Do arthropods and diseases affect the production of fruits on Caryocar brasiliense Camb. (Malpighiales: Caryocaraceae)?

Artrópodes e doenças afetam a produção de frutos em Caryocar brasiliense Camb. (Malpighiales: Caryocaraceae)?

G. L. Demolin-Leite About the author

Abstract

Frequencies, magnitudes, and distributions of occurrence can affect the events. The problem can be worse or the solution better if greater frequencies and magnitudes are presented with aggregated distribution in the production system. Indices, hence, are used to assist in decision-making on certain issues. The system formed by Caryocar brasiliense Camb. (Malpighiales: Caryocaraceae), a typical and economically important Brazilian Cerrado tree species, and its several arthropods are adequate to evaluate a new index. This study aimed to test an index to identify the loss and solution sources and their importance in the system's loss or income gain. The index is: Percentage of Importance Indice % I.I. = ks1×c1×ds1/Σ ks1×c1×ds1 + ks2×c2×ds2 + ksn×cn×dsn x 100. The % I.I. separated the loss sources [e.g., Edessa rufomarginata De Geer, 1773 (Hemiptera: Pentatomidae) on fruits = 41.90%)] on the percentage of reduction of fruit production (e.g., 0.13%), calculated the attention level (e.g., 0.10/fruit), with a total lost production of 1.35% (≈ 307 total lost fruits). The % I.I. also separated the solution sources [e.g., Zelus armillatus (Lep. and Servi., 1825) (Hemiptera: Reduviidae) = 55.48%), the non-attention level (e.g., Z. armillatus: 0.394 for E. rufomarginata on fruit), with total income gain of 0.56% (≈ 128 total saved fruits) on the natural system (e.g., C. brasiliense trees). This index can calculate losses or the effectiveness of the solutions monetarily. Here I test the % I.I., an index that can detect the key loss and solution sources on the system, which can be applied in some knowledge areas.

Keywords:
abundance; aggregation; agriculture; chi-squared test; constancy; frequency; natural system

Resumo

Frequências, magnitudes e distribuição de ocorrência pode afetar os eventos. O problema pode ser pior ou a solução melhor se maiores frequências e magnitudes forem apresentadas com distribuição agregada no sistema de produção. Índices, então, são usados para assistir na decisão de certas questões. O sistema formado pelo Caryocar brasiliense Camb. (Malpighiales: Caryocaraceae), uma espécie arbórea típica e economicamente importante do Cerrado brasileiro, e seus diversos artrópodes são adequados para avaliar um novo índice. A motivação deste trabalho foi testar um índice capaz de identificar as fontes de perda e de soluções, e suas importâncias em termos de perdas ou ganhos no sistema. O índice é: percentagem de importância % I.I. = ks1×c1×ds1/Σ ks1×c1×ds1 + ks2×c2×ds2 + ksn×cn×dsn x 100.O% I.I. separou as fontes de perda [ex., Edessa rufomarginata De Geer, 1773 (Hemiptera: Pentatomidae) em frutos = 41,90%)] na percentagem de redução na produção de frutos (ex., 0,13%), calculando o nível de atenção (ex., 0,10/fruto), com um total de perda de produção de 1,35% (≈ 307 frutos totais perdidos). O % I.I. também separou as fontes de solução [ex., Zelus armillatus (Lep. and Servi., 1825) (Hemiptera: Reduviidae) = 55,48%)], o nível de não atenção (ex., Z. armillatus: 0,394 para E. rufomarginata em fruto), com total de ganho de 0,56% (≈ 128 total de frutos salvos) no sistema natural (ex., árvores de C. brasiliense). Esse índice pode calcular essas perdas ou a eficácia das soluções monetariamente. Aqui eu testo o % I.I., um índice capaz de detectar fatores chaves de perda e de soluções no sistema, capaz de ser aplicado em algumas áreas do conhecimento.

Palavras-chave:
abundância; agregação; agricultura; teste do qui-quadrado; constância; frequência; sistema natural

1. Introduction

Events (e.g., agricultural pest) can have different magnitudes (numerical measurements), frequencies, and distributions (aggregate, random, or regular) of occurrence and I based on this triplet to develop a new index – Percentage of Importance Indice (% I.I.) (Demolin-Leite, 2021DEMOLIN-LEITE, G.L., 2021. Importance indice: loss estimates and solution effectiveness on production. Canadian Journal of Agricultural Science, vol. 55, no. 2, pp. 1-7.). The problem can be worse or the solution better if greater frequencies and magnitudes are presented with aggregated distribution in the production system (e.g., pests versus natural enemies) (Demolin-Leite, 2021DEMOLIN-LEITE, G.L., 2021. Importance indice: loss estimates and solution effectiveness on production. Canadian Journal of Agricultural Science, vol. 55, no. 2, pp. 1-7.). Hence, indices are used to help on decision-making in certain questions and, many of them, determine key-factors in an event, on the agrarian and biological areas: Crop and Ecological Life Tables (Henderson and Southwood, 2016HENDERSON, P.A. and SOUTHWOOD, T.E.R., 2016. Ecological methods. Oxford: John Wiley & Sons.; Silva et al., 2017SILVA, E.M., SILVA, R.S., RODRIGUES-SILVA, N., MILAGRES, C.C., BACCI, L. and PICANÇO, M.C., 2017. Assessment of the natural control of Neoleucinodes elegantalis in tomato cultivation using ecological life tables. Biocontrol Science and Technology, vol. 27, no. 4, pp. 525-538. http://dx.doi.org/10.1080/09583157.2017.1319911.
http://dx.doi.org/10.1080/09583157.2017....
), among others. Usually, these tools use abundance (magnitude) which can be analyzed by correlation, mean or t-tests, multiple or simple regression analysis, etc. (Henderson and Southwood, 2016HENDERSON, P.A. and SOUTHWOOD, T.E.R., 2016. Ecological methods. Oxford: John Wiley & Sons.; Silva et al., 2017SILVA, E.M., SILVA, R.S., RODRIGUES-SILVA, N., MILAGRES, C.C., BACCI, L. and PICANÇO, M.C., 2017. Assessment of the natural control of Neoleucinodes elegantalis in tomato cultivation using ecological life tables. Biocontrol Science and Technology, vol. 27, no. 4, pp. 525-538. http://dx.doi.org/10.1080/09583157.2017.1319911.
http://dx.doi.org/10.1080/09583157.2017....
; Demolin-Leite, 2021DEMOLIN-LEITE, G.L., 2021. Importance indice: loss estimates and solution effectiveness on production. Canadian Journal of Agricultural Science, vol. 55, no. 2, pp. 1-7.).

