Arthropods on Sapindus saponaria (Sapindaceae) saplings as bioindicators for recovery of degraded areaAbstract
Human activities have contributed to various environmental disturbances, including soil degradation, necessitating studies on the restoration of affected areas. The objectives of this study were to evaluate plant biomass production in S. saponaria saplings, assess associated arthropod communities, and analyze their ecological interactions over two years in a degraded area. In the second year after planting, S. saponaria saplings exhibited an increase in the number of leaves/branch. Saplings with higher leaf numbers/branch supported a greater number of Phaneropterinae (Orthoptera: Tettigoniidae) and Brachymyrmex sp. (Hymenoptera: Formicidae), as well as higher abundance, diversity, and species richness of predators of Sternorrhyncha. Additionally, these saplings showed increased defoliation by chewing insects. Conversely, in the first year after planting, sapling leaves harbored higher numbers of herbivorous insects [e.g., Liriomyza sp. (Diptera: Agromyzidae) leaf mines] and greater ecological indices (e.g., species diversity). Similarly, tending ants [e.g., Pheidole sp. (Hymenoptera: Formicidae)] associated with sap-sucking Hemiptera, along with their ecological indices (e.g., species richness), were more abundant in the first year. Predators such as Oxyopidae (Araneae) were also more prevalent during this period. A positive feedback relationship was observed between the species richness of tending ants and that of sap-sucking Hemipterans. Furthermore, the higher number of Pheidole sp. reduced both the abundance and species richness of chewing insects, as well as the percentage of defoliation caused by this group. Similarly, the greater number of Pseudomyrmex termitarius (Hymenoptera: Formicidae) negatively influenced the abundance of chewing insects and the number of Liriomyza sp. mines on S. saponaria leaves.
Keywords:
diversity; ecological interactions; Formicidae; insects; spiders
Resumo
A ação antrópica tem ocasionado diversos problemas, dentre eles, a degradação dos solos e, portanto, sendo necessário estudos que visem recuperar estas áreas. Os objetivos deste trabalho foram estudar a produção de massa vegetal em mudas de S. saponaria, os seus artrópodes e suas interações ecológicas, em dois anos, em uma área degradada. No segundo ano após o plantio, houve aumento no número de folhas/galho nas mudas de S. saponaria. Mudas de S. saponaria com maiores números de folhas/galho apresentaram maiores números de Phaneropterinae (Orthoptera: Tettigoniidae) e de Brachymyrmex sp. (Hymenoptera: Formicidae), de abundância, diversidade e riqueza de espécies de predadores de Sternorrhyncha, e percentagem de desfolha por insetos mastigadores. Os números de insetos herbívoros [(e.g., minas de Liriomyza sp. (Diptera: Agromyzidae)] e seus índices ecológicos (e.g., diversidade de espécies), formigas cuidadoras de Hemiptera sugadores de seiva [(e.g., Pheidole sp. (Hymenoptera: Formicidae)] e seus índices ecológicos (e.g., riqueza de espécies), e de predadores [(e.g., Oxyopidae (Araneae)] foram maiores nas folhas das mudas no primeiro ano de plantio. A maior riqueza de espécies de formigas cuidadoras aumentou a de Hemiptera sugadores de seiva e vice-versa. Os maiores números de Pheidole sp. reduziram a abundância e riqueza de espécies de insetos mastigadores e a percentagem de desfolha por este grupo, e os de Pseudomyrmex termitarius (Hymenoptera: Formicidae) diminuíram a abundância de insetos mastigadores e o número de minas de Liriomyza sp. nas folhas de mudas de S. saponaria.
Palavras-chave:
diversidade; interações ecológicas; Formicidae; insetos; aranhas
1. Introduction
Human activities have led to significant environmental degradation, including the disruption of natural ecosystems (Pörtner et al., 2023; Newton et al., 2024; Demolin-Leite, 2025). To mitigate these detrimental effects and promote ecological recovery, restoration of degraded areas is essential (Demolin-Leite, 2025). A key strategy in this process involves the use of native plant species adapted to local climatic conditions, which exhibit traits such as rapid growth, effective canopy formation, and ground cover capacity (Paula et al., 2018). Besides of this, these plants must produce substantial litter deposition, longevity, well-distributed root systems, and symbiotic associations with diazotrophic bacteria (Paula et al., 2018). Among such species, Sapindus saponaria L. (Sapindaceae) is particularly noteworthy (Calgaro et al., 2015; Silva et al., 2023).
