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Predatory ability of the ant Crematogaster scutellaris on the brown marmorated stink bug Halyomorpha halys

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Abstract

The pest Halyomorpha halys is a recent example of severe worldwide biological invasion. In Italy, after the first detection in 2012, it has rapidly spread and economic damage has already been reported in commercial fruit orchards, eliciting enormous concern for Italian agricultural production. As a long-term solution, biological control investigations are focusing on the potential of natural antagonists, such as generalist predators, in the invaded areas. Due to their biology, ecology and behavior, ants represent one such generalist predator potentially suitable for inflicting mortality on H. halys. In this research, Crematogaster scutellaris was used as a study model. Specifically, the effect of ant predatory behavior on the survival of all H. halys pre-imaginal stages was tested in the laboratory environment. The results suggest that C. scutellaris has a significant predatory impact on all H. halys pre-imaginal stages except for eggs. The reduction of survivorship is between 95 and 85% for instars 1 and 2 and between 38 and 52% for instars 3, 4 and 5. The different levels of predation success suggest that these ants could act as useful generalist predators when associated with other antagonists and/or other control strategies. Although further field investigations are needed, the potential of ants as biocontrol agents of invasive species in agroecosystems deserves consideration in integrated pest management programs.

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References

  • Abram PK, Doyon J, Brodeur J et al (2015) Susceptibility of Halyomorpha halys (Hemiptera: Pentatomidae) eggs to different life stages of three generalist predators. Can Entomol 147:222–226. doi:10.4039/tce.2014.41

    Article  Google Scholar 

  • Baraibar B, Westerman PR, Carrión E, Recasens J (2009) Effects of tillage and irrigation in cereal fields on weed seed removal by seed predators. J Appl Ecol 46:380–387. doi:10.1111/j.1365-2664.2009.01614.x

    Article  Google Scholar 

  • Callot H, Brua C (2013) Halyomorpha halys (Stål, 1855), la Punaise diabolique, nouvelle espece pour la faune de France (Heteroptera Pentatomidae). L’Entomologiste 69:69–71

    Google Scholar 

  • Campolo O, Palmeri V, Malacrinò A et al (2015) Interaction between ants and the Mediterranean fruit fly: New insights for biological control. Biol Control 90:120–127. doi:10.1016/j.biocontrol.2015.06.004

    Article  Google Scholar 

  • Castracani C, Visicchio R, Grasso DA et al (2005) Behavioral bioassays testing the methyl 6-methylsalicylate as a component of the female sex pheromone in the slave-making ant Polyergus rufescens (Hymenoptera, Formicidae). J Insect Behav 18:685–692. doi:10.1007/s10905-005-7019-2

    Article  Google Scholar 

  • Castracani C, Tamarri V, Grasso DA et al (2008) Chemical communication in mating behaviour of the slave-making ant Polyergus rufescens (Hymenoptera, Formicidae): 3-ethyl-4-methylpentanol as a critical component of the queen sex pheromone. Insect Soc 55:137–143. doi:10.1007/s00040-008-0981-x

    Article  Google Scholar 

  • Castracani C, Grasso DA, Fanfani A, Mori A (2010) The ant fauna of Castelporziano Presidential Reserve (Rome, Italy) as a model for the analysis of ant community structure in relation to environmental variation in Mediterranean ecosystems. J Insect Conserv 14:585–594. doi:10.1007/s10841-010-9285-3

    Article  Google Scholar 

  • Castracani C, Maienza A, Grasso DA et al (2015) Biochar–macrofauna interplay: searching for new bioindicators. Sci Total Environ 536:449–456. doi:10.1016/j.scitotenv.2015.07.019

    Article  CAS  PubMed  Google Scholar 

  • Cerdá X, Dejean A (2011) Predation by ants on arthropods and other animals. In: Polidori C (ed) Predation in the Hymenoptera: an evolutionary perspective. Transworld Research Network, Kerala, pp 39–78

