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Revista Brasileira de Entomologia

Print version ISSN 0085-5626On-line version ISSN 1806-9665

Rev. Bras. entomol. vol.61 no.1 São Paulo Jan./Mar. 2017

http://dx.doi.org/10.1016/j.rbe.2016.08.002 

BIOLOGY, ECOLOGY AND DIVERSITY

Characterization of entomogen galls from Mato Grosso do Sul, Brazil

Maria Virginia Urso-Guimarães a   *  

Ana Carolina Devides Castello b  

Eric Yasuo Kataoka a  

Ingrid Koch c  

aUniversidade Federal de São Carlos, Departamento de Biologia, Sorocaba, SP, Brazil

bUniversidade Estadual de São Paulo, Programa de Pós Graduação em Ciências Biológicas (Botânica), Botucatu, SP, Brazil

cUniversidade de Campinas, Departamento de Biologia Vegetal, Campinas, SP, Brazil

ABSTRACT

In this paper we performed a study of occurrence and characterization of entomogen galls from natural vegetation areas in Mato Grosso do Sul. We surveyed natural areas of four biomes from Mato Grosso do Sul State: Pantanal (Corumbá), Atlantic Forest (Bodoquena), Cerrado (Aquidauana), and Chaco (Porto Murtinho). We identified 186 morphotypes of galls in 115 host plant species from 35 families and 73 genera. The richest families were Fabaceae (N = 34), Sapindaceae (N = 24), Bignoniaceae (N = 17), and Myrtaceae (N = 15). Fifty morphotypes of insects (27%) were found in galls of 38 host plants, 78% of which belongs to Diptera, 10% to Hymenoptera, and the other 12% are divided among Hemiptera, Thysanoptera, Coleoptera, and Lepidoptera. In this study, the geographic distribution of gall morphotypes associated to the cecidomyiids Youngomyia pouteriae Maia, 2004, and Trotteria quadridentata Maia, 2004 (Diptera, Cecidomyiidae), and the wasp Mononeuron duguetiae Fischer, 1981 (Hymenoptera, Braconidae, Doryctinae) are expanded to the localities sampled in MS. In addition, four genera and 24 species of plants were recorded for the first time as hosts to entomogen galls. All occurrences of Cecidomyiidae in Mato Grosso do Sul's localities are new records for this family.

Keywords: Atlantic Forest; Cerrado; Chaco; Pantanal; Neotropical region

Introduction

Galls are structures formed via abnormal cell growth in response to stimulation caused by organisms such as insects, nematodes, fungi or bacteria (Carneiro et al., 2009a ; Rohfritsch and Shorthouse, 1982). The global richness of insect galls has been estimated to be about 130,000 species (Espírito-Santo and Fernandes, 2007). Galls are unequivocal markers of species-specific relationships, since about 90% of all gall-forming species are monophagous (Carneiro et al., 2009a ; Raman, 2010), thus they can be applied to understand relationships between gall-maker species richness and plant species diversity of a given area (Butterill and Novotný, 2015), with the potential use of galls as bioindicators (Julião et al., 2005).

The insect orders associated with gall formation are Diptera, Lepidoptera, Hymenoptera, Coleoptera, Hemiptera, and Thysanoptera. There is a large predominance of galls induced by Diptera, especially Cecidomyiidae, with over a thousand records of gall morphotypes in the Neotropical region (Maia, 2006 ; Maia et al., 2008), and a calculated average of 64% of the gall-inducing insect species in the world (Espírito-Santo and Fernandes, 2007). Cecidomyiidae is the main group of gall-forming insects in all zoogeographical regions, with around 4,800 described species of gall makers to the world (Gagné and Jaschhof, 2014).

Despite an increasing number of studies on the occurrence and characterization of galls in Brazil made by Tavares, 1909; Tavares, 1917; Tavares, 1918; Tavares, 1920; Tavares, 1922 ; Tavares, 1925, Houard (1933), and Occhioni, 1979 ; Occhioni, 1981, some biomes remain poorly sampled, such as the Pantanal, Caatinga and the Amazonian forest (Julião et al., 2002; Julião et al., 2014; Carvalho-Fernandes et al., 2012; Santos et al., 2011; Maia, 2011 ; Maia et al., 2014). In this study, we contributed providing the first survey of the galls and gall makers of Mato Grosso do Sul, including four areas of natural vegetation in the Cerrado, Atlantic Forest, Pantanal and Chaco biomes, which compose the flora mosaic in Mato Grosso do Sul. We documented and characterized gall morphology and identified host plants. Gall makers were also identified or inferred when obtained.

