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Establishment in the field of Cleruchoides noackae (Hymenoptera: Mymaridae), an exotic egg parasitoid of Thaumastocoris peregrinus (Hemiptera: Thaumastocoridae).

Eucalyptus species (Myrtales: Myrtaceae) (eucalyptus) are widely cultivated in more than 50 countries and thus represent the most commercially important timber in the world (Iglesias-Trabado & Wilstermann 2008; Shi et al. 2012). Thaumastocoris peregrinus Carpintero and Dellape (Hemiptera: Thaumastocoridae), known as the bronze bug, damages eucalyptus plants worldwide. This pest is a native Australian hemipteran that feeds on the leaves of a wide variety of eucalyptus species and hybrids (Carpintero& Dellape 2006; Noacket al. 2011; Soliman et al. 2012; Mutitu et al. 2013), causing silvering, tanning, and leaf drying. The efficiency of pesticides usage in forest crops is reduced because of the extensive nature of forest plantations, the height of eucalyptus trees, and the behavior of this insect pest (Zanuncio et al. 2010; Mewes et al. 2015).

Thaumastocoris peregrinus has been found in more than 10 countries across Europe, Africa, South America, and Oceania with a very fast spreading rate (Saavedra et al. 2015). Special attention should be paid to the regions of southern USA, Central America, and southern China and nearby countries, where environmental conditions are highly suitable for T. peregrinus population development (Montemayor et al. 2015).

Biological control is one of the strategies for the management of insect pests in forest plantations (Braganca et al. 1998; Pereira et al. 2008b; Garnas et al. 2012; Dias et al. 2014). Cleruchoides noackae Lin and Huber (Hymenoptera: Mymaridae), an egg parasitoid, the lacewings Hemerobius bolivari Banks (Neuroptera: Hemerobiidae) and Chrysoperla externa (Hagen) (Neuroptera: Chrysopidae), and predatory bugs have been reported as the main natural enemies of the bronze bug (Nadel & Noack 2012; Souza et al. 2012; Garcia et al. 2013). Parasitism of T. peregrinus by C. noackae was 25% in the field and 21% in the laboratory in Australia and 32% in the laboratory in South Africa (Mutitu et al. 2013).

The introduction and successful establishment of natural enemies are important to regulate pest populations (Gerard et al. 2011; Thompson & Reddy 2016). For establishment, the parasitoid should be able to find its host at both long and short distances (Cronin & Reeve 2014) and to adapt to environmental variability (Vercken et al. 2016). The objective of this study was to evaluate the parasitism of C. noackae on T. peregrinus under laboratory conditions and on eucalyptus plantations in Brazil.

Materials and Methods

Thaumastocoris peregrinus was reared in the laboratory at 24 + 2 [degrees]C, 60 +10% RH, and a photoperiod of 12:12 h L:D on bouquets of Eucalyptus benthamii Maiden & Cambage (Myrtales: Myrtaceae) branches; the branches were fixed in a piece of foam to prevent drowning in a 500 mL glass flask filled with water (Barbosa et al. 2016).

Ten 0- to 24-h-old T. peregrinus eggs per paper towel strip obtained from a laboratory mass rearing facility (Laboratory of Forest Entomology of the EMBRAPA, Colombo, Brazil) were placed in a polystyrene vial (7.0 cm long and 3.0 cm in diameter) with a central hole and a plastic top sealed with "voile" fabric for airing. The eggs were exposed to C. noackae parasitism for 24 h with 23 replications. The parasitoid adults were obtained from Laboratory of Forest Entomology of the EMBRAPA, Colombo, Brazil). They were fed with 50% honey solution on filter paper strips (0.5 x 5 cm). These vials were kept in chambers at the following conditions: temperature of 23 + 2 [degrees]C, relative humidity of 60 +10%, and a photoperiod of 12:12 h L:D.