    Google Scholar 

  • Cesari M, Maistrello L, Ganzerli F et al (2015) A pest alien invasion in progress: potential pathways of origin of the brown marmorated stink bug Halyomorpha halys populations in Italy. J Pest Sci 88:1–7. doi:10.1007/s10340-014-0634-y

    Article  Google Scholar 

  • Cornelius ML, Dieckhoff C, Hoelmer KA et al (2016) Biological control of sentinel egg masses of the exotic invasive stink bug Halyomorpha halys (Stål) in Mid-Atlantic USA ornamental landscapes. Biol Control 103:11–20. doi:10.1016/j.biocontrol.2016.07.011

    Article  Google Scholar 

  • CREA (2015) Annuario dell’agricoltura italiana 2014. Consiglio per la ricerca in agricoltura e l’analisi dell’economia agraria, Roma

    Google Scholar 

  • De Oliveira RDF, De Almeida LC, De Souza DR et al (2012) Ant diversity (Hymenoptera: Formicidae) and predation by ants on the different stages of the sugarcane borer life cycle Diatraea saccharalis (Lepidoptera: Crambidae). Eur J Entomol 109:381

    Article  Google Scholar 

  • Del Toro I, Ribbons RR, Pelini SL (2012) The little things that run the world revisited: a review of ant-mediated ecosystem services and disservices (Hymenoptera: Formicidae). Myrmecol News 17:133–146

    Google Scholar 

  • Dioli P, Leo P, Maistrello L (2016) Prime segnalazioni in Spagna e in Sardegna della specie aliena Halyomorpha halys (Stål, 1855) e note sulla sua distribuzione in Europa (Hemiptera, Pentatomidae). Rev Gaditana Entomol 7:539–548

    Google Scholar 

  • Ehler LE (1990) Introduction strategies in biological control of insects. In: Mackauer M, Ehler LE, Roland J (eds) Critical Issues in Biological Control. Andover, Intercept, pp 111–134

    Google Scholar 

  • Fanfani R, Pieri R (2016) Il sistema agro-alimentare dell’Emilia-Romagna. Rapporto 2015. Unione regionale delle Camere di commercio dell’Emilia-Romagna Regione Emilia-Romagna, Assessorato agricoltura, caccia e pesca, Bologna

  • Goheen JR, Palmer TM (2010) Defensive plant-ants stabilize megaherbivore-driven landscape change in an African Savanna. Curr Biol 20:1768–1772. doi:10.1016/j.cub.2010.08.015

    Article  CAS  PubMed  Google Scholar 

  • Grasso DA, Pandolfi C, Bazihizina N et al (2015) Extrafloral-nectar-based partner manipulation in plant-ant relationships. AoB PLANTS 7:plv002. doi:10.1093/aobpla/plv002

    Article  PubMed  PubMed Central  Google Scholar 

  • Haye T, Fischer S, Zhang J, Gariepy T (2015a) Can native egg parasitoids adopt the invasive brown marmorated stink bug, Halyomorpha halys (Heteroptera: Pentatomidae), in Europe? J Pest Sci 88(4):693–705

    Article  Google Scholar 

  • Haye T, Gariepy T, Hoelmer K et al (2015b) Range expansion of the invasive brown marmorated stinkbug, Halyomorpha halys: an increasing threat to field, fruit and vegetable crops worldwide. J Pest Sci 88:665–673. doi:10.1007/s10340-015-0670-2

    Article  Google Scholar 

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

    Google Scholar 

  • Hölldobler B, Wilson EO (1990) The ants, new. edizione. Belknap Pr, Cambridge

    Google Scholar 

  • Hölldobler B, Wilson EO (2009) The superorganism: the beauty, elegance, and strangeness of insect societies, 1st edn. W. W. Norton and Company, New York

    Google Scholar 

  • Krispyn J, Todd J (1982) The red imported fire ant as a predator of the southern green stink bug. J Ga Entomol Soc 17:19–26

    Google Scholar 

  • Lee D-H (2015) Current status of research progress on the biology and management of Halyomorpha halys (Hemiptera: Pentatomidae) as an invasive species. Appl Entomol Zool 50:277–290. doi:10.1007/s13355-015-0350-y

