Distribution pattern of arthropods and their ecological interactions on the leaf surfaces of Terminalia argentea saplings

Padrão de distribuição de artrópodes e suas interações ecológicas nas superfícies foliares de mudas de Terminalia argentea

Abstract

Terminalia argentea tree, native to Brazil, is widely used in landscaping, recovering degraded areas, its wood, coal production, and the bark or leaf extracts has medicinal use. Despite of its importance, the arthropod fauna associated to this plant and its interspecific relationships still needs further studies. The objectives of this study were to evaluate the arthropods, their ecological indices and the distribution in the leaf faces on T. argentea saplings. The numbers of phytophagous insects (e.g., Cephalocoema sp.), pollinators (e.g., Tetragonisca angustula), and natural enemies (e.g., Oxyopidae), and their ecological indices (e.g., species richness), were higher on the adaxial leaf faces on T. argentea saplings. Aggregated distribution of phytophagous insects (e.g., Aphis spiraecola), pollinators (e.g., Trigona spinipes), and natural enemies (e.g., Camponotus sp.) on T. argentea saplings was observed. Abundance, diversity, and species richness of natural enemies correlated, positively, with those of phytophagous and pollinators insects. Predators and tending ants followed their prey and sucking insects, respectively. Tending ants protected sucking insects against predators, and reduced chewing insects. The high number of Cephalocoema sp. on T. argentea saplings is a problem, because this insect can feed on leaves of this plant, but its preference for the adaxial leaf face favors its control. The aggregation behavior of arthropods on T. argentea saplings favors the control of potential pests of this plant. There seems to be competition between tending ants for space and food resources on T. argentea saplings.

Keywords:
Apidae; biodiversity; spiders; Sternorrhyncha

Resumo

Terminalia argentea, árvore nativa do Brasil, é muito utilizada no paisagismo, na recuperação de áreas degradadas, sua madeira na produção de carvão e o extrato da casca ou das folhas tem uso medicinal. Apesar de sua importância, a fauna de artrópodes associada a esta planta e suas relações interespecíficas ainda carecem de estudos mais aprofundados. Os objetivos deste estudo foram avaliar os artrópodes, seus índices ecológicos e a distribuição nas faces foliares de mudas de T. argentea. O número de insetos fitófagos (ex.: Cephalocoema sp.), polinizadores (ex.: Tetragonisca angustula), e inimigos naturais (ex.: Oxyopidae), e seus índices ecológicos (ex.: riqueza de espécies), foram maiores nas faces adaxiais das folhas das mudas de T. argentea. Foi observada uma distribuição agregada de insetos fitófagos (ex.: Aphis spiraecola), polinizadores (ex.: Trigona spinipes) e inimigos naturais (ex.: Camponotus sp.) em mudas de T. argentea. A abundância, diversidade e riqueza de espécies de inimigos naturais correlacionaram-se, positivamente, com as de insetos fitófagos e polinizadores. Os predadores e as formigas cuidadoras seguiram as suas presas e os insetos sugadores, respectivamente. As formigas cuidadoras protegeram os insetos sugadores contra os predadores e reduziram os insetos mastigadores. O elevado número de Cephalocoema sp. em mudas de T. argentea é um problema, pois esse inseto pode se alimentar de folhas dessa planta, mas sua preferência pela face adaxial da folha favorece seu controle. O comportamento de agregação de artrópodes em mudas de T. argentea favorece o controle de potenciais pragas dessa planta. Parece haver competição entre as formigas cuidadoras por espaço e recursos alimentares nas mudas de T. argentea.

Palavras-chave:
Apidae; biodiversidade; aranhas; Sternorrhyncha

1. Introduction

Human action degrades natural ecosystems to maintain its population and economic growth (García‐Orth and Martínez‐Ramos, 2011; Magistrali et al., 2019). The recovery of these areas is a priority but requires time (Amaral et al., 2013; Reis et al., 2015; Silva et al., 2020). Terminalia argentea Mart. (Combretaceae), a secondary plant with up to 8 m high, native to the Southeastern and Central-West regions of Brazil, is widely used in landscaping and to recovering degraded areas (Carvalho et al., 2020). Also, T. argentea is used in wood and coal production and its bark or leaf extracts has medicinal use (Costa et al., 2021). Despite of its importance, the arthropod fauna associated to this plant and its interspecific relationships still needs further studies.

