Arthropod communities associated with Acacia auriculiformis saplings during degraded area restorationAbstract
Acacia auriculiformis (Fabaceae) is a fast-growing, hardy pioneer species with nitrifying potential, commonly used in the recovery of degraded areas. This study evaluated plant growth traits in A. auriculiformis saplings, vegetation cover, the associated insect and spider communities, their ecological indices (abundance, diversity, and species richness), and their interactions during a 24-month restoration period. The number of leaves/branch, branches/sapling, and ground cover were higher in A. auriculiformis saplings in the second year. During the first year, greater species richness and abundance of sap-sucking Hemiptera, phytophagous Coleoptera, and phytophagous Orthoptera were observed on A. auriculiformis leaves, along with increased spider abundance, higher numbers of the tending ants Pheidole sp. and Pseudomyrmex termitarius (Hymenoptera: Formicidae), and a greater presence of Cycloneda sanguinea (Coleoptera: Coccinellidae). Saplings with more leaves/branch hosted higher numbers of Brachymyrmex sp. and Camponotus sp. (Hymenoptera: Formicidae), along with an increased abundance of tending ants. The higher number of Bemisia sp. was positively associated with that of Pheidole sp., and vice versa, and the higher number of Aethalium reticulatum (Hemiptera: Aethalionidae) was positively correlated with that of P. termitarius. Conversely, greater numbers of Pheidole sp. and P. termitarius reduced Phaneropterinae and Salticidae numbers, respectively. Increased species richness of tending ants negatively affected those of Orthoptera and their abundance, while higher species richness of spiders reduced that of Coleoptera. The expansion of ground cover with sapling age highlights the importance of A. auriculiformis in restoring degraded areas.
Keywords:
diversity; Formicidae; Hemiptera; spiders
Resumo
A Acacia auriculiformis (Fabaceae) é uma espécie pioneira de crescimento rápido e resistente, com potencial nitrificante, comumente utilizada na restauração de áreas degradadas. Este estudo avaliou características de crescimento em mudas de A. auriculiformis, cobertura vegetal, comunidades de insetos e aranhas associadas, seus índices ecológicos (abundância, diversidade e riqueza de espécies), e suas interações ao longo de um período de restauração de 24 meses. O número de folhas/galho, galhos/muda e a cobertura do solo foram maiores em mudas de A. auriculiformis no segundo ano. Durante o primeiro ano, observou-se maior riqueza e abundância de espécies de Hemiptera sugadores de seiva, Coleoptera fitófagos e Orthoptera fitófagos nas folhas de A. auriculiformis, juntamente com maior abundância de aranhas, maior número de formigas cuidadoras Pheidole sp. e Pseudomyrmex termitarius (Hymenoptera: Formicidae) e maior presença de Cycloneda sanguinea (Coleoptera: Coccinellidae). Mudas com mais folhas por ramo apresentaram maior número de Brachymyrmex sp. e Camponotus sp. (Hymenoptera: Formicidae), juntamente com uma maior abundância de formigas cuidadoras. O maior número de Bemisia sp. foi positivamente associado com o de Pheidole sp. e vice-versa, e o maior número de Aethalium reticulatum (Hemiptera: Aethalionidae) foi positivamente correlacionado com o de P. termitarius. Por outro lado, maiores números de Pheidole sp. e P. termitarius reduziram os números de Phaneropterinae e Salticidae, respectivamente. O aumento da riqueza de espécies de formigas cuidadoras afetou negativamente a de Orthoptera e sua abundância, enquanto uma maior riqueza de espécies de aranhas reduziu a de Coleoptera. A expansão da cobertura do solo com a idade das mudas destaca a importância de A. auriculiformis na restauração de áreas degradadas.
Palavras-chave:
diversidade; Formicidae; Hemiptera; aranhas
1. Introduction
Human activities, particularly agriculture, degrade natural ecosystems to sustain population and economic growth (Demolin-Leite, 2025). Restoring these areas is a priority, but remains time-consuming (Amaral et al., 2013; Reis et al., 2015; Demolin-Leite, 2025). Fabaceae species are widely used in restoration efforts, and Acacia auriculiformis stands out due to its rapid growth, hardiness, adaptability to acidic and infertile soils, and nitrifying capacity (Wang et al., 2013; Dourado et al., 2020). Its high nitrogen fixation rate, facilitated by symbiosis with diazotrophic bacteria, enhances biomass production and nutrient cycling via litter, promoting plant succession (Wang et al., 2013). However, insects such as Aethalion reticulatum (Hemiptera: Aethalionidae), Aleyrodidae (Hemiptera), Stereoma anchoralis (Coleoptera: Chrysomelidae), and Tettigoniidae (Orthoptera) can cause significant damage to this species (Demolin-Leite, 2024).
