Skip to main content
Log in

Performance and host finding behavior in relation to host age of Cosmocomoidea annulicornis, egg parasitoid of a sharpshooter vector of the citrus variegated chlorosis

  • Published:
BioControl Aims and scope Submit manuscript

Abstract

Cosmocomoidea annulicornis (Ogloblin) (Hymenoptera: Mymaridae) is a solitary egg parasitoid of the sharpshooter Tapajosa rubromarginata (Signoret) (Hemiptera: Cicadellidae), vector of the bacterium Xylella fastidiosa Wells, which causes citrus variegated chlorosis in citrus plants. The disease has been reported in several South American countries affecting commercial citrus orchards. A description on the general morphology of the egg of T. rubromarginata and the stages of embryonic development was performed to evaluate the developmental stages that C. annulicornis is able to attack. An assessment on parasitoid parasitism and emergence rates, developmental time and sex ratio was performed to determine the suitability of eggs of different ages (24, 48, 72, 96, 120 and 144 h old) as hosts. In addition, female response to olfactory cues was tested in a Y-tube olfactometer to assess whether host age affects foraging behavior. Embryogenesis would begin after 48 h from oviposition. Parasitism rate significantly varied among host ages, sharply decreasing in older eggs. Emergence rate and sex ratio of the offspring were affected by host age. Parasitoid developmental time was shorter for older host ages (120–144 h). Olfactometer assays showed that C. annulicornis females successfully detected plants carrying host eggs and that host age did not affect host searching behavior. Results reported suggest that host age influences parasitism efficiency of C. annulicornis, but does not play a major role in modulating host searching behavior in response to odors emitted by plants carrying eggs of different ages, as females did not discriminate between fresh and older eggs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

Data availability

The datasets generated and analyzed during the current study are available from the corresponding author on request.

Code availability

Not applicable.

References

  • Abe Y (2009) The effect of the age of the serpentine leafminer Liriomyza trifolii (Diptera: Agromyzidae) on parasitism by the parasitoid wasp Gronotoma micromorpha (Hymenoptera: Figitidae: Eucoilinae). Eur J Entomol 106:595–598

    Article  Google Scholar 

  • Al-Wahaibi AK, Morse JG (2009) Egg morphology and stages of embryonic development of the glassy-winged sharpshooter (Hemiptera: Cicadellidae). Ann Entomol Soc Am 102:241–248

    Article  Google Scholar 

  • Bari MN, Jahan M, Islam KS, Ali MP (2016) Host egg age and supplementary diet influence the parasitism activity of Trichogramma zahiri (Hymenoptera: Trichogrammatidae). J Econ Entomol 109:1102–1108

    Article  CAS  PubMed  Google Scholar 

  • Baumann P (2005) Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu Rev Microbiol 59:155–189

    Article  CAS  PubMed  Google Scholar 

  • Boivin G (2010) Phenotypic plasticity and fitness in egg parasitoids. Neotrop Entomol 39:457–463

    Article  PubMed  Google Scholar 

  • Bin F, Vinson SB, Strand MR, Colazza S, Jones Jr WA (1993) Source of an egg kairomone for Trissolcus basalis, a parasitoid of Nezara viridula. Physiol Entomol 18:7–15

  • Charnov EL, Skinner SW (1985) Complementary approaches to the understanding of parasitoid oviposition decisions. Environ Entomol 14:383–391

    Article  Google Scholar 

  • Chen WL, Leopold RA, Morgan DJ, Harris MO (2006) Development and reproduction of the egg parasitoid, Gonatocerus ashmeadi girault (Hymenoptera: Mymaridae), as a function of temperature. Environ Entomol 35:1178–1187

    Article  Google Scholar 

  • Chen YM, Qu XR, Li TH, Igbal A, Wang X, Ren ZY, Desneux N, Zang LS (2021) Performances of six eupelmid egg parasitoids from China on Japanese giant silkworm Caligula japonica with different host age regimes. J Pest Sci 94:309–319