Material and methods

Study areas

Mato Grosso do Sul State has an approximate area of 358 km2, 4.2% of the total Brazilian territory. The relief of the state consists of plateaus, tablelands and levels, within the Paraná and Paraguay river basins; elevation ranges from 200 m to 700 m (Governo do Mato Grosso do Sul, 2016). According to Köeppen's climate zone classification (Alvares et al., 2013), most of the state's territory is in the tropical climate zone. The following climate types occur in Mato Grosso do Sul: Af (tropical without dry season), Am (tropical monsoon), Aw (tropical with dry winter) and Cfa (humid subtropical with hot summer), with a rainy summer and a dry winter, characterized by average temperatures ranging from 25 °C in the lowlands of Paraguay to 20 °C in the plateau of Bodoquena and Maracaju, and mean annual precipitation of 1500 mm (Governo do Mato Grosso do Sul, 2016).

Vegetation includes Cerrado, Pantanal, Chaco, and Atlantic Forest biomes, with approximately 60% of the area occupied by Cerrado (Silva et al., 2011). The richest plant families in all biomes are Fabaceae, Sapindaceae, Bignoniaceae, and Myrtaceae (Damasceno et al., 2005; Pott and Pott, 1999 ; Frison, 2007). Fabaceae is the most speciose family in Mato Grosso do Sul (Frison, 2007; Mendonça et al., 2008; Baptista-Maria et al., 2009 ; Freitas et al., 2013).

Samplings were carried out in areas of natural vegetation remnants in four municipalities of Mato Grosso do Sul State (IBGE, 2000): Aquidauana, Bodoquena, Corumbá, and Porto Murtinho, in the Cerrado, Atlantic Forest, Pantanal, and Chaco biomes, respectively (Fig. 1).

Fig. 1. Map of the sampling localities and their biomes of Mato Grosso do Sul State, Brazil. ■ sampling points in the municipality, ☆ Cerrado, * Atlantic Forest, • Pantanal, ♦ Chaco. 

Sampling

We selected eight areas for sampling, two areas for each biome: Cerrado, Atlantic Forest, Pantanal, and Chaco (Table 1 and Fig. 1). Samples were collected during three expeditions, April 2012, December 2012, and December 2013, according to a time-based method described by Price et al. (1998). Each area was sampled once, with sampling effort of two hours in each biome, totaling eight hours. According to Fernandes et al. (1995), there is no significant difference in gall abundance in different seasons, thus sampling during one season is sufficient to evaluate the number of galls per habitat. Galls are sessile and remain attached to the host plants, which makes it possible to detect galls even after adult emergence. All samples were collected at trail edges. This environment has high solar incidence and low humidity, with increased gall richness (Price et al., 1998), because galls occurence is associated with hygrothermal stress in several environments (Fernandes and Price, 1991 ; Julião et al., 2014). In addition, route length (L) of each area was measured to better understand gall richness in the sampled areas (Table 1).

Table 1 Sampling localities of Mato Grosso do Sul State informing biomes per locality, coordinates of starting points, and route length. Atlantic Forest. 

Biome Locality Coordinates Route length
Cerrado Aquidauana/Universidade Estadual de Mato Grosso do Sul (UEMS) S 20° 27' 21.4? W 055° 39' 46.1? 290 m
Cerrado Aquidauana/Distrito de Camisão S 20° 26' 58.1? W 055° 38' 16.9? 300 m
Atlantic Forest Bodoquena/Sede Fazenda Califórnia S 20° 42' 18.9? W 56° 51' 17.4? 320 m
Atlantic Forest Bodoquena/Trilha da Gruta S 20° 41' 55.9? W 56° 52' 49.4? 517 m
Pantanal Corumbá/Base de Estudos do Pantanal S 19° 34' 20.09? W 057° 00' 57.09? 400 m
Pantanal Corumbá/Fazenda São Bento S 19° 28' 09.1? W 057° 01' 49.9? 110 m
Chaco Porto Murtinho/Trilha Fazenda Retiro Conceição S 21° 41' 07.6? W 57° 45' 09.0? 662 m
Chaco Porto Murtinho/Trilha Fazenda Campo Florido S 21° 38' 18.3? W 57° 42' 22.7? 550 m

