Elsevier

Crop Protection

Volume 147, September 2021, 105693
Crop Protection

Toxicity of essential oil of Eugenia uniflora (L.) to Thaumastocoris peregrinus (Hemiptera: Thaumastocoridae) and selectivity to the parasitoid Cleruchoides noackae (Lin & Hubert) (Hymenoptera: Mymaridae)

https://doi.org/10.1016/j.cropro.2021.105693Get rights and content

Highlights

  • Eugenia uniflora essential oil is toxic to Thaumastocoris peregrinus.

  • Eugenia uniflora essential oil (0.75%) it is not selective to Cleruchoides noackae.

  • Eugenia uniflora essential oil is safer applied one day after C. noackae parasitism.

Abstract

Thaumastocoris peregrinus Carpintero and Dellapé, 2006 (Hemiptera: Thaumastocoridae) is an exotic insect that causes losses in the production of Eucalyptus sp. The egg parasitoid Cleruchoides noackae Lin and Huber, 2007 (Hymenoptera: Mymaridae) is the principal biological control agent of T. peregrinus. Essential oil, including Eugenia uniflora (L.) have a potential for managing this pest. The objective of this study was to evaluate the toxicity of E. uniflora to T. peregrinus and the selectivity of this oil on the parasitoid C. noackae and its parasitism on T. peregrinus. Toxicity of E. uniflora essential oil was tested at different concentrations to eggs, nymphs and adults of T. peregrinus. The selectivity of this oil was also evaluated in the pre- and post-parasitism of C. noackae on T. peregrinus eggs. The essential oil was analyzed by gas chromatography. Eugenia uniflora essential oil at 0.75% concentration showed insecticidal potential on T. peregrinus adults, nymphs and eggs, and was safer to C. noackae when applied one day after parasitism than pre-parasitism and 7-day post-parasitism. The major compounds found in the E. uniflora essential oil were calamen-10-one (20.20%), silfiperferol-6-em-5-one (10.06%), and germacrone (6.61%). Under laboratory conditions E. uniflora essential oil showed an insecticidal effect to different life stages of T. peregrinus, but it is selective for egg parasitoid C. noackae just one day after the parasitism occurs. Further studies should be carried out on eucalyptus plantations.

Introduction

The Eucalyptus genus has the largest spatial distribution among tree species, as it contains approximately 800 species and hybrids that guarantee its adaptability to several countries (Flores et al., 2016; Oballa et al., 2010). In addition, the Eucalyptus genus is the most widely planted hardwood tree in the world (Myburg et al., 2014). However, some factors can cause productive losses in species of this genus, among which, the bronze bug, Thaumastocoris peregrinus (Carpintero and Dellapé, 2006) (Hemiptera: Thaumastocoridae) stands out. It is a phytophagous insect that feeds on the sap of several species of the genus Eucalyptus, causing the leaves to dry and fall, reducing the photosynthetic area of the plant, and compromising its development, and in some cases causing the trees to die (Jacobs and Neser, 2005; Machado et al., 2016; Santadino et al., 2017; Wilcken et al., 2010).

This insect was first recorded in Australia in 2002, dispersed to the African continent in 2003 (Jacobs and Neser, 2005), and has been recorded in America since 2005 (Carpinteiro and Dellapé, 2006; Ide et al., 2011; Martínez and Bianchi, 2010; Noack et al., 2009; Wilcken et al., 2010), in Oceania since 2012 (Sopow et al., 2012), and in Europe since 2013 (Garcia et al., 2013). However in southern Italy it was recorded only in 2019 (Castiglione et al., 2020). In Brazil, this insect dispersed rapidly in some states (Saliba et al., 2019; Wilcken et al., 2010); between 2008 and 2016 more than 500 thousand hectares of Eucalyptus plantations were affected. It is also estimated that the reduction in the production of wood from plants attacked by T. peregrinus can reach 14%, and in an outbreak of this insect-pest the wood losses represent US $ 380.00 per hectare (Junqueira et al., 2018). The rapid dispersion rate of T. peregrinus and the associated damage have prompted research into the development of potential new insect control methods (Mutitu et al., 2013).

The control of this insect can be accomplished through the use of neonicotinoid and pyrethroid insecticides (Agrofit, 2021; Machado et al., 2016; Noack et al., 2009). However, when used incorrectly and indiscriminately, chemical control can cause risks to human health and the environment (Pinto et al., 2020; Singh et al., 2017). As a result, there is increasing researches using biological and alternative control to be used as a strategy in integrated pest management (IPM). In this sense, have already been described as biological control agents for the control of T. peregrinus (Corallo et al., 2019; Lorencetti et al, 2015, 2018; Mascarin et al., 2012; Soliman et al., 2019; Tedesco et al., 2020). However, the classical biological control using the parasitoid Cleruchoides noackae Lin and Huber, 2007 (Hymenoptera, Mymaridae) has been the main strategy (Barbosa et al., 2017; Lin et al., 2007; Nadel and Noack, 2012). Cleruchoides noackae is a parasitoid of T. peregrinus eggs, originating in Australia (Lin et al., 2007), but has already been obtained in other countries such as Chile, South Africa, Brazil (Barbosa et al., 2017; Mutitu et al., 2013; Nadel and Noack, 2012).

