Arthropods as possible losses and solutions on Terminalia argentea (Combretaceae) saplings

Artrópodes como possíveis fontes de perdas e de soluções em mudas de Terminalia argentea (Combretaceae)

Abstract

Terminalia argentea native tree to Brazil and used in landscaping, wood and coal production, and civil construction, is adapted to poor and dry soils and cultivated in severely disturbed ecosystems. This plant has insecticidal activity, but arthropods can cause damage to its saplings. This study evaluates the herbivorous insects and of their natural enemies on 48 T. argentea saplings which were divided according to the damage they cause or reduce it on these saplings using the percentage of the Importance Index-Production Unknown (% I.I.-P.U.). The Lamprosoma sp., Epitragus sp., Tropidacris collaris, Cerambycidae, Cratosomus sp., Psiloptera sp., Parasyphraea sp., Trigona spinipes, and Aphis spiraecola showed the highest % I.I.-P.U. on leaves of T. argentea. The Aphirape uncifera, Mantis religiosa, Uspachus sp., Podisus sp., and Araneidae, with the highest % I.I.-P.U. on leaves of T. argentea saplings are possible solutions to reduce damage by these pests. These natural enemies can reduce herbivorous insects on T. argentea saplings. However, their populations should be increased, especially spiders. Nevertheless, the Brachymyrmex sp. associated to A. spiraecola, in future T. argentea commercial plantations, can increase populations of sap-sucking insect and, consequently, their damage.

Keywords:
abundance; aggregation; chi-squared test; constancy; frequency

Resumo

Terminalia argentea, árvore nativa do Brasil, é utilizada no paisagismo, produção de madeira e carvão, na construção civil, com adaptação adequada a solos pobres e secos, pode ser utilizada na recuperação de ecossistemas, severamente perturbados. Essa planta tem atividade inseticida, mas artrópodes podem causar danos em suas mudas. Insetos herbívoros e seus inimigos naturais foram avaliados em 48 mudas de T. argentea e classificados, usando a porcentagem do Índice de Importância-Produção Desconhecida (% I.I.-P.U.), de acordo com seus danos ou potencial para reduzir organismos pragas nessas mudas. Lamprosoma sp., Epitragus sp., Tropidacris collaris, Cerambycidae, Cratosomus sp., Psiloptera sp., Parasyphraea sp., Trigona spinipes e Aphis spiraecola apresentaram os maiores % I.I.-P.U. nas folhas de T. argenteae. Aphirape uncifera, Mantis religiosa, Uspachus sp., Podisus sp. e Araneidae, com os maiores % I.I.-P.U. em folhas de mudas de T. argentea, são possíveis soluções por reduzir os danos causados por essas pragas. Esses inimigos naturais podem ser importantes para T. argentea por reduzir as populações de insetos herbívoros em mudas dessa planta. Contudo, suas populações, principalmente as de aranhas, precisam ser aumentadas. No entanto, a associação de Brachymyrmex sp. com A. spiraecola, em futuros cultivos comerciais de T. argentea, pode aumentar os danos por insetos sugadores de seiva.

Palavras-chave:
abundância; agregação; teste qui-quadrado; constância; frequência

1. Introduction

Terminalia argentea Mart. & Zucc. (Myrtales: Combretaceae), a secondary growth deciduous tree, can reach over 8 m. This plant is native to Southeastern and Central-western Brazil is adapted to poor and dry soils and widely used in landscaping, wood and coal production, civil construction, and in programs to recover severely disturbed ecosystems (Lorenzi, 1992). Terminalia argentea is rich in phytochemicals which exudate from its trunk/leaves as gums benefiting visiting insects as Trigona branneri (Crockere, 1912) and Mesembrinella bicolor (Fabricius, 1805) (Hymenoptera: Apidae) (Boff et al., 2008) or with insecticidal activity against pests such as Spodoptera frugiperda (J.E. Smith, 1797) (Lepidoptera: Noctuidae) (Rodrigues et al., 2008). Plants of the genus Terminalia are hosts of insects including species of the genus Lamprosoma (Coleoptera: Chrysomelidae) such as L. seraphinum Lacordaire (after Fiebrig, 1910 and Erber, 1988), L. bicolor W. Kirby, 1818, and L. amethystinum Perty, 1832 (Casari and Teixeira, 2008). Arthropods can cause losses but are also solution sources against pests on T. argentea saplings.

The Importance Index (I.I.) determines the causes of loss and solution sources in a system in specific areas (e.g., agronomy) when the production (e.g., fruits) is known (Demolin-Leite, 2021). The magnitude (numerical measurements), frequencies, and distributions (aggregate, random, or regular) of events and the I.I. bases on this triplet differs (Demolin-Leite, 2021). Usually, the higher the magnitude and frequency of aggregated distribution, greater is the problem or the solution (e.g., natural enemies versus pests) (Demolin-Leite, 2021). The final production of a system is difficult to determine (e.g., degraded area recovery), but a derivation of the I.I. as the percentage of Importance Index-Production Unknown (% I.I.-P.U.) can detect losses and solution sources in systems where the production is unknown (Demolin-Leite, 2024a).

The objective of this study was to determine the sources of losses (e.g., herbivores insects) and solutions (e.g., natural enemies) classifying them according to their importance based on their to damage or as solution source for these damages on 48 T. argentea saplings - system with unknown production.

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).

2.3. Counting the arthropods

The percentage of defoliation (leaf area loss) on a 0–100% scale with 5% increments for leaf area removed (Kogan and Turnipseed, 1980), and the damage score from sap-sucking insects: I = non-damage; II = appearance of yellow chlorotic spots (leaf with 1% to 25% of attack symptoms); III = some yellow chlorotic spots and/or start of black sooty mold (leaf with 26% to 50% of attack symptoms); IV = several yellow chlorotic spots and/or severe blackening of leaves (leaf with 51% to 75% of attack symptoms); and V = yellowing or complete leaf drying (leaf with 76% to 100% of attack symptoms) (Demolin-Leite, 2024a), were assessed visually, 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 number of arthropods on the trunks of these saplings was also assessed in each evaluation. 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).

The definition of what is a loss (L.S.) or solution (S.S.) sources was made by field observation (e.g., leaf damage), feed habits, and literature. This also applied, for prey-predator and sap-sucking insects- tending ant relationships.

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. The distribution type (aggregated, random, or regular) for the L.S. or S.S. was defined by the Chi-square test using the R-package ‘IIProductionUnknown’ (Demolin-Leite and Azevedo, 2022) (Supplementary materials I and II). The data were subjected to simple regression analysis and their parameters were all significant (P< 0.05) using the R-package ‘IIProductionUnknown’ (Demolin-Leite and Azevedo, 2022) (Supplementary material III). The selection of simple equations was based on the criteria: i) data distribution 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 coefficient of determination of these equations (R²). The L.S. and S.S. with P< 0.05 are in the supplementary material III. All the data were used in the Percentage of Importance Index-Production Unknown (% I.I.-P.U.).