    Article  CAS  Google Scholar 

  • Lee D-H, Short BD, Joseph SV et al (2013) Review of the biology, ecology, and management of Halyomorpha halys (Hemiptera: Pentatomidae) in China, Japan, and the Republic of Korea. Environ Entomol 42:627–641. doi:10.1603/EN13006

    Article  PubMed  Google Scholar 

  • Lee D-H, Nielsen AL, Leskey TC (2014a) Dispersal capacity and behavior of nymphal stages of Halyomorpha halys (Hemiptera: Pentatomidae) Evaluated under laboratory and field conditions. J Insect Behav 27:639–651. doi:10.1007/s10905-014-9456-2

    Article  Google Scholar 

  • Lee D-H, Short BD, Nielsen AL, Leskey TC (2014b) Impact of organic insecticides on the survivorship and mobility of Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) in the laboratory. Fla Entomol 97:414–421. doi:10.1653/024.097.0211

    Article  CAS  Google Scholar 

  • Lehner PN (1996) Selection of Statistical test. In: Lehner PN (ed) Handbook of Ethological methods. Cambridge University Press, Cambridge, pp 369–380

    Google Scholar 

  • Lenoir A, d’Ettorre P, Errard C, Hefetz A (2001) Chemical ecology and social parasitism in ants. Annu Rev Entomol 46:573–599

    Article  CAS  PubMed  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 23:218–226. doi:10.1564/23oct07

    Article  Google Scholar 

  • Leskey TC, Lee D-H, Short BD et al (2012b) Impact of insecticides on the invasive Halyomorpha halys (Hemiptera: Pentatomidae): analysis of insecticide lethality. J Econ Entomol 105:1726–1735. doi:10.1603/EC12096

    Article  CAS  PubMed  Google Scholar 

  • Leskey TC, Short BD, Butler BR, Wright SE (2012c) 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 J Entomol. doi:10.1155/2012/535062

    Google Scholar 

  • Lucky A, Savage AM, Nichols LM et al (2014) Ecologists, educators, and writers collaborate with the public to assess backyard diversity in The School of Ants Project. Ecosphere 5(7):78. doi:10.1890/ES13-00364.1

    Article  Google Scholar 

  • Macavei L, Bǎeţan R, Oltean I et al (2015) First detection of Halyomorpha halys, a new invasive species with a high potential of damage on agricultural crops in Romania. Lucr Stiintifice Ser Agron 58:105–108

    Google Scholar 

  • Maistrello L, Dioli P, Vaccari G et al (2014) First records in Italy of the Asian stinkbug Halyomorpha halys, a new threat to fruit crops. ATTI Giornate Fitopatologiche 1:283–288

    Google Scholar 

  • Maistrello L, Costi E, Caruso S et al (2016a) Halyomorpha halys in Italy: first results of field monitoring in fruit orchards. IOBC-WPRS Bull 112:1–5

    Google Scholar 

  • Maistrello L, Dioli P, Bariselli M et al (2016b) Citizen science and early detection of invasive species: phenology of first occurrences of Halyomorpha halys in Southern Europe. Biol Invasions 18:3109–3116. doi:10.1007/s10530-016-1217-z

    Article  Google Scholar 

  • Maňák V, Nordenhem H, Björklund N et al (2013) Ants protect conifer seedlings from feeding damage by the pine weevil Hylobius abietis. Agric For Entomol 15:98–105. doi:10.1111/j.1461-9563.2012.00597.x

    Article  Google Scholar 

  • Marlier JF, Quinet Y, de Biseau JC (2004) Defensive behaviour and biological activities of the abdominal secretion in the ant Crematogaster scutellaris (Hymenoptera: Myrmicinae). Behav Processes 67:427–440. doi:10.1016/j.beproc.2004.07.003

    Article  CAS  PubMed  Google Scholar 

  • Maurel JP, Blaye G, Valladares L et al (2016) Halyomorpha halys (Stål 1855), la punaise diabolique en France, à Toulouse (Heteroptera; Pentatomidae). Carnets Nat 3:21–25

