The survival, development, and reproduction of Gonipterus platensis (Coleoptera: Curculionidae) on the main Eucalyptus (Myrtaceae) genotypes planted in Brazil

Introduction

Planted forests cover around 131 million hectares in the world (FAO, 2020). Brazil is one of the biggest producers with 9.55 million hectares in 2021 to produce raw material for bioenergy, firewood, laminate, pulp and paper, timber, and wall panels (Ribeiro, Rodrigues & Ballarin, 2020; IBÁ, 2021). Eucalyptus L’Hér. (Myrtales: Myrtaceae) is the most prominent plant genus in Brazilian forest plantations with around 78% of the area planted (IBÁ, 2021). The rapid growth, easy regeneration and cultivation, adaptation to different geographic location places, multiple uses, among others, contribute to the expansion of Eucalyptus in the world (Tomé et al., 2021). The large areas with forest plantations and increase in the international trade of the wood products (e.g., wood packaging, tree logs, and wood chips), contribute to the introduction and spread of insect pests to uninfested geographic regions with Eucalyptus plantations (Andrade et al., 2016; Almeida et al., 2018; Meurisse et al., 2019; Tomé et al., 2021).

The Eucalyptus snout beetle, Gonipterus platensis Marelli (Coleoptera: Curculionidae), is native to Australia and is the most widely distributed defoliating beetle of Eucalyptus in the world (Hurley et al., 2016). This insect was reported in the Brazilian states of Espírito Santo, Rio Grande do Sul, Santa Catarina, Paraná, and São Paulo with higher damage in plantations of the latter two states (Wilcken et al., 2008; Souza et al., 2016), especially in Eucalyptus grandis W. Hill. × Eucalyptus urophylla S.T. Blake hybrids (Souza et al., 2016).

Gonipterus platensis adults feed on the young and middle-aged leaves and on soft bark of twigs, while its larvae feed exclusively on shoot tips and young leaves (Souza et al., 2016). High infestations of G. platensis cause dieback of shoot tips, which may induce the development of epicormic shoots and severe defoliation of the upper third of tree canopy. Sequential defoliations may result in growth of multiple leader shoots and mortality of branches or even trees (Tooke, 1955). Damage by G. platensis is low in Australia because of the natural resistance of Eucalyptus species and the suppression of this pest by a diversity of natural enemies (Valente et al., 2017; Valente et al., 2019; Afonso et al., 2019). However, this insect causes severe damage on exotic Eucalyptus species in some African, American, and European countries (Reis et al., 2012; Souza et al., 2016; Valente et al., 2018; Schröder et al., 2020), resulting in a constant search for alternatives to control this pest (Nascimento et al., 2017; Damascena et al., 2020; Schröder et al., 2021).

The susceptibility of Eucalyptus genotypes to Gonipterus spp. Schoenherr varies according to the Eucalyptus sections (taxonomic division of subgenus), species, and hybrids. The Symphormitus subgenus includes about 470 species divided into 11 sections according to their taxonomic and molecular characteristics, of which the Exsertaria, Latoangulatae, and Maidenaria sections represent about 90% of the area planted with Eucalyptus in the world (Nicolle & Jones, 2018; Scanavaca Junior & Garcia, 2021). High populations of the G. platensis and extensive defoliation are more common on Eucalyptus species of the Maidenaria section (Garcia et al., 2019; Gonçalves et al., 2019). Gonipterus platensis in its region of origin infests species of the Maidenaria section including Eucalyptus dalrympleana Maiden, Eucalyptus globulus Labill., Eucalyptus nitens (H. Deane & Maiden) Maiden, Eucalyptus ovata Labill., Eucalyptus rubida H. Deane & Maiden, and Eucalyptus viminalis Labill (Mapondera et al., 2012; Garcia et al., 2019). This pest also infests Eucalyptus species of different sections in countries where it has been introduced. In the Iberian Peninsula, species of the Maidenaria section are defoliated into variable levels, but those of the Latoangulatae section, like Eucalyptus saligna Sm., are only lightly defoliated (Reis et al., 2012; Valente et al., 2018; Gonçalves et al., 2019). In Chile, severe defoliation on E. globulus (Maidenaria section) and on species of the Exsertaria section such as Eucalyptus camaldulensis Dehnh. has been reported (Lanfranco & Dungey, 2001). In Brazil, species of the sections Exsertaria, Latoangulatae and Maidenaria are largely planted but Eucalyptus dunnii Maiden, E. globulus and E. viminalis (Maidenaria section) are the most damaged by G. platensis, which also damages other species such as Eucalyptus saligna (var. protusa) (Latoangulatae section) and the hybrids E. grandis × E. urophylla (=HGU) and E. grandis × E. dunnii (Wilcken et al., 2008; Souza et al., 2016).