Percentage of Importance Index-Production Unknown (% I.I.-P.U.) (Demolin-Leite, 2024a) is: % I.I.-P.U.= [(ks₁ x c₁ x ds₁)/Σ(ks₁ x c₁ x ds₁)+(ks₂ x c₂ x ds₂)+(ks_n x c_n x ds_n)]x100 (Demolin-Leite, 2021), where:

1. the key source (ks) is: ks = damage (non-percentage) (Da.)/total n of the L.S. on the samples or ks = reduction of the total n. of L.S. (R.L.S)/total n. of the S.S on the samples (Demolin-Leite, 2024a), where Da. or R.L.S. = R² x (1 - P), when it is of the first degree, or ((R² x (1 - P))x(β₂/β₁), when it is of the second degree, where R² = determination coefficient and P = significance of ANOVA, β₁ = regression coefficient, and β₂ = regression coefficient (variable²), of the simple regression equation of the loss source (L.S.) or solution source (S.S.) (Demolin-Leite, 2024a).

The separation of Da was separated in two or more L.S. by dividing it among the L.S. as a proportion of their respective “total n”. Da. = 0 when Da. was non-significant for damage or non-detected by L.S. on the system (Demolin-Leite, 2024a). When an S.S. operates in more than one L.S., that caused damage, its ks are summed. R.L.S. = 0 when Da. by L.S. or R.L.S. was non-significant for damage by L.S. or reduced L.S. by S.S. on the system (Demolin-Leite, 2024a).

1. c (constancy) = Σ of occurrence of L.S. or S.S. on samples, where absence = 0 or presence = 1 (Demolin-Leite, 2021).

2. ds (distribution source) = 1 - P of the chi-square test of L.S. or S.S. on the samples (Demolin-Leite, 2021). Counts (non-frequency) of L.S. or S.S. are used to perform the chi-square test.

These data, above, are obtained, by R-package ‘IIProductionUnknown’ (Demolin-Leite and Azevedo, 2022).

Percentage of R.L.S. per S.S. (%R.L.S.S.S.) = (R.L.S.S.S./total n of the L.S. – abundance or damage) x 100, where R.L.S.S.S. = R.L.S. x total n of the S.S., with the R.L.S. not being summed in this case (Demolin-Leite, 2024a). These data, above, are obtained, by R-package ‘IIProductionUnknown’ (Demolin-Leite and Azevedo, 2022).

3. Results

The loss sources with the highest % I.I.-P.U. on leaves of T. argentea saplings were: Lamprosoma sp. (23.78%), Epitragus sp. (Coleoptera: Tenebrionidae) (19.01%), Tropidacris collaris Stoll. 1813 (Orthoptera: Romaleidae) (14.97%), non-identified Cerambycidae (Coleoptera) (11.42%), Cratosomus sp. (Coleoptera: Curculionidae) (9.94%), Psiloptera sp. (Coleoptera: Buprestidae) (9.51%), Parasyphraea sp. (Coleoptera: Chrysomelidae) (4.46%), Trigona spinipes (Fabr. 1793) (Hymenoptera: Apidae) (3.95%), and Aphis spiraecola Patch 1914 (Hemiptera: Aphididae) (2.23%) (maximum damage score = III), among 40 herbivorous arthropods (≈ 0.02%) (Table 1).

Table 1
Total number (n), damage (Da.), key-source (ks), constancy (c), distribution source (ds), number of importance indices (n. I.I.), sum of n. I.I.-P.U. (Σ n. I.I.), and percentage of I.I. by loss source (L.S.) on 48 Terminalia argentea (Combretaceae) saplings.

Loss source
L.S.	n	Da.	ks	c	ds	n. I.I.	Σ n. I.I.	% I.I.
Lamprosoma sp.	42	0.3110	0.0074	23	0.99	0.1694	0.712	23.78
Epitragus sp.	8	0.1906	0.0238	6	0.95	0.1354	0.712	19.01
T. collaris	63	0.2489	0.0040	27	1.00	0.1067	0.712	14.97
Cerambycidae	6	0.1128	0.0188	5	0.87	0.0813	0.712	11.42
Cratosomus sp.	27	0.2389	0.0088	8	1.00	0.0708	0.712	9.94
Psiloptera sp.	5	0.1129	0.0226	3	1.00	0.0677	0.712	9.51
Parasyphraea sp.	47	0.1066	0.0023	14	1.00	0.0318	0.712	4.46
T. spinipes	248	0.4110	0.0017	17	1.00	0.0282	0.712	3.95
A. spiraecola	404	0.8010	0.0020	8	1.00	0.0159	0.712	2.23
Tettigoniidae	28	0.0028	0.0001	18	1.00	0.0018	0.712	0.25
Clytrini	19	0.0019	0.0001	16	0.39	0.0006	0.712	0.09
Cerotoma sp.	13	0.0013	0.0001	8	1.00	0.0008	0.712	0.11
Diorymerus sp.	37	0.0037	0.0001	8	1.00	0.0008	0.712	0.11
Lepidoptera	8	0.0008	0.0001	8	0.24	0.0002	0.712	0.03
D. speciose	4	0.0004	0.0001	4	0.40	0.0002	0.712	0.02
D. brasiliensis	5	0.0005	0.0001	5	0.36	0.0002	0.712	0.02
Walterianela sp.	3	0.0003	0.0001	3	0.44	0.0001	0.712	0.02
Wanderbiltiana sp.	3	0.0003	0.0001	3	0.44	0.0001	0.712	0.02
Alagoasa sp.	10	0.0010	0.0001	1	1.00	0.0001	0.712	0.01
Cephalocoema sp.	4	0.0004	0.0001	1	1.00	0.0001	0.712	0.01
Curculionidae	1	0.0001	0.0001	1	0.53	0.0001	0.712	0.01
Eumolpus sp.	1	0.0001	0.0001	1	0.53	0.0001	0.712	0.01
Gryllidae	1	0.0001	0.0001	1	0.53	0.0001	0.712	0.01
Gynandrobrotica sp.	1	0.0001	0.0001	1	0.53	0.0001	0.712	0.01
Lordops sp.	1	0.0001	0.0001	1	0.53	0.0001	0.712	0.01
Aleyrodidae	59	0.0000	0.0000	6	1.00	0.0000	0.712	0.00
B. hebe	2	0.0000	0.0000	2	0.49	0.0000	0.712	0.00
Cicadellinae	2	0.0000	0.0000	1	1.00	0.0000	0.712	0.00
E. sexguttata	2	0.0000	0.0000	2	0.49	0.0000	0.712	0.00
Euxesta sp.	10	0.0000	0.0000	7	1.00	0.0000	0.712	0.00
Fulgoridae	64	0.0000	0.0000	18	1.00	0.0000	0.712	0.00
Leptoglossus sp.	1	0.0000	0.0000	1	0.53	0.0000	0.712	0.00
Liriomyza sp.	19	0.0000	0.0000	2	1.00	0.0000	0.712	0.00
M. fimbriolata	5	0.0000	0.0000	3	1.00	0.0000	0.712	0.00
Membracidae	3	0.0000	0.0000	3	0.44	0.0000	0.712	0.00
Membracis sp.	1	0.0000	0.0000	1	0.53	0.0000	0.712	0.00
Nasutitermes sp.	100	0.0000	0.0000	2	1.00	0.0000	0.712	0.00
Pentatomidae	15	0.0000	0.0000	8	1.00	0.0000	0.712	0.00
Phenacoccus sp.	10	0.0000	0.0000	1	1.00	0.0000	0.712	0.00
Q. gigas	4	0.0000	0.0000	4	0.40	0.0000	0.712	0.00

