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Papéis Avulsos de Zoologia

versión impresa ISSN 0031-1049versión On-line ISSN 1807-0205

Pap. Avulsos Zool. vol.58  São Paulo  2018  Epub 19-Mar-2018

http://dx.doi.org/10.11606/1807-0205/2018.58.04 

Articles

Insect gall occurrence in savanna and forest remnant sites of Hidrolândia, GO, Brazil Central

Elienai Cândida e Silva1  3 

Benedito Baptista dos Santos1  4 

Walter Santos de Araújo2  5 
http://orcid.org/0000-0003-0157-6151

1Universidade Federal de Goiás (UFG), Instituto de Ciências Biológicas (ICB), Departamento de Ecologia (DECOL). Goiânia, GO, Brasil.

2Universidade Estadual de Montes Claros (UNIMONTES), Centro de Ciências Biológicas e da Saúde (CCBS), Departamento de Biologia Geral. Montes Claros, MG, Brasil.

Abstract

In this study we perform an inventory of the insect galls in savanna and forest sites of Hidrolândia, Goiás, Brazil. We found 150 insect gall morphotypes, distributed on 39 botanical families and 104 plant species. Among the insect galls, 81 gall morphotypes were recorded in the savanna site and 73 in the forest site. The plant taxa richest in insect galls were the family Fabaceae with 22 gall morphotypes, the genus Bauhinia (Fabaceae) with 15, and the species Siparuna guianensis (Siparunaceae) with seven gall morphotypes. We found gall-inducing insects belonging to orders Diptera, Coleoptera, Lepidoptera and Thysanoptera. The galling insects of family Cecidomyiidae (Diptera) were the most common inducing 48.1% of the gall morphotypes. This is the first systematic survey of insect galls realized in the city of Hidrolândia, being this the site with the higher insect gall diversity already cataloged to the Central region of Brazil.

Key-Words. Cerrado; Fabaceae; Host plants; Insect galls; Plant-insect interaction

INTRODUCTION

Galls are abnormal modifications in the vegetal tissues induced mainly by galling insects, and characterized by hypertrophy and hyperplasia of plant cells (Mani, 1964; Shorthouse & Rohfritsch, 1992). From an evolutionary point of view, insect galls are extended phenotypes of the gall-inducers (Stone & Schönrogge, 2003), which leads to each species of galling insect induces a specific morphotype of gall on their host plant (Carneiro et al., 2009a). Galls and galling insects are widely distributed around the globe, especially in the Neotropical region (Espírito-Santo & Fernandes, 2007). In the Neotropics stand out Amazon (Julião et al., 2014), Atlantic Forest (Santos et al., 2014) and Cerrado (Araújo et al., 2014a) as hotspots of insect gall diversity.

The Brazilian Cerrado is composed by a wide variety of vegetation types (Ribeiro & Walter, 2008), and one of the richest floras of Brazil and in the world (Klink & Machado, 2005; Mendonça et al., 2008). This great structural and floristic diversity is one of the main explanations for the high insect gall diversity in the Cerrado (Araújo et al., 2014a). In this sense, although the number of insect gall studies in the Cerrado has been growing in the recent years (Araújo et al., 2014a), evidence points that there are still temporal and spatial gaps in the group sampling (e.g.,Araújo, 2011; Maia et al., 2014).

To the Central Brazil, insect gall inventories have been published only to the following localities: Caldas Novas (Santos et al., 2012), Goiânia (Santos et al., 2010; Silva et al., 2015), Parque Estadual da Serra dos Pireneus (Araújo et al., 2011), and Parque Nacional das Emas (Araújo et al., 2014b). Given these gaps in knowledge of insect galls in the Central Brazil, in the present study we perform an inventory of the insect galls and their host plants in sites of savanna and forest in Hidrolândia, Goiás, Central Brazil.

MATERIALS AND METHODS

The study was realized in the Escola Agrícola (EA) of the Centro de Formação Agroecológico de Hidrolândia (CEFAEH) in the city of Hidrolândia, State of Goiás, Central Brazil (17°00’56”S, 49°12’00”W; Fig. 1). The climate of region is classified as Aw of Köppen, being humid tropical with wet summer and dry winter. EA-CEFAEH has an area of approximately 40 hectares, most covered by natural vegetation with some level of human disturbance. The area is under Cerrado domain being characterized by several vegetation types, such as grasslands (e.g., Rocky Field), savannas (e.g., Cerrado Sensu Stricto or Neotropical savanna) and forests (e.g., Semidecidual Forest and Gallery Forest) (Ribeiro & Walter, 2008).

Figure 1 Localization of study area in the CEFAEH, Hidrolândia, Goiás, Central Brazil. Font: Google Earth. 

The sampling was done monthly between September 2011 and May 2012 in two vegetation remnants being one of Cerrado Sensu Stricto (hereafter called savanna; 17°01’05”S; 49°11’49”W) and other of Semidecidual Forest (hereafter called forest; 17°00’42”S; 49°12’04”W). We performed the collect of insect galls along two transects (one in each vegetation type) sampled by two hours (Araújo et al., 2011). All host plants had their epigeous parts inspected and all observed insect galls were registered. Samples of each insect galls were photographed, collected and transported individually in labeled plastic bags.

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 identified in morphotypes using the host plant species and the gall characteristics (organ of occurrence, form, color, pubescence, and size). In laboratory, the galls were daily observed to verify the emergence of adult insects or dissected to obtainment of immature insects. All obtained insects were fixed in 70% alcohol and identified using the insect gall literature to Neotropics and Brazil (e.g.,Gagné, 1994; Maia & Fernandes, 2004, Araújo et al., 2011). 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 Plant List (http://theplantlist.org).

