Sap-sucking Hemiptera, tending ants, and Sternorrhyncha predators on Acacia auriculiformis saplings fertilized with dehydrated sewage sludge

Hemiptera sugadores de seiva, formigas cuidadoras e predadores de Sternorrhyncha em mudas de Acacia auriculiformis fertilizadas com lodo de esgoto desidratado

Abstract

Soil fertilization with dehydrated sewage sludge accelerates the recovery process of degraded areas, improving nutrient concentration, and favors the development of webs with pioneer plants such as Acacia auriculiformis and insects. This study aimed to evaluate the sap-sucking hemipteran insects, tending ants, and Sternorrhyncha predators in A. auriculiformis saplings fertilized with or without dehydrated sewage sludge, over two years in a degraded area. Acacia auriculiformis saplings fertilized showed higher numbers of sap-sucking Hemiptera Aleyrodidae, Aethalion reticulatum, and Erythrogonia sexguttata, the tending ant Brachymyrmex sp., and the Sternorrhyncha predators Cycloneda sanguinea and Syrphus sp.. Acacia auriculiformis saplings with higher numbers of branches/sapling showed a positive effect on the sap-sucking Hemiptera Achillidae and A. reticulatum and the tending ant Brachymyrmex sp.. The highest numbers of Cephalotes sp., Brachymyrmex sp., and Pheidole sp. were positively associated with those of Aleyrodidae, A. reticulatum, and Membracidae, respectively, in A. auriculiformis saplings. Saplings with high numbers of Cephalotes sp. had low numbers of C. sanguinea. The use of A. auriculiformis, fertilized with dehydrated sewage sludge, is promising in recovering degraded areas due to the increase in sap-sucking Hemiptera, tending ants, and Sternorrhyncha predators. In addition, these ants associated with sap-sucking Hemiptera reduce Sternorrhyncha predators.

Keywords:
fertilization; Formicidae; leafhoppers; natural enemies

Resumo

A fertilização do solo com lodo de esgoto desidratado acelera o processo de recuperação de áreas degradadas, melhorando a concentração de nutrientes e favorecendo o desenvolvimento de teias com plantas pioneiras como Acacia auriculiformis e insetos. Este estudo teve como objetivo avaliar os insetos hemípteros sugadores de seiva, formigas cuidadoras e predadores de Sternorrhyncha em mudas de A. auriculiformis fertilizadas ou não com lodo de esgoto desidratado, ao longo de dois anos, em uma área degradada. As mudas de A. auriculiformis fertilizadas apresentaram maior número de hemípteros sugadores de seiva Aleyrodidae, Aethalion reticulatum e Erythrogonia sexguttata, e da formiga cuidadora Brachymyrmex sp., e os predadores de Sternorrhyncha Cycloneda sanguinea e Syrphus sp.. Mudas de A. auriculiformis com maior número de galhos/muda apresentaram efeito positivo sobre os hemípteros sugadores de seiva Achillidae e A. reticulatum, e sobre a formiga cuidadora Brachymyrmex sp.. Os maiores números de Cephalotes sp., Brachymyrmex sp. e Pheidole sp. foram positivamente associados aos de Aleyrodidae, A. reticulatum e Membracidae, respectivamente, em mudas de A. auriculiformis. Mudas com alto número de Cephalotes sp. apresentaram baixo número de C. sanguinea. O uso de A. auriculiformis, fertilizada com lodo de esgoto desidratado, é promissor na recuperação de áreas degradadas devido ao aumento de hemípteros sugadores de seiva, formigas cuidadoras e predadores do de Sternorrhyncha. Além disso, essas formigas associadas aos hemípteros sugadores de seiva reduzem a população de predadores de Sternorrhyncha.

Palavras-chave:
fertilização; Formicidae; cigarrinhas; inimigos naturais

1. Introduction

Agriculture, among other human activities, degrades natural ecosystems to sustain population and economic growth (Demolin-Leite, 2025). Restoring these areas is a priority, but it still takes time (Amaral et al., 2013; Reis et al., 2015; Demolin-Leite, 2025). Among the Fabaceae species widely used in restoration efforts, is Acacia auriculiformis A. Cunn. ex Beth stands out for its hardiness, rapid growth, 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, increases biomass production, and nutrient cycling via litter, and promotes plant succession (Wang et al., 2013).

