First record of Thaumastocoris peregrinus (Hemiptera, Thaumastocoridae) in Pará state, Brazil

Thaumastocoris peregrinus (Hemiptera, Thaumastocoridae) is a phytophagous pest of eucalyptus plantations. It was introduced in Brazil in 2008, and expanded rapidly due to its adaptive capacity to different climatic conditions. Eucalyptus has been planted in the Brazilian Amazon since the 1980s, being used in silvopastoral systems and for cellulose production. Since its introduction in the southernmost Brazilian state of Rio Grande do Sul, T. peregrinus has expanded its geographical distribution to 117 municipalities in states in the south (Rio Grande do Sul, Santa Catarina and Paraná), southeast (São Paulo, Espirito Santo, Rio de Janeiro and Minas Gerais), mid-west (Mato Grosso do Sul and Goiás) and northeast (Sergipe) of the country. Here we report the first record of T. peregrinus in the Brazilian Amazonian state of Pará.

Thaumastocoris peregrinus feeds on eucalyptus by making small incisions on the leaves (Lorencetti et al. 2015;Cipriani et al. 2015). The adult insect is 3-4 mm long with a brown flattened body that varies according to the development phase (Jacobs and Nesser 2005;Lorencetti et al. 2015;Lunz and Azevedo 2016). Females of T. peregrinus lay an average of 60 black eggs on eucalyptus leaves. The development involves five nymph instars (Jacobs and Nesser 2005) and an approximate 60-day life cycle that can vary with climate conditions (Penteado et al. 2014). Generations overlap along the year, so that great numbers of nymphs and adults can occur simultaneously (Noack and Rose 2007).
Originated from Australia, T. peregrinus was first recorded in South America in November 2005, in the north of Buenos Aires, Argentina (Noack and Coviella 2006), and later in Uruguay, in January 2008 (Martínez and Bianchi 2010). In Brazil, the species was first recorded in early 2008, in the municipality of São Francisco de Assis, in the southern state VOL. 49 (3)   .
The insect rapidly dispersed over eucalyptus plantations throughout Brazil (Figure 1) due to its adaptive capacity, since it can survive under different climate conditions (Pereira et al. 2013). Other favorable aspects for the rapid dispersion of T. peregrinus were the transport of infested vegetal material of eucalyptus across producing regions  and fragile phytosanitary barriers among producing states (Lunz and Azevedo 2016).
In the southeastern region of the state of Pará, in the eastern Brazilian Amazon, soil and climatic conditions are favorable to the development of eucalyptus plantations (Filgueiras et al. 2011). Today, Pará is the 10 th Brazilian state in area planted with eucalyptus, with almost 134,000 ha, being mainly used to supply the energy and cellulose markets (IBA 2017). Reports on the occurrence of new dangerous biotic agents in these plantations are scarce, which is likely due to the lack of periodic monitoring by plantation owners.
Here we provide information on the occurrence of T. peregrinus in eucalyptus plantations from Pará state, extending the geographic distribution of this pest in Brazil. Sampling was carried out in 2015 and 2016, in areas of commercial plantations of Eucalyptus spp. in southeastern Pará, in the municipalities of Paragominas (03°20'07.08"S, 47°11'21.54"W), Ulianópolis (03°58'26.50"S, 47°33'01.96"W), Dom Eliseu (04°30'02.73"S, 47°49'31.50"W) and Rondon do Pará (04°36'32.91"S, 47°57'18.51"W) (Figure 1). The climate type is Awi, according to the Köppen classification. Yellow sticky traps (ISCA Technologies, Brazil) were used in 32 georeferenced points. Traps were placed in the interior of the plantations, at least 100 m from the border. Each trap was located between two trees at 1.60 m from the soil. Traps were replaced monthly. Retrieved traps were analyzed at an entomology laboratory at Universidade Federal Rural da Amazônia, in Belém (Pará state, Brazil) under a stereoscopic microscope QM Q7714Z. Specimens of T. peregrinus were identified through the use of taxonomic keys by  Table 1 for first records in other states). The municipalities in Pará state where the species was first recorded (this study) are indicated in yellow. States in which the species has been reported, but no voucher-based records exist to date, are indicated in pink. This figure is in color in the electronic version ACTA AMAZONICA Carpintero and Dellapé (2006) and Wilcken et al. (2010). Voucher specimens of the collections were deposited in the entomological collection of Embrapa Amazônia Oriental in Belém, Pará, Brazil, under number 2444. Quantitative data of these samplings will be analyzed elsewhere.
A total of 1,358 individuals were collected, 438 (32.2%) in 2015 and 920 (67.8%) in 2016, in all four municipalities sampled. Thaumastocoris peregrinus occurred in clones of E. camaldulensis, E. urophylla, E. grandis, and in hybrid clones of E. camaldulensis. Nymphs and eggs were also observed in neighbor trees around the traps, but these trees showed no sign of serious damage.
Many eucalyptus species are attacked by T. peregrinus, especially E. camaldulensis and the hybrid E. urograndis (Queiroz 2009). Moreover, E. camaldulensis is considered as the most susceptible eucalyptus species to insect pests (Wilcken 2008). Thaumastocoris peregrinus also attacks E. tereticornis and the hybrid of E. camaldulensis x E. grandis (Jacobs and Nesser 2005). Eucalyptus urophylla and E. grandis were also very susceptible to T. peregrinus attacks (Soliman et al. 2012).
Increases in plantation areas normally result in increases in insect species that adapt themselves to the crops (Costa and Araldi 2014). Exotic insect pests in forest plantations can be a threat to forest productivity due to the economic losses coming from plantation damages caused by these insects (Garlet et al. 2016). There is scarce information regarding the efficient management of T. peregrinus.
Probably the T. peregrinus invasion in Pará started from eucalyptus plantations in the neighboring state of Maranhão, where the presence of T. peregrinus has been reported in newsfeeds (SAGRIMA 2014), although no voucher-based record exists yet of the occurrence of the species in this state. Eucalyptus has been cultivated in Pará for more than 30 years without adequate insect pest monitoring by plantation owners. Based on the pest's first records in the mid-western state of Goiás (Table 1) it is reasonable to estimate that T. peregrinus is in Pará since 2013. Furthermore, T. peregrinus can also be present in eucalyptus plantations in Bahia, Piauí, Maranhão and Tocantins (Figure 1), although there are no scientific records of its occurrence published for these states.
Our findings highlight the importance of using periodic and systematic monitoring methods to determine pest infestation levels and population dynamics in eucalyptus commercial plantations, and which eucalyptus species are more susceptible to pests. Systematic studies also help to identify possible native natural enemies of pest species that could favor the use of ecological pest management.
Since its first occurrence, and including the records we present in here, T. peregrinus has now been recorded in 117 Brazilian municipalities, and in 11 federal states (Table 1)