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Susceptibility of Thaumastocoris Peregrinus (Hemiptera: Thaumastocoridae), a Eucalyptus Pest, to Entomopathogenic Fungi

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Susceptibility of Thaumastocoris Peregrinus (Hemiptera: Thaumastocoridae), a Eucalyptus Pest, to Entomopathogenic Fungi DOI: http://dx.doi.org/10.1590/1678-992X-2017-0043 ISSN 1678-992X Note | Susceptibility of Thaumastocoris peregrinus (Hemiptera: Thaumastocoridae), a Eucalyptus pest, to entomopathogenic fungi Everton Pires Soliman1 , Bárbara Monteiro de Castro e Castro2* , Carlos Frederico Wilcken3 , Ana Carolina Firmino4 , Mario Henrique Ferreira Amaral Dal Pogetto5 , Leonardo Rodrigues Barbosa6 , José Cola Zanuncio7 Entomology 1Suzano Papel e Celulose/Tecnologia Florestal, Av. Dr. José ABSTRACT: Thaumastocoris peregrinus Carpintero and Dellape (Hemiptera: Thaumastocoridae) Lembo, 1010 − 18207-78 − Itapetininga, SP − Brasil. is a sap-sucking insect that has become a major pest of eucalypts. The entomopathogenic 2Universidade Federal de Viçosa – Depto. de Fitotecnia,Av. P. fungi Beauveria bassiana (Bals.-Criv.) Vuill. and Metarhizium anisopliae (Metsch.) Sorokin have H. Rolfs, s/n − 36570-900 − Viçosa, MG − Brasil. the potential to control insect pests. This study evaluated the susceptibility of T. peregrinus to 3Universidade Estadual Paulista/FCA – Depto. de Proteção two commercial products based on conidia of B. bassiana and M. anisopliae. The fungi were Vegetal, R. José Barbosa de Barros, 1780 − 18610-307 − sprayed onto adults of T. peregrinus at a concentration of 1 × 108 conidia mL−1 to evaluate their Botucatu, SP − Brasil. pathogenicity and conidial production on the insect cadavers. Beauveria bassiana caused 100 % 4Universidade Estadual Paulista/FCAT, Rod. Comandante João mortality, while M. anisopliae caused more than 80 % mortality of T. peregrinus adults 11 days Ribeiro de Barros, km 651 – 17900-000 – Dracena, SP – Brasil. after fungi application. The fungi colonized the head and thorax regions and caused high mortal- 5Dow AgroSciences – Estação Experimental de Mogi Mirim, ity rates through conidial production. Pathogenicity of entomopathogenic fungi B. bassiana and km 71,5 – 13800-970 – Mogi Mirim, SP − Brasil. M. anisopliae to T. peregrinus show potential to use these fungi in integrated pest management. 6Embrapa Florestas, Estrada da Ribeira, km 111 − 83411- Keywords: Beauveria bassiana, Metarhizium anisopliae, biological control, bronze bug 000 − Colombo, PR − Brasil. 7Universidade Federal de Viçosa – Depto. de Entomologia/ BIOAGRO, Av. P.H. Rolfs, s/n − 36570-900 − Viçosa, MG − Brasil. *Corresponding author <[email protected]> Edited by: Alberto Soares Corrêa Received February 03, 2017 Accepted February 11, 2018 Introduction virulent against T. peregrinus and low densities of this insect were associated with high fungal infection levels The bronze bug Thaumastocoris peregrinus Carpin- (Mascarin et al., 2012). However, studies are needed to tero and Dellape (Hemiptera: Thaumastocoridae), native confirm virulence and potential for control of T. peregri- to Australia, is as a major pest to species of genus Eu- nus with entomopathogenic fungi. calyptus (Laudonia and Sasso, 2012; Garcia et al., 2013; Beauveria bassiana (Bals.-Criv.) Vuill. (Ascomy- Souza et al., 2016). This pest has been introduced to cota: Hypocreales: Cordycipitacea) and Metarhizium more than 10 countries in Europe, Africa, South Ameri- anisopliae (Metsch) Sorokin (Hypocreales: Clavicipi- ca and Oceania (Saavedra et al., 2015). taceae) can rapidly spread in the field (Meyling et al., The short life cycle and high reproductive poten- 2009; Costa et al., 2015) and regulate Eucalyptus pest tial of females of T. peregrinus allow rapid population populations (Sun et al., 2008; Echeverri-Molina and growth of this pest in the field (Soliman et al., 2012; Santolamazza-Carbone, 2010). Thus, this study evalu- Nadel et al., 2015). The damages caused for bronze bug ated the susceptibility of T. peregrinus to two commer- reduces the photosynthetic capacity and causes death to cial products based on conidia of B. bassiana and M. trees that are severely infested (Jacobs and Neser, 2005; anisopliae. Nadel et al., 2010). There are no effective control methods for T. pere- Materials and Methods grinus; therefore, the search for natural biological agents is essential. Biological control is the main approach Insect collection to reduce damage by exotic insect pests in Eucalyptus Thaumatocoris peregrinus was reared in Botucatu (Wingfield et al., 2013). The egg parasitoid Cleruchoides (22º53’09” S; 48º26’42” W; 804 m), São Paulo State, Bra- noackae Lin and Huber (Hymenoptera: Mymaridae) is zil, at 24 ± 2 ºC, 60 ± 10 % RH and 12L: 12D pho- the only available biological control agent used against toperiod, from insects collected in the field. Adults of T. peregrinus (Barbosa et al., 2017). the bronze bug were reared in