We collected branches of gall-bearing plants, which were subsequently photographed, stored, and labeled in plastic bags. Morphological descriptions of galls and identification of host plants and gall makers were conducted in laboratory. Characterization of gall's morphological types followed Isaias et al. (2013). Gall-maker species not obtained by adult emergence were identified via comparisons to several studies of gall-maker's community characterization in dry vegetation (Julião et al., 2002; Malves and Frieiro-Costa, 2012; Urso-Guimarães et al., 2003; Maia and Fernandes, 2004; Urso-Guimarães and Scarelli-Santos, 2006; Carneiro et al., 2009b; Coelho et al., 2009; Maia, 2011; Santos et al., 2011; Saito and Urso-Guimarães, 2012; Araújo et al., 2014; Maia and Carvalho-Fernandes, 2016 ; Nogueira et al., 2016). Plant identification was performed using identification keys, comparison with herbarium material and consultations with experts, and the specimens were deposited in the Universidade Federal de São Carlos, campus Sorocaba Herbarium (SORO). The families are listed according to APG IV (2016). Portions of branches with galls were stored in plastic containers closed with fine mesh to obtain inductors or associated entomofauna. All insect material was stored in 70% ethanol. Gall makers and associated fauna were identified by specialists and were deposited in the Museu de Zoologia da Universidade de São Paulo (MZUSP).

Results and discussion

Overall 186 gall morphotypes (Table 2 and Figs. 2-25, Figs. 26-49, Figs. 50-73, Figs. 74-97, Figs. 98-121, Figs. 122-145, Figs. 146-169 ; Figs. 170-185) were collected in 115 species of host plants belonging to 35 families and 73 genera. Nine of these species were identified only at the family level, and 20 at the genus level. The average number of gall morphotypes per plant species was 1.6 (Table 3). Despite adopting different methodologies, several authors have found similar results in other areas of Neotropical savannas and seasonally dry tropical forests, such as Goiânia (x = 1.8), Ecological Station of Jataí (x = 1.7), Vaçununga State Park (x = 1.4), Delfinópolis (x = 1.2), Boqueirão Biological Reserve (x = 1.4), Serra de São José (x = 1.8), Serra do Cipó (x = 1.8), Cadeia do Espinhaço (x = 1.6), Pernambuco (x = 1.3) (Table 3).

Table 2 Characterization of insect galls recorded in the Mato Grosso do Sul Statebiomesby species of host plant. Figures refer to gall morphotype's picture. 