Observations in the field were performed in Oct 2013 on eucalyptus plantations (growing clone VM01 of the hybrid Eucalyptus urophylla S. T. Blake x Eucalyptus camaldulensis Denhardt; Myrtales: Myrtaceae) of Vallourec Florestal in Minas Gerais State, Brazil (19.2511[degrees]S, 44.4683[degrees]W; 750 m altitude). Eucalyptus leaves with T. peregrinus eggs were collected from 22 points in an area of approximately 2 ha 1 yr after the first release of C. noackae. A sample of 30 viable T. peregrinus eggs (without signs of nymph hatching) was removed from the middle portion of the tree canopy per collection point, stored in polystyrene vials as described earlier for the parasitism experiment, and kept at a temperature of 23 [degrees]C and relative humidity of 60%. Other samples of T. peregrinus eggs were collected at random points of the plantation to evaluate C. noackae dispersion in the field.

The emergence of parasitoids was observed under a stereomicroscope, and they were sexed based on their external morphology. The number of adults emerged per d, the percentage of emergence, and the sex ratio (SR = number of [female]/ number of [male] + [female]) of C. noackae from T. peregrinus eggs in the laboratory experiment and from samples collected in the field were calculated for 20 d.

Results and Discussion

In total, 230 and 660 T. peregrinus eggs were evaluated from those of the laboratory experiment and the field collection, respectively; the percentage of emergence of C. noackae from these eggs was 53% and 52%, respectively (Table 1). The similar parasitism rates on T. peregrinus in the laboratory and the field suggest high efficacy of C. noackae in Brazil, and the rates were higher than those reported in the laboratory (25%) and the field (21%) in Sydney, Australia, and in the laboratory (34%) in Pretoria, South Africa (Mutitu et al. 2013). These results may be due to different strains of this parasitoid as found for Trichogramma species (Hymenoptera: Trichogrammatidae) (Pak et al. 1986; Oliveira et al. 2000) or due to environmental conditions (Grevstad 1999; Vercken et al. 2015).

The parasitism rate of 1-d-old T. peregrinus eggs by C. noackae in the laboratory was higher than that reported on Eucalyptus grandis W. Hill ex Maiden (Myrtales: Myrtaceae) clone Tag 5 in South Africa, which was 34.1 and 16.6% in 0- to 1-d-old and 4- to 5-d-old eggs, respectively, of this host (Mutitu et al. 2013). Hosts in the initial development stages may be more appropriate than those in the late stages for hymenopteran parasitoids (Lytle et al. 2012; Penaflor et al. 2012; Tavares et al. 2013) as shown for C. noackae (Mutitu et al. 2013), Gonatocerus ashmeadi Girault, Gonatocerus triguttatus Girault, and Gonatocerus fasciatus Girault (Hymenoptera: Mymaridae) (Irvin & Hoddle 2005), Trichogramma species (Vianna et al. 2009; Soares et al. 2012), and Eulophidae species (Pereira et al. 2008a,b).

The sex ratio of C. noackae in the laboratory and field was similar, 69 and 65% females, respectively. This result indicates favorable conditions for mass rearing (Heimpel & Lundgren 2000) with a greater female production than that found in the laboratory in Pretoria, South Africa, where the sex ratio was 50% (Mutitu et al. 2013). A high male production could be the result of poor host quality (Pereira et al. 2009; Zanuncio et al. 2010), high parasitoid/host ratio, or inbreeding (Tavares et al. 2009; Vianna et al. 2009).

The emergence of C. noackae in the laboratory was highest on day 17and decreased until day 21 with an average development period of 17.9 d from oviposition to emergence (Fig. 1). The parasitoid can parasitize and complete its development from oviposition to adult emergence in 15.7 d in host eggs (Mutitu et al. 2013).

The information generated in this study is an important step to developing an integrated pest management program that includes releases of the egg parasitoid C. noackae as a biological control agent of T. peregrinus on eucalyptus plantation in Brazil. The recovery of C. noackae from T. peregrinus eggs collected in the field shows that this parasitoid reproduced and dispersed to a distance of over 10 km from its initial release point after 1 yr. This is the first record of the successful establishment and efficiency of C. noackae in the biological control of T. peregrinus in Brazil.


Thanks to Coordenacao de Aperfeicoamento de Pessoal de Nivel Superior (CAPES), Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPq), Fundacao de Amparo a Pesquisa do Estado de Minas Gerais (FAPEMIG), and Empresa Brasileira de Pesquisa Agropecuaria (EMBRAPA) for financial support. Global Edico Services corrected and proofread the English in the first version of this manuscript.