Sapindus saponaria, commonly known as “soldier's soap,” is a tree species distributed across tropical and subtropical regions of Latin America. This species demonstrates high adaptability to diverse edaphic (e.g., soil) and climatic conditions (Lorenzi, 2020; Silva et al., 2023). Its leaves and fruits contain elevated concentrations of saponins and tannins, bioactive compounds that has multiple uses, such as: i) industrial uses (e.g., soap and cosmetic production), ii) medicinal properties (e.g., exhibiting antifungal, anti-inflammatory, treating snakebites, and spermicidal activities), iii) agricultural applications (e.g., allelopathic weed control), iv) bioenergy (e.g., biodiesel production), and v) ecological restoration (e.g., landscaping and reforestation) (Lorenzi, 2020; Silva et al., 2023; Sundar et al., 2024). Besides its ecological and economic value, S. saponaria serves as a host for various insect herbivores (Demolin-Leite, 2024).
Arthropods, the most abundant and taxonomically diverse animal group, occupy diverse ecological niches and play an essential role in the dynamics and functioning of all natural ecosystems (Sánchez-Bayo and Wyckhuys, 2019). In degraded ecosystems, arthropods contribute critically to ecological restoration through their roles as decomposers, herbivores, parasitoids, predators, and pollinators, thereby influencing population dynamics and community structure (Pal et al., 2017; Pereira et al., 2018). Consequently, shifts in arthropod community structure (species richness, abundance, and diversity) and trophic interactions serve as sensitive bioindicators of environmental disturbance and ecosystem health (Pereira et al., 2018; Slivinsky et al., 2019). Supporting this, Souza et al. (2023) demonstrated that the abundance and diversity of herbivorous insects and their natural enemies on S. saponaria saplings, fertilized with sewage sludge, were positively correlated with the numbers of branches, leaves, and canopy architecture. Phytophagous insect populations are particularly influenced by bottom-up controls, including plant age, biomass allocation, secondary metabolite production, nutrient availability, and physical plant traits (Rzanny et al., 2013).
The objectives of this work were to study the biomass production in S. saponaria saplings, associated arthropods and ecological indices (abundance, diversity, and species richness), and their ecological interactions (e.g., predation), in S. saponaria saplings, over two years in a degraded area. Five hypotheses were tested: i) older S. saponaria saplings will exhibit greater biomass production, enhancing degraded area recovery; ii) increased sapling biomass will favor arthropods (Biogeography Island Theory-BGI), iii) younger saplings will experience higher herbivory pressure (due to reduced defensive compounds), resulting in elevated abundance, diversity, and richness of arthropod groups (trophic cascade effect); iv) tending ant number will positively correlate with that of sap-sucking Hemiptera but negatively affect other herbivores and predators; and v) interspecific competition will occur among functional groups (e.g., sap-sucking vs. chewing herbivores).
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 (16°51’38” S, 44°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 S. saponaria saplings 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 2 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), with first-year and second-year post-planting as treatments.
2.3. Arthropod sampling
Arthropods (insects and spiders) were quantified twice monthly between 7:00-11:00 AM via direct visual observation of the first 12 expanded leaves (both the upper and underside of leaf) 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 (12 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, ≤3 specimens per species were aspirated weekly (2 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.
2.4. Sapling biomass 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 S. saponaria saplings.
2.5. Statistical analyses of the ecological indices
Each replication is the total of individuals collected on 12 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 Professional, Version 2 (© 1997 The Natural History Museum: http://www.sams.ac.uk/dml/projects/benthic/bdpro/index.htm) (Krebs, 1989). Abundance and species richness were the total individuals and species per sapling, respectively (Begon et al., 2007). Diversity was calculated using Hill's N1= exp (Shannon-Weaver H’) (Hill, 1973).
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., facultative mutualism) 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 to 3), and the others are in Supplementary Material.
Abundance (Abun.), diversity (D.), and species richness (S.R.) of chewing insects (Chew.), phytophagous Hemiptera (Hem.), tending ants (Ants), Sternorrhyncha predators (Pred.), spiders (Spid.), number of branches/sapling and leaves/branch, percentages of ground cover and defoliation by insects per Sapindus saponaria (Sapindaceae) saplings (mean ± SE) and planting year.