Just like biological control, the botanical insecticides, involving the use of essential oils may be a safe option for the control of T. peregrinus in eucalyptus plantations, in addition to respecting the principles and criteria of the FSC (Forest Stewardship Council) regarding the use of products of plant origin. Essential oils may have repellent or even insecticidal effects. The repellent effect of essential oils has already been demonstrated for several Hemiptera (de Andrade et al., 2013; Lima et al., 2008; Saad et al., 2017) and certain essential oils have an insecticidal effect on Hemiptera (Gomes and Favero, 2011; Li and Tian, 2020; Saad et al., 2017; Turchen et al., 2016).

However, little is known about the use of botanical insecticides as a repellent and insecticide of T. peregrinus (Haas et al., 2016; Lorencetti et al., 2015). Among the most promising plants evaluated for insecticidal potential and consequent evaluation of selectivity is Eugenia uniflora (L.) (Myrtaceae) (pitangueira). The essential oil of this plant contains sesquiterpenes, phenolic compounds, and alkaloids with antimicrobial activity (Auricchio and Bacchi, 2003). Some terpenes present in essential oils can act on the central nervous system of insects by inhibiting acetylcholinesterase (AChe) (Dambolena et al., 2016), have demonstrated insecticidal activity in Atta laevigata (Smith, 1858) (Hymenoptera: Formicidae) (Jung et al., 2013), cause toxicity in Drosophila melanogaster (Meigen, 1830) (Diptera: Drosophilidae) (Cunha et al., 2015), and repel larvae and reduce oviposition of Diaphania hyalinata (L.,1758) (Lepidoptera: Crambidae) (Lobo et al., 2019).

While this botanical insecticide is less toxic to humans and the environment when compared to the use of synthetic pesticides, essential oils may also interfere with the behavior and biology of the pest's natural enemies (Lima et al., 2020; Parreira et al., 2018; Rampelotti-Ferreira et al., 2017). However, studies evaluating the insecticidal potential of E. uniflora essential oil on T. peregrinus and its selectivity to C. noackae are nonexistent. Considering the efficiency of essential oils as an insecticide and/or insect repellent and because the raw materials of products are easily found in nature, studies examining this interaction in the laboratory are vital in order to be able to estimate results in the field and, later, to test them in this environment for possible use in IPM. The objective of this work was thus to evaluate the toxicity of E. uniflora essential oil to different life stages of T. peregrinus, and the selectivity of this oil to C. noackae.

Section snippets

Thaumastocoris peregrinus

Thaumastocoris peregrinus were reared on branches of Eucalyptus dunnii (Maiden) (Myrtales: Myrtaceae) collected in the reforestation of the Federal University of Technology - Paraná (Câmpus Dois Vizinhos) (Dois Vizinhos, Brazil) and supported when necessary by Embrapa Florestas (Colombo, Brazil). The branches were kept in the shape of a “bouquet” in 500 mL−1 Erlenmeyer flasks (model 148) with water (changed weekly) to preserve leaf turgidity. Insect oviposition was facilitated via strips of

Toxicity of E. uniflora essential oils to T. peregrinus

Leaves of E. dunnii treated with different concentrations of E. uniflora essential oil caused mortality in T. peregrinus. Adult survival decreased as the concentration of oil increased (Fig. 1).

The treatments 0.75%, 1.00%, and 1.25% showed greater reductions in the survival of T. peregrinus when compared to the other treatments and to the control during the 7 days of evaluation. In addition, when the medium lethal concentration (LC50) for adults of T. peregrinus was verified, after 7 days, the

Discussion

In the current study, the essential oil of E. uniflora caused significant interference with survival in a shorter period of time when in contact with the adults and nymphs of T. peregrinus, as well as affecting the hatching of T. peregrinus nymphs. This insecticidal potential has also been observed in Sitophilus zeamais (Mots., 1855) (Coleoptera: Curculionidae) adults, causing repellence (88.5%) and mortality (100%) (Coitinho et al., 2010). Similarly, a concentration of 1.25% caused mortality

CRediT authorship contribution statement

Luma Dalmolin Stenger: Conceptualization, Data curation, Methodology, Investigation, Supervision, Writing – original draft, Roles/Writing - original draft. Raiza Abati: Formal analysis, Writing – original draft, Roles/Writing - original draft, Validation, Visualization. Igor Gallo Pawlak: Investigation. Gabriela Osowski Varpechoski: Investigation. Edgar De Souza Vismara: Software, Formal analysis, Validation, Visualization. Leonardo Rodrigues Barbosa: Resources, Funding acquisition, Writing –

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

To the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Universidade Tecnológica Federal do Paraná (UTFPR) for promoting the research.

