Native to Australia Gonipterus platensis Marelli (Coleoptera: Curculionidae) is the main beetle defoliator of eucalyptus worldwide, causing damage in various regions in which it was introduced, where its management relies mostly on biological control with the parasitoid Anaphes nitens (Girault) (Hymenoptera: Mymaridae). In this report, we present the first laboratory evidence of efficient predation by Podisus nigrispinus Dallas (Hemiptera: Pentatomidae) on G. platensis larvae. This predatory species is native to Brazil and a promising biological control agent for use in the integrated pest management of G. platensis.
The genus Gonipterus (Coleoptera: Curculionidae) is originally from Australia (Mally 1924; Mapondera et al. 2012) and has a wide geographic distribution, having been reported in Africa, Europe, North America, Asia, and South America (Lanfranco & Dungey 2001; EPPO 2005). Gonipterus was detected for the first time in Brazil in 1928, but in field manuals, the first scientific report was given in 1982 from the state of Santa Catarina with the species Gonipterus platensis Marelli and Gonipterus gibberus Boisduval (Fenilli 1982), which later spread to the state of São Paulo (Rosado-Neto 1993).
The introduction of G. platensis, the main eucalyptus leaf-eating beetle in the world, causes economic losses in various regions. The larvae feed on young leaves and defoliate the top parts of the plant canopy (Mansilla-Vázquez 1992), and the adults feed on the edges of mature leaves (Mally 1924), impairing the growth of the plant. The larval stage has 4 instars, each lasting approximately 1 wk (Santolomazza-Carbone 2002). The females lay up to 800 eggs (Arzone & Meotto 1978). Since the discovery of this pest in Brazil, this scientific report is the first to document the action of a predatory species, Podisus nigrispinus Dallas (Hemiptera: Pentatomidae), preying on larvae and adults of G. platensis.
Predators in the order Hemiptera and the family Pentatomidae, such as Supputius cincticeps Stål (Souza et al. 2012), Brontocoris tabidus (Signoret) (Zanuncio et al. 2000), and P. nigrispinus (Torres et al. 2008) are reported as biological control agents of forest pests. Podisus nigrispinus also preys on various agricultural pests in Brazil, being a significant natural enemy and widespread in the whole country (Zanuncio et al. 2008; Torres et al. 2006). This paper evaluates the potential of P. nigrispinus to be used in an integrated pest management program following the first worldwide observation of P. nigrispinus nymphs preying on G. platensis larvae in a commercial plantation near Itararé, São Paulo, Brazil. Gonipterus species are currently being controlled in Brazil, and in other countries where they occur, with the egg parasitoid Anaphes nitens (Girault) (Hymenoptera: Mymaridae) (Wilcken et al. 2008; Reis et al. 2012) and the entomopathogenic fungus Beauveria bassiana (Bals.-Criv.) Vuill. (Cordycipitaceae) (Berti-Filho et al. 1992). Additionally, the larva parasitoid Entendon magnificus (Girault & Dodd) (Hymenoptera: Eulophidae) has been studied in Chile (Gumovsky et al. 2015). The introductions of new parasitoid species highlight the limitation of the current biological control efforts with A. nitens.
In this study, we evaluated the predation efficiency of P. nigrispinus on G. platensis in the Forest Protection Laboratory of Suzano Pulp and Paper Company. Larvae and adults of G. platensis were collected 3 d before the experiment from an infested field site and were kept on Eucalyptus urophylla S. T. Blake × Eucalyptus grandis W. Hill ex Maiden (Myrtaceae) leaves at a constant temperature of 24 ± 2°C. Nymphs and adults of the predator P. nigrispinus were reared at the Forest Protection Laboratory and fed Tenebrio molitor L. (Coleoptera: Tenebrionidae) larvae.
The experiment was conducted at a temperature of 24 ± 2 °C, relative humidity of 60 ± 10%, and a photoperiod of 12:12 h L:D. The experimental setup was completely randomized with 4 replications of the following treatments: 20 adults of G. platensis (T1, control), 20 larvae of G. platensis (T2, control), 2 adults (1 male and 1 female) of P. nigrispinus with 20 adults of G. platensis (T3), 2 adults (1 male and 1 female) of P. nigrispinus with 20 larvae of G. platensis (T4), 2 nymphs of P. nigrispinus with 20 larvae of G. platensis (T5), and 2 nymphs of P. nigrispinus with 20 adults of G. platensis (T6). The insects were kept in plastic pots (250 mL) covered with a voile cloth lid, upon which a damp cotton ball was placed as a water source for the predator. Leaves of E. urophylla × E. grandis served as a food source for Gonipterus and were replaced daily throughout the assay. In the treatments with prey larvae (T2, T4, and T5) 11, 6, and 3 larvae in the 2nd, 3rd, and 4th instar were offered, respectively. Adults of P. nigrispinus were newly emerged and the nymphs were in the 4th instar.
Fig. 1.
Cumulative efficiency of predation (%) by Podisus nigrispinus nymphs and adults on of G. platensis larvae and adults over a period of 5 d: 2 adults (1 male and 1 female) of P. nigrispinus with 20 adults of G. platensis (T3), 2 adults (1 male and 1 female) of P. nigrispinus with 20 larvae of G. platensis (T4), 2 nymphs of P. nigrispinus with 20 larvae of G. platensis (T5), and 2 nymphs of P. nigrispinus with 20 adults of G. platensis (T6)

Table 1.
Average number ± SE of dead Gonipterus platensis larvae or adults on each evaluation day of predation by Podisus nigrispinus nymphs or adults tested in the laboratory (temperature of 24 ± 2 °C, photoperiod of 12:12 h L:D, and total duration of predation of 5 d).

The numbers of dead prey insects were recorded 1, 2, 3, 4, and 5 d after pest—predator contact. Mean numbers of insects preyed per d were compared by analysis of variance and means separated with the Tukey test at 5% probability, using SISVAR® Version 5.6 software (Ferreira 2008). The efficiency of predation was calculated based on the number of live insects using the Abbott formula: efficiency (%) = [1 - (number of live insects in the predation treatment / number of live insects in the predation-free control)] × 100 (Abbott 1925).
The results showed that adults and nymphs of P. nigrispinus were efficient in preying on G. platensis larvae, causing 98 and 74% mortality, respectively, after 5 d (Fig. 1). Observation over time showed a gradual daily increase in the consumption of prey insects (Table 1) indicating that P. nigrispinus could be a suitable biocontrol agent in the integrated management of G. platensis. However, the preying on G. platensis adults by adults and nymphs of P. nigrispinus was lower, with efficiency rates of 4 and 14%, respectively, after 5 d (Fig. 1). Other species of Pentatomidae, such as Podisus mucronatus Uhler and Podisus maculiventris (Say), were reported preying on Curculionidae (Costello et al. 2002; Medal & Santa Cruz 2014).
This first laboratory evidence of P. nigrispinus as an efficient native predator of G. platensis larvae in Brazil is an important step in the development of integrated management tactics to control this exotic pest. At Suzano Pulp and Paper Company, P. nigrispinus is being studied for simultaneous releases with A. nitens and applications of B. bassiana to target various life stages of G. platensis and ultimately combine these biological control agents in an efficient integrated pest management program against G. platensis.