Relationships between abundance (Abun.) of chewing insects (Chew.), phytophagous Hemiptera (Hem.), tending ants (Ants), spiders (Spid.), and Sternorrhyncha predators (Pred.), diversity (D.) of ants, spiders (Spid.), and Pred., species richness (S.R) of ants, Chew., Hem., and Pred., numbers of Aethalium reticulatum (Aret.), Araneidae (Aran.), Brachymyrmex sp. (Brach.), Camponotus sp. (Camp.), Dolichopodidae (Doli.), Fulgoridae (Fulg.), Mantis religiosa (Mrel.), mines of Liriomyza sp. (Lirio.), Nasutitermes sp. (Nasu.), Phenacoccus sp. (Phen.), Pheidole sp. (Phei.), Polybia sp. (Poly.), Pseudomyrmex termitarius (Pter.), Salticidae (Salti.), Tetranychidae (Tetra.), Phaneropterinae (Phan.), Trigona spinipes (Tspi.), Tropidacris collaris (Tcoll.), percentage of defoliation (Def.), branches/sapling (Branches), and leaves/branch (Leaves) per Sapindus saponaria (Sapindaceae) sapling.
3. Results
3.1. Plant mass production
In the second year after planting, S. saponaria saplings exhibited an increase in the number of leaves/branch (Table 1). Saplings with a higher number of leaves/branch showed a greater number of Phaneropterinae (Orthoptera: Tettigoniidae) and Brachymyrmex sp. (Hymenoptera: Formicidae), as well as increased abundance, diversity, and species richness of Sternorrhyncha predators, and percentage of defoliation by chewing insects. Additionally, saplings with more branches/sapling had higher numbers of Brachymyrmex sp. on leaves and Nasutitermes sp. (Blattodea: Termitidae) on trunks (Table 2).
Order, family, and species of mites and spiders (Class Arachnidae) and insects (Class Insecta) per Sapindus saponaria (Sapindaceae) sapling (mean ± SE) and planting year.
3.2. Arthropods and their ecological indices
The numbers of herbivorous insects Cerotoma sp. (Coleoptera: Chrysomelidae), mines of Liriomyza sp. (Diptera: Agromyzidae), Anastrepha sp. (Diptera: Tephritidae), Bemisia sp. (Hemiptera: Aleyrodidae), Pentatomidae (Hemiptera), Tropidacris collaris (Orthoptera: Romaleidae), and Phaneropterinae, abundance, diversity, and species richness of chewing insects, abundance and species richness of sap-sucking Hemipterans, and percentage of defoliation by chewing insects; tending ants of sap-sucking Hemiptera Ectatoma sp., Pheidole sp., and Pseudomyrmex termitarius (Hymenoptera: Formicidae), abundance and species richness of this last group; and the predators Oxyopidae (Araneae) were higher on the leaves of the saplings in the first year of planting. On the other hand, the number of phytophagous arthropods Tetranychidae (Acaridae); xylophagous insect Nasutitermes sp.; tending ants of sap-sucking Hemiptera Camponotus sp. (Hymenoptera: Formicidae); and predators Araneidae (Araneae), and the abundance of spiders were lower in the first year after planting in the S. saponaria saplings (Table 3).
3.3. Ecological relationships among arthropods
The increase in the number of Fulgoridae (Hemiptera) and the diversity of chewing insects increased the diversity of spider species. The greater numbers of predators Dolichopodidae (Diptera) and Salticidae (Araneae) reduced the numbers of Phenacoccus sp. (Hemiptera: Pseudococcidae), and that of Mantis religiosa (Mantodea: Mantidae) reduced the abundance of sap-sucking Hemiptera. The higher species richness of tending ants increased that of sap-sucking Hemiptera and vice versa. Higher numbers of Pheidole sp. reduced the abundance and species richness of chewing insects and the percentage of defoliation by this group, and that of P. termitarius reduced the abundance of chewing insects and the number of Liriomyza sp. mines in the leaves of S. saponaria saplings. The higher numbers of Camponotus sp. reduced those of Tetranychidae on the leaves and Nasutitermes sp. on the trunks of these saplings. Higher numbers of Camponotus sp. reduced the abundance of spiders. However, leaves of S. saponaria saplings with higher numbers of Araneidae had lower numbers of Pheidole sp. and smaller abundance and diversity of tending ants species. Leaves of S. saponaria saplings with high numbers of Phenacoccus sp. and Aethalion reticulatum (Hemiptera: Aethalionidae) had lower chewing insect species richness and percentage defoliation, respectively. Saplings with greater numbers of Phaneropterinae, T. collaris, and Polybia sp. (Hymenoptera: Vespidae) had lower species richness of sap-sucking Hemiptera, and numbers of Phaneropterinae and Trigona spinipes (Hymenoptera: Apidae), respectively (Table 2).
