Skip to main content
Log in

Targeted RT-PCR Based Gut Content Analysis for Potato Psyllid Predation in Laboratory Assays

  • Published:
American Journal of Potato Research Aims and scope Submit manuscript

Abstract

RT-PCR was used to test whether DNA from potato psyllid (Bactericera cockerelli (Šulc)) could be detected in generalist predators that had been allowed to feed on psyllids in laboratory feeding trials. The assay used primers that had been developed in Europe to amplify a region of the ITS2 gene in psyllids for use in identifying psyllid specimens intercepted at border inspection stations or discovered in regions currently free of the pest. We conducted feeding trials with arthropod generalist predators in diverse taxonomic groups (Araneae, Acari, and two orders of Insecta). RT-PCR readily detected potato psyllid DNA in predators that had recently fed upon the insect. DNA from a closely related psyllid, Bactericera dorsalis (Crawford), was not detected, suggesting that our approach is unlikely to lead to false positives. RT-PCR was found to be more sensitive than conventional PCR at detecting very dilute quantities of potato psyllid DNA. Predator taxa differed in how long after a feeding event prey DNA could be detected. Signal retention was longer in spiders and a predatory mite (Anystis) than in predatory true bugs (Hemiptera). We believe this new molecular tool will be of value in identifying potentially important sources of psyllid biological control under field conditions.

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

Similar content being viewed by others

References

  • Acorn, J. 2007. Ladybugs of Alberta: finding the spots and connecting the dots. Edmonton, Alberta: University of Alberta Press.

    Google Scholar 

  • Agustí, N., T. R. Unruh, and S. C. Welter. 2003. Detecting Cacopsylla pyricola (Hemiptera: Psyllidae) in predator guts using COI mitochondrial markers. Bulletin Of Entomological Research 93: 179–185.

    Article  PubMed  Google Scholar 

  • Bradley, R. A. 2013. Common spiders of North America. California: University of California Press.

    Google Scholar 

  • Butler, C. D., and J. T. Trumble. 2012a. The potato psyllid, Bactericera cockerelli (Sulc) (Hemiptera: Triozidae): life history, relationship to plant diseases, and management strategies. Terrestrial Arthropod Reviews 5: 87–111.

    Article  Google Scholar 

  • Butler, C. D., and J. T. Trumble. 2012b. Identification and impact of natural enemies of Bactericera cockerelli (Hemiptera: Triozidae) in Southern California. Journal Of Economic Entomology 105: 1509–1519.

    Article  PubMed  Google Scholar 

  • Calvo, F. J., A. Torres-Ruiz, J. C. Velázquez-González, E. Rodríguez-Leyva, and J. R. Lomeli-Flores. 2016. Evaluation of Dicyphus hesperus for biological control of sweet potato whitefly and potato psyllid on greenhouse tomatoes. Biocontrol 61: 415–424.

    Article  Google Scholar 

  • Castillo Carrillo, C. I., Z. Fu, A. S. Jensen, and W. E. Snyder. 2016. Arthropod pests and predators associated with bittersweet nightshade, a noncrop host of the potato psyllid (Hemiptera: Triozidae). Environmental Entomology 45: 873–882.

    Article  CAS  PubMed  Google Scholar 

  • Castillo Carrillo, C. I., Z. Fu, and D. Burckhardt. 2019. First record of the tomato potato psyllid Bactericera cockerelli from South America. Bull Insectology 72: 85–91.

    Google Scholar 

  • Cohen, A. C. 1995. Extra-oral digestion in predaceous terrestrial Arthropoda. Annu Rev Entomol 40: 85–103.

    Article  CAS  Google Scholar 

  • Cooper, W. R., D. R. Horton, E. Miliczky, C. H. Wohleb, and T. D. Waters. 2019. The weed link in zebra chip epidemiology: suitability of non-crop Solanaceae and Convolvulaceae to potato psyllid and “Candidatus Liberibacter solanacearum.”. American Journal Of Potato Research 96: 262–271.

    Article  Google Scholar 

  • Cooper, W. R., G. Esparza-Diaz, M. R. Wildung, D. R. Horton, I. E. Badillo-Vargas, and S. E. Halbert. 2023. Association of two Bactericera species (Hemiptera: Triozidae) with native Lycium spp. (Solanales: Solanaceae) in the potato growing regions of the Rio Grande Valley of Texas. Environ Entomol (in review).

  • Cuthbertson, A. G. S., C. C. Fleming, and A. K. Murchi. 2003. Detection of Rhopalosiphum insertum (apple-grass aphid) predation by the predatory mite Anystis baccarum using molecular gut analysis. Agri Forest Entomol 5: 219–225.

