Susceptibility of Thaumastocoris peregrinus (Hemiptera: Thaumastocoridae), a Eucalyptus pest, to entomopathogenic fungi

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).

Figure 1
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.

Figure 2
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.

Table 1
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).

Treatment	Conidia/cadaver	1Potential of conidial production
BUS	144.9 ± 9.5	1.3
BIT	117.4 ± 8.5	1.0
MTO	141.4 ± 16.4	1.2
MUS	112.6 ± 16.0	-

• ¹
  Potential of conidial production = conidia produced per product × divided by the conidia produced by MUS.

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.

References

• Agboton, B.V.; Hanna, R.; Onzo, A.; Vidal, S.; von Tiedemann, A. 2013. Interactions between the predatory mite Typhlodromalus aripo and the entomopathogenic fungus Neozygites tanajoae and consequences for the suppression of their shared prey/host Mononychellus tanajoa Experimental and Applied Acarology 60: 205–217.
• Alves, S.B.; Lecuona, R.E. 1998. Epizootiology applied to the microbial control of insects = Epizootiologia aplicada ao controle microbiano de insetos. p. 97-169. In: Alves, S.B., coord. Microbial control of insects = Controle microbiano de insetos. FEALQ, Piracicaba, SP, Brazil (in Portuguese).
• Amnuaykanjanasin, A.; Jirakkakul, J.; Panyasiri, C.; Panyarakkit, P.; Nounurai, P.; Chantasingh, D.; Eurwilaichitr, L.; Cheevadhanarak, S.; Tanticharoen, M. 2013. Infection and colonization of tissues of the aphid Myzus persicae and cassava mealybug Phenacoccus manihoti by the fungus Beauveria bassiana BioControl 58: 379-391.
• Avery, P.B.; Hunter, W.B.; Hall, D.G.; Jackson, M.A.; Powell, C.A.; Rogers, M.E. 2009. Diaphorina citri (Hemiptera: Psyllidae) infection and dissemination of the entomopathogenic fungus Isaria fumosorosea (Hypocreales: Cordycipitaceae) under laboratory conditions. Florida Entomologist 92: 608-618.
• Barbosa, L.R.; Rodrigues, A.P.; Soler, L.S.; Fernandes, B.V.; Castro, B.M.C.C.; Wilcken, C.F.; Zanuncio, J.C. 2017. Establishment in the field of Cleruchoides noackae (Hymenoptera: Mymaridae), an exotic egg parasitoid of Thaumastocoris peregrinus (Hemiptera: Thaumastocoridae). Florida Entomologist 100: 372-374.
• Charley, A.K. 1997. Entomopathogenic fungi and their role in pest control. p. 185-201. In: Wicklow, D.; Doderstrom, M., coords. The mycota. IV. Environmental and microbial. Springer, Heidelberg, Germany.
• Chow, A.; Dunlap, C.A.; Jackson, M.A.; Flores, D.; Patt, J.M.; Sétamou, M. 2016. Oviposition behavior and survival of Tamarixia radiate (Hymenoptera: Eulophidae), an ectoparasitoid of the Asian citrus psyllid, Diaphorina citri (Hemiptera: Liviidae), on hosts exposed to an entomopathogenic fungus, Isaria fumosorosea (Hypocreales: Cordycipitaceae), under laboratory conditions. Journal of Economic Entomology 109: 1995-2000.
• Costa, V.H.D.; Soares, M.A.; Dimaté Rodríguez, F.A.; Zanuncio, J.C.; Silva, I.M.; Valicente, F.H. 2015. Nomuraea rileyi (Hypocreales: Clavicipitaceae) in Helicoverpa armigera (Lepidoptera: Noctuidae) larvae in Brazil. Florida Entomologist 98: 796-798.
