Habitat complexity and mite population on Caryocar brasiliense trees

The objective was to study the habitat complexity of mite populations on Caryocar brasiliense trees under natural and cultivated field conditions. The study was performed in the municipality of Montes Claros, in the state of Minas Gerais, Brazil, over 3 years. Three types of areas were studied: 1) Cerrado, 2) pasture, and 3) a university Campus. Several chlorotic spots were detected on leaves with larger populations of Tetranychus sp. and Eutetranychus sp. (Tetranychidae). The greatest numbers of Agistemus sp. (Stigmaeidae) on leaves and Histiostoma sp. (Histiostomidae) and Proctolaelaps sp. (Ascidae) on fruits were observed in the pasture, and that of Histiostoma sp. on leaves in the pasture and on the university Campus. In general, the herbivorous mites (e.g., Tetranychus sp.) found on C. brasiliense plants were correlated with more clayey soils with a higher cationic exchange capacity; larger populations of mites (e.g., Agistemus sp. and Histiostoma sp.) were found on the C. brasiliense trees with the largest crown sizes; and associations between predator mites (e.g., Agistemus sp.) and phytophagous mites (e.g., Tetranychus sp.1) were observed. Greater habitat diversity and more complex plant architectures favored the mite populations. The positive effect of loamier soil on herbivorous mites indicates that these species are adapted to Cerrado conditions. Some recorded species of herbivorous mites can be pests in commercial plantations of C. brasiliense.


Introduction
The Cerrado occupies approximately 2 million km 2 of the Brazilian territory, in which Caryocar brasiliense Camb. (Malpighiales: Caryocaraceae) trees are widely distributed (Pinheiro & Monteiro, 2010;Santos et al., 2018). The fruits of this tree are used as food and lubricants and are employed in the pharmaceutical industry and the production of cosmetics (Moura, Chaves, & Naves, 2013). Caryocar brasiliense flowers are important as food for Agouti paca (L.) (Rodentia: Agoutidae) and Mazamagoua zoupira (G. Fischer) (Artiodactyla: Cervidae) and the flowers of this plant are pollinated by bats, bees, and moths, and its fruits dispersed by Didelphisal biventris (Lund) (Mammalia: Marsupialia) and Cyanocorax cristatellus (Temminck) (Passeriformes: Corvidae) (Oliveira, 1997;Almeida, Proença, Sano, & Ribeiro, 1998;Macedo & Veloso, 2002). Caryocar brasiliense trees are protected by federal law and left isolated in deforested areas of the Cerrado. This situation increases leaf and fruit damage by mites. Despite the biological and social importance of C. brasiliense, its associated mite species are unknown.
The diversity and abundance of mites can vary between environments. This has been attributed to the fact that the numbers of herbivorous mite species (e.g., species richness) and their predators associated with a host plant are generally lower (e.g., abundances) in more complex environments (1) (Eichelberger, Johann, Majolo, & Ferla, 2011), while soil characteristics that are more favorable to trees increase phytophagous mite numbers (e.g., nutritional quality) (2) (Carvalho et al., 2013;Chacon-Hernandez et al., 2018).
The objective here was to study mites on C. brasiliense trees and the effect of more complex environments and soil characteristics on the diversity and abundance of phytophagous mites and their predators under three
The study design was completely randomized with 10 replications (10 trees) and three treatments (areas) with the goal of testing the effect of environment complexity. The hypothesis regarding soil characteristics was tested considering each tree evaluated as a replication (30 trees and replications). We walked (~600 m) in straight lines in each area, and every 50 m, one randomly selected adult C. brasiliense tree (producing fruits) was sampled per collection time, except on the lawn of the university Campus, where the same trees were evaluated every time. Four expanded leaves, four flowers (Aug.-Sep.), and four fruits (Oct.-Jan.) from each stratum of the canopy (bottom, medium, and apical part) and from each cardinal orientation of the branches (North, South, West, and East) were collected from 30 trees monthly (in the morning) during each of the three years. These plant materials were placed in transparent white plastic bags, which were sealed and transported to the laboratory, where the numbers of the nymphs and adults (sum) of mites (phytophagous and predators) were counted. The counting started within 2 h after material collection on average and was performed by examining the leaves and flowers under a binocular microscope with 12.5X magnification, while the mites on the fruits were directly counted (without using a lens). The mites were counted in three fields located in the central area (equidistant between the principal vein and the margin) of each leaf (abaxial and adaxial surface) and randomly distributed on the flowers. The mites present on each whole fruit were counted. The mites on C. brasiliense leaves, flowers, and fruits were collected with a brush and preserved in vials with 70% alcohol for identification by Dr. A.L. Matioli (several families) and Dr. Eddie A. Ueckermann (Agistemus).