Arthropods serve as bioindicators of environmental change due to their rapid responses to ecological shifts (Beiroz et al., 2014; Prosser et al., 2016; Pereira et al., 2018). Their population dynamics (e.g., diversity) reflect alterations in ecosystem structure (e.g., reduced plant richness) (Pereira et al., 2018). Phytophagous insects and natural enemies exhibit variable reproduction, growth, and survival rates depending on fertilization, plant age, and leaf mass, which influence chemical and nutritional defenses (Bowers and Stamp, 1993; Oliveira et al., 2014). The biogeographical island theory (BGIs) predicts that extinction rates are higher on smaller islands because they cannot support large populations of organisms, making the rarest species vulnerable to extinction (Burns, 2016). The canopy of a tree is a small-scale biogeographic island. Larger plants may support higher arthropod abundance and diversity by functioning as BGIs, which reduce extinction risks for rarer species (Burns, 2016; Leite et al., 2017). However, interspecific competition among arthropods can occur through interference (e.g., aggression, chemical deterrence) or exploitative competition (e.g., resource depletion) (Bhuyain and Lim, 2019; Boulay et al., 2019). Mutualistic interactions, such as those between tending ants (e.g., Camponotus sp.) and Hemiptera (e.g., A. reticulatum), involve protection (e.g., natural enemies) in exchange for honeydew, a food rich in carbohydrates, glucose, fructose, and sucrose, and free amino acids, lipids, starch, minerals, and vitamin B (Zanuncio et al., 2015; Araujo et al., 2016).
The objectives of this study were to evaluate the production of plant biomass and litter in A. auriculiformis saplings, associated arthropod communities, and their ecological indices (abundance, diversity, and species richness), and their interactions over 24 months in a degraded area. Four hypotheses were tested: i) older A. auriculiformis saplings develop larger canopies and produce more litter, thereby enhancing the recovery of the degraded area; ii) arthropod numbers and associated ecological indices are higher on older saplings, due to their larger canopies (greater BGI); iii) the abundances of tending ants and predators are directly proportional to those of sap-sucking Hemiptera and their prey, respectively; and iv) higher abundance of tending ants reduces the abundance of both predators and chewing insects.
2. Material and Methods
2.1. Experimental site
The study was conducted in a degraded area at the “Instituto de Ciências Agrárias da Universidade Federal de Minas Gerais (ICA/UFMG)” in Montes Claros, Minas Gerais State, Brazil (16º 51’ 38” S, 44º 55’ 00” W, 620 m.a.l.s.) from April 2020 to March 2022. The region has a tropical dry climate (Köppen classification), characterized by annual precipitation of 1000–1300 mm, distinct dry winters, and mean annual temperatures ≥ 26°C. Soil is classified as Litholic Neosol with an Alic horizon.
2.2. Experimental design
In March 2019, 24 A. auriculiformis seedlings were prepared in a nursery using 16 × 24 cm plastic bags containing a substrate amended with 160 g of reactive natural phosphate. Saplings (30 cm height at transplantation) were planted in September 2019 in 40 × 40 × 40 cm pits spaced two m apart. Soil amendments included dolomitic limestone (to raise base saturation to 50%), natural phosphate, gypsum, FTE (Fritted Trace Elements), potassium chloride, and micronutrients, as per soil analysis recommendations. Each sapling received 20 L of dehydrated sewage sludge [single application; biochemical composition detailed in Silva et al. (2020)]. Irrigation was performed twice weekly until the onset of rain (October). The completely randomized design comprised 24 replicates (one sapling each), and comparisons were made between the first and second year after planting.
2.3. Production of vegetal mass and ground cover
The number of leaves/branch and branches/sapling, and the percentage of ground cover by litter, herbaceous, and grassy plants were evaluated visually and monthly per plot (one m2) in the crown projection of each one of the 24 A. auriculiformis saplings.
2.4. Counting the arthropods
Arthropods (insects and spiders) were quantified biweekly between seven and eleven hours AM via direct visual observation of the first twelve expanded leaves (both leaf faces) and trunk per sapling. Leaves were randomly selected across vertical (basal: 0–33%; middle: 34–66%; apical: 67–100% of height) and horizontal (N, S, E, W) canopy axes (one leaf per position). Over 24 months, 13,824 leaves were evaluated (twelve leaves × 24 saplings × 48 sampling events). The adaxial surface was assessed first; the abaxial surface was examined by gently lifting leaves when necessary. Mobile taxa (e.g., Orthoptera) were recorded if identifiable to order before escaping. Arthropods remained in situ (not collected) during counts. For taxonomic identification, ≤ three specimens per species were aspirated weekly (two h sessions) during the establishment phase (transplantation to first evaluation), preserved in 70% ethanol, sorted to morphospecies, and verified by specialists (see Acknowledgments). New morphospecies encountered in subsequent samplings were similarly processed.
