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OCCURRENCE AND CHARACTERIZATION OF INSECT GALLS IN THE FLORESTA NACIONAL DE SILVÂNIA, BRAZIL

ABSTRACT

In the present paper we investigated the insect gall distribution along savanna and forest sites in the Floresta Nacional de Silvânia, Goiás, Brazil. The insect gall fauna was surveyed bi-monthly between December 2009 and June 2010. In total we found 186 insect gall morphotypes, distributed on 35 botanical families and 61 plant species. Ninety-nine insect gall morphotypes were recorded in the forest and 87 in the savanna. Gall-inducing insects belonged to Coleoptera, Diptera, Hemiptera, Lepidoptera and Thysanoptera, with highlight to Cecidomyiidae (Diptera) that induced 34.1% of the gall morphotypes. Parasitoids and/or inquilines were recorded in 38 morphotypes, mainly from the families Eulophidae, Eurytomidae and Torymidae (Hymenoptera). Fabaceae was the botanical family with the greatest richness of galls, followed by Asteraceae and Sapindaceae, being Protium (Burseraceae), Siparuna (Siparunaceae) and Serjania (Sapindaceae) the main host genera. This is the first systematic survey of insect galls realized in the Flona-Silvânia, which result in six plant species are recorded for the first time in Brazil as host of insect galls.

KEY-WORDS:
Cecidomyiidae; Cerrado; Fabaceae; Plant-insect interaction

RESUMO

No presente estudo foi investigada a distribuição de galhas de insetos ao longo de áreas de cerrado e floresta na Floresta Nacional de Silvânia, Goiás, Brasil. A fauna de insetos galhadores foi amostrada bimensalmente entre dezembro de 2009 e junho de 2010. No total foram encontrados 186 morfotipos de galhas de insetos, distribuídos em 35 famílias botânicas e 61 espécies de plantas. Foram registrados 99 morfotipos de galhas de insetos na floresta e 87 no cerrado. Os insetos galhadores pertenceram à Coleoptera, Diptera, Hemiptera, Lepidoptera e Thysanoptera, com destaque para Cecidomyiidae (Diptera) que induziu 34,1% dos morfotipos de galhas. Parasitoides e/ou inquilinos foram registrados em 38 morfotipos de galhas, principalmente das famílias Eulophidae, Eurytomidae e Torymidae (Hymenoptera). Fabaceae foi a família botânica com maior riqueza de galhas, seguida por Asteraceae e Sapindaceae, enquanto Protium (Burseraceae), Siparuna (Siparunaceae) e Serjania (Sapindaceae) foram os principais gêneros hospedeiros. Este é o primeiro levantamento sistemático de galhas de insetos na Flona-Silvânia, o que resultou em seis espécies de plantas sendo registradas pela primeira vez no Brasil como hospedeiras de galhas de insetos.

PALAVRAS-CHAVE:
Cecidomyiidae; Cerrado; Fabaceae; Interação inseto-planta

INTRODUCTION

The Cerrado is the second largest phytogeographical domain of Brazil, occupying 23% of the national territory (Oliveira & Marquis, 2002OLIVEIRA-FILHO, A.T. & RATTER, J.A. 2002. Vegetation physiognomies and wood flora of the bioma Cerrado. In: Oliveira, P.S. & Marquis, R.J. (Eds.). The Cerrados of Brazil: ecology and natural history of a Neotropical Savanna. Columbia, Columbia University Press . p. 91-120.). The region is composed by many different types of vegetation, which can be characterized in savanna (e.g., grasslands, rock fields and typical savannas) and forest formations (e.g., semidecidual forest and gallery forest) (Ribeiro & Walter, 2008RIBEIRO, J.F. & WALTER, B.M.T. 2008. As principais fitofisionomias do Bioma Cerrado. In: Sano, S.M.; Almeida, S.P. & Ribeiro, J.F. (Eds.). Cerrado: ecologia e flora. Brasília, Embrapa Cerrados. p. 151-212.). The great vegetation heterogeneity of Cerrado is caused by variations in fire, climate, water availability and soil fertility (Oliveira-Filho & Ratter, 2002OLIVEIRA-FILHO, A.T. & RATTER, J.A. 2002. Vegetation physiognomies and wood flora of the bioma Cerrado. In: Oliveira, P.S. & Marquis, R.J. (Eds.). The Cerrados of Brazil: ecology and natural history of a Neotropical Savanna. Columbia, Columbia University Press . p. 91-120.), turning the region in a mosaic of xeric (i.e., poor in water and nutrients) and mesic vegetation (i.e., rich in water and nutrients). Because of this great structural and floristic diversity the Cerrado is one of the hotspots of insect gall diversity in the globe (Araújo et al., 2014aARAÚJO, W.S.; SANTOS, B.B.; GUILHERME, F.A.G. & SCARELI-SANTOS, C. 2014a. Galling insects in the Brazilian Cerrado: ecological patterns and perspectives. In: Fernandes, G.W. & Santos, J.C. (Eds.). Neotropical Insect Galls. New York, Springer. p. 257-272.), which justify the efforts to diminish temporal and spatial gaps in the group sampling (e.g.,Araújo, 2011ARAÚJO, W.S. 2011. Can host plant richness be used as a surrogate for galling insect diversity? Tropical Conservation Science, 4:420-427.; Maia et al., 2014MAIA, V.C.; RODRIGUES, A.R.; ASCENDINO, S.H.S. & BOGGI, M. 2014. The insect gall collection of the Museu Nacional/Universidade Federal do Rio de Janeiro: biome cerrado, rupestrian fields. Brazilian Journal of Biology, 74:S207-S217.).