    Article  Google Scholar 

  • Filimonova, S. A. 2008. The fine structure of the midgut in the mite Anystis baccarum (L.) (Acari, Actinedida: Anystidae). Arthropod Structure & Development 37: 299–309.

    Article  Google Scholar 

  • Foelix, R. F. 1982. Biology of spiders. Cambridge, MA: Harvard University Press.

    Google Scholar 

  • Gajski, D., and S. Pekár. 2021. Assessment of the biocontrol potential of natural enemies against psyllid populations in a pear tree orchard during spring. Pest Management Science 77: 2358–2366.

    Article  CAS  PubMed  Google Scholar 

  • Gariepy, T. D., U. Kuhlmann, C. Gillott, and M. Erlandson. 2007. Parasitoids, predators and PCR: the use of diagnostic molecular markers in biological control of Arthropods. Journal Of Applied Entomology 131: 225–240.

    Article  CAS  Google Scholar 

  • Geary, I. J., C. N. Merfield, R. J. Hale, M. D. Shaw, and S. Hodge. 2016. Predation of nymphal tomato potato psyllid, Bactericera cockerelli (Šulc) (Hemiptera: Triozidae), by the predatory mite, Anystis baccarum L. (Trombidiformes: Anystidae). N Z Entomol 39: 110–116.

    Article  Google Scholar 

  • Goldmann, A. 2017. Predators of Asian citrus psyllid (Diaphorina citri) in Southern California. Ph.D. Dissertation, University of California, Riverside, California.

  • Hansen, A. K., J. T. Trumble, R. Stouthamer, and T. D. Paine. 2008. A new huanglongbing species, “Candidatus liberibacter psyllaurous,“ found to infect tomato and potato, is vectored by the psyllid Bactericera cockerelli (Sulc). Appl Environ Microb 74: 5862–5865.

    Article  CAS  Google Scholar 

  • Harwood, J. D., and J. J. Obrycki. 2005. Quantifying aphid predation rates of generalist predators in the field. Eur J Entomol 102: 335–350.

    Article  Google Scholar 

  • Herard, F. 1985. Analysis of parasite and predator populations observed in pear orchards infested by psylla pyri (L.) (Hom.: Psyllidae) in France. Agronomie 5: 773–778.

    Article  Google Scholar 

  • Hoogendoorn, M., and G. E. Heimpel. 2001. PCR-based gut content analysis of insect predators: using ribosomal ITS-1 fragments from prey to estimate predation frequency. Mol Ecol 10: 2059–2067.

  • Horton, D. R., D. A. Broers, T. Hinojosa, T. M. Lewis, E. R. Miliczky, and R. R. Lewis. 2002. Diversity and phenology of predatory arthropods overwintering in cardboard bands placed in pear and apple orchards of Central Washington State. Annals Of The Entomological Society Of America 95: 469–480.

    Article  Google Scholar 

  • Horton, D. R., E. Miliczky, T. M. Lewis, W. R. Cooper, J. E. Munyaneza, T. Mustafa, J. Thinakaran, T. D. Waters, C. H. Wohleb, and A. S. Jensen. 2017. New geographic records for the nearctic psyllid Bactericera maculipennis (Crawford) with biological notes and descriptions of the eggs and fifth-instar nymph (Hemiptera: Psylloidea: Triozidae). Proceedings Of The Entomological Society Of Washington 119: 191–214.

    Article  Google Scholar 

  • Jacobsen, S. K., L. Sigsgaard, K. Hansen, J. D. Harwood, E. G. Chapman, M. A. Hurtado, and A. B. Jensen. 2019. Generalist predator contributions to control of Tetranychus urticae in strawberry crops documented by PCR-based gut content analysis. Experimental And Applied Acarology 77: 133–143.

    Article  CAS  PubMed  Google Scholar 

  • Jones, I. M., P. T. Madeira, J. Z. Blair, and E. C. Lake. 2021. Using molecular gut content analysis to identify key predators in classical weed biological control system: a study with Neomusotima conspurcatalis (lepidotera: Crambidae). BioControl 66: 825–836.

    Article  CAS  Google Scholar 

  • Kelton, L. A. 1963. Synopsis of the genus Orius Wolff in America north of Mexico (Heteroptera: Anthochoridae). The Canadian Entomologist 95: 631–636.

    Article  Google Scholar 

  • King, R. A., D. S. Read, M. Traugott, and W. O. C. Symondson. 2008. Molecular analysis of predation: a review of best practice for DNA-based approaches. Molecular Ecology 17: 947–963.

    Article  CAS  PubMed  Google Scholar 

  • Knowlton, G. F. 1933. Ladybird beetles as predators of the potato psyllid. The Canadian Entomologist 65: 241–243.