4. Discussion
In the second year after planting, S. saponaria exhibited a significant increase in the number of leaves/branch and a significant trend towards more branches/sapling (p= 0.06). These findings confirm the first hypothesis: older S. saponaria saplings show greater biomass production, enhancing degraded area recovery. Similar patterns have been reported for Acacia mangium and Platycyamus regnellii (Fabaceae), which increased plant biomass and litter production in their second year in degraded environments (Bispo et al., 2023; Lima et al., 2021).
Sapindus saponaria saplings with higher plant production (leaves/branch- higher BGI) supported a greater number of chewing insects (Phaneropterinae), defoliation, xylophagous insects (Nasutitermes sp.), and elevated ecological indices for Sternorrhyncha predators. These results support the second hypothesis: increased sapling biomass favors arthropods (> BGI). In this context, the tree functions as a BGI, harboring a more diverse herbivore-insect community and their natural enemies (e.g., spiders), which benefit from increased prey availability (Leite et al., 2016, 2017; Mota et al., 2021; Silva et al., 2020, 2021; Souza et al., 2023).
The highest numbers of herbivorous insects (e.g., Bemisia sp.), their ecological indices (e.g., species richness), leaf mines, and defoliation and associated tending ants (e.g., Pheidole sp.) and predators (e.g., Oxyopidae) were observed on S. saponaria saplings in their first-year post-planting. These findings support the third hypothesis: younger saplings are more susceptible to herbivory (e.g., due to lower defensive compound concentrations), leading to higher arthropod abundance, diversity, and species richness (a cascading predator-prey effect). During the first year, sewage sludge fertilization (nitrogen-rich) (Wierzbowska et al., 2021) likely accelerated plant growth, increasing leaf palatability and nutritional quality (e.g., free amino acids (Cristina et al., 2020; Lee et al., 2021) while reducing leaf hardness (e.g., lower lignin content (Zeng et al., 2024) and potentially diluting insecticidal compounds (e.g., saponins and trypsin inhibitors - SSTIs (Ibrahim et al., 2011; Macedo et al., 2011; Singh and Kaur, 2018). These changes led to higher herbivore pressure and consequently elevated ecological indices, as documented for A. mangium (Silva et al., 2020) and S. saponaria (Souza et al., 2023) in degraded areas. This aligns with the plant maturation hypothesis: young plants are more vulnerable to herbivory but develop stronger chemical (e.g., saponins) and structural (e.g., leaf thickness) defenses as they mature (Barton and Koricheva, 2010; Castagneyrol et al., 2019). For example, the high number of Bemisia sp. (a sap-sucking hemipteran) in the first year provided honeydew resources for tending ants (e.g., Pheidole sp. (Silva et al., 2021). However, by the second year, reduced fertilization effects and enhanced plant defenses likely decreased sap-sucking insect populations, thereby limiting honeydew availability to tending ants (Barton and Koricheva, 2010; Souza et al., 2023).
The number of Tetranychidae, Nasutitermes sp., Camponotus sp., Araneidae, and the abundance of spiders were higher in the second year after planting the S. saponaria saplings. The rise in Tetranychidae may reflect its tolerance to secondary plant compounds (e.g., saponins) and/or the absence of specialized predators capable of regulating its population. The increase in Nasutitermes sp. likely resulted from accumulated leaf litter, driven by greater leaf production in S. saponaria, which provides a suitable resource for this genus (Issoufou et al., 2019; Ibrahima et al., 2020). Denser, more heterogeneous environments offer enhanced resources (e.g., leaves and wood) and shelter, benefiting herbivores and xylophagous insects (Macedo-Reis et al., 2019). As perennial plants mature, they accumulate biomass and strengthen their defenses (Stiegel et al., 2017). Additionally, a “top-down” effect may occur, where predators (e.g., spiders) regulate herbivore populations (Venturino et al., 2008; Vidal and Murphy, 2018), indicating a more balanced ecosystem (Schmitz and Barton, 2013; Pettorelli et al., 2015). Spiders, as obligate predators, including chewing insects, play a critical role in agroecosystems (Landis et al., 2000; Lang, 2003; Venturino et al., 2008), in native systems (e.g., Caryocar brasiliense trees) (Leite et al., 2012), and in degraded area (e.g., A. mangium saplings) (Silva et al., 2020). Along with productivity gradients, trophic complexity increases, with herbivores alternately limited by resources and primary predators (Letnic and Ripple, 2017).