    Article  Google Scholar 

  • Clausen CP (1940) Entomophagous insects. McGraw-Hill, New York

    Google Scholar 

  • Colazza S, Fucarino A, Peri E, Salerno G, Conti E, Bin F (2004) Insect oviposition induces volatile emission in herbaceous plants that attracts egg parasitoids. J Exp Biol 207:47–53

    Article  PubMed  Google Scholar 

  • Colinet H, Salin C, Boivin G, Hance TH (2005) Host age and fitness-related traits in a koinobiont aphid parasitoid. Ecol Entomol 30:473–479

    Article  Google Scholar 

  • Dellapé G, Paradell SL (2013) New records of Proconiini (Hemiptera: Cicadellidae) from Argentina. Rev Soc Entomol Arg 72:231–235

    Google Scholar 

  • Dellapé G, Paradell S, Semorile L, Delfederico L (2016) Potential vectors of Xylella fastidiosa: a study of leafhoppers and treehoppers in citrus agroecosystems affected by citrus variegated chlorosis. Entomol Exp Appl 161:92–103

    Article  Google Scholar 

  • Denno RF, Roderick GK (1990) Population biology of planthoppers. Annu Rev Entomol 35:489–520

    Article  Google Scholar 

  • Fatouros NE, Bukovinszkine’Kiss G, Dicke M, Hilker M (2007) The response specificity of Trichogramma egg parasitoids towards infochemicals during host location. J Insect Behav 20:53–65

    Article  Google Scholar 

  • Freytag PH (1985) The insect parasites of leafhoppers, and related groups. In: Nault LR, Rodriguez J (eds) The leafhoppers and planthoppers. Wiley, New York, pp 423–467

    Google Scholar 

  • Gabriel D, Gottwald TR, Lopes SA, Wulff NA (2020) Bacterial pathogens of citrus: citrus canker, citrus variegated chlorosis and huanglongbing. In: Talon M, Caruso M, Gmitter FG (eds) The genus citrus. Woodhead Publishing, Elsevier, Duxford, pp 371–389

    Chapter  Google Scholar 

  • Gonçalves FP, Stuchi ES, da Silva SR, Reiff ET, Amorim L (2011) Role of healthy nursery plants in orange yield during eight years of citrus variegated chlorosis epidemics. Sci Hort 129:343–345

    Article  Google Scholar 

  • Hilker M, Meiners T (2006) Early herbivore alert: insect eggs induce plant defense. J Chem Ecol 32:1379–1397

    Article  CAS  PubMed  Google Scholar 

  • Hill JG, Luft Albarracin E, Coll Araoz MV, Virla EG (2019) Effects of host species and host age on biological parameters of Anagrus virlai (Hymenoptera: Mymaridae), an egg parasitoid of Dalbulus maidis (Hemiptera: Cicadellidae) and Peregrinus maidis (Hemiptera: Delphacidae). Biol Control 131:74–80

    Article  Google Scholar 

  • Hou YY, Yang X, Zang LS, Zhang C, Monticelli LS, Desneux N (2018) Effect of oriental armyworm Mythimna separata egg age on the parasitism and host suitability for five Trichogramma species. J Pest Sci 91:1181–1189

    Article  Google Scholar 

  • Irvin N, Hoddle MS (2005a) Determination of Homalodisca coagulata (Hemiptera: Cicadellidae) egg ages suitable for oviposition by Gonatocerus ashmeadi, Gonatocerus triguttatus, and Gonatocerus fasciatus (Hymenoptera: Mymaridae). Biol Control 32:391–400

    Article  Google Scholar 

  • Irvin N, Hoddle MS (2005b) The competitive ability of three mymarid egg parasitoids (Gonatocerus spp.) for glassy-winged sharpshooter (Homalodisca coagulata) eggs. Biol Control 34:204–214

    Article  Google Scholar 

  • Irvin NA, Hoddle MS (2010) Comparative assessments of Gonatocerus ashmeadi and the ‘new association’ parasitoid Gonatocerus tuberculifemur (Hymenoptera: Mymaridae) as biological control agents of Homalodisca vitripennis (Hemiptera: Cicadellidae). Biol Control 55:186–196