Arthropods can damage different parts of the plant or leaves (adaxial and abaxial faces). The sucking insects prefer the abaxial leaf face due to its softer tissue, thin epidermis and more protruding veins, besides greater protection against natural enemies and climatic factors (e.g., solar radiation) (Leite et al., 2008; Damascena et al., 2017). On the other hand, the arthropods may prefer the adaxial leaf face due to lower force applied to remain on this face (Salerno et al., 2018). The determination of the leaf face preferred by insect pests is important to improving their control (Leite et al., 2008), which is more difficult for those living and feeding on the abaxial leaf surface (Naranjo and Flint, 1995). The distribution of arthropods can be entirely randomly (i); in groups, such as aggregated or contagious distribution (ii); or spread evenly through regular or uniform distribution (iii), and this knowledge is important to sampling plans and pest management (Nickele et al., 2010). Relationships between insects can be intraspecific (within the same species) or interspecific (between species), and can be harmonic, without injuring the individuals involved, or disharmonious, when at least one is harmed (Begon et al., 2007). The harmonic interspecific relationship includes protocooperation, with individuals cooperating with each other, but not depending on each other to survive. The disharmonious relationships include predation (Begon et al., 2007), when one individual kills the other for food, and competition, with disputes over resources such as food, territory, etc (Leite et al., 2012).

The objectives of this study were to evaluate the arthropods, their ecological indices and the distribution (random, regular, or aggregated) in the leaf faces on T. argentea saplings. The three hypothesis were tested: (i) the arthropods may prefer the adaxial leaf face, (ii) the arthropods may prefer the aggregated distribution; and (iii) the arthropods have harmonic (e.g., protocooperation) or disharmonious (e.g., predation) relationships.

2. Material and Methods

2.1. Experimental site

This study was carried out in a degraded area (≈ 1 ha) of the Instituto de Ciências Agrárias - Universidade Federal de Minas Gerais (ICA/UFMG) in the municipality of Montes Claros, Minas Gerais state, Brazil (latitude 16º 51' 38" S, longitude 44º 55' 00" W, altitude 620 m) for 24 months (April 2015 to March 2017). The climate of this area, according to the Köppen classification, is tropical dry, with annual precipitation and temperatures between 1,000 and 1,300 mm and ≥ 24ºC, respectively (Alvares et al., 2013). The soil is Neosol Litolic with an Alic horizon (Silva et al., 2020).

2.2. Experimental design

The T. argentea seedlings were prepared, in March 2014, in a nursery in plastic bags (16 x 24 cm) with reactive natural phosphate mixed with substrate at a dosage of 160g and planted at the same time in September 2014. Each T. argentea seedling was planted in a hole (40 x 40 x 40 cm) when they reached 30 cm high at 2-meter spacing between them. The soil was corrected with dolomitic limestone with the base saturation increased to 50%, natural phosphate, gypsum, FTE (Fried Trace Elements), potassium chloride, and micronutrients based on the soil analysis. A total of 20 L of dehydrated sewage sludge with defined biochemical characteristics (Silva et al., 2020) was placed in a single dose per hole. The 48 T. argentea saplings (young trees in the vegetative period) were irrigated twice a week until the beginning of the rainy season (October). The experimental design was completely randomized with two treatments (adaxial and abaxial leaf faces) with 24 replications, one sapling each.