References (64)

  • G.R. Brun et al.

    Chemical characterization and antimicrobial activity of the volatile oil of pitanga “Brazilian Cherry” (Eugenia uniflora L.)

    Perspectivas

    (2010)
  • D.L. Carpinteiro et al.

    A new species of Thaumastocoris kirkaldy from Argentina (heteroptera: Thaumastocoridae: thaumastocorinae)

    Zootaxa

    (2006)
  • E. Castiglione et al.

    First record from Calabria (southern Italy) of the “bronze bug” Thaumastocoris peregrinus Carpintero & Dellapé, 2006, alien Eucalyptus pest native to Australia (Hemiptera: heteroptera: Thaumastocoridae)

    J. Entomol. Acarol. Res.

    (2020)
  • J.V. de Oliveira et al.

    Persistência de óleos essenciais em milho armazenado, submetido à infestação de gorgulho do milho

    Ciência Rural.

    (2010)
  • B. Corallo et al.

    Entomopathogenic fungi naturally infecting the eucalypt bronze bug, Thaumastocoris peregrinus (Heteroptera: Thaumastocoridae), in Uruguay

    J. Appl. Entomol.

    (2019)
  • A.A. Correia et al.

    Microscopic analysis of Spodoptera frugiperda (Lepidoptera: noctuidae) embryonic development before and after treatment with azadirachtin, lufenuron, and deltamethrin

    J. Econ. Entomol.

    (2013)
  • F.A.B. Cunha et al.

    Eugenia uniflora leaves essential oil induces toxicity in Drosophila melanogaster: involvement of oxidative stress mechanisms

    Toxicol. Res. (Camb).

    (2015)
  • J.S. Dambolena et al.

    Terpenes: natural products for controlling insects of importance to human health—a structure-activity relationship study

    Psyche A J. Entomol. 2016

    (2016)
  • L.H. de Andrade et al.

    Efeito repelente de azadiractina e óleos essenciais sobre Aphis gossypii Glover (Hemiptera: aphididae) em algodoeiro

    Rev. Cienc. Agron.

    (2013)
  • T. Flores et al.

    Eucalyptus no Brasil: Zoneamento climático e guia para identificação

    (2016)
  • A. Garcia et al.

    First record of Thaumastocoris peregrinus in Portugal and of the neotropical predator Hemerobius bolivari in Europe

    Bull. Insectol.

    (2013)
  • F.R. García et al.

    Produccion y manejo de Trichogramma en Colombia

    (1998)
  • P.G.E. George et al.

    Toxic effects of insecticides in the histomorphology of alimentary canal , testis and ovary in a reduviid Rhynocoris kumarii Ambrose and Livingstone (Hemiptera : reduviidae)

    J. Adv. Zool.

    (2004)
  • L. Gobbo-Neto et al.

    Plantas medicinais: fatores de influência no conteúdo de metabólitos secundários

    Quim. Nova

    (2007)
  • S.P. Gomes et al.

    Avaliação de óleos essenciais de plantas aromáticas com atividade inseticida em Triatoma infestans (Klug, 1834) (Hemiptera: reduviidae)

    Acta Sci. Health Sci.

    (2011)
  • R. de C.R. Gonçalves-Gervásio et al.

    Efeito de extratos de Meliáceas sobre o parasitóide de ovos Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae)

    Neotrop. Entomol.

    (2004)
  • J. Haas et al.

    Toxicity and repellency of plant extracts on Thaumastocoris peregrinus (carpintero dellap) (Hemiptera: Thaumastocoridae)

    Afr. J. Agric. Res.

    (2016)
  • S.M. Ide et al.

    Detección de Thaumastocoris peregrinus (Hemiptera: Thaumastocoridae) asociado a Eucalyptus spp. en Chile

    Bosque

    (2011)
  • D.H. Jacobs et al.

    Thaumastocoris australicus Kirkaldy (Heteroptera: Thaumastocoridae): a new insect arrival in South Africa, damaging to Eucalyptus trees

    South Afr. J. Sci.

    (2005)
  • P.H. Jung et al.

    Atividade inseticida de Eugenia uniflora L. e Melia azedarach L. sobre Atta laevigata Smith

    Floresta e Ambient

    (2013)
  • L.R. Junqueira et al.

    Quantification of damages by Thaumastocoris peregrinus (Hemiptera: Thaumastocoridae) in eucalypt

  • E.L. Kaplan et al.

    Nonparametric estimation from incomplete observations

    J. Am. Stat. Assoc.

    (1958)
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