    Google Scholar 

  • Milonas PG, Partsinevelos GK (2014) First report of brown marmorated stink bug Halyomorpha halys Stål (Hemiptera: Pentatomidae) in Greece. EPPO Bull 44:183–186. doi:10.1111/epp.12129

    Article  Google Scholar 

  • Mityushev IM (2016) First record of marmorated bug detection in Russia. Zashchita Karantin Rasteniĭ 3:48

    Google Scholar 

  • Morrison WR, Mathews CR, Leskey TC (2016) Frequency, efficiency, and physical characteristics of predation by generalist predators of brown marmorated stink bug (Hemiptera: Pentatomidae) eggs. Biol Control 97:120–130. doi:10.1016/j.biocontrol.2016.03.008

    Article  Google Scholar 

  • Morrison WR III, Bryant AN, Poling B, Quinn NF, Leskey TC (2017) Predation of Halyomorpha halys (Hemiptera: Pentatomidae) from web-building spiders associated with anthropogenic dwellings. J Insect Behav 30:70–85. doi:10.1007/s10905-017-9599-z

    Article  Google Scholar 

  • Offenberg J (2015) Review: ants as tools in sustainable agriculture. J Appl Ecol 52:1197–1205. doi:10.1111/1365-2664.12496

    Article  Google Scholar 

  • Ogburn EC, Bessin R, Dieckhoff C et al (2016) Natural enemy impact on eggs of the invasive brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), in organic agroecosystems: a regional assessment. Biol Control 101:39–51. doi:10.1016/j.biocontrol.2016.06.002

    Article  Google Scholar 

  • Olson DM, Ruberson JR (2012) Crop-specific mortality of southern green stink bug eggs in Bt- and non-Bt cotton, soybean and peanut. Biocontrol Sci Technol 22:1417–1428. doi:10.1080/09583157.2012.731495

    Article  Google Scholar 

  • Ottonetti L, Tucci L, Chelazzi G, Santini G (2008) Stable isotopes analysis to assess the trophic role of ants in a Mediterranean agroecosystem. Agric For Entomol 10:29–36

    Article  Google Scholar 

  • Pansa MG, Asteggiano L, Costamagna C et al (2013) First discovery of Halyomorpha halys in peach orchards in Piedmont. Informatore Agrario 69:60–61

    Google Scholar 

  • Rabitsch W, Friebe GJ (2015) From the west and from the east? First records of Halyomorpha halys (Stål 1855) (Hemiptera: Heteroptera: Pentatomidae) in Vorarlberg and Vienna. Beitr Entomof 16:115–139

    Google Scholar 

  • Rosumek FB, Silveira FAO, Neves F FDS et al (2009) Ants on plants: a meta-analysis of the role of ants as plant biotic defenses. Oecologia 160:537–549. doi:10.1007/s00442-009-1309-x

    Article  PubMed  Google Scholar 

  • Schatz B, Hossaert-McKey M (2010) Ants use odour cues to exploit fig–fig wasp interactions. Acta Oecol 36:107–113. doi:10.1016/j.actao.2009.10.008

    Article  Google Scholar 

  • Šeat J (2015) Halyomorpha halys (Stål, 1855) (Heteroptera: Pentatomidae) a new invasive species in Serbia. Acta Entomol Serbica 20:167–171

    Google Scholar 

  • Simov N (2016) The invasive brown marmorated stink bug Halyomorpha halys (Stål 1855 (Heteroptera: Pentatomidae) already in Bulgaria. Ecol Montenegrina 9:51–53

    Google Scholar 

  • Solida L, Scalisi M, Fanfani A et al (2010) Interspecific space partitioning during the foraging activity of two syntopic species of Messor harvester ants. J Biol Res 13:3–12

    Google Scholar 

  • Solida L, Grasso DA, Testi A et al (2011) Differences in the nesting sites microhabitat characteristics of two syntopic species of Messor harvester ants in a phytosociological homogeneous grassland area. Ethol Ecol Evol 23:229–239. doi:10.1080/03949370.2011.570379

