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Papéis Avulsos de Zoologia

Print version ISSN 0031-1049On-line version ISSN 1807-0205

Pap. Avulsos Zool. vol.57 no.32 São Paulo  2017

http://dx.doi.org/10.11606/0031-1049.2017.57.32 

Article

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

BÁRBARA ARAÚJO RIBEIRO BERGAMINI1  3 

LEONARDO LIMA BERGAMIN1  4 

BENEDITO BAPTISTA DOS SANTOS1  5 

WALTER SANTOS DE ARAÚJO2  6 

1Universidade Federal de Goiás (UFG), Instituto de Ciências Biológicas (ICB), Departamento de Ecologia (DECOL). Avenida Esperança, 1.533, Campus Samambaia (Campus II), CEP 74690-900, Goiânia, GO, Brasil.

2Universidade Estadual de Montes Claros (UNIMONTES), Centro de Ciências Biológicas e da Saúde (CCBS), Depto. de Biologia Geral. Avenida Rui Braga, s/nº, Campus Universitário Professor Darcy Ribeiro, Vila Mauricéia, CEP 39401-089, Montes Claros, MG, Brasil.

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, 2002). 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, 2008). The great vegetation heterogeneity of Cerrado is caused by variations in fire, climate, water availability and soil fertility (Oliveira-Filho & Ratter, 2002), 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., 2014a), which justify the efforts to diminish temporal and spatial gaps in the group sampling (e.g.,Araújo, 2011; Maia et al., 2014).

Taxonomic knowledge of galling insects in the Cerrado is scarce, because the most of galling species have not yet been described (Araújo et al., 2014a). 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, 2001; Maia & Fernandes, 2004; Araújo et al., 2011). Cecidomyiidae is responsible for approximately 70% of all gall morphospecies from the Cerrado (Araújo et al., 2014a), being this also the main group of galling insects in the Neotropical region (Gagné, 1994). Furthermore, insect gall inventories in the Cerrado found recurrently that the Fabaceae is the most important host plant family (Fernandes et al., 1997; Gonçalves-Alvim & Fernandes, 2001; Maia & Fernandes, 2004; Urso-Guimarães & Scareli-Santos, 2006; Araújo et al., 2011). Other host plant families often recorded in studies performed in the Cerrado are the Asteraceae and Myrtaceae (Maia & Fernandes, 2004; Urso-Guimarães & Scareli-Santos, 2006; Malves & Frieiro-Costa, 2012). All these families are listed among those with the highest plant species richness in the Cerrado (Mendonça et al., 2008).

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., 2014a). 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., 2012). 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., 2012). Recent studies in the park pointed a great phytophysiological complexity in the vegetation (Araújo et al., 2012), and a high floristic diversity, with 244 phanerogamic species recorded (Francener et al., 2012). 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., 2012). The climate of the Flona-Silvânia region is classified as Aw of Köppen (Alvares et al., 2013), 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., 2011; Santos et al., 2012; Silva et al., 2015). 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. (2013). 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, 1994; Maia & Fernandes, 2004; Araújo et al., 2011). 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., 2009a). 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. 