Taxonomic knowledge of galling insects in the Cerrado is scarce, because the most of galling species have not yet been described (Araújo et al., 2014aARAÚJO, W.S.; SANTOS, B.B.; GUILHERME, F.A.G. & SCARELI-SANTOS, C. 2014a. Galling insects in the Brazilian Cerrado: ecological patterns and perspectives. In: Fernandes, G.W. & Santos, J.C. (Eds.). Neotropical Insect Galls. New York, Springer. p. 257-272.). Because of this, inventories of insect galls in the Cerrado identify galling insects only at the order or family level, with Diptera (Cecidomyiidae), Lepidoptera and Hemiptera being the most speciose taxa (Gonçalves-Alvim & Fernandes, 2001GONÇALVES-ALVIM, S.J. & FERNANDES, G.W. 2001. Biodiversity of galling insects: historical, community and habitat effects in four neotropical savannas. Biodiversity and Conservation, 10:79-98.; Maia & Fernandes, 2004MAIA, V.C. & FERNANDES, G.W. 2004. Insect galls from Serra de São José (Tiradentes, MG, Brazil). Brazilian Journal of Biology, 6:423-445.; Araújo et al., 2011ARAÚJO, W.S.; SANTOS, B.B. & GOMES-KLEIN, V.L. 2011. Insect galls from Serra dos Pireneus, GO, Brazil. Biota Neotropica, 11:357-365.). Cecidomyiidae is responsible for approximately 70% of all gall morphospecies from the Cerrado (Araújo et al., 2014aARAÚJO, W.S.; SANTOS, B.B.; GUILHERME, F.A.G. & SCARELI-SANTOS, C. 2014a. Galling insects in the Brazilian Cerrado: ecological patterns and perspectives. In: Fernandes, G.W. & Santos, J.C. (Eds.). Neotropical Insect Galls. New York, Springer. p. 257-272.), being this also the main group of galling insects in the Neotropical region (Gagné, 1994GAGNÉ, R. 1994. The Gall Midges of the Neotropical Region. Cornell, Cornell University Press. 360p.). Furthermore, insect gall inventories in the Cerrado found recurrently that the Fabaceae is the most important host plant family (Fernandes et al., 1997FERNANDES, G.W.; ARAÚJO, R.C.; ARAÚJO, S.C.; LOMBARDI, J.A.; PAULA, A.S.; LOYOLA-JÚNIOR, R. & CORNELISSEN, T.G. 1997. Insect-galls from savanna and rocky fields of the Jequitinhonha valley, Minas Gerais, Brazil. Naturalia, 22:221-244.; Gonçalves-Alvim & Fernandes, 2001GONÇALVES-ALVIM, S.J. & FERNANDES, G.W. 2001. Biodiversity of galling insects: historical, community and habitat effects in four neotropical savannas. Biodiversity and Conservation, 10:79-98.; Maia & Fernandes, 2004MAIA, V.C. & FERNANDES, G.W. 2004. Insect galls from Serra de São José (Tiradentes, MG, Brazil). Brazilian Journal of Biology, 6:423-445.; Urso-Guimarães & Scareli-Santos, 2006URSO-GUIMARÃES, M.V. & SCARELLI-SANTOS, C. 2006. Galls and gall makers in plants from the Pé de Gigante Cerrado Reserve, Santa Rita do Passa Quatro, SP, Brazil. Brazilian Journal of Biology, 66:357-369.; Araújo et al., 2011ARAÚJO, W.S.; SANTOS, B.B. & GOMES-KLEIN, V.L. 2011. Insect galls from Serra dos Pireneus, GO, Brazil. Biota Neotropica, 11:357-365.). Other host plant families often recorded in studies performed in the Cerrado are the Asteraceae and Myrtaceae (Maia & Fernandes, 2004MAIA, V.C. & FERNANDES, G.W. 2004. Insect galls from Serra de São José (Tiradentes, MG, Brazil). Brazilian Journal of Biology, 6:423-445.; Urso-Guimarães & Scareli-Santos, 2006URSO-GUIMARÃES, M.V. & SCARELLI-SANTOS, C. 2006. Galls and gall makers in plants from the Pé de Gigante Cerrado Reserve, Santa Rita do Passa Quatro, SP, Brazil. Brazilian Journal of Biology, 66:357-369.; Malves & Frieiro-Costa, 2012MALVES, K. & FRIEIRO-COSTA, F.A. 2012. List of plants with galls induced by insects fromthe UNILAVRAS/Boqueirão Biological Reserve, Ingaí, State of Minas Gerais, Brazil. Check List, 8:426-431.). All these families are listed among those with the highest plant species richness in the Cerrado (Mendonça et al., 2008MENDONÇA, R.C.; FELFILI, J.M.; WALTER, B.M.T.; SILVA-JÚNIOR, M.C.; REZENDE, A.V.; FILGUEIRAS, T.S.; NOGUEIRA, P.E. & FAGG, C.W. 2008. Flora vascular do Bioma Cerrado: checklist com 12.356 espécies. In: Sano, S.M.; Almeida, S.P. & Ribeiro, J.F. (Eds.). Cerrado: ecologia e flora. Brasília, EMBRAPA. p. 421-1279.).