RESULTS AND DISCUSSION

We found 150 insect gall morphotypes distributed on 39 botanical families and 104 plant species in the EA-CEFAEH (Table 1). Previous studies that inventoried the insect gall diversity in the Cerrado sites ranged from 22 (Urso-Guimarães et al., 2003) to 241 (Carneiro et al., 2009b) gall morphotypes. The insect gall richness recorded in the present study is almost twice of 86.8 morphotypes, which is the average number of gall morphotypes recorded in the different surveys performed in the Brazilian Cerrado (review in Araújo et al., 2014a). For studies in Central region of Brazil, the insect gall richness in the EA-CEFAEH exceeds all previously cataloged sites (Table 2), as for example, the Parque Nacional das Emas that had 97 gall morphotypes recorded (Araújo et al., 2014b). Additionally, the average number of gall morphotypes per host plant species was of 1.44 in the present study, which was very similar to mean of 1.5 listed to Cerrado (Araújo et al., 2014a). These variations in the number of insect gall morphotypes and galls per plant species can be explained by differences in the sampling efforts and number of sampled host plants in the different inventories.

Table 1 Number of host plant species and insect gall morphotypes in the host plant families recorded in EA-CEFAEH, Hidrolândia, Goiás, Brazil. 

Host plantfamily Number of plant species Number of gall morphotypes Gall richness per vegetation types
Savanna Savanna/Forest Forest
Anacardiaceae 2 2 2 0 0
Annonaceae 2 4 2 0 2
Apocynaceae 2 4 2 0 2
Araliaceae 1 1 1 0 0
Asteraceae 1 2 2 0 0
Bignoniaceae 1 1 0 0 1
Burseraceae 1 2 0 0 2
Caryocaraceae 1 2 1 1 0
Celastraceae 2 2 2 0 0
Combretaceae 1 2 2 0 0
Connaraceae 3 4 4 0 0
Dilleniaceae 1 2 2 0 0
Ebenaceae 1 1 1 0 0
Elaeocarpaceae 1 2 0 0 2
Erythroxylaceae 3 9 5 0 4
Euphorbiaceae 3 4 3 0 1
Fabaceae 6 22 17 0 5
Lamiaceae 1 2 2 0 0
Lauraceae 2 4 0 0 4
Lorantaceae 1 1 0 0 1
Lythraceae 1 1 0 0 1
Malpighiaceae 6 13 7 0 6
Melastomataceae 3 6 4 0 2
Meliaceae 1 3 0 0 3
Myristicaceae 1 1 0 0 1
Myrtaceae 2 9 2 0 7
Nyctaginaceae 1 1 1 0 0
Ochnaceae 1 1 1 0 0
Proteaceae 1 3 3 0 0
Rhamnaceae 1 1 0 0 1
Rubiaceae 2 5 0 0 5
Rutaceae 1 1 1 0 0
Santalaceae 1 1 0 0 1
Sapindaceae 3 11 4 0 7
Siparunaceae 1 7 0 0 7
Smilacaceae 1 3 2 0 1
Styracaceae 1 1 0 0 1
Vitaceae 3 3 2 0 1
Vochysiaceae 4 6 3 2 1
TOTAL 71 150 78 3 69

Table 2 Comparison between the insect gall surveys performed in different areas of Brazil Central. 

Surveys Sampling Number of recorded taxa Reference
Locality Coordinates Collect period Vegetation studied Host plant families Host plant species Insect gall species
EA-CEFAEH 17°00’S, 49°12’W September 2011 to May 2012 Semidecidual Forest, Savanna 39 104 150 Present study
Campus Samambaia da UFG 16°36’S, 49°15’W January 2005 to January 2007 Semidecidual Forest 12 20 34 Santos et al. (2010)
Parque Estadual da Serra dos Pireneus 15°48’S, 48°52’W August 2006 to July 2008 Gallery and Semidecidual Forest, Savanna 28 51 62 Araújo et al. (2011)
Caldas Novas 17°42’S, 48°38’W November 2008 to August 2009 Savanna 21 34 56 Santos et al. (2012)
Parque Nacional das Emas 17°49’S, 52°39’W November 2013 Grassland, Savanna 24 44 97 Araújo et al. (2014b)
Mata da Veterinária 16°36’S, 49°16’W September 2009 to April 2010 Semidecidual Forest 20 22 42 Silva et al. (2015)

The plant families richest in insect galls were Fabaceae, with 22 gall morphotypes, Malpighiaceae with 13, Sapindaceae with 11, and Erythroxylaceae and Myrtaceae with nine gall morphotypes each (Table 1). Our results are according to previous studies that point Fabaceae as the most important host family of insect galls in the Cerrado (e.g.,Maia & Fernandes, 2004; Santos et al., 2010; Araújo et al., 2011; Santos et al., 2012; Silva et al., 2015). The main explanation for the high insect gall richness hosted by Fabaceae in the Cerrado is its high species number (Southwood, 1960, 1961; Araújo et al., 2014a) of nearly 800 (Mendonça et al., 2008). Malpighiaceae and Myrtaceae also frequently appear in the ranking of insect gall host families most important of Cerrado (Araújo et al., 2014a).

The plant genera Bauhinia (Fabaceae), Erythroxylum (Erythroxylaceae), Myrcia (Myrtaceae), and Siparuna (Siparunaceae) were the most diverse hosts of insect galls with 15, nine, seven, and seven gall morphotypes, respectively (Table 3). The plant species Siparuna guianensis (Siparunaceae), Bauhinia brevipes (Fabaceae), and Erythroxylum sp. (Erythroxylaceae), with seven, six, and five gall morphotypes, respectively, were the most important host plant species. Recent studies have recorded Bauhinia as a very diverse host plant genus of insect galls, which probably is due to genus be very speciose (Costa et al., 2014; Nogueira et al., 2016). The species S. guianensis and B. brevipes also have been previously recorded as important hosts of insect galls (Coelho et al., 2014; Silva et al., 2015). In our study, the most of recorded insect galls occurred on leaves (66.8%) and stems (24.1%), which corroborates the pattern of that Neotropical insect galls are more common in leaves and branches (Fernandes et al., 1988; Santos et al., 2010; Araújo et al., 2011). Insect gall morphotypes also vary greatly in form, color and trichome presence or absence (Table 3), being that the most common were globoids (43.3%), greens (43.3%) and glabrous (61.1%). This great variation in the insect gall morphology can be explained by high specificity of gall-inducing insects associated to their host plants (Carneiro et al., 2009a).