• Dal Pogetto, M.H.F.A.; Wilcken, C.F.; Gimenes, M.J.; Christovam, R.S.; Prado, E.P. 2011a. Control of red-gum lerp psyllid with formulated mycoinsecticides under semi-field conditions. International Journal of Tropical Insect Science 31: 85-91.
• Dal Pogetto, M.H.F.A.; Wilcken, C.F.; Christovam, R.S.; Prado, E.P.; Gimenes, M.J. 2011b. Effect of formulated entomopatogenic fungi on red gum lerp psyllid Glycaspis brimblecombei Research Journal of Forestry 5: 99-106.
• Echeverri-Molina, D.; Santolamazza-Carbone, S. 2010. Toxicity of synthetic and biological insecticides against adults of the Eucalyptus snout-beetle Gonipterus scutellatus Gyllenhal (Coleoptera: Curculionidae). Journal of Pest Science 83: 297-305.
• Furlong, M.J. 2004. Infection of the immature stages of Diadegma semiclausum, an endolarval parasitoid of the diamondback moth, by Beauveria bassiana Journal of Invertebrate Pathology 86: 52-55.
• Garcia, A.; Figueiredo, E.; Valente, C.; Monserrat, V.J.; Branco, M. 2013. First record of Thaumastocoris peregrinus in Portugal and of the neotropical predator Hemerobius bolivari in Europe. Bulletin of Insectology 66: 251-256.
• Hernández-Domínguez, C.; Guzmán-Franco, A.W.; Carrillo-Benítez, M.G.; Alatorre-Rosas, R.; Rodríguez-Leyva, R.; Villanueva-Jiménez, J.A. 2016. Specific diversity of Metarhizium isolates infecting Aeneolamia spp. (Hemiptera: Cercopidae) in sugarcane plantations. Neotropical Entomology 45: 80-87.
• Hussain, A.; Rizwan-Ul-Haq, M.; Al-Ayedh, H.; Al-Jabr, A.M. 2014. Mycoinsecticides: potential and future perspective. Recent Patents on Food, Nutrition and Agriculture 6: 45-53.
• Jacobs, D.H.; Neser, S. 2005. Thaumastocoris australicus Kirkaldy (Heteroptera: Thaumastocoridae): a new insect arrival in South Africa, damaging to Eucalyptus trees. South African Journal of Science 101: 233-236.
• Laudonia, S.; Sasso, R. 2012. The bronze bug Thaumastocoris peregrinus: a new insect recorded in Italy, damaging to Eucalyptus trees. Bulletin of Insectology 65: 89-93.
• Leemon, D.M.; Jonsson, N.N. 2012. Comparative studies on the invasion of cattle ticks (Rhipicephalus (Boophilus) microplus) and sheep blowflies (Lucilia cuprina) by Metarhizium anisopliae (Sorokin). Journal of Invertebrate Pathology 109: 248-259.
• Lemes, P.G.; Zanuncio, J.C.; Serrão, J.E.; Lawson, S.A. 2017. Forest stewardship council (FSC) pesticide policy and integrated pest management in certified tropical plantations. Environmental Science and Pollution Research 24:1283-1295.
• Lezama-Gutiérrez, R.; Molina-Ochoa, J.; Chávez-Flores, O.; Ángel-Sahagún, C.A.; Skoda, S.R.; Reyes-Martínez, G.; Barba-Reynoso, M.; Rebolledo-Domínguez, O.; Ruíz-Aguilar, G.M.L.; Foster, J.E. 2012. Use of the entomopathogenic fungi Metarhizium anisopliae, Cordyceps bassiana and Isaria fumosorosea to control Diaphorina citri (Hemiptera: Psyllidae) in Persian lime under field conditions. International Journal of Tropical Insect Science 32: 39-44.
• Li, M.; Li, S.; Xu, A.; Lin, H.; Chen, D.; Wang, H. 2014. Selection of Beauveria isolates pathogenic to adults of Nilaparvata lugens Journal of Insect Science 14:1-12.