Sewage sludge can be applied as fertilizer, mainly in plantations of tree species such as A. auriculiformis and Acacia mangium Willd. (Fabaceae) (Dourado et al., 2020; Silva et al., 2020). Its adequate application in non-edible cropping systems that aim for minimal environmental impact is relevant due to the high levels of concentration of nutrients, pathogens, heavy metals, and persistent organic pollutants (Martins et al., 2016; Caldeira et al., 2018). Due to its significant content of organic matter and nutrients, this fertilizer improves the development of plant species, the physicochemical and biological properties of the soil, and ecological processes (e.g., insect-plant interactions) (Dourado et al., 2020; Silva et al., 2020). Furthermore, sewage sludge, through its nutrients, can impact insect populations where N levels are above or below average, affecting the physiology, diversity, and distribution of phytophagous insects (Dourado et al., 2020; Silva et al., 2020). Insects can cause significant damage to this species such as Aethalion reticulatum (Hemiptera: Aethalionidae), among others (Demolin-Leite, 2022).

Arthropods serve as bioindicators of environmental change due to their rapid responses to ecological changes (Prosser et al., 2016; Pereira et al., 2018). Their population dynamics (e.g., diversity) reflect changes in ecosystem structure (e.g., reduction in plant richness) (Pereira et al., 2018). Phytophagous insects and natural enemies present variables of reproduction, growth, and survival rates, depending on fertilization, plant age, and leaf mass, which influences chemical and nutritional defenses (Bowers and Stamp, 1993; Oliveira et al., 2014). Larger plants can support greater abundance and diversity of arthropods, functioning as biogeographic islands (BGIs), which reduce the extinction risks of rarer species (Burns, 2016; Leite et al., 2017). However, interspecific competition among arthropods can occur through interference (e.g., aggression and 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 and sap-sucking hemipterans, involve protection (e.g., natural enemies) in exchange for honeydew, a food rich in carbohydrates, glucose, fructose, and sucrose, as well as free amino acids, lipids, starch, minerals, and vitamin B (Zanuncio et al., 2015; Araujo et al., 2016).

This study aimed to evaluate the sap-sucking Hemiptera, tending ants, and Sternorrhyncha predators in A. auriculiformis saplings fertilized with or without dehydrated sewage sludge, over two years in a degraded area. The hypotheses tested were that fertilized saplings presented a greater number of sap-sucking Hemiptera, tending ants, and Sternorrhyncha predators (i), and that tending ants associated with sap-sucking Hemiptera reduce Sternorrhyncha predators (ii).

2. Material and Methods

2.1. Experimental site

The study was carried out in a degraded area of the Institute of Agricultural Sciences (ICA) of the Federal University of Minas Gerais (UFMG), Montes Claros city, Minas Gerais State, Brazil (latitude 16°43’41” S, longitude 43°51’54” W, altitude 638 m) from March 2017 to February 2019 (24 months; arthropod collection period). Data on climate, soil type and its physicochemical characteristics, collection and chemical and fecal coliform analyses of dehydrated sewage sludge, data on leaves/branch and branches/saplings of A. auriculiformis fertilized or not with this fertilizer, and soil cover (e.g., litter) are described in Dourado et al. (2020).

2.2. Experimental design

In March 2016, A. auriculiformis seeds were obtained from five-year-old trees grown at the ICA/UFMG. The seedlings were produced in a nursery using plastic bags (8×12 cm) filled with a substrate composed of 30% organic compost, 30% clay soil, 30% sand, and 10% reactive natural phosphate (160 g/hole). The organic compost consisted of three parts by volume: two parts of shredded prunings (≤ 5 cm) and one part of aged manure. The soil pH was corrected with the application of dolomitic limestone, with a relative total neutralization power of 90% (187 g/hole), increasing the base saturation to 50%. In addition, natural phosphate (80 g/hole), fried trace elements (FTE) (10 g/hole), and marble dust (1 kg/hole) were added, according to the nutritional needs of the soil. After six months, the A. auriculiformis saplings, approximately 30 cm tall, were transplanted into 40×40×40 cm holes, with two meters between saplings, distributed in six parallel rows on flat ground. In September 2016, 24 saplings received a single application of 20 L of dehydrated sewage sludge per hole, while the other 24 remained without fertilization. Irrigation was performed twice a week until the beginning of the rainy season when it was suspended. Pruning was performed when the branches reached 5 cm in length, using a sterilized razor for each sapling, cutting the stems and additional branches up to 1/3 of the crown height, leaving out only the best stem. Pruning residues were left between the planting lines. The experiment followed a completely randomized design, with two treatments (with and without dehydrated sewage sludge) and 24 replicates (each replicate is one sapling).