2.3. Counting the arthropods

The number of arthropods were assessed, and all insects and spiders 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 [sampling unit (n) – one leaf]. Leaves were randomly assessed on the branch (one leaf per position) in the basal, middle, and apical parts of the canopy – vertical axis – (0 to 33%, 34 to 66%, and 67 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 48 T. argentea saplings (age = 12 months) starting six months after transplantation for 24 months (27,648 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 carefully approached, firstly assessing the adaxial leaf surface and, if in the possibility of nor visualizing the abaxial one, the leaf was lifted in a delicate and slow movement, and visualized. Insects with greater mobility (e.g., Orthoptera), that flew on approach were counted if 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 with an aspirator (two hours per week) between transplantation and first evaluation, six months after, stored in flasks with 70% alcohol, separated into morph species, 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 each group (e.g., family).

2.4. Statistical analysis

Each replication was a sapling with the insects collected on 12 leaves (three heights and four sides of the sapling) for 24 months. Ecological indices (abundance, Hill’s diversity, and species richness) were calculated per treatment (leaf surface)/sapling. The ecological indices of arthropods and their numbers were subjected to Wilcoxon test. The type of aggregation (aggregated, random, or regular) of arthropods was defined by the Chi-square test. Interspecific arthropod relationships were subjected to second degree or principal component regressions (PCR) (P< 0.05). The regression model known as PCR, or regression on principal components, uses principal component analysis, based on the covariance matrix, to perform regression (Bair et al., 2006). Thus, it can reduce the regression dimension by excluding the dimensions that contribute to causing multicollinearity problem, that is, linear relationships between the independent variables. The parameters used in these regressions were those significant (P < 0.05) for the selection of the variables for the method ‘‘Stepwise’’. The data presented are statistically significant (P <0.05). The data showed are the significant ones (P <0.05) (Tables 1-3) and the others are in supplementary materials I-II.

Table 1
Number (average ± SE) of phytophagous, pollinators, and natural enemies and theirs ecological indices in the leaf faces on Terminalia argentea/sapling.

Phytophagous and pollinators	Leaf face		WT *
	Abaxial	Adaxial	VT £	P
Coleoptera, Psiloptera sp.	0.06±0.03	0.02±0.02	1.75	0.04
Disonycha brasiliensis	0.02±0.02	0.75±0.28	2.97	0.00
Gynandrobrotica sp.	0.00±0.00	0.02±0.02	4.98	0.00
Parasyphraea sp.	0.02±0.02	0.27±0.10	7.16	0.00
Curculionidae (not identified)	0.08±0.05	0.21±0.08	2.03	0.02
Cratosomus sp.	0.00±0.00	0.04±0.02	2.40	0.01
Hemiptera, Aleyrodidae (not identified)	0.00±0.00	0.21±0.20	1.75	0.04
Mahanarva fimbriolata	0.00±0.00	0.40±0.28	2.26	0.01
Cicadellinae (not identified)	0.02±0.02	0.08±0.04	5.63	0.00
Quesada gigas	0.19±0.07	0.21±0.07	2.03	0.02
Leptoglossus sp.	0.00±0.00	0.02±0.02	2.85	0.00
Membracis sp.	0.00±0.00	0.02±0.02	2.68	0.00
Hymenoptera, Tetragonisca angustula	0.00±0.00	0.04±0.02	1.75	0.04
Lepidoptera (not identified)	0.10±0.05	0.73±0.14	4.14	0.00
Orthoptera, Cephalocoema sp.	0.21±0.13	4.83±0.85	2.68	0.00
Tropidacris collaris	0.17±0.08	1.06±0.23	1.75	0.04
Ecological indices
Abundance of phytophagous	7.65±4.06	9.90±2.27	3.31	0.00
Diversity of phytophagous	1.75±0.36	5.33±1.06	1.90	0.02
Species richness of phytophagous	1.04±0.16	3.50±0.40	4.97	0.00
Abundance of pollinators	0.00±0.00	3.29±0.86	4.80	0.00
Diversity of pollinators	0.00±0.00	0.00±0.00	---	---
Species richness of pollinators	0.00±0.00	0.46±0.08	4.83	0.00
Natural enemies
Araneae, Teudis sp.	0.00±0.00	0.02±0.02	1.75	0.04
Oxyopidae (not identified)	0.08±0.04	2.42±0.56	4.84	0.00
Oxyopes salticus	0.08±0.04	0.19±0.07	2.05	0.02
Salticidae (not identified)	0.04±0.02	0.00±0.00	2.21	0.01
Aphirape uncifera	0.06±0.03	0.02±0.02	1.75	0.04
Leucauge sp.	0.04±0.02	0.13±0.04	2.24	0.01
Aphantochilus rogersi	1.00±0.55	0.23±0.20	4.94	0.00
Hemiptera, Podisus sp.	0.08±0.04	0.40±0.10	4.65	0.00
Hymenoptera, Braconidae (not identified)	0.19±0.10	2.33±0.56	3.85	0.00
Brachymyrmex sp.	0.00±0.00	0.04±0.02	1.69	0.04
Camponotus sp.	0.00±0.00	0.04±0.02	2.03	0.02
Ectatomma sp.	0.02±0.02	1.29±0.26	1.75	0.04
Neuroptera, Chrysoperla sp.	0.04±0.04	0.23±0.08	4.49	0.00
Ecological indices
Abundance of natural enemies	1.71±0.29	17.60±2.33	6.89	0.00
Diversity of natural enemies	2.83±0.55	8.04±1.14	2.68	0.00
Species richness of natural enemies	1.35±0.21	5.06±0.40	6.51	0.00

