Skip to main content
Log in

Behavioral Responses of the Social Wasp Polistes myersi to Prey Infected with Fungi Used in Biological Control

  • Published:
Journal of Insect Behavior Aims and scope Submit manuscript

Abstract

Metarhizium anisopliae and Beauveria bassiana are commonly used entomopathogenic fungi, but their non-target effects over generalist predatory insects, which can contribute to pest control, are not well known. We studied the capacity of the social wasp Polistes myersi to detect the pathogens in either a powdered form or in Galleria mellonella larvae infected with either of the two pathogens offered as prey. The effects of these treatments were compared considering wasp behaviors such as prey preference, frequency, duration and transitions of both hunting and grooming behaviors. Additionally, the effects of each entomopathogenic fungus on the wasp’s mortality were measured. Wasps seem not to detect the pathogens in powdered form but preferred healthy over infected larvae. Seventeen behavioral units for hunting and 34 for grooming were recognized. There were no differences in grooming frequency but there were significant differences on grooming duration, hunting behaviors and the patterns of transitions. Exposure of wasp colonies to either B. bassiana or M. anisopliae had no detectable impact on the mortality of adults, but mortality of larvae increased. For the first time, this study documented behavioral changes that indicated the capacity of social wasps to detect pathogens before physical contact and the display of hygienic strategies once contact occurs. The study also suggested a potential non-target effect of these entomopathogenic fungi on a generalist predator.

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

Data Availability

Authors are willing to provide data if required.

Code Availability

Not applicable.

References

  • Andrade FR, Prezoto F (2001) Horários de atividade forrageadora e material coletado por Polistes ferreri Saussure, 1853 (Hymenoptera, Vespidae), nas diferentes fases de seu ciclo biológico. Rev Bras Zool 3:117–128

    Google Scholar 

  • Arathi HS, Burns I, Spivak M (2000) Ethology of hygienic behaviour in the honey bee Apis mellifera L. (Hymenoptera: Apidae): behavioural repertoire of hygienic bees. Ethology 106:365–379

    Article  Google Scholar 

  • Babcock T, Borden JH, Gries R, Carroll C, Lafontaine JP, Moore M, Gries G (2019) Inter–kingdom signaling symbiotic yeasts produce semiochemicals that attract their yellowjacket hosts. Entomol Exp Appl 167:220–230

    Article  CAS  Google Scholar 

  • Baracchi D, Mazza G, Turillazzi S (2012) From individual to collective immunity: the role of the venom as antimicrobial agent in the Stenogastrinae wasp societies. J Insect Physiol 58:188–193

    Article  CAS  PubMed  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Casida JE, Durkin KA (2013) Neuroactive insecticides: targets. Selectivity, Resistance, and Secondary Effects Annu Rev Entomol 58:99–117

    CAS  PubMed  Google Scholar 

  • Castrillo LA, Griggs MH, Liu H, Bauer LS, Vandenberg JD (2010) Assessing deposition and persistence of Beauveria bassiana GHA (Ascomycota: Hypocreales) applied for control of the emerald ash borer, Agrilus planipennis (Coleoptera: Buprestidae), in a commercial tree nursery. Biol Control 54:61–67

    Article  Google Scholar 

  • Cheruiyot SK, Lattorff HMG, Kahuthia-Gathu R, Mbugi JP, Muli E (2018) Varroa-specific hygienic behavior of Apis mellifera scutellata in Kenya. Apidologie 49:439–449

    Article  CAS  Google Scholar 

  • Colwell RK (2013) EstimateS: statistical estimation of species richness and shared species from samples. Version 9.1.0. Persistent purl.oclc.org/estimates

  • Cruz JF, Durán T, Navarro V, Fierro J, Pardo D (2017) Field evaluation of Beauveria bassiana as biological control of ticks Rhipicephalus microplus in Colombia. Thünen Report 54:564–567

    Google Scholar 

  • Danfa A, Van der Valk HCHG (1999) Laboratory testing of Metarhizium spp. and Beauveria bassiana on Sahelian non-target arthropods. Biocontrol Sci Techn 9:187–198