2.5. Statistical analysis
Each replication is the total of individuals collected on twelve leaves (three heights and four sides of the sapling) per sapling. The ecological indices (abundance, diversity, and species richness) were calculated per functional group (e.g., chewing insects) and treatments (first and second year after planting) using the Biodiversity software. Abundance and species richness were the total individuals and species per sapling, respectively. Diversity was calculated using Hill's N1= exp (Shannon–Weaver H’).
The data for abundance, diversity, and species richness of groups (e.g., spiders) were subjected to a non-parametric statistical hypothesis, the Wilcoxon signed rank test (p-value< 0.05) using the Statistics and Genetics Analysis (SAEG) program, version 9.1 (Supplier: “Universidade Federal de Viçosa”, Brazil). The data were subjected to second-degree regression or principal component regression (PCR), when linear (p-value< 0.05) to verify the possible interactions (e.g., protocooperation) between groups of arthropods (e.g., tending ants). All arthropods sampled were included in the analyses.
Simple equations were selected based on the criteria: i) distribution of the data in the figures (linear or quadratic response), ii) the parameters used in these regressions were the most significant ones (p-value < 0.05), iii) p-value < 0.05 and F of the Analysis of Variance of these regressions, and iv) the determination coefficient of these equations (R2). The PCR model uses principal component analysis to obtain the regression based on a covariance matrix. These reduce the regression dimensions, excluding those that contribute to collinearity, that is, linear relations between the independent variables. The parameters used in these equations were all significant (p-value <0.05) according to the selection of the variables by the “Stepwise” method using the statistical program mentioned. The data presented are the significant ones (p-value <0.05) (Tables 1-3), and the others are in supplementary material I (after references).
Abundance (Abun.), Diversity (D.), and species richness (S.R) of phytophagous Coleoptera (Col.), phytophagous Hemiptera (Hem.), phytophagous Orthoptera (Ort.), pollinators (Pol.) tending ants (Ants), Sternorrhyncha predators (Pred.), spiders (Spid.), number of branches/sapling and leaves/branch, percentages of ground cover and defoliation by insects per Acacia auriculiformis (Fabaceae) saplings (mean ± SE) and planting year.
Order, family, and species of spiders (Class Arachnidae) and insects (Class Insecta) per Acacia auriculiformis (Fabaceae) sapling (mean ± SE) and planting year.
Relationships between abundance (Abun.), diversity (D.), species richness (S.R.), and number of tending ants (Ants), Aethalium reticulatum (A.ret.), Apis mellifera (A.mel.), Balclutha hebe (B.heb.), Bemisia sp. (Bem.), Brachymyrmex sp.(Brac.), Camponotus sp. (Camp.), Cerotoma sp. (Cer.), Diabrotica speciosa (D.spec.), Lepidoptera (Lep.), Oxyopidae (Oxyo.), Pheidole sp. (Phei.), phytophagous Coleoptera (Col.), phytophagous Hemiptera (Hem.), phytophagous Orthoptera (Ort.), Pseudomyrmex termitarius (P.term.), Salticidae (Salt.), spiders (Spid.), Stereoma anchoralis (S.anch.), Tetragonista angustula (T.ang.), Phaneropterinae (Phan.), leaves/branch (Leaves) and branches/sapling (Branches), and percentage of defoliation (Def.) on Acacia auriculiformis (Fabaceae) saplings.
3. Results
3.1. Plant biomass production
The number of leaves/branch, branches/sapling, and ground cover (litter, herbaceous plants, and grasses) were higher in A. auriculiformis saplings in the second year (Table 1).
3.2. Arthropods and their ecological indices
During the first year after planting, a higher number of sap-sucking hemipterans- Bemisia sp. (Aleyrodidae), Balclutha hebe (Cicadellidae), and Membracidae (Hemiptera)- were observed, along with greater abundance and species richness in this group. Similarly, defoliating coleopterans-Cerotoma sp., Diabrotica speciosa, and S. anchoralis (Coleoptera: Chrysomelidae) numbers- exhibited higher abundance and species richness, as did orthopterans- Tropidacris collaris (Romaleidae) and Phaneropterinae (Orthoptera) numbers- and their abundance and species richness, and lepidopteran caterpillars. The increased presence of defoliating insects in the first year led to greater defoliation in saplings. Additionally, higher numbers of tending ants- Pheidole sp. and Pseudomyrmex termitarius (Hymenoptera: Formicidae)- and predators Salticidae (Araneae) were recorded, along with increased spider abundance and Cycloneda sanguinea (Coleoptera: Coccinellidae) number on A. auriculiformis leaves during the first year. In contrast, greater numbers of the tending ant Camponotus sp. (Hymenoptera: Formicidae) and the predatory Dolichopodidae (Diptera) were observed in the second year (Tables 1 and 2).
