Skip to main content
SpringerLink
Log in

Assessing the use of antimicrobials to sterilize brown marmorated stink bug egg masses and prevent symbiont acquisition

  • Original Paper
  • Published:
Journal of Pest Science Aims and scope Submit manuscript

Abstract

The brown marmorated stink bug, Halyomorpha halys (Stål), is dependent on a beneficial obligate symbiont for successful development, survival, and fecundity. The bacteria are deposited on the egg mass surface by the female, and first instar nymphs become inoculated with the bacteria by feeding on the egg chorions upon hatching. Targeting the bacteria exposed on the egg mass surface may prove to be a viable management strategy for the stink bug. Egg masses were surface-treated with several antimicrobials and surfactants to determine whether exposure to these products adversely affected the fitness of newly hatched nymphs and/or sterilized the egg mass surface to prevent nymphal acquisition of the symbiont. Laboratory results showed that egg hatch rate was significantly reduced by Agri-Mycin and Naiad, nymphal survival was significantly impacted by AzaGuard and Naiad, and symbiont acquisition was significantly disrupted by Naiad, AzaGuard, and Liquid Copper Fungicide. Under field conditions, there were no significant treatment effects on nymphal survival or symbiont acquisition, but egg hatch rate was reduced by Naiad and Triton-X. Products with both antimicrobial effects and the ability to penetrate the coating covering the bacteria provided the best chance for disrupting symbiont acquisition.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abe Y, Mishiro K, Takanashi M (1995) Symbiont of brown-winged green bug, Plautia stali Scott. Jpn J Appl Entomol Zool 39(2):109–115

    Article  Google Scholar 

  • Bansal R, Michel AP, Sabree ZL (2014) The crypt-dwelling primary bacterial symbiont of the polyphagous pentatomid pest Halyomorpha halys (Hemiptera: Pentatomidae). Environ Entomol 43(3):617–625

    Article  CAS  PubMed  Google Scholar 

  • Bing X, Yang J, Zchori-Fein E, Wang X, Liu S (2012) Characterization of a newly discovered symbiont of the whitefly Bemisia tabaci (Hemiptera: Aleyrodidae). Appl Environ Microbiol 79(2):569–575

    Article  PubMed  Google Scholar 

  • Buchner P (1965) Endosymbionts of animals with plant microorganisms. Interscience, New York

    Google Scholar 

  • Donald KJ, Clarke HV, Mitchell C, Cornwell RM, Hubbard SF, Karley AJ (2016) Protection of pea aphids associated with coinfecting bacterial symbionts persists during superparasitism by a braconid wasp. Microbiol Ecol 71(1):1–4

    Article  CAS  Google Scholar 

  • Douglas AE (1998) Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43(1):17–37

    Article  CAS  PubMed  Google Scholar 

  • Douglas AE (2007) Symbiotic microorganisms: untapped resources for insect pest control. Trends Biotechnol 25(8):338–342

    Article  CAS  PubMed  Google Scholar 

  • Enders LS, Miller NJ (2016) Stress-induced changes in abundance differ among obligate and facultative endosymbionts of the soybean aphid. Ecol Evol 6(3):818–829

    Article  PubMed  PubMed Central  Google Scholar 

  • Ferrater JB, de Jong PW, Dicke M, Chen YH, Horgan FG (2013) Symbiont-mediated adaptation by planthoppers and leafhoppers to resistant rice varieties. Arthropod Plant Interact 7(6):591–605

    Article  Google Scholar 

  • Fukatsu T, Hosokawa T (2002) Capsule-transmitted gut symbiotic bacterium of the Japanese common plataspid stinkbug, Megacopta punctatissima. Appl Environ Microbiol 68(1):389–396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haye T, Gariepy T, Hoelmer K, Rossi J, Streito J, Tassus X, Desneux N (2015) Range expansion of the invasive brown marmorated stinkbug, Halyomorpha halys: an increasing threat to field, fruit and vegetable crops worldwide. J Pest Sci 88(4):665–673

    Article  Google Scholar 

  • Himler AG, Adachi-Hagimori T, Bergen JE, Kozuch A, Kelly SE, Tabashnik BE, Chiel E, Duckworth VE, Dennehy TJ, Zchori-Fein E, Hunter MS (2011) Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. Science 332(6026):254–256

    Article  CAS  PubMed  Google Scholar 

  • Hoebeck ER, Carter ME (2003) Halyomorpha halys (Stål) (Heteroptera: Pentatomidae): a polyphagous plant pest from Asia newly detected in North America. Proc Entomol Soc Wash 105(1):225–237

    Google Scholar 

  • Irish BM, Correll JC, Morelock TE (2002) The effect of synthetic surfactants on disease severity of white rust on spinach. Plant Dis 86(7):791–796

    Article  CAS  Google Scholar 

  • Kaiwa N, Hosokawa T, Kikuchi Y, Nikoh N, Meng XY, Kimura N, Ito M, Fukatsu T (2010) Primary gut symbiont and secondary, Sodalis-allied symbiont of the scutellerid stinkbug Cantao ocellatus. Appl Environ Microbiol 76(11):3486–3494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kenyon LJ, Meulia T, Sabree ZL (2015) Habitat visualization and genomic analysis of “Candidatus Pantoea carbekii”, the primary symbiont of the brown marmorated stink bug. Genome Biol Evol 7(2):620–635

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leskey TC, Hamilton GC, Nielsen AL et al (2012a) Pest status of the brown marmorated stink bug, Halyomorpha halys in the USA. Outlooks Pest Manag 23(5):218–226