    Article  Google Scholar 

  • Knowlton, G. F. 1934. A big-eyed bug predator of the potato psyllid. The Florida Entomologist 18: 40–43.

    Article  Google Scholar 

  • Knowlton, G. F., and M. Allen. 1936. Three hemipterous predators of the potato psyllid. Proc Utah Acad Sci 13: 293–294.

    Google Scholar 

  • Koss, A. M., A. S. Jensen, A. Schreiber, K. S. Pike, and W. E. Snyder. 2005. A comparison of predator and pest communities in Washington potato fields treated with broad-spectrum, selective, or organic insecticides. Environmental Entomology 34: 87–95.

    Article  CAS  Google Scholar 

  • Kuusk, A.-K., A. Cassel-Lundhagen, A. Kvarnheden, and B. Ekbom. 2008. Tracking aphid predation by lycosid spiders in spring-sown cereals using PCR-based gut-content analysis. Basic Appl Eco 9: 718–725.

    Article  CAS  Google Scholar 

  • MacDonald, F. H., P. G. Connolly, N. J. Larsen, and G. P. Walker. 2016. The voracity of five insect predators on Bactericera cockerelli (Sulc) (Hemiptera: Triozidae) (tomato potato psyllid; TPP). N Z Entomol 39: 15–22.

    Article  Google Scholar 

  • Macías-Hernández, N., K. Athey, V. Tonzo, W. S. Wangensteen, M. Arnedo, and J. D. Harwood. 2018. Molecular gut content analysis of different spider body parts. Plos One 13 (5): e0195689. https://doi.org/10.1371/journal.pone.0196589.

    Article  CAS  Google Scholar 

  • Molina, P., M. T. Martínez-Ferrer, J. M. Campos-Rivela, J. Riudavets, and N. Agustí. 2021. Development of a PCR-based method for the screening of potential predators of the african citrus psyllid Trioza erytreae (Del Guercio). Biological Control 160: 104661. https://doi.org/10.1016/j.biocontrol.2021.104661.

    Article  CAS  Google Scholar 

  • Monzó, C., B. Sabater-Muñoz, A. Urbaneja, and P. Castañera. 2010. Tracking medfly predation by the wolf spider, Pardosa cribata Simon, in citrus orchards sing PCR-based gut-content analysis. Bulletin Of Entomological Research 100: 145–152.

    Article  PubMed  Google Scholar 

  • Munyaneza, J. E. 2012. Zebra chip disease of potato: biology, epidemiology, and management. American Journal Of Potato Research 89: 329–350.

    Article  Google Scholar 

  • Munyaneza, J. E., J. M. Crosslin, and J. E. Upton. 2007. Association of Bactericera cockerelli (Homoptera: Psyllidae) with “zebra chip,“ a new potato disease in southwestern United States and Mexico. Journal Of Economic Entomology 100: 656–663.

    Article  CAS  PubMed  Google Scholar 

  • Murray, M. G., and W. F. Thompson. 1980. Rapid isolation of high molecular weight plant DNA. Nucleic Acids Research 8: 4321–4325.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patel, K., and Z.-Q. Zhang. 2017. Functional and numerical responses of Amblydromalus limonicus and Neoseiulus cucumeris to eggs and first instar nymph of tomato/potato psyllid (Bactericera cockerelli). Syst Appl Acarol 22: 1476–1488.

    Google Scholar 

  • Pletsch, D. J. 1947. The potato psyllid Paratrioza cockerelli (Sulc): its biology and control. Montana Agricultural Experiment Station, Bozeman, MT, Bulletin 446, 95 pp.

  • Pugh, A. R., D. M. O’Connell, and S. D. Wratten. 2015. Further evaluation of the southern ladybird (Cleobora mellyi) as a biological control agent of the invasive tomato-potato psyllid (Bactericera cockerelli). Biological Control 90: 157–163.

    Article  Google Scholar 

  • Reyes Corral, C. A., W. R. Cooper, D. R. Horton, and A. V. Karasev. 2020. Susceptibility of Physalis longifolia (Solanales: Solanaceae) to Bactericera cockerelli (Hemiptera: Triozidae) and “Candidatus Liberibacter solanacearum.”. Journal Of Economic Entomology 113: 2595–2603.

    Article  PubMed  Google Scholar 

  • Saito, T., and M. Brownbridge. 2021. Efficacy of Anystis baccarum against foxglove aphids, Asulacarthum solani, in laboratory and small-scale greenhouse trials. Insects 12: 709.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sengoda, V. G., J. E. Munyaneza, J. M. Crosslin, J. L. Buchman, and H. R. Pappu. 2010. Phenotypic and etiological differences between psyllid yellows and zebra chip diseases of potato. American Journal Of Potato Research 87: 41–49.