    Article  Google Scholar 

  • Irvin N, Suarez-Espinoza J, Hoddle M (2009) Functional response of Gonatocerus ashmeadi and the “new association” parasitoid G. tuberculifemur attacking eggs of Homalodisca vitripennis. Environ Entomol 38:1634–1641

    Article  PubMed  Google Scholar 

  • Jacob HS, Joder A, Batchelor KL (2006) Biology of Stethynium sp. (Hymenoptera: Mymaridae), a native parasitoid of an introduced weed biological control agent. Environ Entomol 35:630–636

    Article  Google Scholar 

  • King BH (2000) Sex ratio and oviposition responses to host age and the fitness consequences to mother and offspring in the parasitoid wasp Spalangia endius. Behav Ecol Sociobiol 48:316–320

    Article  Google Scholar 

  • Kobiałka M, Michalik A, Walczak M, Junkiert Ł, Szklarzewicz T (2016) Sulcia symbiont of the leafhopper Macrosteles laevis (Ribaut, 1927) (Insecta, Hemiptera, Cicadellidae: Deltocephalinae) harbors Arsenophonus bacteria. Protoplasma 253:903–912

    Article  PubMed  Google Scholar 

  • Krugner R, Sisterson MS, Lin H (2012) Effects of gender, origin, and age on transmission of Xylella fastidiosa to grapevines by Homalodisca vitripennis (Hemiptera: Cicadellidae). Ann Entomol Soc Am 105:280–286

    Article  Google Scholar 

  • Laranjeira FF, Silva LG, Fonseca EL, Silva SX, Rocha JB, Santos-Filho HP, Ledo CAS, Hau B (2008) Prevalence, incidence and distribution of citrus variegated chlorosis in Bahia, Brazil. Trop Plant Pathol 33:339–347

    Article  Google Scholar 

  • Lawrence PO (1990) The biochemical and physiological effects of insect hosts on the development and ecology of their insect parasites: an overview. Arch Insect Biochem Physiol 13:217–228

    Article  CAS  Google Scholar 

  • Li WB, Zhou CH, Pria WD, Teixeira DC, Miranda VS, Pereira EO, Ayres AJ, He CH, Costa PI, Hartung JS (2002) Citrus and coffee strains of Xylella fastidiosa induce Pierce’s disease in grapevine. Plant Dis 86:1206–1210

    Article  PubMed  Google Scholar 

  • Li WB, Pria WD, Lacava PM, Qin X, Hartung JS (2003) Presence of Xylella fastidiosa in sweet orange fruit and seeds and its transmission to seedlings. Phytopathology 93:953–958

    Article  PubMed  Google Scholar 

  • Logarzo GA, Virla EG, Triapitsyn SV, Jones WA (2004) Biology of Zagella delicata (Hymenoptera: Trichogrammatidae), an egg parasitoid of the sharpshooter Tapajosa rubromarginata (Hemiptera: Clypeorrhyncha: Cicadellidae) in Argentina. Fla Entomol 87:511–517

    Article  Google Scholar 

  • Luft Albarracin E, Virla EG, Ordano M (2021) Influence of the site of oviposition on the level of egg parasitism in the corn leafhopper, Dalbulus maidis (Hemiptera: Cicadellidae). An Acad Bras Cienc 93(1):e20190686

    Article  Google Scholar 

  • Lytle JM, Bernal JS, Morse JG (2012) Biology of Pseudoligosita plebeia (Hymenoptera: Trichogrammatidae), an egg parasitoid of Homalodisca spp. (Hemiptera: Cicadellidae) collected from Northwestern Mexico as a potential biocontrol agent of H. vitripennis in California. J Econ Entomol 105:1532–1539

    Article  CAS  PubMed  Google Scholar 

  • Mackauer M, Sequeira R, Otto M (1997) Growth and development in parasitoid wasps: adaptation to variable host resources. In: Dettmer K, Baur G, Volkl W (eds) Vertical food web interactions. Springer, Berlin, pp 191–203

    Chapter  Google Scholar 

  • Manzano C, Benzal G, Logarzo GA, Coll Araoz MV, Virla EG, Luft Albarracin E (2021) Biological traits of Cosmocomoidea annulicornis (Hymenoptera: Mymaridae), an egg parasitoid of the sharpshooter Tapajosa rubromarginata (Hemiptera: Cicadellidae), a vector of Xylella fastidiosa in citrus orchards. Biol Control 157:104589