• Lomer, C.J.; Bateman, R.P.; Johnson, D.L.; Langewald, J.; Thomas, M. 2001. Biological control of locust and grasshoppers. Annual Review of Entomology 44: 667-702.
• Mascarin, G.M.; Duarte, V.S.; Brandão, M.M.; Delalibera Jr., I. 2012. Natural occurrence of Zoophthora radicans (Entomophthorales: Entomophthoraceae) on Thaumastocoris peregrinus (Heteroptera: Thaumastocoridae), an invasive pest recently found in Brazil. Journal of Invertebrate Pathology 110: 401-404.
• Meyling, N.V.; Lübeck, M.; Buckley, E.P.; Eilenberg, J.; Rehner, S.A. 2009. Community composition, host range and genetic structure of the fungal entomopathogen Beauveria in adjoining agricultural and seminatural habitats. Molecular Ecology Resources 18: 1282-1293.
• Nadel, R.L.; Noack, A.E. 2012. Current understanding of the biology of Thaumastocoris peregrinus in the quest for a management strategy. International Journal of Pest Management 58: 257-266.
• Nadel, R.L.; Slippers, B.; Scholes, M.C.; Lawson, S.A.; Noack, A.E.; Wilcken, C.F.; Bouvet, J.P.; Wingfield, M.J. 2010. DNA bar-coding reveals source and patterns of Thaumastocoris peregrinus invasions in South Africa and South America. Biological Invasions 12: 1067-1077.
• Nadel, R.L.; Wingfield, M.J.; Scholes, M.C.; Garnas, J.R.; Lawson, S.A.; Slippers, B. 2015. Population dynamics of Thaumastocoris peregrinus in Eucalyptus plantations of South Africa. Journal of Insect Science 88: 97-106.
• Neves, P.M.O.J.; Hirose, E. 2005. Beauveria bassiana Strains Selection for Biological Control of the Coffee Berry Borer, Hypothenemus hampei (Ferrari) (Coleoptera: Scolytidae). Neotropical Entomology 34: 77-82 (in Portuguese, with abstract in English).
• Noack, A.E.; Kaapro, J.; Bartimote-Aufflick, K.; Mansfield, S.; Rose, H.A. 2009. Efficacy of Imidacloprid in the control of Thaumastocoris peregrinus on Eucalyptus scoparia in Sydney, Australia. Arboriculture & Urban Forestry 35: 192-196.
• Noack, A.E.; Rose, H.A. 2007. Life-history of Thaumastocoris peregrinus and Thaumastocoris sp. in the laboratory with some observations on behaviour. General and Applied Entomology 36: 27-33.
• Orduño-Cruz, N.; Guzmán-Franco, A.W.; Rodríguez-Leyva, E.; Alatorre-Rosas, R.; González-Hernández, H.; Mora-Aguilera, G. 2015. In vivo selection of entomopathogenic fungal isolates for control of Diaphorina citri (Hemiptera: Liviidae). Biological Control 90: 1-5.
• Oreste, M.; Bubici, G.; Poliseno, M.; Tarasco, E. 2016. Effect of Beauveria bassiana and Metarhizium anisopliae on the Trialeurodes vaporariorum-Encarsia formosa system. Journal of Pest Science 89: 153-160.
• Pelizza, S.A.; Mariottini, Y.; Russo, M.L.; Cabello, M.N.; Lange, C.E. 2013. Survival and fecundity of Dichroplus maculipennis and Ronderosia bergi (Orthoptera: Acrididae: Melanoplinae) following infection by Beauveria bassiana (Ascomycota: Hypocreales) under laboratory conditions. Biocontrol Science and Technology 23: 701-710.
• Peng, C.Y.S.; Zhou, X.; Kaya, H.K. 2002. Virulence and site of infection of the fungus Hirsutella thompsonii, to the honeybee ectoparasitic mite Varroa destructor Journal of Invertebrate Pathology 81: 185-195