Host plants Insect gall morphology Insect taxa
Plant family Plant species Morphotype Organ Shape Color Surface Size (cm) Occurrence Galling insects Other insects
Acanthaceae Acanthaceae sp. Gall 1 Leaf/midvein Fusiform Brown Glabrous 0.7 F - -
Gall 2 Leaf/midvein Fusiform Green Pubescent - F Lepidoptera -
Gall 3 Leaf/midvein Fusiform Green Roughened 0.5 F - -
Gall 4 Leaf/midvein Fusiform Yellow Glabrous - F - Chalcididae (Hymenoptera) (parasitoid)
Anacardiaceae Anacardiaceae sp. Gall 5 Leaf Globoid Green Roughened 0.2 F - Eurytomidae (Hymenoptera) (parasitoid)
Lithraea molleoides (Vell.) Engl Gall 6 Leaf Lenticular Green Roughened 0.2 S Coccoidea (Hemiptera) -
Gall 7 Leaf Lenticular Pink Roughened 0.3 S - -
Annonaceae Xylopia sericea A. St.-Hil. Gall 8 Leaf Fusiform Green Pubescent 0.8 F - -
Gall 9 Leaf Globoid Green Glabrous 0.2 F - -
Apocynaceae Aspidosperma sp. Gall 10 Leaf Lenticular Green Glabrous 0.5 S Coccoidea (Hemiptera) -
Aspidosperma tomentosum Mart. Gall 11 Leaf Cylindrical Yellow Pubescent 0.2 S Hemiptera -
Gall 12 Leaf Lenticular Yellow Glabrous 0.2 S - -
Asteraceae Asteraceae sp. Gall 13 Leaf Globoid Green Pubescent 0.2 S - Eulophidae (Hymenoptera) (parasitoid)
Gall 14 Leaf/midvein/petiole Fusiform Green Pubescent 1.0 S - -
Gall 15 Stem Fusiform Brown Roughened 1.5 S - -
Gall 16 Stem Fusiform Green Pubescent 1.0 S - Sciaridae (Diptera) (inquiline), Torymidae (Hymenoptera) (parasitoid)
Gall 17 Stem Globoid Brown Pubescent 0.7 S - -
Gall 18 Stem Globoid Green Glabrous 5.0 S - Eulophidae (Hymenoptera) (parasitoid)
Gall 19 Leaf Lenticular Brown Glabrous 0.2 S - -
Eremanthus sp. Gall 20 Leaf Globoid Yellow Roughened 0.5 S - -
Eremanthus sp. Gall 21 Stem Globoid Brown Roughened 1.0 S - -
Gochnatia barrosii Cabrera Gall 22 Leaf Lenticular Green Pubescent 0.2 S - -
Gall 23 Leaf Lenticular Yellow Roughened 0.5 S - -
Gall 24 Leaf Globoid Brown Pubescent - S Cecidomyiidae (Diptera) -
Gall 25 Leaf Globoid Yellow Pubescent 0.3 S - -
Gall 26 Stem Fusiform Gray Roughened 1.3 S - Sciaridae (Diptera) (inquiline)
Piptocarpha rotundifolia (Less.) Baker Gall 27 Leaf Fusiform Brown Roughened 1.0 S - -
Gall 28 Leaf Fusiform Green Pubescent 0.5 S Cecidomyiidae (Diptera) -
Gall 29 Stem Globoid Brown Roughened 1.0 S - -
Bignoniaceae Fridericia sp. Gall 30 Stem Fusiform Brown Roughened 1.2 F Cecidomyiidae (Diptera) -
Gall 31 Stem Fusiform Green Roughened 0.5 F Cecidomyiidae (Diptera) -
Gall 32 Stem Fusiform Green Roughened 1.5 F Cecidomyiidae (Diptera) -
Tabebuia sp. Gall 33 Stem Fusiform Yellow Roughened 1.0 S Curculionidae (Coleoptera) -
Burseraceae Protium heptaphyllum (Aubl.) Marchand Gall 34 Leaf Cylindrical Green Pubescent 0.2 F Cecidomyiidae (Diptera) -
Gall 35 Leaf Lenticular Brown Roughened 0.1 F Cecidomyiidae (Diptera) -
Gall 36 Leaf Lenticular Green Glabrous 0.2 F Cecidomyiidae (Diptera) -