The Percentage of Importance Indice (% I.I.) is effective in identifying loss sources on the system (e.g., reduction in production) (Demolin-Leite, 2021DEMOLIN-LEITE, G.L., 2021. Importance indice: loss estimates and solution effectiveness on production. Canadian Journal of Agricultural Science, vol. 55, no. 2, pp. 1-7.), it is simpler than a Crop Life Table (Silva et al., 2017SILVA, E.M., SILVA, R.S., RODRIGUES-SILVA, N., MILAGRES, C.C., BACCI, L. and PICANÇO, M.C., 2017. Assessment of the natural control of Neoleucinodes elegantalis in tomato cultivation using ecological life tables. Biocontrol Science and Technology, vol. 27, no. 4, pp. 525-538. http://dx.doi.org/10.1080/09583157.2017.1319911.
http://dx.doi.org/10.1080/09583157.2017....
), but it does not replace it (Demolin-Leite, 2021DEMOLIN-LEITE, G.L., 2021. Importance indice: loss estimates and solution effectiveness on production. Canadian Journal of Agricultural Science, vol. 55, no. 2, pp. 1-7.). The use of % I.I. is for cases (e.g., natural system, Cerrado) in which it is not possible to evaluate all flowers and fruits of all plants in the experimental useful plot, identifying the factors of plant loss (Demolin-Leite, 2021DEMOLIN-LEITE, G.L., 2021. Importance indice: loss estimates and solution effectiveness on production. Canadian Journal of Agricultural Science, vol. 55, no. 2, pp. 1-7.), as done by Crop Life Table (Silva et al., 2017SILVA, E.M., SILVA, R.S., RODRIGUES-SILVA, N., MILAGRES, C.C., BACCI, L. and PICANÇO, M.C., 2017. Assessment of the natural control of Neoleucinodes elegantalis in tomato cultivation using ecological life tables. Biocontrol Science and Technology, vol. 27, no. 4, pp. 525-538. http://dx.doi.org/10.1080/09583157.2017.1319911.
http://dx.doi.org/10.1080/09583157.2017....
). Parameters of Life Table supply reliable information, e.g. reproductive potential and mortality factors of species (Henderson and Southwood, 2016HENDERSON, P.A. and SOUTHWOOD, T.E.R., 2016. Ecological methods. Oxford: John Wiley & Sons.). The % I.I. is, also, effective in identifying solution sources on the system (e.g., increasing production) (Demolin-Leite, 2021DEMOLIN-LEITE, G.L., 2021. Importance indice: loss estimates and solution effectiveness on production. Canadian Journal of Agricultural Science, vol. 55, no. 2, pp. 1-7.), similar to an Ecological Life Table (Henderson and Southwood, 2016HENDERSON, P.A. and SOUTHWOOD, T.E.R., 2016. Ecological methods. Oxford: John Wiley & Sons.). The % I.I. does not replace an Ecological Life Table (Henderson and Southwood, 2016HENDERSON, P.A. and SOUTHWOOD, T.E.R., 2016. Ecological methods. Oxford: John Wiley & Sons.). The use of % I.I. is for cases (e.g., natural system, Cerrado) in which it is not able to mark and monitor the animal (e.g., pest insects), identifying the cause of its mortality (Demolin-Leite, 2021DEMOLIN-LEITE, G.L., 2021. Importance indice: loss estimates and solution effectiveness on production. Canadian Journal of Agricultural Science, vol. 55, no. 2, pp. 1-7.), as done by Ecological Life Table (Henderson and Southwood, 2016HENDERSON, P.A. and SOUTHWOOD, T.E.R., 2016. Ecological methods. Oxford: John Wiley & Sons.). Insect pest rearing, detailed field studies, time, and researchers trained to identify and quantify the control of natural factors daily until the insect pest life cycle is complete, are the most significant steps to determine the parameters of a Life Table of pest insects (Silva et al., 2017SILVA, E.M., SILVA, R.S., RODRIGUES-SILVA, N., MILAGRES, C.C., BACCI, L. and PICANÇO, M.C., 2017. Assessment of the natural control of Neoleucinodes elegantalis in tomato cultivation using ecological life tables. Biocontrol Science and Technology, vol. 27, no. 4, pp. 525-538. http://dx.doi.org/10.1080/09583157.2017.1319911.
http://dx.doi.org/10.1080/09583157.2017....
). The % I.I. can be significant for preserving native areas from helping traditional communities, like the quilombolas (rebellious slaves refuge area in the Brazilian colonial period), indigenous, collectors (e.g., of fruits), etc., to identify the true loss sources of production in native plants. Thus, together with the help of extension researchers, they can plan the best management of these potential pests.

The system's composition with Caryocar brasiliense Camb. (Malpighiales: Caryocaraceae), a typical and economically important Cerrado tree species (Leite et al., 2006LEITE, G.L.D., VELOSO, R.V.S., ZANUNCIO, J.C., FERNANDES, L.A. and ALMEIDA, C.I.M., 2006. Phenology of Caryocar brasiliense in the Brazilian Cerrado region. Forest Ecology and Management, vol. 236, no. 2-3, pp. 286-294. http://dx.doi.org/10.1016/j.foreco.2006.09.013.
http://dx.doi.org/10.1016/j.foreco.2006....
), and its several arthropods (e.g., herbivorous and natural enemies) in central Brazil (Leite, 2014LEITE, G.L.D., 2014. Galling insects on Caryocar brasiliense Camb. (Caryocaraceae). In: G.W. FERNANDES and J.C. SANTOS, eds. Neotropical insect galls. Berlin: Springer-Verlag, pp.179-192. http://dx.doi.org/10.1007/978-94-017-8783-3_12.
http://dx.doi.org/10.1007/978-94-017-878...
; Leite et al., 2022LEITE, G.L.D., VELOSO, R.V.S., AZEVEDO, A.M., ALMEIDA, C.I.M., SOARES, M.A., PEREIRA, A.I.A., LEMES, P.G. and ZANUNCIO, J.C., 2022. Distribution of galling insects and their parasitoids on Caryocar brasiliense tree crowns. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 82, pp. e235017. http://dx.doi.org/10.1590/1519-6984.235017. PMid:34076163.
http://dx.doi.org/10.1590/1519-6984.2350...
) are adequate to evaluate a new index. Caryocar brasiliense trees, protected by Brazilian federal laws, are the primary income source of many communities (Leite et al., 2006LEITE, G.L.D., VELOSO, R.V.S., ZANUNCIO, J.C., FERNANDES, L.A. and ALMEIDA, C.I.M., 2006. Phenology of Caryocar brasiliense in the Brazilian Cerrado region. Forest Ecology and Management, vol. 236, no. 2-3, pp. 286-294. http://dx.doi.org/10.1016/j.foreco.2006.09.013.
http://dx.doi.org/10.1016/j.foreco.2006....
). Hence, these trees are left in the Cerrado areas even after being converted to pasture, urban or agricultural areas, with a common scenario of isolated individual plants in the agro-urban landscape.