bouquets of eucalyptus Entomopathogenic fungus associated with the branches secured with a piece of foam in 500 mL Er- bronze bug was reported in Brazil. Zoophthora radicans lenmeyer flasks filled with water to prevent the insects (Entomophthorales: Entomophthoraceae) seems to be from submerging. Sci. Agric. v.76, n.3, p.255-260, May/June 2019 Soliman et al. Biological control of bronze bug Commercial products Statistical analyses The fungus M. anisopliae was obtained from the The mortality data were submitted to the analysis commercial products Toyobo - 4 × 109 conidia mL−1 of variance with the F test and the means compared by (MTO) and Usina Paulista - 1.9 × 109 conidia mL−1 the Tukey test (p ≤ 0.05) with the SAS (Statistical Anal- (MUS) and B. bassiana from Koppert- 5 × 108 conidia ysis System, version 9.0). Data were submitted to the mL−1 - strain ESALQ-PL63 (BIT) and Usina Paulista - 4.8 survival analysis with the Kaplan-Meier estimator (Log- ×109 conidia mL−1 (BUS). These mycoinsecticides are rank method) using Origin Pro (OriginLab Corporation, formulated as soluble powders. The conidia count per version 9.1). Bronze bugs that survived to the end of the mL was performed in a Neubauer chamber (to confirm experiment (11 DAA) were treated as censored data. commercial product concentration) and then diluted in distilled water to standardize the concentration of all Results mycoinsecticides at 1 × 108 conidia mL−1. Tween (20 0.02 %) adjuvant was added. The control used only dis- The mycoinsecticides were pathogenic to adults of tilled water and Tween 20 0.02 %. The products were T. peregrinus at the dose of 1 × 108 conidia mL−1. Beauveria stored in a freezer for 40 (BIT), 30 (BUS and MUS) and bassiana and M. anisopliae penetrated and presented my- 21 (MTO) days. The product manufacturers guarantee celial growth in the insect body, mainly in the head and minimum fungi viability of 90 %. thorax structures of T. peregrinus. Beauveria bassiana (BIT) mycelial growth was observed in the mouthparts and on Bioassays intersegmental membranes of prothoracic legs in the thigh Eight adults of T. peregrinus were placed on Petri and trochanter of T. peregrinus (Figures 1A-E). The myce- dishes (8.5 cm diameter) with diluted agricultural gel lial growth of B. bassiana (BUS) was more evident on the (hydroplan- EB/HyC, SNF S.A Floger) (1 g in 400 mL of legs (Figure 1G). Mycelia of M. anisopliae (MUS) grew on distilled water) near a leaf of Eucalyptus urophylla S.T. the head, especially in the mouthparts (Figure 1F) with the Blake (Myrtaceae) with an area of 16.5 cm² per plot hyphae (MTO) visible on the thorax (Figure 1H). with five replications (40 insects per treatment). The Mycoinsecticides with the B. bassiana fungus caused mycoinsecticides (2 mL of suspension) (treatments: M. 100 % mortality of T. peregrinus (BUS: 8.00 ± 0.0 and anisopliae (Toyobo – MTO and Usina – MUS); B. bassaina BIT: 8.00 ± 0.0) and commercial products with M. aniso- (Boveril - BIT and Usina - BUS) and control (distilled wa- pliae caused 83 and 88% mortality, respectively (Figure 2) ter and Tween 20 (0.02 %)) were sprayed on Petri dishes (MTO: 6.66 ± 0.5 and MUS: 7.00 ± 0.5) (F = 59.3, p < with insects with a Potter spray tower and transferred to 0.05), of T. peregrinus adults 11 days after fungi application. a room with temperature regulated at 25 ± 3 °C, 60 ± The conidiogenesis on T. peregrinus from all fungi 10 % RH with a photoperiod of 12h12 L:D. T. peregrinus (Table 1) confirms the sporulation detected with SEM adult mortality was evaluated at one, two, three, five, images (Figure 1). The BUS showed the highest conidial seven, nine, and eleven days after treatment application production on insect cadavers. (DAA) and dead insects were transferred to plastic pots (100 mL) with a damp cotton ball and stored without Discussion light (mortality data confirmation). In addition, dead adults of T. peregrinus were stored under refrigeration The entomopathogenic action of B. bassiana and in Karnovsky gel (2.5 glutaraldehyde, paraformaldehyde M. anisopliae on T. peregrinus is important because these 2.0 %, phosphate buffer 0.05 M, pH 7.2) and analyzed fungi have a wide distribution and host range, easy with a DSM 940 A scanning electron microscope (SEM) production, with low risk to humans, animals and the (Carl Zeiss, Jena, Germany) of the Federal University of São Paulo, 21 days after mycoinsecticide application. Fungal development sites in the insect in tegument were Table 1 – Number of conidia per cadaver of Thaumastocoris identified from the photomicrographs. peregrinus (Hemiptera: Thaumastocoridae) after 11 days of application (mean ± SE) and potential of conidial production after Quantification of sporulation on T. peregrinus 21 days of application of Beauveria bassiana (Usina Paulista - cadavers BUS; Koppert - BIT) and Metarhizium anisopliae (Toyobo – MTO; Conidial production was evaluated in
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