ABSTRACT:
Thaumastocoris peregrinus Carpintero and Dellape (Hemiptera: Thaumastocoridae) is a sap-sucking insect that has become a major pest of eucalypts. The entomopathogenic fungi Beauveria bassiana (Bals.-Criv.) Vuill. and Metarhizium anisopliae (Metsch.) Sorokin have the potential to control insect pests. This study evaluated the susceptibility of T. peregrinus to two commercial products based on conidia of B. bassiana and M. anisopliae. The fungi were sprayed onto adults of T. peregrinus at a concentration of 1 × 108 conidia mL−1 to evaluate their pathogenicity and conidial production on the insect cadavers. Beauveria bassiana caused 100 % mortality, while M. anisopliae caused more than 80 % mortality of T. peregrinus adults 11 days after fungi application. The fungi colonized the head and thorax regions and caused high mortality rates through conidial production. Pathogenicity of entomopathogenic fungi B. bassiana and M. anisopliae to T. peregrinus show potential to use these fungi in integrated pest management.
Keywords: Beauveria bassiana; Metarhizium anisopliae; biological control; bronze bug
Introduction
The bronze bug Thaumastocoris peregrinus Carpintero and Dellape (Hemiptera: Thaumastocoridae), native to Australia, is as a major pest to species of genus Eucalyptus (Laudonia and Sasso, 2012; Garcia et al., 2013; Souza et al., 2016). This pest has been introduced to more than 10 countries in Europe, Africa, South America and Oceania (Saavedra et al., 2015).
The short life cycle and high reproductive potential of females of T. peregrinus allow rapid population growth of this pest in the field (Soliman et al., 2012; Nadel et al., 2015). The damages caused for bronze bug reduces the photosynthetic capacity and causes death to trees that are severely infested (Jacobs and Neser, 2005; Nadel et al., 2010).
There are no effective control methods for T. peregrinus; therefore, the search for natural biological agents is essential. Biological control is the main approach to reduce damage by exotic insect pests in Eucalyptus (Wingfield et al., 2013). The egg parasitoid Cleruchoides noackae Lin and Huber (Hymenoptera: Mymaridae) is the only available biological control agent used against T. peregrinus (Barbosa et al., 2017).
Entomopathogenic fungus associated with the bronze bug was reported in Brazil. Zoophthora radicans (Entomophthorales: Entomophthoraceae) seems to be virulent against T. peregrinus and low densities of this insect were associated with high fungal infection levels (Mascarin et al., 2012). However, studies are needed to confirm virulence and potential for control of T. peregrinus with entomopathogenic fungi.
Beauveria bassiana (Bals.-Criv.) Vuill. (Ascomycota: Hypocreales: Cordycipitacea) and Metarhizium anisopliae (Metsch) Sorokin (Hypocreales: Clavicipitaceae) can rapidly spread in the field (Meyling et al., 2009; Costa et al., 2015) and regulate Eucalyptus pest populations (Sun et al., 2008; Echeverri-Molina and Santolamazza-Carbone, 2010). Thus, this study evaluated the susceptibility of T. peregrinus to two commercial products based on conidia of B. bassiana and M. anisopliae.
Materials and Methods
Insect collection
Thaumatocoris peregrinus was reared in Botucatu (22º53’09” S; 48º26’42” W; 804 m), São Paulo State, Brazil, at 24 ± 2 ºC, 60 ± 10 % RH and 12L: 12D photoperiod, from insects collected in the field. Adults of the bronze bug were reared in bouquets of eucalyptus branches secured with a piece of foam in 500 mL Erlenmeyer flasks filled with water to prevent the insects from submerging.
Commercial products
The fungus M. anisopliae was obtained from the commercial products Toyobo − 4 × 109 conidia mL−1 (MTO) and Usina Paulista - 1.9 × 109 conidia mL−1 (MUS) and B. bassiana from Koppert- 5 × 108 conidia mL−1 - strain ESALQ-PL63 (BIT) and Usina Paulista − 4.8 ×109 conidia mL−1 (BUS). These mycoinsecticides are formulated as soluble powders. The conidia count per mL was performed in a Neubauer chamber (to confirm commercial product concentration) and then diluted in distilled water to standardize the concentration of all mycoinsecticides at 1 × 108 conidia mL−1. Tween (20 0.02 %) adjuvant was added. The control used only distilled water and Tween 20 0.02 %. The products were stored in a freezer for 40 (BIT), 30 (BUS and MUS) and 21 (MTO) days. The product manufacturers guarantee minimum fungi viability of 90 %.