The vast majority of insect gall inventories in the Cerrado have been performed in southeastern Brazil, whereas other regions which host the largest Cerrado area are still poorly studied (review in Araújo et al., 2014aARAÚJO, W.S.; SANTOS, B.B.; GUILHERME, F.A.G. & SCARELI-SANTOS, C. 2014a. Galling insects in the Brazilian Cerrado: ecological patterns and perspectives. In: Fernandes, G.W. & Santos, J.C. (Eds.). Neotropical Insect Galls. New York, Springer. p. 257-272.). The Floresta Nacional de Silvânia (Flona-Silvânia) is a sustainable use conservation unit located in the city of Silvânia, State of Goiás, Midwest Brazil. The area of the park is of 466.55 ha being mostly composed by a flat tableland at 900 m asl (Francener et al., 2012FRANCENER, A.; HALL, C.F.; PORFÍRIO-JÚNIOR, E.D. & ARAÚJO, W.S. 2012. Flora fanerogâmica da Floresta Nacional de Silvânia, Goiás, Brasil. Enciclopédia Biosfera, 8:1263-1277.). The Flona-Silvânia exhibits almost all types of Cerrado vegetation, but mainly typical savanna and forest (gallery forest and semidecidual forest), which occupy 70% of the area of the park (Araújo et al., 2012ARAÚJO, W.S.; PORFÍRIO-JÚNIOR, E.D.; FRANCENER A. & HALL, C.F. 2012. Composição florística e estrutura fitossociológica de áreas de campo sujo e cerrado sentido restrito na Floresta Nacional de Silvânia, Goiás, Brasil. Insula Revista de Botânica, 41:42-58.). Recent studies in the park pointed a great phytophysiological complexity in the vegetation (Araújo et al., 2012ARAÚJO, W.S.; PORFÍRIO-JÚNIOR, E.D.; FRANCENER A. & HALL, C.F. 2012. Composição florística e estrutura fitossociológica de áreas de campo sujo e cerrado sentido restrito na Floresta Nacional de Silvânia, Goiás, Brasil. Insula Revista de Botânica, 41:42-58.), and a high floristic diversity, with 244 phanerogamic species recorded (Francener et al., 2012FRANCENER, A.; HALL, C.F.; PORFÍRIO-JÚNIOR, E.D. & ARAÚJO, W.S. 2012. Flora fanerogâmica da Floresta Nacional de Silvânia, Goiás, Brasil. Enciclopédia Biosfera, 8:1263-1277.). Therefore, the objective of the present study was to inventory the galling insects and their host plants in forest and savanna areas in the Flona-Silvânia, Goiás, Brazil.

MATERIAL AND METHODS

Study site

The study was performed in the Flona-Silvânia (Fig. 1) in areas of typical savanna (16°38’11.79”S and 48°39’50.82”W) and gallery forest (16°37’52.90”S and 48°39’52.38”W). The typical savanna vegetation is characterized by spaced trees and a matrix of shrubs and grasses, while the gallery forest is located on the banks of a stream and dominated by trees and high and closed canopy (Araújo et al., 2012ARAÚJO, W.S.; PORFÍRIO-JÚNIOR, E.D.; FRANCENER A. & HALL, C.F. 2012. Composição florística e estrutura fitossociológica de áreas de campo sujo e cerrado sentido restrito na Floresta Nacional de Silvânia, Goiás, Brasil. Insula Revista de Botânica, 41:42-58.). The climate of the Flona-Silvânia region is classified as Aw of Köppen (Alvares et al., 2013ALVARES, C.A.; STAPE, J.L.; SENTELHAS, P.C.; MORAES, J.L.G. & SPAROVEK, G. 2013. Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift, 22:711-728.), being humid tropical with well-defined dry (April to September) and rainy (October to March) seasons.

FIGURE 1:
Location and characterization of the study area. (A) Location of the Flona-Silvânia (marked by the star) in the city of Silvânia, State of Goiás, Midwest of Brazil. (B) Map of the Flona-Silvânia showing the areas of savanna (clear areas) and forest (dark areas).

Data collection

The insect gall sampling was done bi-monthly between December 2009 and June 2010 through active searches, with duration of 01h30min, along four fixed transects, being two in each vegetation type. In each transect, two collectors inspected the epigeous parts of all host plants and all observed insect galls were registered (Araújo et al., 2011ARAÚJO, W.S.; SANTOS, B.B. & GOMES-KLEIN, V.L. 2011. Insect galls from Serra dos Pireneus, GO, Brazil. Biota Neotropica, 11:357-365.; Santos et al., 2012SANTOS, B.B.; RIBEIRO, B.A.; SILVA, T.M. & ARAÚJO, W.S. 2012. Galhas de insetos em uma área de cerrado sentido restrito na região semi-urbana de Caldas Novas (Goiás, Brasil). Revista Brasileira de Biociências, 10:439-445.; Silva et al., 2015SILVA, T.M.; ARAÚJO, W.S. & SANTOS, B.B. 2015. Ocorrência e caracterização de galhas de insetos em um fragmento de mata semicaducifólia do Campus Samambaia, Goiânia, GO, Brasil. Revista de Biologia Neotropical, 12:26-38.). Samples of each insect galls were photographed, collected and transported individually in labeled plastic bags. Plant branches of each host plant were collected, part of the material being dried and mounted for botanical identification, the remainder being used to obtain the immature and adult insects, in the laboratory. The identification of the host plant species was made by comparison with the collection of UFG herbarium. We checked plant species nomenclature and synonymy using the database of The Plant List (2017) (http://theplantlist.org).