    Article  Google Scholar 

  • Davis TS, Crippen TL, Hofstetter RW, Tomberlin JK (2013) Microbial volatile emissions as insect semiochemicals. J Chem Ecol 39:840–859

    Article  CAS  PubMed  Google Scholar 

  • de Conceição JP, de Lyra Neves CM, da Silva Sodré G, de Carvalho CAL, Souza AV, Ribeiro GS, de Campos Pereira R (2014) Susceptibility of Melipona scutellaris Latreille, 1811 (Hymenoptera: Apidae) worker bees to Beauveria bassiana (Bals.). Vuill Sociobiology 61:184–188

    Google Scholar 

  • Elisei T, Vaz J, Junior CR, Junior AJF, Prezoto F (2011) Uso da vespa social Polistes versicolor no controle de desfolhadores de eucalipto. Pesqui Agropecu Bras 45:958–964

    Article  Google Scholar 

  • Ellis AR, Burchett WW, Harrar SW, Bathke AC (2017) Nonparametric inference for multivariate data: the R package npmv. J Stat Softw 76:1–18

    Google Scholar 

  • Elmquist DC, Landolt PJ (2018) Associative learning of food odors by the European paper wasp, Polistes dominulus Christ (Hymenoptera, Vespidae). Environ Entomol 47:960–968

    Article  CAS  PubMed  Google Scholar 

  • Espinosa-Ortiz E, Lara-Reyna J, Otero-Colina G, Alatorre-Rosas R, Valdez-Carrasco J (2011) Susceptibilidad de larvas, pupas y abejas adultas a aislamientos de Beauveria bassiana (Bals.) Vuill., Metarhizium anisopliae (Sorokin) y Paecilomyces fumosoroseus (Wize). Interciencia 36:148–152

    Google Scholar 

  • Fox J, Weisberg S (2019) An R Companion to Applied Regression. 3rd edn. Sage, Thousand Oaks CA. https://socialsciences.mcmaster.ca/jfox/Books/Companion/

  • Harris RJ, Harcourt SJ, Glare TR, Rose EAF, Nelson TJ (2000) Susceptibility of Vespula vulgaris (Hymenoptera: Vespidae) to generalist entomopathogenic fungi and their potential for wasp control. J Invertebr Pathol 75:251–258

    Article  CAS  PubMed  Google Scholar 

  • Hokkanen HMT, Zeng QQ, Menzler-Hokkanen I (2003) Assessing the impacts of Metarhizium and Beauveria on bumblebees. In: Hokkanen HMT, Hajek AE (eds) Environmental impacts of microbial insecticides. Springer, Dordrecht, pp 63–71

    Chapter  Google Scholar 

  • Joop G, Vilcinskas A (2016) Coevolution of parasitic fungi and insect hosts. Zoology 119:350–358

    Article  PubMed  Google Scholar 

  • Lacey LA, Grzywacz D, Shapiro-Ilan DI, Frutos R, Brownbridge M, Goettel MS (2015) Insect pathogens as biological control agents: Back to the future. J Inv Path 132:1–41

    Article  CAS  Google Scholar 

  • Landolt PJ, Cha DH, Werle CT, Adamczyk JJ, Meagher RL, Gilbride RL, Clepper TS, Reed HC, Teal PEA, Sampson BJ (2014) Polistes spp. (Hymenoptera: Vespidae) orientation to wine and vinegar. Fla Entomol 97:1620–1630

    Article  Google Scholar 

  • Van Leeuwen, Vontas J, Tsagkarakou A, Dermauw W, Tirry L (2010) Acaricide resistance mechanisms in the two-spotted spider mite Tetranychus urticae and other important Acari: a review. Ins Biochem Mol Biol 40: 563–572

  • Lehner PN (1979) Handbook of ethological methods. Garland STPM Press, New York

    Google Scholar 

  • Liu C, Bathke AC, Harrar SW (2011) A nonparametric version of Wilks’ lambda asymptotic results and small sample approximations. Stat Probabil Let 81:1502–1506