Bioassays
Eight adults of T. peregrinus were placed on Petri dishes (8.5 cm diameter) with diluted agricultural gel (hydroplan- EB/HyC, SNF S.A Floger) (1 g in 400 mL of distilled water) near a leaf of Eucalyptus urophylla S.T. Blake (Myrtaceae) with an area of 16.5 cm² per plot with five replications (40 insects per treatment). The mycoinsecticides (2 mL of suspension) (treatments: M. anisopliae (Toyobo – MTO and Usina – MUS); B. bassaina (Boveril - BIT and Usina - BUS) and control (distilled water and Tween 20 (0.02 %)) were sprayed on Petri dishes with insects with a Potter spray tower and transferred to a room with temperature regulated at 25 ± 3 °C, 60 ± 10 % RH with a photoperiod of 12h12 L:D. T. peregrinus adult mortality was evaluated at one, two, three, five, seven, nine, and eleven days after treatment application (DAA) and dead insects were transferred to plastic pots (100 mL) with a damp cotton ball and stored without light (mortality data confirmation). In addition, dead adults of T. peregrinus were stored under refrigeration in Karnovsky gel (2.5 glutaraldehyde, paraformaldehyde 2.0 %, phosphate buffer 0.05 M, pH 7.2) and analyzed with a DSM 940 A scanning electron microscope (SEM) (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 identified from the photomicrographs.
Quantification of sporulation on T. peregrinus cadavers
Conidial production was evaluated in four T. peregrinus cadavers after 21 days of mycoinseticide application, with five replications per treatment (20 insects per treatment). Four insects were washed with 10 mL distilled water and Tween 20 0.02 %. The conidia in this solution were counted in a Neubauer chamber. Potential of conidial production was obtained as recommended for Hypothenemus hampei Ferrari (Coleoptera: Scolytidae) (Neves and Hirose, 2005) by dividing the production of different isolates by the production of isolate with lower production.
Statistical analyses
The mortality data were submitted to the analysis of variance with the F test and the means compared by the Tukey test (p ≤ 0.05) with the SAS (Statistical Analysis System, version 9.0). Data were submitted to the survival analysis with the Kaplan-Meier estimator (Log-rank method) using Origin Pro (OriginLab Corporation, version 9.1). Bronze bugs that survived to the end of the experiment (11 DAA) were treated as censored data.
Results
The mycoinsecticides were pathogenic to adults of T. peregrinus at the dose of 1 × 108 conidia mL−1. Beauveria bassiana and M. anisopliae penetrated and presented mycelial growth in the insect body, mainly in the head and thorax structures of T. peregrinus. Beauveria bassiana (BIT) mycelial growth was observed in the mouthparts and on intersegmental membranes of prothoracic legs in the thigh and trochanter of T. peregrinus (Figures 1A-E). The mycelial growth of B. bassiana (BUS) was more evident on the legs (Figure 1G). Mycelia of M. anisopliae (MUS) grew on the head, especially in the mouthparts (Figure 1F) with the hyphae (MTO) visible on the thorax (Figure 1H).
Dorsal (A) and ventral view of the body (B), dorsal view (C) and ventral (D) of the head of Thaumastocoris peregrinus (Hemiptera: Thaumastocoridae) without the application of mycoinsecticides. Ventral view of the head of this insect with application of Beauveria bassiana (Koppert - BIT) (E) and (Usina Paulista -BUS) (G) and Metarhizium anisopliae (Toyobo - MTO) (F) and (Usina Paulista - MUS) (H) at the concentration 1 × 108 conidia mL−1. Black arrows indicate conidia attached to the host cuticle.
Mycoinsecticides with the B. bassiana fungus caused 100 % mortality of T. peregrinus (BUS: 8.00 ± 0.0 and BIT: 8.00 ± 0.0) and commercial products with M. anisopliae caused 83 and 88% mortality, respectively (Figure 2) (MTO: 6.66 ± 0.5 and MUS: 7.00 ± 0.5) (F = 59.3, p < 0.05), of T. peregrinus adults 11 days after fungi application.
Survival curves of Thaumastocoris peregrinus (Hemiptera: Thaumastocoridae) up to 11 days after application of Beauveria bassiana (Usina Paulista - BUS; Koppert - BIT) and Metarhizium anisopliae (Toyobo – MTO; Usina Paulista - MUS) formulated as commercial products at the concentration of 1 × 108 conidia mL−1 and control using the Kaplan-Meier method and compared using the log-rank test (X2= 191.2; p = 0.001).
The conidiogenesis on T. peregrinus from all fungi (Table 1) confirms the sporulation detected with SEM images (Figure 1). The BUS showed the highest conidial production on insect cadavers.
Number of conidia per cadaver of Thaumastocoris peregrinus (Hemiptera: Thaumastocoridae) after 11 days of application (mean ± SE) and potential of conidial production after 21 days of application of Beauveria bassiana (Usina Paulista - BUS; Koppert - BIT) and Metarhizium anisopliae (Toyobo – MTO; Usina Paulista - MUS) formulated as commercial products at the concentration of 1 × 108 conidia mL−1 (25 ± 3 °C and a photoperiod of 12 h) (n = 20).