• I.I.-P.U. = ks x c x ds. ks = Da./total n of the L.S.. Da. = R² x (1 - P) when it is of the first degree, or ((R² x (1 - P))x(β₂/β₁) when it is of the second degree, where ² = determination coefficient and P = significance of ANOVA, β₁ = regression coefficient, and β₂ = regression coefficient (variable²), of the simple regression equation, or non-percentage of damage per L.S.. c = Σ of occurrence of L.S. on each sample, 0 = absence or 1 = presence. ds = 1 - P of chi-square test of the L.S.. Da. = 0 when Da. non-significant for damage or non-detected by L.S..

The solution sources with the highest % I.I.-P.U. on leaves of T. argentea saplings were: Aphirape uncifera Tullgren 1905 (Araneae: Salticidae) (50.96%), Mantis religiosa L. 1758 (Mantodea: Mantidae) (26.86%), Uspachus sp. (Araneae: Salticidae) (12.79%), Podisus sp. (Hemiptera: Pentatomidae) (5.45%), non-identified Araneidae (Araneae) (2.17%), and the tending ants Ectatoma sp. (0.88%), Brachymyrmex sp. (0.53%), and Pheidole sp. (0.37%) among 26 natural enemies (= 0.00%). The numbers of M. religiosa reduced those of Wanderbiltiana sp. (Coleoptera: Chrysomelidae) (50.26%); those of Araneidae those of Cephalocoema sp. (Orthoptera: Proscopiidae) (27.04%), Psiloptera sp. (17.19%), and Cratosomus sp. (2.10%) (a total reduction of 46.33%), and A. uncifera decreased those of Alagoasa sp. (Coleoptera: Chrysomelidae) (7.00%), Disonycha brasiliensis Costa Lima 1954 (Coleoptera: Chrysomelidae) (9.38%), and Diorymerus sp. (Coleoptera: Curculionidae) (1.21%) (a total reduction of 17.59%). Similar effects were observed between the numbers of Uspachus sp. and Camponotus sp. in relation to that of Lamprosoma sp. (0.63 and 3.86% of reduction, respectively). The numbers of Podisus sp. and Ectatoma sp. reduced those of T. spinipes and Cerambycidae in 0.10 and 11.65%, respectively. The numbers of Pheidole sp. decreased those of T. collaris, non-identified Tettigoniidae (Orthoptera) in 1.03% and 2.95% and those of Brachymyrmex sp. that of Parasyphraea sp. in 2.70%, respectively. However, the numbers of Brachymyrmex sp. increased the damage by A. spiraecola (69.65%) on T. argentea saplings (Tables 2 and 3).

Table 2
Total number (n), reduction of L.S. (R.L.S.), key-source (ks), constancy (c), distribution source (ds), number of importance indices (n. I.I.), sum of n. I.I.-P.U. (Σ n. I.I.), and percentage of I.I. by solution source (S.S.) on 48 Terminalia argentea (Combretaceae) saplings.

Solution source
S.S.	n	R.L.S.	ks	c	ds	n. I.I.	Σ n. I.I.	% I.I.
A. uncifera	6	0.2692	0.04487	5	0.86	0.193	0.379	50.96
M. religiosa	10	0.1508	0.01508	7	0.96	0.102	0.379	26.86
Uspachus sp.	4	0.0664	0.01661	3	0.97	0.048	0.379	12.79
Podisus sp.	7	0.0362	0.00517	4	1.00	0.021	0.379	5.45
Araneidae	82	0.0306	0.00037	22	1.00	0.008	0.379	2.17
Ectatoma sp.	58	0.0120	0.00021	16	1.00	0.003	0.379	0.88
Brachymyrmex sp.	136	0.0093	0.00007	29	1.00	0.002	0.379	0.53
Pheidole sp.	183	0.0080	0.00004	32	1.00	0.001	0.379	0.37
A. rogersi	4	0.0000	0.00000	4	0.40	0.000	0.379	0.00
Braconidae	2	0.0000	0.00000	2	0.49	0.000	0.379	0.00
C. sanguinea	5	0.0000	0.00000	3	1.00	0.000	0.379	0.00
Camponotus sp.	307	0.0000	0.00000	42	1.00	0.000	0.379	0.00
Cephalotes sp.	1	0.0000	0.00000	1	0.53	0.000	0.379	0.00
Chrysoperla sp.	5	0.0000	0.00000	5	0.36	0.000	0.379	0.00
Dolichopodidae	64	0.0000	0.00000	26	1.00	0.000	0.379	0.00
Leucauge sp.	3	0.0000	0.00000	3	0.44	0.000	0.379	0.00
O. salticus	2	0.0000	0.00000	2	0.49	0.000	0.379	0.00
Oxyopidae	14	0.0000	0.00000	12	0.77	0.000	0.379	0.00
P. termitarius	125	0.0000	0.00000	26	1.00	0.000	0.379	0.00
Photinus sp.	8	0.0000	0.00000	5	1.00	0.000	0.379	0.00
Polybia sp.	23	0.0000	0.00000	17	0.75	0.000	0.379	0.00
Quemedice sp.	4	0.0000	0.00000	4	0.40	0.000	0.379	0.00
Salticidae	19	0.0000	0.00000	14	0.76	0.000	0.379	0.00
Syrphus sp.	5	0.0000	0.00000	5	0.36	0.000	0.379	0.00
Teudis sp.	1	0.0000	0.00000	1	0.53	0.000	0.379	0.00
Tmarus sp.	2	0.0000	0.00000	2	0.49	0.000	0.379	0.00

• I.I.-P.U. = ks x c x ds. ks = R.L.S./total n. of the S.S.. R.L.S.= R² x (1 - P) when it is of the first degree, or ((R² x (1 - P))x(β₂/β₁) when it is of the second degree, where ² = determination coefficient and P = significance of ANOVA, β₁ = regression coefficient, and β₂ = regression coefficient (variable²), of the simple regression equation. c = Σ of occurrence of S.S. on each sample, 0 = absence or 1 = presence. ds = 1 - P of chi-square test of the S.S.. When a S.S. operates in more than one L.S., that caused damage, its ks are summed. E.S.. = 0 when Da. by L.S. or E.S. non-significant for damage by L.S. or reduced L.S. by S.S..