Higher species richness of tending ants correlated with increased that of sap-sucking Hemiptera. On the other hand, tending ants (e.g., Pheidole sp.) reduced the ecological indices of chewing insects (e.g., abundance) and their defoliation, Diptera leaf mines, and spider abundance. These findings support the fourth hypothesis: tending ants enhances sap-sucking Hemiptera while suppressing other herbivores and predators. This mutualism involves ants obtaining honeydew and food residues from Phenacoccus sp. in exchange for protection, indirectly reducing herbivory (Rosumek et al., 2009; Novgorodova, 2015; Silva et al., 2021). Similar patterns have been observed, including reduced defoliation in A. mangium (Bertuol et al., 2008) and fewer leaf mines in C. brasiliense (Leite et al., 2012), highlighting ants’ potential role in biological control (Gonthier et al., 2013). However, leaves with high Araneidae densities had fewer Pheidole sp. and lower tending ant abundance/diversity on S. saponaria saplings, reflecting intraguild predation dynamics where predators adjust to prey availability (Gagnon et al., 2011; Michalko and Pekár, 2017; Wise et al., 2023). These results align with studies on generalist predators in agroecosystems (Michalko and Pekár, 2017; Sow et al., 2020). Additionally, reduced sap-sucking Hemiptera may benefit plants by minimizing damage and pathogen transmission (Navas-Castillo et al., 2011).
Leaves with high sap-sucking Hemiptera (e.g., Phenacoccus sp.) exhibited lower chewing insect richness and defoliation, whereas saplings with more Phaneropterinae had reduced sap-sucking Hemiptera richness. High T. collaris densities correlated with fewer Phaneropterinae, and frequent Polybia sp. visits reduced Trigona spinipes presence in S. saponaria saplings. These findings confirm the fifth hypothesis: competition occurs both within and between insect groups (e.g., sap-sucking vs. defoliators). Such interactions form mutualistic networks among plants, hemipterans, and ants, shaping community structure (Del-Claro and Oliveira, 2000). Tending ants protect sap-sucking Hemiptera in exchange for honeydew, but when dietary lipids/proteins are scarce, ants may prey on hemipterans (Pérez-Rodríguez et al., 2021). Thus, mutualism stability depends on resource availability and trophobiont density. The inverse relationship between Phaneropterinae and T. collaris suggests intraguild competition, where species with overlapping niches compete for resources (Amarasekare, 2007), potentially leading to competitive exclusion [(e.g., Spodoptera frugiperda (Lepidoptera: Noctuidae) and Ostrinia furnacalis (Lepidoptera: Crambidae)] (Guo et al., 2024). Similarly, Polybia wasps compete with bees for nectar/honeydew, especially under resource scarcity (Corujo et al., 2011; Oliveira et al., 2023).
Supplementary Material
Supplementary material accompanies this paper.
Supplementary material I
This material is available as part of the online article from https://doi.org/10.1590/1519-6984.297895
Acknowledgements
To the taxonomists Dr. Antônio Domingos Brescovit (Instituto Butantan, São Paulo State, Brazil) (Arachnida) and Dr. Ayr de Moura Bello (Oswaldo Cruz Foundation, Rio de Janeiro State, Brazil) (Coleoptera), for their identifications. The voucher numbers are IBSP 36921-36924 (spiders: Instituto Butantan, São Paulo State, Brazil) and for insects 1595/02 and 1597/02 (UFPR-CDZOO, Paraná State, Brazil). To the “Conselho Nacional de Desenvolvimento Científico e Tecnológico” (CNPq), “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior” (CAPES), “Fundação de Amparo à Pesquisa do Estado de Minas Gerais” (FAPEMIG), and “Programa de Proteção Florestal” (PROTEF) by “Instituto de Pesquisas Florestais” for financial support.
Data Availability Statement
The entire dataset supporting the results of this study has been published in the paper itself
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