Insects, tending ants, and spiders on Terminalia argentea (Combretaceae) saplings as bioindicators for the recovery of degraded area

Insetos, formigas cuidadoras e aranhas em mudas de Terminalia argentea (Combretaceae) como bioindicadores para a recuperação de área degradada

Abstract

Anthropogenic activities have intensified soil degradation and disrupted essential ecological processes, underscoring the need for effective ecological restoration strategies. Terminalia argentea, a pioneer species of the Cerrado, has demonstrated potential for recovering degraded areas and facilitating arthropod recolonization. Arthropods are sensitive to environmental changes and are thus recognized as bioindicators. This study aimed to assess the recovery of a degraded area by evaluating insect and spider ecological indices, their interactions, and the plant biomass of T. argentea saplings over a two-year field establishment period. Saplings with greater biomass (e.g., more leaves/branch) supported a higher abundance and richness of tending ants. During the first year after planting, the leaves of T. argentea saplings exhibited higher numbers of chewing insects (e.g., Cerotoma sp.) and their ecological indices (e.g., diversity), spiders (e.g., Oxyopidae) and their species richness, bees (e.g., Trigona spinipes) and their abundance, and tending ants (e.g., Brachymyrmex sp.) and their diversity and richness of species. In contrast, saplings in the second year after planting hosted higher numbers of sap-sucking insects (e.g., Aphis spiraecola), their tending ant Camponotus sp., and their Dolichopodidae predators. Saplings with more sap-sucking insects (e.g., Phenacoccus sp.) also had more tending ants (e.g., Camponotus sp.). However, an increase in tending ants (e.g., Ectatomma sp.) was associated with a reduction in predators (e.g., Photinus sp.) and chewing insects (e.g., Lamprosoma sp.). The presence of spiders (e.g., Araneidae) was correlated with higher numbers of chewing insects (e.g., Cephalocoema sp.), while Mantis religiosa and Polybia sp. were more common on saplings with higher defoliation percentages, and Syrphus sp. was associated with Bemisia sp.. These results indicate that trophic interactions, mediated by both bottom-up and top-down mechanisms, structure the arthropod community on T. argentea, promoting the coexistence of functional groups and enhancing ecological indices. Future studies involving predator exclusion and leaf chemical analyses will be essential to deepen this understanding.

Keywords:
arthropods; Formicidae; insects; spiders; trophic interactions

Resumo

As atividades antropogênicas intensificaram a degradação do solo e interromperam processos ecológicos essenciais, ressaltando a necessidade de estratégias eficazes de restauração ecológica. Terminalia argentea, uma espécie pioneira do Cerrado, tem demonstrado potencial para a recuperação de áreas degradadas e para facilitar a recolonização por artrópodes. Os artrópodes são sensíveis às mudanças ambientais e, portanto, são reconhecidos como bioindicadores. Este estudo teve como objetivo avaliar a recuperação de uma área degradada por meio da análise de índices ecológicos de insetos e aranhas, suas interações e a biomassa de mudas de T. argentea durante um período de dois anos de cultivo em campo. Mudas com maior biomassa (ex.: mais folhas/galho) apresentaram maior abundância e riqueza de formigas cuidadoras. Durante o primeiro ano após o plantio, as folhas das mudas de T. argentea apresentaram maior número de insetos mastigadores (ex.: Cerotoma sp.) e seus índices ecológicos (ex.: diversidade), aranhas (ex.: Oxyopidae) e sua riqueza de espécies, abelhas (ex.: Trigona spinipes) e sua abundância, e formigas cuidadoras (ex.: Brachymyrmex sp.) e sua diversidade e riqueza de espécies. Em contraste, as mudas no segundo ano após o plantio apresentaram maior número de insetos sugadores de seiva (ex.: Aphis spiraecola), sua formiga cuidadora Camponotus sp. e seus predadores da família Dolichopodidae. Mudas com maior número de insetos sugadores de seiva (ex.: Phenacocus sp.) também apresentaram maior número de formigas cuidadoras (ex.: Camponotus sp.). Contudo, o aumento de formigas cuidadoras (ex.: Ectatomma sp.) foi associado à redução de predadores (ex.: Photinus sp.) e insetos mastigadores (ex.: Lamprosoma sp.). A presença de aranhas (ex.: Araneidae) correlacionou-se com um maior número de insetos mastigadores (ex.: Cephalocoema sp.), enquanto Mantis religiosa e Polybia sp. foram mais comuns em mudas com maiores percentuais de desfolha, e Syrphus sp. foi associado a Bemisia sp.. Esses resultados indicam que as interações tróficas, mediadas por mecanismos ascendentes e descendentes, estruturam a comunidade de artrópodes em T. argentea, promovendo a coexistência de grupos funcionais e aprimorando os índices ecológicos. Estudos futuros envolvendo a exclusão de predadores e análises químicas foliares serão essenciais para aprofundar esse entendimento.

Palavras-chave:
artrópodes; Formicidae; insetos; aranhas; interações tróficas

1. Introduction

The restoration of degraded areas is a global challenge, particularly in biomes like the Cerrado, where biodiversity loss and soil degradation are critical (Costa et al., 2020; Oliveira et al., 2020; Rodrigues et al., 2020; Demolin-Leite, 2025). In this context, fertilization with sewage sludge and the introduction of native pioneer species are valuable tools for ecological recovery. These practices enhance soil quality, increase plant biomass, and accelerate restoration, thereby helping to reestablish local and regional ecological functions (Sampaio et al., 2012; Dourado et al., 2020; Silva et al., 2020; Guerrini et al., 2021).

Pioneer plant species such as Terminalia argentea Mart. (Combretaceae) are notable for their ability to establish in nutrient-poor, arid soils and to promote natural regeneration and ecosystem stabilization (Lorenzi, 2020; Vieira et al., 2021). Known as “capitão-do-campo,” T. argentea is a tree native to Brazil, widely used in ecological restoration, landscaping, and timber production (Carvalho et al., 2020; Lorenzi, 2020; Vieira et al., 2021; Leite et al., 2024; Lima et al., 2024a; Longui et al., 2024). Beyond its ecological importance, T. argentea possesses medicinal properties derived from secondary metabolites- including phenolic compounds, flavonoids, saponins, tannins, and phytosterols- which can influence its interactions with arthropods (Fahmy et al., 2015; Beserra et al., 2018; Moreira et al., 2020; Venturini et al., 2023).

Arthropods are crucial for maintaining ecological functionality in both natural and restored environments. By acting as herbivores, predators, decomposers, and pollinators, they serve as excellent bioindicators (Sánchez-Bayo and Wyckhuys, 2019). Key groups interacting with T. argentea include phytophagous insects, predators, pollinators, tending ants, and spiders (Carvalho et al., 2020; Costa et al., 2021). These interactions are sensitive to factors such as organic fertilization, plant growth stage, and changes in vegetation characteristics like leaf biomass and structural complexity, all of which directly affect resource availability and arthropod community dynamics (El-Shafie, 2022; Demolin-Leite, 2023; Leite et al., 2024; Oliveira et al., 2024). In this context, a T. argentea sapling can be conceptualized as a small-scale biogeographic island (Méndez-Castro et al., 2018; Carvalho et al., 2020; Matthews and Triantis, 2021; Al-Namazi and Bonser, 2022; Mech et al., 2024).