3.3. Ecological relationships among Arthropod groups
Saplings of A. auriculiformis with a higher number of leaves/branch supported increased numbers of Brachymyrmex sp. and Camponotus sp. (Hymenoptera: Formicidae), along with a greater abundance of tending ants. Conversely, greater foliar and or branch development in A. auriculiformis saplings was associated with a reduced number of B. hebe and overall abundance of sap-sucking Hemiptera; decreased lepidopteran caterpillar number; lower Phaneropterinae and reduced abundance and species richness of phytophagous Orthoptera; diminished Pheidole sp. number with concomitant reductions in species richness and diversity of tending ants; and fewer Apis mellifera (Hymenoptera: Apidae) individuals (Table 3).
Positive reciprocal relationships were observed between Bemisia sp. and Pheidole sp. numbers, as well as between A. reticulatum and P. termitarius numbers. Increased tending ant’ abundance was positively correlated with A. reticulatum number on A. auriculiformis leaves. Similarly, species richness of sap-sucking Hemiptera showed mutual positive relationships with tending ant species richness, while Hemiptera diversity positively influenced tending ant diversity (Table 3). The numbers of Phaneropterinae and Salticidae were negatively associated with those of Pheidole sp. and P. termitarius, respectively. The abundance and species richness of phytophagous Orthoptera were negatively associated with species richness of tending ants (Table 3).
Defoliation percentage showed significant associations with Cerotoma sp., S. anchoralis, and Phaneropterinae numbers. These defoliators positively influenced spider species diversity but negatively impacted the number of A. mellifera. Tetragonisca angustula (Hymenoptera: Apidae) number exhibited a negative association with the Coleoptera species diversity. The Oxyopidae number was positively correlated with the number of B. tabaci and Coleoptera diversity. Similarly, the Salticidae number was positively associated with those of D. speciosa and Phaneropterinae, and Orthoptera species diversity. Conversely, Coleoptera species richness was negatively associated with that of the spider (Table 3).
4. Discussion
The expanded canopy (e.g., increased branching) and enhanced soil cover (e.g., litter accumulation) were observed in second-year A. auriculiformis saplings, confirming the first hypothesis: that older saplings develop larger canopies and greater litter production, thereby accelerating the recovery of degraded areas. These findings align with growth patterns reported for other Fabaceae species (Acacia mearnsii De Wild, Ateleia glazioviana Baill, and Mimosa scabrella Benth) and Eucalyptus grandis (Myrtaceae) W. Hill ex Maiden (Eloy et al., 2018). The gradual nature of ecological recovery is exemplified by a decommissioned gold mining site in Diamantina, Minas Gerais, Brazil, where vegetation inventories recorded 707 vs. 909 individuals (diameter ≥ 3.0 cm) across 29 vs. 30 families, 57 vs. 64 genera, and 77 vs. 86 species in 2008 and 2010, respectively (Amaral et al., 2013). Similarly, cerrado regeneration showed high resilience following initial cutting, yet remained in intermediate succession stages after nearly 40 years in Nova Xavantina, Mato Grosso, Brazil (Reis et al., 2015). These comparative data highlight A. auriculiformis's exceptional potential for restoration, demonstrating both rapid growth in degraded soils and efficient nitrogen fixation (Wang et al., 2013; Dourado et al., 2020).