2.3. Insect sampling

Insects were visually counted every two weeks between 7 and 11 a.m. on the adaxial and abaxial surfaces of the leaves, on the apical, middle, and basal parts of the canopy, and in the north, south, east, and west directions, totaling 12 leaves/plant/evaluation, on each of the 48 six-month-old A. auriculiformis saplings, for 24 months. Insects were not removed from the plants during the evaluations. The total sampling effort was 27,648 leaves, covering the entire plant (vertical and horizontal axes), to observe the largest possible number of insect species, especially the rarest ones. At least three specimens per insect species were captured with a vacuum cleaner, stored in glass vials with 70% ethanol or mounted, separated into morphospecies, and sent for identification.

2.4. Statistical analyses

Data on sap-sucking Hemiptera, tending ants, and Sternorrhyncha predators were submitted to the non-parametric statistical hypothesis test, Wilcoxon signed-rank test (P < 0.05) (Wilcoxon, 1946). As the data collected did not present a normal distribution, we chose the non-parametric Wilcoxon test as it is the most powerful test locally among all the classification methods (see Salov, 2014). In addition, simple regression analyses (P < 0.05) were performed to investigate the interactions between these insect groups and the total number of leaves and branches in A. auriculiformis saplings. 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 < 0.05), iii) P < 0.05 and F of the Analysis of Variance of these regressions, and iv) the determination coefficient of these equations (R²).

3. Results

The leaves of A. auriculiformis saplings fertilized with dehydrated sewage sludge showed higher numbers of sap-sucking Hemiptera Aleyrodidae, A. reticulatum, and Erythrogonia sexguttata (Cicadellidae), tending ant Brachymyrmex sp. (Hymenoptera: Formicidae), and Sternorrhyncha predators Cycloneda sanguinea (Coleoptera: Coccinellidae) and Syrphus sp. (Diptera: Syrphidae). On the other hand, the number of Camponotus sp. (Hymenoptera: Formicidae) was higher in unfertilized saplings (Table 1).

Table 1
Number of insects per Acacia auriculiformis saplings (mean ± SE) with and without dehydrated sewage sludge.

Insects	Dehydrated sewage sludge		Wilcoxon test
Order: Family: Species	With	Without	VT **	P
Coleoptera: Cantharidae: Cantharis sp.	0.04 ± 0.04	0.00 ± 0.00	1.00	0.16
Coccinellidae: Cycloneda sanguinea L.	0.17 ± 0.07	0.00 ± 0.00	2.06	0.02
Diptera: Dolichopodidae: N.I.*	1.00 ± 0.24	0.79 ± 0.19	0.48	0.31
Syrphidae: Syrphus sp.	0.25 ± 0.10	0.04 ± 0.04	1.74	0.04
Hemiptera: Achillidae: N.I.	0.08 ± 0.05	0.00 ± 0.00	1.00	0.16
Aleyrodidae: N.I.	3.46 ± 1.87	1.71 ± 1.45	1.67	0.04
Aethalionidae: Aethalion reticulatum L.	1.54 ± 0.80	0.00 ± 0.00	2.07	0.02
Cicadellidae: Acrogonia sp.	0.00 ± 0.00	0.04 ± 0.04	1.00	0.16
Balclutha hebe Kirkaldy	0.50 ± 0.19	0.29 ± 0.18	1.31	0.09
Erythrogonia sexguttata Fabricius	0.17 ± 0.09	0.00 ± 0.00	1.77	0.04
Cicadidae: Quesada gigas Oliver	0.04 ± 0.04	0.04 ± 0.04	0.00	0.50
Coreidae: Leptoglossus sp.	0.04 ± 0.04	0.00 ± 0.00	1.00	0.16
Fulgoridae: N.I.	0.00 ± 0.00	0.04 ± 0.04	1.00	0.16
Membracidae: N.I.	1.13 ± 0.41	0.42 ± 0.15	1.51	0.06
Membracis sp.	0.13 ± 0.06	0.08 ± 0.05	0.47	0.32
Nogodinidae: N.I.	0.04 ± 0.04	0.00 ± 0.00	1.00	0.16
Pentatomidae: N.I.	0.54 ± 0.19	0.46 ± 0.12	0.14	0.44
Scutelleridae: Pachycoris torridus Scopoli	0.50 ± 0.19	0.21 ± 0.13	1.17	0.12
Hymenoptera: Formicidae: Brachymyrmex sp.	8.71 ± 2.86	1.63 ± 0.59	2.24	0.01
Camponotus sp.	3.00 ± 0.65	4.79 ± 0.78	2.15	0.02
Cephalotes sp.	0.13 ± 0.09	0.25 ± 0.25	0.54	0.29
Ectatomma sp.	0.92 ± 0.30	0.67 ± 0.24	0.37	0.36
Pheidole sp.	4.08 ± 1.25	2.88 ± 0.40	0.28	0.39
Pseudomyrmex termitarius Smith.	1.46 ± 0.49	1.13 ± 0.27	0.33	0.37
Neuroptera: Chrysopidae: Chrysoperla sp.	0.08 ± 0.05	0.00 ± 0.00	1.43	0.07