Table 3
Percentage of reduction in abundance and/or damage (%R.) of loss source (L.S.) per solution source (S.S.), sum (Σ), and total of Σ of R.L.S. (T.Σ) on 48 Terminalia argentea (Combretaceae) saplings.

	%R.L.S.S.S.- abundance
	Solution sources
Loss sources	Araneidae	A. uncifera	Uspachus sp.	Podisus sp.	Brachymyrmex sp.	Camponotus sp.	Ectatoma sp.	Pheidole sp.	M. religiosa	* T.Σ
Alagoasa sp.	---	7.00	---	---	---	---	---	---	---	7.00
Lamprosoma sp.	---	---	0.63	---	---	3.86	---	---	---	4.49
Parasyphraea sp.	---	---	---	---	2.70	---	---	---	---	2.70
Wanderbiltiana sp.	---	---	---	---	---	---	---	---	50.26	50.26
D. brasiliensis	---	9.38	---	---	---	---	---	---	---	9.38
Diorymerus sp.	---	1.21	---	---	---	---	---	---	---	1.21
Psiloptera sp.	17.19	---	---	---	---	---	---	---	---	17.19
Cratosomus sp.	2.10	---	---	---	---	---	---	---	---	2.10
Cerambycidae	---	---	---	---	---	---	11.65	---	---	11.65
T. spinipes	---	---	---	0.10	---	---	---	---	---	0.10
Cephalocoema sp.	27.04	---	---	---	---	---	---	---	---	27.04
T. collaris	---	---	---	---	---	---	---	1.03	---	1.03
Tettigoniidae	---	---	---	---	---	---	---	2.95	---	2.95
*T.Σ	46.33	17.59	0.63	0.10	2.70	3.86	11.65	3.98	50.26	137.1
	%R.L.S.S.S.- damage
Loss sources	Solution sources
	Brachymyrmex sp.
A. spiraecola	-69.65

• --- = L.S. was not reduced per S.S. %R.L.S.S.S. = (R.L.S.S.S./total n of the L.S. – abundance or damage) x 100, where R.L.S.S.S. = R.L.S. x total n of the S.S.. R.L.S. = R² x (1 - P) when it is of the first degree, or ((R² x (1 - P))x(β₂/β₁) when it is of the second degree, where ² = determination coefficient and P = significance of ANOVA, β₁ = regression coefficient, and β₂ = regression coefficient (variable²), of the simple regression equation.
• ^*
  T.Σ = total of Σ of R.L.S.

4. Discussion

The loss sources Lamprosoma sp., Epitragus sp., T. collaris, Cerambycidae, Cratosomus sp., Psiloptera sp., Parasyphraea sp., T. spinipes, and A. spiraecola on leaves of T. argentea saplings presented the highest % I.I.-P.U. The genus Lamprosoma includes L. seraphinum on Teminalia hassleriana Chod. (Myrtales: Combretaceae), L. bicolor and L. amethystinum on Terminalia catappa L. (Myrtales: Combretaceae), L. chorisiae Monrós 1948 on Chorisia speciosa A. St.-Hil. and C. insignis Kunth. (Malvales: Malvaceae) plants, and L. azureum Germar 1824 on Psidium cattleianum Sabine (Myrtales: Myrtaceae) plants (Casari and Teixeira, 2008), and Lamprosoma sp. on Acacia mangium Willd. (Fabales: Fabaceae) saplings (Silva et al., 2020; Demolin-Leite, 2024a). Epitragus sp. was observed on A. mangium saplings (Silva et al., 2020; Demolin-Leite, 2024a) and E. sallaei (Champion 1884) on Mangifera indica L. (Sapindales: Anacardiaceae) (Cruz-Lopez et al., 2001). Tropidacris collaris damages on T. argentea saplings confirms its polyphagy because it was reported damaging Acacia auriculiformis (Fabales: Fabaceae), A. mangium Willd., Azadirachta indica A. Juss. (Sapindales: Meliaceae), Casuarina glauca Sieber (Casuarinales: Casuarinaceae), Leucaena leucocephala (Lam.) de Wit (Fabales: Fabaceae), and Platycyamus regnellii (Benth) (Fabales: Fabaceae) plants (Poderoso et al., 2013; Damascena et al., 2017; Silva et al., 2020; Demolin-Leite, 2022a,b, 2023, 2024a; Mota et al., 2023). Many Cerambycidae species are pests [e.g., Anoplophora chinensis (Forster 1771)], on some plants [e.g., Citrus spp.(Sapindales: Rutaceae)] girdling and detaching branches and tree trunks for oviposition (Lemes et al., 2015; Herard and Maspero, 2019.). These insects were observed on A. mangium and A. auriculiformis leaves (Silva et al., 2020; Mota et al., 2023; Demolin-Leite, 2023, 2024a). Oncideres saga (Dalman 1823) and Acanthophorus confinis (Castelnau 1840) are important pests of Stryphnodendron adstringens (Mart.) Coville (Fabales: Fabaceae) (Soares et al., 2022) and of Acacia senegal (Hasbab), and Acacia seyal (Talh) (Fabales: Fabaceae) plants, respectively (Jamal, 1994). Cratosomus sp. damages Annona muricata L. (Magnoliales: Annonaceae) (Sobrinho et al., 1999) and it was found, at low densities, on A. auriculiformis saplings (Mota et al., 2023; Demolin-Leite, 2024a). Psiloptera sp., a pest on Acacia senegal (Hasbab) and Acacia seyal (Talh) (Fabales: Fabaceae) (Jamal, 1994), was found in low numbers on A. mangium saplings (Silva et al., 2020; Demolin-Leite, 2023). Parasyphraea sp. was reported in high numbers on A. mangium (≈0.30/tree) and A. auriculiformis (≈0.80/tree) saplings (Silva et al., 2020; Mota et al., 2023). Trigona spinipes damages shoots and plant growth by removing fibers to build nests, as reported on A. mangium, A. indica, and L. leucocephala (Damascena et al., 2017; Silva et al., 2020; Demolin-Leite, 2022a, 2023). This bee also damaged the flowers of Zantedeschia aethiopica (L.) Spreng. (Commelinales: Araceae) plants and Caryocar brasiliense Camb. (Malpighiales: Caryocaraceae) trees (Carvalho et al., 2018; Demolin-Leite, 2024b). In addition, it can reduce pollination on Cucurbita moschata Dusch (Cucurbitales: Cucurbitaceae) plants due to insufficient pollen transportation (small body size) and/or chasing other pollinators by flying in flocks and with aggressive behavior (Serra and Campos, 2010) which has been led to the destruction of its nest (Demolin-Leite, 2024b). A. spiraecola damages Baccharis trimera (Less.) DC. and Calendula officinalis L. (Asterales: Asteraceae), and Citrus sp. grunting of new leaves and sooty mold production from honeydew deposition resulting in lower photosynthetic activity (Leite et al., 2011; Wäckers et al., 2017; Kaneko, 2018), as reported for T. argentea saplings in this study.