    Article  Google Scholar 

  • Lord JC (2001) Response of the wasp Cephalonomia tarsalis (Hymenoptera: Bethylidae) to Beauveria bassiana (Hyphomycetes: Moniliales) as free conidia or infection in its host, the Sawtoothed grain beetle, Oryzaephilus surinamensis (Coleoptera: Silvanidae). Biol Control 21:300–304

    Article  Google Scholar 

  • Mackenzie JK, Landolt PJ, Richard SZ (2008) Sex attraction in Polistes dominulus (Christ) demonstrated using olfactometers and morphological source extracts. J Entomol Soc Brit Columbia 105:35–44

    Google Scholar 

  • Madden AA, Grassetti A, Soriano JN, Starks PT (2013) Actinomycetes with antimicrobial activity isolated from paper wasp (Hymenoptera: Vespidae: Polistinae) nests. Environ Entomology 42:703–710

    Article  Google Scholar 

  • Manfredini F, Dallai R, Ottaviani E (2008) Circulating hemocytes from larvae of the paper wasp Polistes dominulus (Hymenoptera, Vespidae). Tissue Cell 40:103–112

    Article  PubMed  Google Scholar 

  • Masterman R, Ross R, Mesce K, Spivak M (2001) Olfactory and behavioral response thresholds to odors of diseased brood differ between hygienic and non-hygienic honey bees (Apis mellifera L.). J Comp Physiol A 187:441–452

    Article  CAS  PubMed  Google Scholar 

  • Mburu DM, Ochola L, Maniania NK, Njagi PGN, Gitonga LM, Ndung’u MW, Hassanali A (2009) Relationship between virulence and repellency of entomopathogenic isolates of Metarhizium anisopliae and Beauveria bassiana to the termite Macrotermes michaelseni. J Insect Physiol 55:774–780

    Article  CAS  PubMed  Google Scholar 

  • Meikle M, Nansen G (2007) Duration and spread of an entomopathogenic fungus, Beauveria bassiana (Deuteromycota: Hyphomycetes), used to treat varroa mites (Acari: Varroidae) in honey bee (Hymenoptera: Apidae) hives. J Econ Entomol 100:1–10

    Article  CAS  PubMed  Google Scholar 

  • Mesquita ALM, Lacey LA (2001) Interactions among the entomopathogenic fungus, Paecilomyces fumosoroseus (Deuteromycotina: Hyphomycetes), the parasitoid, Aphelinus asychis (Hymenoptera: Aphelinidae), and their aphid host. Biol Control 22:51–59

    Article  Google Scholar 

  • Meyling NV, Pell JK (2006) Detection and avoidance of an entomopathogenic fungus by a generalist insect predator. Ecol Entomol 31:162–171

    Article  Google Scholar 

  • Mukherjee K, Altincicek B, Hain T, Domann E, Vilcinskas A, Chakraborty T (2010) Galleria mellonella as a model system for studying Listeria pathogenesis. Appl Environ Microbiol 76:310–317

    Article  CAS  PubMed  Google Scholar 

  • Mylonakis E, Moreno R, El Khoury JB, Idnurm A, Heitman J, Calderwood SB, Ausubel FM, Diener A (2005) Galleria mellonella as a model system to study Cryptococcus neoformans pathogenesis. Infect Immun 73:3842–3850

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oi DH, Pereira RM (1993) Ant behavior and microbial pathogens (Hymenoptera: Formicidae). Fla Entomol 76:63–74

    Article  Google Scholar 

  • Otterstatter MC, Thomson JD (2017) Does pathogen spillover from commercially reared bumble bees threaten wild pollinators? PLoS One 3:e2771

    Article  Google Scholar 

  • Poidatz J, Plantey RL, Thiéry D (2018) Indigenous strains of Beauveria and Metharizium as potential biological control agents against the invasive hornet Vespa velutina. J Invertebr Pathol 153:180–185

    Article  CAS  PubMed  Google Scholar 

  • Poulsen M, Bot AN, Boomsma JJ (2003) The effect of metapleural gland secretion on the growth of a mutualistic bacterium on the cuticle of leaf-cutting ants. Naturwissenschaften 90:406–409