Table 3 Host plants, insect gall morphotypes and insect taxa recorded in savanna and forest remnant sites of EA-CEFAEH, Hidrolândia, Goiás, Brazil. Legend: Gall size: L = Length, W = Width; Vegetation type: S = Savanna, F = Forest. 

Host plants Insect gall morphotypes Insect taxa
Family Species Gall Organ Form Colour Pubescence Size (cm) Vege-tation Gall-inducers Parasitoids or inquilines
Anacardiaceae Anacardium humile A. St.-Hil. 1 Leaf Conical Yellow Glabrous L ± 0.4; W ± 0.4 S Cecidomyiidae
Anacardiaceae Myracrodruon urundeuva M. Allemão 2 Leaf Conical Brown Hairy L ± 0.5; W ± 0.4 S Cecidomyiidae
Annonaceae Annonaceae sp. 3 Leaf Discoid Yellow Hairy L ± 0.1; W ± 0.1 S Unidentified
Annonaceae Annonaceae sp. 4 Leaf Discoid Yellow Hairy L ± 0.2; W ± 0.2 S Unidentified
Annonaceae Annonaceae sp. 5 Stem Globose Brown Glabrous L ± 1.3; W ± 1.3 F Unidentified
Annonaceae Cardiopetalum sp. 6 Apical bud Fusiform Green Hairy L ± 0.3; W ± 0.2 F Unidentified
Apocynaceae Aspidosperma sp. 7 Leaf Globose Green Glabrous L ± 0.3; W ± 0.3 F Cecidomyiidae Pteromalidae
Apocynaceae Aspidosperma sp. 8 Leaf Globose Green Glabrous L ± 0.5; W ± 0.5 S Cecidomyiidae
Apocynaceae Aspidosperma sp. 9 Stem Fusiform Brown Glabrous L ± 2.0; W ± 0.5 F Cecidomyiidae
Apocynaceae Aspidosperma tomentosum Mart. 10 Leaf Globose Green Hairy L ± 0.3; W ± 0.3 S Cecidomyiidae
Araliaceae Schefflera macrocarpa (Cham. & Schltdl.) Frodin 11 Leaf Globose Green Hairy L ± 0.1; W ± 0.1 S Cecidomyiidae
Asteraceae Asteraceae sp. 12 Midvein Globose White Hairy L ± 0.7; W ± 0.5 S Unidentified
Asteraceae Asteraceae sp. 13 Stem/Petiole Globose Green Glabrous L ± 1.0; W ± 1.0 S Unidentified
Bignoniaceae Fridericia sp. 14 Stem Fusiform Brown Hairy L ± 1.7; W ± 0.7 F Cecidomyiidae
Burseraceae Protium sp. 15 Leaf Globose Yellow Glabrous L ± 0.3; W ± 0.3 F Cecidomyiidae
Burseraceae Protium sp. 16 Leaf/Stem/Petiole Fusiform Green Glabrous L ± 0.6; W ± 0.6 F Cecidomyiidae
Caryocaraceae Caryocar brasiliense A. St.-Hil. 17 Leaf Discoid Yellow Hairy L ± 0.3; W ± 0.3 S Cecidomyiidae
Caryocaraceae Caryocar brasiliense A. St.-Hil. 18 Leaf Globose Yellow Hairy L ± 0.3; W ± 0.3 S/F Cecidomyiidae Eulophidae/Eurytomidae/Torymidae
Celastraceae Celastraceae sp. 19 Leaf Discoid Green Glabrous L ± 0.3; W ± 0.3 S Unidentified
Celastraceae Plenckia populnea Reissek 20 Stem Globose Brown Glabrous L ± 1.5; W ± 1.5 S Cecidomyiidae Braconidae
Combretaceae Terminalia argentea Mart. 21 Leaf Discoid Green Hairy L ± 0.3; W ± 0.3 S Cecidomyiidae
Combretaceae Terminalia argentea Mart. 22 Leaf Globose Brown Hairy L ± 0.7; W ± 0.7 S Cecidomyiidae
Connaraceae Connaraceae sp. 23 Inflorescence Globose Brown Glabrous L ± 0.7; W ± 0.7 S Cecidomyiidae Eurytomidae
Connaraceae Connarus sp. 24 Leaf Globose Brown Glabrous L ± 0.5; W ± 0.5 S Cecidomyiidae
Connaraceae Connarus sp. 25 Stem Fusiform Brown Glabrous L ± 2.5; W ± 1.0 S Unidentified Eulophidae
Connaraceae Connarus suberosus Planch. 26 Leaf Discoid Green Glabrous L ± 0.3; W ± 0.3 S Cecidomyiidae
Dilleniaceae Davilla sp. 27 Inflorescence Fusiform Green Hairy L ± 1.0; W ± 0.5 S Lepidoptera
Dilleniaceae Davilla sp. 28 Leaf Discoid Yellow Glabrous L ± 0.3; W ± 0.3 S Cecidomyiidae
Ebenaceae Diospyros hispida A. DC. 29 Apical bud Globose Green Hairy L ± 3.0; W ± 3.0 S Lepidoptera
Elaeocarpaceae Sloanea sp. 30 Leaf Globose Green Glabrous L ± 0.4; W ± 0.3 F Unidentified
Elaeocarpaceae Sloanea sp. 31 Leaf Globose Brown Hairy L ± 0.4; W ± 0.4 F Unidentified
Erythroxylaceae Erythroxylum sp. 32 Leaf Amophous Green Glabrous L ± 1.0; W ± 0.2 S Cecidomyiidae
Erythroxylaceae Erythroxylum sp. 33 Leaf Discoid Green Glabrous L ± 0.2; W ± 0.2 F Cecidomyiidae Eulophidae
Erythroxylaceae Erythroxylum sp. 34 Leaf Discoid Green Glabrous L ± 0.4; W ± 0.4 F Cecidomyiidae
Erythroxylaceae Erythroxylum sp. 35 Leaf Globose Brown Hairy L ± 0.6; W ± 0.6 S Cecidomyiidae Pteromalidae
Erythroxylaceae Erythroxylum sp. 36 Leaf Globose Brown Hairy L ± 0.5; W ± 0.5 S Cecidomyiidae
Erythroxylaceae Erythroxylum sp. 37 Midvein Globose Brown Hairy L ± 0.5; W ± 0.5 F Cecidomyiidae Pteromalidae
Erythroxylaceae Erythroxylum sp. 38 Stem Globose Brown Glabrous L ± 0.6; W ± 0.6 F Cecidomyiidae
Erythroxylaceae Erythroxylum suberosum A. St.-Hil. 39 Leaf Globose Brown Hairy L ± 2.0; W ± 2.0 S Myrciariamyia admirabilis Maia & Fernandes, 2007 (Cecidomyiidae) Encyrtidae/Eulophidae/Torymidae
Erythroxylaceae Erythroxylum tortuosum Mart. 40 Leaf Globose Green Glabrous L ± 0.1; W ± 0.1 S Cecidomyiidae
Euphorbiaceae Euphorbiaceae sp. 41 Stem/Petiole Fusiform Red Glabrous L ± 3.0; W ± 0.5 F Unidentified Eulophidae/Eurytomidae
Euphorbiaceae Manihot sp. 42 Leaf Conical Yellow Glabrous L ± 1.0; W ± 0.3 S Iatrophobia sp. Pteromalidae
Euphorbiaceae Manihot sp. 43 Leaf Conical Yellow Glabrous L ± 0.7; W ± 0.2 S Iatrophobia sp.
Euphorbiaceae Maprounea guianensis Aubl. 44 Stem Fusiform Red Glabrous L ± 0.7; W ± 0.5 S Unidentified
Fabaceae Acosmium dasycarpum (Vogel) Yakovlev 45 Leaf Discoid Green Glabrous L ± 0.5; W ± 0.5 S Cecidomyiidae
Fabaceae Bauhinia brevipes Vogel. 46 Leaf Discoid Yellow Hairy L ± 0.1; W ± 0.1 S Cecidomyiidae