The losses in wood yield by G. platensis in Brazil varies within plant genetic materials from a mean annual increment (MAI) reduction of 10.0% on E. grandis to 42.8% on E. grandis × E. dunnii hybrids (Souza et al., 2016). In 2003, G. platensis damaged around 50,000 ha of a HGU clonal plantation in Espírito Santo State with its aggressiveness associated with the high susceptibility of this plant material (Wilcken et al., 2008).

Chemical, nutritional and/or morphological differences in leaves between Eucalyptus genotypes, such as secondary compounds, leaf waxes, nitrogen and tannin levels affect the host selection (Gripenberg et al., 2010) and the insect development (Ohmart & Edwards, 1991; Koul , 2008; Behmer, 2009; Gherlenda et al., 2016), which may explain the susceptibility of Eucalyptus genotypes to G. platensis. The selection of host plants by G. platensis is influenced by the emission of volatiles from green leaves and terpenes, such as terpenol 1,8-cineole (Bouwer et al., 2014; Branco et al., 2019), which is more concentrated in Maidenaria species susceptible to G. platensis than Latoangulatae species.

Species of the Latoangulatae section are the most planted Eucalyptus in Brazil and their susceptibility to G. platensis is poorly known, especially in tropical areas, for lack of information on the suitability of these Eucalyptus species to this insect. Field observation, host plant response, and insect pest performance are methods used to evaluate host-plant suitability to phytophagous insects (Donatelli et al., 2017). The field observation method integrates the host plant response and insect pest performance with environmental conditions in natural and uniform outbreaks over experimental areas where uncontrolled environments can lead to experimental errors (Sallé et al., 2017). The host plant response in the field is difficult to evaluate for Gonipterus - Eucalyptus interactions because this insect feeds on trees from one to six years old, with reduced possibilities of being monitored in field conditions. Therefore, the insect pest performance in laboratory, under controlled conditions, allows a more adequate assessment of biological parameters at all stages of the insect than that on field studies.

The objective of this work was to evaluate the development, reproduction and survival of G. platensis fed with leaves of E. camaldulensis, E. grandis, E. urophylla, and of the hybrids HGU ‘H13’ and ‘VR3748’ of Eucalyptus grandis × E. urophylla under controlled conditions, and to determine the susceptibility of these plants to this insect pest. Our hypothesis was that commercial Eucalyptus species/clones cultivated in Brazil affect differently the development, reproduction, and survival of G. platensis. The information can be used to manage this pest, avoiding extensive plantations with susceptible Eucalyptus species, and reducing the risks of population outbreaks in commercial plantations.

Material & Methods

Results

Adult complete lifespan and longevity

The adult (females + males) complete lifespan was longer in E. urophylla (223.9 ± 11.2 days) than in the hybrids ‘VR3748’ and ‘H13’ (171.3 ± 14.01 and 146.1 ± 10.6 days, respectively), E. grandis (61.9 ± 16.9 days), and E. camaldulensis (75.2 ± 8.4 days). The longevity of adult females was longer in E. urophylla (283.3 ± 18.3 days) than in E. camaldulensis (103.8 ± 12.6 days) and E. grandis (65.3 ± 27.5 days) and that of males longer in E. urophylla (175.8 ± 10.5 days), ‘VR3748’ (149.8 ± 11.6 days) than in ‘H13’ (127.4 ± 11.0 days), with the second lowest duration on E. camaldulensis (68.1 ± 9.4 days) and the lowest longevity in E. grandis (60.8 ± 21.4 days) (Table 2).