The 65% of reduction in loss sources (e.g., Psiloptera sp.) on leaves of T. argentea saplings by spiders (e.g., A. uncifera) as the main solution sources, confirms the importance of these predators on A. auriculiformis, A. mangium, and P. regnellii saplings in Brazilian degraded areas (Silva et al., 2020; Demolin-Leite, 2022b, 2023, 2024a; Mota et al., 2023; Lima et al., 2024); against coleopteran defoliators on C. brasiliense trees in the Brazilian Cerrado (Leite et al., 2012a, b) and Orthoptera (Greek pastures and forests); and other agroecosystem in Europe and USA (Landis et al., 2000; Öberg et al., 2008; Venturino et al., 2008; Zografou et al., 2017). Mantis religiosa, a generalist predator negatively impacted the beetle Wanderbiltiana sp. and, in general, it decreased biomass and numbers of other arthropods, except herbivorous Miridae (Hemiptera). It probably happens due to an indirect effect (Fagan and Hurd, 1994), maybe a greater free space. The impact of Tenodera sinensis (Saussure, 1871) (Mantodea: Mantidae) is usually displayed weaker on arthropod density compared to of M. religiosa, but it is more frequent (Fagan et al., 2002). The negative impact of Mantids is, in general, weaker on the density for most taxa, but stronger on some taxa, like T. sinensis against Diptera and Hemiptera (herbivores as a group), and Stagmomantis carolina (Johansson, 1763) (Mantodea: Mantidae) negative or non-significant (Fagan et al., 2002). The abundance of defoliators and pollinators increased that of predators, including M. religiosa on A. mangium saplings (Silva et al., 2020), with a density of around 0.15 per tree, higher than on A. auriculiformis saplings (≈0.04/tree) (Mota et al., 2023). Podisus sp. decreased the number of T. spinipes by around 0.10% on T. argentea saplings. Podisus placidus Uhl. and Podisus maculiventris Say fed on honeybees (Bromley, 1948). Species of this genus are important predators as Podisus distinctus (Stål, 1860) and P. nigrispinus (Dallas, 1851) preying on larvae and pupae of Coleoptera and Lepidoptera defoliators on Eucalyptus spp. (Myrtales: Myrtaceae) (Zanuncio et al., 2014). However, the density of Podisus spp. is, generally, low on plants, as found in A. mangium (0.08/tree) and A. auriculiformis (0.06/tree) saplings (Silva et al., 2020; Mota et al., 2023). This makes it necessary to release P. nigrispinus when population levels of caterpillars are below the economic injury level (e.g., nine caterpillars/100 leaves) on Eucalyptus spp. (Zanuncio et al., 2014). This predator preys on 4-5 first and second instars larvae or 2-3 fourth and fifth instar caterpillars per day (Zanuncio et al., 2014). Finally, the tending ants (e.g., Ectatoma sp.), reduced 22.2% defoliator insect numbers (e.g., Lamprosoma sp.), representing 16.19% of the total reduction in T. argentea saplings. However, Brachymyrmex sp. increased the damage by A. spiraecola by around 70% on T. argentea saplings. This may not be a problem but, depending on the conditions (e.g., monoculture, climate, soil, and/or favorable fertilization), it can increase this sap-sucking insect population and, probably, the tending becoming a problem on T. argentea trees, especially in monoculture. The role of tending ants in productive systems is controversial, but its higher populations on leaves and extrafloral nectaries reduce the percentage of defoliation by herbivorous Lepidoptera and Coleoptera, and the numbers of Eunica bechina Talbot 1928 (Lepidoptera: Nymphalidae), Edessa rufomarginata De Geer 1773 (Hemiptera: Pentatomidae), Prodiplosis floricola (Felt, 1907) (Diptera: Cecidomyiidae), petiole gall insects (Hymenoptera: Chalcidoidea) on C. brasiliense trees (Freitas and Oliveira, 1996; Oliveira, 1997; Leite et al., 2012a, b, c), and Cephalocoema sp. (Orthoptera: Proscopiidae) on A. auriculiformis saplings (Demolin-Leite, 2024a). Besides, these ants are bioindicators of recovering degraded areas (Sanchez, 2015). However, Crematogaster sp. increased the abundance of Pseudococcus sp. (Hemiptera: Pseudococcidae) and Dikrella caryocar (Coelho, Leite, and Da-Silva, 2014) (Hemiptera: Cicadellidae) on C. brasiliense trees (Leite et al., 2015). Brachymyrmex sp. increased (≈93%) populations of Aethalion reticulatum L. 1767 (Hemiptera: Aethalionidae) and Cephalotes sp. that of Aleyrodidae (Hemiptera) (≈2%), and damage by Aleyrodidae (≈30%) on A. auriculiformis saplings (Demolin-Leite, 2024a). Sap-sucking insects, especially at high densities, are associated with ants (mutual benefit) with a direct correlation between these groups (Leite et al., 2012c, 2015, 2016; Novgorodova, 2015; Sanchez et al. 2019). These ants collectively and aggressively defend these phytophagous insects (their food resources) (Novgorodova, 2015) reducing the biological control of sap-sucking hemipterans (Karami-Jamour et al., 2018; Tong et al., 2019), and, in the agricultural systems, this fact can increase pest problems (Sagata and Gibb, 2016). High population levels of these predator populations per herbivorous insect may control herbivore’s abundance (e.g., Psiloptera sp.) through top-down effects, increasing the survival of T. argentea.

5. Conclusions

The loss sources Lamprosoma sp., Epitragus sp., T. collaris, Cerambycidae, Cratosomus sp., Psiloptera sp., Parasyphraea sp., T. spinipes, and A. spiraecola showed the highest % I.I.-P.U. on leaves of T. argentea saplings and may be problems in commercial crops. The solution sources spiders, the main predator group, Araneidae, A. uncifera, and Uspachus sp. (Araneae: Salticidae), M. religiosa, Podisus sp., and tending ants Ectatoma sp. and Pheidole sp. had the highest % I.I.-P.U. on leaves of T. argentea saplings. These natural enemies can reduce herbivorous insect numbers on T. argentea saplings, but it is necessary to increase their populations, especially spiders. Brachymyrmex sp. associated with A. spiraecola increased the numbers and damage by this sap-sucking insect.

Supplementary material

Supplementary material accompanies this paper

Supplementary Material I. Aggregated (Agg.), regular (Reg.), or random (Ran.) distribution (Dist.) of the loss sources on 48 Terminalia argentea (Combretaceae) saplings.. Supplementary Material II. Aggregated (Agg.), regular (Reg.), or random (Ran.) distribution (Dist.) of the solution sources on 48 Terminalia argentea (Combretaceae) saplings. Supplementary Material III. Simple regression equations of damage per loss source (L.S.) and reduction or increase of abundance or damage (Da.) of L.S. per solution source (S.S.) on Terminalia argentea (Combretaceae) saplings.

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].