This study aimed to test a new index, which can determine the loss and solution sources, classifying them according to their importance in terms of loss or income gain on the system – C. brasiliense trees.

2. Material and methods

2.1. Percentage of Importance Indice (% I.I.)

The type of distribution (aggregated, random, or regular) of lost source (L.S). or solution source (S.S.) was defined by the Chi-square test using the BioDiversity Professional program, version 2 (Krebs, 1989KREBS, C.J., 1989 [viewed 2 May 2018]. Bray-Curtis cluster analysis [online]. Available from: http://biodiversity-pro.software.informer.com/.
http://biodiversity-pro.software.informe...
). The data were subjected to simple regression analysis and their parameters were all significant (P< 0.05) using the statistical program System for Analysis Statistics and Genetics (SAEG, 2007SISTEMA PARA ANÁLISES ESTATÍSTICAS E GENÉTICAS – SAEG, 2007 [viewed 2 May 2018]. Version 9.1 [online]. Available from: http://arquivo.ufv.br/saeg/.
http://arquivo.ufv.br/saeg/...
), version 9.1 (Table 1). Simple equations were selected by observing the criteria: i) distribution of 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 coefficient of determination of these equations (R2). Only loss sources and solution sources with P< 0.05 were shown in Table 1. It is necessary knowledge of the system to select the possible loss and solution sources.

Table 1
Aggregated (Agg.), regular (Reg.), or random (Ran.) distribution (Dist.) of the loss or solution sources; and simple regression equations with their coefficients of determination (R2), significance (P) and F of the analysis of variance (Var.) (ANOVA) of reductions of total fruit production (F.P.) by phytophagous arthropods and diseases and reductions of these pests by natural enemies in branch (b.), leaf (l.), flower (f.), fruit (fr.), and/or trunk (t.) on 20 Caryocar brasiliense trees.

The equation of the % of Importance Indice (% I.I.) (Demolin-Leite, 2021DEMOLIN-LEITE, G.L., 2021. Importance indice: loss estimates and solution effectiveness on production. Canadian Journal of Agricultural Science, vol. 55, no. 2, pp. 1-7.) is Equation 1:

% I . I . = k s 1 × c 1 × d s 1 / Σ k s 1 × c 1 × d s 1 + k s 2 × c 2 × d s 2 + k s n × c n × d s n × 100 (1)

where,

i)key source (ks) is:

ks = reduction on production (R.P.)/total n of the L.S. or effectiveness of the solution (E.S.)/total n of the S.S..

Where,

R.P. or E.S. = R2 x (1 - P) when it is of the first degree, or R.P. or E.S. = ((R2 x (1 - P))x(β21) 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 L.S. or S.S..

When a S.S. acts on more than one L.S., theirs E.S. are summed. E.S. or R.P. = 0 when E.S. or R.P. is non-significant on the L.S. or R.P., respectively.

ii)constancy (c) is (Demolin-Leite, 2021DEMOLIN-LEITE, G.L., 2021. Importance indice: loss estimates and solution effectiveness on production. Canadian Journal of Agricultural Science, vol. 55, no. 2, pp. 1-7.):

c = Σ of occurrence of L.S. or S.S. on the samples.

Where,

absence = 0 or presence = 1.

iii)distribution source (ds) (Demolin-Leite, 2021DEMOLIN-LEITE, G.L., 2021. Importance indice: loss estimates and solution effectiveness on production. Canadian Journal of Agricultural Science, vol. 55, no. 2, pp. 1-7.) is:

ds = 1 - P of the chi-square test of L.S. or S.S. on the samples.

2.2. Loss estimates and solutions effectiveness

Percentage of loss of production per loss source (% L.P.L.S.) is Equation 2:

% L . P . L . S . = L . P . L . S . / M . E . P . × 100. (2)

Where,

Loss of production per loss source (L.P.L.S.) = total n of the L.S. x R.P. of the L.S.,

and

maximum estimated production (M.E.P.) = Total production (P.) + Σ L.P.L.S.1 + ....L.P.L.S.n.

Income gain (I.G.) = L.P.L.S. x E.S.

and %I.G. is Equation 3

% I . G . = I . G . / M . E . P . * 100 (3)

In this case, the E.S. of the S.S. is separated per L.S..

2.3. Attention and non-attention levels

Attention level (A.L.) is Equation 4

A . L . = n o f t h e L . S . p e r s a m p l e x 0.75 / % L . P . L . S (4)

Where,

n of the L.S. per sample = n/(number of trees/evaluation frequency/years/number of plant parts evaluated).

In this paper, the number of trees = 20; evaluation frequency = 12 months per year for leaves, trunks, and branches, two months for bunches of flowers per year, and three months for bunches of fruits per year; years = three; and the number of plant parts evaluated = 12 leaves, 12 bunches of flowers and/or fruits, and one trunk per tree/evaluation.

And,

0.75 = 1% of loss fruits x 0.75 (safety margin)

Non-attention level (N.A.L.) is Equation 5

N . A . L . = A . L . × 1.25 / E . S . (5)

And,

1.25 = 25% plus as safety margin.