• ^*
  WT= Wilcoxon test;
• ^£VT= value of test.
• n= 24 per treatment. --- = non generated.

Table 3
Relationships between abundance (Ab.), diversity (D.), and species richness (S.R.) of phytophagous insects (Phy.I.), pollinators (Pol.I.), natural enemies (N.E.), Brachymyrmex sp. (Bra.), Fulgoridae (Fu.), among others, on Terminalia argentea saplings.

Principal component regression equations	R2	F	P
Ab. N.E.= 6,05 + 1,50 x Ab. Pol.I. + 0,13 x Ab. Phy.I.	0.31	20.38	0.00
D. N.E.= 3,93 + 0,43 x D. Phy.I.	0.13	14.33	0.00
S.R. N.E.= 1,18 + 1.94 x S.R. Pol.I. + 0.70 x S.R. Phy.I.	0.67	93.66	0.00
Fu.= -0,03 + 0,06 x P. termitarius + 0,05 x Pheidole sp. + 0,05 x Bra.	0.28	12.13	0.00
Araneidae= 0,18 + 2,18 x Fulg. + 0,20 x T. spinipes	0.23	13.91	0.00
Bra.= 0,93 + 2,01 x Fulg.	0.16	17.34	0.00
Camponotus sp.= 1,99 + 3,20 x Fulg.	0.16	17.17	0.00
Pheidole sp.= 1,03 + 1,74 x Fulg.	0.15	17.07	0.00
P. termitarius= 0,93 x 1,92 x Fulg.	0.14	15.59	0.00
Second-degree regression equations
Lamprosoma sp.= 0,11+0,18xCamponotus sp.-0,01xCamponotus sp.2	0.32	22.07	0.00
Lamprosoma sp.=0,19+0,36xP. termitarius-0,02xP. termitarius2	0.27	17.50	0.00
Diorymerus sp.=0,05+0,41xBra.-0,02xBra.2	0.18	10.00	0.00
Parasyphraea sp.=0,13+0,44xBra.-0,02xBra.2	0.23	14.07	0.00
Dolichopodidae=0,22+0,31xCamponotus sp.-0,01xCamponotus sp.2	0.20	11.42	0.00
Bra.=0,17+0,63xCamponotus sp.-0,02xCamponotus sp.2	0.31	20.69	0.00
Camponotus sp.=0,83+2,11xBra.-0,09xBra.2	0.39	30.17	0.00
Camponotus sp.= 1,22+2,40xP. termitarius -0,16xP. termitarius2	0.25	15.50	0.00
Pheidole sp.=0,61+0,80xBra.-0,03xBra.2	0.26	16.08	0.00
P. termitarius= 0,29+0,0,62xCamponotus sp.-0,02xCamponotus sp.2	0.23	13.52	0.00

• n=48.

