Skip to main content
Log in

Parasitism-Mediated Interactions Between the Ring-Legged Earwig and Sugarcane Borer Larvae

  • Biological Control
  • Published:
Neotropical Entomology Aims and scope Submit manuscript

Abstract

Sugarcane is one of the most economically important crops in Brazil. The damage caused by Diatraea saccharalis (F.) (Lepidoptera: Crambidae) results in high costs for its production. Cotesia flavipes Cameron (Hymenoptera: Braconidae) is the most efficient means of controlling this pest. The prohibition of burning and the preservation of soil cover through non-tillage practices increased many population densities of natural enemies of the sugarcane borer (SCB) in sugarcane fields. Euborellia annulipes (Lucas) (Dermaptera: Anisolabididae) is a predator found in sugarcane fields and is associated with predation of SCB. This study aimed to evaluate the influence of parasitism of D. saccharalis by C. flavipes on predation by E. annulipes adult females. For this purpose, fourth instar sugarcane borer larvae were exposed to parasitism over a 5-day period or were not parasitized. Subsequently, the prey was supplied to the predator in arenas under choice and no-choice conditions and under different densities to evaluate the feeding preference over a 12-h period and functional response of the predator over a 24-h period. E. annulipes killed 2–3 fourth instar larvae of the sugarcane borer over a 12-h period. SCB parasitism did not affect the feeding preference of the predator and did not alter the type II functional response. However, the handling time of the predator was lower (1.943 h) and there was a higher T/Th ratio on the non-parasitized larvae (12.352). Our findings indicate E. annulipes as a promising biological control agent of D. saccharalis, with a potential to assist in the sugarcane borer management approaches and could to reduce the costs of parasitoid release in the field.

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.

Institutional subscriptions

Fig 1
Fig 2

Similar content being viewed by others

References

  • Abramson CI, Wanderley PA, Miná AJS, Wanderley MJA (2007) Capacity of earwig Marava arachidis (Yersin) to access fennel plants Foeniculum vulgare Mill in laboratory and field. Ciênc Rural 37:1524–1528

    Google Scholar 

  • Attarzadeh M, Rajabpour A, Farkhari M, Rasekh A (2019) Interactions between Orius albidipennis and Aphidius colemani (Hymenoptera: Braconidae) for the control of Aphis gossypii on greenhouse cucumber. J Crop Prot 8:21–31

    Google Scholar 

  • Beckage NE, Gelman DB (2004) Wasp parasitoid disruption of host development: implications for new biologically based strategies for insect control. Annu Rev Entomol 49:299–330

    CAS  PubMed  Google Scholar 

  • Bento CB, Filoso S, Pitombo LM, Cantarella H, Rossetto R, Martinelli LA, Carmo JB (2018) Impacts of sugarcane agriculture expansion over low-intensity cattle ranch pasture in Brazil on greenhouse gases. J Environ Manag 206:980–988

    CAS  Google Scholar 

  • Beuzelin JM, Akbar W, Mészáros A, Reay-Jones FPF, Reagan TE (2010) Field assessment of novaluron for sugarcane borer, Diatraea saccharalis (F.) (Lepidoptera: Crambidae), management in Louisiana sugarcane. Crop Prot 29:1168–1176

    CAS  Google Scholar 

  • Bilu E, Coll M (2009) Parasitized aphids are inferior prey for a coccinellid predator: implications for intraguild predation. Environ Entomol 38:153–158

    PubMed  Google Scholar 

  • Bordonal RO, Carvalho JLN, Lal R, Figueiredo EB, Oliveira BG, La Scala JN (2018) Sustainability of sugarcane production in Brazil. A review. Agron Sustain Dev 38:13. https://doi.org/10.1007/s13593-018-0490-x

    Article  Google Scholar 

  • Botelho PSM, Macedo N (2002) Cotesia flavipes para controle de Diatraea saccharalis. In: Parra JRP, Botelho PSM, Corrêa-Ferreira BS, Bento JMS (eds) Controle biológico no Brasil: parasitoides e predadores. Manole, São Paulo, pp 409–425

    Google Scholar 

  • Bukovinszky T, van Veen FF, Jongema Y, Dicke M (2008) Direct and indirect effects of resource quality on food web structure. Science 319:804–807