The correlations of the numbers of individuals of each predator species with each herbivorous mite species, the chemical characteristics of the soils and plant height and crown size (see Leite et al., 2006;same areas) were subjected to principal component regression (PCR) (p < 0.05). The applied regression model uses principal component analysis based on the covariance matrix to perform regression. Thus, it can exclude the dimensions that contribute to multicollinearity problems (e.g., the linear relationships between independent variables) to reduce the regression dimensions. The parameters used in these regressions were those that were considered significant (p < 0.05) after selection via the ''stepwise'' method. The effects of the three different areas and the host plant attributes on the number of individuals of each species of herbivorous mite and their predators were subjected to √x + 0.5 transformation and tested with ANOVA (p < 0.05) and Tukey's test (p < 0.05).

Results and discussion
The populations of Tetranychus sp.1 and sp.2 and Eutetranychus (Tetranychidae) were larger on C. brasiliense leaves with chlorotic spots, and they probably reduced photosynthetic leaf area, particularly during the dry period; these mite genera are pests of other plants as well (e.g., rose and apple) (Silva et al., 2009;Carvalho et al., 2013;Hardman et al., 2013;Chacon-Hernandez et al., 2018). The abundance of Histiostoma sp. (Histiostomidae) was high, especially on fruits, but this may not pose a problem for C. brasiliense because these mites consume the tissue around the seeds without injuring the fruit skin (e.g., crack or groove) or reducing its size. Histiostoma sp. was associated with fruit peel decomposition, and its populations were large on the fruits stored in the lab with rotting skin (data not shown). Histiostoma polypori (Oud.) is necromenic with the earwig Forficula auricularia (De Geer) (Dermaptera: Forficulidae), H. piceae Scheucher is a phoretic mite associated with Ipstypographus L. (Curculionidae: Scolytinae), and H. polypori and H. feroniarum (Dufour)are phoretic mites associated with F. auricularia (Chmielewski, 2009;Takov, Pilarska, & Moser, 2009;Wirth, 2009).
The populations of predatory Agistemus sp. (Stigmaeidae) mites were largest on the C. brasiliense trees with the largest crown size (height x width) and greatest populations of predatory Proctolaelaps sp. (Ascidae) and Tetranychus sp.1 mites. However, the number of Agistemus sp. was lowest on the trees with the tallest or widest crowns, in soils with the highest percentage of loamier soil and the largest populations of Tetranychus sp.2, Acaridae, and Histiostoma sp. The greatest numbers of Acaridae, Tetranychus sp.2 and the predatory Agistemus sp. mites and the lowest number of Tetranychus sp.1 were associated with an increase in the population of predatory Proctolaelaps sp. mites on C. brasiliense trees, independent of the soil or tree crown characteristics. The number of Tetranychussp.1 was highest on C. brasiliense trees in soils with the highest pH and cationic exchange capacity and the lowest percentage of soil base saturation with the cationic exchange capacity at pH 7.0. The numbers of Tetranychus sp.2 and Acaridae mites were highest on C. brasiliense trees in the soils with the highest percentage of loamier soil and pH levels, respectively (Table 1). The correlations between the predatory (e.g., Agistemu ssp.) and phytophagous (e.g., Tetranychus sp.1) mites on C. brasiliense leaves were positive in the studied areas. Predatory mites are important for the biological control of herbivorous mites in native and cultivated areas (e.g., orange orchard), and an increase in their prey and floristic diversity maintain or increase their populations (Saber & Rasmy, 2010;Eichelberger et al., 2011). Competition was not observed among the herbivorous and predatory mites on C. brasiliense trees, but competition among predatory mites for free space (Hammen, Montserrat, Sabelis, Roos, & Janssen, 2012;Strodl & Schausberger, 2012) and among females of Tetranychus urticae (Koch) (Tetranychidae) (Macke et al., 2012) has been reported.