The collected insect galls were taken to the laboratory of Universidade Federal de Goiás (UFG) and packed in plastic container with moistened paper. Insect galls were classified into morphotypes using the host plant species and external morphology (organ of occurrence, shape, color, pubescence and size). Nomenclature of the insect gall morphotypes was standardized according to the proposed by Isaías et al. (2013ISAIAS, R.M.S.; CARNEIRO, R.G.S.; OLIVEIRA, D.C. & SANTOS, J.C. 2013. Illustrated and annotated checklist of Brazilian gall morphotypes. Neotropical Entomology, 42:230-239.). In laboratory, the galls were daily observed to verify the emergence of adult insects or dissected to obtainment of immature insects. All insects were fixed in 70% alcohol and identified using the insect gall literature from Neotropic and Brazil (e.g.,Gagné, 1994GAGNÉ, R. 1994. The Gall Midges of the Neotropical Region. Cornell, Cornell University Press. 360p.; Maia & Fernandes, 2004MAIA, V.C. & FERNANDES, G.W. 2004. Insect galls from Serra de São José (Tiradentes, MG, Brazil). Brazilian Journal of Biology, 6:423-445.; Araújo et al., 2011ARAÚJO, W.S.; SANTOS, B.B. & GOMES-KLEIN, V.L. 2011. Insect galls from Serra dos Pireneus, GO, Brazil. Biota Neotropica, 11:357-365.). Gall morphotypes were used as a surrogate for species of gall-inducing insects because there is a consensus in the literature about host-specificity and morphological-fidelity of insect galls (reviewed in Carneiro et al., 2009aCARNEIRO, M.A.A.; BRANCO, C.S.A.; BRAGA, C.E.D.; ALMADA, E.D.; COSTA, M.B.M.; MAIA, V.C. & FERNANDES, G.W. 2009a. Are gall midge species (Diptera, Cecidomyiidae) host-plant specialists? Revista Brasileira de Entomologia, 53:365-378.). Galls, insects and host plants were deposited in the insect gall collection of the Laboratory of Entomology of UFG.

RESULTS

A total of 186 insect gall morphotypes from five insect orders, and 61 species of host plants from 35 plant families were recorded in the Flona-Silvânia (Table 1, Figs. 2-6). The average number of gall morphotypes per plant species was 3.0. We found gall-inducing insects belonging to Coleoptera, Diptera, Hemiptera, Lepidoptera and Thysanoptera (Table 2). The most common insect taxon was Cecidomyiidae (Diptera), which induced 64 (34.4%) gall morphotypes. Insect galls induced by other insect orders summed 9.7% of the insect gall morphotypes. The taxa of gall-inducing insects could not be determined for 55% of the gall morphotypes. Other insects such as hymenopteran parasitoids (Chalcididae, Braconidae, Elasmidae, Eulophidae, Eupelmidae, Eurytomidae, Tetracampidae, Torymidae and Trichogrammatidae), and dipteran (Sciaridae and Brachycera), hymenopteran (Tanaostigmatidae) and thysanopteran (Phlaeothripidae) inquilines occurred in 38 (20%) insect galls (see Table 1).

TABLE 1:
Characterization of the insect gall morphotypes recorded in host plants of gallery forest (F) and typical savanna (S) vegetation in the Flona-Silvânia, Goiás, Brazil.

FIGURE 2:
Insect galls of Flona-Silvânia, Goiás, Brazil. (A) Acanthaceae sp. (Gall 1), (B) Anacardiaceae sp. (Gall 5), (C) Lithraea molleoides (Vell.) Engl (Gall 7), (D) Xylopia sericea A. St.-Hil. (Gall 8), (E) Aspidosperma sp. (Gall 10), (F) Aspidosperma tomentosum Mart. (Gall 11), (G) A. tomentosum (Gall 12), (H) Asteraceae sp. (Gall 14), (I) Asteraceae sp. (Gall 15), (J) Asteraceae sp. (Gall 16), (K) Eremanthus sp. (Gall 19), (L) Eremanthus sp. (Gall 20), (M) Gochnatia barrosii Cabrera (Gall 21), (N) G. barrosii (Gall 22), (O) Piptocarpha rotundifolia (Less.) Baker (Gall 27), (P) Asteraceae sp. (Gall 29), (Q) Fridericia sp. (Gall 31), (R) Fridericia sp. (Gall 32), (S) Protium heptaphyllum (Aubl.) Marchand (Gall 35), (T) P. heptaphyllum (Gall 36), (U) P. heptaphyllum (Gall 37), (V) P. heptaphyllum (Gall 39), (W) P. heptaphyllum (Gall 43), (X) Hirtella sp. (Gall 58).

FIGURE 3:
Insect galls of Flona-Silvânia, Goiás, Brazil. (A) Kielmeyera sp. (Gall 60), (B) Connarus suberosus Planch. (Gall 62), (C) Davilla elliptica A. St.-Hil. (Gall 63), (D) D. elliptica (Gall 64), (E) D. elliptica (Gall 65), (F) Dilleniaceae sp. (Gall 67), (G) Dilleniaceae sp. (Gall 68), (H) Doliocarpus sp. (Gall 69), (I) Diospyros sp. (Gall 70), (J) Erythroxylum sp. (Gall 72), (K) Erythroxylum suberosum A. St.-Hil. (Gall 74), (L) E. suberosum (Gall 75), (M) Manihot sp. (Gall 76), (N) Andira paniculata Benth. (Gall 77), (O) A. paniculata (Gall 78), (P) Bauhinia rufa (Bong.) Steud. (Gall 79), (Q) B. rufa (Gall 80), (R) B. rufa (Gall 81), (S) B. rufa (Gall 82), (T) B. rufa (Gall 83), (U) B. rufa (Gall 84), (V) B. rufa (Gall 85), (W) B. rufa (Gall 86), (X) Bauhinia sp. (Gall 87).