    CAS  PubMed  Google Scholar 

  • Butler SJ, Vickery JA, Norris K (2007) Farmland biodiversity and the footprint of agriculture. Science 315:381–384

    CAS  PubMed  Google Scholar 

  • Chailleux A, Bearez P, Pizzol J, Amiens-Desneux E, Ramirez-Romero R, Desneux N (2013) Potential for combined use of parasitoids and generalist predators for biological control of the key invasive tomato pest Tuta absoluta. J Pest Sci 86:533–541

    Google Scholar 

  • Chailleux A, Wajnberg E, Zhou Y, Amiens-Desneux E, Desneux N (2014) New parasitoid-predator associations: female parasitoids do not avoid competition with generalist predators when sharing invasive prey. Naturwissenschaften 101:1075–1083

    CAS  PubMed  Google Scholar 

  • Cherubin MR, Franco AL, Guimarães RM, Tormena CA, Cerri CE, Karlen DL, Cerri CC (2017) Assessing soil structural quality under Brazilian sugarcane expansion areas using Visual Evaluation of Soil Structure (VESS). Soil Tillage Res 173:64–74

    Google Scholar 

  • Colfer RJ, Rosenheim JA (2001) Predation on immature parasitoids and its impact on aphid suppression. Oecologia 126:292–304

    CAS  PubMed  Google Scholar 

  • Coll M, Wajnberg E (2017) Environmental pest management: challenges for agronomists, economists, and policymakers. John Wiley and Sons 448 pp

  • Di Stefano J (2005) Effect size estimates and confidence intervals: an alternative focus for the presentation and interpretation of ecological data. In: Burk AR (ed) New trends in ecology research. New York, Nova Science, pp 71–102

    Google Scholar 

  • Dias-Pini NDS, Broglio SMF, Costa SDS, Santos JMD, Guzzo EC (2012) Biological characteristics of Telenomus alecto and Trichogramma galloi reared on eggs of the sugarcane borer Diatraea flavipennella. Rev Bras Entomol 56:515–518

    Google Scholar 

  • Dinardo-Miranda LL (2008) Pragas. In: Dinardo-Miranda LL, Vasconcelos ACM, Landell MGA (eds) . Cana-de-açúcar. Campinas, Instituto Agronômico, pp 349–404

    Google Scholar 

  • Dinardo-Miranda LL, Anjos IAD, Costa VPD, Fracasso JV (2012) Resistance of sugarcane cultivars to Diatraea saccharalis. Pesq Agropec Bras 47:1–7

    Google Scholar 

  • Dinardo-Miranda LL, Fracasso JV, Costa VP, Lopes OT (2014) Dispersal of Cotesia flavipes in sugarcane field and implications for parasitoid releases. Bragantia 73:163–170

    Google Scholar 

  • Frago E (2016) Interactions between parasitoids and higher order natural enemies: Intraguild predation and hyperparasitoids. Curr Opin Insect Sci 14:81–86

    PubMed  Google Scholar 

  • Franco AL, Bartz ML, Cherubin MR, Baretta D, Cerri CE, Feigl BJ, Wall DH, Davies CA, Cerri CC (2016) Loss of soil (macro) fauna due to the expansion of Brazilian sugarcane acreage. Sci Total Environ 563:160–168. https://doi.org/10.1016/j.scitotenv.2016.04.116

    Article  CAS  PubMed  Google Scholar 

  • Freitas FC, Castro AMC, Barbosa NCCP, Fernandes OA (2018) Characterization and comparison of genetic variation in Cotesia flavipes (Hymenoptera: Braconidae) mass reared for biological pest control using microsatellite markers. Neotrop Entomol 47:433–439

    CAS  PubMed  Google Scholar 

  • Gontijo LM, Beers EH, Snyder WE (2015) Complementary suppression of aphids by predators and parasitoids. Biol Control 90:83–91

    Google Scholar 

  • Hassell MP, Lawton JH, Beddington JR (1977) Sigmoid functional responses by invertebrate predators and parasitoids. J Anim Ecol 46:249–262

    Google Scholar 

  • Herrick NJ, Reitz SR, Carpenter JE, O’Brien CW (2008) Predation by Podisus maculiventris (Hemiptera: Pentatomidae) on Plutella xylostella (Lepidoptera: Plutellidae) larvae parasitized by Cotesia plutellae (Hymenoptera: Braconidae) and its impact on cabbage. Biol Control 45:386–395