Fabaceae Bauhinia brevipes Vogel. 47 Leaf Globose Yellow Hairy L ± 0.2; W ± 0.2 S Cecidomyiidae
Fabaceae Bauhinia brevipes Vogel. 48 Leaf Globose Yellow Hairy L ± 0.1; W ± 0.1 S Cecidomyiidae
Fabaceae Bauhinia brevipes Vogel. 49 Leaf Globose Brown Hairy L ± 0.4; W ± 0.4 S Cecidomyiidae
Fabaceae Bauhinia brevipes Vogel. 50 Stem Fusiform Green Hairy L ± 5.5; W ± 0.6 S Cecidomyiidae Eulophidae/Braconidae
Fabaceae Bauhinia brevipes Vogel. 51 Stem Fusiform Brown Hairy L ± 1.8; W ± 0.8 S Cecidomyiidae
Fabaceae Bauhinia curvula Benth. 52 Leaf Globose Green Hairy L ± 0.8; W ± 0.4 S Cecidomyiidae
Fabaceae Bauhinia curvula Benth. 53 Stem Fusiform Brown Glabrous L ± 3.0; W ± 1.0 S Cecidomyiidae
Fabaceae Bauhinia sp. 54 Apical bud Fusiform Green Hairy L ± 1.0; W ± 1.3 S Unidentified
Fabaceae Bauhinia sp. 55 Leaf Fusiform Green Hairy L ± 0.4; W ± 0.3 S Cecidomyiidae Eulophidae/Braconidae/Pteromalidae
Fabaceae Bauhinia sp. 56 Leaf Globose Green Hairy L ± 0.5; W ± 0.5 S Cecidomyiidae
Fabaceae Bauhinia sp. 57 Leaf Globose Yellow Hairy L ± 0.2; W ± 0.2 S Unidentified
Fabaceae Bauhinia sp. 58 Leaf Globose Brown Hairy L ± 0.2; W ± 0.2 F Unidentified
Fabaceae Bauhinia sp. 59 Stem Fusiform Brown Glabrous L ± 2.0; W ± 0.8 F Unidentified Braconidae
Fabaceae Bauhinia sp. 60 Stem Globose Brown Hairy L ± 2.5; W ± 2.0 S Lepidoptera Torymidae
Fabaceae Fabaceae sp. 61 Leaf Discoid Red Glabrous L ± 0.4; W ± 0.4 F Unidentified
Fabaceae Fabaceae sp. 62 Leaf Globose Green Glabrous L ± 0.2; W ± 0.2 F Unidentified
Fabaceae Fabaceae sp. 63 Leaf Globose Yellow Glabrous L ± 0.3; W ± 0.3 S Unidentified
Fabaceae Fabaceae sp. 64 Leaf Globose Green Hairy L ± 0.3; W ± 0.3 S Unidentified
Fabaceae Fabaceae sp. 65 Petiole Globose Green Glabrous L ± 0.3; W ± 0.3 F Unidentified
Fabaceae Sclerolobium paniculatum Vogel. 66 Leaf Globose Green Hairy L ± 0.1; W ± 0.1 S Unidentified
Lamiaceae Lamiaceae sp. 67 Midvein Fusiform Green Hairy L ± 0.4; W ± 0.2 S Unidentified
Lamiaceae Lamiaceae sp. 68 Stem Fusiform Brown Hairy L ± 1.5; W ± 0.5 S Unidentified
Lauraceae Lauraceae sp. 69 Leaf Globose Green Glabrous L ± 0.5; W ± 0.5 F Unidentified
Lauraceae Nectandra cuspidata Nees & Mart. 70 Leaf Discoid White Hairy L ± 0.3; W ± 0.3 F Cecidomyiidae Eulophidae
Lauraceae Nectandra cuspidata Nees & Mart. 71 Leaf Discoid Green Glabrous L ± 0.9; W ± 0.9 F Phlaeothripidae
Lauraceae Nectandra cuspidata Nees & Mart. 72 Leaf Globose Brown Hairy L ± 0.4; W ± 0.4 F Unidentified Eulophidae
Lorantaceae Lorantaceae sp. 73 Leaf Discoid Green Glabrous L ± 0.5; W ± 0.5 F Unidentified
Lythraceae Diplusodon sp. 74 Stem/Petiole Fusiform White Glabrous L ± 1.0; W ± 0.4 F Unidentified
Malpighiaceae Byrsonima sp. 75 Leaf Conical Green Hairy L ± 0.4; W ± 0.2 S Cecidomyiidae
Malpighiaceae Diplopterys pubipetala (A. Juss.) W.R.Anderson & C.Davis 76 Leaf Conical Green Glabrous L ± 1.0; W ± 0.3 S/F Phlaeothripidae Eulophidae
Malpighiaceae Diplopterys pubipetala (A. Juss.) W.R.Anderson & C.Davis 77 Leaf Discoid Green Glabrous L ± 0.5; W ± 0.5 F Unidentified Eurytomidae
Malpighiaceae Diplopterys pubipetala (A. Juss.) W.R.Anderson & C.Davis 78 Leaf Discoid Green Glabrous L ± 0.6; W ± 0.6 S Unidentified
Malpighiaceae Heteropterys eglandulosa A. Juss. 79 Leaf Discoid Yellow Hairy L ± 0.3; W ± 0.3 S Unidentified
Malpighiaceae Heteropterys sp. 80 Leaf Amophous Yellow Glabrous L ± 1.5; W ± 0.7 S Unidentified Eulophidae
Malpighiaceae Malpighiaceae sp. 81 Apical bud Fusiform Green Glabrous L ± 2.5; W ± 2.0 F Unidentified
Malpighiaceae Malpighiaceae sp. 82 Leaf Discoid Green Glabrous L ± 0.6; W ± 0.6 F Phlaeothripidae Eulophidae
Malpighiaceae Malpighiaceae sp. 83 Stem Globose Brown Glabrous L ± 2.5; W ± 2.5 F Cecidomyiidae
Malpighiaceae Malpighiaceae sp. 84 Leaf Globose Green Glabrous L ± 0.5; W ± 0.5 F Unidentified
Malpighiaceae Malpighiaceae sp. 85 Leaf Globose Green Glabrous L ± 0.5; W ± 0.4 F Unidentified
Malpighiaceae Malpighiaceae sp. 86 Stem Globose Brown Glabrous L ± 2.0; W ± 1.5 S Cecidomyiidae
Malpighiaceae Peixotoa sp. 87 Leaf Globose Brown Hairy L ± 0.6; W ± 0.6 S Cecidomyiidae Eulophidae
Melastomataceae Melastomataceae sp. 88 Leaf/Petiole Globose Green Hairy L ± 0.5; W ± 0.5 F Unidentified
Melastomataceae Melastomataceae sp. 89 Stem Fusiform Brown Glabrous L ± 3.5; W ± 1.3 S Unidentified Torymidae
Melastomataceae Melastomataceae sp. 90 Stem Fusiform Brown Glabrous L ± 5.0; W ± 2.3 S Unidentified
Melastomataceae Miconia sp. 91 Leaf Discoid Green Hairy L ± 0.5; W ± 0.5 F Unidentified
Melastomataceae Miconia sp. 92 Leaf Globose Brown Hairy L ± 0.2; W ± 0.2 S Lepidoptera
Melastomataceae Tibouchina sp. 93 Stem Fusiform Brown Glabrous L ± 2.0; W ± 1.0 S Lepidoptera
Meliaceae Trichilia sp. 94 Leaf Discoid Yellow Glabrous L ± 0.1; W ± 0.1 F Unidentified
Meliaceae Trichilia sp. 95 Midvein Fusiform Yellow Glabrous L ± 0.9; W ± 0.3 F Unidentified
Meliaceae Trichilia sp. 96 Stem Fusiform Brown Glabrous L ± 2.6; W ± 0.6 F Unidentified Eulophidae
Myristicaceae Myristicaceae sp. 97 Leaf Conical Brown Hairy L ± 0.4; W ± 0.4 F Unidentified