• Raafat, I.; Meshrif, W.S.; El Husseiny, M.E.; El-Hariry, M.; Seif, A.I. 2015. Nezara viridula (Hemiptera: Pentatomidae) cuticle as a barrier for Beauveria bassiana and Paecilomyces sp. infection. African Entomology 23: 75-87.
• Ramos, E.Q.; Alves, S.B.; Demétrio, C.G.B.; Costa, S.C. 2004. Selection of entomopatogenic fungi to control Bemisia tabaci biotype B. Manejo Integrado de Plagas y Agroecología 73: 21-28 (in Portuguese, with abstract in English).
• Rios-Velasco, C.; Pérez-Corral, D.A.; Salas-Marina, M.A.; Berlanga-Reyes, D.I.; Ornelas-Paz, J.J.; Muñiz, C.H.C.; Cambero-Campos, J.; Jacobo-Cuellar, J.L. 2014. Pathogenicity of the Hypocreales fungi Beauveria bassiana and Metarhizium anisopliae against insect pests of tomato. Southwestern Entomologist 39: 739-750.
• Saavedra, M.C.; Avila, G.A.; Withers, T.M.; Holwell, G.I. 2015. The potential global distribution of the bronze bug Thaumastocoris peregrinus Carpintero and Dellapé (Hemiptera: Thaumastocoridae). Agricultural and Forest Entomology 17: 375-388.
• Soliman, E.P.; Wilcken, C.F.; Pereira, J.M.; Dias, T.K.R.; Zaché, B.; Dal Pogetto, M.H.F.A.; Barbosa, L.R. 2012. Biology of Thaumastocoris peregrinus Carpintero & Dellapé (Hemiptera: Thaumastocoridae) in different eucalyptus species and hybrids. Phytoparasitica 40: 223-230.
• Souza, A.R.; Candelaria, M.C.; Barbosa, L.R.; Wilcken, C.F.; Campos, J.M.; Serrão, J.E.; Zanuncio, J.C. 2016. Longevity of Cleruchoides noackae (Hymenoptera: Mymaridae), an egg parasitoid of Thaumastocoris peregrinus Hemiptera: Thaumastocoridae), with various honey concentrations and at several temperatures. Florida Entomologist 99: 33-37.
• Souza, G.K.; Pikart, T.G.; Pikart, F.C.; Serrão, J.E.; Wilcken, C.F.; Zanuncio, J.C. 2012. First record of a native heteropteran preying on the introduced eucalyptus pest, Thaumastocoris peregrinus (Hemiptera: Thaumastocoridae), in Brazil. Florida Entomologist 95: 517-520.
• Sun, J.Z.; Fuxa, J.R.; Richter, A.; Ring, D. 2008. Interactions of Metarhizium anisoplae and tree-based mulches in repellence and mycoses against Coptotermes formosanus (Isoptera: Rhinotermitidae). Environmental Entomology 37: 755-763.
• Wingfield, M.J.; Roux, J.; Slippers, B.; Hurley, B.P.; Garnas, J.; Myburg, A.A.; Wingfield, B.D. 2013. Established and new technologies reduce increasing pest and pathogen threats to Eucalypt plantations. Forest Ecology and Management 301: 35-42.
• Wu, S.; Gao, Y.; Xu, X.; Wang, D.; Li, J.; Wang, H.; Wang, E.; Lei, Z. 2015. Feeding on Beauveria bassiana-treated Frankliniella occidentalis causes negative effects on the predatory mite Neoseiulus barkeri Scientific Reports 5: 12033.
• Zanuncio, J.C.; Lemes, P.G.; Antunes, L.R.; Maia, J.L.S.; Mendes, J.E.P.; Tanganelli, K.M.; Salvador, J.F.; Serrão, J.E. 2016. The impact of the Forest Stewardship Council (FSC) pesticide policy on the management of leaf-cutting ants and termites in certified forests in Brazil. Annals of Forest Science 73: 205-214.

Edited by

Edited by: Alberto Soares Corrêa

Publication Dates

• Publication in this collection
  May-Jun 2019

History

• Received
  03 Feb 2017
• Accepted
  11 Feb 2018