3. Results

3.1. Distribution of arthropods on leaf surfaces

The numbers of the phytophagous Coleoptera Disonycha brasiliensis, Gynandrobrotica sp. (Chrysomelidae), Parasyphraea sp. (Chrysomelidae), Cratosomus sp. (Curculionidae), Hemiptera Aleyrodidae, Mahanarva fimbriolata (Cercopidae), Cicadellinae (Cicadellidae), Quesada gigas (Cicadidae), Leptoglossus sp. (Coreidae), and Membracis sp. (Membracidae), Lepidoptera and Orthoptera Cephalocoema sp. (Proscopiidae) and Tropidacris collaris (Romaleidae) were highest on the adaxial leaf faces, resulting in higher ecological indices on T. argentea saplings. The numbers of pollinators Hymenoptera Tetragonisca angustula (Apidae); and natural enemies Araneae Teudis sp. (Anyphaenidae), Oxyopes salticus (Oxyopidae), and Leucauge sp. (Tetragnathidae), Hemiptera Podisus sp. (Pentatomidae), Hymenoptera Braconidae, Brachymyrmex sp., Camponotus sp., and Ectatomma sp. (Formicidae), and Neuroptera Chrysoperla sp. (Chrysopidae) also were biggest on the adaxial leaf faces, resulting in higher ecological indices on these saplings. The numbers of phytophagous Psiloptera sp. (Coleoptera: Buprestidae) and natural enemies Araneae Aphirape uncifera (Salticidae) and Aphantochilus rogersi (Thomisidae) were highest on the abaxial leaf faces. The Cephalocoema sp. was the phytophagous with highest number on T. argentea saplings (Table 1).

3.2. Random, regular or aggregated distribution of arthropods

Phytophagous insects Psiloptera sp., Cerambycidae, Alagoasa sp., Cerotoma sp., Lamprosoma sp. (Coleoptera: Chrysomelidae), Parasyphraea sp., Cratosomus sp., Diorymerus sp. (Curculionidae), and Epitragus sp. (Tenebrionidae); Diptera Liriomyza sp. (Agromyzidae); Hemiptera Aleyrodidae, Aphis spiraecola (Aphididae), M. fimbriolata, Cicadellinae, Fulgoridae, Pentatomidae, and Phenacoccus sp. (Pseudococcidae); and T. collaris and Tettigoniidae showed aggregated distribution. Also pollinators Hymenoptera Apis mellifera and Trigona spinipes (Apidae); and natural enemies Araneae Araneidae, Oxyopidae, A. uncifera, and Uspachus sp. (Salticidae), Coleoptera Cycloneda sanguinea (Coccinellidae) and Photinus sp. (Lampyridae), Diptera Dolichopodidae, Podisus sp., Brachymyrmex sp., Camponotus sp., Cephalotes sp., Ectatomma sp., Pheidole sp., and Pseudomyrmex termitarius (Hymenoptera: Formicidae) showed aggregated distribution. On the other hand, A. uncifera and Hymenoptera Polybia sp. (Vespidae) showed random distribution on T. argentea saplings (Table 2).

Table 2
Random (Ra.) or aggregated (Ag.) distribution of arthropods on Terminalia argentea/saplings.