Myrtaceae Myrcia sp. 98 Leaf Amophous Yellow Glabrous L ± 1.0; W ± 1.0 F Phlaeothripidae
Myrtaceae Myrcia sp. 99 Leaf Discoid Green Glabrous L ± 0.3; W ± 0.2 F Cecidomyiidae
Myrtaceae Myrcia sp. 100 Leaf Globose Green Hairy L ± 0.1; W ± 0.1 F Cecidomyiidae
Myrtaceae Myrcia sp. 101 Stem Fusiform Brown Glabrous L ± 1.0; W ± 0.5 F Unidentified Eurytomidae
Myrtaceae Myrcia sp. 102 Stem Fusiform Brown Glabrous L ± 2.0; W ± 1.0 F Unidentified
Myrtaceae Myrcia sp. 103 Stem Fusiform Brown Glabrous L ± 3.5; W ± 0.7 F Unidentified
Myrtaceae Myrcia sp. 104 Stem Fusiform Brown Glabrous L ± 4.0; W ± 0.6 F Unidentified
Myrtaceae Myrtaceae sp. 105 Leaf bud Globose Green Hairy L ± 1.3; W ± 1.3 S Cecidomyiidae
Myrtaceae Myrtaceae sp. 106 Stem Globose Brown Glabrous L ± 0.5; W ± 0.5 S Unidentified
Nyctaginaceae Guapira sp. 107 Leaf Discoid Red Glabrous L ± 0.5; W ± 0.5 S Cecidomyiidae Eulophidae
Ochnaceae Ouratea hexasperma (A. St.-Hil.) Baill. 108 Leaf Discoid Red Glabrous L ± 0.3; W ± 0.3 S Cecidomyiidae
Proteaceae Roupala montana Aubl. 109 Leaf Conical Green Hairy L ± 0.7; W ± 0.3 S Cecidomyiidae Eulophidae
Proteaceae Roupala Montana Aubl. 110 Leaf Discoid Green Hairy L ± 0.4; W ± 0.4 S Cecidomyiidae
Proteaceae Roupala montana Aubl. 111 Stem Globose Brown Glabrous L ± 1.3; W ± 1.3 S Lepidoptera
Rhamnaceae Rhamnidium sp. 112 Lateral bud Globose Brown Glabrous L ± 1.0; W ± 0.7 F Unidentified
Rubiaceae Landia sp. 113 Leaf Fusiform Green Glabrous L ± 0.8; W ± 0.3 F Unidentified
Rubiaceae Rubiaceae sp. 114 Leaf Fusiform Yellow Hairy L ± 0.2; W ± 0.1 F Unidentified
Rubiaceae Rubiaceae sp. 115 Leaf Globose Green Glabrous L ± 0.1; W ± 0.1 F Unidentified
Rubiaceae Rubiaceae sp. 116 Leaf Globose Yellow Glabrous L ± 0.3; W ± 0.3 F Unidentified
Rubiaceae Rubiaceae sp. 117 Stem Fusiform Brown Glabrous L ± 1.2; W ± 0.6 F Unidentified
Rutaceae Zanthoxylum sp. 118 Leaf Discoid Green Hairy L ± 0.1; W ± 0.1 S Unidentified
Santalaceae Phoradendron sp. 119 Leaf Discoid Green Glabrous L ± 0.2; W ± 0.2 F Unidentified
Sapindaceae Paullinia sp. 120 Axilary bud Globose Green Hairy L ± 0.7; W ± 0.7 F Unidentified Eulophidae
Sapindaceae Paullinia sp. 121 Stem Conical Red Hairy L ± 0.3; W ± 0.2 F Unidentified
Sapindaceae Sapindaceae sp. 122 Leaf Discoid Yellow Glabrous L ± 0.3; W ± 0.3 F Unidentified
Sapindaceae Sapindaceae sp. 123 Leaf Globose Green Glabrous L ± 0.3; W ± 0.3 S Unidentified
Sapindaceae Sapindaceae sp. 124 Leaf Globose Green Glabrous L ± 0.2; W ± 0.2 S Unidentified
Sapindaceae Sapindaceae sp. 125 Stem Conical Green Glabrous L ± 1.3; W ± 0.5 F Unidentified Eulophidae
Sapindaceae Serjania sp. 126 Leaf Discoid Green Glabrous L ± 0.8; W ± 0.2 F Cecidomyiidae
Sapindaceae Serjania sp. 127 Leaf Discoid Green Glabrous L ± 0.5; W ± 0.5 S Cecidomyiidae
Sapindaceae Serjania sp. 128 Leaf Discoid Yellow Glabrous L ± 0.5; W ± 0.5 S Cecidomyiidae
Sapindaceae Serjania sp. 129 Stem Fusiform Brown Hairy L ± 2.5; W ± 1.5 F Cecidomyiidae Eurytomidae
Sapindaceae Serjania sp. 130 Tendril Fusiform Brown Glabrous L ± 2.0; W ± 1.7 F Cecidomyiidae
Siparunaceae Siparuna guianensis Aubl. 131 Leaf Discoid Green Glabrous L ± 0.5; W ± 0.5 F Cecidomyiidae
Siparunaceae Siparuna guianensis Aubl. 132 Leaf Fusiform Green Glabrous L ± 0.6; W ± 0.4 F Cecidomyiidae
Siparunaceae Siparuna guianensis Aubl. 133 Midvein Fusiform Green Glabrous L ± 0.5; W ± 0.3 F Cecidomyiidae
Siparunaceae Siparuna guianensis Aubl. 134 Petiole Globose Brown Glabrous L ± 0.4; W ± 0.4 F Cecidomyiidae
Siparunaceae Siparuna guianensis Aubl. 135 Stem Fusiform Green Glabrous L ± 1.0; W ± 0.7 F Cecidomyiidae
Siparunaceae Siparuna guianensis Aubl. 136 Stem Globose Brown Glabrous L ± 0.4; W ± 0.4 F Cecidomyiidae Eurytomidae
Siparunaceae Siparuna guianensis Aubl. 137 Stem/Petiole Fusiform Green Glabrous L ± 2.0; W ± 0.6 F Cecidomyiidae
Smilacaceae Smilax sp. 138 Leaf Globose Yellow Glabrous L ± 0.2; W ± 0.2 S Unidentified Eulophidae/Torymidae
Smilacaceae Smilax sp. 139 Leaf Globose Green Glabrous L ± 0.6; W ± 0.6 S Unidentified
Smilacaceae Smilax sp. 140 Leaf/Stem Fusiform White Glabrous L ± 2.5; W ± 2.0 F Unidentified
Styracaceae Styrax pohlii A. DC. 141 Leaf Discoid Yellow Glabrous L ± 0.1; W ± 0.1 F Cecidomyiidae
Vitaceae Cissus erosa Rich. 142 Stem Globose Brown Glabrous L ± 4.0; W ± 3.3 S Curculionidae
Vitaceae Cissus sp. 143 Leaf Globose Green Glabrous L ± 0.4; W ± 0.4 F Unidentified
Vitaceae Vitaceae sp. 144 Stem/Petiole Globose Green Hairy L ± 0.4; W ± 0.4 S Unidentified
Vochysiaceae Qualea dichotoma (Mart.) Warm. ex Wille 145 Leaf Globose Green Hairy L ± 0.2; W ± 0.2 F Cecidomyiidae
Vochysiaceae Qualea grandiflora Mart. 146 Leaf Discoid Yellow Glabrous L ± 0.3; W ± 0.3 S Cecidomyiidae
Vochysiaceae Qualea multiflora Mart. 147 Leaf Globose Green Hairy L ± 0.4; W ± 0.4 F/S Cecidomyiidae Eulophidae
Vochysiaceae Qualea multiflora Mart. 148 Leaf Globose Yellow Hairy L ± 0.6; W ± 0.6 F/S Cecidomyiidae Braconidae/Eulophidae
Vochysiaceae Qualea parviflora Mart. 149 Leaf Discoid Green Glabrous L ± 0.2; W ± 0.2 S Cecidomyiidae
Vochysiaceae Qualea parviflora Mart. 150 Leaf Globose Yellow Glabrous L ± 0.4; W ± 0.4 S Cecidomyiidae Encyrtidae