FIGURE 4:
Insect galls of Flona-Silvânia, Goiás, Brazil. (A) Copaifera langsdorffii Desf. (Gall 90), (B) C. langsdorffii (Gall 91), (C) C. langsdorffii (Gall 92), (D) Inga sp. (Gall 94), (E) Lamiaceae sp. (Gall 96), (F) Lauraceae sp. (Gall 97), (G) Nectandra sp. (Gall 99), (H) Strychnos pseudoquina A. St.-Hil. (Gall 100), (I) Diplusodon sp. (Gall 101), (J) Byrsonima verbascifolia (L.) DC. (Gall 102), (K) B. verbascifolia (Gall 103), (L) B. verbascifolia (Gall 105), (M) B. verbascifolia (Gall 106), (N) Peixotoa goiana C.E. Anderson (Gall 107), (O) P. goyana (Gall 108), (P) Malvaceae sp. (Gall 110), (Q) Melastomataceae sp. (Gall 113), (R) Guarea sp. (Gall 114), (S) Meliaceae sp. (Gall 115), (T) Eugenia bimarginata DC. (Gall 118), (U) Myrtaceae sp. (Gall 120), (V) Myrtaceae sp. (Gall 122), (W) Myrtaceae sp. (Gall 123), (X) Myrtaceae sp. (Gall 124).

FIGURE 5:
Insect galls of Flona-Silvânia, Goiás, Brazil. (A) Myrtaceae sp. (Gall 125), (B) Myrtaceae sp. (Gall 126), (C) Myrtaceae sp. (Gall 127), (D) Ouratea hexasperma (A. St.-Hil.) Baill. (Gall 132), (E) Ouratea sp. (Gall 133), (F) Piper arboreum Aubl. (Gall 134), (G) Roupala montana Aubl. (Gall 135), (H) Roupala sp. (Gall 137), (I) Roupala sp. (Gall 139), (J) Cordiera macrophylla (K. Schum.) Kuntze (Gall 140), (K) Palicourea rigida Kunth (Gall 141), (L) Rubiaceae sp. (Gall 143), (M) Rubiaceae sp. (Gall 146), (N) Rubiaceae sp. (Gall 149), (O) Sapindaceae sp. (Gall 155), (P) Serjania sp. (Gall 161), (Q) Serjania sp. (Gall 164), (R) Serjania sp. (Gall 165), (S) Serjania sp. (Gall 166), (T) Serjania sp. (Gall 167), (U) Siparuna guianensis Aubl. (Gall 170), (V) S. guianensis Gall 171), (W) S. guianensis (Gall 173), (X) S. guianensis (Gall 174).

FIGURE 6:
Insect galls of Flona-Silvânia, Goiás, Brazil. (A) Gall 175), (B) Siparuna guianensis Aubl. (Gall 176), (C) S. guianensis (Gall 178), (D) S. guianensis (Gall 179), (E) Styrax ferrugineus Nees and Mart. (Gall 181), (F) S. ferrugineus (Gall 182), (G) Qualea grandiflora Mart. (Gall 184), (H) Q. grandiflora (Gall 185).

TABLE 2:
Insect order, number of insect gall morphotypes and number of host plant species recorded in the Flona-Silvânia, Goiás, Brazil.

The plant families that showed the greatest richness of insect galls were Fabaceae, with 18 morphotypes, Asteraceae with 17, Sapindaceae with 16, Burseraceae and Myrtaceae with 14, Siparunaceae with 12, and Celastraceae and Rubiaceae with 10 morphotypes (Table 3). The remaining families had less than 10 insect gall morphotypes each. The plant genera Protium (Burseraceae), Siparuna (Siparunaceae), Serjania (Sapindaceae) and Bauhinia (Fabaceae) were the richest hosts in number of insect gall morphotypes (14, 12, 12 and 10, respectively). Also noteworthy are the plant species Protium heptaphyllum (Aubl.) Marchand, Siparuna guianensis Aubl. and Serjania sp. that hosted 14, 12 and 12 insect gall morphotypes, respectively.

TABLE 3:
Number of insect gall morphotypes and host plant species in the different host plant families recorded in the Flona-Silvânia, Goiás, Brazil.

About the gall occurrence and morphology, most of the recorded insect galls occurred on leaf lamina (68.2%), and were fusiform (38.7%), greens (38.7%) and glabrous (37.6%). Among the 61 host plant species listed in the survey, six species (9.8%) have the first report hosting galls: Cordiera macrophylla (K. Schum.) Kuntze, Eugenia bimarginata DC., Gochnatia barrosii Cabrera, Lithraea molleoides (Vell.) Engl, Peixotoa goiana C.E. Anderson and Xylopia sericea A. St.-Hil. These plant species combined hosted 15 gall morphotypes, representing 8.0% of total. Considering the different sampled habitats, we recorded 99 insect gall morphotypes in the forest and 87 morphotypes in the savanna vegetation, being that none insect gall morphotype occurred in both habitats (Table 1).