Despite their fundamental role, the interactions between T. argentea and arthropods, and the effects of the recovery period on these dynamics, remain poorly understood. This study, therefore, aimed to evaluate the restoration of a degraded area by analyzing the ecological indices of insects and spiders (as bioindicators), their trophic interactions, and plant biomass production in T. argentea saplings over two years following planting. We tested the following four hypotheses: i) older T. argentea saplings will exhibit greater biomass production, thereby making a greater contribution to the recovery of the degraded area; ii) the diversity, richness, and abundance of arthropods will be higher on T. argentea saplings with greater biomass; iii) an increase in sap-sucking hemipterans will lead to a greater number of tending ants, which in turn will reduce the numbers of predators and chewing insects; and iv) predators will follow their prey.

2. Material and Methods

2.1. Experimental site

The work was established in a degraded area of the “Instituto de Ciências Agrárias da Universidade Federal de Minas Gerais (ICA/UFMG)” in Montes Claros, Minas Gerais State, Brazil (16° 51’ 38” S, 44° 55’ 00” W, 620 m.a.l.s.) from April 2020 to March 2022. According to the Köppen climate classification, this area’s climate is tropical dry, with annual precipitation between 1000 and 1300 mm, dry winter, and average annual temperature ≥ 26 °C. The soil is Neosol Litolic with an Alic horizon (Silva et al., 2020).

2.2. Experimental design

In March 2019, 24 T. argentea seedlings were prepared in a nursery in plastic bags (16 × 24 cm) with reactive natural phosphate mixed with the substrate at a dosage of 160 g. After that, they were planted in the final location in September of the same year. All of them were planted in holes (40 × 40 × 40 cm) when they were 30 cm high, with a 2-m spacing between them. The soil was corrected with dolomitic limestone, increasing base saturation to 50%, natural phosphate, gypsum, FTE (Fried Trace Elements), potassium chloride, and micronutrients equivalent to the needs determined in the soil analysis. A total of 20 L of dehydrated sewage sludge, in a single dose, was placed in each, and the biochemical characteristics of this fertilizer have been reported (Silva et al., 2020). The seedlings were irrigated twice a week until the beginning of the rainy season (October). The design was completely randomized with 24 replications (one sapling each) with first-year and second-year post-planting as treatments.

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 (1m²) in the crown projection of each one of the 24 T. argentea saplings.

2.4. Counting the arthropods

All insects and spiders were counted, between 7:00 A.M. and 11:00 A.M., by visual observation, every two weeks on the adaxial and abaxial surfaces of the first 12 leaves expanded, per sapling. These leaves were assessed, randomly, on branches (one leaf per position) in the basal, middle, and apical parts of the canopy - vertical axis - (0 to 33%, 33 to 66%, and 66 to 100% of total sapling height, respectively) and in the north, south, east, and west directions- horizontal axis. A total of 12 leaves/sapling/evaluation were observed on 24 T. argentea saplings starting six months after transplantation during 24 months (13,824 total leaves), covering the entire sapling (vertical and horizontal axis), capturing the highest possible number of arthropods (insects and spiders), especially the rarest ones. The evaluator approached, carefully, firstly assessing the adaxial leaf surface and, if it was not possible to visualize the abaxial one, with a delicate and slow movement, lifting the leaf to visualize it. Insects with greater mobility (e.g., Orthoptera) that flew, on approach, were counted as long as they were recognized (e.g., Order). The arthropods (insects and spiders) were not removed from the saplings during the evaluation.

A few arthropod specimens (up to 3 individuals) per species were collected using an aspirator (two hours per week) at the beginning of the study (between transplantation and first evaluation, six months after), stored in flasks with 70% alcohol, separated into morphospecies, and sent to specialists for identification (see acknowledgments). Any visible arthropod, not yet computed in previous evaluations, was collected, coded, and sent to a taxonomist of its group.

2.5. Statistical analysis

Each replication is the total of individuals collected on 12 leaves (three heights and four sides of the sapling). The ecological indices (abundance, diversity, and species richness) were calculated per group (e.g., chewing insects) and treatments (first and second year after planting) using the BioDiversity Professional, version 2 (© 1997). Abundance and species richness were the total numbers of individuals and species, respectively, per sapling. Diversity was calculated using the Hill’ formula (1st order): N1= exp (H’), where H’ is the Shannon-Weaver diversity index, calculating the diversity with the actual species number.

The data for abundance, diversity, and species richness of phytophagous insects, pollinators, and natural enemies 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. 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., spiders). 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 to 3), and the others are in Supplementary Material I.

Table 1
Abundance (Abun.), Diversity (D.) and species richness (S.R) of phytophagous chewing insects (Chew.), Hemiptera phytophagous (Hem.), pollinators (Poll.), tending ants (Ants), Sternorrhyncha predators (Pred.), spiders (Spid.), number of branches/sapling and leaves/branch, percentages of defoliation by insects and ground cover per Terminalia argentea (Combretaceae) sapling (mean ± SE) and planting year.

Variables	Year		TW *
	First	Second	VT£	P
Abun. Chew.	7.58 ± 1.10	3.50 ± 0.57	2.68	0.00
D. Chew.	7.77 ± 1.10	4.61 ± 0.73	2.03	0.02
S.R. Chew.	3.58 ± 0.37	2.25 ± 0.27	2.50	0.00
Abun. Hem.	5.63 ± 2.80	15.42 ± 8.14	0.31	0.37
D. Hem.	1.23 ± 0.37	1.25 ± 0.45	0.00	0.50
S.R. Hem.	1.08 ± 0.19	0.88 ± 0.21	0.94	0.17
Abun. Poll.	8.71 ± 2.64	1.63 ± 0.55	1.98	0.02
D. Poll.	0.48 ± 0.14	0.57 ± 0.17	0.20	0.42
S.R. Poll.	0.63 ± 0.10	0.50 ± 0.13	1.05	0.14
Abun. Ants	16.42 ± 2.85	12.25 ± 1.86	0.87	0.19
D. Ants	4.64 ± 0.49	2.41 ± 0.25	3.48	0.00
S.R. Ants	2.83 ± 0.17	1.71 ± 0.18	3.78	0.00
Abun. Pred.	1.46 ± 0.41	1.83 ± 0.31	1.41	0.07
D. Pred.	1.03 ± 0.26	1.05 ± 0.25	0.03	0.48
S.R. Pred.	0.83 ± 0.13	0.96 ± 0.12	0.70	0.24
Abun. Spid.	1.42 ± 0.29	2.96 ± 1.41	1.08	0.14
D. Spid.	1.27 ± 0.49	0.61 ± 0.23	0.42	0.33
S.R. Spid.	1.25 ± 0.22	0.67 ± 0.14	1.89	0.02
Leaves/branch	12.05 ± 0.39	10.61 ± 0.33	2.66	0.00
Branches/sapling	27.44 ± 1.34	29.59 ± 2.04	0.85	0.19
Ground cover	10.65 ± 0.97	14.89 ± 2.15	0.78	0.21
Defoliation	8.47 ± 0.45	7.62 ± 0.27	1.16	0.12

• ^*
  TW = Test of Wilcoxon;
• ^£VT = value of test; n = 24 per treatment.

Table 3
Order, family, and species of spiders (Class Arachnidae) and insects (Class Insecta) per Terminalia argentea (Combretaceae) sapling (mean ± SE) and planting year.