    Google Scholar 

  • Holling CS (1959) Some characteristics of simple types of predation and parasitism. Can Entomol 91:384–398

    Google Scholar 

  • Holling CS (1966) The functional response of invertebrate predators to prey density. Mem Entomol Soc Can 98:5–86

    Google Scholar 

  • Huang F, Leonard BR, Andow DA (2007) Sugarcane borer (Lepidoptera: Crambidae) resistance to transgenic Bacillus thuringiensis maize. J Econ Ecol 100:164–171

    Google Scholar 

  • Juliano SA (2001) Nonlinear curve fitting: predation and functional response curves. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Oxford University Press, New York, pp 178–196

    Google Scholar 

  • Kaçar G, Wang XG, Biondi A, Daane KM (2017) Linear functional response by two pupal Drosophila parasitoids foraging within single or multiple patch environments. PLoS ONE 12:e0183525

    PubMed  PubMed Central  Google Scholar 

  • Kharboutli MS, Mack TP (1993) Effect of temperature, humidity, and prey density on feeding rate of the striped earwig (Dermaptera: Labiduridae). Environ Entomol 22:1134–1139

    Google Scholar 

  • Klostermeyer EC (1942) The life history and habits of the ringlegged earwig, Euborellia annulipes (Lucus) (Order Dermaptera). J Kansas Entomol Soc 15:13–18

    Google Scholar 

  • Kocarek P, Dvorak L, Kirstova M (2015) Euborellia annulipes (Dermaptera: Anisolabididae), a new alien earwig in Central European greenhouses: potential pest or beneficial inhabitant? Appl Entomol Zool 50:201–206

    CAS  Google Scholar 

  • Lemos WP, Ramalho FDS, Zanuncio JC (2003) Age-dependent fecundity and life-fertility tables for Euborellia annulipes (Lucas) (Dermaptera: Anisolabididae) a cotton boll weevil predator in laboratory studies with an artificial diet. Environ Entomol 32:592–601

    Google Scholar 

  • Manly BJF (1974) A model for certain types of selection experiments. Biometrics 30:281–294

    Google Scholar 

  • Michaud JP (2018) Problems inherent to augmentation of natural enemies in open agriculture. Neotrop Entomol 47:161–170

    CAS  PubMed  Google Scholar 

  • Moral RA, Demétrio CGB, Hinde J, Godoy WAC, Fernandes FS (2017) Parasitism-mediated prey selectivity in laboratory conditions and implications for biological control. Basic Appl Ecol 19:67–75

    Google Scholar 

  • Muştu M, Kilinçer N, Ülgentürk S, Kaydan MB (2008) Feeding behavior of Cryptolaemus montrouzieri on mealybugs parasitized by Anagyrus pseudococci. Phytoparasitica 36:360–367

    Google Scholar 

  • Naranjo-Guevara N, Peñaflor MFG, Cabezas-Guerrero MF, Bento JMS (2017) Nocturnal herbivore-induced plant volatiles attract the generalist predatory earwig Doru luteipes Scudder. Sci Nat 104:77

    Google Scholar 

  • Negm AA, Hensley SD (1969) Evaluation of certain biological control agents of the sugarcane borer in Louisiana. J Econ Entomol 62:1008–1013

    Google Scholar 

  • Nunes GS, Dantas TAV, Figueiredo WRS, Souza MDS, Nascimento IN, Batista JL (2018) Predation of diamondback moth larvae and pupae by Euborellia annulipes. Rev Bras Cienc Agr 13:5557

    Google Scholar 

  • Nunes GS, Dantas TAV, Souza MS, Nascimento IN, Batista JL, Malaquias JB (2019) Life stage and population density of Plutella xylostella affect the predation behavior of Euborellia annulipes. Entomol Exp Appl 167:544–552

    Google Scholar 

  • Parra JRP, Coelho A (2019) Applied biological bontrol in Brazil: from laboratory assays to field application. J Insect Sci 19:5

    Google Scholar 

  • Pennacchio F, Strand MR (2006) Evolution of developmental strategies in parasitic Hymenoptera. Annu Rev Entomol 51:233–258