Phytophagous and pollinators			Chi-square test.
	Var. £	Median	Chi-square	P	Di.
Coleoptera:Psiloptera sp.	0.13	0.06	184.20	0.00	Ag.
Cerambycidae (not identified)	0.08	0.06	115.40	0.02	Ag.
Chrysomelidae, Alagoasa sp.	1.16	0.12	850.00	0.00	Ag.
Cerotoma sp.	0.22	0.15	125.92	0.00	Ag.
Lamprosoma sp.	0.72	0.47	132.00	0.00	Ag.
Parasyphraea sp.	1.99	0.55	309.81	0.00	Ag.
Cratosomus sp.	0.30	0.16	158.00	0.00	Ag.
Diorymerus sp.	2.34	0.43	462.73	0.00	Ag.
Epitragus sp.	0.11	0.07	137.33	0.00	Ag.
Diptera:Liriomyza sp.	2.13	0.22	818.37	0.00	Ag.
Hemiptera: Aleyrodidae (not identified)	9.35	0.69	1158.11	0.00	Ag.
Aphis spiraecola	521.41	4.70	9434.50	0.00	Ag.
Mahanarva fimbriolata	0.13	0.06	184.20	0.00	Ag.
Cicadellinae (not identified)	0.05	0.02	170.00	0.00	Ag.
Fulgoridae (not identified)	0.39	0.19	177.50	0.00	Ag.
Pentatomidae (not identified)	0.30	0.16	158.00	0.00	Ag.
Phenacoccus sp.	1.16	0.12	845.00	0.00	Ag.
Hymenoptera: Apis mellifera	0.31	0.08	324.71	0.00	Ag.
Trigona spinipes	22.01	1.73	1079.82	0.00	Ag.
Orthoptera: Tropidacris collaris	1.87	0.69	231.07	0.00	Ag.
Tettigoniidae (not identified)	0.50	0.31	135.44	0.00	Ag.
Natural enemies
Araneae: Araneidae (not identified)	14.39	0.94	1298.19	0.00	Ag.
Oxyopidae (not identified)	0.20	0.15	112.69	0.02	Ag.
Aphirape uncifera	0.09	0.07	108.67	0.04	Ra.
Uspachus sp.	0.07	0.05	125.00	0.00	Ag.
Coleoptera: Cycloneda sanguinea	0.13	0.06	184.20	0.00	Ag.
Photinus sp.	0.16	0.09	142.50	0.00	Ag.
Diptera: Dolichopodidae (not identified)	2.32	0.73	268.71	0.00	Ag.
Hemiptera:Podisus sp.	0.22	0.08	226.43	0.00	Ag.
Hymenoptera:Brachymyrmex sp.	9.92	1.41	598.98	0.00	Ag.
Camponotus sp.	25.17	2.81	760.15	0.00	Ag.
Cephalotes sp.	0.01	0.01	340.00	0.00	Ag.
Ectatomma sp.	5.08	0.63	688.15	0.00	Ag.
Pheidole sp.	7.45	1.48	428.95	0.00	Ag.
Pseudomyrmex termitarius	9.96	1.40	606.70	0.00	Ag.
Vespidae, Polybia sp.	0.34	0.27	107.87	0.04	Ra.

• ^£Var.= variance;
• Freedom degree = 85.

3.3. Ecological interactions of arthropods

Abundance, diversity, and species richness of natural enemies correlated, positively, with those of phytophagous and pollinators insects. Number of Fulgoridae (Hemiptera) correlated, positively, with those of Brachymyrmex sp., Pheidole sp., and P. termitarius; that of Camponotus sp. that of Fulgoridae; that of Araneidae (Araneae) those of Fulgoridae and T. spinipes. Higher number of Camponotus sp. correlated, negatively, with those of Brachymyrmex sp., Dolichopodidae, Lamprosoma sp., and P. termitarius; that of Brachymyrmex sp. those of Camponotus sp., Diorymerus sp., Parasyphraea sp., and Pheidole sp.; that of P. termitarius those of Camponotus sp. and Lamprosoma sp. (Table 3).