Host family Host species Organ Shape Color Pubescence Locality/Biome No. of figure
Annonaceae Annona emarginata (Schltdl.) H.Rainer Leaf Cylindrical Green Yes Aquidauana/Cerrado 2
Annonaceae Duguetia furfuracea (A.St.-Hil.) Saff. Leaf Globoid Yellow Yes Aquidauana/Cerrado 3
Annonaceae Duguetia furfuracea (A.St.-Hil.) Saff. Leaf Lenticular Yellow No Aquidauana/Cerrado 4
Annonaceae Annonaceae sp. Stem Globoid Green No Bodoquena/Atlantic Forest 5
Apocynaceae Aspidosperma cylindrocarpon Müll.Arg. Leaf Lenticular Brown No Corumbá/Pantanal 6
Apocynaceae Aspidosperma olivaceum Müll.Arg. Leaf Globoid Yellow No Bodoquena/Atlantic Forest 7
Apocynaceae Aspidosperma olivaceum Müll.Arg. Leaf Triangular Green No Bodoquena/Atlantic Forest 8
Apocynaceae Aspidosperma subincanum Mart. Leaf Lenticular Yellow No Bodoquena/Atlantic Forest 9
Apocynaceae Forsteronia rufa Müll.Arg. Leaf Lenticular Brown No Bodoquena/Atlantic Forest 10
Apocynaceae Forsteronia rufa Müll.Arg. Leaf Globoid Green Yes Porto Murtinho/Chaco 11
Apocynaceae Forsteronia rufa Müll.Arg. Leaf Globoid Green No Porto Murtinho/Chaco 12
Apocynaceae Forsteronia rufa Müll.Arg. Leaf Globoid Green No Bodoquena/Atlantic Forest 13
Apocynaceae Forsteronia velloziana (A.DC.) Woodson Leaf Lenticular Yellow No Corumbá/Pantanal 14
Apocynaceae Forsteronia velloziana (A.DC.) Woodson Leaf Globoid Brown No Corumbá/Pantanal 14
Asteraceae Asteraceae sp. 1 Leaf Lenticular Brown No Bodoquena/Atlantic Forest 15
Asteraceae Asteraceae sp. 2 Leaf Wrinkle Green No Bodoquena/Atlantic Forest 16
Asteraceae Mikania sp. Leaf Lenticular Brown No Bodoquena/Atlantic Forest 17
Asteraceae Vernonia polyanthes Less Stem Globoid Green No Bodoquena/Atlantic Forest 18
Asteraceae Vernonanthura brasiliana (L.) H.Rob. Leaf Amorphous Brown No Bodoquena/Atlantic Forest 19
Asteraceae Vernonanthura brasiliana (L.) H.Rob. Leaf Lenticular Yellow No Bodoquena/Atlantic Forest 20
Asteraceae Vernonanthura brasiliana (L.) H.Rob. Leaf Globoid Green Yes Bodoquena/Atlantic Forest 21
Asteraceae Vernonanthura brasiliana (L.) H.Rob. Stem Globoid Brown No Bodoquena/Atlantic Forest 22
Bignoniaceae Adenocalymma bracteatum (Cham.) DC. Leaf vein Fusiform Green No Corumbá/Pantanal 23
Bignoniaceae Fridericia chica (Bonpl.) L.G.Lohmann Leaf Lenticular Cream No Bodoquena/Atlantic Forest 24
Bignoniaceae Fridericia chica (Bonpl.) L.G.Lohmann Leaf Lenticular Brown No Bodoquena/Atlantic Forest 25
Bignoniaceae Fridericia chica (Bonpl.) L.G.Lohmann Leaf Lenticular Cream No Bodoquena/Atlantic Forest 26
Bignoniaceae Fridericia chica (Bonpl.) L.G.Lohmann Leaf Globoid Green Yes Bodoquena/Atlantic Forest 27
Bignoniaceae Fridericia chica (Bonpl.) L.G.Lohmann Stem Fusiform Brown No Bodoquena/Atlantic Forest 28
Bignoniaceae Fridericia chica (Bonpl.) L.G.Lohmann Stem Globoid Orange No Bodoquena/Atlantic Forest 29
Bignoniaceae Fridericia chica (Bonpl.) L.G.Lohmann Stem Globoid Brown No Bodoquena/Atlantic Forest 30
Bignoniaceae Fridericia caudigera (S.Moore) L.G.Lohmann Tendril Fusiform Green No Bodoquena/Atlantic Forest 31
Bignoniaceae Handroanthus chrysotrichus (Mart. ex DC.) Mattos Leaf Lenticular Green/brown Yes Aquidauana/Cerrado 32