DISCUSSION

Compared to previous inventories of insect galls in the Brazilian Cerrado (Table 4), our results indicated high insect gall diversity in the Flona-Silvânia. For example, the number of insect gall morphotypes recorded in our study stays behind only of the 241 morphotypes recorded in the Serra do Espinhaço by Carneiro et al. (2009bCARNEIRO, M.A.A.; BORGES, R.A.X.; ARAÚJO, A.P.A. & FERNANDES, G.W. 2009b. Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, Minas Gerais, Brasil. Revista Brasileira de Entomologia, 53:570-592.) and of the 236 morphotypes registered in the Vale do Jequitinhonha by Fernandes et al. (1997FERNANDES, G.W.; ARAÚJO, R.C.; ARAÚJO, S.C.; LOMBARDI, J.A.; PAULA, A.S.; LOYOLA-JÚNIOR, R. & CORNELISSEN, T.G. 1997. Insect-galls from savanna and rocky fields of the Jequitinhonha valley, Minas Gerais, Brazil. Naturalia, 22:221-244.), both localities situated in the State of Minas Gerais, Southeastern Brazil). It is important to note that in both these studies the authors sampled, for less time, a higher number of localities along the Espinhaço mountain ranges (60 sites sampled one single time by Carneiro et al., 2009bCARNEIRO, M.A.A.; BORGES, R.A.X.; ARAÚJO, A.P.A. & FERNANDES, G.W. 2009b. Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, Minas Gerais, Brasil. Revista Brasileira de Entomologia, 53:570-592. and 10 sites sampled two times by Fernandes et al., 1997FERNANDES, G.W.; ARAÚJO, R.C.; ARAÚJO, S.C.; LOMBARDI, J.A.; PAULA, A.S.; LOYOLA-JÚNIOR, R. & CORNELISSEN, T.G. 1997. Insect-galls from savanna and rocky fields of the Jequitinhonha valley, Minas Gerais, Brazil. Naturalia, 22:221-244.), unlike our study that sampled only two sites by four times. We also found that the average number of gall morphotypes per plant species was 3.0, which is high when compared to other Cerrado areas (Table 4). These variations in the insect gall richness and number of gall morphotypes per plant species can be explained by differences in the sampling type (e.g., fixed transects, random walks), collection effort (e.g., sampling duration and number of collectors) and sampled host plants (e.g., only woody plants or all herbs, shrubs and trees).

TABLE 4:
Number of insect gall morphotypes, host plant species, host plant families and mean number of galls per host plant species in different localities of the Brazilian Cerrado. Modified of Araújo et al. (2014ARAÚJO, W.S.; SOBRAL, F.L. & MARACAHIPES, L. 2014B. Insect galls of the Parque Nacional das Emas (Mineiros, GO, Brazil). Check List, 10:1445-1451.a).

Our results are in agreement with previous studies in the Brazilian savannas that point the dominance of gall-midges as gallers (Maia & Fernandes, 2004MAIA, V.C. & FERNANDES, G.W. 2004. Insect galls from Serra de São José (Tiradentes, MG, Brazil). Brazilian Journal of Biology, 6:423-445.; Santos et al., 2010SANTOS, B.B.; FERREIRA, H.D. & ARAÚJO, W.S. 2010. Ocorrência e caracterização de galhas em uma área de floresta estacional semidecídua em Goiânia, Goiás. Acta Botanica Brasilica, 24:217-223.; Araújo et al., 2011ARAÚJO, W.S.; SANTOS, B.B. & GOMES-KLEIN, V.L. 2011. Insect galls from Serra dos Pireneus, GO, Brazil. Biota Neotropica, 11:357-365., 2014bARAÚJO, W.S.; SOBRAL, F.L. & MARACAHIPES, L. 2014B. Insect galls of the Parque Nacional das Emas (Mineiros, GO, Brazil). Check List, 10:1445-1451.; Nogueira et al., 2016NOGUEIRA, R.M.; COSTA, E.C.; CARVALHO-FERNANDES, S.P. & SANTOS-SILVA, J. 2016. Insect galls from Serra Geral, Caetité, BA, Brazil. Biota Neotropica, 16:e20150035.; Urso-Guimarães et al., 2016URSO-GUIMARÃES, M.V.; CASTELLO, A.C.D.; KATAOKA, E.Y. & KOCH, I. 2016. Characterization of entomogen galls from Mato Grosso do Sul, Brazil. Revista Brasileira de Entomologia, 61:25-42.). Cecidomyiidae is considered the main galling insect group in the world with more of 6,000 known species (Gagné & Jaschhof, 2014GAGNÉ, R. & JASCHHOF, M. 2014. A catalog of the Cecidomyiidae (Diptera) of the world. Digital version 2. Entomological Society of Washington. 493p.), and a huge estimated number of species not yet known (Araújo et al., 2014aARAÚJO, W.S.; SANTOS, B.B.; GUILHERME, F.A.G. & SCARELI-SANTOS, C. 2014a. Galling insects in the Brazilian Cerrado: ecological patterns and perspectives. In: Fernandes, G.W. & Santos, J.C. (Eds.). Neotropical Insect Galls. New York, Springer. p. 257-272.; Grandez-Rios et al., 2015GRANDEZ-RIOS, J.M.; GARCÍA-VILLACORTA, R.; CUEVAS-REYES, P. & ARAÚJO, W.S. 2015. Insectos inductores de agallas en América Latina: ecología, importancia y nuevas perspectivas. Revista de Biologia Neotropical, 12:92-103.). In the Cerrado, cecidomyiids are responsible for approximately 70% of all known gall morphospecies (Araújo et al., 2014aARAÚJO, W.S.; SANTOS, B.B.; GUILHERME, F.A.G. & SCARELI-SANTOS, C. 2014a. Galling insects in the Brazilian Cerrado: ecological patterns and perspectives. In: Fernandes, G.W. & Santos, J.C. (Eds.). Neotropical Insect Galls. New York, Springer. p. 257-272.). Although in the present study gall-midges induced only 34.4% of gall morphotypes, since we could not get the insect inducers for most galls, Cecidomyiidae galls accounted for approx. 76% of the morphotypes when considering only galls for which the inducer was obtained. Hemiptera and Lepidoptera were other important groups of galling insects obtained from Flona-Silvânia, which is in accordance with the general pattern found in Cerrado areas (reviewed in Araújo et al., 2014aARAÚJO, W.S.; SANTOS, B.B.; GUILHERME, F.A.G. & SCARELI-SANTOS, C. 2014a. Galling insects in the Brazilian Cerrado: ecological patterns and perspectives. In: Fernandes, G.W. & Santos, J.C. (Eds.). Neotropical Insect Galls. New York, Springer. p. 257-272.).