    Article  Google Scholar 

  • Sheppard, S. K., and J. D. Harwood. 2005. Advances in molecular ecology: tracking trophic links through predator-prey food-webs. Functional Ecology 19: 751–762.

    Article  Google Scholar 

  • Solomon, M. G., J. V. Cross, J. D. Fitzgerald, C. A. M. Campbell, R. L. .Jolly, R. W. Olszak, E.Niemczyk, and H. Vogt. 2000. Biocontrol of pests of apples and pears in Northern and Central Europe-3. Predators. Biocontrol Science And Technology 10: 91–128.

    Article  Google Scholar 

  • Sorensen, J. T., D. N. Kinn, R. L. Doutt, and J. R. Cate. 1976. Biology of the mite, Anystis agilis (Acari: Anystidae): a California vineyard predator. Annals Of The Entomological Society Of America 69: 905–910.

    Article  Google Scholar 

  • Staudacher, K., M. Jonsson, and M. Traugott. 2016. Diagnostic PCR assays to unravel food web interactions in cereal crops with focus on biological control of aphids. Journal Of Pest Science 89: 281–293.

    Article  PubMed  Google Scholar 

  • Sumner-Kalkun, J. C., M. J. Sjölund, Y. M. Arnsdorf, M. Carnegie, F. Highet, and D. Ouvrard. 2020. A diagnostic real-time PCR assay for the rapid identification of the tomato-potato psyllid, Bactericera cockerelli (Šulc, 1909) and development of a psyllid barcoding database. PLoS one 15: e0230741.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Swisher, K. D., J. E. Munyaneza, and J. M. Crosslin. 2012. High resolution melting analysis of the cytochrome oxidase I gene identifies three haplotypes of the potato psyllid in the United States. Environmental Entomology 41: 1019–1028.

    Article  CAS  Google Scholar 

  • Symondson, W. O. C. 2002. Molecular identification of prey in predator diets. Mol Ecology 11: 627–641.

    Article  CAS  Google Scholar 

  • Teulon, D. A. J., P. J. Workman, K. L. Thomas, and M.-C. Nielsen. 2009. Bactericera cockerelli: incursion, dispersal and current distribution on vegetable crops in New Zealand. New Zealand Plant Protection 62: 136–144.

    Article  Google Scholar 

  • Thinakaran, J., D. R. Horton, W. R. Cooper, A. S. Jensen, C. H. Wohleb, J. Dahan, T. Mustafa, A. V. Karasev, and J. E. Munyaneza. 2017. Association of potato psyllid (Bactericera cockerelli; Hemiptera: Triozidae) with Lycium spp. (Solanaceae) in potato growing regions of Washington, Idaho, and Oregon. American Journal Of Potato Research 94: 490–499.

    Article  Google Scholar 

  • Ubick, D., P. Paquin, P. E. Cushing, and V. Roth, eds. 2005. Spiders of North America: an identification manual. 377 pages. American Arachnology Society.

  • Unruh, T. R., T. Yu, L. S. Willett, S. F. Garczynski, and D. R. Horton. 2008. Development of monoclonal antibodies to pear psylla (Hemiptera: Psyllidae) and evaluation of field predation by two key predators. Annals Of The Entomological Society Of America 101: 887–898.

    Article  CAS  Google Scholar 

  • Wallis, R. L. 1955. Ecological studies on the potato psyllid as a pest of potatoes. USDA Technical Bulletin 1107: 24 pp.

    Google Scholar 

  • Wenninger, E. J., J. Dahan, M. Thornton, and A. V. Karasev. 2019. Associations of the potato psyllid and “Candidatus Liberibacter solanacearum” in Idaho with the noncrop host plants bittersweet nightshade and field bindweed. Environmental Entomology 48: 747–754.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

Pauline Anderson and Heather Headrick provided technical support for psyllids and molecular testing. Funding was provided by Washington Potato Commission and by USDA-ARS Office of National Programs through the ARS-State Potato Partnership Program. Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the United States Department of Agriculture. USDA is an equal opportunity provider and employer.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to B. J. Ohler.

Ethics declarations

Conflict of Interest

The authors have no conflict of interest.

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ohler, B.J., Corral, C.A.R., Cooper, W.R. et al. Targeted RT-PCR Based Gut Content Analysis for Potato Psyllid Predation in Laboratory Assays. Am. J. Potato Res. 100, 371–381 (2023). https://doi.org/10.1007/s12230-023-09920-8

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12230-023-09920-8

Keywords

Navigation