    Article  CAS  PubMed  Google Scholar 

  • Prior C (1997) Susceptibility of target acridoids and non-target organisms to Metarhizium anisopliae and M. flavoviride, in: Krall, S., Peveling, R., and Diallo, B. D. (ed.), New strategies in locust control. Birkhäuser Basel, pp. 369–375

  • Rännbäck LM, Cotes B, Anderson P, Rämert B, Meyling NV (2015) Mortality risk from entomopathogenic fungi affects oviposition behavior in the parasitoid wasp Trybliographa rapae. J Invertebr Pathol 124:78–86

    Article  PubMed  Google Scholar 

  • Roy HE, Steinkraus DC, Eilenberg J, Hajek AE, Pell JK (2006) Bizarre interactions and endgames: entomopathogenic fungi and their arthropod hosts. Annu Rev Entomol 51:331–357

    Article  CAS  PubMed  Google Scholar 

  • Sadd BM, Barribeau SM (2013) Heterogeneity in infection outcome: lessons from a bumblebee–trypanosome system. Parasite Immunol 35:339–349

    CAS  PubMed  Google Scholar 

  • Sarmiento C (1997) Véspidos de Colombia (Hymenoptera: Vespidae) (Tesis dissertation, M. Sc. Universidad Nacional de Colombia, Instituto de Ciencias Naturales, Bogotá)

  • Sumana A, Starks PT (2004) Grooming patterns in the primitively eusocial wasp Polistes dominulus. Ethology 110:825–833

    Article  Google Scholar 

  • Thompson SR, Brandenburg RL, Arends JJ (2006) Impact of moisture and UV degradation on Beauveria bassiana (Balsamo) Vuillemin conidial viability in turfgrass. Biol Control 39:401–407

    Article  Google Scholar 

  • Vänninen I, Tyni-Juslin J, Hokkanen H (2000) Persistence of augmented Metarhizium anisopliae and Beauveria bassiana in Finnish agricultural soils. Biocontrol 45:201–222

    Article  Google Scholar 

  • Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New York

    Book  Google Scholar 

  • Wagner-Ziemka A, Gonzalez-Szwacka A, Korczynska J, Kieruzel M, Fialkowska B, Godzinska EJ (2008) Comparison of the behavior of nurses and foragers of the carpenter ant, Camponotus melanocnemis, during dyadic Nestmate Reunion tests carried out after a period of social isolation (Hymenoptera: Formicidae). Sociobiology 52:667–702

    Google Scholar 

Download references

Acknowledgements

The authors thank Juan José Lagos Oviedo, Andrea Carvajal, Angie Zuleidi Amézquita, André Rodríguez, and Angela Amarillo for help with field and colony management. Authors also thank Casa Buenos Aires for lodging and to the Universidad Nacional de Colombia for funding this study.

Funding

This project was founded by the Vicerrectoría of the Universidad Nacional de Colombia grant number Hermes 34846.

Author information

Authors and Affiliations

Authors

Contributions

DM-Ch.: conceptualization, data curation, formal analysis, research, methodology, validation, visualization, writing - original draft, writing - review and editing. NCCC: Colony maintenance and data curation. CR: conceptualization, data curation, formal analysis, funding acquisition, research, methodology. CES: conceptualization, formal analysis, Funding acquisition, methodology, project administration, resources, supervision, visualization, writing - original draft, writing - review and editing.

Corresponding author

Correspondence to Carlos E. Sarmiento.

Ethics declarations

Ethics Approval

All applicable national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain studies with human participants.

Consent to Participate

Not applicable.

Consent for Publication

All authors agree.

Conflicts of Interest/Competing Interests

The authors declare that they 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.

Supplementary Information

ESM 1

(TIFF 596 kb)

ESM 2

(TIFF 587 kb)

ESM 3

(TIFF 548 kb)

ESM 4

(TIFF 549 kb)

ESM 5

(DOCX 16 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mayorga-Ch, D., Castro-Cortés, N.C., Rodríguez, C. et al. Behavioral Responses of the Social Wasp Polistes myersi to Prey Infected with Fungi Used in Biological Control. J Insect Behav 34, 136–149 (2021). https://doi.org/10.1007/s10905-021-09775-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10905-021-09775-z

Keywords

Navigation