Possible explanations for the low emergence of gall-inducers in the laboratory can be the immature insects have not completed their development after the galls were detached from the plants or galls collected were already empty. Because insect galls remain in the plant even after insects have hatched, some galls may have been collected after the emergence of insects. Other possible explanation can be the high incidence of parasitoids. We found hymenopteran parasitoids from several families in 20% of the gall morphotypes. Hymenopteran parasitoids are very frequent in Neotropical insect galls (Araújo et al., 2014aARAÚJO, W.S.; SANTOS, B.B.; GUILHERME, F.A.G. & SCARELI-SANTOS, C. 2014a. Galling insects in the Brazilian Cerrado: ecological patterns and perspectives. In: Fernandes, G.W. & Santos, J.C. (Eds.). Neotropical Insect Galls. New York, Springer. p. 257-272.) and are among the main causes of galler mortality (Maia & Azevedo, 2009MAIA, V.C. & AZEVEDO, M.A.P. 2009. Micro-himenópteros associados com galhas de Cecidomyiidae (Diptera) em Restingas do Estado do Rio de Janeiro (Brasil). Biota Neotropica, 9:151-164.).

Many inventories on the gall diversity in the Cerrado indicate Fabaceae (Fernandes et al., 1997FERNANDES, G.W.; ARAÚJO, R.C.; ARAÚJO, S.C.; LOMBARDI, J.A.; PAULA, A.S.; LOYOLA-JÚNIOR, R. & CORNELISSEN, T.G. 1997. Insect-galls from savanna and rocky fields of the Jequitinhonha valley, Minas Gerais, Brazil. Naturalia, 22:221-244.; Maia & Fernandes, 2004MAIA, V.C. & FERNANDES, G.W. 2004. Insect galls from Serra de São José (Tiradentes, MG, Brazil). Brazilian Journal of Biology, 6:423-445.; Urso-Guimarães & Scareli-Santos, 2006URSO-GUIMARÃES, M.V. & SCARELLI-SANTOS, C. 2006. Galls and gall makers in plants from the Pé de Gigante Cerrado Reserve, Santa Rita do Passa Quatro, SP, Brazil. Brazilian Journal of Biology, 66:357-369.; Santos et al., 2010SANTOS, B.B.; FERREIRA, H.D. & ARAÚJO, W.S. 2010. Ocorrência e caracterização de galhas em uma área de floresta estacional semidecídua em Goiânia, Goiás. Acta Botanica Brasilica, 24:217-223.; Araújo et al., 2014ARAÚJO, W.S.; SOBRAL, F.L. & MARACAHIPES, L. 2014B. Insect galls of the Parque Nacional das Emas (Mineiros, GO, Brazil). Check List, 10:1445-1451.b; Nogueira et al., 2016NOGUEIRA, R.M.; COSTA, E.C.; CARVALHO-FERNANDES, S.P. & SANTOS-SILVA, J. 2016. Insect galls from Serra Geral, Caetité, BA, Brazil. Biota Neotropica, 16:e20150035.) and Asteraceae (Carneiro et al., 2009CARNEIRO, M.A.A.; BORGES, R.A.X.; ARAÚJO, A.P.A. & FERNANDES, G.W. 2009b. Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, Minas Gerais, Brasil. Revista Brasileira de Entomologia, 53:570-592.b; Fernandes et al., 1997FERNANDES, G.W.; ARAÚJO, R.C.; ARAÚJO, S.C.; LOMBARDI, J.A.; PAULA, A.S.; LOYOLA-JÚNIOR, R. & CORNELISSEN, T.G. 1997. Insect-galls from savanna and rocky fields of the Jequitinhonha valley, Minas Gerais, Brazil. Naturalia, 22:221-244.; Malves & Frieiro-Costa, 2012MALVES, K. & FRIEIRO-COSTA, F.A. 2012. List of plants with galls induced by insects fromthe UNILAVRAS/Boqueirão Biological Reserve, Ingaí, State of Minas Gerais, Brazil. Check List, 8:426-431.) as the most important host families, which were also observed in the present study. Araújo et al. (2014aARAÚJO, W.S.; SANTOS, B.B.; GUILHERME, F.A.G. & SCARELI-SANTOS, C. 2014a. Galling insects in the Brazilian Cerrado: ecological patterns and perspectives. In: Fernandes, G.W. & Santos, J.C. (Eds.). Neotropical Insect Galls. New York, Springer. p. 257-272.) discussed that the main explanation for the high insect gall richness hosted by Fabaceae and Asteraceae in the Cerrado is its high number of plant species. There is the expectation that the higher the species number in the plant family higher is the galling diversity that they host (Araújo, 2011ARAÚJO, W.S. 2011. Can host plant richness be used as a surrogate for galling insect diversity? Tropical Conservation Science, 4:420-427.; Gonçalves-Alvim & Fernandes, 2001GONÇALVES-ALVIM, S.J. & FERNANDES, G.W. 2001. Biodiversity of galling insects: historical, community and habitat effects in four neotropical savannas. Biodiversity and Conservation, 10:79-98.). Additionally, we found that the host plants of the genera Protium (Burseraceae), Siparuna (Siparunaceae), Serjania (Sapindaceae) and Bauhinia (Fabaceae) were the most diverse in insect gall morphotypes, in line with recent studies in the Brazilian Cerrado (Silva et al., 2015SILVA, T.M.; ARAÚJO, W.S. & SANTOS, B.B. 2015. Ocorrência e caracterização de galhas de insetos em um fragmento de mata semicaducifólia do Campus Samambaia, Goiânia, GO, Brasil. Revista de Biologia Neotropical, 12:26-38.; Nogueira et al., 2016NOGUEIRA, R.M.; COSTA, E.C.; CARVALHO-FERNANDES, S.P. & SANTOS-SILVA, J. 2016. Insect galls from Serra Geral, Caetité, BA, Brazil. Biota Neotropica, 16:e20150035.; Urso-Guimarães et al., 2016URSO-GUIMARÃES, M.V.; CASTELLO, A.C.D.; KATAOKA, E.Y. & KOCH, I. 2016. Characterization of entomogen galls from Mato Grosso do Sul, Brazil. Revista Brasileira de Entomologia, 61:25-42.). Insect gall morphotypes vary greatly in the occurrence and morphology, which can be explained by high specificity of gall-inducing insects associated to their host plants (Carneiro et al., 2009aCARNEIRO, M.A.A.; BRANCO, C.S.A.; BRAGA, C.E.D.; ALMADA, E.D.; COSTA, M.B.M.; MAIA, V.C. & FERNANDES, G.W. 2009a. Are gall midge species (Diptera, Cecidomyiidae) host-plant specialists? Revista Brasileira de Entomologia, 53:365-378.). In the present study, the most of insect gall occurred in the leaves (leaf lamina), and the more common gall morphology was fusiform shape, green color and absence of pubescence, which also was observed in previous studies in the Cerrado (Urso-Guimarães et al., 2003URSO-GUIMARÃES, M.V.; SCARELI-SANTOS, C. & BONIFÁCIO-SILVA, A.C. 2003. Occurrence and characterization of entomogen galls in plants from natural vegetation areas in Delfinópolis, MG, Brazil. Brazilian Journal of Biology, 63:705-715.; Maia & Fernandes, 2004MAIA, V.C. & FERNANDES, G.W. 2004. Insect galls from Serra de São José (Tiradentes, MG, Brazil). Brazilian Journal of Biology, 6:423-445.; Araújo et al., 2011ARAÚJO, W.S.; SANTOS, B.B. & GOMES-KLEIN, V.L. 2011. Insect galls from Serra dos Pireneus, GO, Brazil. Biota Neotropica, 11:357-365.; Malves & Frieiro-Costa, 2012MALVES, K. & FRIEIRO-COSTA, F.A. 2012. List of plants with galls induced by insects fromthe UNILAVRAS/Boqueirão Biological Reserve, Ingaí, State of Minas Gerais, Brazil. Check List, 8:426-431.).