2.4. Study sites

This study was performed in Montes Claros, Minas Gerais state, Brazil, for 3 consecutive years (June 2016 through June 2019). This region has dry winters and rainy summers with an Aw: tropical savanna climate, according to Köppen. The study was developed in the sensu stricto Cerrado area (16º 44’ 55.6ˮ S, 43º 55’ 7.3ˮ W, at an elevation of 943 masl, with dystrophic yellow-red oxisol soil with sandy texture) which was described by Leite et al. (2006)LEITE, G.L.D., VELOSO, R.V.S., ZANUNCIO, J.C., FERNANDES, L.A. and ALMEIDA, C.I.M., 2006. Phenology of Caryocar brasiliense in the Brazilian Cerrado region. Forest Ecology and Management, vol. 236, no. 2-3, pp. 286-294. http://dx.doi.org/10.1016/j.foreco.2006.09.013.
http://dx.doi.org/10.1016/j.foreco.2006....
. Permission to collect arthropods in these locations/activities was granted by the landowner (Universidade Federal de Minas Gerais) and the collected arthropods are neither endangered nor protected species. Adult C. brasiliense trees (reproductive stage) in the Cerrado (20 trees) were ≈11.5 m height, ≈14.1 m crown width, and ≈0.31 m trunk diameter (1.5 m height).

2.5. Data collection

Data were collected on 20 C. brasiliense adult trees (reproductive stage) at every 40 m along a 500 m transect at the site (Cerrado area, 10 ha), during 3 consecutive years. No fertilizers or pesticides were used in this area. The numbers of arthropods, defoliation, leaf miners, galls, termite nests and disease symptoms were recorded on 12 fully expanded leaves (three leaflets/leaf), 12 branches, 12 bunches of flowers, and 12 bunches of fruits - one plant part (e.g., leaf) in each vertical (apical, median, and basal = 0 to 33%, 34 to 66%, and 67 to 100% of total tree height, respectively) and horizontal (north, south, east, and west) stratifications of the canopy, on 20 C. brasiliense trees. Sampling was performed in the morning (7:00-11:00 A.M) by direct visual observation or hand lens -10 x magnification, three fields/leaf with 1cm2 of the fixed field - for phytophagous and predator mites (immature and adults sum), once a month. Each month, these trees were also evaluated by the number of trunk borers attacked by Cossidae (Lepidoptera) (number of roles per trunk) and termite nests.

The number of fruits was counted in a bunch per side of the crown (north, south, east, and west) and along with the canopy (apical, middle, and basal) of the 20 trees, monthly, in the Cerrado area. The total production of fruits/tree was obtained by multiplying the total number of bunches per tree by the number of fruits per bunch evaluated.

Insects were collected with tweezers, brushes, or aspirators and preserved in vials with 70% alcohol for identification by taxonomists (see acknowledgments). The leaves were collected and transported to the laboratory. Subsequently, the leaves were placed inside a white plastic pot (temperature 25°C) and the emergence of galling insects, parasitoids, hyperparasitoids, and inquilines was evaluated per sample every two days for 30 days. The emerged insects were collected and preserved as described for identification (see acknowledgments). In the case of mites, these arthropods were collected in the leaves when they arrived in the laboratory, with brushes - (using a binocular microscope with 12.5 × magnification), and preserved in vials with 70% alcohol for identification (see acknowledgments).

3. Results

The loss sources (L.S.), per individual or symptom (e.g., disease), Edessa rufomarginata De Geer, 1773 (Hemiptera: Pentatomidae) on fruits, fruit borer Carmenta sp. (Lepidoptera: Sesiidae), E. rufomarginata on leaves, trunk borer Cossidae, Trigona spinipes Fabr., 1793 (Hymenoptera: Apidae) on flowers, Phomopsis sp. (Sacc.) Bubák (Coelomyceto) on branches, E. rufomarginata on branches, fruit scraper Naupactus sp.1 (Coleoptera: Curculionidae) on fruits, Aconophora sp. (Hemiptera: Membracidae) on fruits, and leaf galling insect Eurytoma sp. (Hymenoptera: Eurytomidae) showed, among the 39 L.S., the highest % I.I. (41.90, 18.58, 16.30, 10.48, 5.20, 3.66, 3.60, 0.24, 0.05, and 0.001%, respectively) on 20 C. brasiliense trees. The total number of loss of fruits and percentage of production reduction, respectively, per L.S., on 20 C. brasiliense trees were: E. rufomarginata on branches = 145.93 and 0.64%, Phomopsis sp. 57.43 and 0.25% on branches, Carmenta sp. 47.04 and 0.21% on fruits, E. rufomarginata on fruits 30.40 and 0.13%, E. rufomarginata on leaves 13.16 and 0.06%, Eurytoma sp. on leaves 4.99 and 0.02%, Naupactus sp.1 on fruits 4.01 and 0.02%, Cossidae 1.72 and 0.01% on trunks, T. spinipes on flowers 1.61 and 0.01%, and Aconophora sp. on fruits 0.68 and 0.003%, totalizing on 306.95 lost fruits and 1.35% of production reduction (Tables 2, 3). The attention levels (A.L.) for these L.S. were: Phomopsis sp. 0.05/branch; E. rufomarginata 0.04, 0.07, and 0.10 per branch, leaf, and fruit, respectively; Carmenta sp. 0.14/fruit; T. spinipes 1.92/flower; Cossidae 2.21/trunk; Naupactus sp.1 4.15/fruit; Aconophora sp. 11.91/fruit, and Eurytoma sp. 19.98/leaf on C. brasiliense tree (Tables 2, 3).

Table 2
Total number (n), reduction on production (R.P.), effectiveness of the solution (E.S.), key-source (ks), constancy (c), distribution source (ds), number of importance indice (n.I.I.), sum of n. I.I.n.I.I.), and percentage of I.I. by loss source (L.S.) or solution source (S.S.) by L.S. on 20 Caryocar brasiliense trees.
Table 3
Loss sources (L.S.), loss of production by loss source (L.P.L.S.), % of L.P.L.S., and attention level (A.L.); effectiveness of the solution (E.S.) per solution source (S.S.), income gain (I.G.) and its %, and non-attention level (N.A.L.) by S.S and partial and total sum (Σ) on 20 Caryocar brasiliense trees.

