Introduction

The Cerrado is the second-largest biome in Brazil in terms of land area. Occupying 22% of the country's area, it covers ten states and the Federal District and is considered a global hotspot due to the high rates of endemism among its fauna and flora. This biome comprises 11 main ecoregions, which are divided more broadly into forests, savannas, and grasslands. The forests are further divided into riparian forests (Mata Ciliar), gallery forests (Mata de Galeria), and the Cerradao. The savannas are comprised of the Cerrado sensu stricto, the Cerrado park (Parque de Cerrado), palm groves (Palmeiral), and the Vereda, while the grasslands consist of the Campo Sujo, Campo Limpo, and Campo Rupestre. Accounting for additional subtypes, a total of 25 distinct ecoregions are recognized in the Cerrado (^{Ribeiro and Walter, 2008}).

The Cerrado has already lost about 50% of its original vegetation cover, with deforestation closely linked to the replacement of natural areas with areas of planted pasture, annual agriculture, and perennial agriculture (^{PPCerrado, 2018}). The resulting decrease in natural areas can lead to habitat destruction and the consequent extinction of fauna and flora species, as well as causing soil erosion, aquifer pollution, regional climate change, and biome fragmentation (^{Klink and Machado, 2005}).

In this regard, permanent preservation and legal reserve areas play a fundamental role in maintaining floral diversity and providing shelter and food for animal life. However, forest fragmentation can lead to the edge effects, which consist of abiotic and biotic changes that occur at the edges of fragmented forest ecosystems, where ecological interactions can be affected by increased exposure to hot and dry winds, reduced air and soil moisture, increased solar incidence, and modification of the species structure and composition (^{Aronson et al., 2011}).

Insects are considered bioindicators as they establish direct and indirect interactions with surrounding organisms and respond to human actions that affect environmental quality. Surveys of insect life, especially of indicator species, are thus important methods for assessing the negative impact of human activities, such as agricultural and forestry practices, on the ecosystem function (^{Oliveira et al., 2014}).

This study aims to carry out a survey of the arthropod fauna associated with the tree canopies at the edges of a remaining fragment of the Cerrado biome to evaluate the arthropod diversity, with a particular focus on potential biological indicators.

Material and methods

Collection of canopy arthropods

The canopy net methodology was used to verify the composition, density, and population fluctuation of arthropods found in the tree canopies. The net consisted of an aluminum ring measuring ~40 cm in diameter and a tapered 80 cm long cotton cloth bag with a rounded end with a handle.

The arthropod fauna was surveyed at the edge of the fragment, with trees located an average of 26.275 m from the coffee plantation. In the study area, 20 trees, of the same species or not, were randomly chosen along a linear distance of approximately 248 m, with each tree located approximately ~15 m from the others. After selecting the trees, the net bag was wrapped around a branch and shaken five times; the bag was positioned so as to include branches located in the four cardinal directions in relation to the sampled tree.

The material collected from each plant was placed in plastic bags with a capacity of 5 kg that were properly sealed and identified. The bags were then packaged so as not to damage the collected specimens. The samples were then taken to the Forest Entomology Laboratory at the Federal University of Uberlándia (UFU), Uberlándia, MG, where they were kept refrigerated at a temperature of ~ -6 °C until sorting.

Between August 2018 and July 2019, collections were performed every 30 days in the crowns of the 20 selected trees (Table 1) for a total of 240 samples throughout the sampling period. The collections were carried out in the morning between 9 a.m. and 12 p.m. Two editions of Árvores Brasileiras by Harri ^{Lorenzi (1992}; 1998) were used for the identification and information on forest species (Table 1).

Table 1 List of forest species sampled in the edge area and their respective botanical family, flowering season, and fruiting season. Juliana farm, Monte Carmelo, Minas Gerais, Brazil. 

Results and discussion

In the sampling period, 804 individuals belonging to the classes Arachnida and Insecta were collected and identified into 56 taxonomic groups at the following levels: subclass, order, suborder, superfamilies, families, and subfamilies (Table 2).

Table 2 Faunistic analysis of taxonomic groups of arthropods associated with the canopy of trees at the edge of a forest fragment in the Cerrado between August 2018 and July 2019. Juliana farm, Monte Carmelo, Minas Gerais, Brazil. 