Order: Family: Specie	Year		TW *
	First	Second	VT£	P
Ara.: Oxyopidae: Not identified	0.33 ± 0.11	0.08 ± 0.05	1.86	0.03
Col.: Buprestidae: Psiloptera sp.	0.21 ± 0.13	0.00 ± 0.00	1.77	0.03
Chrysomelidae: Clytrini	0.04 ± 0.04	0.21 ± 0.08	1.73	0.04
Cerotoma sp.	0.46 ± 0.19	0.00 ± 0.00	2.59	0.00
Lamprosoma sp.	1.21 ± 0.21	0.42 ± 0.15	3.09	0.00
Curculionidae: Diorymerus sp.	1.17 ± 0.48	0.00 ± 0.00	2.59	0.00
Lampyridae: Photinus sp.	0.33 ± 0.15	0.00 ± 0.00	2.33	0.00
Dip.: Dolichopodidae: Not identified	0.75 ± 0.41	1.63 ± 0.28	3.22	0.00
Otitidae: Euxesta sp.	0.04 ± 0.04	0.38 ± 0.14	2.31	0.01
Hem.: Aphididae: Aphis spiraecola	2.83 ± 2.83	13.88 ± 8.18	1.95	0.02
Hym.: Apidae: Trigona spinipes	8.67 ± 2.64	1.50 ± 0.51	1.97	0.02
Formicidae: Brachymyrmex sp.	3.75 ± 1.08	1.38 ± 0.52	1.79	0.03
Camponotus sp.	0.13 ± 0.06	10.50 ± 1.78	5.64	0.00
Ectatoma sp.	2.25 ± 0.85	0.04 ± 0.04	3.81	0.00
Pheidole sp.	6.25 ± 1.97	0.13 ± 0.06	5.05	0.00
Pseudomyrmex termitarius	4.04 ± 1.01	0.17 ± 0.09	4.20	0.00
Vespidae: Polybia sp.	0.63 ± 0.15	0.13 ± 0.06	2.83	0.00
Lep.: Not identified	0.25 ± 0.09	0.04 ± 0.04	2.02	0.02

• ^*
  TW= Test of Wilcoxon;
• ^£VT= value of test;
• n = 24 per treatment.

3. Results

3.1. Plant biomass production and defoliation

The number of leaves/branch on T. argentea saplings decreased in the second year after planting (Table 1). Saplings with a higher number of leaves/branch supported a greater number of Ectatomma sp., Pheidole sp. (Hymenoptera: Formicidae), as well as higher overall abundance and richness of tending ants. Furthermore, saplings with more branches/sapling exhibited a higher number of Camponotus sp. and Euxesta sp. (Diptera: Otitidae) (Table 2). Increased defoliation was positively correlated with the species richness of chewing insects and with the number of Trigona spinipes (Apidae: Hymenoptera).

Table 2
Relationships between abundance (Abun.) of chewing insects (Chew.), phytophagous Hemiptera (Hem.), tending ants (Ants), and spiders (Spid.), diversity (D.) of ants, and species richness (S.R) of ants and Chew., numbers of Aphis spiraecola (Aphis), Araneidae (Aran.), Bemisia sp. (Bemi.), Camponotus sp. (Camp.), Cerambycidae (Ceram.), Cerotoma sp. (Cero.), Cephalocoema sp. (Cephal.), Cycloneda sanguinea (Csang.), Diorymerus sp. (Diory.), Ectatoma sp. (Ecta.), Epitragus sp. (Epi.), Euxesta sp. (Eux.), Fulgoridae (Fulg.), Lamprosoma sp. (Lampr.), Mantis religiosa (Mrel.), Oxyopidae (Oxyo.), Pentatomidae (Pent.), Phenacoccus sp. (Phen.), Pheidole sp. (Phei.), Photinus sp. (Phot.), Polybia sp. (Poly.), Pseudomyrmex termitarius (Pter.), Syrphus sp. (Syrp.), Phaneropterinae (Phan.), Trigona spinipes (Tspi.), Tropidacris collaris (Tcoll.), percentage of defoliation (Def.), branches/sapling (Branches), and leaves/branch (Leaves) on Terminalia argentea (Combretaceae) saplings.

Principal component regressions	R2	F	P
Abun.Spid=1.01+7.12xCeram.+3.50xCephal.	0.45	18.59	0.00
Aran.=0.24+7.44xCeram.+3.69xCephal.	0.50	22.24	0.00
Camp.=-3.16+2.58xPhen.+0.26xBranches+0.08xAphis	0.42	10.76	0.00
Def.=6.79+S.R.Chew.+0.10xTspi.	0.38	13.54	0.00
Mrel.=-0.41+0.44xCsang.+0.21xPhan.+0.07xFulg.+0.05xDef.	0.59	15.64	0.00
Poly.=-0.57+0.08xDef.+0.07xFulg.+0.04xAb.Chew.	0.34	7.57	0.00
First and Second degree regressions
Ab.Ants=-15.32+2.62xLeaves	0.18	10.00	0.00
Ab.Chew.=2.02+0.36xAb.Ants-0.005xAb.Ants2	0.18	4.82	0.01
Ab.Chew.=0.72+2.21xD.Ants-0.17xD.Ants2	0.14	3.75	0.03
Ab.Chew.=4.31+0.65xPhei-0.01xPhei.2	0.16	4.37	0.01
Ab.Hem.=3.89+1.25xCamp.	0.11	5.88	0.01
S.R.Ants=0.08+0.19xLeaves	0.13	6.58	0.01
Aphis=1.93+1.21xCamp.	0.10	5.36	0.02
Ecta.=-6.89+0.71xLeaves	0.19	10.67	0.00
Epi.=0.04+0.18xPter.-0.01xPter.2	0.16	4.35	0.01
Eux.=0.05+0.07xCamp.-0.002xCamp.2	0.14	3.75	0.03
Eux.=-0.40+0.02xBranches	0.11	5.67	0.02
Lampr.=0.54+0.15xPhei-0.003xPhei.2	0.18	4.89	0.01
Oxyo.=0.16+0.23xCero.	0.13	7.13	0.01
Oxyo.=0.15+0.10xDiory.	0.14	7.42	0.00
Pent.=0.13+0.09xPhei-0.002xPhei.2	0.16	4.24	0.02
Phei.=-15.74+1.67xLeaves	0.18	10.40	0.00
Phen.=-0.26+0.09xCamp.	0.24	14.33	0.00
Poly.=0.22+0.09xPhei-0.002xPhei.2	0.16	4.32	0.01
Phot.=0.08+0.23xEcta.-0.02xEcta.2	0.13	3.34	0.04
Syrp.=0.06+0.09xBemi.	0.21	11.90	0.00
Tcoll.=0.61+0.23xPhei-0.005xPhei.2	0.15	3.88	0.02

• n = 48.

3.2. Arthropods and their ecological indices

In the first year after planting, the leaves of T. argentea saplings supported a higher number of several arthropod groups and their ecological indices. These included i) chewing insects, Psiloptera sp. (Coleoptera: Buprestidae), Cerotoma sp. and Lamprosoma sp. (Coleoptera: Chrysomelidae), Diorymerus sp. (Coleoptera: Curculionidae), and caterpillars (Lepidoptera). The overall abundance, diversity, and species richness of this group were also higher. ii) natural enemies: Oxyopidae (Araneae), Photinus sp. (Coleoptera: Lampyridae), Polybia sp. (Hymenoptera: Vespidae). Spider species richness was also elevated. iii) pollinators: Trigona spinipes (Hymenoptera: Apidae), along with a higher overall abundance of pollinators. And iv) tending ants: Brachymyrmex sp., Ectatomma sp., Pheidole sp., and Pseudomyrmex termitarius (Hymenoptera: Formicidae). This group also exhibited greater diversity and species richness. Conversely, the second year after planting was characterized by higher numbers of different groups, specifically: i) herbivorous insects: Clytrini (Coleoptera: Chrysomelidae), Euxesta sp. (Diptera: Otitidae), and Aphis spiraecola (Hemiptera: Aphididae); ii) predators: Dolichopodidae (Diptera); and iii) tending ants: Camponotus sp. (Hymenoptera: Formicidae) (Tables 1 and 3).