4. Discussion

The greatest numbers of phytophagous (e.g., Cephalocoema sp.), pollinators (e.g., T. angustula), and natural enemies (e.g., Oxyopidae), increased the ecological indices values (e.g., species richness) of these species on the adaxial leaf face of T. argentea saplings, probably, due to the lower force applied by these arthropods to remain on this face compared to the abaxial one (Prüm et al., 2012; Salerno et al., 2018). These facts above confirmed the first hypothesis: the arthropods may prefer the adaxial leaf face. Factors such as wax content, hairiness, roughness, regular shape or not and the type and number of veins in the leaves of host plants can affect the ability of insects to walk, opting for the leaf surface (adaxial or abaxial) that requires lower force applied to the movement (Prüm et al., 2012; Salerno et al., 2018). The leaves of T. argentea have few and very short trichomes, concentrated on the abaxial leaf face (Linsingen et al., 2009), and thus are probably an example of a surface with low contact for insects to fix themselves on it, affecting their abundance on this leaf face.

Aggregate behavior of arthropods on T. argentea is similar to that of other insects, such as Aethalion reticulatum (Hemiptera: Aethalionidae) and Camponotus sp. on Bauhinia forficata (Fabaceae), Acrididae (Orthoptera) in several plants, B. tabaci on Capsicum annuum (Solanales: Solanaceae), Dendroctonus ponderosae (Coleoptera: Curculionidae) on pine and T. spinipes on cucurbits (Bashir and Hassanali, 2010; Serra and Campos, 2010; Barônio et al., 2012; Goodsman et al., 2016; Kim et al., 2017). These results confirmed the second hypotheses: the arthropods may prefer the aggregated distribution. This behavior can increase the local population density of these arthropods (Goff et al., 2009), thus facilitating the acquisition of food and sexual partners and protection against predators; however, it can also result in conflicts (e.g., competition) between them (Goff et al., 2009; Boulay et al., 2019), maybe explaining the random distribution of A. uncifera and Polybia sp. on T. argentea saplings. Aphis spiraecola, with high number on T. argentea, can be a problem because it is a pest of Citrus sp. (Rutaceae) (Kaneko, 2018).

Positive correlation between abundance, diversity, and species richness of natural enemies with phytophagous and pollinators insects on T. argentea saplings was, probably, due to these natural enemies followed these preys as related on Caryocar brasiliense (Caryocaraceae), Leucaena leucocephala (Fabaceae), and Pistacia lentiscus (Anacardiaceae) trees (Auslander et al., 2003; Damascena et al., 2017; Leite et al., 2017). The increase of Araneidae number with those of Fulgoridae and T. spinipes on T. argentea saplings is due to spiders prey insects on insects in natural and agricultural systems (Venturino et al., 2008; Leite et al., 2012, 2016). Reduction in the number of individual Sternorryncha predators (e.g., Dolichopodidae) with increase in that of tending ants is, possibly, due to interactions between tending ants (e.g., Camponotus sp.) with phytophagous Hemiptera (e.g., Fulgoridae) on T. argentea saplings. Trophobiotic interactions between ants (offering protection against natural enemies) and Sternorryncha (supplying sugary food substances) are one of the main mechanisms that maintain the overabundance of ants in ecosystems (Kaminski et al., 2010; Silva and Fernandes, 2016; Klimes et al., 2018), which may decrease the abundance of natural enemies, including Sternorryncha predators (Karami-Jamour et al., 2018; Tong et al., 2019). Number of chewing insects (e.g., Lamprosoma sp.) reduction with increase in that of tending ants (e.g., P. termitarius) on T. argentea saplings. This fact, is, probably, due to for these ants protect sucking insects also of food resource competitors and, consequently, trees have less defoliating by insects, as observed in Fabaceae, Caryocaraceae, Malvacea, Musaceae, and Poaceae family plants, where the greater number of these ants reduced defoliation beetles, miners and caterpillars (Lepidoptera) (Ruberson et al., 1994; Eubanks 2001; Way et al., 2002; Leite et al., 2012). The reduction of Brachymyrmex sp. and P. termitarius numbers with increase that of Camponotus sp.; those of Camponotus sp. and Pheidole sp. that of Brachymyrmex sp.; and that of Camponotus sp. that of P. termitarius on T. argentea saplings indicates possible competition for food and space between these ants confirm our last hipothesis: it has competition among tending ants. This fact was observed between sympatric Paratrechina longicornis (Latreille) and Tetramorium bicarinatum (Nylander) (Hymenoptera: Formicidae) with Tapinoma melanocephalum (Fabricius), the latter with a close mutual relationship with Phenacoccus solenopsis (Hemiptera: Pseudococcidae), by the honeydew of this sucking insect (Liu et al., 2020). The competition, by interference, between T. melanocephalum and P. longicornis interrupted the mutualism of the first species with P. solenopsis and reduced the escape activity of these ants, with aggressiveness, when their workers were in exploratory activity (Liu et al., 2020). The monopolization of resources by an ant species suggests mechanisms of coexistence between dominant and subordinate species as the monopolization suggests this (Houadria and Menzel, 2020). The niche variability of the ant Carebara sp.1 (Hymenoptera: Formicidae), more common, was greater than that of Recurvidris sp.2 (Hymenoptera: Formicidae), with lower monopolization rates. Carebara is more common because it is more competitive than those of Lophomyrmex longicornis Rigato (Hymenoptera: Formicidae) (Houadria and Menzel, 2020). These facts above confirming the third hypothesis: the arthropods have harmonic (e.g., protocooperation) or disharmonious (e.g., predation) relationships on T. argentea saplings.