    Article  Google Scholar 

  • Leskey TC, Short BD, Butler BR, Wright SE (2012b) Impact of the invasive brown marmorated stink bug, Halyomorpha halys (Stål), in mid-Atlantic tree fruit orchards in the United States: case studies of commercial management. Psyche 2012:1–14

  • Mathews CR, Barry S (2014) Compost tea reduces egg hatch and early-stage nymphal development of Halyomorpha halys (Hemiptera: Pentatomidae). Fla Entomol 97(4):1726–1732

    Article  Google Scholar 

  • Mickler CJ (2002) Evaluation of surfactants and new oomycete fungicides for the control of Phytophthora root rot of citrus, caused by Phytophthora parasitica, Doctoral Dissertation. OCLC Number 802370720

  • Moran NA, Telang A (1998) Bacteriocyte-associated symbionts of insects. Bioscience 48(4):295–304

    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(2):116–126

    Article  CAS  PubMed  Google Scholar 

  • Moran NA, Tran P, Gerardo NM (2005) Symbiosis and insect diversification: an ancient symbiont of sap-feeding insects from the bacterial phylum Bacteroidetes. Appl Environ Microbiol 71(12):8802–8810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moran NA, Mccutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42(1):165–190

    Article  CAS  PubMed  Google Scholar 

  • Noda H, Watanabe K, Kawai S, Yukuhiro F, 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(3):217–225

    Article  CAS  Google Scholar 

  • Oliver KM, Russell JA, Moran NA, Hunter MS (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci USA 100(4):1803–1807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Otero-Bravo A, Sabree ZL (2015) Inside or out? Possible genomic consequences of extracellular transmission of crypt-dwelling stinkbug mutualists. Front Ecol Evol 3:64

    Article  Google Scholar 

  • Prado SS, Almeida RP (2009) Role of symbiotic gut bacteria in the development of Acrosternum hilare and Murgantia histrionica. Entomol Exp Appl 132(1):21–29

    Article  Google Scholar 

  • Prado SS, Zucchi TD (2012) Host-symbiont interactions for potentially managing heteropteran pests. Psyche 2012:1–9

    Article  Google Scholar 

  • Prado SS, Rubinoff D, Almeida RP (2006) Vertical transmission of a pentatomid caeca-associated symbiont. Ann Entomol Soc Am 99(3):577–585

    Article  Google Scholar 

  • SAS Institute Inc. (2013) The SAS System, Release 9.4. Cary, NC

  • Stanghellini ME (1987) Inhibitory and lytic effects of a nonionic surfactant on various asexual stages in the life cycle of Pythium and Phytophthora species. Phytopathology 77(1):112

    Article  CAS  Google Scholar 

  • Stanghellini ME (1996) Control of root rot of peppers caused by Phytophthora capsica with a nonionic surfactant. Plant Dis 80(10):1113

    Article  Google Scholar 

  • Stanghellini ME, Miller RM (1997) BIOSURFACTANTS: Their identity and potential efficacy in the biological control of zoosporic plant pathogens. Plant Dis 81(1):4–12

    Article  CAS  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(13):4175–4191

    Article  CAS  PubMed  Google Scholar 

  • Taylor CM, Coffey PL, Delay BD, Dively GP (2014) The importance of gut symbionts in the development of the brown marmorated stink bug, Halyomorpha halys (Stål). PLoS One 9(3):e90312

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu D, Daugherty SC, Van Aken SE, Pai GH, Watkins KL, Khouri H, Tallon LJ, Zaborsky JM, Dunbar HE, Tran PL, Moran NA, Eisen JA (2006) Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters. PLoS Biol 4(6):e188

    Article  PubMed  PubMed Central  Google Scholar 

  • Zchori-Fein E, Brown JK (2002) Diversity of prokaryotes associated with Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae). Ann Entomol Soc Am 95(6):711–718

    Article  Google Scholar 

  • Zhang Y, Cao W, Zhong L, Godfray HC, Liu X (2016) Host plant determines the population size of an obligate symbiont Buchnera aphidicola in aphids. Appl Environ Microbiol 82(8):2336–2346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank Dr. Kathryn Everts for her assistance in choosing the products tested in the study, as well as Dr. Julie Dunning-Hotopp and Nikhil Kumar for providing the positive control primers used to test the quality of the DNA samples. We also thank Dr. Thomas Kuhar for providing locations in Virginia to collect H. halys adults when populations were low in Maryland. This work was funded by the following grant: United States Department of Agriculture-National Institute of Food and Agriculture (USDA-NIFA) Specialty Crop Research Initiative (SCRI) #2011-51181-30937: Biology, Ecology, and Management of Brown Marmorated Stink Bug in orchard Crops, Small Fruit, Grapes, Vegetables and Ornamentals. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Author information

Authors and Affiliations

  1. Department of Entomology, University of Maryland, College Park, MD, USA

    Christopher Taylor, Veronica Johnson & Galen Dively

Authors
  1. Christopher Taylor
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Veronica Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Galen Dively
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christopher Taylor.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by T. Haye.

“Special Issue: The brown marmorated stink bug Halyomorpha halys - an emerging pest of global concern”.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Taylor, C., Johnson, V. & Dively, G. Assessing the use of antimicrobials to sterilize brown marmorated stink bug egg masses and prevent symbiont acquisition. J Pest Sci 90, 1287–1294 (2017). https://doi.org/10.1007/s10340-016-0814-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10340-016-0814-z

Keywords

Search

Navigation