    CAS  PubMed  Google Scholar 

  • Pineda S, Cruz G, Valle J, De La Rosa JF, Chavarrieta JM, Ordoñez-Reséndiz M, Martínez AM (2012) Arthropod abundance in two maize fields in western central Mexico. J Kansas Entomol Soc 85:340–352

    Google Scholar 

  • Poelman EH, Harvey JA, Loon JJ, Vet LE, Dicke M (2013) Variation in herbivore-induced plant volatiles corresponds with spatial heterogeneity in the level of parasitoid competition and parasitoid exposure to hyperparasitism. Funct Ecol 27:1107–1116

    Google Scholar 

  • Polis GA, Myers CA, Holt RD (1989) The ecology and evolution of intraguild predation: potential competitors that eat each other. Annu Rev Ecol Syst 20:297–330

    Google Scholar 

  • Pratissoli D, Grecco ED, Nihei SS, Polanczyk RA, Celestino FN, Carvalho JD, Barbosa WF (2010) Ocorrência de Lixophaga sp. (Diptera: Tachinidae) parasitando lagartas de Diaphania nitidalis (L.) (Lepidoptera: Crambidae) em Cucurbita moschata no Brasil. Arq Ins Biol 77:719–721

    Google Scholar 

  • Ramamurthi BN, Solayappan AR (1980) Dermapteran predators in the biological regulation of sugarcane borers in India. Curr Sci 49:72–73

    Google Scholar 

  • Rankin SM, Palmer JO (2009) Dermaptera: (Earwigs). In: Resh VH, Cardé RT (eds) Encyclopedia of insects. Academic Press, New York, pp 259–261

    Google Scholar 

  • Rogers D (1972) Random search and insect population models. J Anim Ecol 41:369–383

    Google Scholar 

  • Rossoni C, Loureiro EDS, Pereira FF, Kassab SO, Costa DP, Barbosa RH (2014) Selectivity of Metarhizium anisopliae and Beauveria bassiana (Hypocreales: Clavicipitaceae) on adults of Cotesia flavipes (Hymenoptera: Braconidae). Folia Biol 62:269–275

    Google Scholar 

  • Roy S, Roy MM, Jaiswal AK, Baitha A (2018) Soil arthropods in maintaining soil health: thrust areas for sugarcane production systems. Sugar Tech 20:1–16

    Google Scholar 

  • Sabelis MW (1992) Predatory arthropods. In: Crawley MJ (ed) Natural enemies, the population biology of predators, parasites and diseases. Blackwell Scientific, Oxford, pp 225–264

    Google Scholar 

  • Sandhu HS, Cherry RH (2014) Effects of tillage practices on arthropod ground predators in florida sugarcane. J Entomol Sci 49:415–419

    Google Scholar 

  • Santos LAO, Naranjo-Guevara N, Fernandes OA (2017) Diversity and abundance of edaphic arthropods associated with conventional and organic sugarcane crops in Brazil. Fla Entomol 100(1):134–144

    Google Scholar 

  • SAS Institute (2015) SAS/IML® User’sGuide. SAS Institute, Cary

    Google Scholar 

  • Shah MA, Khan AA (2013) Functional response- a function of predator and prey species. Bioscan 8:751–758

    Google Scholar 

  • Sherratt T, Harvey IF (1993) Frequency-dependent food selection by arthropods: a review. Biol J Linn Soc 48:167–186

    Google Scholar 

  • Showler AT, Reagan TE (1991) Effects of sugarcane borer, weed, and nematode control strategies in Louisiana sugarcane. Environ Entomol 20:358–370

    Google Scholar 

  • Sidhu JK, Stout MJ, Blouin DC, Datnoff LE (2013) Effect of silicon soil amendment on performance of sugarcane borer, Diatraea saccharalis (Lepidoptera: Crambidae) on rice. Bull Entomol Res 103:656–664

    CAS  PubMed  Google Scholar 

  • Silva AB, Batista JL, Brito CH (2009) Capacidade predatória de Euborellia annulipes (Lucas, 1847) sobre Spodoptera frugiperda (Smith, 1797). Acta Sci Agron 31:7–11

    Google Scholar 

  • Silva ITFA, Oliveira R, Oliveira LVQ, Nascimento Júnior JL, Batista JL (2018) Biological development of Euborellia annulipes reared with artificial diets and Ephestia kuehniella eggs. Pesq Agrop Trop 48:295–298