Comparisons between different vegetation types in the Cerrado have pointed higher insect gall richness in the sclerophyllous habitats, with savannas often having greater species richness than the forests (review in Araújo et al., 2014aARAÚJO, W.S.; SANTOS, B.B.; GUILHERME, F.A.G. & SCARELI-SANTOS, C. 2014a. Galling insects in the Brazilian Cerrado: ecological patterns and perspectives. In: Fernandes, G.W. & Santos, J.C. (Eds.). Neotropical Insect Galls. New York, Springer. p. 257-272.). Our results contrast with this pattern of higher frequency of insect galls in xeric habitats than in mesic ones. A possible explanation to this distinct pattern is the greater frequency of super-host taxa in the forest (e.g., Protium, Serjania and Siparuna), which can increment significantly the insect gall richness at the local level (Araújo et al., 2014aARAÚJO, W.S.; SANTOS, B.B.; GUILHERME, F.A.G. & SCARELI-SANTOS, C. 2014a. Galling insects in the Brazilian Cerrado: ecological patterns and perspectives. In: Fernandes, G.W. & Santos, J.C. (Eds.). Neotropical Insect Galls. New York, Springer. p. 257-272.). Even though some of these plant genera also occur in the savanna, they are more common in the forest, where most of their gall morphotypes were registered.

This is the first systematic survey of insect galls realized in the Flona-Silvânia. In this context, 186 gall morphotypes have been described for this area and six new records of host plants were presented from Brazil. The higher number of insect galls recorded in the park, compared to previous studies in the Brazilian Cerrado, demonstrates the importance of the inventories of insect galls. In front of growing fragmentation and loss of vegetation cover of the biome, which have caused the extinction of many species and threatened the Cerrado biodiversity (Klink & Machado, 2005KLINK, C.A. & MACHADO, R.B. 2005. Conservation of the Brazilian Cerrado. Conservation Biology, 19:707-713.), inventories of insect gall diversity in the region must be done emergently (Araújo, 2011ARAÚJO, W.S.; SANTOS, B.B. & GOMES-KLEIN, V.L. 2011. Insect galls from Serra dos Pireneus, GO, Brazil. Biota Neotropica, 11:357-365.).

ACKNOWLEDGEMENTS

We thank to trainees of Laboratory of Entomology (UFG) for help in the field and laboratory; to the team of the Laboratory of Morphology and Plant Taxonomy (UFG) for the help in the identification of the host plants; to PRPPG-UFG for the grant to the first author, and the Instituto de Ciências Biológicas (UFG) for the logistical support.

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    Editor Responsável: Carlos José Einicker Lamas
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Publication Dates

  • Publication in this collection
    2017

History

  • Received
    29 June 2017
  • Accepted
    15 Sept 2017
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