References Cited

Barbosa LR, Santos F, Buhrer CB, Nichele LA, Wilcken CF, Soliman EP. 2016. Criacao massal do percevejo bronzeado, Thaumastocoris peregrinus Carpinteiro & Dellape, 2006 (Hemiptera: Thaumastocoridae). Embrapa, Brasilia, Brasil. DOI: 10.13140/RG.2.2.36424.11528. [In Portuguese]

Braganca MAL, De Souza O, Zanuncio JC. 1998. Environmental heterogeneity as a strategy for pest management in Eucalyptus plantations. Forest Ecology and Management 102:9-1.

Carpintero DL, Dellape PM. 2006. A new species of Thaumastocoris kirkaldy from Argentina (Heteroptera: Thaumastocoridae: Thaumastocorinae). Zootaxa 1228: 61-68.

Cronin J, Reeve J. 2014. An integrative approach to understanding host-parasitoid population dynamics in real landscapes. Basic and Applied Ecology 15:101-113.

Dias TKR, Wilcken CF, Soliman EE, Barbosa LR, Serrao JE, Zanuncio JC. 2014. Predation of Thaumastocoris peregrinus (Hemiptera: Thaumastocoridae) by Atopozelus opsimus (Hemiptera: Reduviidae) in Brazil. Invertebrate Survival Journal 11:224-227.

Garcia A, Figueiredo E, Valente C, Monserrat VJ, 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.

Garnas JR, Hurley BP, Slippers B, Wingfield MJ. 2012. Biological control of forest plantation pests in an interconnected world requires greater international focus. International Journal of Pest Management 58:211-223.

Gerard PJ, Wilson DJ, Eden TM. 2011. Field release, establishment and initial dispersal of Irish Microctonus aethiopoides in Sitona lepidus populations in northern New Zealand pastures. BioControl 56:861-870.

Grevstad FS. 1999. Factors influencing the chance of population establishment: implications for release strategies in biocontrol. Ecological Applications 9:1439-1447.

Heimpel GE, Lundgren JGJ. 2000. Sex ratios of commercially reared biological control agents. Biological Control 19:77-93.

Iglesias-Trabado G, Wilstermann D. 2008. Eucalyptus universalis. Global Cultivated Eucalypt Forests Map 2008, Version 1.0.1, (last accessed 14 Jun 2016).

Irvin NA, Hoddle MS. 2005. Determination of Homalodisca coagulata (Hemiptera: Cicadellidae) egg ages suitable for oviposition by Gonatocerus ashmeadi, Gonatocerustriguttatus, and Gonatocerusfasciatus (Hymenoptera: Mymaridae). Biological Control 32: 391-400.

Lytle J, Morse JG, Triapitsyn SV. 2012. Biology and host specificity of Gonatocerus deleoni (Hymenoptera: Mymaridae), a potential biocontrol agent of Homalodisca vitripennis (Hemiptera: Cicadellidae) in California, USA. BioControl 57:61-69.

Montemayor SI, Dellape PM, Melo MC. 2015. Geographical distribution modeling of the bronze bug: a worldwide invasion. Agricultural and Forest Entomology 17:129-137.

Mewes WLC, Teixeira MM, Fernandes HC, Zanuncio JC, Tiburcio RAS. 2015. Parametros caracteristicos da pulverizacao pneumatica em copas de arvores de eucalipto. Revista Arvore 39:635-640. [In Portuguese]

Mutitu EK, Garnas JR, Hurley BP, Wingfield MJ, Harney M, Bush SJ, Slippers B. 2013. Biology and rearing of Cleruchoides noackae (Hymenoptera: Mymaridae), an egg parasitoid for the biological control of Thaumastocoris peregrinus (Hemiptera: Thaumastocoridae). Journal of Economic Entomology 106: 197-198.

Nadel RL, Noack AE. 2012. Current understanding of the biology of Thaumastocoris peregrinus in the quest for a management strategy. International Journal of Pest Management 58:257-266.