Gall 37 Leaf Fusiform Green Glabrous 0.8 F Cecidomyiidae (Diptera) -
Gall 38 Leaf Fusiform Yellow Glabrous 0.9 F Phlaeothripidae -
Gall 39 Leaf Globoid Green Roughened 0.3 F Cecidomyiidae (Diptera) -
Gall 40 Leaf/midvein Lenticular Green Roughened 0.3 F Cecidomyiidae (Diptera) -
Gall 41 Leaf/midvein Fusiform Brown Roughened 0.7 F Cecidomyiidae (Diptera) -
Gall 42 Leaf/midvein Fusiform Green Glabrous 0.3 F Cecidomyiidae (Diptera) -
Gall 43 Leaf/midvein Fusiform Yellow Glabrous 0.3 F Cecidomyiidae (Diptera) -
Gall 44 Leaf/midvein Fusiform Yellow Roughened 0.5 F Cecidomyiidae (Diptera) -
Gall 45 Leaf/stem Fusiform Green Glabrous 1.0 F Cecidomyiidae (Diptera) -
Gall 46 Leaf/stem Globoid Green Glabrous 0.8 F Cecidomyiidae (Diptera) Torymidae (Hymenoptera) (parasitoid)
Gall 47 Stem Globoid Brown Roughened - F Cecidomyiidae (Diptera) -
Celastraceae Celastraceae sp. Gall 48 Leaf Conical Green Glabrous 0.1 F - -
Gall 49 Leaf Lenticular Brown Glabrous - F - -
Gall 50 Leaf Lenticular Brown Roughened 0.4 F - -
Gall 51 Leaf Lenticular Green Glabrous 0.5 F - -
Gall 52 Leaf Lenticular Yellow Glabrous 0.6 F - -
Gall 53 Leaf Globoid Brown Pubescent 0.2 F - -
Gall 54 Leaf Globoid Green Glabrous 0.2 F - Eulophidae (Hymenoptera) (parasitoid)
Gall 55 Stem Fusiform Brown Roughened 2.0 F - -
Gall 56 Stem Fusiform Green Roughened 1.4 F - -
Gall 57 Stem Globoid Brown Roughened 0.4 F - Eurytomidae, Torymidae (Hymenoptera) (parasitoid)
Chrysobalanaceae Hirtella sp. Gall 58 Leaf Globoid Brown Pubescent 0.3 F Cecidomyiidae (Diptera) Torymidae (Hymenoptera) (parasitoid)
Clusiaceae Kielmeyera sp. Gall 59 Leaf Lenticular Green Glabrous - S - -
Gall 60 Leaf Lenticular Yellow Glabrous - S - -
Connaraceae Connarus suberosus Planch. Gall 61 Leaf Lenticular Green Glabrous 0.3 S Cecidomyiidae (Diptera) Hymenoptera (parasitoid)
Gall 62 Stem Fusiform Brown Roughened 1.4 S - -
Dilleniaceae Davilla elliptica A. St.-Hil. Gall 63 Leaf Lenticular Brown Roughened 0.2 S Cecidomyiidae (Diptera) -
Gall 64 Leaf Lenticular Yellow Pubescent 0.3 S Cecidomyiidae (Diptera) Eulophidae (Hymenoptera) (parasitoid)
Gall 65 Stem Fusiform Brown Pubescent 1.5 S - -
Dilleniaceae sp. Gall 66 Apical bud Globoid Green Pubescent 1.5 F Cecidomyiidae (Diptera) -
Gall 67 Apical bud Globoid White Pubescent 1.6 F - -
Gall 68 Stem Fusiform Brown Roughened 4.0 F Lepidoptera -
Doliocarpus sp. Gall 69 Stem Cylindrical Pink Pubescent 2.0 F Cecidomyiidae (Diptera) Elasmidae, Eurytomidae, Eulophidae, Torymidae (Hymenoptera) (parasitoid), Sciaridae (Diptera) (inquiline)
Ebenaceae Diospyros sp. Gall 70 Leaf Globoid Brown Pubescent 0.5 S - -
Erythroxylaceae Erythroxylum deciduum A. St.-Hil. Gall 71 Leaf Fusiform Brown Glabrous - S Cecidomyiidae (Diptera) -
Erythroxylum sp. Gall 72 Stem Globoid Brown Roughened 0.9 F - -
Erythroxylum suberosum A. St.-Hil. Gall 73 Leaf Lenticular Yellow Glabrous 0.2 S Cecidomyiidae (Diptera) -