    Article  Google Scholar 

  • Symondson WOC, Sunderland KD, Greenstone MH (2002) Can generalist predators be effective biocontrol agents? Annu Rev Entomol 47:561–594

    Article  CAS  PubMed  Google Scholar 

  • Tillman PG (2010) Parasitism and predation of stink bug (Heteroptera: Pentatomidae) eggs in Georgia corn fields. Environ Entomol 39:1184–1194. doi:10.1603/EN09323

    Article  CAS  PubMed  Google Scholar 

  • Tillman PG (2011) Natural biological control of stink bug (Heteroptera: Pentatomidae) Eggs in corn, peanut, and cotton farmscapes in Georgia. Environ Entomol 40:303–314. doi:10.1603/EN10154

    Article  Google Scholar 

  • Tillman PG, Greenstone MH, Hu JS (2015) Predation of stink bugs (Hemiptera: Pentatomidae) by a complex of predators in cotton and adjoining soybean habitats in Georgia, USA. Fla Entomol 98:1114–1126. doi:10.1653/024.098.0416

    Article  Google Scholar 

  • Tognon R, Sant’Ana J, Zhang Q-H, Millar JG, Aldrich JR, Zalom FG (2016) Volatiles Mediating Parasitism of Euschistus conspersus and Halyomorpha halys Eggs by Telenomus podisi and Trissolcus erugatus. J Chem Ecol 42:1016–1027. doi:10.1007/s10886-016-0754-

    Article  CAS  PubMed  Google Scholar 

  • USDA-NIFA SCRI (2017) Stop BMSB. Biology, ecology, and management of brown marmorated stink bug in specialty crop. In: Stop BMSB. http://www.stopbmsb.org. Accessed 20 Jan 2017

  • VéTek G, Papp V, Haltrich A, RéDei D (2014) First record of the brown marmorated stink bug, Halyomorpha halys (Hemiptera: Heteroptera: Pentatomidae), in Hungary, with description of the genitalia of both sexes. Zootaxa 3780:194–200. doi:10.11646/zootaxa.3780.1.8

    Article  PubMed  Google Scholar 

  • Wermelinger B, Wyniger D, Forster B (2008) First records of an invasive bug in Europe: Halyomorpha halys Stal (Heteroptera: Pentatomidae), a new pest on woody ornamentals and fruit trees? Mitteilungen-Schweiz Entomol Ges 81:1–8

    Google Scholar 

  • Zhu G, Bu W, Gao Y, Liu G (2012) Potential geographic distribution of brown marmorated stink bug invasion (Halyomorpha halys). PLoS ONE 7:e31246. doi:10.1371/journal.pone.0031246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This research has been supported by grants from University of Parma (UNIPR) assigned to Prof. A. Mori (FIL-2016) and Prof. D.A. Grasso (FIL-2015). The authors are grateful to Dr Karen E. Wells for English editing and to the reviewers for the valuable suggestions and the revision of the manuscript.

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Authors and Affiliations

  1. Department of Chemistry, Life Sciences and Environmental Sustainability, Università di Parma, Parco Area delle Scienze, 11/a, 43124, Parma, Italy

    Cristina Castracani, Giacomo Bulgarini, Daniele Giannetti, Fiorenza A. Spotti, Alessandra Mori & Donato A. Grasso

  2. Department of Life Sciences, Università di Modena Reggio Emilia, Via G. Amendola 2, 42122, Reggio-Emilia, Italy

    Lara Maistrello

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  1. Cristina Castracani
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  2. Giacomo Bulgarini
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  3. Daniele Giannetti
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  4. Fiorenza A. Spotti
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  6. Alessandra Mori
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  7. Donato A. Grasso
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Correspondence to Cristina Castracani.

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Communicated by T. Haye.

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

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Castracani, C., Bulgarini, G., Giannetti, D. et al. Predatory ability of the ant Crematogaster scutellaris on the brown marmorated stink bug Halyomorpha halys . J Pest Sci 90, 1181–1190 (2017). https://doi.org/10.1007/s10340-017-0889-1

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