Skip to main content
Log in

Tamarixia triozae, an important parasitoid of Bactericera cockerelli: circadian rhythms and their implications in pest management

  • Published:
BioControl Aims and scope Submit manuscript

Abstract

Tamarixia triozae (Burks) (Hymenoptera: Eulophidae) is an important primary parasitoid of Bactericera cockerelli (Šulc) (Hemiptera: Triozidae). This study aimed to unveil the parasitoid’s circadian rhythms and provide information for enhancement of its biological control. Most emergence occurred in the morning and most mating took place early next morning. Oviposition only occurred during the daytime, peaking between mid-morning and mid-afternoon while host feeding had three peaks in the early morning, late afternoon and dawn, respectively. We demonstrate that circadian activity peaks for different life functions did not overlap, suggesting that T. triozae have developed strategies for maximal fitness gain. These findings have implications in pest management, which can be tested under field conditions. For example, release of sexually mature and host-fed adults in the early morning may help achieve better control. Moreover, insecticide sprays, when necessary, may be applied as late in the evening as possible to reduce side effects on this parasitoid.

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
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Archontoulis SV, Miguez FE (2015) Nonlinear regression models and applications in agricultural research. Agron J 107:786–798

    Article  Google Scholar 

  • Barnes H (2017) New biocontrol agent released. NZGrower 72:18–20

    Google Scholar 

  • Bertossa RC, van Dijk J, Beersma DG, Beukeboom LW (2010) Circadian rhythms of adult emergence and activity but not eclosion in males of the parasitic wasp Nasonia vitripennis. J Insect Physiol 56:805–812

    Article  CAS  PubMed  Google Scholar 

  • Bertossa RC, van Dijk J, Diao W, Saunders D, Beukeboom LW, Beersma DG (2013) Circadian rhythms differ between sexes and closely related species of Nasonia wasps. PLoS ONE 8(3):e60167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bravo M, López L (2007) Principales plagas del chile de agua en los valles centrales de Oaxaca. Agroprod Fund Prod Oaxaca AC 7:12–15

    Google Scholar 

  • Brown MW, Schmitt JJ (2001) Seasonal and diurnal dynamics of beneficial insect populations in apple orchards under different management intensity. Environ Entomol 30:415–424

    Article  Google Scholar 

  • Burger JM, Kormany A, van Lenteren JC, Vet LE (2005) Importance of host feeding for parasitoids that attack honeydew-producing hosts. Entomol Exp Appl 117:147–154

    Article  Google Scholar 

  • Buteler M, Stadler T (2011) A review on the mode of action and current use of petroleum distilled spray oils. In: Stoytcheva M (ed) Pesticides in the modern world—pesticides use and management. InTech, pp 119–136

  • Butler CD, Trumble JT (2012a) The potato psyllid, Bactericera cockerelli (Sulc) (Hemiptera: Triozidae): life history, relationship to plant diseases, and management strategies. Terr Arthropod Rev 5:87–111

    Article  Google Scholar 

  • Butler CD, Trumble JT (2012b) Identification and impact of natural enemies of Bactericera cockerelli (Hemiptera: Triozidae) in southern California. J Econ Entomol 105:1509–1519

    Article  PubMed  Google Scholar 

  • CABI (2018) Invasive species compendium - Bactericera cockerelli (tomato/potato psyllid). https://www.cabi.org/isc/datasheet/45643#tosummaryOfInvasiveness. Accessed 16 April 2020

  • Caudillo Ruiz K (2010) Descripción morfológica, biología y susceptibilidad de Tamarixia triozae (Burks) (Hymenoptera: Eulophidae), parasitoide de Bactericera cockerelli (Sulc) (Hemiptera: Triozidae), a diferentes insecticidas. Masters thesis, Universidad Michoacana de San Nicolás de Hidalgo, Morelia, Michoacan, Mexico

  • Cerna E, Ochoa Y, Aguirre L, Flores M, Landeros J (2013) Determination of insecticide resistance in four populations of potato psillid Bactericera cockerelli (Sulc.) (Hemiptera: Triozidae). Int J Exp Bot 82:63–68

    Google Scholar 

  • Cerón-González C, Lomeli-Flores JR, Rodríguez-Leyva E, Torres-Ruíz A (2014) Fecundidad y alimentación de Tamarixia triozae (Hymenoptera: Eulophidae) sobre el psílido de la papa Bactericera cockerelli. Rev Mex Cienc Agríc 5:893–899

    Google Scholar 

  • Chávez EC, Bautista OH, Flores JL, Uribe LA, Fuentes YMO (2015) Insecticide-resistance ratios of three populations of Bactericera cockerelli (Hemiptera: Psylloidea: Triozidae) in regions of northern Mexico. Fla Entomol 98:950–953