Gall 74 Leaf Globoid Red Pubescent 3.0 S Myrciaryiamia admirabilis Maia, 2007 (Diptera, Cecidomyiidae) -
Gall 75 Stem Globoid Yellow Roughened 0.9 S - Eurytomidae (Hymenoptera) (parasitoid)
Euphorbiaceae Manihot sp. Gall 76 Leaf Cylindrical Red Glabrous 0.5 S Iatrophobia sp. (Diptera, Cecidomyiidae) -
Fabaceae Andira paniculata Benth. Gall 77 Leaf Lenticular Green Glabrous 0.4 S Cecidomyiidae (Diptera) -
Gall 78 Leaf Lenticular Yellow Glabrous 0.1 S Cecidomyiidae (Diptera) -
Bauhinia rufa (Bong.) Steud. Gall 79 Leaf Lenticular Yellow Glabrous 0.3 S - -
Gall 80 Leaf Fusiform Yellow Roughened 0.5 S Cecidomyiidae (Diptera) Eulpelmidae, Torymidae (Hymenoptera) (parasitoid)
Gall 81 Leaf Globoid Yellow Pubescent 0.2 S Cecidomyiidae (Diptera) Torymidae (Hymenoptera) (parasitoid)
Gall 82 Leaf/midvein Fusiform Brown Roughened 0.8 S - -
Gall 83 Pulvine Lenticular Green Glabrous 0.5 S - -
Gall 84 Stem Fusiform Brown Pubescent 2.0 S Cecidomyiidae (Diptera) Eulpelmidae (Hymenoptera) (parasitoid)
Gall 85 Stem Fusiform Brown Roughened 1.5 S Cecidomyiidae (Diptera) Eupelmidae, Tetracampidae (Hymenoptera) (parasitoid)
Gall 86 Stem Fusiform Green Pubescent 2.5 S Cecidomyiidae (Diptera) Torymidae (Hymenoptera) (parasitoid)
Bauhinia sp. Gall 87 Leaf Globoid Brown Pubescent 0.4 F Cecidomyiidae (Diptera) Braconidae, Eulophidae, Torymidae (Hymenoptera) (parasitoid)
Gall 88 Stem Fusiform Brown Roughened 0.8 F - -
Copaifera langsdorffii Desf. Gall 89 Leaf Globoid Brown Glabrous 0.1 F - -
Gall 90 Leaf Globoid Brown Pubescent 0.2 F - -
Gall 91 Leaf Globoid Green Pubescent 0.2 F - -
Gall 92 Leaf Globoid Yellow Roughened 0.4 F - -
Fabaceae sp. Gall 93 Leaf Lenticular Yellow Glabrous - S - -
Inga sp. Gall 94 Leaf/stem Globoid Brown Pubescent 0.4 F - -
Lamiaceae Hyptis sp. Gall 95 Stem Fusiform Brown Pubescent 1.0 S - -
Gall 96 Leaf Lenticular Yellow Pubescent - S - -
Lauraceae Lauraceae sp. Gall 97 Leaf Globoid Green Glabrous - F - -
Gall 98 Leaf Globoid White Pubescent - F - -
Nectandra sp. Gall 99 Leaf Conical Green Glabrous 0.1 F Hemiptera -
Loganiaceae Strychnos pseudoquina A. St.-Hil. Gall 100 Leaf Lenticular Yellow Glabrous 0.4 S - -
Lythraceae Diplusodon sp. Gall 101 Stem Globoid Green Glabrous 0.8 S - Brachycera (Diptera) (inquiline)
Malpighiaceae Byrsonima verbascifolia (L.) DC. Gall 102 Leaf Conical Brown Pubescent 0.5 S Cecidomyiidae (Diptera) Eulophidae (Hymenoptera) (parasitoid)
Gall 103 Leaf/midvein Fusiform Brown Pubescent 0.3 S Cecidomyiidae (Diptera) -
Gall 104 Leaf/midvein Fusiform Brown Roughened 0.9 S - -
Gall 105 Stem Fusiform Brown Roughened 1.0 S - -
Gall 106 Stem Fusiform Brown Roughened 1.2 S Lepidoptera Eurytomidae (Hymenoptera) (parasitoid)
Peixotoa goiana C.E. Anderson Gall 107 Leaf Globoid Yellow Pubescent 0.3 S - Hymenoptera (parasitoid)
Gall 108 Leaf Globoid Yellow Roughened 0.3 S Cecidomyiidae (Diptera) Torymidae (Hymenoptera) (parasitoid), Phlaeothripidae (Thysanoptera) (inquiline)