Bignoniaceae Handroanthus ochraceus (Cham.) Mattos Leaf Cylindrical Green Yes Aquidauana/Cerrado 33
Bignoniaceae Handroanthus ochraceus (Cham.) Mattos Leaf Globoid Green Yes Aquidauana/Cerrado 34
Bignoniaceae Handroanthus heptaphyllus (Vell.) Mattos Leaf Lenticular Green No Corumbá/Pantanal 35
Bignoniaceae Handroanthus heptaphyllus (Vell.) Mattos Leaf/stem Fusiform Brown No Porto Murtinho/Chaco 36
Bignoniaceae Tabebuia roseoalba (Ridl.) Sandwith Leaf vein Fusiform Green No Bodoquena/Atlantic Forest 37
Bignoniaceae Tanaecium pyramidatum (Rich.) L.G.Lohmann Leaf vein Fusiform Cream No Aquidauana/Cerrado 38
Bignoniaceae Bignoniaceae sp. Leaf Conical Green Yes Aquidauana/Cerrado 39
Burseraceae Protium heptaphyllum (Aubl.) Marchand Leaf Globoid Green Yes Aquidauana/Cerrado 40
Cannabaceae Celtis spinosa Spreng. Stem Conical Green Yes Bodoquena/Atlantic Forest 41
Cannabaceae Celtis spinosa Spreng. Stem Fusiform Brown No Porto Murtinho/Chaco 42
Caryocaraceae Caryocar brasiliense Cambess. Leaf Lenticular Yellow Yes Aquidauana/Cerrado 43
Combretaceae Terminalia argentea Mart. Leaf Lenticular Brown No Aquidauana/Cerrado 44
Combretaceae Terminalia cf. fagifolia Leaf Globoid Yellow Yes Aquidauana/Cerrado 45
Connaraceae Connarus cf. suberosus Planch. Leaf Globoid Cream Yes Aquidauana/Cerrado 46
Connaraceae Connarus cf. suberosus Planch. Leaf Fusiform Brown No Aquidauana/Cerrado 47
Convolvulaceae Ipomoea alba L. Stem Fusiform Brown No Bodoquena/Atlantic Forest 48
Dilleniaceae Davilla elliptica A.St.-Hil. Stem Globoid Brown No Bodoquena/Atlantic Forest 49
Erythroxylaceae Erythroxylum suberosum A.St.-Hil. Leaf Amorphous Brown Yes Aquidauana/Cerrado 50
Euphorbiaceae Manihot tripartita (Spreng.) Müll.Arg. Leaf Cylindrical Green/red No Aquidauana/Cerrado 51
Euphorbiaceae Croton floribundus Spreng. Leaf Globoid Green No Bodoquena/Atlantic Forest 52
Euphorbiaceae Croton sp. 1 Stem Fusiform Brown No Bodoquena/Atlantic Forest 53
Euphorbiaceae Croton sp. 2 Leaf vein Fusiform Green No Corumbá/Pantanal 54
Euphorbiaceae Croton sp. 2 Leaf Marginal roll Green No Corumbá/Pantanal 55
Euphorbiaceae Sapium glandulosum (L.) Morong Leaf vein Fusiform Green No Porto Murtinho/Chaco 56
Fabaceae Anadenanthera peregrina var. falcata (Benth.) Altschul Leaflets Globoid with spur Brown No Porto Murtinho/Chaco 57
Fabaceae Bauhinia mollis (Bong.) D.Dietr. Leaf Lenticular Brown No Porto Murtinho/Chaco 58
Fabaceae Bauhinia holophylla (Bong.) Steud. Leaflets junction Globoid Green No Porto Murtinho/Chaco 59
Fabaceae Bauhinia holophylla (Bong.) Steud. Leaf Lenticular Cream No Aquidauana/Cerrado 60
Fabaceae Bauhinia holophylla (Bong.) Steud. Leaf Globoid Cream Yes Aquidauana/Cerrado 61
Fabaceae Bauhinia longifolia (Bong.) Steud. Stem Amorphous Brown No Aquidauana/Cerrado 62
Fabaceae Bauhinia ungulata L. Leaf Conical Brown No Porto Murtinho/Chaco 63
Fabaceae Bauhinia ungulata L. Leaf Globoid Green/red No Porto Murtinho/Chaco 64
Fabaceae Bauhinia ungulata L. Stem Fusiform Brown No Aquidauana/Cerrado 65
Fabaceae Copaifera langsdorffii Desf. Leaf Lenticular Brown No Aquidauana/Cerrado 66