    Article  Google Scholar 

  • Cranshaw W (1994) The potato (tomato) psyllid, Paratrioza cockerelli (Sulc), as a pest of potatoes. In: Zehnder GW, Powelson ML, Hansson RK, Raman KV (eds) Advances in potato pest biology and management. APS Press, St. Paul, pp 83–95

    Google Scholar 

  • Crosslin JM, Munyaneza JE, Brown JK, Liefting LW (2010) A history in the making: potato zebra chip disease associated with a new psyllid-borne bacterium—A tale of striped potatoes. https://www.apsnet.org/edcenter/apsnetfeatures/Pages/PotatoZebraChip.aspx. Accessed 13 May 2020

  • Dávila M, Cerna C, Aguirre U, García M, Ochoa F, Gallegos M, Landeros F (2012) Susceptibility and resistance mechanisms to insecticides in Bactericera cockerelli (Sulc.) in Coahuila, Mexico. Rev Mex Cienc Agríc 3:1145–1155

    Google Scholar 

  • England S (1995) Diel emergence patterns of the parasitoid Bathyplectes curculionis (Thomson) (Hymenoptera: Ichneumonidae) at two photoperiods. J Kansas Entomol Soc 68:470–473

    Google Scholar 

  • Fantinou A, Alexandri M, Tsitsipis J (1998) Adult emergence rhythm of the egg-parasitoid Telenomus busseolae. BioControl 43:141–151

    Article  Google Scholar 

  • FAO (2017) Detection of Bactericera cockerelli (tomato-potato psyllid) in Western Australia.

  • https://www.ippc.int/en/countries/australia/pestreports/2017/02/detection-of-bactericera-cockerelli-tomato-potato-psyllid-in-western-australia/. Accessed 16 April 2020

  • Gebiola M, Gomez-Marco F, Simmons GS, Stouthamer R (2018) Effect of host feeding on life history traits of Tamarixia radiata, parasitoid of the Asian citrus psyllid, Diaphorina citri. BioControl 63:763–771

    Article  Google Scholar 

  • Gharalari A, Nansen C, Lawson D, Gilley J, Munyaneza J, Vaughn K (2009) Knockdown mortality, repellency, and residual effects of insecticides for control of adult Bactericera cockerelli (Hemiptera: Psyllidae). J Econ Entomol 102:1032–1038

    Article  CAS  PubMed  Google Scholar 

  • Hanan A, He XZ, Shakeel M, Wang Q (2009) Diurnal rhythms of emergence, host feeding and oviposition of Eretmocerus warrae (Hymenoptera: Aphelinidae). N Z Plant Prot 62:156–160

    Google Scholar 

  • He XZ, Wang Q, Teulon DAJ (2004) Emergence, sexual maturation and oviposition of Aphidius ervi (Hymenoptera: Aphidiidae). N Z Plant Prot 57:214–220

    Google Scholar 

  • Jervis M, Kidd N (1986) Host-feeding strategies in hymenopteran parasitoids. Biol Rev 61:395–434

    Article  Google Scholar 

  • Julious SA (2004) Using confidence intervals around individual means to assess statistical significance between two means. Pharm Stat J Appl Stat Pharm Ind 3:217–222

    Google Scholar 

  • Kainoh Y (1986) Mating behavior of Ascogaster reticulatus Watanabe (Hymenoptera: Braconidae), an egg-larval parasitoid of the smaller tea tortrix moth, Adoxophyes sp. (Lepidoptera: Tortricidae) I. Diel patterns of emergence and mating, and some conditions for mating. Appl Entomol Zool 21:1–7

    Article  Google Scholar 

  • Karpova S (2006) The role of endogenous and exogenous factors in regulation of synchronous emergence of Trichogramma embryophagum Hartig and T. principium Sug. et Sor. (Hymenoptera, Trichogrammatidae). Entomol Rev 86:252–263

    Article  Google Scholar 

  • Lankinen P (1986) Geographical variation in circadian eclosion rhythm and photoperiodic adult diapause in Drosophila littoralis. J Comp Physiol A 159:123–142

    Article  Google Scholar 

  • Li XW, Jiang HX, Zhang XC, Shelton AM, Feng JN (2014) Post-mating interactions and their effects on fitness of female and male Echinothrips americanus (Thysanoptera: Thripidae), a new insect pest in China. PLoS ONE 9(1):e87725

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu TX, Stansly PA (1995) Toxicity and repellency of some biorational insecticides to Bemisia argentifolii on tomato plants. Entomol Exp Appl 74:137–143

    Article  Google Scholar 

  • Liu TX, Zhang YM, Peng LN, Rojas P, Trumble JT (2012) Risk assessment of selected insecticides on Tamarixia triozae (Hymenoptera: Eulophidae), a parasitoid of Bactericera cockerelli (Hemiptera: Trizoidae). J Econ Entomol 105:490–496