Noack AE, Cassis G, Rose HA. 2011. Systematic revision of Thaumastocoris Kirkaldy (Hemiptera: Heteroptera: Thaumastocoridae). Zootaxa 3121:1-60.

Oliveira HN, Zanuncio JC, Pratisssoli D, Cruz I. 2000. Parasitism rate and viability of Trichogramma maxacalii (Hym.: Trichogrammatidae) parasitoid of the Eucalyptus defoliator Euselasia apisaon (Lep.: Riodinidae), on eggs of Anagasta kuehniella (Lep.: Pyralidae). Forest Ecology and Management 130:1-6.

Pak GA, Buis CEM, Heck ICC, Hermans MLG. 1986. Behavioural variations among strains of Trichogramma spp.: host-age selection. Entomologia Experimentalis et Applicata 40:247-258.

Penaflor MFGV, Sarmento MMM, Bezerra da Silva CS, Werneburg AG, Bento JM. 2012. Effect of host egg age on preference, development and arrestment of Telenomus remus (Hymenoptera: Scelionidae). European Journal of Entomology 109:15-20.

Pereira FF, Zanuncio TV, Zanuncio JC, Pratissoli D, Tavares MT. 2008a. Species of Lepidoptera defoliators of eucalypt as new hosts for the polyphagous parasitoid Palmistichus elaeisis (Hymenoptera: Eulophidae). Brazilian Archives of Biology and Technology 51:259-262.

Pereira FF, Zanuncio JC, Tavares MT, Pastori P, Jacques GC, Vilela EF. 2008b. New record of Trichospilus diatraeae as parasitoid of the eucalypt defoliator Thyrinteina arnobia in Brasil. Phytoparasitica 36:304-306.

Pereira FF, Zanuncio JC, Serrao JE, Pratissoli DP. 2009. Progenie de Palmistichus elaeisis Delvare & LaSalle (Hymenoptera: Eulophidae) em pupas de Bombyx mori Linnaeus (Lepidoptera: Bombycidae) de diferentes idades. Neotropical Entomology 38:660-664. [In Portuguese]

Saavedra MC, Avila GA, Withers TM, Holwell Gl. 2015. The potential global distribution of the bronze bug Thaumastocoris peregrinus Carpintero and Dellape (Hemiptera: Thaumastocoridae). Agricultural and Forest Entomology 17:375-388.

Shi Z, Xu D, Yang X, Jia Z, Guo H, Zhang N. 2012. Ecohydrological impacts of eucalypt plantations: a review. Journal of Food, Agriculture and Environment 10: 1419-1426.

Soares MA, Leite GLD, Zanuncio JC, Sa VGM, Ferreira CS, Rocha SL, Pires EM, Serrao JE. 2012. Quality control of Trichogramma atopovirilia and Trichogramma pretiosum (Hym.: Trichogrammatidae) adults reared under laboratory conditions. Brazilian Archives of Biology and Technology 55:305-311.

Soliman EP, Wilcken CF, Pereira JM, Dias TKR, Zache B, Dal Pogetto MHFA, Barbosa LR. 2012. Biology of Thaumastocoris peregrinus in different Eucalyptus species and hybrids. Phytoparasitica 40:223-230.

Souza GK, Pikart TG, Pikart FC, Serrao JE, Wilcken CF, Zanuncio JC. 2012. First record of a native heteropteran preying on the introduced eucalyptus pest, Thaumastocoris peregrinus (Hemiptera: Thaumastocoridae), in Brazil. Florida Entomologist 95:517-520.

Tavares WS, Cruz I, Petacci F, Assis Junior SL, Freitas SS, Zanuncio JC, Serrao JE. 2009. Potential use of Asteraceae extracts to control Spodoptera frugiperda (Lepidoptera: Noctuidae) and selectivity to their parasitoids Trichogramma pretiosum (Hymenoptera: Trichogrammatidae) and Telenomus remus (Hymenoptera: Scelionidae). Industrial Crops and Products 30:384-388.