Fabaceae Copaifera langsdorffii Desf. Leaf Globoid Yellow No Corumbá/Pantanal 67
Fabaceae Dipteryx alata Vogel Leaf Lenticular Brown No Aquidauana/Cerrado 68
Fabaceae Dipteryx alata Vogel Leaf Wrinkle Green No Aquidauana/Cerrado 69
Fabaceae Fabaceae sp. Leaf Lenticular Green No Bodoquena/Atlantic Forest 70
Fabaceae Galactia striata (Jacq.) Urb. Leaf vein Fusiform Green Yes Porto Murtinho/Chaco 71
Fabaceae Guibourtia hymenaeifolia (Moric.) J.Léonard Leaf Lenticular Brown No Aquidauana/Cerrado 72
Fabaceae Guibourtia hymenaeifolia (Moric.) J.Léonard Leaf vein Fusiform Green No Aquidauana/Cerrado 73
Fabaceae Guibourtia hymenaeifolia (Moric.) J.Léonard Leaf Globoid Brown No Aquidauana/Cerrado 74
Fabaceae Hymenaea stigonocarpa Mart. ex Hayne Leaf Lenticular Green Yes Aquidauana/Cerrado 75
Fabaceae Hymenaea stigonocarpa Mart. ex Hayne Leaf vein Lenticular Green No Aquidauana/Cerrado 76
Fabaceae Hymenaea stigonocarpa Mart. ex Hayne Leaf Globoid Brown No Aquidauana/Cerrado 77
Fabaceae Hymenaea stigonocarpa Mart. ex Hayne Leaf Lenticular Green No Aquidauana/Cerrado 78
Fabaceae Inga vera Willd. Leaf Globoid Brown No Corumbá/Pantanal 79
Fabaceae Inga vera Willd. Leaf Lenticular Green No Aquidauana/Cerrado 80
Fabaceae Inga vera Willd. Leaf Lenticular Green No Corumbá/Pantanal 81
Fabaceae Inga vera Willd. Leaf Globoid Red Yes Bodoquena/Atlantic Forest 82
Fabaceae Machaerium amplum Benth. Leaf Lenticular Yellow No Aquidauana/Cerrado 83
Fabaceae Mimosa sp. 1 Stem Fusiform Green No Aquidauana/Cerrado 84
Fabaceae Mimosa sp. 2 Leaflets Fusiform Green/red No Porto Murtinho/Chaco 85
Fabaceae Mimosa sp. 2 Stem Fusiform Brown No Porto Murtinho/Chaco 86
Fabaceae Mimosa sp. 3 Leaflets Leaflets junction Green No Porto Murtinho/Chaco 87
Fabaceae Peltogyne confertiflora (Mart. ex Hayne) Benth. Leaf Lenticular Green Yes Aquidauana/Cerrado 88
Fabaceae Peltogyne confertiflora (Mart. ex Hayne) Benth. Leaf Globoid Brown No Aquidauana/Cerrado 89
Fabaceae Senna velutina (Vogel) H.S.Irwin & Barneby Leaf Lenticular Brown Yes Aquidauana/Cerrado 90
Lamiaceae Hyptis brevipes Poit. Inflorescence Floral tube Not apply Not apply Corumbá/Pantanal 91
Lamiaceae Hyptis sp Leaf Globoid Green Yes Corumbá/Pantanal 92
Lauraceae Lauraceae sp. Leaf Lenticular Green No Bodoquena/Atlantic Forest 93
Lauraceae Persea sp. Leaf Triangular Green No Corumbá/Pantanal 94
Loganiaceae Strychnos parvifolia A.DC. Leaf Globoid Green Yes Bodoquena/Atlantic Forest 95
Malpighiaceae Amorimia pubiflora (A.Juss.) W.R.Anderson Leaf Lenticular Green No Aquidauana/Cerrado 96
Malpighiaceae Amorimia pubiflora (A.Juss.) W.R.Anderson Leaf Triangular Green No Aquidauana/Cerrado 97
Malpighiaceae Amorimia pubiflora (A.Juss.) W.R.Anderson Leaf Globoid with spur Green No Aquidauana/Cerrado 98
Malpighiaceae Byrsonima crassifolia (L.) Kunth Leaf Lenticular Red Yes Aquidauana/Cerrado 99
Malpighiaceae Bunchosia paraguariensis Nied. Leaf Globoid Brown Yes Aquidauana/Cerrado 100
Malpighiaceae Mascagnia cordifolia (A.Juss.) Griseb. Leaf Globoid Green Yes Aquidauana/Cerrado 101
Malpighiaceae Mascagania sepium (A.Juss.) Griseb. Leaf Lenticular Brown No Corumbá/Pantanal 102