The effective solution sources (S.S.), per individual, predator Zelus armillatus (Lep. and Servi., 1825) (Hemiptera: Reduviidae) on leaves, Crematogaster sp. (Hymenoptera: Formicidae) on leaves (mean 10.80±1.81 S.E.), flowers (mean 10.40±2.96 S.E.) and fruits (mean 3.25±1.36 S.E.), Epipolops sp. (Hemiptera: Geocoridae) on leaves, Pseudomyrmex termitarius (Smith, 1877) (Hymenoptera: Formicidae) on leaves (mean 0.85±0.16 S.E.) and fruits (mean 0.05±0.05 S.E.), and Eurytoma sp. parasitoids Ablerus magistretti Blanchard, 1942 (Hymenoptera: Aphelinidae) and Sycophila sp. (Hymenoptera: Eurytomidae) on leaves, showed, among the 16 S.S., the highest % I.I. (55.48, 22.08, 13.13, 9.17, 0.13, and 0.01%, respectively) on 20 C. brasiliense trees. Crematogaster sp. reduced production loss per Carmenta sp. on fruits, E. rufomarginata on branches, on fruits, and in leaves, Eurytoma sp. on leaves, and Naupactus sp.1 on fruits (18.77, 68.53, 20.67, 3.77, 0.04, and 0.02 total saved fruit – I.G., respectively) increasing in % of income gain (0.082, 0.301, 0.091, 0.017, 0.0001, and 0.0001%, respectively) on C. brasiliense production. Pseudomyrmex termitarius decreased production loss (4.43 total saved fruit) per E. rufomarginata on fruits increasing in income gain (0.019%) on C. brasiliense production. The predator Z. armillatus decreased production loss per E. rufomarginata on fruits, Eurytoma sp. on leaves, and Naupactus sp.1 on fruits (9.64, 0.61, and 0.67 total saved fruit, respectively) increasing in percentage of income gain (0.042, 0.003, and 0.003%, respectively) on C. brasiliense production. The parasitoids A. magistretti and Sycophila sp. and the predator Epipolops sp. decreased production loss per Eurytoma sp. on leaves (0.03, 0.01, and 0.46 total saved fruit, respectively) increasing in percentage of income gain (0.0001, 0.0001, and 0.0020%, respectively) on C. brasiliense production. The total reduction in production loss due to loss sources was 127.65 total saved fruit, with an increase in system productivity of 0.56% due to the solution sources cited above. The non-attention levels (N.A.L.) for these S.S. were: i) Crematogaster sp.: 0.44 for Carmenta sp. on fruit; 0.11, 0.18, and 0.31 for E. rufomarginata on the branch, on fruit, and in leaf, respectively; 3062.41 for Eurytoma sp. on the leaf, and 849.45 for Naupactus sp.1 on fruit; ii) P. termitarius: 0.86 for E. rufomarginata on fruit; iii) Z. armillatus: 0.394 for E. rufomarginata on fruit, 31.261 for Eurytoma sp. on the leaf, and 31.26 for Naupactus sp.1 on fruit; iv) 3735.13 A. magistretti, 9941.29 Sycophila sp. and 273.88 Epipolops sp. for Eurytoma sp. on the leaf, on one plant part evaluated/C. brasiliense tree (Tables 2, 3).

4. Discussion

The Percentage of Importance Indice (% I.I.) effectively identified the loss sources on the system. The use of % I.I. is for cases in which it is impossible to evaluate all flowers and fruits of all plants in the experimental useful plot, identifying the factors of plant loss (Demolin-Leite, 2021DEMOLIN-LEITE, G.L., 2021. Importance indice: loss estimates and solution effectiveness on production. Canadian Journal of Agricultural Science, vol. 55, no. 2, pp. 1-7.). Fruit production and arthropods on branches, flowers, fruits, leaves, and trunks data, used to test % I.I., were collected on C. brasiliense trees, over 10 m high, randomly, in the Cerrado area, in three years, monthly. Flowers and fruits were evaluated on some tree branches and then estimated the total per tree, thus, the use of this index is for cases where it is not possible to use a Crop Life Table (Demolin-Leite, 2021DEMOLIN-LEITE, G.L., 2021. Importance indice: loss estimates and solution effectiveness on production. Canadian Journal of Agricultural Science, vol. 55, no. 2, pp. 1-7.).

The loss sources E. rufomarginata, Carmenta sp., Cossidae, T. spinipes, Phomopsis sp., Naupactus sp.1, Aconophora sp., and Eurytoma sp. showed the highest % I.I. on 20 C. brasiliense trees, reducing, around 1.4%, the fruit production (less ≈ 307 total fruits). The % I.I. shows the importance of these loss sources, observing the individual capacity to cause damage and if the attack occurs in an aggregate and frequent way in the samples. With this index, it is possible to separate these loss sources on production, assuming a cutoff point (e.g., % I.I. below 1%). Therefore, it would be unnecessary to calculate L.P.L.S., % L.P.L.S., and A.L. such as for Naupactus sp.1 (% I.I. = 0.235) and Aconophora sp. (% I.I. = 0.051) on fruits and Eurytoma sp. (% I.I. = 0.001) on leaves on C. brasiliense trees, showing highest A.L. (4.15/fruit, 11.91/fruit, and 19.98/leaf, respectively) and, consequently, N.A.L. (e.g., Sycophila sp. versus Eurytoma sp. = 9941.29/leaf) per plant part/tree/evaluation.