    Article  Google Scholar 

  • Moran NA, Dale C, Dunbar H, Smith WA, Ochman H (2003) Intracellular symbionts of sharpshooters (Insecta: Hemiptera: Cicadellinae) form a distinct clade with a small genome. Environ Microbiol 5:116–126

    Article  CAS  PubMed  Google Scholar 

  • Mutitu EK, Garnas JR, Hurley BP, Wingfield MJ, Harney M, Bush SJ, Slippers B (2013) Biology and rearing of Cleruchoides noackae (Hymenoptera: Mymaridae), an egg parasitoid for the biological control of Thaumastocoris peregrinus (Hemiptera: Thaumastocoridae). J Econ Entomol 106:1979–1985

    Article  PubMed  Google Scholar 

  • Noda H, Watanabe K, Kawai S, Yukuhiro S, Miyoshi T, Tomizawa M, Koizumi Y, Nikoh N, Fukatsu T (2012) Bacteriome-associated endosymbionts of the green rice leafhopper Nephotettix cincticeps (Hemiptera: Cicadellidae). Appl Entomol Zool 47:217–225

    Article  CAS  Google Scholar 

  • Otto M, Mackauer M (1998) The developmental strategy of an idiobiont ectoparasitoid, Dendrocerus carpenteri: influence of variations in host quality on offspring growth and fitness. Oecologia 117:353–364

    Article  PubMed  Google Scholar 

  • Parra JRP (2009) Mass rearing of egg parasitoids for biological control programs. In: Cônsoli F, Parra J, Zucchi R (eds) Egg parasitoids in agroecosystems with emphasis on Trichogramma. Springer, Dordrecht, pp 267–292

    Chapter  Google Scholar 

  • Pashalidou FG, Gols R, Berkhout BW, Weldegergis BT, van Loon JJ, Dicke M, Fatouros NE (2014) To be in time: egg deposition enhances plant-mediated detection of young caterpillars by parasitoids. Oecologia 177:477–486

    Article  PubMed  Google Scholar 

  • Peña JE, Jacas JA, Triapitsyn S, Ulmer BJ, Duncan RE (2009) Biological control with egg parasitoids other than Trichogramma—the citrus and grape cases. In: Cônsoli F, Parra J, Zucchi R (eds) Egg parasitoids in agroecosystems with emphasis on Trichogramma. Springer, Dordrecht, pp 341–371

    Chapter  Google Scholar 

  • Peñaflor MFGV, de Moraes Sarmento MM, Bezerra da Silva CS, Werneburg AG, Bento JMS (2012) Effect of host egg age on preference, development and arrestment of Telenomus remus (Hymenoptera: Scelionidae). Eur J Entomol 109:15–20

    Article  Google Scholar 

  • Pizzol J, Desneux N, Wajnberg E, Thiéry D (2012) Parasitoid and host egg ages have independent impact on various biological traits in a Trichogramma species. J Pest Sci 85:489–496

    Article  Google Scholar 

  • R Core Team (2021) R: A language and environment for statistical computing. R Foundation for statistical computing, Vienna, Austria. https://www.r-project.org/. Accessed 10 Oct 2021

  • Redak RA, Purcell AH, Lopes JR, Blua MJ, Mizell RF, Andersen PC (2004) The biology of xylem fluid–feeding insect vectors of Xylella fastidiosa and their relation to disease epidemiology. Annu Rev Entomol 49:243–270

    Article  CAS  PubMed  Google Scholar 

  • Roitberg BD, Boivin G, Vet LEM (2001) Fitness, parasitoids, and biological control: an opinion. Can Entomol 133:429–438

    Article  Google Scholar 

  • Takiya DM, Tran PL, Dietrich CH, Moran NA (2006) Co-cladogenesis spanning three phyla: leafhoppers (Insecta: Hemiptera: Cicadellidae) and their dual bacterial symbionts. Mol Ecol 15:4175–4191