5. Conclusions

Higher number of Cephalocoema sp. may be a problem on T. argentea saplings because some Proscopiidae species are pests of plants, e.g. Eucalyptus sp. (Myrtaceae) (Flechtmann and Ottati, 1997), but its preference for the adaxial face, facilitates its control. The aggregation behavior of arthropods (e.g., A. spiraecola) on T. argentea saplings also favors the control of those, potentially, pests of this plant. Predators (e.g., Araneidae) and tending ants (e.g., Camponotus sp.) followed their prey (e.g., T. spinipes) and sucking insects (e.g., Fulgoridae), respectively. Tending ants (e.g., P. termitarius) protected sucking insects against predators (e.g., Dolichopodidae), and reduced chewing insects (e.g., Diorymerus sp.). There seems to be competition between tending ants (e.g., Pheidole sp. versus Brachymyrmex sp.) for space and food resources on T. argentea saplings.

Supplementary Material

Supplementary material accompanies this paper.

Supplementary material I. Number (average ± SE) of arthropods in the leaf faces on Terminalia argentea/sapling.

Supplementary material II. Random (Ra.), regular (Re.), or aggregated (Ag.) distribution of arthropods on Terminalia argentea/sapling.

This material is available as part of the online article from https://doi.org/10.1590/1519-6984.281588

Acknowledgements

To the Dr. A.D. Brescovit (Instituto Butantan, São Paulo, Brasil) (Arachnida), Dr. A.M. Bello (Fundação Oswaldo Cruz, Rio de Janeiro, Brasil) (Coleoptera), Dr. C.R.S. Silva (Aphididae) and Dr. A.L.B.G. Peront (Pseudococcidae) (Universidade Federal de São Carlos, São Paulo, Brasil), Dr. C. Matrangolo (UNIMONTES, Minas Gerais, Brasil) (Formicidae), Dr. I.C. Nascimento (EMBRAPA-Ilhéus, Bahia, Brasil) (Formicidae), Dr. L.B.N. Coelho (Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brasil) (Cicadellidae), and Dr. P.S.F. Ferreira (Hemiptera) (Universidade Federal de Viçosa, Minas Gerais, Brasil) by species identifications. This work was supported by the “Conselho Nacional de Desenvolvimento Científico e Tecnológico” (CNPq) [grant number 305057/2018-9] and “Fundação de Amparo à Pesquisa do Estado de Minas Gerais” (FAPEMIG) [grant number PPM-00080-17].

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Publication Dates

• Publication in this collection
  31 May 2024
• Date of issue
  2024

History

• Received
  19 Dec 2023
• Accepted
  15 Apr 2024