Gall 109 Leaf/stem Globoid Brown Roughened 0.6 S - -
Malvaceae Malvaceae sp. Gall 110 Leaf Lenticular Brown Pubescent 0.1 F - -
Gall 111 Leaf Fusiform Green Pubescent 1.5 F - Torymidae, Eurytomidae (Hymenoptera) (parasitoid)
Gall 112 Leaf Globoid Green Pubescent 0.3 F - -
Melastomataceae Melastomataceae sp. Gall 113 Stem Globoid Green Pubescent 0.5 F - Sciaridae (Diptera) (inquiline)
Meliaceae Guarea sp. Gall 114 Stem Globoid Brown Roughened - F - -
Meliaceae Meliaceae sp. Gall 115 Leaf Globoid Brown Roughened 0.2 F - Eulophidae (Hymenoptera) (parasitoid)
Monimiaceae Monimiaceae sp. Gall 116 Leaf Lenticular Yellow Glabrous - F - -
Gall 117 Stem Fusiform Green Glabrous 0.8 F - -
Myrtaceae Eugenia bimarginata DC. Gall 118 Stem Fusiform Brown Roughened 1.2 S - -
Gall 119 Stem Fusiform Yellow Roughened 1.5 S - -
Myrtaceae sp. Gall 120 Leaf Lenticular Brown Glabrous 0.1 F - -
Gall 121 Leaf Lenticular Brown Roughened 0.4 F - Eulophidae (Hymenoptera) (parasitoid)
Gall 122 Leaf Lenticular Green Glabrous 0.6 F - -
Gall 123 Leaf Lenticular Green Pubescent 0.2 S Cecidomyiidae (Diptera) Hymenoptera (parasitoid)
Gall 124 Leaf Fusiform Yellow Glabrous 0.8 S - Eurytomidae (Hymenoptera) (parasitoid)
Gall 125 Leaf Fusiform Yellow Pubescent 0.3 S Cecidomyiidae (Diptera) -
Gall 126 Leaf Marginal leaf roll Brown Pubescent 1.5 F - -
Gall 127 Stem Fusiform Brown Roughened 1.2 F Cecidomyiidae (Diptera) Torymidae (Hymenoptera) (parasitoid)
Gall 128 Stem Fusiform Yellow Roughened 0.3 S - -
Gall 129 Stem Fusiform Yellow Roughened 1.2 F - -
Gall 130 Leaf Cylindrical Pink Pubescent 0.7 F Hemiptera -
Psidium sp. Gall 131 Leaf Globoid Brown Pubescent 0.4 S Psyllidae (Hemiptera) -
Ochnaceae Ouratea hexasperma (A. St.-Hil.) Baill. Gall 132 Leaf Lenticular Green Glabrous 0.2 S Cecidomyiidae (Diptera) -
Ochnaceae Ouratea sp. Gall 133 Leaf Lenticular Green Glabrous 0.3 F Cecidomyiidae (Diptera) -
Piperaceae Piper arboreum Aubl. Gall 134 Leaf Lenticular Green Glabrous 0.5 F Cecidomyiidae (Diptera) -
Proteaceae Roupala montana Aubl. Gall 135 Leaf Conical Green Glabrous 0.8 S Lepidoptera -
Gall 136 Leaf Conical Green Pubescent 0.4 S Hemiptera -
Roupala sp. Gall 137 Leaf Lenticular Brown Glabrous 0.3 F Cecidomyiidae (Diptera) -
Gall 138 Leaf Lenticular Green Glabrous 0.6 F Cecidomyiidae (Diptera) -
Gall 139 Stem Fusiform Brown Roughened 3.5 F - -
Rubiaceae Cordiera macrophylla (K. Schum.) Kuntze Gall 140 Leaf Globoid White Glabrous 0.4 F Coccoidea (Hemiptera) -
Palicourea rígida Kunth Gall 141 Leaf Fusiform Yellow Glabrous 0.3 S Cecidomyiidae (Diptera) -
Rubiaceae sp. Gall 142 Leaf Lenticular Brown Roughened 0.3 F - -
Gall 143 Leaf Lenticular Green Roughened 0.1 F - -
Gall 144 Leaf/midvein Fusiform Green Glabrous - F - -
Gall 145 Leaf/stem Lenticular Green Pubescent 0.4 S Cecidomyiidae (Diptera) -