*N., number of individuals. Frequency: if, infrequent; f, frequent; vf, very frequent. Abundance: r, rare; s, scarce; c, common; a, abundant; va, very abundant. Evenness: W, constant; Y, accessory; Z, accidental. Dominance: D, dominant; ND, non-dominant.** Predominant taxonomic groups.

The most common taxa collected in the area were the order Araneae (class Arachnida) and the families Asilidae (order Diptera), Tephritidae (order Diptera), and Formicidae (order Hymenoptera), all belonging to the class Insecta (Table 2).

The order Araneae is particularly diverse in Brazil compared to other countries. Brazil is home to the second-largest known number of arachnids, totaling approximately 49,235 species distributed in 128 families (^{World Spider Catalog, 2021}). In the Cerrado, 625 described species are currently known, of which 169 occur only in this biome (^{Oliveira et al., 2017}). Spiders are potential predators of pest insects (^{Riechert and Lockley, 1984}).

Diptera is one of the most diverse insect groups, representing the second most diverse order worldwide, with approximately 155,000 known species (^{Stork, 2018}). According to ^{Pape et al. (2009}), Tachinidae, Syrphidae, and Dolichopodidae are the dipteran families with the greatest numbers of species described in the Cerrado. Dipterans have a phytophagous or saprophagous habit and can be parasitoids, predators, or pollinators (^{Skevington and Dang, 2011}).

The family Asilidae, which belongs to the order Diptera, has a high level of species diversity and is considered one of the largest groups of flies (Oak et al., 2012). According to ^{Carvalho et al. (2012}), there are 101 genera distributed in 458 species in Brazil. Adult insects (flies) and larvae of this family are exclusively predators and, due to their great diversity, can be found in various environments, with a preference for dry and open areas (^{Cezar, 2017}).

The family Tephritidae, also belonging to the order Diptera, was also representative of the collections. This insect group is popularly known as fruit flies. According to ^{Orth et al. (1986}), these insects feed on fruit pulp and can thus pose risks to the fruit sector, causing economic damage to producers. In the present study, tephritids were found in ten of the sampled tree species. ^{Uchoa and Nicácio (2010}) verified frugivorous species of Tephritidae in Alibertia edulis (puruí) and Miconia albicans (canela de velho).

Another group of Insecta also classified as predominant is the Formicidae, belonging to the order Hymenoptera. According to the AntWeb (2020), ~27,771 species are currently described for this family worldwide, distributed into 502 genera. In Brazil, 1,528 species belonging to 115 genera are known (^{AntWeb, 2020}). Ants have been very important predators and herbivores for over 100 million years and continue to influence numerous other organisms and the ecological dynamics of forests (^{Brandao et al., 2009}). Plant species with extrafloral nectaries are common in the Cerrado biome, many of which have documented mutualistic interactions with ants (^{Belchior et al., 2016}).

The three species of trees with the greatest diversity arthropod taxa were Xylopia aromatica, where 50% (N = 28) of the observed taxa were found, followed by Clethra scabra with 46.4% (N = 26), and Qualea grandiflora with 39.2% (N = 22). Cassia leptophylla, Styrax ferrugineus, and Didymopanax macrocarpus had the lowest number of taxa, with 10.7% (N = 6) present on each species (Figure 1). There was a significant and positive correlation = 0.6084; p < 0.01) between the number of tephritids and the maximum daily temperature (Table 3). Indeed, 85.7% of tephritids (N = 42) were collected on days with a maximum daily temperature between 30.1 °C and 32 °C. According to ^{Silveira Neto et al. (1976}), the optimum temperature for insects is around 25 °C, with minimum and maximum temperature thresholds of 15 °C and 38°C, respectively.

Figure 1 Number of arthropod taxa found in the canopy of trees at the edge of a forest fragment in the Cerrado between August 2018 and July 2019. Juliana farm, Monte Carmelo, Minas Gerais, Brazil. 

Table 3 Spearman's correlation (r _s ) between the number of arthropods associated with the canopy of edge trees and daily climate variables from August 2018 to July 2019. Juliana farm, Monte Carmelo, Minas Gerais, Brazil. 

Daily climate variables: average temperature (average T.), maximum temperature (maximum T.), minimum temperature (minimum T.), precipitation (PP), and relative humidity (RH). Spearman's correlation (rs): ** significant correlation (p < 0.01); ns non-significant correlation (p> 0.05).

No significant correlation was found between the other predominant groups (Table 3) and climate variables. Although there was no significant correlation with climate variables, the highest densities of individuals belonging to the order Araneae were observed during the region's cool and dry winter (Figure 2).