Discussion
The entomopathogenic action of B. bassiana and M. anisopliae on T. peregrinus is important because these fungi have a wide distribution and host range, easy production, with low risk to humans, animals and the environment, and they penetrate the external cuticle of arthropods (Hussain et al., 2014). The use of fungi can complement the biological control of T. peregrinus with Cleruchoides noackae (Hymenoptera: Mymaridae), Hemerobius bolivari (Neuroptera: Hemerobiidae), and Chysoperla externa (Neuroptera: Chrysopidae) as the main natural enemies reported for this pest (Nadel and Noack, 2012; Souza et al., 2012; Garcia et al., 2013). However, entomopathogenic fungi can cause adverse effects to the biological life history parameters of natural enemies (Agboton et al., 2013; Wu et al., 2015). Thus, the application of entomopathogenic fungi should be carefully adjusted to complement the biological systems of pest control (Furlong, 2004; Oreste et al., 2016). Temporal separation of the fungus application and parasitoid release could reduce antagonism and enhance pest control (Chow et al., 2016). This would reduce the possible detrimental effects of fungi on parasitoid development.
Mycelial growth of B. bassiana in T. peregrinus is more evident on the legs, similar to reports for fungus Hirsutella thompsonii on mite Varroa destructor (Acari: Varroidae) (Peng et al., 2002). The basal portion of the legs provides a favorable microclimate (e.g., higher humidity for germination and growth) and the lower sclerotized tissue of the intersegmental membrane of the insect favors fungi development. Besides, high hair density facilitates conidia attachment. In our study, colonization by B. bassiana began in the labium and spread to other parts of the bodies of Myzus persicae Sulzer (Hemiptera: Aphididae) and Phenacoccus manihoti Matile-Ferrero (Hemiptera: Pseudococcidae) (Amnuaykanjanasin et al., 2013).
Colonization of T. peregrinus mouthparts by M. anisopliae confirms reports of this fungus in the buccal cavity of blowfly Lucilia cuprina Wiedemann (Diptera: Calliphoridae) (Leemon and Jonsson, 2012). Fungal attachment in highly susceptible host locations is essential for successful pathogenesis (Amnuaykanjanasin et al., 2013). Conidia densities of B. bassiana and M. anisopliae were greater on legs, wings, and thorax of Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae), Bactericera cockerelli Sulc. (Hemiptera: Triozidae) and Frankliniella occidentalis Pergande (Thysanoptera: Thripidae) (Rios-Velasco et al., 2014).
Conidial production by fungi in T. peregrinus cadavers shows the dissemination capacity of these biological agents in the field (Ramos et al., 2004). High sporulation rate and epizootic potential are important characteristics for such control agents (Charley, 1997) allowing greater permanence (Alves and Lecuona, 1998) and residual effects of isolates in the field.
Susceptibility of T. peregrinus to the mycoinsecticides B. bassiana and M. anisopliae is similar to that reported for other Hemiptera pests, such as Nilaparvata lugens Stål (Hemiptera: Delphacidae) (Li et al., 2014), Diaphorina citri Kuwayama (Hemiptera: Liviidae) (Orduño-Cruz et al., 2015), Nezara viridula Linnaeus (Hemiptera: Pentatomidae) (Raafat et al., 2015), Aeneolamia spp. (Hemiptera: Cercopidae) (Hernández-Domínguez et al., 2016) and Glycaspis brimblecombei (Dal Pogetto et al., 2011a; 20011b).
Damage by T. peregrinus in eucalyptus plantations and the need for products that comply with forest certification requirements (Zanuncio et al., 2016; Lemes et al., 2017) show the importance of entomopathogenic fungi for the management of this pest. These studies are significant because B. bassiana and M. anisopliae caused 79 % mortality of adults of N. lugens 10 days after inoculation (Li et al., 2014) and 50 and 60 % mortality, respectively, to D. citri (Lezama-Gutiérrez et al., 2012). Other pathogenic fungi for these insects include Hirsutella citriformis Kuwayama (Ascomycota: Hypocreales: Ophiocordyceps) with 100 % mortality for D. citri (Orduño-Cruz et al., 2015). The microbial action of entomopathogenic fungi is slow and requires relatively long periods to induce insect mortality compared to chemicals (Lomer et al., 2001); however, infected insects have low feeding activity (Avery et al., 2009; Pelizza et al., 2013) and, therefore, damage caused by T. peregrinus may be reduced after application of entomopathogenic fungi. The aggregative behavior of T. peregrinus (Jacobs and Neser, 2005; Noack and Rose, 2007; Noack, 2009) may facilitate epizootic conditions for these microbial agents, similar to reports for Zoophthora radicans (Entomophthorales: Entomophthoraceae) (Mascarin et al., 2012).
Pathogenicity shows that B. bassiana and M. anisopliae have potential for the biological control of T. penegrinus and therefore should be considered in the integrated management of this pest. However, field studies are still needed. This is the first report on pathogenicity of these fungi to T. peregrinus.
Acknowledgements
We extend our thanks to the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) and Programa Cooperativo sobre Proteção Florestal of the Instituto de Pesquisas e Estudos Florestais (PROTEF/IPEF) for the financial support. Dr. Phillip Villani revised and corrected the English language used in this manuscript.
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Edited by
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Edited by: Alberto Soares Corrêa
Publication Dates
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Publication in this collection
May-Jun 2019
History
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Received
03 Feb 2017 -
Accepted
11 Feb 2018