Gall 146 Stem Fusiform Brown Roughened 1.0 F Cecidomyiidae (Diptera) Eupelmidae, Tanaostigmatidae (Hymenoptera) (inquiline)
Gall 147 Stem Fusiform Green Glabrous 1.6 F Cecidomyiidae (Diptera) -
Gall 148 Stem Fusiform Green Roughened 1.0 F - Torymidae (Hymenoptera) (parasitoid)
Gall 149 Stem Globoid Green Glabrous 0.5 F - -
Salicaceae Casearia sylvestris Sw. Gall 150 Leaf Globoid Yellow Glabrous 0.1 S - -
Gall 151 Leaf Lenticular Green Glabrous - S - -
Gall 152 Stem Fusiform Brown Roughened - S - Hymenoptera (parasitoid)
Sapindaceae Sapindaceae sp. Gall 153 Leaf Lenticular Brown Roughened 0.2 F - -
Gall 154 Leaf Fusiform Green Glabrous 1.0 F - -
Gall 155 Stem Fusiform Brown Roughened 0.5 F - -
Gall 156 Stem Fusiform Green Pubescent - F Lepidoptera -
Serjania sp. Gall 157 Leaf Lenticular Green Glabrous 0.3 S Cecidomyiidae (Diptera) Eulophidae, Torymidae (Hymenoptera) (parasitoid)
Gall 158 Leaf Lenticular Green Roughened 0.3 S Lepidoptera -
Gall 159 Leaf Lenticular Yellow Glabrous 0.1 S Cecidomyiidae (Diptera) -
Gall 160 Leaf Fusiform Green Glabrous 0.3 S Cecidomyiidae (Diptera) -
Gall 161 Leaf Fusiform Yellow Glabrous 1.0 S Cecidomyiidae (Diptera) -
Gall 162 Leaf Globoid Brown Roughened 0.5 F Cecidomyiidae (Diptera) -
Gall 163 Leaf Globoid Green Glabrous 0.2 F Cecidomyiidae (Diptera) -
Gall 164 Leaf/midvein Fusiform Green Glabrous 0.5 F Cecidomyiidae (Diptera) -
Gall 165 Leaf/midvein Fusiform Green Glabrous 1.2 S Cecidomyiidae (Diptera) -
Gall 166 Stem Fusiform Brown Roughened 1.5 F - -
Gall 167 Stem Globoid Brown Roughened 0.7 F - -
Gall 168 Stem Fusiform Green Glabrous - F - -
Siparunaceae Siparuna guianensis Aubl. Gall 169 Leaf Cylindrical Green Pubescent 0.3 F Cecidomyiidae (Diptera) -
Gall 170 Leaf Lenticular Green Glabrous 0.4 F Cecidomyiidae (Diptera) -
Gall 171 Leaf Fusiform Brown Roughened 0.5 F Cecidomyiidae (Diptera) -
Gall 172 Leaf Fusiform Green Glabrous 0.8 F Cecidomyiidae (Diptera) -
Gall 173 Leaf Fusiform Yellow Glabrous - F - -
Gall 174 Leaf Globoid Brown Pubescent - S - -
Gall 175 Leaf/midvein Fusiform Green Glabrous 0.5 F - -
Gall 176 Stem Fusiform Green Glabrous 1.0 F - Torymidae (Hymenoptera) (parasitoid)
Gall 177 Stem Fusiform Green Roughened - F - -
Gall 178 Stem Globoid Brown Roughened 0.4 F - -
Gall 179 Stem Globoid Green Glabrous 1.5 F - -
Gall 180 Stem/petiole Globoid Brown Roughened 0.5 F - Eurytomidae (Hymenoptera) (parasitoid)
Styracaceae Styrax ferrugineus Nees and Mart. Gall 181 Leaf Lenticular Yellow Glabrous 0.4 S Cecidomyiidae (Diptera) -
Gall 182 Stem Fusiform Brown Pubescent 1.5 S - -
Gall 183 Stem Fusiform Brown Roughened 1.5 S Lepidoptera -
Vochysiaceae Qualea grandiflora Mart. Gall 184 Leaf Lenticular Brown Glabrous 0.2 S Lepidoptera -
Gall 185 Leaf Lenticular Brown Roughened 0.2 S Cecidomyiidae (Diptera) -
Gall 186 Stem Globoid Brown Roughened 1.3 S Cecidomyiidae (Diptera) -