In this study we found gall-inducing insects belonging to orders Diptera, Coleoptera, Lepidoptera and Thysanoptera (Table 4). The Figs. 2-8 illustrates the gall morphotypes induced by galling insects. The most common galling taxon was Cecidomyiidae (Diptera), which induced 48.1% of the insect gall morphotypes. Galling insects of other taxonomic groups were much less frequent (only 7.2%), while from 44.7% of the insect gall morphotypes we did not find taxa of gall-inducers. Our results corroborate previous studies in the Brazilian savannas that point the dominance of Cecidomyiidae (Maia & Fernandes, 2004; Santos et al., 2010; Araújo et al., 2011), which is considered the main galling insect group of world (Gagné, 2010). The high cecidomyiid diversity in the Cerrado is hypothesized to be due to richest flora and the strongly opportunistic adaptive radiation of group (Araújo et al., 2014a). Besides of gall-inducing insects, we also record several hymenopteran parasitoids from families Braconidae, Encyrtidae, Eulophidae, Eurytomidae, Pteromalidae and Torymidae. Hymenopteran parasitoids are very frequently in Neotropical insect galls (Fernandes & Santos, 2014) and are the main natural enemies of Cecidomyiidae (Maia & Azevedo, 2009).

Table 4 Number and percentage of insect gall morphotypes in the different taxa of galling insects recorded in EA-CEFAEH, Hidrolândia, Goiás, Brazil. 