• ^*
  N.I. = non identified;
• ^**
  VT = value of the test. n = 24 per treatment.

The A. auriculiformis saplings with greater numbers of branches/sapling showed a positive effect on the sap-sucking Hemiptera Achillidae and A. reticulatum, and the tending ant Brachymyrmex sp., with the latter also being positively affected by the greater number of leaves/branch (Table 2).

Table 2
Relationships between the numbers of Aleyrodidae, Cephalotes sp. (Cepha), Aethalion reticulatum, Brachymyrmex sp., Balclutha hebe, Membracidae (Membra.), Pseudomyrmex termitarius (Ptermit.), Cycloneda sanguinea, Pheidole sp., Achillidae, number of branches/sapling (Branches), and leaves/branch (Leaves) in Acacia auriculiformis saplings.

Simple regression analysis	ANOVA
	R2	F	P
Aleyrodidae=1.70+4.78xCepha.	0.29	18.32	0.00
Aethalion reticulatum=0.25+0.10xBrachymyrmex sp.	0.14	7.50	0.01
Balclutha hebe=0.05+0.75xMembra.-0.08xMembra.2	0.28	8.74	0.00
Balclutha hebe=0.09+0.49xPtermit.-0.06xPtermit.2	0.15	3.89	0.02
Cycloneda sanguinea=0.06+0.49xCepha.-0.08xCepha.2	0.15	4.07	0.02
Membra.=-0.01+0.03xPheidole sp.	0.22	12.58	0.00
Membra.=0.41-0.28xPtermit.	0.12	6.09	0.01
Membra.=0.64+7.03x√¯Cepha.-3.10xCepha.	0.26	7.99	0.00
Achillidae=1.00-0.06xBranches+0.001xBranches2	0.19	3.53	0.03
Aethalion reticulatum=-1.84+0.07xBranches	0.11	5.84	0.01
Brachymyrmex sp.=-2.92+0.01xLeaves	0.14	7.28	0.00
Brachymyrmex sp.=-4.46+0.26xBranches	0.11	5.66	0.02

• ANOVA. n = 48, degrees of freedom: treatment= 1, repetitions= 23, and residual= 23.

The higher number of Cephalotes sp. (Hymenoptera: Formicidae) positively affected that of Aleyrodidae, but negatively affected those of Membracidae (Hemiptera) and C. sanguinea in A. auriculiformis saplings. The higher number of Brachymyrmex sp. increased that of A. reticulatum; the number of Pheidole sp. (Hymenoptera: Formicidae) increased that of Membracidae, but the number of Pseudomyrmex termitarius (Hymenoptera: Formicidae) reduced those of Balclutha hebe (Hemiptera: Cicadellidae) and Membracidae in the saplings. Saplings with a high number of Membracidae showed a low number of B. hebe (Table 2).