Malpighiaceae Malpighiaceae sp Leaf Wrinkle Brown No Corumbá/Pantanal 103
Malvaceae Luehea divaricata Mart. & Zucc. Leaf Globoid Cream Yes Aquidauana/Cerrado 104
Malvaceae Malvaceae sp. Leaf Lenticular Brown No Bodoquena/Atlantic Forest 105
Malvaceae Byttneria dentata Pohl Leaf Globoid Green Yes Corumbá/Pantanal 106
Malvaceae Waltheria indica L. Stem Fusiform Brown No Porto Murtinho/Chaco 107
Melastomataceae Melastomataceae sp. Leaf Lenticular Green Yes Aquidauana/Cerrado 108
Meliaceae Guarea guidonia (L.) Sleumer Leaf vein Globoid Cream No Aquidauana/Cerrado 109
Menispermaceae Cissampelos pareira L. Stem Fusiform Brown No Aquidauana/Cerrado 110
Moraceae Brosimum gaudichaudii Trécul Leaf Lenticular Brown No Aquidauana/Cerrado 111
Myrtaceae Campomanesia pubescens (Mart. ex DC.) O.Berg Leaf Riniform Green/red Yes Aquidauana/Cerrado 112
Myrtaceae Eugenia bimarginata DC. Leaf Lenticular Yellow No Aquidauana/Cerrado 113
Myrtaceae Eugenia florida DC. Leaf Lenticular Brown No Aquidauana/Cerrado 114
Myrtaceae Eugenia florida DC. Leaf Lenticular Brown No Bodoquena/Atlantic Forest 115
Myrtaceae Eugenia florida DC. Leaf Globoid Brown No Bodoquena/Atlantic Forest 116
Myrtaceae Eugenia florida DC. Leaf Marginal roll Green/red No Bodoquena/Atlantic Forest 117
Myrtaceae Eugenia florida DC. Leaf Cylindrical Green No Corumbá/Pantanal 118
Myrtaceae Eugenia florida DC. Leaf Lenticular Brown No Corumbá/Pantanal 119
Myrtaceae Eugenia punicifolia (Kunth) DC. Leaf Lenticular Black No Aquidauana/Cerrado 120
Myrtaceae Eugenia punicifolia (Kunth) DC. Leaf Lenticular Black No Porto Murtinho/Chaco 121
Myrtaceae Eugenia punicifolia (Kunth) DC. Stem Fusiform Brown No Aquidauana/Cerrado 122
Myrtaceae Eugenia punicifolia (Kunth) DC. Stem Fusiform Brown No Porto Murtinho/Chaco 123
Myrtaceae Myrcia sp. Leaf Lenticular Green No Aquidauana/Cerrado 124
Myrtaceae Myrcia sp. Stem Globoid Red No Aquidauana/Cerrado 125
Myrtaceae Psidium guajava L. Leaf Marginal roll Brown Not apply Bodoquena/Atlantic Forest 126
Onagraceae Ludwigia longifolia (DC.) H.Hara Leaf Lenticular Green No Porto Murtinho/Chaco 127
Piperaceae Piper sp. Leaf Marginal roll Green Not apply Bodoquena/Atlantic Forest 128
Proteaceae Roupala montana Aubl. Leaf Lenticular Brown No Aquidauana/Cerrado 129
Rubiaceae Bathysa sp. Leaf Lenticular Brown No Corumbá/Pantanal 130
Rubiaceae Guettarda pohliana Müll.Arg. Stem Fusiform Green No Bodoquena/Atlantic Forest 131
Rubiaceae Psychotria carthagenensis Jacq Leaf Lenticular Green No Bodoquena/Atlantic Forest 132
Rubiaceae Psychotria carthagenensis Jacq Leaf Globoid Orange No Bodoquena/Atlantic Forest 133
Rubiaceae Psychotria carthagenensis Jacq Leaf Globoid Red Yes Bodoquena/Atlantic Forest 134
Rubiaceae Psychotria carthagenensis Jacq. Leaf Globoid Yellow No Bodoquena/Atlantic Forest 135
Rubiaceae Psychotria carthagenensis Jacq. Leaf Fusiform Brown No Bodoquena/Atlantic Forest 136
Rubiaceae Randia armata (Sw.) DC. Leaf vein Lenticular Green No Bodoquena/Atlantic Forest 137
Rubiaceae Randia armata (Sw.) DC. Leaf Globoid Brown No Corumbá/Pantanal 138
Rubiaceae Rubiaceae sp. 1 Stem Fusiform Brown No Porto Murtinho/Chaco 139