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. 

Insect order Insect gall morphotypes Host plant species
Richness % Richness %
Diptera 64 34.40 28 45.90
Hemiptera 8 4.30 8 13.11
Lepidoptera 8 4.30 8 13.11
Coleoptera 1 0.54 1 1.64
Thysanoptera 1 0.54 1 1.64
Undetermined 104 55.91 43 70.49

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. 

Host plant family Host plant species Insect gall morphotypes Host plant family Host plant species Insect gall morphotypes
Fabaceae 6 18 Salicaceae 1 3
Asteraceae 5 17 Styracaceae 1 3
Sapindaceae 3 16 Vochysiaceae 1 3
Burseraceae 1 14 Annonaceae 1 2
Myrtaceae 3 14 Clusiaceae 1 2
Siparunaceae 1 12 Connaraceae 1 2
Celastraceae 1 10 Lamiaceae 2 2
Rubiaceae 3 10 Meliaceae 2 2
Malpighiaceae 2 8 Monimiaceae 1 2
Dilleniaceae 3 7 Ochnaceae 2 2
Erythroxylaceae 3 5 Chrysobalanaceae 1 1
Proteaceae 2 5 Ebenaceae 1 1
Acanthaceae 1 4 Euphorbiaceae 1 1
Bignoniaceae 2 4 Loganiaceae 1 1
Anacardiaceae 2 3 Lythraceae 1 1
Apocynaceae 2 3 Melastomataceae 1 1
Lauraceae 2 3 Piperaceae 1 1
Malvaceae 1 3 TOTAL 61 186