Tavares WS, Soares MA, Mielke OHH, Poderoso JCM, Serrao JE, Zanuncio JC. 2013. Emergence of Palmistichus elaeisis Delvare & LaSalle, 1993 (Hymenoptera: Eulophidae) from pupae of Heraclides anchisiades capys (Hubner, [1809]) (Lepidoptera: Papilionidae) in the laboratory. Folia Biologica (Krakow) 61: 233-238.

Thompson BM, Reddy GVP. 2016. Status of Sitodiplosis mosellana (Diptera: Cecidomyiidae) and its parasitoid, Macroglenes penetrans (Hymenoptera: Pteromalidae), in Montana. Crop Protection 84: 125-131.

Vercken E, Fauvergue X, Ris N, Crochard D, Mailleret L. 2015. Temporal autocorrelation in host density increases establishment success of parasitoids in an experimental system. Ecology and Evolution 5:2684-2693.

Vianna UR, Pratissoli D, Zanuncio JC, Lima ER, Brunner J, Pereira FF, Serrao JE. 2009. Insecticide toxicity to Trichogramma pretiosum (Hymenoptera: Trichogrammatidae) females and effect on descendant generation. Ecotoxicology 18:180-186.

Zanuncio AJV, Pastori PL, Kirkendall LR, Lino-Neto J, Serrao JE, Zanuncio JC. 2010. Megaplatypus mutates (Chapuis) (Coleoptera: Curculionidae: Platypodinae) attacks hybrid Eucalyptus (L.) Heritier de Brutelle clones in southern Espirito Santo, Brazil. The Coleopterists Bulletin 64:81-83.

Leonardo Rodrigues Barbosa (1), Angelo Pemffo Rodrigues (1), Lorena da Silva Soler (1), Bianca Vique Femandes (2), Barbara Monteiro de Castro e Castro (3), Carlos Frederico Wilcken (4), and Jose Cola Zanuncio (5,*)

(1) Empresa Brasileira de Pesquisa Agropecuaria--Embrapa Florestas, 83411-000, Colombo, Parana, Brasil; E-mail: (L. R. B.), (A. P. R.), (L. S. S.)

(2) Centro de Competencia FlorestahVallourec Florestal, 35.774-000, Paraopeba, Minas Gerais, Brasil; E-mail: (B. V. F.)

(3) Departamento de Fitotecnia, Universidade Federal de Vicosa, 36570-900, Vicosa, Minas Gerais, Brasil; E-mail: (B. M. C. C.)

(4) Faculdade de Ciencias Agronomicas, Departamento de Protecao Vegetal, 18610-307, Botucatu, Sao Paulo, Brasil; E-mail: (C. F. W.)

(5) Departamento de Entomologia/BIOAGRO, Universidade Federal de Vicosa, 36570-900, Vicosa, Minas Gerais, Brasil; E-mail: (J. C. Z.)

(*) Corresponding author; E-mail: (J. C. Z.)

Caption: Fig. 1. Total number of Cleruchoides noackae (Hymenoptera: Mymaridae) adults emerged from Thaumastocoris peregrinus (Hemiptera: Thaumastocoridae) eggs per d that were parasitized in the laboratory (23 [+ or -] 2 [degrees]C, 60 [+ or -] 10% RH, and 12:12 h L:D photoperiod) and from eggs of this pest collected in the field.

Please Note: Illustration(s) are not available due to copyright restrictions.
Table 1. Total number of eggs and adults, percentage of emergence, and
sex ratio (mean [+ or -] SE) of Cleruchoides noackae (Hymenoptera:
Mymaridae) from Thaumastocoris peregrinus (Hemiptera: Thaumastocoridae)
eggs perd.

Site         Eggs(n)   Adults (n)   Emergence (%)   Sex ratio

Laboratory   230       123          53 [+ or -]3    0.69 [+ or -] 0.02
Field (a)    660       342          52 [+ or -]3    0.65 [+ or -] 0.02

(a) Paraopeba, Minas Gerais State, Brazil.
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Author:Barbosa, Leonardo Rodrigues; Rodrigues, Angelo Pemffo; Soler, Lorena da Silva; Femandes, Bianca Viqu
Publication:Florida Entomologist
Article Type:Report
Geographic Code:3BRAZ
Date:Jun 1, 2017
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