4. Discussion

The leaves of A. auriculiformis saplings fertilized with dehydrated sewage sludge showed higher numbers of sap-sucking Hemiptera (e.g., Aleyrodidae), tending ant Brachymyrmex sp., and Sternorrhyncha predators (e.g., Syrphus sp.). These facts confirm the first hypothesis: fertilized saplings showed higher numbers of these insects. These results corroborate those found in Sapindus saponaria (Sapindaceae) saplings fertilized with these fertilizer-rich nutrients (e.g., N), observing higher numbers of Aleyrodidae and Liriomyza sp. (Diptera: Agromyzidae), abundance and species richness of phytophagous hemipterans, tending ants, spiders, and greater abundance and species richness of Sternorrhyncha predatory compared to unfertilized plants (Silva et al., 2023). The ecological indices of phytophagous arthropods, pollinators, and predators increased in Terminalia argentea (Combretaceae) saplings fertilized with this sludge (Carvalho et al., 2020). The greater amount of proteins and free amino acids in the plant sap, with greater nitrogen fertilization, favors phytophagous arthropods (Taiz et al., 2017; Dourado et al., 2020; Silva et al., 2020, 2023). This reinforces the importance of sewage sludge for fauna recovery, as reported for saplings of A. auriculiformis, A. mangium, S. saponaria, and T. argentea in degraded areas (Carvalho et al., 2020; Dourado et al., 2020; Silva et al., 2020, 2023). Furthermore, the larger canopy of saplings fertilized with dewatered sewage sludge (e.g., >branches/sapling= >A. reticulatum and Brachymyrmex sp.) acts as a biogeographic island, supporting greater diversity and abundance of herbivorous insects, and their natural enemies (Leite et al., 2017), and reducing the extinction of rare species (Burns, 2016; Leite et al., 2017).

The highest numbers of tending ants (e.g., Pheidole sp.) were positively associated with sap-sucking Hemiptera (e.g., Membracidae) in A. auriculiformis saplings. These saplings with higher numbers of Cephalotes sp. had lower numbers of C. sanguinea. These facts confirm the second hypothesis: tending ants, associated with sap-sucking Hemiptera, reduce Sternorrhyncha predators. These facts corroborate those of other studies. The number of Aleyrodidae increased with the number of Cephalotes sp. (2.10%) and of A. reticulatum with that of Brachymyrmex sp. (93.01%), totaling a 95.11% increase in these sap-sucking Hemiptera in A. auriculiformis saplings (Demolin-Leite, 2022). The higher number of Brachymyrmex sp. in S. saponaria saplings fertilized with dehydrated sewage sludge may be due to protocooperation with sap-sucking Aleyrodidae and Phenacoccus sp. and, consequently, to the reduction in the number of C. sanguinea, spiders, and Liriomyza sp. mines in this plant (Silva et al., 2023). The abundance of phytophagous Coleoptera decreased with of phytophagous Hemiptera and tending ants in T. argentea saplings (Carvalho et al., 2020).

However, the greater number of P. termitarius reduced those of B. hebe and Membracidae, that of Cephalotes sp. reduced that of Membracidae, and that of Membracidae reduced that of B. hebe in A. auriculiformis saplings. The P. termitarius was not associated with any sap-sucking Hemiptera, but reduced the number of Cephalocoema sp. (Orthoptera: Proscopiidae) in A. auriculiformis saplings (Demolin-Leite, 2022). The greater number of Tetranychidae and Aleyrodidae reduced that of Liriomyza sp. in S. saponaria saplings (Silva et al., 2023). Eurytoma sp. (Eurytomidae), among the other leaf-galling hymenopterans, dominates more quickly and with greater biotic potential parts of plants or leaves of trees of Caryocar brasiliense Camb. (Caryocaraceae) in cerrado (Leite et al., 2017). Phytophagous hemipterans and tending ants in T. argentea saplings reduced the number of phytophagous beetles, the population of phytophagous orthopterans reduced in response to total predators; and the number of spiders increased proportionally with the number of Liriomyza sp. (Carvalho et al., 2020).

5. Conclusions

Acacia auriculiformis fertilized with dehydrated sewage sludge is promising in recovering degraded areas due to the increase of insects. In addition, tending ants associated with sap-sucking Hemiptera reduce Sternorrhyncha predators. This fact can be a problem in a commercial crop of this Acacia genus.