    Article  CAS  PubMed  Google Scholar 

  • Tian JC, Wang ZC, Wang GR, Zhong LQ, Zheng XS, Xu HX, Zang LS, Lu ZX (2017) The effects of temperature and host age on the fecundity of four Trichogramma species, egg parasitoids of the Cnaphalocrocis medinalis (Lepidoptera: Pyralidae). J Econ Entomol 110:949–953

    Article  PubMed  Google Scholar 

  • Vet LE, Hemerik L, Visser ME, Wäckers FL (2002) Flexibility in host-search and patch-use strategies of insect parasitoids. In: Lewis EE, Campbell JF, Sukhedo MVK (eds) The behavioural ecology of parasites. CABI Publishing, Wallingford, pp 39–64

    Chapter  Google Scholar 

  • Vinson SB (1998) The general host selection behavior of parasitoid hymenoptera and a comparison of initial strategies utilized by larvaphagous and oophagous species. Biol Control 11:79–96

    Article  Google Scholar 

  • Vinson SB, Iwantsch GF (1980) Host suitability for insect parasitoids. Annu Rev Entomol 25:397–419

    Article  Google Scholar 

  • Virla EG, Luft Albarracin E (2012) Potencialidad de especies antagonistas en el manejo racional de poblaciones de vectores de enfermedades del maíz causadas por virus en Argentina. In: Pecci MPG, Laguna LG, Lenardón S (eds) Enfermedades del maíz producidas por virus y mollicutes en Argentina. Buenos Aires, Argentina, pp 151–168

    Google Scholar 

  • Virla EG, Logarzo GA, Jones WA, Triapitsyn S (2005) Biology of Gonatocerus tuberculifemur (Hymenoptera: Mymaridae), an egg parasitoid of the sharpshooter, Tapajosa rubromarginata (Hemiptera: Cicadellidae). Fla Entomol 88:67–72

    Article  Google Scholar 

  • Virla EG, van Nieuwenhove GA, Palottini F, Triapitsyn SV, Logarzo GA (2019) Spatial and seasonal distribution of egg parasitoids of the sharpshooter Tapajosa rubromarginata (Hemiptera: Cicadellidae: Proconiini) on feral Johnson grass and commercial citrus host in Argentina. Biol Control 132:81–88

    Article  Google Scholar 

  • Zhang JJ, Ren BZ, Yuan XH, Zang LS, Ruan CC, Sun GZ, Shao XW (2014) Effects of host-egg ages on host selection and suitability of four Chinese Trichogramma species, egg parasitoids of the rice striped stem borer, Chilo suppressalis. BioControl 59:159–166

    Article  CAS  Google Scholar 

  • Zhou Y, Abram PK, Boivin G, Brodeur J (2014) Increasing host age does not have the expected negative effects on the fitness parameters of an egg parasitoid. Entomol Exp App 151:106–111

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by PICT 2015 1147 (FONCYT, Fondo para la Investigación Científica y Tecnológica, Argentina). We thank to “Vivero Lules” for providing the citrus plants used in assays. Carolina Manzano thanks CONICET (Consejo Nacional de Investigaciones Científicas y Técnicas, Argentina) for the scholarship granted

Author information

Authors and Affiliations

Authors

Contributions

ELA, MVCA and EGV conceived the research. CM and NAM conducted insect field collections. CM carried out the experiments, conducted statistical analyses and wrote the manuscript. ELA, EGV and MVCA supervised the project, revised the manuscript and secured funding. All authors helped shape the research, analysis and approved the manuscript.

Corresponding author

Correspondence to Erica Luft Albarracin.

Ethics declarations

Conflict of interest

The authors declare that they do not have any conflict of interest associated with this work.

Additional information

Handling Editor: Stefano Colazza.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 15 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Manzano, C., Melchert, N.A., Coll Araoz, M.V. et al. Performance and host finding behavior in relation to host age of Cosmocomoidea annulicornis, egg parasitoid of a sharpshooter vector of the citrus variegated chlorosis. BioControl 67, 27–37 (2022). https://doi.org/10.1007/s10526-021-10121-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-021-10121-7

Keywords