3.3. Ecological relationships among arthropod groups

A mutualistic relationship was observed between the tending ant Camponotus sp. and the sap-sucking hemipterans Phenacoccus sp. and A. spiraecola, where increases in one group corresponded to increases in the other on T. argentea saplings. The presence of certain tending ants had suppressive effects on other arthropods. A higher number of Ectatomma sp. and Pheidole sp. was associated with reduced numbers of the predators Photinus sp. and Polybia sp., respectively. Furthermore, Pheidole sp. was negatively associated with the phytophagous insects Lamprosoma sp., Tropidacris collaris (Orthoptera: Romaleidae), and Pentatomidae (Hemiptera), as well as with the overall abundance of chewing insects. Similarly, P. termitarius and Camponotus sp. were linked to decreases in Epitragus sp. (Coleoptera: Tenebrionidae) and Euxesta sp., respectively. In general, a greater abundance and diversity of tending ant species were associated with reduced abundance of chewing insects (Table 2).

Predator abundances were positively linked to the availability of their prey. Saplings with higher numbers of the chewing insects Cerambycidae (Coleoptera) and Cephalocoema sp. (Orthoptera: Proscopiidae) supported increased numbers of Araneidae and a higher overall spider abundance. Similarly, increases in Oxyopidae were associated with more Cerotoma sp. and Diorymerus sp.. The number of the predator Mantis religiosa (Mantodea: Mantidae) increased with higher numbers of the phytophagous insects Phaneropterinae (Orthoptera: Tettigoniidae) and Fulgoridae (Hemiptera), the predator Cycloneda sanguinea (Coleoptera: Coccinellidae), and with the percentage of defoliation. The number of the predator Polybia sp. was also higher on saplings with greater defoliation, a higher overall abundance of chewing insects, and more Fulgoridae. Finally, the number of Syrphus sp. (Diptera: Syrphidae) was positively correlated with that of Bemisia sp. (Hemiptera: Aleyrodidae) (Table 2).

4. Discussion

In the second year after planting, T. argentea saplings exhibited a reduction in the number of leaves/branch. This finding does not support our first hypothesis, which proposed that older saplings would have greater plant biomass production. The sustained vertical growth and maintained vegetation cover between the first and second years were likely facilitated by fertilization with sewage sludge, a rich source of macro- and micronutrients such as nitrogen, phosphorus, and potassium (Costanzo et al., 2021). Sewage sludge has been shown to promote increased biomass and accelerated growth in various plant species, including Brassica napus (Brassicaceae), Eucalyptus grandis (Myrtaceae), Helianthus annuus (Asteraceae), Miscanthus giganteus (Poaceae), and Zea mays (Poaceae) (Silva et al., 2011; Dubis et al., 2020; Kominko et al., 2022). As pioneer species like T. argentea respond rapidly to nutrient availability, they often prioritize structural growth and height gain over leaf production and longevity (Coll et al., 2008; Selaya and Anten, 2010; Bardy et al., 2023; Shannon et al., 2023). Furthermore, competition for light within the developing canopy can drive the reallocation of resources to new, higher tissues. This accelerates the senescence of lower, shaded leaves and favors monopodial growth, thereby promoting more efficient light capture (Selaya and Anten, 2010). Therefore, the observed reduction in leaf biomass in T. argentea likely reflects a strategic physiological (e.g., trade-off between growth and leaf maintenance) adjustment to support sustained vertical growth rather than a simple loss of biomass (source-drain relationship).

In the first year after planting, the leaves of T. argentea saplings supported higher numbers of chewing insects (e.g., Psiloptera sp.), spiders (e.g., Oxyopidae), bees (e.g., T. spinipes), and tending ants (e.g., Brachymyrmex sp.), as well as greater ecological indices (e.g., abundance, diversity, or species richness) for these groups. These patterns are consistent with the Theory of Island Biogeography (BGI). According to this theory, increased plant biomass (e.g., more leaves/branch) expands the availability of resources such as food and shelter, creating more niches and microhabitats, thereby supporting a greater “carrying capacity” for arthropods (Silva et al., 2020, 2021; Mota et al., 2023; Souza et al., 2023). This condition facilitates higher arthropod ecological indices, as previously documented for T. argentea (Carvalho et al., 2020; Costa et al., 2021), and favors the diversity of herbivores and tending ants, which in turn supports their natural enemies (Leite et al., 2016, 2017, 2024; Macedo-Reis et al., 2019; Oliveira et al., 2024). These findings support hypothesis ii, which predicted that arthropod diversity, richness, and abundance would be higher on T. argentea saplings with greater biomass. Furthermore, this ecological cascade was likely initiated by the accelerated growth of saplings promoted by nitrogen-rich sewage sludge fertilization (Wierzbowska et al., 2021). Beyond simply increasing biomass, fertilization enhanced host plant quality by improving palatability (e.g., reducing leaf toughness) (Zeng et al., 2024) and nutritional value (e.g., elevating free amino acid levels) (Cristina et al., 2020; Lee et al., 2021). This improvement in host quality intensified colonization by herbivorous insects and, consequently, by their associated arthropod communities on the more robust T. argentea saplings.

In the second year after planting, an increase in the abundance of sap-sucking hemipterans (e.g., A. spiraecola) was accompanied by a rise in their tending ant, Camponotus sp. Conversely, saplings with a higher number of other tending ants (e.g., Ectatomma sp.) supported fewer predators (e.g., Polybia sp.) and chewing insects (e.g., T. collaris). These findings confirm our third hypothesis that an increase in sap-sucking hemipterans would lead to greater numbers of tending ants, which in turn would reduce populations of predators and chewing insects on T. argentea. These patterns result from mutualistic interactions, where ants protect sap-sucking hemipterans from natural enemies in exchange for honeydew, while also directly suppressing herbivores through top-down control, thereby reducing defoliation (Venturino et al., 2008; Vidal and Murphy, 2018; Camacho and Avilés, 2021; Nelson and Mooney, 2022). Similar trophic outcomes have been documented for Acacia auriculiformis (Mota et al., 2023; Teixeira et al., 2024), Acacia mangium (Lima et al., 2024b), Caryocar brasiliense (Demolin-Leite et al., 2024), Sapindus saponaria (Souza et al., 2023; Demolin-Leite, 2024), and T. argentea (Carvalho et al., 2020; Costa et al., 2021). Collectively, these findings underscore the critical role of such interactions in the establishment, stability, and maintenance of arthropod communities (Schmitz and Barton, 2013; Pettorelli et al., 2015).

The fourth hypothesis- that predator abundance follows prey availability- was confirmed. This was evidenced by several specific relationships: higher numbers of spiders (e.g., Oxyopidae) on T. argentea saplings were associated with increased numbers of chewing insects (e.g., Cerotoma sp.); higher numbers of prey (e.g., Phaneropterinae) and related herbivory indices (e.g., percentage of defoliation) led to more M. religiosa; and increased numbers of Bemisia sp. resulted in more Syrphus sp.. The greater structural complexity generated by increased sapling biomass directly benefits predators such as spiders. Plant architecture provides essential web support and modulates microhabitat conditions, thereby influencing spider diversity and community composition (Uetz, 1991; Langellotto and Denno, 2004). This relationship is functionally critical, given the role of spiders as obligate predators (Landis et al., 2000; Lang, 2003; Venturino et al., 2008; Leite et al., 2012; Silva et al., 2020). These findings highlight an interplay between bottom-up and top-down forces. A bottom-up effect, where plant complexity creates niches for various herbivore and predator guilds (Filloy et al., 2023; Pequeno et al., 2023), is coupled with top-down control, where predators (e.g., spiders, wasps, and mantids) regulate prey populations (Michelutti et al., 2017; Michalko et al., 2019; Rankin et al., 2023). Consequently, the correlation between phytophagous insects and their predators demonstrates that trophic interactions respond dynamically to resource availability. This dynamic promotes cascading effects that regulate the community, facilitate the coexistence of different functional groups, and sustain high ecological indices (Halaj and Wise, 2001; Klauschies et al., 2016; Vidal and Murphy, 2018; Iwashita et al., 2022; Saha et al., 2023).