References

• ALVARES, C.A., STAPE, J.L., SENTELHAS, P.C., GONÇALVES, J.L.M. and SPAROVEK, G., 2013. Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift, vol. 22, no. 6, pp. 711-728. http://dx.doi.org/10.1127/0941-2948/2013/0507
  » http://dx.doi.org/10.1127/0941-2948/2013/0507
• BOFF, S., GRACIOLLI, G., BOARETTO, A.G. and MARQUES, M.R., 2008. Visiting insects of exudated gums by Terminalia argentea Mart. & Zucc (Combretaceae). Revista Brasileira de Entomologia, vol. 52, no. 3, pp. 477-479. http://dx.doi.org/10.1590/S0085-56262008000300025
  » http://dx.doi.org/10.1590/S0085-56262008000300025
• BROMLEY, S.W., 1948 [viewed 3 March 2023]. Honey-bee predators. Journal of the New York Entomological Society [online], vol. 56, no. 3, pp. 195-199. Available from: https://www.jstor.org/stable/25005271
  » https://www.jstor.org/stable/25005271
• CARVALHO, L.M., LADEIRA, V.A., ALMEIDA, E.F.A., SANTA-CECILIA, L.C., BRIGHENTI, D.M. and RESENDE, E., 2018. Bagging to protect calla lily flowers against stingless bee (Trigona spinipes). Ornamental Horticulture, vol. 24, no. 4, pp. 353-360. http://dx.doi.org/10.14295/oh.v24i4.1193
  » http://dx.doi.org/10.14295/oh.v24i4.1193
• CASARI, S.A. and TEIXEIRA, E.P., 2008. Immatures of Lamprosoma amethystinum Perty, 1832 (Chrysomelidae, Lamprosomatinae). Zootaxa, vol. 171, no. 1, pp. 39-46.
• CRUZ-LOPEZ, L., JIMENEZ-ZUNIGA, J.A., SANTIESTEBAN-HERNANDEZ, A. and VIRGEN-SANCHEZ, A., 2001. Response of Epitragus sallaei (Champion) (Coleoptera: Tenebrionidae) to the odor of Mangifera indica flowers. The Southwestern Entomologist, vol. 26, no. 2, pp. 165-170.
• DAMASCENA, J.G., LEITE, G.L.D., SILVA, F.W.S., SOARES, M.A., GUANABENS, R.E.M., SAMPAIO, R.A. and ZANUNCIO, J.C., 2017. Spatial distribution of phytophagous insects, natural enemies, and pollinators on Leucaena leucocephala (Fabales: Fabaceae) trees in the Cerrado. The Florida Entomologist, vol. 100, no. 3, pp. 558-565. http://dx.doi.org/10.1653/024.100.0311
  » http://dx.doi.org/10.1653/024.100.0311
• DEMOLIN-LEITE, G.L., 2021 [viewed 3 March 2023]. Importance indice: loss estimates and solution effectiveness on production. Canadian Journal of Agricultural Science [online], vol. 55, no. 2, pp. 1-7. http://scielo.sld.cu/pdf/cjas/v55n2/2079-3480-cjas-55-02-e10.pdf
  » http://scielo.sld.cu/pdf/cjas/v55n2/2079-3480-cjas-55-02-e10.pdf
• DEMOLIN-LEITE, G.L., 2022a. Arthropods on Azadirachta indica A. Juss. (Sapindales: Meliaceae) saplings. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 82, e263551. http://dx.doi.org/10.1590/1519-6984.263551
  » http://dx.doi.org/10.1590/1519-6984.263551
• DEMOLIN-LEITE, G.L., 2022b. Arthropods as possible loss and solution sources on Platycyamus regnellii (Benth) (Fabales: Fabaceae) saplings. International Journal of Pest Management In press. http://dx.doi.org/10.1080/09670874.2022.2131933
  » http://dx.doi.org/10.1080/09670874.2022.2131933
• DEMOLIN-LEITE, G.L., and AZEVEDO, A.M., 2022 [viewed 3 March 2023]. Package ‘IIProductionUnknown’: analyzing data through of percentage of importance indice (production unknown) and its derivations: manual package [online]. Vienna: R Foundation for Statistical Computing, pp. 1-18. Available from: https://CRAN.R-project.org/package=IIProductionUnknown
  » https://CRAN.R-project.org/package=IIProductionUnknown
• DEMOLIN-LEITE, G.L., 2023. Arthropods as possible loss or solution sources on Acacia mangium (Fabales: Fabaceae) saplings. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 83, e267130. http://dx.doi.org/10.1590/1519-6984.267130 PMid:37075423.
  » http://dx.doi.org/10.1590/1519-6984.267130
• DEMOLIN-LEITE, G.L., 2024a. Percentage of importance indice-production unknown: loss and solution sources identification on system. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 84, e253218. http://dx.doi.org/10.1590/1519-6984.253218
  » http://dx.doi.org/10.1590/1519-6984.253218
• DEMOLIN-LEITE, G.L., 2024b. Do arthropods and diseases affect the production of fruits on Caryocar brasiliense Camb. (Malpighiales: caryocaraceae)? Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 84, e253215. http://dx.doi.org/10.1590/1519-6984.253215
  » http://dx.doi.org/10.1590/1519-6984.253215
• FAGAN, W.F. and HURD, L.E., 1994. Hatch density variation of a generalist arthropod predator: population consequences and community impact. Ecology, vol. 75, no. 7, pp. 2022-2032. http://dx.doi.org/10.2307/1941607
  » http://dx.doi.org/10.2307/1941607
• FAGAN, W.F., MORAN, M.D., RANGO, J.J. and HURD, L.E., 2002. Community effects of praying mantids: a meta-analysis of the influences of species identity and experimental design. Ecological Entomology, vol. 27, no. 4, pp. 385-395. http://dx.doi.org/10.1046/j.1365-2311.2002.00425.x
  » http://dx.doi.org/10.1046/j.1365-2311.2002.00425.x
• FREITAS, A.V.L. and OLIVEIRA, P.S., 1996. Ants as selective agents on herbivore biology: effects on the behaviour of a non-myrmecophilous butterfly. Journal of Animal Ecology, vol. 65, no. 2, pp. 205-210. http://dx.doi.org/10.2307/5723
  » http://dx.doi.org/10.2307/5723
• HÉRARD, F. and MASPERO, M., 2019. History of discoveries and management of the citrus longhorned beetle, Anoplophora chinensis, in Europe. Journal of Pest Science, vol. 92, no. 1, pp. 117-130. http://dx.doi.org/10.1007/s10340-018-1014-9
  » http://dx.doi.org/10.1007/s10340-018-1014-9
