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 Dellapé (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 & Dellapé 2006; Noack et 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 (Bragança 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 °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 × 5 cm). These vials were kept in chambers at the following conditions: temperature of 23 ± 2 °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 × Eucalyptus camaldulensis Denhardt; Myrtales: Myrtaceae) of Vallourec Florestal in Minas Gerais State, Brazil (19.2511°S, 44.4683°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 °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 ♀ / number of ♂+♀) 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).

Table 1.

Total number of eggs and adults, percentage of emergence, and sex ratio (mean ± SE) of Cleruchoides noackae (Hymenoptera: Mymaridae) from Thaumastocoris peregrinus (Hemiptera: Thaumastocoridae) eggs per d.

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; Peñaflor 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).

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 ± 2 °C, 60 ± 10% RH, and 12:12 h L:D photoperiod) and from eggs of this pest collected in the field.

The emergence of C. noackae in the laboratory was highest on day 17 and 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.