la Pêche (UTAP), Kairouan, Tunisia, for facilitating the field work in the governorate of Kairouan. The authors are grateful to Joshua Gearing for English editing that improved the quality of the manuscript.
Funding
No funding was received for this work.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
No conflict of interest exists. We wish to confirm that there are no known conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Othmen, S.B., Hafsi, A., Elimem, M. et al. Parasitism rate of Bactericera trigonica hodkinson nymphs by Tamarixia pronomus walker under field and laboratory conditions. Int J Trop Insect Sci 43, 1497–1503 (2023). https://doi.org/10.1007/s42690-023-01055-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42690-023-01055-x