Introduction

Plants are primary producers that affect a wide range of different groups of organisms (e.g. phytophagous insects) in terrestrial food webs, providing them food and habitat. They are also present in resource-driven webs in which they provide profound bottom-up effects on higher trophic levels (^{Price 2002}). Terrestrial food webs are composed of at least three interacting trophic levels: plants, herbivores, and natural enemies, and are controlled from the bottom-up via plant nutrition or from the top down via herbivory (^{Price et al. 1980}; ^{Rosemond et al. 1993}). These hypotheses have been tested and empirically studied on two Quercus species, with fertilization used as the bottom-up effect, and the removal of natural enemies as top-down effects (^{Cornelissen and Stiling 2006}). The authors found that fertilization affects herbivores density while the removal of natural enemies did not, suggesting that herbivores are more responsive to bottom-up compared to top-down effects.

Sewage sludge is a by-product from industrial or municipal waste treatment, rich in organic matter and, ideal for soil fertilization or substrate in seedling production (^{Antonkiewicz et al. 2019}; ^{Carvalho et al. 2020}). This wasting product may be used in forest plantations and the recovery of degraded areas, ameliorating the risk of toxic elements entering the human food chain (^{Kimberley et al. 2004}). Sewage sludge has the potential for usage as fertilizer in agriculture, and forests, reducing the production costs, the residual accumulation and environmental problems, and giving it an appropriate destination (^{Caldeira et al. 2014}).

Platycyamus regnellii Benth (Fabaceae) is a native tree in Brazil, distributed in the states of Bahia, Minas Gerais, Espírito Santo, Rio de Janeiro, Paraná, São Paulo, and Goiás, especially in the semi-deciduous highland forests (^{Lorenzi 2008}). This tree species is used in the reforestation of degraded areas and landscaping, ornamentation of parks and gardens (^{Brandão et al. 2002}). Platycyamus regnellii has medicinal properties against fever, maldigestion, and inappetence, and is a proper wood for civil construction, carpentry, and manufacturing (^{Ferreira et al. 2015}).Although there is a broad knowledge on its use as an ecological restorer, and other uses, little is known on the effects of sewage sludge on P. regnellii tree production and there are no studies on arthropods community associated with this tree species. Sewage sludge increases humus content in the soil (^{Silva et al. 2011}; ^{Abreu et al. 2017}) and is rich in phosphorus, nitrogen, macro (Ca, Mg), and micronutrients (Cu and Zn) (^{Nogueira et al. 2007}), which favors the plant development and, consequently, increases ecological indices of phytophagous insects (> biogeographic island - BGI) and their natural enemies (^{Auslander et al. 2003}). Changes in soil fertility may directly affect the nutrition and chemical defenses of the host plant, and this impacts the diversity of phytophagous insects and their natural enemies (^{Cornelissen and Stiling 2006}; ^{Staley et al. 2010}; ^{Graff et al. 2020}). Insects are very susceptible to environmental changes, and such can be useful for monitoring the recovery of degraded areas (^{Burgio et al. 2015}).

While interactions in terrestrial food webs depend on bottom‐up effects on plant and herbivore communities, these interactions and forest productivity are usually structured by mutualism between ants and sap-sucking insects (^{Clark et al.2019}). Ants are an important group of insects that affect the interactions in host plant-herbivore systems in different ways, by attacking herbivores whilst defending the trophobionts; as seen in the positive relationship between ants and herbivores trophobiont richness on Baccharis dracunculifolia DC (Asteraceae) (^{Monteiro et al. 2020}). Trophobiont-tending ants, hereafter, are those who defend hemipterans in exchange for food (honeydew) (^{Freitas and Rossi 2015}).The aim here was to assess leaf mass production and per-centage of ground cover (leaf litter, herbaceous plants, and grasses) of P. regnellii trees fertilized and unfertilized with dehydrated sewage sludge and associated arthropods community on the trees over 24 months. The assumptions in the study were that i) trees fertilized with sewage sludge would have larger canopies, and therefore, an increased ground cover; ii) trees fertilized with sewage sludge would have larger canopies (> BGI) and thus an increased abundance of phytophagous insects and iii) larger trees would have more trophobiont-tending ants and natural enemies attracted by phytophagous insects.