• JAMAL, A., 1994. Major insect pests of gum-arabic trees Acacia-senegal Willd and Acacia-seyal L in Western Sudan. Journal of Applied Entomology, vol. 117, no. 1-5, pp. 10-20. http://dx.doi.org/10.1111/j.1439-0418.1994.tb00702.x
  » http://dx.doi.org/10.1111/j.1439-0418.1994.tb00702.x
• KANEKO, S., 2018. Larvae of the exotic predatory ladybird Platynaspidius maculosus (Coleoptera: Coccinellidae) on citrus tree: prey aphid species and behavioral interactions with aphid-attending ants in Japan. Applied Entomology and Zoology, vol. 53, no. 1, pp. 85-91. http://dx.doi.org/10.1007/s13355-017-0531-y
  » http://dx.doi.org/10.1007/s13355-017-0531-y
• KARAMI-JAMOUR, T., MIRMOAYEDI, A., ZAMANI, A. and KHAJEHZADEH, Y., 2018. The impact of ant attendance on protecting Aphis gossypii against two aphidophagous predators and it’s role on the intraguild predation between them. Journal of Insect Behavior, vol. 31, no. 2, pp. 222-239. http://dx.doi.org/10.1007/s10905-018-9670-4
  » http://dx.doi.org/10.1007/s10905-018-9670-4
• KOGAN, M. and TURNIPSEED, S.G., 1980. Soybean growth and assessment of damage by arthropods. In: M. KOGAN and D.C. HERZOG, eds. Sampling methods in soybean entomology. New York: Springer. Springer Series in Experimental Entomology. http://dx.doi.org/10.1007/978-1-4612-9998-1_1
  » http://dx.doi.org/10.1007/978-1-4612-9998-1_1
• LANDIS, D.A., WRATTEN, S.D. and GURR, G.M., 2000. Habitat management to conserve natural enemies of arthropod pests in agriculture. Annual Review of Entomology, vol. 45, no. 1, pp. 175-201. http://dx.doi.org/10.1146/annurev.ento.45.1.175 PMid:10761575.
  » http://dx.doi.org/10.1146/annurev.ento.45.1.175
• LEITE, G.L.D., ARAÚJO, C.B.O., AMORIM, C.A.D., MARTINS, E.R. and D’ÁVILA, V.A., 2011. Effect of canopy height and surface leaf on arthropods in medicinal plants. Journal of Medicinal Plants Research, vol. 5, no. 9, pp. 1613-1621.
• LEITE, G.L.D., VELOSO, R.V.D.S., ZANUNCIO, J.C., ALMEIDA, C.I.M.E., FERREIRA, P.S.F., FERNANDES, G.W. and SOARES, M.A., 2012a. Habitat complexity and Caryocar brasiliense herbivores (Insecta; Arachnida; Araneae). The Florida Entomologist, vol. 95, no. 4, pp. 819-830. http://dx.doi.org/10.1653/024.095.0402
  » http://dx.doi.org/10.1653/024.095.0402
• LEITE, G.L.D., VELOSO, R.V.S., ZANUNCIO, J.C., ALMEIDA, C.I.M., FERREIRA, P.S.F., SERRÃO, J.E. and RAMALHO, F.S., 2012b. Seasonal damage caused by herbivorous insects on Caryocar brasiliense (Caryocaraceae) trees in the Brazilian savanna. Revista Colombiana de Entomologia, vol. 38, no. 1, pp. 35-40.
• LEITE, G.L.D., VELOSO, R.V.D.S., ZANUNCIO, J.C., FERNANDES, G.W., ALMEIDA, C.I.M., FERREIRA, P.S.F., ALONSO, J. and SERRÃO, J.E., 2012c. Seasonal abundance of hemipterans on Caryocar brasiliense (Malpighiales: Caryocaraceae) trees in the Cerrado. The Florida Entomologist, vol. 95, no. 4, pp. 862-872. http://dx.doi.org/10.1653/024.095.0407
  » http://dx.doi.org/10.1653/024.095.0407
• LEITE, G.L.D., VELOSO, R.V.S., ZANUNCIO, J.C., FERNANDES, G.W., ALMEIDA, C.I.M., FERREIRA, P.S.F., ALONSO, J. and SERRÃO, J.E., 2015. Cardinal distribution of sucking insects in Caryocar brasiliense (Caryocaraceae) in Cerrado (Brazil). Revista Colombiana de Entomologia, vol. 41, no. 1, pp. 105-111.
• LEITE, G.L.D., VELOSO, R.V.S., ZANUNCIO, J.C., ALONSO, J., FERREIRA, P.S.F., ALMEIDA, C.I.M., FERNANDES, G.W. and SERRÃO, J.E., 2016. Diversity of Hemiptera (Arthropoda: Insecta) and their natural enemies on Caryocar brasiliense (Malpighiales: Caryocaraceae) trees in the Brazilian Cerrado. The Florida Entomologist, vol. 99, no. 2, pp. 239-247. http://dx.doi.org/10.1653/024.099.0213
  » http://dx.doi.org/10.1653/024.099.0213
• LEMES, P.G., CORDEIRO, G., JORGE, I.R., ANJOS, N.D. and ZANUNCIO, J.C., 2015. Cerambycidae and other Coleoptera associated with branches girdled by Oncideres saga Dalman (Coleoptera: Cerambycidae: Lamiinae: Onciderini). Coleopterists Bulletin, vol. 69, no. 1, pp. 159-166. http://dx.doi.org/10.1649/0010-065X-69.1.159
  » http://dx.doi.org/10.1649/0010-065X-69.1.159
• LIMA, J.S., LEITE, G.L.D., GUANABENS, P.F.S., SOARES, M.A., SILVA, J.L., MOTA, M.V.S., LEMES, P.G. and ZANUNCIO, J.C., 2024. Insects and spiders on Acacia mangium (Fabaceae) saplings as bioindicators for the recovery of tropical degraded areas. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 84, no. 4, e252088. http://dx.doi.org/10.1590/1519-6984.252088
  » http://dx.doi.org/10.1590/1519-6984.252088
• LORENZI, H., 1992. Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas nativas do Brasil. Nova Odessa: Plantarum, 373 p.
• MOTA, M.V.S., DEMOLIN-LEITE, G.L., GUANABENS, P.F.S., TEIXEIRA, G.L., SOARES, M.A., SILVA, J.L., SAMPAIO, R.A. and ZANUNCIO, J.C., 2023. Chewing insects, pollinators, and predators on Acacia auriculiformis A. Cunn. ex Beth (Fabales: Fabaceae) plants fertilized with dehydrated sewage sludge. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 83, e248305. http://dx.doi.org/10.1590/1519-6984.248305
  » http://dx.doi.org/10.1590/1519-6984.248305
• NOVGORODOVA, T.A., 2015. Organization of honeydew collection by foragers of different species of ants (Hymenoptera: formicidae). European Journal of Entomology, vol. 112, no. 4, pp. 688-697. http://dx.doi.org/10.14411/eje.2015.077
  » http://dx.doi.org/10.14411/eje.2015.077
• ÖBERG, S., MAYR, S. and DAUBER, J., 2008. Landscape effects on recolonisation patterns of spiders in arable fields. Agriculture, Ecosystems & Environment, vol. 123, no. 1-3, pp. 211-218. http://dx.doi.org/10.1016/j.agee.2007.06.005