Acknowledgments

We want to thank Dr. Antônio Domingos Brescovit (Araneae) (“Instituto Butantan”), Ayr de Moura Bello (Coleoptera) (“Laboratório de Biodiversidade Entomológica, Instituto Oswaldo Cruz”), Ivan Cardoso Nascimento (EMBRAPA-ILHÉUS Centro de Pesquisas do Cacau, CEPLAC, Itabuna, BA) (Formicidae), Luci Boa Nova Coelho (Cicadellidae) (Universidade Federal do Rio de Janeiro), and Paulo Sérgio Fiuza Ferreira (Hemiptera) (Universidade Federal de Viçosa) for identifying the collected specimens. Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (302887/2015-6) and Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) (PPM 00080-17).

Data Availability Statement

The entire data set 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 = Revista Brasileira de Biologia, 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
• 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., HÉDOUIN, V., 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
• CALDEIRA, M.V.W., FAVALESSA, M., DELARMELINA, W.M., GONÇALVES, E.O. and MOURA, R.R.S., 2018. Sewage sludge assessment on growth of Acacia mangium seedlings by principal components analysis and orthogonal contrasts. Journal of Plant Nutrition, vol. 41, no. 10, pp. 1303-1311. https://doi.org/10.1080/01904167.2018.1450421
  » https://doi.org/10.1080/01904167.2018.1450421
• 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
• DEMOLIN-LEITE, G.L., 2022. Percentage of importance indice-production unknown: loss and solution sources identification on system. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 84, 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. London: 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, e0237261. https://doi.org/10.1371/journal.pone.0237261 PMid:32804957.
  » https://doi.org/10.1371/journal.pone.0237261
• 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
• MARTINS, M.N.C., SOUZA, V.V. and SOUZA, T.S., 2016. Genotoxic and mutagenic effects of sewage sludge on higher plants. Ecotoxicology and Environmental Safety, vol. 124, pp. 489-496. https://doi.org/10.1016/j.ecoenv.2015.11.031 PMid:26643763.
  » https://doi.org/10.1016/j.ecoenv.2015.11.031
• OLIVEIRA, M.A., GOMES, C.F.F., PIRES, E.M., MARINHO, C.G.S. and DELLA LUCIA, 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
• SALOV, G.I., 2014. On the power of a new statistical test and two-sample Wilcoxon test. Optoelectronics, Instrumentation and Data Processing, vol. 50, no. 1, pp. 36-48. https://doi.org/10.3103/S8756699014010051
  » https://doi.org/10.3103/S8756699014010051
• SILVA, J.L., LEITE, G.L.D., TAVARES, W.S., SILVA, F.W.S., ARRUDA, R.S., 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 a 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., TEIXEIRA, D.L., SAMPAIO, R.A., AZEVEDO, A.M., GUANABENS, P.F.S., ZANUNCIO, J.C., FERNANDES, G.W. and SOARES, M.A., 2023. The association of beneficial and pest arthropods on Sapindus saponaria saplings fertilized with sewage sludge in a degraded area. Phytoparasitica, vol. 51, no. 4, pp. 883-897. https://doi.org/10.1007/s12600-023-01085-8
  » https://doi.org/10.1007/s12600-023-01085-8
• TAIZ, L., ZEIGER, E., MOLLER, I.M. and MURPHY, A., 2017. Fisiologia e desenvolvimento vegetal. Porto Alegre: Artmed.
• 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. 1-2, pp. 207-218. https://doi.org/10.1007/s11104-012-1353-x
  » https://doi.org/10.1007/s11104-012-1353-x
• WILCOXON, F., 1946. Individual comparisons of grouped data by ranking methods. Journal of Economic Entomology, vol. 39, no. 2, pp. 269-270. https://doi.org/10.1093/jee/39.2.269 PMid:20983181.
  » https://doi.org/10.1093/jee/39.2.269
• 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

• Editor:
  Takako Matsumura Tundisi

Publication Dates

• Publication in this collection
  23 Mar 2026
• Date of issue
  2026

History

• Received
  01 Nov 2025
• Accepted
  03 Feb 2026