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. (2009b) and of the 236 morphotypes registered in the Vale do Jequitinhonha by Fernandes et al. (1997), 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., 2009b and 10 sites sampled two times by Fernandes et al., 1997), 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. (2014a). 

Locality Insect gall morphotypes Host plant species Host plant families Gall morphotypes per host plant species Reference
Floresta Nacional de Silvânia - GO 186 61 35 3.0 Present study
Serra Geral - BA 49 14 13 3.5 Nogueira et al. (2016)
Aquidauana - MS 68 46 20 1.5 Urso-Guimarães et al. (2016)
Mata da Veterinária da UFG - GO 42 22 20 1.9 Silva et al. (2015)
Parque Nacional das Emas - GO 97 44 24 2.2 Araújo et al. (2014b)
Caldas Novas - GO 56 34 21 1.6 Santos et al. (2012)
Reserva Biológica Boqueirão - MG 57 43 18 1.3 Malves & Friero-Costa (2012)
Serra dos Pireneus - GO 62 51 28 1.2 Araújo et al. (2011)
Semidecidual Forest in Goiânia - GO 34 20 12 1.7 Santos et al. (2010)
Serra do Espinhaço - MG 241 142 29 1.7 Carneiro et al. (2009a)
Fazenda Bulcão - MG 29 24 12 1.2 Fernandes & Negreiros (2006)
Santa Rita do Passa Quatro - SP 36 24 15 1.5 Urso-Guimarães & Scareli-Santos (2006)
Serra de São José - MG 137 73 30 1.9 Maia & Fernandes (2004)
Delfinópolis - MG 22 19 19 1.2 Urso-Guimarães et al. (2003)
Estação Ecológica de Pirapitinga - MG 92 62 28 1.5 Gonçalves-Alvim & Fernandes (2001)
Vale do Jequitinhonha - MG 236 134 27 1.8 Fernandes et al. (1997)
Campus Pampulha - MG 37 22 11 1.7 Fernandes et al. (1988)

Our results are in agreement with previous studies in the Brazilian savannas that point the dominance of gall-midges as gallers (Maia & Fernandes, 2004; Santos et al., 2010; Araújo et al., 2011, 2014b; Nogueira et al., 2016; Urso-Guimarães et al., 2016). Cecidomyiidae is considered the main galling insect group in the world with more of 6,000 known species (Gagné & Jaschhof, 2014), and a huge estimated number of species not yet known (Araújo et al., 2014a; Grandez-Rios et al., 2015). In the Cerrado, cecidomyiids are responsible for approximately 70% of all known gall morphospecies (Araújo et al., 2014a). 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., 2014a).

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., 2014a) and are among the main causes of galler mortality (Maia & Azevedo, 2009).

Many inventories on the gall diversity in the Cerrado indicate Fabaceae (Fernandes et al., 1997; Maia & Fernandes, 2004; Urso-Guimarães & Scareli-Santos, 2006; Santos et al., 2010; Araújo et al., 2014b; Nogueira et al., 2016) and Asteraceae (Carneiro et al., 2009b; Fernandes et al., 1997; Malves & Frieiro-Costa, 2012) as the most important host families, which were also observed in the present study. Araújo et al. (2014a) 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, 2011; Gonçalves-Alvim & Fernandes, 2001). 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., 2015; Nogueira et al., 2016; Urso-Guimarães et al., 2016). 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., 2009a). 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., 2003; Maia & Fernandes, 2004; Araújo et al., 2011; Malves & Frieiro-Costa, 2012).

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., 2014a). 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., 2014a). 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, 2005), inventories of insect gall diversity in the region must be done emergently (Araújo, 2011).

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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1Editor Responsável: Carlos José Einicker Lamas

Publicado com o apoio financeiro do Programa de Apoio às Publicações Científicas Periódicas da USP

3Os periódicos Papéis Avulsos de Zoologia e Arquivos de Zoologia estão licenciados sob uma Licença CC-BY da Creative Commons.

Received: June 29, 2017; Accepted: September 15, 2017

3 E-mail: barbaralien@gmail.com

4 E-mail: llbergamini@gmail.com

5 E-mail: benecosantos@yahoo.com.br

6 E-mail: walterbioaraujo@yahoo.com.br (corresponding author)

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