  » http://dx.doi.org/10.1016/j.agee.2007.06.005
• OLIVEIRA, P.S., 1997. The ecological function of extrafloral nectaries: herbivore deterrence by visiting ants and reproductive output in Caryocar brasiliense (Caryocaraceae). Functional Ecology, vol. 11, no. 3, pp. 323-330. http://dx.doi.org/10.1046/j.1365-2435.1997.00087.x
  » http://dx.doi.org/10.1046/j.1365-2435.1997.00087.x
• PODEROSO, J.C.M., DA COSTA, M.K.M., CORREIA-OLIVEIRA, M.E., DANTAS, P.C., ZANUNCIO, J.C. and RIBEIRO, G.T., 2013. Occurrence of Tropidacris collaris (Orthoptera; Acridoidea; Romaleidae) damaging Casuarina glauca (Casuarinaceae) plants in the municipality of Central Bahia, Brazil. The Florida Entomologist, vol. 96, no. 1, pp. 268-269. http://dx.doi.org/10.1653/024.096.0143
  » http://dx.doi.org/10.1653/024.096.0143
• RODRIGUES, S.R., COUTINHO, G.V., GARCEZ, W.S., GARCEZ, F.R. and ZANELLA, D.P.F., 2008 [viewed 3 March 2023]. Activity insecticide of etanolic extract of plants on Spodoptera frugiperda (J.E. Smith) (Lepidoptera: noctuidae). Agrarian [online], vol. 1, no. 1, pp. 133-144. Available from: https://agris.fao.org/agris-search/search.do?recordID=BR2012401379
  » https://agris.fao.org/agris-search/search.do?recordID=BR2012401379
• SAGATA, K. and GIBB, H., 2016. The effect of temperature increases on an ant-Hemiptera-plant interaction. PLoS One, vol. 11, no. 7, e0155131. http://dx.doi.org/10.1371/journal.pone.0155131 PMid:27434232.
  » http://dx.doi.org/10.1371/journal.pone.0155131
• SANCHEZ, A., 2015. Fidelity and promiscuity in an ant-plant mutualism: a case study of Triplaris and Pseudomyrmex. PLoS One, vol. 10, no. 12, e0143535. http://dx.doi.org/10.1371/journal.pone.0143535 PMid:26630384.
  » http://dx.doi.org/10.1371/journal.pone.0143535
• SANCHEZ, J.A., LÓPEZ-GALLEGO, E. and LA-SPINA, M., 2019. The impact of ant mutualistic and antagonistic interactions on the population dynamics of sap‐sucking hemipterans in pear orchards. Pest Management Science, vol. 76, no. 4, pp. 1422-1434. http://dx.doi.org/10.1002/ps.5655 PMid:31628776.
  » http://dx.doi.org/10.1002/ps.5655
• SERRA, B.D. and CAMPOS, L.A., 2010. Entomophilic pollination of squash, Cucurbita moschata (Cucurbitaceae). Neotropical Entomology, vol. 39, no. 2, pp. 153-159. http://dx.doi.org/10.1590/S1519-566X2010000200002 PMid:20498949.
  » http://dx.doi.org/10.1590/S1519-566X2010000200002
• SILVA, J.L., DEMOLIN LEITE, G.L., DE SOUZA TAVARES, W., SOUZA SILVA, F.W., SAMPAIO, R.A., AZEVEDO, A.M., SERRÃO, J.E. and ZANUNCIO, J.C., 2020. Diversity of arthropods on Acacia mangium (Fabaceae) and production of this plant with dehydrated sewage sludge in degraded area. Royal Society Open Science, vol. 7, no. 2, e191196. http://dx.doi.org/10.1098/rsos.191196 PMid:32257306.
  » http://dx.doi.org/10.1098/rsos.191196
• SOARES, I.J.A., COSTA, R.F., CARVALHO, A.G., LEMES, P.G., ZANUNCIO, J.C., LEITE, G.L.D. and ASSIS JÚNIOR, S.L., 2022. Oncideres saga Dalman: first record damaging Stryphnodendron adstringens Mart. Coville (Fabaceae) in Brazil. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 82, e239747. http://dx.doi.org/10.1590/1519-6984.239747
  » http://dx.doi.org/10.1590/1519-6984.239747
• SOBRINHO, R.B., BANDEIRA, C.T. and MESQUITA, A.L.M., 1999. Occurrence and damage of soursop pests in northeast Brazil. Crop Protection, vol. 18, no. 8, pp. 539-541. http://dx.doi.org/10.1016/S0261-2194(99)00051-4
  » http://dx.doi.org/10.1016/S0261-2194(99)00051-4
• TONG, H., AO, Y., LI, Z., WANG, Y. and JIANG, M., 2019. Invasion biology of the cotton mealybug, Phenacoccus solenopsis Tinsley: current knowledge and future directions. Journal of Integrative Agriculture, vol. 18, no. 4, pp. 758-770. http://dx.doi.org/10.1016/S2095-3119(18)61972-0
  » http://dx.doi.org/10.1016/S2095-3119(18)61972-0
• VENTURINO, E., ISAIA, M., BONA, F., CHATTERJEE, S. and BADINO, G., 2008. Biological controls of intensive agroecosystems: wanderer spiders in the Langa astigiana. Ecological Complexity, vol. 5, no. 2, pp. 157-164. http://dx.doi.org/10.1016/j.ecocom.2007.10.003
  » http://dx.doi.org/10.1016/j.ecocom.2007.10.003
• WÄCKERS, F.L., ALBEROLA, J.S., GARCIA-MARÍ, F. and PEKAS, A., 2017. Attract and distract: manipulation of a food-mediated protective mutualism enhances natural pest control. Agriculture, Ecosystems & Environment, vol. 246, pp. 168-174. http://dx.doi.org/10.1016/j.agee.2017.05.037
  » http://dx.doi.org/10.1016/j.agee.2017.05.037
• ZANUNCIO, J.C., TAVARES, W.D., FERNANDES, B.V., WILCKEN, C.F. and ZANUNCIO, T.V., 2014. Production and use of Heteroptera predators for the biological control of eucalyptus pests in Brazil. Ekoloji Çevre Dergisi, vol. 23, no. 91, pp. 98-104. http://dx.doi.org/10.5053/ekoloji.2014.9112
  » http://dx.doi.org/10.5053/ekoloji.2014.9112
• ZOGRAFOU, K., ADAMIDIS, G.C., KOMNENOV, M., KATI, V., SOTIRAKOPOULOS, P., PITTA, E. and CHATZAKI, M., 2017. Diversity of spiders and orthopterans respond to intra-seasonal and spatial environmental changes. Journal of Insect Conservation, vol. 21, no. 3, pp. 531-543. http://dx.doi.org/10.1007/s10841-017-9993-z
  » http://dx.doi.org/10.1007/s10841-017-9993-z

Publication Dates

• Publication in this collection
  27 Nov 2023
• Date of issue
  2023

History

• Received
  03 Mar 2023
• Accepted
  17 Oct 2023