The sap-sucking E. rufomarginata on branches, leaves, and fruits, and fruit borer Carmenta sp. are related, causing fall of flowers and fruits and damaging fruits, respectively, reducing the production of C. brasiliense trees (Leite et al., 2012aLEITE, G.L.D., VELOSO, R.V.S., ZANUNCIO, J.C., ALMEIDA, C.I.M., 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...
, 2016LEITE, G.L.D., LOPES, P.S.N., ZANUNCIO, J.C., MARTINS, C.P.S., MOREIRA, T.M.B. and COSTA, R.I.F., 2016. Effects of environmental and architectural diversity of Caryocar brasiliense (Malpighiales: Caryocaraceae) on Edessa ruformaginata (Hemiptera: Pentatomidae) and its biology. Acta Scientiarum. Agronomy, vol. 38, no. 1, pp. 19-27. http://dx.doi.org/10.4025/actasciagron.v38i1.26244.
http://dx.doi.org/10.4025/actasciagron.v...
). Edessa rufomarginata and Carmenta sp. showed very low A.L. (0.04/branch, 0.07/leaf, 0.10/fruit, and 0.14/fruit respectively) on C. brasiliense trees. A suggestion of control tactic for E. rufomarginata is the collection of fallen leaves and their burial, during the renewal of leaves and flowering of C. brasiliense trees (Leite et al., 2006LEITE, G.L.D., VELOSO, R.V.S., ZANUNCIO, J.C., FERNANDES, L.A. and ALMEIDA, C.I.M., 2006. Phenology of Caryocar brasiliense in the Brazilian Cerrado region. Forest Ecology and Management, vol. 236, no. 2-3, pp. 286-294. http://dx.doi.org/10.1016/j.foreco.2006.09.013.
http://dx.doi.org/10.1016/j.foreco.2006....
), as E. rufomarginata takes refuge under these leaves, while waiting for the new leaves. The same applies to Carmenta sp., as the bored fruits must be collected and buried so this pest does not complete its life cycle. The lower percentage of live C. brasiliense trees and healthy branches were found in the Savanna of Ibiracatu, Minas Gerais, Brazil, where only 30% of the trees were healthy and without visible signs of attack by trunk borer Cossidae and, principally, by fungus Phomopsis sp. (Leite et al., 2012bLEITE, G.L.D., NASCIMENTO, A.F., ALVES, S.M., LOPES, P.S.N., SALES, N.L.P. and ZANUNCIO, J.C., 2012b. The mortality of Caryocar brasiliense in northern Minas Gerais State, Brazil. Acta Scientiarum. Agronomy, vol. 34, no. 2, pp. 131-137. http://dx.doi.org/10.4025/actasciagron.v34i2.13120.
http://dx.doi.org/10.4025/actasciagron.v...
). Cossidae showed A.L. of 2.2/trunk and Phomopsis sp. A.L. 0.05/branch. The control of Cossidae is relatively easy; sprinkling is performed in the active holes in the trunk (with fresh sawdust), with entomopathogenic fungus Beauveria bassiana powder. However, the control of Phomopsis sp. is not easy. One indication of control is the cutting and burial of the branches when they present the first attack symptoms.

Moreover, T. spinipes is a pest that can reduce pollination on Cucurbita moschata Dusch (Cucurbitales: Cucurbitaceae) plants owing to insufficient pollen transportation (small body size) and/or chasing other pollinators by flying in flocks and with aggressive behavior (Serra and Campos, 2010SERRA, B.D.V. and CAMPOS, L.A.O., 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/S1519-566X2010...
). In addition, T. spinipes damages shoots and plant growth regions by removing fibers to construct their nests, as reported on Acacia mangium Willd. (Fabales: Fabaceae) and Leucaena leucocephala (Lam.) de Wit. (Fabales: Fabaceae) (Silva et al., 2014SILVA, F.W.S., LEITE, G.L.D., GUAÑABENS, R.E.M., SAMPAIO, R.A., GUSMÃO, C.A.G. and ZANUNCIO, J.C., 2014. Spatial distribution of arthropods on Acacia mangium (Fabales: Fabaceae) trees as windbreaks in the Cerrado. The Florida Entomologist, vol. 97, no. 2, pp. 631-638. http://dx.doi.org/10.1653/024.097.0240.
http://dx.doi.org/10.1653/024.097.0240...
; Damascena et al., 2017DAMASCENA, J.G., LEITE, G.L.D., SILVA, F.W.S., SOARES, M.A., GUAÑABENS, 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...
; Silva et al., 2020SILVA, J.L., DEMOLIN-LEITE, G.L., TAVARES, W.S., SILVA, F.W.S., 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, pp. 191196. http://dx.doi.org/10.1098/rsos.191196. PMid:32257306.
http://dx.doi.org/10.1098/rsos.191196...
; Gomes et al., 2023GOMES, G.N., LEITE, G.L.D., SOARES, M.A., GUANÃBENS, R.E.M., LEMES, P.G. and ZANUNCIO, J.C., 2023. Arthropod fauna on the abaxial and adaxial surfaces of Acacia mangium (Fabaceae) leaves. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 83, pp. e245536. http://dx.doi.org/10.1590/1519-6984.245536. PMid:34669792.
http://dx.doi.org/10.1590/1519-6984.2455...
; Lima et al., 2024LIMA, 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, pp. e252088. http://dx.doi.org/10.1590/1519-6984.252088. PMid:34755814.
http://dx.doi.org/10.1590/1519-6984.2520...
), besides it damages flowers such as Zantedeschia aethiopica (L.) Spreng. (Commelinales: Araceae) (Carvalho et al., 2018CARVALHO, 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...
). Trigona spinipes showed A.L. of 1.92/flower and, traditionally, what is recommended is the location and destruction of its nest.

The % I.I. was, also, effective in identifying solution sources on the system. The use of % I.I. is for cases in which it cannot mark and monitor the animal, identifying the cause of its mortality (Demolin-Leite, 2021DEMOLIN-LEITE, G.L., 2021. Importance indice: loss estimates and solution effectiveness on production. Canadian Journal of Agricultural Science, vol. 55, no. 2, pp. 1-7.), as done by Ecological Life Table (Henderson and Southwood, 2016HENDERSON, P.A. and SOUTHWOOD, T.E.R., 2016. Ecological methods. Oxford: John Wiley & Sons.). The evaluation of herbivorous insects and their natural enemies, including spiders, on C. brasiliense trees, was not done individually during their lives, nor would it be possible due to the height of these plants in Cerrado areas. But, with the application of this index, it was possible to determine the effects of these natural enemies on herbivores and fruit production per tree on the natural system.

The solution sources Z. armillatus, Crematogaster sp., Epipolops sp., P. termitarius, A. magistretti, and Sycophila sp. showed the highest % I.I. on C. brasiliense trees, increasing on system productivity by 0.56% (≈ 128 total saved fruits). Similar to the loss sources of production, this index showed the individual capacity of the natural enemies to reduce damage per L.S., and if the predation attack occurs in an aggregate and frequent way in the samples (Demolin-Leite, 2021DEMOLIN-LEITE, G.L., 2021. Importance indice: loss estimates and solution effectiveness on production. Canadian Journal of Agricultural Science, vol. 55, no. 2, pp. 1-7.). Crematogaster sp. reduced production loss per Carmenta sp. on fruits and E. rufomarginata on fruits, branches, and leaves, with N.A.L. of 0.44, 0.18, 0.11, and 0.31 per plant part/tree/evaluation, respectively; and those of Z. armillatus and P. termitarius that of E. rufomarginata on fruits, with N.A.L. of 0.39 and 0.86, respectively, per plant part/tree/evaluation.