Discussion

The environmental conditions in the Eucalyptus plantations in South and Southeast Brazil are similar to those of the Gonipterus distribution in Australia, which are a humid subtropical zone with a temperate climate and hot or temperate summers (Crosbie et al., 2012; Mapondera et al., 2012; Alvares et al., 2013). The damage by G. platensis was low in these areas up to 2012 and increased from the end of 2012 (Souza et al., 2016), probably because of the replacement of E. grandis by more productive HGU clones (C.F.W. personal information, 2022). The G. platensis survival, development and reproduction differ among the Eucalyptus species and hybrids with E. urophylla being the most suitable host for this insect, the HGU ‘H13’ and ‘VR3748’ intermediate, and E. grandis and E. camaldulensis the least suitable ones. Higher viability, adult longevity, and fecundity of G. platensis on E. urophylla indicate that species of Latoangulatae section can be suitable hosts for this insect. Nevertheless, the susceptibility of E. saligna, another species of the Latoangulatae, to G. platensis is low (Gonçalves et al., 2019). This suggests different susceptibilities among species within this section. However, E. grandis and E. camaldulensis were poor suitable hosts, and feeding on leaves of these species reduced survival, adult longevity and fecundity of this beetle. Eucalyptus urophylla is native to islands of the Indonesian archipelago and Timor (Hodge & Dvorak, 2015) and is not one of the native hosts of G. platensis in its native region, Tasmania (Australia) (Mapondera et al., 2012). This fact indicates possibilities of G. platensis to adapt to novel hosts as reported for Gonipterus sp. n.2 (Newete, Oberprieler & Byrne, 2011) and other insects. Paropsisterna bimaculata Olivier (Coleoptera: Chrysomelidae) become a pest of E. nitens (Maidenaria section) after this host was introduced in Tasmania. In the past, the insect was thought to be host-specific for species of the subgenus Eucalyptus (de Little & Madden, 1976; Paine, Steinbauer & Lawson, 2011). The oviposition site selection by P. bimaculata females depends on host morphological characteristics because the insect holds the leaf edge while ovipositing and plant kairomones seem to be of low importance (Howlett & Clarke, 2003). On the other hand, Anoplognathus montanus Macleay and A. pallidicollis Blanchard (Coleoptera: Scarabaeidae) that are considered host specific to eucalyptus, can also feed on Schinus molle L. (Anacardiaceae), an exotic plant from South America. This unusual feeding behavior was explained by the presence of similar monoterpenes in both host plants (Steinbauer & Wanjura, 2002).

The shorter larval stage duration on E. urophylla than on other species, possibly, because it has better nutritional value for the larval development of G. platensis. Similarly, E. globulus foliage (Maidenaria section) is considered one the most preferred host to G. platensis in Spain, with a shorter duration of the larval stage (22.1 days) than other species (Cordero-Rivera & Santolamazza-Carbone, 2000; Santolamazza-Carbone, Rodríguez-Illamamola & Cordero Rivera, 2006; Gonçalves et al., 2019). The intermediate larval stage duration of G. platensis on the hybrids HGU ‘H13’ (20.8 ± 0.4 days) and ‘VR3748’ (21.3  ± 0.3 days) is similar to that of this insect on E. globulus (Santolamazza-Carbone, Rodríguez-Illamamola & Cordero Rivera, 2006). The low larval stage viability on E. grandis indicates that this species is inadequate for G. platensis larval development.

The shorter pupal period on E. urophylla indicates the quality of this Eucalyptus species for G. platensis. Higher survival and shorter development period indicate better host quality, as the development duration is extended in inadequate hosts to increase the food intake, especially when the nutrient balance becomes sub-optimal (Chapman, 2013; Bawin et al., 2016). In that case, E. urophylla has both parameters, but a short development period and lower survival of the pupal stage of this insect were found on E. camaldulensis. The higher pupal viability with E. urophylla, HGU ‘H13’ and ‘VR3748’ indicates again the quality of E. urophylla (also presented in the HGUs) for G. platensis development and its mortality in the pupal stage reflecting the conditions to which its larva was exposed (Nestel et al., 2016), with poorer diets increasing pupa mortality (Mohammadzadeh & Izadi, 2018). The lower pupa viability of G. platensis on E. camaldulensis may be due to chemical and/or morphological differences of leaves between Eucalyptus genotypes such as secondary compounds, leaf waxes, nitrogen levels, and tannins (Ohmart & Edwards, 1991; Gherlenda et al., 2016) affecting insect development. Eucalyptus camaldulensis was also inadequate to Gonipterus pulverulentus Lea with lower food conversion efficiency and larval weight among the evaluated hosts, indicating worse larval fitness (Riquelme Virgala et al., 2018).