Figure 2 Population fluctuations of the predominant arthro-pod taxa found in the canopies of trees at the edge of a forest fragment in the Cerrado between August 2018 and July 2019. Juliana farm, Monte Carmelo, Minas Gerais, Brazil. Climate variables: average temperature (average T.), relative humidity (RH), and precipitation (PP). 

The order Araneae, along with the family Formicidae (Hymenoptera), are known to include potential predatory species; both families were found in all sampled tree species (Table 4). The order Araneae can assist in the natural biological control of insects since it includes predatory species (^{Riechert and Lockley, 1984}). The same applies to the Formicidae family, in which the following guilds are found: predatory generalist epigeic and hypogeic species, predatory Dacetini species, and arboreal predatory species (^{Brandao et al., 2009}), which can also assist in biological control of insects.

Table 4 shows other taxa that can perform control through interspecific ecological relationships of predation or parasitism.

Table 4 Classification of arthropod taxa as potential biological control agents (parasitoids and predators). Species found in the canopy of trees at the edges of a forest fragment in the Cerrado between August 2018 and July 2019. Juliana farm, Monte Carmelo, Minas Gerais, Brazil. 

* Classification of insect families with parasitoid species based on ^{Parra et al. (2011}) and with predator species based on ^{Torres and Silva-Torres (2011}). Spider classification was carried out following ^{Riechert and Lockley (1984}). ** Tree species: AE - Alibertia edulis; AT - Aspidosperma tomentosum; CB ― Caryocar brasiliense; CL ― Cassia leptophylla; CS - Clethra scabra; DM - Didymopanax macrocarpus; ER ― Erythroxylum sp.; ED - Eugenia dysenterica; HE - Heteropterys sp.; MA - Miconia albicans; QG - Qualea grandiflora; SF -Styrax ferrugineus; XA - Xylopia aromatica.

The same tree species that stood out for the total number of arthropod taxa they contained (Figure 1) also contained the highest number of potential biological control agents (Table 4). The largest number of such taxa were identified for X. aromatica (N = 14), followed by Q. grandiflora (N = 12) and Clethra scabra (N = 11) (Table 4).

Xylopia aromatica (Annonaceae) is commonly known in Brazil as pindaíba or pimenta-de-macaco. The species is characterized as semi-deciduous, heliophyte, and selective xerophyte (^{Lorenzi, 1992}). It is an ornamental plant, and its wood is light and of low durability. Xylopia aromatica occurs in several Brazilian states along the Cerrado and is more common in the Cerrado sensu stricto and Cerradao ecoregions (^{Marimon-Junior and Haridasan, 2005}).

Qualea grandiflora (Vochysiaceae) is popularly known in Brazil as pau-terra. It occurs in the Cerrado Mineiro and in fragments of the states of Amazonas, Sao Paulo, Goiás, and Mato Grosso do Sul (^{Lorenzi, 1992}). According to Lorenzi (1992), it is a deciduous, heliophyte plant and can be used in land restoration, reforestation, and landscaping. Its wood can also be used for several purposes.

Clethra scabra (Clethraceae), popularly known in Brazil as vassourao, occurs in the states from Rio de Janeiro to Santa Catarina, as well as Minas Gerais. It is a semi-deciduous, heliophyte, selective xerophyte, and a pioneer plant. It can be used for reforestation and restoration, and its wood is recommended for box work and charcoal (^{Lorenzi, 1998}).

The study area contained a high diversity of tree species, which stood out for the diversity of taxonomic groups of arthropods found in their crowns. Moreover, they offer a variety of economic products, allowing the owner to sustainably use products such as seeds and fruits under the current legislation for legal reserves of this kind. Such areas can therefore contribute to the generation of extra income for rural producers and serve as survival sites for a diversity of arthropod groups that provide important ecosystem services, such as potential natural enemies of pest insects (^{Skorupa, 2003}).

Conclusions

Legal reserves and fragments of the Cerrado biome contribute to the conservation of the arthropod fauna associated with tree species, especially the order Araneae and the families Asilidae and Tephritidae (Diptera) and Formicidae (Hymenoptera). Maintaining such areas is therefore of particular importance for the local ecology.

Of the tree species in the area, X. aromatica, C. scabra, and Q. grandiflora had the greatest potential as survival sites for natural enemies and other canopy arthropods in fragments of the Cerrado biome.