5. Conclusions

The structure of the arthropod community on T. argentea saplings is shaped by a complex interplay between the plant's growth strategy and resultant trophic cascades. The rejection of the first hypothesis reveals a key physiological adjustment in the plant, favoring competitive vertical growth over simple foliar biomass accumulation. Despite this, initial sewage sludge fertilization initiated strong bottom-up effects, confirming that greater plant biomass enhances arthropod ecological indices (supporting hypothesis ii). Subsequent trophic interactions- including mutualism between tending ants and sap-sucking hemipterans, and classic predator-prey dynamics- were fundamental to community regulation, thereby confirming hypotheses iii and iv and underscoring the role of top-down control. Our findings demonstrate that both bottom-up and top-down processes are pivotal in structuring arthropod communities within recovering ecosystems. Future research should employ predator exclusion experiments and plant tissue chemical analyses to further elucidate the mechanisms driving these community dynamics throughout ecological succession.

Supplementary Material

Supplementary material accompanies this paper.

Supplementary material I

Order, family, and species of spiders (Class Arachnidae) and insects (Class Insecta) per Terminalia argentea (Combretaceae) sapling (mean ± SE) and planting year.

This material is available as part of the online article from https://doi.org/10.1590/1519-6984.302611

Data Availability Statement

The entire data set supporting the results of this study has been published in the paper itself.