The percentage of defoliation by herbivorous Lepidoptera and Coleoptera had a negative correlation with Crematogaster sp. and P. termitarius on C. brasiliense trees (Leite et al., 2012cLEITE, 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., 2012c. 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.), but Crematogaster sp. increased the abundance of Dikrella caryocar (Coelho, Leite and Da-Silva, 2014) (Hemiptera: Cicadellidae) and Pseudococcus sp. (Hemiptera: Pseudococcidae) on these trees (Leite et al., 2015LEITE, 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. http://dx.doi.org/10.1038/s41598-017-16954-6.https://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=29192234&dopt=Abstract
http://dx.doi.org/10.1038/s41598-017-169...
). Caryocar brasiliense loses its leaves in August/September with new ones in September (Leite et al., 2006LEITE, G.L.D., VELOSO, R.V.S., ZANUNCIO, J.C., FERNANDES, L.A. and ALMEIDA, C.I.M., 2006. Phenology of Caryocar brasiliense in the Brazilian Cerrado region. Forest Ecology and Management, vol. 236, no. 2-3, pp. 286-294. http://dx.doi.org/10.1016/j.foreco.2006.09.013.
http://dx.doi.org/10.1016/j.foreco.2006....
). The ants Crematogaster sp. and P. termitarius were more abundant during the formation of new leaves and flowers, with positive correlations, at end of the winter, probably due to the nectaries of leaves and flowers (Leite et al., 2012cLEITE, 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., 2012c. 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., 2012dLEITE, 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., 2012d. 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...
). Higher ant visitation to extrafloral nectaries can favor the production of flowers or fruits and reduce damage on C. brasiliense trees by herbivorous insects, such as Eunica bechina Talbot, 1928 (Lepidoptera: Nymphalidae), E. rufomarginata, Prodiplosis floricola (Felt, 1907) (Diptera: Cecidomyiidae), and petiole gall insects (Hymenoptera: Chalcidoidea) (Freitas and Oliveira, 1996FREITAS, 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...
; Oliveira, 1997OLIVEIRA, 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.1365-2435.19...
; Leite et al., 2012dLEITE, 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., 2012d. 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...
). The Zelus genus is an efficient predator in natural systems and commercial crops (Zhang et al., 2016ZHANG, G., HART, E.R. and WEIRAUCH, C., 2016. A taxonomic monograph of the assassin bug genus Zelus Fabricius (Hemiptera: Reduviidae): 71 species based on 10,000 specimens. Biodiversity Data Journal, vol. 4, no. 4, pp. e8150. http://dx.doi.org/10.3897/BDJ.4.e8150. PMid:27651730.
http://dx.doi.org/10.3897/BDJ.4.e8150...
). The predators Epipolops sp. and Z. armillatus and parasitoids A. magistretti and Sycophila sp., a major Eurytoma sp. parasitoid, are important in controlling galling insect Eurytoma sp. (Leite et al., 2017LEITE, G.L.D., VELOSO, R.V.S., 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. http://dx.doi.org/10.1038/s41598-017-16954-6. PMid:29192234.
http://dx.doi.org/10.1038/s41598-017-169...
). However, Z. armillatus may prefer attacking Eurytoma sp. galls parasitized by Sycophila sp., evidence of “prudence strategy” (Leite et al., 2017LEITE, G.L.D., VELOSO, R.V.S., 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. http://dx.doi.org/10.1038/s41598-017-16954-6. PMid:29192234.
http://dx.doi.org/10.1038/s41598-017-169...
), whereby predators fed on parasitized prey, preserving the healthy prey as a food reserve for future generations, without endangering prey populations (Slobodkin, 1968SLOBODKIN, L.B., 1968. How to be a predator. American Zoologist, vol. 8, no. 1, pp. 43-51. http://dx.doi.org/10.1093/icb/8.1.43.
http://dx.doi.org/10.1093/icb/8.1.43...
).

5. Conclusions

The % I.I. separated the loss sources (e.g., Carmenta sp. on fruits = 18.58%) on production reduction (e.g., 0.21%) and the solution sources (e.g., Crematogaster sp. = 11.61%) with total income gain (e.g., 0.56%) on the natural system (e.g., C. brasiliense trees), with the possibility to calculate, monetarily, these losses or effectiveness of the solutions. The % I.I. can help, to determine which pests, e.g. exotic mammals, insects, plant diseases, and weeds, cause the biggest problems in plant production and the best control methods (e.g., biological control) are more harmful or effective on the system (e.g., crops) and how much money is lost or saved. Here I tested the %I.I. This index can detect the loss or solution key-sources on a system, making it possible to obtain loss and income gain on some knowledge areas.

6. Acknowledgements

To the Dr. A.L. Matioli (Instituto Biológico, São Paulo, Brasil) (Acari), 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), Dr. O.H.H. Mielke (A. magistretti, Bruchophagus sp., Eulophidae, Hymenoptera, and Sycophila sp.) (CDZOO, Universidade Federal do Paraná, Paraná, Brasil), Dr. O.F.F. Souza (Termitidae) and Dr. P.S.F. Ferreira (Hemiptera) (Universidade Federal de Viçosa, Minas Gerais, Brasil), Dr. R.C. Monteiro (Thysanoptera) (ESALQ/USP, São Paulo, Brasil), and Dr. V.C. Maia (Alycaulini) and Dr. M.A.P. Azevedo (Eurytomidae) (Museu de História Natural, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brasil), by species identifications. The vouchers are IBSP 36921–36924 (Instituto Butantan, São Paulo, Brasil) for spiders, and 1595/02 and 1597/02 (CDZOO, Universidade Federal do Paraná, Paraná, Brasil) for insects.