The increased Camponotus sp. and Dolichopodidae numbers observed during the second year of cultivation may reflect the greater number of leaves (e.g., higher tending ant abundance) in these more developed plants (>BGI effect). These findings partially support the second hypothesis that arthropod abundance and ecological indices would be greater in older plants due to their expanded canopies (>BGI) (Leite et al., 2017; Silva et al., 2020). The elevated tending ant’ abundance and Camponotus sp. number, in second-year A. auriculiformis saplings, likely resulted from the plants' larger canopy size and the presence of extrafloral nectaries at the leaf bases, which provide enhanced food resources. These observations align with patterns reported for Brachymyrmex sp., Camponotus sp., and Trigona spinipes (Hymenoptera: Apidae) in Leucaena leucocephala (Lam.) (Fabaceae) (Damascena et al., 2017). In contrast, first-year saplings exhibited a higher number of sap-sucking hemipterans (e.g., Bemisia sp.) and their associated ecological indices (e.g., species richness), defoliating coleopterans (e.g., S. anchoralis), orthopterans (e.g., T. collaris), chewing insect damage (e.g., defoliation), tending ants (e.g., Pheidole sp.), spiders (e.g., Salticidae) and their abundance, and C. sanguinea number. This pattern likely reflects the rapid growth phase of young saplings (e.g., plant vigor hypothesis), which produce tender leaves with elevated nitrogen content (including higher protein and free amino acid concentrations) due to sewage sludge fertilization (Taiz et al., 2017; Silva et al., 2020). The preference of Bemisia sp., as an example, for young vegetation is well documented; this pest typically colonizes new leaves of juvenile Glycine max L. (Fabaceae) plants, where sap contains higher concentrations of nutritionally valuable free amino acids (Cruz et al., 2016).
The observed positive relationships between tending ant numbers (e.g., Pheidole sp. and P. termitarius) and its species richness and of sap-sucking Hemiptera numbers (e.g., Bemisia sp. and A. reticulatum) and its ecological indices (e.g., abundance), predator numbers (particularly spiders) and phytophagous insect numbers (e.g., defoliators), Salticidae and D. speciosa numbers occurrence in A. auriculiformis saplings collectively are consistent with the third hypothesis: that tending ants and predator abundance are directly proportional to phytophagous Hemiptera and prey populations, respectively (Dourado et al., 2020; Demolin-Leite, 2024). These trophic interactions reflect well-documented mutualistic relationships, particularly the direct correlation between sap-sucking hemipterans and tending ants (e.g., Camponotus and Brachymyrmex spp.), which derive reciprocal benefits from their association (Novgorodova, 2015; Sanchez et al., 2019). Specifically, our findings align with previous reports showing increased populations of Aleyrodidae and A. reticulatum corresponding with higher numbers of Cephalotes sp. (Hymenoptera: Formicidae) and Brachymyrmex sp., respectively, in A. auriculiformis saplings (Demolin-Leite, 2024). Furthermore, spiders demonstrated significant biocontrol potential, effectively reducing insect-mediated damage (particularly from defoliators) in both A. auriculiformis and A. mangium saplings within degraded areas (Silva et al., 2020; Demolin-Leite, 2024).
The observed inverse relationships between Pheidole sp. and Phaneropterinae numbers, P. termitarius and Salticidae numbers, along with the negative correlation between tending ant species richness and both Orthoptera species richness and abundance, collectively support the fourth hypothesis regarding the suppressive effect of tending ant abundance on predator and chewing insect populations (Wäckers et al., 2017; Demolin-Leite, 2024). These dynamics reflect well-established trophobiotic interactions, where ants protect in exchange for honeydew resources from Sternorrhyncha. This mutualism represents a key mechanism for promoting elevated ant abundance in ecosystems (Klimes et al., 2018) while simultaneously reducing populations of natural enemies, including spiders (e.g., Oxyopidae preying on phytophagous Hemiptera) and other Sternorrhyncha predators. Such interactions may compromise the biological control of sap-sucking insects (Wäckers et al., 2017; Kaneko, 2018; Tong et al., 2019). Conversely, ants demonstrate beneficial ecological roles by suppressing defoliator and boring insect populations (e.g., Coleoptera and Lepidoptera) (Fagundes et al., 2017; Dassou et al., 2019) while simultaneously serving as valuable bioindicators of ecological restoration in degraded habitats (Sanchez, 2015).
5. Conclusions
In conclusion, vegetative biomass production (including branch development) and ground cover (through litter accumulation) showed positive correlations with sapling age in A. auriculiformis, accompanied by increased arthropod abundance (particularly tending ants). These findings demonstrate this species' potential for ecological restoration of degraded areas. Furthermore, our results revealed a trophic cascade wherein elevated populations of sap-sucking hemipterans supported greater tending ant abundance, which in turn suppressed both predator guilds and herbivorous insects.
Supplementary Material
Supplementary material accompanies this paper.
Supplementary material I
This material is available as part of the online article from https://doi.org/10.1590/1519-6984.305988
Acknowledgements
We express our gratitude to the following taxonomists for specimen identifications: Dr. Antônio Domingos Brescovit (Instituto Butantan, São Paulo, Brazil) for Arachnida, and Dr. Ayr de Moura Bello (Oswaldo Cruz Foundation, Rio de Janeiro, Brazil) for Coleoptera. Voucher specimens have been deposited with the following accession numbers: IBSP 36921-36924 (Instituto Butantan, São Paulo) for arachnids, and 1595/02 and 1597/02 (UFPR-CDZOO, Paraná) for insects.