    Article  CAS  PubMed  Google Scholar 

  • Luna-Cruz A, Lomeli-Flores JR, Rodríguez-Leyva E, Ortega-Arenas LD, Huerta-de La Peña A (2011) Toxicidad de cuatro insecticidas sobre Tamarixia triozae (Burks) (Hymenoptera: Eulophidae) y su hospedero Bactericera cockerelli (Sulc) (Hemiptera: Triozidae). Acta Zool Mex 27:509–526

    Google Scholar 

  • Marchand D, McNeil JN (2000) Effects of wind speed and atmospheric pressure on mate searching behavior in the aphid parasitoid Aphidius nigripes (Hymenoptera: Aphidiidae). J Insect Behav 13:187–199

    Article  Google Scholar 

  • Martinez AM, Chavarrieta JM, Morales SI, Caudillo KB, Figueroa JI, Diaz O, Bujanos R, Gomez B, Viñuela E, Pineda S (2015) Behavior of Tamarixia triozae females (Hymenoptera: Eulophidae) attacking Bactericera cockerelli (Hemiptera: Triozidae) and effects of three pesticides on this parasitoid. Environ Entomol 44:3–11

    Article  CAS  PubMed  Google Scholar 

  • McClure M, Whistlecraft J, McNeil JN (2007) Courtship behavior in relation to the female sex pheromone in the parasitoid, Aphidius ervi (Hymenoptera: Braconidae). J Chem Ecol 33:1946–1959

    Article  CAS  PubMed  Google Scholar 

  • Miranda M, Sivinski J, Rull J, Cicero L, Aluja M (2015) Niche breadth and interspecific competition between Doryctobracon crawfordi and Diachasmimorpha longicaudata (Hymenoptera: Braconidae), native and introduced parasitoids of Anastrepha spp. fruit flies (Diptera: Tephritidae). Biol Control 82:86–95

    Article  Google Scholar 

  • Morales SI, Martínez AM, Viñuela E, Chavarrieta JM, Figueroa JI, Schneider MI, Tamayo F, Pineda S (2018) Lethal and sublethal effects on Tamarixia triozae (Hymenoptera: Eulophidae), an ectoparasitoid of Bactericera cockerelli (Hemiptera: Triozidae), of three insecticides used on solanaceous crops. J Econ Entomol 111:1048–1055

    Article  CAS  PubMed  Google Scholar 

  • Morbey YE, Ydenberg RC (2001) Protandrous arrival timing to breeding areas: a review. Ecol Lett 4:663–673

    Article  Google Scholar 

  • Munyaneza J, Crosslin J, Upton J (2007) Association of Bactericera cockerelli (Homoptera: Psyllidae) with “zebra chip”, a new potato disease in southwestern United States and Mexico. J Econ Entomol 100:656–663

    Article  CAS  PubMed  Google Scholar 

  • Munyaneza JE (2012) Zebra chip disease of potato: biology, epidemiology, and management. Am J Potato Res 89:329–350

    Article  Google Scholar 

  • Munyaneza JE, Buchman JL, Upton JE, Goolsby JA, Crosslin JM, Bester G, Miles GP, Sengoda VG (2008) Impact of different potato psyllid populations on zebra chip disease incidence, severity, and potato yield. Subtrop Plant Sci 60:27–37

    Google Scholar 

  • Ogden S (2011) Tomato potato psyllid and liberibacter in New Zealand—Impact and research programme overview. In: Workneh F, Rashed A, Rush CM (eds) Proceedings of the 11th annual zebra chip reporting session. San Antonio, TX, pp 173–177

  • Panda S, Hogenesch JB, Kay SA (2002) Circadian rhythms from flies to human. Nature 417:329–335

    Article  CAS  PubMed  Google Scholar 

  • Pérez-Sayas C, Aguilar-Fenollosa E, Hurtado MA, Jaques JA, Pina T (2018) When do predatory mites (Phytoseiidae) attack? Understanding their diel and seasonal predation patterns. Insect Sci 25:1056–1064

    Article  PubMed  Google Scholar 

  • Prager S, Kund G, Trumble J (2016) Low-input, low-cost IPM program helps manage potato psyllid. Calif Agric 70:89–95

    Article  Google Scholar 

  • Quicke DLJ (1997) Parasitic wasps. Chapman Hall, London

    Google Scholar 

  • Ramírez-Ahuja ML, Rodríguez-Leyva E, Lomeli-Flores JR, Torres-Ruiz A, Guzmán-Franco AW (2017) Evaluating combined use of a parasitoid and a zoophytophagous bug for biological control of the potato psyllid, Bactericera cockerelli. Biol Control 106:9–15

    Article  Google Scholar 

  • Rojas P, Rodríguez-Leyva E, Lomeli-Flores JR, Liu TX (2015) Biology and life history of Tamarixia triozae, a parasitoid of the potato psyllid Bactericera cockerelli. BioControl 60:27–35