Mites were not found on C. brasiliense flowers. The number of Agistemus sp. mites was highest on leaves (F = 3.075, P = 0.0467, df = 6989), while the numbers of Histiostoma sp. (F = 10.170, P = 0.00000, df = 691) and Proctolaelaps sp. (F = 8.820, P = 0.00007, df = 691) were highest on fruits in the pasture, and the numbers of Histiostoma sp. (F = 5.556, P = 0.00390, df = 5282) were highest on leaves in the pasture and the university Campus. The abundance of Eutetranychus sp., Tetranychus sp.1 and sp.2, Proctolaelaps sp. and Acaridae was similar (p > 0.05) on leaves on C. brasiliense in the three areas (Table 2). The greater numbers of species of phytophagous mites and, consequently, their predators found on C. brasiliense trees in the pasture than in the Cerrado or in the university Campus may be explained by a combination of factors: the C. brasiliense trees in the pasture environment grew in the presence of grass and other trees and shrubs (see Leite et al., 2006;; the crowns of these trees were wider with more complex structures, and fruit production was higher in the pasture than in the other two areas (Leite et al., 2006); and the soil characteristics (e.g., loamier, higher aluminum levels and lower pH levels) in the pasture were more favorable to C. brasiliense trees (Leite et al., 2006), thereby indirectly favoring herbivorous mites and their predators. Both habitat complexity and host-plant attributes (e.g., architecture and nutritional quality) influence the diversity of herbivores and predatory mites (Silva et al., 2009). The number of species associated with a given host in a less complex environment may be lower, and the abundance of each species may generally be higher, increasing the likelihood that herbivores of economically valuable plants will become pests (Benaoun, Elbakkey, & Ferchichi, 2014;Pollier, Guillomo, Tricault, Plantegenest, & Bischoff, 2018). The wind currents may have influenced the larger mite populations (e.g., Agistemus sp. and Histiostoma sp.) found on the C. brasiliense trees with the largest crown sizes (pasture area) because the dispersion of these small arthropods, is probably strongly influenced by the wind (Kumar, Raghuraman, & Singh, 2015). A larger tree canopy could favor the migration of mites carried by the wind, as reported for winged termites on C. brasiliense (Leite et al., 2011). In addition, the supply of food available (leaves and fruits) to herbivorous mites and their predators is greater on larger trees. The herbivorous mites (e.g., Tetranychus sp.1 and sp.2) found on C. brasiliense plants were correlated with more clayey soils with a higher cationic exchange capacity. The damage caused by Tetranychus sp. on Lippia sidoides Charm (Verbenaceae) on seedlings was higher on plants that were not supplied with calcium and magnesium but were fertilized with nitrogen (Silva et al., 2009). Phosphorus and magnesium deficiency may block protein synthesis in plants, resulting in the accumulation of free amino acids and, thus, better nutrition available to mites (Silva et al., 2009). The presence of lepidopteran leaf miners and defoliation (%) on C. brasiliensis trees were positively and negatively correlated with the aluminum and pH levels of the soil, respectively (Leite et al., 2012 b). On the other hand, the mortality of C. brasiliense trees caused by Cossidae (Lepidoptera) and Phomopsis sp. fungi was higher in soils with lower aluminum and higher pH levels (Leite et al., 2012a).

Conclusion
Greater habitat diversity and more complex plant architectures increased the number of mite species. The positive effect of loamier soil on herbivorous mites indicates that these species are adapted to Cerrado conditions. Some of the recorded species of herbivorous mites can be pests in commercial plantations of C. brasiliense.