This work was supported by the “Conselho Nacional de Desenvolvimento Científico e Tecnológico” (CNPq) [grant number 305057/2018-9] and “Fundação de Amparo à Pesquisa do Estado de Minas Gerais” (FAPEMIG) [grant number PPM-00080-17].
Data Availability Statement
The entire dataset supporting the results of this study has been published in the paper itself.
References
-
AMARAL, W.G., PEREIRA, I.M., AMARAL, C.S., MACHADO, E.L.M. and RABELO, L.D.O., 2013. Dynamics of the shrub and tree vegetation colonizing a degraded area by gold mined in Diamantina, Minas Gerais State. Ciência Florestal, vol. 23, no. 4, pp. 713-725. https://doi.org/10.5902/1980509812355
» https://doi.org/10.5902/1980509812355 -
ARAUJO, E.S., BENATTO, A., MÓGOR, A.F., PENTEADO, S.C. and ZAWADNEAK, M.A.C., 2016. Biological parameters and fertility life table of Aphis forbesi Weed, 1889 (Hemiptera: Aphididae) on strawberry. Brazilian Journal of Biology, vol. 76, no. 4, pp. 937-941. https://doi.org/10.1590/1519-6984.04715 PMid:27143052.
» https://doi.org/10.1590/1519-6984.04715 -
BEIROZ, W., AUDINO, L.D., QUEIROZ, A.C.M., RABELLO, A.M., BORATTO, I.A., SILVA, Z. and RIBAS, C.R., 2014. Structure and composition of edaphic arthropod community and its use as bioindicators of environmental disturbance. Applied Ecology and Environmental Research, vol. 12, no. 2, pp. 481-491. https://doi.org/10.15666/aeer/1202_481491
» https://doi.org/10.15666/aeer/1202_481491 -
BHUYAIN, M.M.H. and LIM, U.T., 2019. Interference and exploitation competition between Frankliniella occidentalis and F. intonsa (Thysanoptera: Thripidae) in laboratory assays. The Florida Entomologist, vol. 102, no. 2, pp. 322-328. https://doi.org/10.1653/024.102.0206
» https://doi.org/10.1653/024.102.0206 -
BOULAY, J., AUBERNON, C., RUXTON, G.D., EDOUIN, V.H., DENEUBOURG, J.L. and CHARABIDZE, D., 2019. Mixed-species aggregations in arthropods. Insect Science, vol. 26, no. 1, pp. 2-19. https://doi.org/10.1111/1744-7917.12502 PMid:28657138.
» https://doi.org/10.1111/1744-7917.12502 -
BOWERS, M.D. and STAMP, N.E., 1993. Effects of plant age, genotype and herbivory on Plant ago performance and chemistry. Ecology, vol. 74, no. 6, pp. 1778-1791. https://doi.org/10.2307/1939936
» https://doi.org/10.2307/1939936 -
BURNS, K.C., 2016. Native–exotic richness relationships: a biogeographic approach using turnover in island plant populations. Ecology, vol. 97, no. 11, pp. 2932-2938. https://doi.org/10.1002/ecy.1579 PMid:27870029.
» https://doi.org/10.1002/ecy.1579 -
CRUZ, P.L., BALDIN, E.L., GUIMARÃES, L.R., PANNUTI, L.E., LIMA, G.P., HENG-MOSS, T.M. and HUNT, T.E., 2016. Tolerance of KS-4202 soybean to the attack of Bemisia tabaci biotype B (Hemiptera: aleyrodidae). The Florida Entomologist, vol. 99, no. 4, pp. 600-607. https://doi.org/10.1653/024.099.0403
» https://doi.org/10.1653/024.099.0403 -
DAMASCENA, J.G., LEITE, G.L.D., SILVA, F.W.S., SOARES, M.A., GUAÑABENS, R.E.M., SAMPAIO, R.A. and ZANUNCIO, J.C., 2017. Spatial distribution of phytophagous insects, natural enemies, and pollinators on Leucaena leucocephala (Fabaceae) trees in the Cerrado. The Florida Entomologist, vol. 100, no. 3, pp. 558-565. https://doi.org/10.1653/024.100.0311
» https://doi.org/10.1653/024.100.0311 -
DASSOU, A.G., VODOUHÉ, S.D., BOKONON-GANTA, A., GOERGEN, G., CHAILLEUX, A., DANSI, A., CARVAL, D. and TIXIER, P., 2019. Associated cultivated plants in tomato cropping systems structure arthropod communities and increase the Helicoverpa armigera regulation. Bulletin of Entomological Research, vol. 109, no. 6, pp. 733-740. https://doi.org/10.1017/S0007485319000117 PMid:30968787.