References

• AL-NAMAZI, A.A. and BONSER, S.P., 2022. Island biogeography, competition, and abiotic filtering together control species richness in habitat islands formed by nurse tree canopies in an arid environment. Communicative & Integrative Biology, vol. 15, no. 1, pp. 232-239. https://doi.org/10.1080/19420889.2022.2139471 PMid:36339474.
  » https://doi.org/10.1080/19420889.2022.2139471
• BARDY, L.R., DEBIASI, T.V., SANADA, K., RONDINA, A.B.L., TOREZAN, J.M.D., STOLF-MOREIRA, R., BIANCHINI, E., PIMENTA, J.A. and OLIVEIRA, H.C., 2023. Effect of nitrogen addition to the soil on Atlantic Forest tree seedlings. Forests, vol. 14, no. 6, pp. 1-15. https://doi.org/10.3390/f14061111
  » https://doi.org/10.3390/f14061111
• BESERRA, A.M.S., VILEGAS, W., TANGERINA, M.M.P., ASCÊNCIO, S.D., SOARES, I.M., PAVAN, E., DAMAZO, A.S., RIBEIRO, R.V. and MARTINS, D.T.O., 2018. Chemical characterisation and toxicity assessment in vitro and in vivo of the hydroethanolic extract of Terminalia argentea Mart. leaves. Journal of Ethnopharmacology, vol. 227, pp. 56-68. https://doi.org/10.1016/j.jep.2018.08.025 PMid:30142424.
  » https://doi.org/10.1016/j.jep.2018.08.025
• CAMACHO, L. and AVILÉS, L., 2021. Resource exchange and partner recognition mediate mutualistic interactions between prey and their would-be predators. Biology Letters, vol. 17, no. 8, pp. 20210316. https://doi.org/10.1098/rsbl.2021.0316 PMid:34376075.
  » https://doi.org/10.1098/rsbl.2021.0316
• CARVALHO, J.C.N., SILVA, F.W.S., LEITE, G.L.D., AZEVEDO, A.M., TEIXEIRA, G.L., SOARES, M.A., ZANUNCIO, J.C. and LEGASPI, J.C., 2020. Does fertilization with dehydrated sewage sludge affect Terminalia argentea (Combretaceae) and associated arthropods community in a degraded area? Scientific Reports, vol. 10, no. 1, pp. 11811. https://doi.org/10.1038/s41598-020-68747-z PMid:32678241.
  » https://doi.org/10.1038/s41598-020-68747-z
• COLL, L., POTVIN, C., MESSIER, C. and DELAGRANGE, S., 2008. Root architecture and allocation patterns of eight native tropical species with different successional status used in open-grown mixed plantations in Panama. Trees, vol. 22, no. 4, pp. 585-596. https://doi.org/10.1007/s00468-008-0219-6
  » https://doi.org/10.1007/s00468-008-0219-6
• COSTA, T., IWATA, B., ROCHA, I., SOUZA, Í., PORTO, S., ALVES, A., FERREIRA, P. and RODRIGUES, N., 2020. Diagnosis and proposal for the recovery of degraded area under physiognomy of Cerrado in Corrente – Piauí. Brazilian Journal of Development, vol. 6, no. 12, pp. 93976-93989. https://doi.org/10.34117/bjdv6n12-020
  » https://doi.org/10.34117/bjdv6n12-020
• COSTA, S.S.D., LEITE, G.L.D., SILVA, F.W.S., SANTOS, J.B.D., AZEVEDO, A.M., SAMPAIO, R.A. and ZANUNCIO, J.C., 2021. Arthropods on Terminalia argentea (Combretaceae) fertilized with sewage sludge. The Florida Entomologist, vol. 104, no. 2, pp. 131-135. https://doi.org/10.1653/024.104.0209
  » https://doi.org/10.1653/024.104.0209
• COSTANZO, N., CESARO, A., DI-CAPUA, F. and ESPOSITO, G., 2021. Exploiting the nutrient potential of anaerobically digested sewage sludge: a review. Energies, vol. 14, no. 23, pp. 1-25. https://doi.org/10.3390/en14238149
  » https://doi.org/10.3390/en14238149
• CRISTINA, G., CAMELIN, E., TOMMASI, T., FINO, D. and PUGLIESE, M., 2020. Anaerobic digestates from sewage sludge used as fertilizer on a poor alkaline sandy soil and on a peat substrate: effects on tomato plants growth and on soil properties. Journal of Environmental Management, vol. 269, pp. 110767. https://doi.org/10.1016/j.jenvman.2020.110767 PMid:32560992.
  » https://doi.org/10.1016/j.jenvman.2020.110767
• DEMOLIN-LEITE, G.L., 2023. Arthropods as possible losses and solutions on Terminalia argentea (Combretaceae) saplings. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 83, e272987. https://doi.org/10.1590/1519-6984.272987 PMid:38018523.
  » https://doi.org/10.1590/1519-6984.272987
• DEMOLIN-LEITE, G.L., 2024. A preliminary study on the occurrence and significance of phytophagous arthropods and natural enemies on Sapindus saponaria saplings. Technology in Agronomy, vol. 4, no. 1, pp. 1-6. https://doi.org/10.48130/tia-0024-0001
  » https://doi.org/10.48130/tia-0024-0001
• DEMOLIN-LEITE, G.L., 2025. Tropical forests. In: G.L. DEMOLIN-LEITE, ed. Innovative conservation techniques and perspectives London: Academic Press, chap. 17, 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
• DEMOLIN-LEITE, G.L., VELOSO, R.V.S., AZEVEDO, A.M., SILVA, J.L., SILVA, L.F., GUANABENS, P.F.S., GOMES, J.B., PEREIRA, W.R., SILVA, R.S. and ZANUNCIO, J.C., 2024. Sucking insects and their predators on tree canopies of a monocultural stand of Caryocar brasiliense. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 84, e253598. https://doi.org/10.1590/1519-6984.253598 PMid:35043835.
  » https://doi.org/10.1590/1519-6984.253598
• DOURADO, L., DEMOLIN-LEITE, G.L., SOARES, M., TEIXEIRA, G., SILVA, F., SAMPAIO, R., ZANUNCIO, J. and LEGASPI, J., 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, e0237261. https://doi.org/10.1371/journal.pone.0237261 PMid:32804957.
  » https://doi.org/10.1371/journal.pone.0237261
• DUBIS, B., JANKOWSKI, K.J., ZAŁUSKI, D. and SOKÓLSKI, M., 2020. The effect of sewage sludge fertilization on the biomass yield of Giant miscanthus and the energy balance of the production process. Energy, vol. 206, pp. 1-13. https://doi.org/10.1016/j.energy.2020.118189
  » https://doi.org/10.1016/j.energy.2020.118189
• EL-SHAFIE, H.A.F., 2022. Impacts of organic farming on insect abundance and diversity. In: H.A.F. EL-SHAFIE, ed. Global decline of insects. London: IntechOpen, pp. 1-11. https://doi.org/10.5772/intechopen.102035
  » https://doi.org/10.5772/intechopen.102035
• FAHMY, N.M., AL-SAYED, E. and SINGAB, A.N., 2015. Genus Terminalia: a phytochemical and biological review. Medicinal & Aromatic Plants, vol. 4, no. 5, pp. 1-21. https://doi.org/10.4172/2167-0412.1000218
  » https://doi.org/10.4172/2167-0412.1000218
• FILLOY, J., OXBROUGH, A., ODDI, J., RAMOS, C., RIBERO, M., SANTOANDRÉ, S. and VACCARO, A., 2023. Understorey structural complexity mediated by plantation management as a driver of predation events on potential eucalypt pests. Forest Ecology and Management, vol. 531, pp. 1-9. https://doi.org/10.1016/j.foreco.2023.120799
  » https://doi.org/10.1016/j.foreco.2023.120799
• GUERRINI, I.A., SAMPAIO, T.F., BOGIANI, J.C., BACKES, C., HARRISON, R.B., OLIVEIRA, F.C., GAVA, J.L., TRABALLI, R.C., MOTA, R.G., RODER, L.R., GRILLI, E., GANGA, A., JAMES, J.N. and CAPRA, G.F., 2021. Sewage sludge as a pedotechnomaterial for the recovery of soils compacted by heavy machinery on Eucalyptus commercial plantation. Journal of Cleaner Production, vol. 325, pp. 1-13. https://doi.org/10.1016/j.jclepro.2021.129320
  » https://doi.org/10.1016/j.jclepro.2021.129320
• HALAJ, J. and WISE, D.H., 2001. Terrestrial trophic cascades: how much do they trickle? The American Naturalist, vol. 157, no. 3, pp. 262-281. https://doi.org/10.1086/319190 PMid:18707289.
  » https://doi.org/10.1086/319190
• IWASHITA, G., YAMAWO, A. and KONDOH, M., 2022. Predator discrimination of prey promotes the predator-mediated coexistence of prey species. Royal Society Open Science, vol. 9, no. 12, pp. 220859. https://doi.org/10.1098/rsos.220859 PMid:36483759.
  » https://doi.org/10.1098/rsos.220859
• KLAUSCHIES, T., VASSEUR, D. and GAEDKE, U., 2016. Trait adaptation promotes species coexistence in diverse predator and prey communities. Ecology and Evolution, vol. 6, no. 12, pp. 4141-4159. https://doi.org/10.1002/ece3.2172 PMid:27516870.