    Article  Google Scholar 

  • Rymer J, Bauernfeind AL, Brown S, Page TL (2007) Circadian rhythms in the mating behavior of the cockroach, Leucophaea maderae. J Biol Rhythm 22:43–57

    Article  Google Scholar 

  • Sakurai G, Kasuya E (2008) The costs of harassment in the adzuki bean beetle. Anim Behav 75:1367–1373

    Article  Google Scholar 

  • SAS Institute Inc (2019) SAS/STAT® 14.3 User’s guide. SAS Institute Inc, Cary

  • Saunders DS (2002) Insect clocks. Elsevier Science Technology, Oxford

    Google Scholar 

  • Saunders DS (2020) Dormancy, diapause, and the role of the circadian system in insect photoperiodism. Annu Rev Entomol 65:373–389

    Article  CAS  PubMed  Google Scholar 

  • Szczepaniec A, Varela KA, Kiani M, Paetzold L, Rush CM (2019) Incidence of resistance to neonicotinoid insecticides in Bactericera cockerelli across Southwest US. Crop Prot 116:188–195

    Article  CAS  Google Scholar 

  • Teulon D, Workman P, Thomas K, Nielsen M (2009) Bactericera cockerelli: incursion, dispersal and current distribution on vegetable crops in New Zealand. N Z Plant Prot 62:136–144

    Google Scholar 

  • van Lenteren JC, Szabo P, Huisman PWT (1992) The parasite–host relationship between Encarsia formosa Gahan (Hymenoptera, Aphelinidae) and Trialeurodes vaporariorum (Westwood) (Homoptera, Aleyrodidae) XXXVII. Adult emergence and initial dispersal pattern of E. formosa. J Appl Entomol 114:392–399

    Article  Google Scholar 

  • Vaze KM, Sharma VK (2013) On the adaptive significance of circadian clocks for their owners. Chronobiol Int 30:413–433

    Article  PubMed  Google Scholar 

  • Vega Chávez JLA, Valdez MVMS (2010) Determinacion de alimentacion y preferencia de Tamarixia triozae (Burks) (Himenoptera: Eulophidae) sobre estadíos de Bactericera cockerelli (Sulc) (Hemíptera: Psillidae). Bacheloŕs thesis, Universidad Autónoma Agraria Antonio Narro, Saltillo, Coahuila, Mexico

  • Vogt EA, Nechols JR (1991) Diel activity patterns of the squash bug egg parasitoid Gryon pennsylvanicum (Hymenoptera: Scelionidae). Ann Entomol Soc Am 84:303–308

    Article  Google Scholar 

  • Waage JK, Ming NS (1984) The reproductive strategy of a parasitic wasp: I. optimal progeny and sex allocation in Trichogramma evanescens. J Anim Ecol 53:401–415

    Article  Google Scholar 

  • Weseloh RM (1972) Diel periodicities of some parasitoids of the gypsy moth and noctuid cutworms. Ann Entomol Soc Am 65:1126–1131

    Article  Google Scholar 

  • Wright PJ, Walker GP, MacDonald FH, Gardner-Gee R, Hedderley DI (2017) Mineral oil foliar applications in combination with insecticides affect tomato potato psyllid (Bactericera cockerelli) and beneficial insects in potato crops. N Z J Crop Hortic Sci 45:263–276

    Article  CAS  Google Scholar 

  • Yang XB, Campos-Figueroa M, Silva A, Henne DC (2015) Functional response, prey stage preference, and mutual interference of the Tamarixia triozae (Hymenoptera: Eulophidae) on tomato and bell pepper. J Econ Entomol 108:414–424

    Article  PubMed  Google Scholar 

  • Yang XB, Liu TX (2009) Life history and life tables of Bactericera cockerelli (Homoptera: Psyllidae) on eggplant and bell pepper. Environ Entomol 38:1661–1667

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Mr. B. Gatimel and Mr. J. Thompson of Bioforce Ltd., Auckland, New Zealand, for providing the insects for this study and advice on their rearing, and the handling editor, Editor-in-Chief and two anonymous reviewers for their constructive comments, which have significantly improved the paper. This work was supported by the China Scholarship Council-Massey University Joint Scholarship Program and a Massey University Research Fund.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Qiao Wang.

Ethics declarations

Conflict of interest

All authors declare that we have made all efforts to meet the standard and believe that we have met the standard.

Additional information

Handling Editor: Josep Anton Jaques Miret.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, C., He, X.Z., Zhou, P. et al. Tamarixia triozae, an important parasitoid of Bactericera cockerelli: circadian rhythms and their implications in pest management. BioControl 65, 537–546 (2020). https://doi.org/10.1007/s10526-020-10023-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-020-10023-0

Keywords

Navigation