Coleoborers (Curculionidae: Scolytinae) in native and homogeneous systems of Brazil nut (Bertholletia excelsa bonpl.) in the Southern Amazon, Brazil

Brazil nut is one of the most important species of the Amazon due to its socioeconomic importance. Especially in homogeneous production systems, it may be susceptible to damage by wood-boring insects, as by the subfamily Scolytinae (Coleoptera: Curculionidae); thus, inadequate management conditions can cause economic damage. Therefore, the objective of the present work is to evaluate the occurrence of wood-boring insects (Curculionidae: Scolytinae) in native and homogeneous systems of Brazil nut in the Meridional Amazonian, Brazil. The study was conducted in three environments: Conserved Native Planting nut, Anthropized Native Planting nut and Homogeneous Planting nut. Twelve ethanol traps were installed in each environment during four sampling periods. The data were submitted to entomofaunistic analysis, Pearson’s correlation analysis and cluster analysis. A total of 2,243 individuals from 31 species were sampled, of which 23 were from the Anthropized Native Planting nut, 24 from the Homogeneous Planting nut and 26 from the Conserved Native Planting nut. In the faunistic analysis, we highlight the species Xyleborus affinis (Eichhoff, 1868), which was the most representative one in the three environments and a super-dominant species in all four sampling periods. There was a greater similarity between the Anthropized Native Planting nut and the Conserved Native Planting nut; these two environments showed dissimilarity with the Homogeneous Planting nut. Monitoring coleoborers in Brazil nut agroecosystems is fundamental for the establishment of integrated pest management strategies.


53
Considered one of the most important extractive species in the Amazon and 54 Brazil, Brazil nut (Bertholletia excelsa Bonpl.: Lecythidaceae) is part of the 55 socioeconomic support base of many traditional communities and has become a crop of 56 interest for commercial exploitation in homogeneous forest stands [1][2][3]. 57 Mainly because of deforestation, the decrease in Brazil nut trees in natural 58 areas compromises the sustainability of the extractive production chain. It is possible to 59 point to a tendency for declining extractive activity and, at the same time, the potential 60 for the rise of Brazil nut plantations, with greater technification, enhanced management 61 strategies and the use of sustainable agricultural practices [4,5]. In this way, the 62 development of silvicultural studies of Brazil nut as an alternative in the exploration of 63 forest and non-forest products is of paramount importance, aiming at the development 64 of effective management strategies [6]. 65 In forest systems, insects perform fundamental functions and interactions in 66 maintaining and regulating the conditions and resources of ecosystems. However, 67 insect-plant interactions in certain circumstances can compromise production in 68 agroecosystems, whether in direct or indirect damage, due to log boring, defoliation, 69 seed drilling in the field or in storage; they may also be vectors of several plant diseases. 70 Attacks of Hypothenemus hampei (Ferrari, 1867) have been verified in Brazil nut stands 71 in southeastern Pará, making this coleoborer a potential cause of damage in these 72 production systems [7]. In addition, Tribolium castaneum (Herbst, 1797), Rhyzopertha 73 dominica (Fabricius, 1792), Ephestia kuehniella (Zeller) and Plodia interpunctella 74 (Hübner) have great potential to cause damage to stored almonds [8][9][10][11][12]. 75 Forest massifs, characterised by homogeneous planting systems, become 76 susceptible to the development of insect-plant interactions harmful to crops, especially when considering the Amazon region, which has a rich biodiversity and potential for the 78 emergence of new interactions of this type [13]. The implementation of homogeneous 79 plantations can cause an increase in insects harmful to forest species, making it 80 necessary to conduct population studies of possible pests to outline strategies to reduce 81 negative impacts, especially in the Southern Amazon, where studies of wood-boring 82 insects are still scarce [14]. 83 Wood-boring insects, in particular those belonging to the subfamily 84 Scolytinae (Coleoptera: Curculionidae), form one of the most important groups of forest 85 pests [15], with more than 6,000 described species [16,17]. This group of insects has 86 great potential for damage by promoting the opening of galleries in the tree trunks 87 making them weak and stressed, in addition to allowing the infection of plant tissues by 88 fungi [18].

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To understand the events involving the occurrence of wood-boring insects, 90 one must primarily consider the proper identification of the insect [16]; thus, a 91 monitoring program becomes essential to assess population levels. In this context, the 92 objective of the present work is to evaluate the occurrence of wood-boring insects 93 (Scolytinae) in three different production systems of Brazil nut (Bertholletia excelsa 94 Bonpl.) in the Southern Amazon.