Galling insect taxa Insect gall morphotypes
N %
Cecidomyiidae (Diptera) 72 48.1
Lepidoptera 6 4.0
Thysanoptera (Phlaeothripidae) 4 2.6
Coleoptera 1 0.6
Unidentified 67 44.7
TOTAL 150 100

Figure 2 Insect gall morphotypes recorded in EA-CEFAEH, Hidrolândia, Goiás, Brazil. (A) Anacardium humile (Gall 1), (B) Myracrodruon urundeuva (Gall 2), (C) Annonaceae sp. (Gall 3), (D) Annonaceae sp. (Gall 4), (E) Annonaceae sp. (Gall 5), (F) Cardiopetalum sp. (Gall 6), (G) Aspidosperma sp. (Gall 7), (H) Aspidosperma sp. (Gall 8), (I) Aspidosperma sp. (Gall 9), (J) Aspidosperma tomentosum (Gall 10), (K) Schefflera macrocarpa (Gall 11), (L) Asteraceae sp. (Gall 12), (M) Asteraceae sp. (Gall 13), (N) Fridericia sp. (Gall 14), (O) Protium sp. (Gall 15), (P) Protium sp. (Gall 16), (Q) Caryocar brasiliense (Gall 17), (R) C. brasiliense (Gall 18), (S) Celastraceae sp. (Gall 19), (T) Plenckia populnea (Gall 20), (U) Terminalia argentea Mart. (Gall 21), (V) T. argentea (Gall 22), (W) Connaraceae sp. (Gall 23), (X) Connarus sp. (Gall 24). 

Figure 3 Insect gall morphotypes recorded in EA-CEFAEH, Hidrolândia, Goiás, Brazil. (A) Connarus sp. (Gall 25), (B) Connarus suberosus (Gall 26), (C) Davilla sp. (Gall 27), (D) Davilla sp. (Gall 28), (E) Diospyros hispida (Gall 29), (F) Sloanea sp. (Gall 30), (G) Sloanea sp. (Gall 31), (H) Erythroxylum sp. (Gall 32), (I) Erythroxylum sp. (Gall 33), (J) Erythroxylum sp. (Gall 34), (K) Erythroxylum sp. (Gall 35), (L) Erythroxylum sp. (Gall 36), (M) Erythroxylum sp. (Gall 37), (N) Erythroxylum sp. (Gall 38), (O) Erythroxylum suberosum (Gall 39), (P) Erythroxylum tortuosum (Gall 40), (Q) Euphorbiaceae sp. (Gall 41), (R) Manihot sp. (Gall 42), (S) Manihot sp. (Gall 43), (T) Maprounea guianensis (Gall 44), (U) Acosmium dasycarpum (Gall 45), (V) Bauhinia brevipes (Gall 46), (W) B. brevipes (Gall 47), (X) B. brevipes (Gall 48). 

Figure 4 Insect gall morphotypes recorded in EA-CEFAEH, Hidrolândia, Goiás, Brazil. (A) B. brevipes (Gall 49), (B) B. brevipes (Gall 50), (C) B. brevipes (Gall 51), (D) Bauhinia curvula (Gall 52), (E) B. curvula (Gall 53), (F) Bauhinia sp. (Gall 54), (G) Bauhinia sp. (Gall 55), (H) Bauhinia sp. (Gall 56), (I) Bauhinia sp. (Gall 57), (J) Bauhinia sp. (Gall 58), (K) Bauhinia sp. (Gall 59), (L) Bauhinia sp. (Gall 60), (M) Fabaceae sp. (Gall 61), (N) Fabaceae sp. (Gall 62), (O) Fabaceae sp. (Gall 63), (P) Fabaceae sp. (Gall 64), (Q) Fabaceae sp. (Gall 65), (R) Sclerolobium paniculatum (Gall 66), (S) Lamiaceae sp. (67), (T) Lamiaceae sp. (Gall 68), (U) Lauraceae sp. (Gall 69), (V) Nectandra cuspidata (Gall 70), (W) N. cuspidata (Gall 71), (X) N. cuspidata (Gall 72). 