Materials and methods

Results

Discussion

We found that fertilization with dehydrated sewage sludge improved P. regnellii trees leaf mass and ground cover and increased the diversity of trophobiont-tending ants and natural enemies. To our knowledge, this is the first study on the arthropods community associated with this tree species. Dehydrated sewage sludge fertilization favored the development of P. regnellii trees as this organic waste product is rich in nitrogen (^{Nogueira et al. 2007}). Trees fertilized with dehydrated sewage sludge had larger canopy width (> BGI) that results in more food resources for phytophagous insects (^{Ferrier and Price 2004}; ^{Leite et al. 2017}). In our study, the most abundant herbivorous insect was found exclusively on fertilized plants, attracting more trophobiont-tending ants and natural enemies (^{Auslander et al. 2003}) compared to unfertilized trees (as seen in the positive regression).

Platycyamus regnellii trees fertilized with sewage sludge developed better, i.e. they had a higher number of leaves (> 1.4) and branches (> 1.5), and this reflected in a higher percentage of ground cover (> 3.9) compared to unfertilized trees. This confirms the first assumption that fertilization with dehydrated sewage sludge on P. regnellii trees would speed up the recovery process of degraded areas by increasing soil fertility and decrease laminar erosion (^{Franco et al. 2002}). The recovery of degraded areas is a slow process (^{Ferreira et al. 2007}), so the use of fertilization such as organic waste products on P. regnellii trees is promising. In fact, sewage sludge has been broadly used for fertilization of arboreal species such as Araucaria angustifolia (Bertol) Kuntze (Arauca-riaceae), Cedrela fissilis Vell (Meliaceae), Eucalyptus grandis Hill (Myrtaceae), Lafoensia pacari Saint-Hilaire (Lythraceae) and Senna spectabilis Schrad (Fabaceae) (^{Silva et al. 2011}; ^{Abreu et al. 2017}) and also for natural regeneration in riparian forests (^{Campos and Landgraf 2001}).

The fact that twice as many insects were observed on fertilized P. regnellii trees (in absolute numbers) probably was due to the higher amount and quality of leaves, which are food resources to phytophagous insects. This confirms the second assumption that the abundance of hemipterans is usually higher in trees with higher leaf mass (^{Ferrier and Price 2004}; ^{Leite et al. 2017}). Furthermore, the amount of free amino acids and protein in leaf sap usually increases with nitrogen fertilization on trees, thus favoring sucking insects (^{Taiz et al.2017}) such as Phenacoccus sp. (≈ 1.5 insects per tree). Sewage sludge used as biofertilizer is also helpful in the ecological recovery of macrofauna, including larvae and adults of Scarabaeidae (Coleoptera) in degraded areas of Cerrado (^{Kitamura et al. 2008}).

The highest abundance and species richness of trophobiont-tending ants and species richness of total natural enemies, including spiders, were observed on fertilized P. regnellii trees compared to those unfertilized, with a positive correlation between phytophagous (sucking) insects. The results confirm the third assumption that trees with larger canopy width (> BGI) would have more trophobiont-tending ants (e.g. Camponotus sp. and Cephalotes sp.) and natural enemies attracted by sucking insects. This tritrophic interaction among plants => sap-sucking insects => trophobiont-tending ants is one of the most critical interactions found in nature (^{Stadler and Dixon 2005}; ^{Araujo et al. 2016}). The presence of trophobiont-tending ants on P. regnellii trees is likely due to a mutualistic relationship with phytophagous insects such as Hemiptera (^{Stadler and Dixon 2005}; ^{Araujo et al.2016}). Beyond the ecological importance, ants are also used as bioindicators of ecological restoration of degraded areas as they respond quickly to environmental changes (^{Chomicki et al. 2015}).

Platycyamus regnellii fertilized with dehydrated sewage sludge had larger canopy width (higher number of leaves and branches) that favors ground cover. Bigger and leafy trees could present a better resource for phytophagous (sucking) insects, such as hemipterans, which in turn attract a greater abundance and richness of trophobiont-tending ants and richness of species of natural enemies. To our knowledge, this is the first study on arthropods communities associated with this tree species. It suggests that, upon fertilization, P regnellii is an adequate option for the recovery of degraded areas as it developed faster and favored the local biodiversity