  » https://doi.org/10.1002/ece3.2172
• KOMINKO, H., GORAZDA, K. and WZOREK, Z., 2022. Effect of sewage sludge-based fertilizers on biomass growth and heavy metal accumulation in plants. Journal of Environmental Management, vol. 305, pp. 114417. https://doi.org/10.1016/j.jenvman.2021.114417 PMid:34991023.
  » https://doi.org/10.1016/j.jenvman.2021.114417
• LANDIS, D., WRATTEN, S.D. and GURR, G.M., 2000. Habitat management to conserve natural enemies of arthropod pests in agriculture. Annual Review of Entomology, vol. 45, no. 1, pp. 175-201. https://doi.org/10.1146/annurev.ento.45.1.175 PMid:10761575.
  » https://doi.org/10.1146/annurev.ento.45.1.175
• LANG, A., 2003. Intraguild interference and biocontrol effects of generalist predators in a winter wheat field. Oecologia, vol. 134, no. 1, pp. 144-153. https://doi.org/10.1007/s00442-002-1091-5 PMid:12647191.
  » https://doi.org/10.1007/s00442-002-1091-5
• LANGELLOTTO, G.A. and DENNO, R.F., 2004. Responses of invertebrate natural enemies to complex-structured habitats: a meta-analytical synthesis. Oecologia, vol. 139, no. 1, pp. 1-10. https://doi.org/10.1007/s00442-004-1497-3 PMid:14872336.
  » https://doi.org/10.1007/s00442-004-1497-3
• LEE, J., NAKAMURA, M. and HIURA, T., 2021. Effects of large-scale nitrogen fertilization on insect–plant interactions in the canopy of tall alder trees with N₂-fixing traits in a cool temperate forest. Forests, vol. 12, no. 210, pp. 1-9. https://doi.org/10.3390/f12020210
  » https://doi.org/10.3390/f12020210
• LEITE, G.L.D., TEIXEIRA, D.L., SILVA, C.A.D., LEMES, P.G., TAVARES, W.S., SERRÃO, J.E., ZANUNCIO, J.C. and ZANETTI, R., 2024. Interspecific insect relationships on Terminalia argentea (Myrtales: Combretaceae) trees in the Cerrado biome. Environmental Entomology, vol. 53, no. 2, pp. 230-236. https://doi.org/10.1093/ee/nvae011 PMid:38437574.
  » https://doi.org/10.1093/ee/nvae011
• 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
• LEITE, G.L.D., VELOSO, R.V.D.S., ZANUNCIO, J.C., ALMEIDA, C.I.M.E., FERREIRA, P.S.F., FERNANDES, G.W. and SOARES, M.A., 2012. Habitat complexity and Caryocar brasiliense herbivores (Insecta: Arachnida: Araneae). The Florida Entomologist, vol. 95, no. 4, pp. 819-830. https://doi.org/10.1653/024.095.0402
  » https://doi.org/10.1653/024.095.0402
• LEITE, G.L.D., VELOSO, R.V.D.S., ZANUNCIO, J.C., ALONSO, J., FERREIRA, P.S.F., ALMEIDA, C.I.M. and SERRÃO, J.E., 2016. Diversity of Hemiptera (Arthropoda: Insecta) and their natural enemies on Caryocar brasiliense (Malpighiales: Caryocaraceae) trees in the Brazilian Cerrado. The Florida Entomologist, vol. 99, no. 2, pp. 239-247. https://doi.org/10.1653/024.099.0213
  » https://doi.org/10.1653/024.099.0213
• LIMA, F.B., SOUZA, Á.N., MATRICARDI, E.A.T., GASPAR, R.O., LIMA, I.B., SOUZA, H.J., SANTOS, M.L., MIGUEL, E.P., BORGES, L.A.C., SANTOS, C.R.C., GOUVEIA, F.N. and LIMA, M.F.B., 2024a. Alternative tree species for sustainable forest management in the Brazilian Amazon. Forests, vol. 15, no. 10, pp. 1-14. https://doi.org/10.3390/f15101763
  » https://doi.org/10.3390/f15101763
• LIMA, J.S., LEITE, G.L.D., GUANABENS, P.F.S., SOARES, M.A., SILVA, J.L., MOTA, M.V.S., LEMES, P.G. and ZANUNCIO, J.C., 2024b. Insects and spiders on Acacia mangium (Fabaceae) saplings as bioindicators for the recovery of tropical degraded areas. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 84, e252088. https://doi.org/10.1590/1519-6984.252088 PMid:34755814.
  » https://doi.org/10.1590/1519-6984.252088
• LONGUI, E.L., CUSTÓDIO, G.H., RANZINI, M., SILVA, A.M., FREITAS, M.L.M., CAMBUIM, J., MORAES, M.L.T. and LIMA, I.L., 2024. Wood properties of three South American species planted in consortium. Revista Árvore, vol. 48, no. 1, pp. 1-14. https://doi.org/10.53661/1806-9088202448263803
  » https://doi.org/10.53661/1806-9088202448263803
• LORENZI, H., 2020. Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas do Brasil 8. ed. Nova Odessa: Instituto Plantarum, 384 p.
• MACEDO-REIS, L., QUESADA, M. and NEVES, F., 2019. Forest cover drives insect guild diversity at different landscape scales in tropical dry forests. Forest Ecology and Management, vol. 443, pp. 36-42. https://doi.org/10.1016/j.foreco.2019.04.007
  » https://doi.org/10.1016/j.foreco.2019.04.007
• MATTHEWS, T. and TRIANTIS, K., 2021. Island biogeography. Current Biology, vol. 31, no. 19, pp. 1201-1207. https://doi.org/10.1016/j.cub.2021.07.033 PMid:34637732.
  » https://doi.org/10.1016/j.cub.2021.07.033
• MECH, A.M., LIEBHOLD, A.M., TROMBIK, J., BJÖRKMAN, C., GANDHI, K.J.K., LYYTIKÄINEN-SAARENMAA, P., PURESWARAN, D.S., SYNEK, J. and KLAPIK, M.J., 2024. Island biogeography theory and the assembly patterns of native versus non-native forest insects. Oikos, vol. 2025, no. 3, pp. 1-11. https://doi.org/10.1111/oik.10768
  » https://doi.org/10.1111/oik.10768
• MÉNDEZ-CASTRO, F.E., BADER, M.Y., MENDIETA-LEIVA, G. and RAO, D., 2018. Islands in the trees: a biogeographic exploration of epiphyte-dwelling spiders. Journal of Biogeography, vol. 45, no. 10, pp. 2262-2271. https://doi.org/10.1111/jbi.13422
  » https://doi.org/10.1111/jbi.13422
• MICHALKO, R., PEKÁR, S., DUĽA, M. and ENTLING, M., 2019. Global patterns in the biocontrol efficacy of spiders: a meta‐analysis. Global Ecology and Biogeography, vol. 28, no. 9, pp. 1366-1378. https://doi.org/10.1111/geb.12927
  » https://doi.org/10.1111/geb.12927
• MICHELUTTI, K., SOARES, E., PREZOTO, F. and ANTONIALLI-JÚNIOR, W., 2017. Opportunistic strategies for capture and storage of prey of two species of social wasps of the genus Polybia Lepeletier (Vespidae, Polistinae, Epiponini). Sociobiology, vol. 64, no. 1, pp. 105-110. https://doi.org/10.13102/sociobiology.v64i1.1142
  » https://doi.org/10.13102/sociobiology.v64i1.1142
• MOREIRA, M.D.R., SALES-CAMPOS, H., FONTANARI, C., MEIRELES, A.F.G., PRADO, M.K.B., ZOCCAL, K.F., SORGI, C.A., DA SILVA, C.T., GROPPO, M. and FACCIOLI, L.H., 2020. The ethanolic extract of Terminalia argentea Mart. & Zucc. bark reduces the inflammation through the modulation of cytokines and nitric oxide mediated by the downregulation of NF-κB. Journal of Ethnopharmacology, vol. 261, pp. 1-10. https://doi.org/10.1016/j.jep.2020.113150
  » https://doi.org/10.1016/j.jep.2020.113150
• MOTA, M.V.S., DEMOLIN-LEITE, G.L., GUANABENS, P.F.S., TEIXEIRA, G.L., SOARES, M.A., SILVA, J.L., SAMPAIO, R.A. and ZANUNCIO, J.C., 2023. Chewing insects, pollinators, and predators on Acacia auriculiformis A. Cunn. ex Beth (Fabales: Fabaceae) plants fertilized with dehydrated sewage sludge. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 83, e248305. https://doi.org/10.1590/1519-6984.248305 PMid:34669795.
  » https://doi.org/10.1590/1519-6984.248305
• NELSON, A. and MOONEY, K., 2022. The evolution and ecology of interactions between ants and honeydew-producing hemipteran insects. Annual Review of Ecology, Evolution, and Systematics, vol. 53, no. 1, pp. 379-402. https://doi.org/10.1146/annurev-ecolsys-102220-014840
  » https://doi.org/10.1146/annurev-ecolsys-102220-014840
• OLIVEIRA, A.M.E., WENDLING, B., CARVALHO ERICSSON, D.B., XAVIER, M.A.S. and XAVIER, A.R.E.O., 2020. Métodos de propagação e fatores que interferem na germinação das principais gramíneas nativas de Cerrado. Revista Brasileira de Economia, vol. 12, pp. 1-8. https://doi.org/10.35699/2447-6218.2020.15845
  » https://doi.org/10.35699/2447-6218.2020.15845