References

  • 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
  • DAMASCENA, J.G., LEITE, G.L.D., SILVA, F.W.S., SOARES, M.A., GUAÑABENS, 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. Importance indice: loss estimates and solution effectiveness on production. Canadian Journal of Agricultural Science, vol. 55, no. 2, pp. 1-7.
  • 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
  • GOMES, G.N., LEITE, G.L.D., SOARES, M.A., GUANÃBENS, R.E.M., LEMES, P.G. and ZANUNCIO, J.C., 2023. Arthropod fauna on the abaxial and adaxial surfaces of Acacia mangium (Fabaceae) leaves. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 83, pp. e245536. http://dx.doi.org/10.1590/1519-6984.245536 PMid:34669792.
    » http://dx.doi.org/10.1590/1519-6984.245536
  • HENDERSON, P.A. and SOUTHWOOD, T.E.R., 2016. Ecological methods Oxford: John Wiley & Sons.
  • KREBS, C.J., 1989 [viewed 2 May 2018]. Bray-Curtis cluster analysis [online]. Available from: http://biodiversity-pro.software.informer.com/
    » http://biodiversity-pro.software.informer.com/
  • LEITE, G.L.D., 2014. Galling insects on Caryocar brasiliense Camb. (Caryocaraceae). In: G.W. FERNANDES and J.C. SANTOS, eds. Neotropical insect galls Berlin: Springer-Verlag, pp.179-192. http://dx.doi.org/10.1007/978-94-017-8783-3_12
    » http://dx.doi.org/10.1007/978-94-017-8783-3_12
  • LEITE, G.L.D., LOPES, P.S.N., ZANUNCIO, J.C., MARTINS, C.P.S., MOREIRA, T.M.B. and COSTA, R.I.F., 2016. Effects of environmental and architectural diversity of Caryocar brasiliense (Malpighiales: Caryocaraceae) on Edessa ruformaginata (Hemiptera: Pentatomidae) and its biology. Acta Scientiarum. Agronomy, vol. 38, no. 1, pp. 19-27. http://dx.doi.org/10.4025/actasciagron.v38i1.26244
    » http://dx.doi.org/10.4025/actasciagron.v38i1.26244
  • LEITE, G.L.D., NASCIMENTO, A.F., ALVES, S.M., LOPES, P.S.N., SALES, N.L.P. and ZANUNCIO, J.C., 2012b. The mortality of Caryocar brasiliense in northern Minas Gerais State, Brazil. Acta Scientiarum. Agronomy, vol. 34, no. 2, pp. 131-137. http://dx.doi.org/10.4025/actasciagron.v34i2.13120
    » http://dx.doi.org/10.4025/actasciagron.v34i2.13120
  • LEITE, G.L.D., VELOSO, R.V.S., AZEVEDO, A.M., ALMEIDA, C.I.M., SOARES, M.A., PEREIRA, A.I.A., LEMES, P.G. and ZANUNCIO, J.C., 2022. Distribution of galling insects and their parasitoids on Caryocar brasiliense tree crowns. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 82, pp. e235017. http://dx.doi.org/10.1590/1519-6984.235017 PMid:34076163.
    » http://dx.doi.org/10.1590/1519-6984.235017
  • LEITE, G.L.D., VELOSO, R.V.S., ZANUNCIO, J.C., ALMEIDA, C.I.M., 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., 2012c. 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.S., 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. http://dx.doi.org/10.1038/s41598-017-16954-6 PMid:29192234.
    » http://dx.doi.org/10.1038/s41598-017-16954-6
  • 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., 2012d. 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. http://dx.doi.org/10.1038/s41598-017-16954-6https://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=29192234&dopt=Abstract
    » http://dx.doi.org/10.1038/s41598-017-16954-6
  • LEITE, G.L.D., VELOSO, R.V.S., ZANUNCIO, J.C., FERNANDES, L.A. and ALMEIDA, C.I.M., 2006. Phenology of Caryocar brasiliense in the Brazilian Cerrado region. Forest Ecology and Management, vol. 236, no. 2-3, pp. 286-294. http://dx.doi.org/10.1016/j.foreco.2006.09.013
    » http://dx.doi.org/10.1016/j.foreco.2006.09.013
  • 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, pp. e252088. http://dx.doi.org/10.1590/1519-6984.252088 PMid:34755814.
    » http://dx.doi.org/10.1590/1519-6984.252088
  • 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
  • SERRA, B.D.V. and CAMPOS, L.A.O., 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, E.M., SILVA, R.S., RODRIGUES-SILVA, N., MILAGRES, C.C., BACCI, L. and PICANÇO, M.C., 2017. Assessment of the natural control of Neoleucinodes elegantalis in tomato cultivation using ecological life tables. Biocontrol Science and Technology, vol. 27, no. 4, pp. 525-538. http://dx.doi.org/10.1080/09583157.2017.1319911
    » http://dx.doi.org/10.1080/09583157.2017.1319911
  • SILVA, F.W.S., LEITE, G.L.D., GUAÑABENS, R.E.M., SAMPAIO, R.A., GUSMÃO, C.A.G. and ZANUNCIO, J.C., 2014. Spatial distribution of arthropods on Acacia mangium (Fabales: Fabaceae) trees as windbreaks in the Cerrado. The Florida Entomologist, vol. 97, no. 2, pp. 631-638. http://dx.doi.org/10.1653/024.097.0240
    » http://dx.doi.org/10.1653/024.097.0240
  • SILVA, J.L., DEMOLIN-LEITE, G.L., TAVARES, W.S., SILVA, F.W.S., 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, pp. 191196. http://dx.doi.org/10.1098/rsos.191196 PMid:32257306.
    » http://dx.doi.org/10.1098/rsos.191196
  • SISTEMA PARA ANÁLISES ESTATÍSTICAS E GENÉTICAS – SAEG, 2007 [viewed 2 May 2018]. Version 9.1 [online]. Available from: http://arquivo.ufv.br/saeg/
    » http://arquivo.ufv.br/saeg/
  • SLOBODKIN, L.B., 1968. How to be a predator. American Zoologist, vol. 8, no. 1, pp. 43-51. http://dx.doi.org/10.1093/icb/8.1.43
    » http://dx.doi.org/10.1093/icb/8.1.43
  • ZHANG, G., HART, E.R. and WEIRAUCH, C., 2016. A taxonomic monograph of the assassin bug genus Zelus Fabricius (Hemiptera: Reduviidae): 71 species based on 10,000 specimens. Biodiversity Data Journal, vol. 4, no. 4, pp. e8150. http://dx.doi.org/10.3897/BDJ.4.e8150 PMid:27651730.
    » http://dx.doi.org/10.3897/BDJ.4.e8150

Publication Dates

  • Publication in this collection
    11 Feb 2022
  • Date of issue
    2024

History

  • Received
    12 June 2021
  • Accepted
    09 Dec 2021
Instituto Internacional de Ecologia R. Bento Carlos, 750, 13560-660 São Carlos SP - Brasil, Tel. e Fax: (55 16) 3362-5400 - São Carlos - SP - Brazil
E-mail: bjb@bjb.com.br