» https://doi.org/10.1017/S0007485319000117 -
DEMOLIN-LEITE, G.L., 2024. Percentage of importance indice-production unknown: loss and solution sources identification on system. Brazilian Journal of Biology, vol. 84, pp. e253218. https://doi.org/10.1590/1519-6984.253218 PMid:35019097.
» https://doi.org/10.1590/1519-6984.253218 -
DEMOLIN-LEITE, G.L., 2025. Tropical forests. In: G.L. DEMOLIN-LEITE, ed., Innovative conservation techniques and perspectives: global biome conservation and global warming impacts on ecology and biodiversity Amsterdam: Academic Press, pp. 245-263. https://doi.org/10.1016/B978-0-443-40490-0.00017-9
» https://doi.org/10.1016/B978-0-443-40490-0.00017-9 -
DOURADO, L.R., DEMOLIN-LEITE, G.L., SOARES, M.A., TEIXEIRA, G.L., SILVA, F.W.S., SAMPAIO, R.A., ZANUNCIO, J.C. and LEGASPI, J.C., 2020. Ecological indices of phytophagous Hemiptera and their natural enemies on Acacia auriculiformis (Fabales: Fabaceae) plants with or without dehydrated sewage sludge application in a degraded area. PLoS One, vol. 15, no. 8, pp. e0237261. https://doi.org/10.1371/journal.pone.0237261 PMid:32804957.
» https://doi.org/10.1371/journal.pone.0237261 -
ELOY, E., SILVA, D.A.D., CARON, B.O., ELLI, E.F. and SCHWERZ, F., 2018. Effect of age and spacing on biomass production in forest plantations. Revista Árvore, vol. 42, no. 2, pp. e420214. https://doi.org/10.1590/1806-90882018000200014
» https://doi.org/10.1590/1806-90882018000200014 -
FAGUNDES, R., DÁTTILO, W., RIBEIRO, S.P., RICO-GRAY, V., JORDANO, P. and DEL-CLARO, K., 2017. Differences among ant species in plant protection are related to production of extrafloral nectar and degree of leaf herbivory. Biological Journal of the Linnean Society. Linnean Society of London, vol. 122, no. 1, pp. 71-83. https://doi.org/10.1093/biolinnean/blx059
» https://doi.org/10.1093/biolinnean/blx059 -
KANEKO, S., 2018. Larvae of the exotic predatory ladybird Platynaspidius maculosus (Coleoptera: Coccinellidae) on citrus tree: prey aphid species and behavioral interactions with aphid-attending ants in Japan. Applied Entomology and Zoology, vol. 53, no. 1, pp. 85-91. https://doi.org/10.1007/s13355-017-0531-y
» https://doi.org/10.1007/s13355-017-0531-y - KLIMES, P., BOROVANSKA, M., PLOWMAN, N. and LEPONCE, M., 2018. How common is trophobiosis with hoppers (Hemiptera: Auchenorrhyncha) inside ant nests (Hymenoptera: Formicidae)? Novel interactions from New Guinea and a worldwide overview. Myrmecological News, vol. 26, pp. 31-45.
-
LEITE, G.L.D., VELOSO, R.V., ZANUNCIO, J.C., AZEVEDO, A.M., SILVA, J.L., WILCKEN, C.F. and SOARES, M.A., 2017. Architectural diversity and galling insects on Caryocar brasiliense trees. Scientific Reports, vol. 7, no. 1, pp. 16677. https://doi.org/10.1038/s41598-017-16954-6 PMid:29192234.
» https://doi.org/10.1038/s41598-017-16954-6 -
NOVGORODOVA, T.A., 2015. Organization of honeydew collection by foragers of different species of ants (Hymenoptera: formicidae). European Journal of Entomology, vol. 112, no. 4, pp. 688-697. https://doi.org/10.14411/eje.2015.077
» https://doi.org/10.14411/eje.2015.077 -
OLIVEIRA, M.A., GOMES, C.F.F., PIRES, E.M., MARINHO, C.G.S. and DELLA, L.T.M.C., 2014. Bioindicadores ambientais: insetos como um instrumento desta avaliação. Revista Ceres, vol. 61, no. 1, (suppl.), pp. 800-807. https://doi.org/10.1590/0034-737x201461000005
» https://doi.org/10.1590/0034-737x201461000005 -
PEREIRA, A.P.A., ZAGATTO, M.R.G., BRANDANI, C.B., MESCOLOTTI, D.L., COTTA, S.R., GONÇALVES, J.L.M. and CARDOSO, E.J.N., 2018. Acacia changes microbial indicators and increases C and N in soil organic fractions in intercropped Eucalyptus plantations. Frontiers in Microbiology, vol. 9, no. 1, pp. 655. https://doi.org/10.3389/fmicb.2018.00655 PMid:29670606.