    Google Scholar 

  • Silva-Brandão KL, Santos TV, Cônsoli FL, Omoto C (2015) Genetic diversity and structure of Brazilian populations of Diatraea saccharalis (Lepidoptera: Crambidae): Implications for pest management. J Econ Entomol 108:307–316

    PubMed  Google Scholar 

  • Simões RA, Reis LG, Bento JM, Solter LF, Delalibera I Jr (2012) Biological and behavioral parameters of the parasitoid Cotesia flavipes (Hymenoptera: Braconidae) are altered by the pathogen Nosema sp. (Microsporidia: Nosematidae). Biol Control 63:164–171

    Google Scholar 

  • Snyder WE, Ives AR (2003) Interactions between specialist and generalist natural enemies: parasitoids, predators, and pea aphid biocontrol. Ecology 84:91–107

    Google Scholar 

  • Solomon ME (1949) The natural control of animal populations. J Anim Ecol 18:1–35

    Google Scholar 

  • Sueldo MR, Bruzzone OA, Virla EG (2010) Characterization of the earwig, Doru lineare, as a predator of larvae of the fall armyworm, Spodoptera frugiperda: a functional response study. J Insect Sci 10:38

    PubMed  PubMed Central  Google Scholar 

  • Tomaz AC, Coutinho AE, Soares BO, Peternelli LA, Pereira EJG, Barbosa MHP (2017) Assessing resistance of sugarcane varieties to sugarcane borer Diatraea saccharalis Fab. (Lepidoptera: Crambidae). Bull Entomol Res 108:547–555

    PubMed  Google Scholar 

  • Tonnang HE, Nedorezov LV, Owino JO, Ochanda H, Löhr B (2009) Evaluation of discrete host–parasitoid models for diamondback moth and Diadegma semiclausum field time population density series. Ecol Model 220:1735–1744

    Google Scholar 

  • Vacari AM, De Bortoli SA, Borba DF, Martins MI (2012) Quality of Cotesia flavipes (Hymenoptera: Braconidae) reared at different host densities and the estimated cost of its commercial production. Biol Control 63:102–106

    Google Scholar 

  • van Veen FJF, Müller CB, Pell JK, Godfray HCJ (2008) Food web structure of three guilds of natural enemies: predators, parasitoids and pathogens of aphids. J Anim Ecol 77:191–200

    PubMed  Google Scholar 

  • Venzon M, Pallini A, Janssen A (2001) Interactions mediated by predators in arthropod food webs. Neotrop Entomol 30:1–9

    Google Scholar 

  • Wiedenmann RN, Smith JW Jr, Darnell PO (1992) Laboratory rearing and biology of the parasite Cotesia flavipes (Hymenoptera: Braconidae) using Diatraea saccharalis (Lepidoptera: Pyralidae) as a host. Environ Entomol 21:1160–1167

    Google Scholar 

  • Xue Y, Bahlai CA, Frewin A, McCreary CM, Des Marteaux LE, Schaafsma AW, Hallett RH (2012) Intraguild predation of the aphid parasitoid Aphelinus certus by Coccinella septempunctata and Harmonia axyridis. BioControl 57:627–634

    Google Scholar 

Download references

Acknowledgements

The authors thank Usina São Martinho for helping with the material for the research

Funding

This study was financially supported by the Coordination for the Improvement of Higher Education Personnel – Brazil (CAPES – Finance Code 001) and the São Paulo State Foundation for Research Aid (FAPESP – Processo 18/00045-8).

Author information

Authors and Affiliations

Authors

Contributions

GSN planed and designed the work, conducted data analyses and wrote the manuscript; GSN, DGR, NAS, CCT, CPC and NFV executed experimental work; and SAB revised the manuscript.

Corresponding author

Correspondence to G S Nunes.

Additional information

Edited by Angelo Pallini – UFV

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nunes, G.S., Ramalho, D.G., dos Santos, N.A. et al. Parasitism-Mediated Interactions Between the Ring-Legged Earwig and Sugarcane Borer Larvae. Neotrop Entomol 48, 919–926 (2019). https://doi.org/10.1007/s13744-019-00731-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13744-019-00731-3

Keywords

Navigation