• OLIVEIRA, F.M.M., DEMOLIN-LEITE, G.L., VELOSO, R.V.S., GUANÃBENS, R.E.M., SILVA, Y.O.R. and AMARAL, F.L., 2024. Distribution pattern of arthropods and their ecological interactions on the leaf surfaces of Terminalia argentea saplings. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 84, e281588. https://doi.org/10.1590/1519-6984.281588 PMid:38896730.
  » https://doi.org/10.1590/1519-6984.281588
• PEQUENO, P.A.C.L., CAMPOS, C. and BARBOSA, R.I., 2023. Ants offset bottom-up control of spiders in Amazonian savanna trees. Acta Oecologica, vol. 121, pp. 1-7. https://doi.org/10.1016/j.actao.2023.103955
  » https://doi.org/10.1016/j.actao.2023.103955
• PETTORELLI, N., HILBORN, A., DUNCAN, C. and DURANT, S.M., 2015. Individual Variability. Advances in Ecological Research, vol. 52, pp. 19-44. https://doi.org/10.1016/bs.aecr.2015.01.001
  » https://doi.org/10.1016/bs.aecr.2015.01.001
• RANKIN, E., KNOWLTON, J., SHMERLING, A. and HOEY-CHAMBERLAIN, R., 2023. Diets of two non-native praying mantids (Tenodera sinensis and Mantis religiosa) show consumption of arthropods across all ecological roles. Food Webs, vol. 35, pp. 1-11. https://doi.org/10.1016/j.fooweb.2023.e00280
  » https://doi.org/10.1016/j.fooweb.2023.e00280
• RODRIGUES, A., GIULIATTI, N. and JÚNIOR, A., 2020. Application of methodologies for degraded areas recovering in the Brazilian Biomes. Brazilian Journal of Environmental Science, vol. 4, no. 1, pp. 333-369. https://doi.org/10.34115/basrv4n1-021
  » https://doi.org/10.34115/basrv4n1-021
• SAHA, S., SAHOO, D. and SAMANTA, G., 2023. Role of predation efficiency in prey-predator dynamics incorporating switching effect. Mathematics and Computers in Simulation, vol. 209, pp. 299-323. https://doi.org/10.1016/j.matcom.2023.02.017
  » https://doi.org/10.1016/j.matcom.2023.02.017
• SAMPAIO, T.F., GUERRINI, I.A., BACKES, C., HELIODORO, J.C.A., RONCHI, H.S., TANGANELLI, K.M., CARVALHO, N.C. and OLIVEIRA, F.C., 2012. Soil physical characteristics after the application of sewage sludge as soil conditioner. Revista Brasileira de Ciência do Solo, vol. 36, no. 5, pp. 1-9. https://doi.org/10.1590/S0100-06832012000500028
  » https://doi.org/10.1590/S0100-06832012000500028
• SÁNCHEZ-BAYO, F. and WYCKHUYS, K.A.G., 2019. Worldwide decline of the entomofauna: A review of its drivers. Biological Conservation, vol. 232, pp. 8-27. https://doi.org/10.1016/j.biocon.2019.01.020
  » https://doi.org/10.1016/j.biocon.2019.01.020
• SCHMITZ, O.J. and BARTON, B.T., 2013. Climate change effects on behavioral and physiological ecology of predator–prey interactions: implications for conservation biological control. Biological Control, vol. 75, pp. 87-96. https://doi.org/10.1016/j.biocontrol.2013.10.001
  » https://doi.org/10.1016/j.biocontrol.2013.10.001
• SELAYA, N.G. and ANTEN, N.P.R., 2010. Leaves of pioneer and later-successional trees have similar lifetime carbon gain in tropical secondary forest. Ecology, vol. 91, no. 4, pp. 1102-1113. https://doi.org/10.1890/08-2111.1 PMid:20462124.
  » https://doi.org/10.1890/08-2111.1
• SHANNON, D.P., TIANSAWAT, P., DASOON, S., ELLIOTT, S. and PHEERA, W., 2023. Effects of fertilizer on growth and biomass allocation of three evergreen tree species from seasonally dry tropical forests. Trends in Sciences, vol. 20, no. 8, pp. 1-9. https://doi.org/10.48048/tis.2023.6416
  » https://doi.org/10.48048/tis.2023.6416
• SILVA, P.H.M., POGGIANI, F. and LACLAU, J.P., 2011. Applying sewage sludge to Eucalyptus grandis plantations: effects on biomass production and nutrient cycling through litterfall. Applied and Environmental Soil Science, vol. 2011, pp. 1-11. https://doi.org/10.1155/2011/710614
  » https://doi.org/10.1155/2011/710614
• 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
• SILVA, J.L., LEITE, G.L.D., GUANABENS, R.E.M., AZEVEDO, A.M., FERNANDES, G.W. and ZANUNCIO, J.C., 2021. Fertilization with dehydrated sewage sludge affects the phytophagous Hemiptera, tending ants, and Sternorryncha predators on Acacia mangium (Fabaceae). The Annals of Applied Biology, vol. 179, no. 3, pp. 345-353. https://doi.org/10.1111/aab.12706
  » https://doi.org/10.1111/aab.12706
• SOUZA, R.F.A., LEITE, G.L.D., SOARES, M.A., TEIXEIRA, D.L., SILVA, J.L., SAMPAIO, R.A., GUANABENS, R.E.M., SANTOS, M.M., FAUSTINO-JUNIOR, W., SILVA, R.S. and ZANUNCIO, J.C., 2023. Spatial distribution, ecological indices and interactions of arthropods on Sapindus saponaria (Sapindaceae) plants. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 83, e265435. https://doi.org/10.1590/1519-6984.265435 PMid:36700592.
  » https://doi.org/10.1590/1519-6984.265435
• TEIXEIRA, D.L., LEITE, G.L.D., SILVA, L.F., VELOSO, R.V.S., SILVA, R.S., GUANABENS, P.F.S., SILVA, W.M., SILVA-JUNIOR, A.S.P., MUNHOZ, E.J.M.M., GOMES, J.B. and ZANUNCIO, J.C., 2024. Positive relationships between insects and negative with spiders on Acacia auriculiformis (Fabaceae) plants in the savannah biome and their distribution pattern. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 84, e260721. https://doi.org/10.1590/1519-6984.260721 PMid:35674588.
  » https://doi.org/10.1590/1519-6984.260721
• UETZ, G.W., 1991. Habitat structure and spider foraging. In: S.S. BELL, E.D. MCCOY and H.R. MUSHINSKY, eds. Habitat structure Dordrecht: Springer, pp. 325-348. Population and Community Biology Series, no. 8. https://doi.org/10.1007/978-94-011-3076-9_16
  » https://doi.org/10.1007/978-94-011-3076-9_16
• VENTURINI, C.L., DAMAZO, A.S., SILVA, M.J.D., MULLER, J.A.I., OLIVEIRA, D.M., FIGUEIREDO, F.D.F., SERIO, B.F., ARUNACHALAM, K. and MARTINS, D.T.O., 2023. Antiulcer activity and mechanism of action of the hydroethanolic extract of leaves of Terminalia argentea Mart. in different in vivo and in vitro experimental models. Journal of Ethnopharmacology, vol. 318, no. Pt B, pp. 116972. https://doi.org/10.1016/j.jep.2023.116972 PMid:37517568.
  » https://doi.org/10.1016/j.jep.2023.116972
• VENTURINO, E., ISAIA, M., BONA, F., CHATTERJEE, S. and BADINO, G., 2008. Biological controls of intensive agroecosystems: wanderer spiders in the Langa astigiana. Ecological Complexity, vol. 5, no. 2, pp. 157-164. https://doi.org/10.1016/j.ecocom.2007.10.003
  » https://doi.org/10.1016/j.ecocom.2007.10.003
• VIDAL, C.M. and MURPHY, M.S., 2018. Bottom-up vs. top-down effects on terrestrial insect herbivores: a meta-analysis. Ecology Letters, vol. 21, no. 1, pp. 138-150. https://doi.org/10.1111/ele.12874 PMid:29098754.
  » https://doi.org/10.1111/ele.12874
• VIEIRA, D.A., SILVA, P.H.F., MATIAS, R.A.M., VALADÃO, M.B.X., MARTINS, T.O., RIBEIRO, F.P., PINTO, J.R.R. and GATTO, A., 2021. Forest species in ecological restoration of Cerrado vegetation. Scientia Forestalis, vol. 49, no. 132, pp. 1-11. https://doi.org/10.18671/scifor.v49n132.05
  » https://doi.org/10.18671/scifor.v49n132.05
• WIERZBOWSKA, J., SIENKIEWICZ, S. and ZAŁUSKI, D., 2021. Nitrogen fractions in soil fertilized with waste organic materials. Agronomy (Basel), vol. 11, no. 8, pp. 1474. https://doi.org/10.3390/agronomy11081474
  » https://doi.org/10.3390/agronomy11081474
• ZENG, Z.X., SHI, J.H., QIU, C.L., FAN, T., LU, J., ABDELNABBY, H. and WANG, M.Q., 2024. Nitrogen input reduces the physical defense of rice plant against planthopper, Nilaparvata lugens (Hemiptera: delphacidae). Journal of Economic Entomology, vol. 117, no. 6, pp. 2440-2449. https://doi.org/10.1093/jee/toae240 PMid:39436764.
  » https://doi.org/10.1093/jee/toae240

Edited by

• Editor:
  Takako Matsumura Tundisi

Publication Dates

• Publication in this collection
  10 Apr 2026
• Date of issue
  2026

History

• Received
  11 Nov 2025
• Accepted
  25 Feb 2026