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Study area 97 The study was developed in three Brazil nut areas in the Southern Amazon, ha. Homogeneous Brazil Nut (Environment 2), located in Paranaíta, Mato Grosso, has a 103 total area of 28 ha, spaced 6 x 6 m, with an age of approximately 17 years. This system 104 presents a high level of densification, since there has been no thinning since its 105 implantation, which has promoted a greater overlap of crowns and increased shading.  The region's climate is classified as Aw, with bimodal precipitation and a 110 clear distinction between two seasons, a dry winter and a rainy season [19]. The annual 111 average temperature is 26ºC, with an annual precipitation between 2,800 and 3,100 mm, 112 concentrated between November and May.

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Sampling and identification of species 114 To monitor the occurrence of insects in the study areas, 36 ethanolic traps 115 (attractive alcohol 96º GL) were used, adapted from the Pet-Santa Maria model [20] and 116 installed at a height of 1.5 m. In each study area, 12 traps were established at three 117 sampling points, which were composed of a set of four traps arranged in the shape of a 118 cross and 40 m apart.

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Based on the characteristics of rainfall distribution in the Alta Floresta  analyses, the PAST statistical software was used [23].

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Over the four sampling periods, 2,243 individuals were collected, of which  Table 1 shows the entomofaunistic analysis of the species of Scolytinae 154 in the three different environments.