» https://doi.org/10.3389/fmicb.2018.00655 -
PROSSER, R.S., ANDERSON, J.C., HANSON, M.L., SOLOMON, K.R. and SIBLEY, P.K., 2016. Indirect effects of herbicides on biota in terrestrial edge-of-field habitats: A critical review of the literature. Agriculture, Ecosystems & Environment, vol. 232, no. 1, pp. 59-72. https://doi.org/10.1016/j.agee.2016.07.009
» https://doi.org/10.1016/j.agee.2016.07.009 -
REIS, S.M., MARIMON, B.S., MARIMON-JUNIOR, B.H., GOMES, L., MORANDI, P.S., FREIRE, E.G. and LENZA, E., 2015. Resilience of savanna forest after clear-cutting in the cerrado-amazon transition zone. Bioscience Journal, vol. 31, no. 5, pp. 1519-1529. https://doi.org/10.14393/BJ-v31n5a2015-26368
» https://doi.org/10.14393/BJ-v31n5a2015-26368 -
SANCHEZ, A., 2015. Fidelity and promiscuity in an ant-plant mutualism: a case study of Triplaris and Pseudomyrmex. PLoS One, vol. 10, no. 12, pp. e0143535. https://doi.org/10.1371/journal.pone.0143535 PMid:26630384.
» https://doi.org/10.1371/journal.pone.0143535 -
SANCHEZ, J.A., LÓPEZ‐GALLEGO, E. and LA‐SPINA, M., 2019. The impact of ant mutualistic and antagonistic interactions on the population dynamics of sap‐sucking hemipterans in pear orchards. Pest Management Science, vol. 76, no. 4, pp. 1422-1434. https://doi.org/10.1002/ps.5655 PMid:31628776.
» https://doi.org/10.1002/ps.5655 -
SILVA, J.L., LEITE, G.L.D., TAVARES, W.S., SILVA, F.W.S., SAMPAIO, R.A., AZEVEDO, A.M., SERRÃO, J.E. and ZANUNCIO, J.C., 2020. Diversity of arthropods on Acacia mangium (Fabaceae) and production of this plant with dehydrated sewage sludge in degraded area. Royal Society Open Science, vol. 7, no. 2, pp. 191196. https://doi.org/10.1098/rsos.191196 PMid:32257306.
» https://doi.org/10.1098/rsos.191196 - TAIZ, L., ZEIGER, E., MOLLER, I.M. and MURPHY, A., 2017. Fisiologia e desenvolvimento vegetal Porto Alegre: Artmed Editora.
-
TONG, H., AO, Y., LI, Z., WANG, Y. and JIANG, M., 2019. Invasion biology of the cotton mealybug, Phenacoccus solenopsis Tinsley: current knowledge and future directions. Journal of Integrative Agriculture, vol. 18, no. 4, pp. 758-770. https://doi.org/10.1016/S2095-3119(18)61972-0
» https://doi.org/10.1016/S2095-3119(18)61972-0 -
WÄCKERS, F.L., ALBEROLA, J.S., GARCIA-MARÍ, F. and PEKAS, A., 2017. Attract and distract: manipulation of a food-mediated protective mutualism enhances natural pest control. Agriculture, Ecosystems & Environment, vol. 246, pp. 168-174. https://doi.org/10.1016/j.agee.2017.05.037
» https://doi.org/10.1016/j.agee.2017.05.037 -
WANG, F., ZHU, W., ZOU, B., NEHER, D.A., FU, S., XIA, H. and LI, Z., 2013. Seedling growth and soil nutrient availability in exotic and native tree species: implications for afforestation in southern China. Plant and Soil, vol. 364, no. 1, pp. 207-218. https://doi.org/10.1007/s11104-012-1353-x
» https://doi.org/10.1007/s11104-012-1353-x -
ZANUNCIO, A.J.V., SERRÃO, J.E., PEREIRA, A.I.A., SOARES, M.A., WILCKEN, C.F., LEITE, G.L.D. and ZANUNCIO, J.C., 2015. Aethalion reticulatum (Hemiptera: Aethalionidae) feeding on Erythrina speciosa (Fabales: Fabaceae): first record of its host plant and damage characteristics. The Florida Entomologist, vol. 98, no. 1, pp. 175-177. https://doi.org/10.1653/024.098.0130
» https://doi.org/10.1653/024.098.0130
Edited by
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Editor:
Takako Matsumura Tundisi