The shorter larva to adult period and higher survival rates on E. urophylla indicate that this species is a suitable food source to G. platensis (Bawin et al., 2016). Chemical analysis to identify which compounds are responsible for suitable food sources need to be further investigated. In contrast, longer development period in inadequate host plants, as on E. grandis, can increase larval exposure to natural enemies and mortality of G. platensis in the field, according to the slow-growth high-mortality hypothesis (Clancy & Price, 1987; Uesugi, 2015). Variations in the development period of G. platensis among Eucalyptus host species and hybrids suggest an effect of the food quality, as generally reported for insect herbivores (Behmer, 2009). This development period reflects nutritional, morphological, chemical composition, and plant-defence differences between host plants (Paine, Steinbauer & Lawson, 2011; Malishev & Sanson, 2015; Oates et al., 2015; Santadino et al., 2017).

The oviposition period was similar between E. urophylla and HGUs hybrids, the only hosts with oviposition by G. platensis. The higher numbers of egg capsules/female on the ‘VR3748’ and E. urophylla are related to host choice with herbivorous insects choosing those with better conditions for survival and development of their progeny (Gripenberg et al., 2010). The number of egg capsules of Gonipterus sp. n.2 was also high on E. urophylla in South Africa (Newete, Oberprieler & Byrne, 2011). This species laid eggs on E. grandis and E. camaldulensis (Newete, Oberprieler & Byrne, 2011) whereas G. platensis did not, showing different oviposition preferences between these two Gonipterus species. The emission of volatile organic compounds, such as green leaf volatiles and terpenes may influence host plant selection by G. platensis (Bouwer et al., 2014; Branco et al., 2019). The terpenoid 1,8-cineole is probably responsible for the attractiveness and its metabolization by G. platensis results in the production of hydroxylated derivatives that are likely to act as sex pheromones for this beetle (Branco et al., 2020). This terpenoid is highly abundant in the leaf oil composition of Maidenaria species susceptible to G. platensis, like E. dunnii (43.67%), E. globulus (69.10%), E. nitens (47.9%), and E. viminalis (63.73%) and with a low percentage in Latoangulatae species with low damage by G. platensis like E. grandis (0.45%), and E. saligna (0.11%) (Boland, Brophy & House, 1991; Batista-Pereira et al., 2006). The high percentage of 1,8-cineole (53.11%) in the E. urophylla (Latoangulatae section) (Batista-Pereira et al., 2006), makes this species attractive to G. platensis, similar to Maidenaria species.

The unsuitability of E. camaldulensis and E. grandis to G. platensis, compared to the longer pre-oviposition period, lower number of egg capsules/female, and egg viability with the hybrid ‘H13’ indicate the potential of those species for planting as a management strategy for this pest. These plant materials can be used in separate stands on most of the available area or in mixed ones in mosaic or using E. grandis as a barrier in a mosaic landscape (Forrester, Bauhus & Khanna, 2004; Martins et al., 2014).

Conclusions

The shortest egg-to-adult development period, greatest longevity, reproduction, and viability of E. urophylla indicate the suitability of this plant for G. platensis. The intermediate values of the evaluated parameters for G. platensis that fed on the HGU ‘VR3748’ and ‘H13’ indicate that these plants are also appropriate to this pest. The egg-to-adult development period was shorter and the larval stage viability high for G. platensis on E. camaldulensis, but the low larva to adult viability and reproduction impaired the establishment of G. platensis on E. camaldulensis. The longest period and the lowest viability of the larval stage and reproduction of G. platensis on E. grandis indicated this is the least suitable host tested for this insect.

The insect performance method utilized to assess the suitability of Eucalyptus genotypes to G. platensis, allowed to evaluate how host quality affects the survival, development, and reproduction of this insect, and can be replicated for other pest species of economic importance.

The information can be used to manage G. platensis, by avoiding extensive plantations with susceptible species, and reducing the risks of population outbreaks in commercial plantations.

Supplemental Information