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In Environment 1, 10 species were considered dominant or super-dominant, 156 accounting for 43% of the species. Environment 2 was characterised by 11 dominant or 157 super-dominant species, equivalent to 45% of the total species. In Environment 3, there 158 were 10 dominant or super-dominant species, representing 38% of the total species.  Table 1. Entomofaunistic analysis of Scolytinae in the different environments analysed in the Southern Amazon.  The Venn diagram (Fig. 1) shows that 16 species were common among the three environments. Of the 31 species identified in this study, 9 were classified as ecological indicators, as they reached the maximum categories in all analysed indices, according to the entomofaunistic criteria [22]. Entomofaunistic analyses of these species in the three environments and in each sampling period allow inferring about the effects of environmental conditions on the population density of the Scolytinae and their categories of dominance, abundance, frequency and constancy, as shown in Tables 2-4. Table 2. Entomofaunistic analysis of the Scolytinae indicator species occurring in Environment 1 in four sampling periods in the Southern Amazon. PERÍODO  In Environment 1, there was variation in the behaviour of the indicator species over the four sampling periods (      In general, the correlation analysis between population fluctuation of species and climatic variables was not statistically significant, as shown in Table 5. In Environment 1, there was no significant correlation for any of the climatic variables analysed in relation to species abundance in the four sampling periods. The species Premnobius cavipennis showed a high negative correlation for the minimum temperature variable in Environments 2 and 3, which means that with decreasing temperatures, the number of individuals increased. Similarity analysis of the three environments and the diversity of the Scolytinae (Fig. 2) demonstrates the formation of a group of greater similarity between Environments 1 and 3 and their dissimilarity with Environment 2.  It is important to point out, as shown in the Venn Diagram (Fig 1), that in Environment 2, there were 16 species common to native environments, which corroborates that several species of Scolytinae found favourable conditions for their development in the homogeneous systems. The species that were restricted to some environments presented low frequency values in relation to the sampled totals and therefore were not classified, in the entomofaunistic analysis, as possible ecological indicators. Species with low population levels, categorised as non-dominant, infrequent, rare or dispersed, should be considered important in assessing the environment, since these species, under certain conditions of resource availability or interspecific relationships, can raise their fauna levels [28].
The majority of species collected in this study fall into the group of xylomycetophages, which are highly common in tropical environments, with the exception of the species Cnesinus dryografus, phloem borer, and Coccotrypes palmarum, seed pest.
The Shannon-Wiener Diversity Index was lower in Environment 1 (1.53), and for Environment 2 (1.75) and Environment 3 (1.71), the values were similar. In general, structurally more complex environments, which present greater dynamics of ecological niches, such as native systems, are characterised by greater diversity. However, it is noteworthy that it is not uncommon in studies of Scolytinae diversity to verify rates for homogeneous or intercropped areas, similar or even higher, to those calculated for native areas [24,27,29]. Scolytinae mainly act in the degradation of plant material that accumulates in environments, their diversity being related, among other environmental factors, to the amount of litter. Forested areas generally have a greater amount of material that can serve as a place of development, such as plant residues, broken trunks and branches, which provide conditions for the population growth of Scolytinae [30]. Thus, Environment 2, due to the high density of Brazil nut trees and the great availability and deposition of plant material, provided conditions for an expressive number of species and an abundance of Scolytinae individuals, which is also reflected in the value of the Shannon-Wiener index, which was similar to that of Environment 3. In addition, it is also possible to infer that the small difference found between the index values between these two environments may have been determined by equitability, which was slightly higher for Environment 2.
The equitability of Environment 2 (0.55) and considered as those that receive the impact of the environment and change it [33]; therefore, these species have significant importance for population monitoring, since they can cause the appearance or disappearance of other species.
The species Xyleborus affinis was classified as super-dominant in the three studied environments, with frequency values above 40% in relation to the total number of individuals in each environment. This species is xylomycetophagous and common in almost all types of forest environments; it can cause damage to the wood by boring or even staining woody fabrics, due to the presence of a symbiotic fungus [34]. Xyleborus affinis was also highly representative in studies evaluating wood-boring insects (Coleoptera) in savanna areas in southern Mato Grosso [29,35,36], although with lower frequency values than those found in this study.
The species Xyleborus ferrugineus was dominant in Environments 1 and 2. It is common in forest environments [34], and in addition to directly causing damage, it is also a vector of the pathogenic fungus Ceratocystis fimbriata [37].
The species classified as indicators allow characterising environments in which ecological changes occurred. In this sense, species of the genus Cryptocarenus are indicators of environments in a state of ecological disturbance [16]. The species Premnobius cavipennis has been reported in several studies in homogeneous forest systems and in altered forest remnants [14,26,29,38,39]. Xyleborus spinulosus was verified as a dominant species in homogeneous eucalyptus systems [29,31,39]. In general, the species of the genera Sampsonius have been recorded in altered native areas or forest stands, albeit at low frequencies.
The species X. affinis and X. ferrugineus, which were also classified as indicators, can be classified as generalist species given their wide distribution in different phytographic regions in Brazil, being common species in almost all forest environments in the typologies of Mato Grosso [34,40] and with records of economic damage in homogeneous production systems The climatic variables are directly related to the flight, reproduction and dispersion of these insects [34]; in addition, they influence the physiological conditions of the trees, making them more or less susceptible to interaction with broachers. Sampling with shorter intervals may allow a better understanding of environmental factors and the population dynamics of Scolytinae. In addition, it must be considered that several interactions also occur, given the existence of microclimate relationships produced in forest environments, as these can promote microclimates in divergence from the regional climate, where variables such as wind, temperature, humidity and rainfall can change due to composition and vegetation levels, as well as allowing the existence of distinct niches for several species [43].
In the present study, the non-significance of most of the analysed climatic variables may be related to the small variation of these over the months analysed. The population fluctuation of Scolytidae varies among seasons and is correlated with the life cycle, biological opportunity and other environmental factors [44]. Furthermore, monitoring the population fluctuation of Scolytinae throughout the year is essential for the construction of strategic bases for integrated pest management in production systems of Brazil nut.
Similar to the results found in this work, Rodriguez, Cognato and Righi [27], studying the diversity of Scolytinae in native forest areas as well as intercropped and homogeneous forest systems, found that the native forest environments were grouped in greater similarity, and these in dissimilarity in relation to each other to another grouping between homogeneous planting of rubber (Hevea brasiliensis Willd. ex A. Juss., Müll. Arg) and coffee cultivation (Coffea arabica L).

Conclusions
The three Brazil nut areas analysed, with their differences in vegetation structure, presented similar species richness. In addition, of the 31 identified species, 16 were common to the three environments. Environment 2 presented an expressive number of Scolytinae species, which demonstrates their effective association with the silvicultural conditions of the homogeneous production system.
The species Xyleborus affinis was the most representative in the three study environments and remained as a super-dominant species in all four sampled periods.

Xyleborus affinis, Cryptocarenus seriatus, Cryptocarenus diadematus and Premnobius
cavipennis represented 70% of the total of sampled individuals and should be considered as potential pest insects in production systems of Brazil nuts.
This shows that population monitoring of Scolytinae in Brazil nut production systems, especially homogeneous systems, is of fundamental importance for the construction of strategies for integrated pest management and the sustainability of these agroecosystems in the Amazon.