Figure 5 Insect gall morphotypes recorded in EA-CEFAEH, Hidrolândia, Goiás, Brazil. (A) Lorantaceae sp. (Gall 73), (B) Diplusodon sp. (Gall 74), (C) Byrsonima sp. (Gall 75), (D) Diplopterys pubipetala (Gall 76), (E) D. pubipetala (Gall 77), (F) D. pubipetala (Gall 78), (G) Heteropterys eglandulosa (Gall 79), (H) Heteropterys sp. (Gall 80), (I) Malpighiaceae sp. (Gall 81), (J) Malpighiaceae sp. (Gall 82), (K) Malpighiaceae sp. (Gall 83), (L) Malpighiaceae sp. (Gall 84), (M) Malpighiaceae sp. (Gall 85), (N) Malpighiaceae sp. (Gall 86), (O) Peixotoa sp. (Gall 87), (P) Melastomataceae sp. (Gall 88), (Q) Melastomataceae sp. (Gall 89), (R) Melastomataceae sp. (Gall 90), (S) Miconia sp. (Gall 91), (T) Miconia sp. (Gall 92), (U) Tibouchina sp. (Gall 93), (V) Trichilia sp. (Gall 94), (W) Trichilia sp. (Gall 95), (X) Trichilia sp. (Gall 96). 

Figure 6 Insect gall morphotypes recorded in EA-CEFAEH, Hidrolândia, Goiás, Brazil. (A) Myristicaceae sp. (Gall 97), (B) Myrcia sp. (Gall 98), (C) Myrcia sp. (Gall 99), (D) Myrcia sp. (Gall 100), (E) Myrcia sp. (Gall 101), (F) Myrcia sp. (Gall 102), (G) Myrcia sp. (Gall 103), (H) Myrcia sp. (Gall 104), (I) Myrtaceae sp. (Gall 105), (J) Myrtaceae sp. (Gall 106), (K) Guapira sp. (Gall 107), (L) Ouratea hexasperma (Gall 108), (M) Roupala montana (Gall 109), (N) R. montana (Gall 110), (O) R. montana (Gall 111), (P) Rhamnidium sp. (Gall 112), (Q) Landia sp. (Gall 113), (R) Rubiaceae sp. (Gall 114), (S) Rubiaceae sp. (Gall 115), (T) Rubiaceae sp. (116), (U) Rubiaceae sp. (Gall 117), (V) Zanthoxylum sp. (Gall 118), (W) Phoradendron sp. (Gall 119), (X) Paullinia sp. (Gall 120). 

Figure 7 Insect gall morphotypes recorded in EA-CEFAEH, Hidrolândia, Goiás, Brazil. (A) Paullinia sp. (Gall 121), (B) Sapindaceae sp. (Gall 122), (C) Sapindaceae sp. (Gall 123), (D) Sapindaceae sp. (Gall 124), (E) Sapindaceae sp. (Gall 125), (F) Serjania sp. (Gall 126), (G) Serjania sp. (Gall 127), (H) Serjania sp. (Gall 128), (I) Serjania sp. (Gall 129), (J) Serjania sp. (Gall 130), (K) Siparuna guianensis (Gall 131), (L) S. guianensis (Gall 132), (M) S. guianensis (Gall 133), (N) S. guianensis (Gall 134), (O) S. guianensis (Gall 135), (P) S. guianensis (Gall 136), (Q) S. guianensis (Gall 137), (R) Smilax sp. (Gall 138), (S) Smilax sp. (Gall 139), (T) Smilax sp. (Gall 140), (U) Styrax pohlii A. DC. (Gall 141), (V) Cissus erosa (Gall 142), (W) Cissus sp. (Gall 143), (X) Vitaceae sp. (Gall 144). 

Figure 8 Insect gall morphotypes recorded in EA-CEFAEH, Hidrolândia, Goiás, Brazil. (A) Qualea dichotoma (Gall 145), (B) Qualea grandiflora (Gall 146), (C) Qualea multiflora (Gall 147), (D) Q. multiflora (Gall 148), (E) Qualea parviflora (Gall 149), (F) Q. parviflora (Gall 150). 

Of the 150 insect gall morphotypes recorded in our study, 81 were recorded in the savanna site and 73 in the forest site. Only the globoid gall morphotype (Gall 18) recorded on Caryocar brasiliense (Caryocaraceae), the conical gall morphotype (Gall 76) of Diplopterys pubipetala (Malpighiaceae) and the two gall morphotypes (Galls 147 and 148) recorded on Qualea multiflora (Vochysiaceae) were common between savanna and forest sites. Comparisons between different vegetation types in the Cerrado have pointed higher insect gall richness in the sclerophyllous habitats, with savannas often have greater species richness than the forests (Gonçalves-Alvim & Fernandes, 2001; Araújo et al., 2011; Araújo et al., 2014a). Our results corroborate the pattern of higher frequency of insect galls in xeric habitats than in mesics (although it was not the objective of the work to test statistically these differences). Among the possible explanations to this pattern are that in xeric environments the plants are more nutritive to galling insects and the attack frequency of natural enemies (e.g., parasitoids) is lower as compared to mesic habitats, as predicted by hydrothermal stress hypothesis at community level (Fleck & Fonseca, 2007; Araújo et al., 2014a).

CONCLUSIONS

This is the first systematic survey of insect galls realized in the EA-CEFAEH and region of Hidrolândia city. Although the study area is relatively anthropized and little fragments, the sampled sites presented great insect gall richness as compared to other sites cataloged to the Central region of Brazil. The EA-CEFAEH area had more insect gall morphotypes than the Parque Estadual da Serra dos Pireneus (62, Araújo et al., 2011) and Parque Nacional das Emas (97, Araújo et al., 2014b). Despite the possible effects of sampling effort differences between these studies, as previously discussed, our results show that any vegetation fragment can be a potential shelter to conserve insect galls. Finally, the observed results about host plant taxa, galling insect groups, gall morphology and occurrence between vegetation types confirm the known patterns of Brazilian Cerrado.

ACKNOWLEDGEMENTS

The authors are thankful to Julio Miguel Grandes Rios for suggestions to the manuscript; to Rodolph Delfino Sartin for support in the project execution; to trainees of Laboratory of Entomology and Laboratory of Morphology and Plant Taxonomy (UFG) for help in the field and laboratory; 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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1Edited by: Carlos José Einicker Lamas

Published with the financial support of the "Programa de Apoio às Publicações Científicas Periódicas da USP"

3Seção de Publicações - Museu de Zoologia da Universidade de São Paulo

Recibido: 13 de Marzo de 2017; Aprobado: 26 de Octubre de 2017

3 E-mail: elienaibio@gmail.com

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

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

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