Rubiaceae Rubiaceae sp. 2 Stem Fusiform Brown No Bodoquena/Atlantic Forest 140
Rutaceae Zanthoxylum sp. Leaf Lenticular Brown No Bodoquena/Atlantic Forest 141
Rutaceae Zanthoxylum sp. Leaf Lenticular White No Bodoquena/Atlantic Forest 142
Rutaceae Zanthoxylum sp. Stem Fusiform Green No Bodoquena/Atlantic Forest 143
Rutaceae Zanthoxylum riedelianum Engl. Leaf Lenticular Green No Bodoquena/Atlantic Forest 144
Salicaceae Casearia sp. Leaf vein Fusiform Green No Bodoquena/Atlantic Forest 145
Salicaceae Casearia gossypiosperma Briq. Leaf Lenticular Brown No Bodoquena/Atlantic Forest 146
Salicaceae Casearia sylvestris Sw. Leaf Lenticular Brown No Bodoquena/Atlantic Forest 147
Salicaceae Casearia sylvestris Sw. Leaf Triangular Green No Bodoquena/Atlantic Forest 148
Salicaceae Casearia sylvestris Sw. Stem Fusiform Brown No Bodoquena/Atlantic Forest 149
Salicaceae Xylosma sp. Leaf Lenticular Brown No Corumbá/Pantanal 150
Sapindaceae Magonia pubescens A.St.-Hil. Leaf Globoid Green No Aquidauana/Cerrado 151
Sapindaceae Magonia pubescens A.St.-Hil. Leaf Globoid Green No Porto Murtinho/Chaco 152
Sapindaceae Magonia pubescens A.St.-Hil. Leaf Globoid Green No Porto Murtinho/Chaco 153
Sapindaceae Matayba guianensis Aubl. Leaf Lenticular Green Yes Aquidauana/Cerrado 154
Sapindaceae Serjania cf. caracasana (Jacq.) Willd. Leaf Lenticular Green No Corumbá/Pantanal 155
Sapindaceae Serjania cf. caracasana (Jacq.) Willd. Leaf Globoid Green No Corumbá/Pantanal 156
Sapindaceae Serjania cf. crassifolia Radlk. Leaf Globoid Green No Aquidauana/Cerrado 157
Sapindaceae Serjania cf. crassifolia Radlk. Leaf Amorphous Green No Aquidauana/Cerrado 158
Sapindaceae Serjania cf. glabrata Kunth Leaf vein Fusiform Green No Aquidauana/Cerrado 159
Sapindaceae Serjania cf. glabrata Kunth Leaf Cylindrical Green Yes Bodoquena/Atlantic Forest 160
Sapindaceae Serjania cf. glabrata Kunth Leaf Lenticular Green No Bodoquena/Atlantic Forest 161
Sapindaceae Serjania cf. glabrata Kunth Leaf Lenticular Green No Corumbá/Pantanal 162
Sapindaceae Serjania cf. glabrata Kunth Leaf vein Globoid Green No Bodoquena/Atlantic Forest 163
Sapindaceae Serjania cf. glabrata Kunth Leaf Globoid Brown No Bodoquena/Atlantic Forest 164
Sapindaceae Serjania cf. glabrata Kunth Leaf Conical Green No Bodoquena/Atlantic Forest 165
Sapindaceae Serjania sp. 1 Leaf Globoid Green No Aquidauana/Cerrado 166
Sapindaceae Serjania sp. 2 Leaf Cylindrical Brown No Corumbá/Pantanal 167
Sapindaceae Serjania sp. 2 Leaf Lenticular Brown No Corumbá/Pantanal 168
Sapindaceae Serjania sp. 2 Leaf Conical Green Yes Corumbá/Pantanal 168
Sapindaceae Serjania sp. 2 Tendril Fusiform Green Yes Corumbá/Pantanal 169
Sapindaceae Serjania sp. 3 Leaf Lenticular Cream No Corumbá/Pantanal 170
Sapindaceae Serjania sp. 3 Leaf Globoid Brown No Corumbá/Pantanal 171
Sapindaceae Serjania sp. 4 Leaf Cylindrical Green/pink No Aquidauana/Cerrado 172
Sapindaceae Serjania sp. 4 Leaf Lenticular Brown Yes Aquidauana/Cerrado 173
Sapotaceae Chrysophyllum marginatum (Hook. & Arn.) Radlk. Leaf Lenticular Green No Bodoquena/Atlantic Forest 174
Sapotaceae Pouteria torta (Mart.) Radlk. Leaf Cylindrical Green Yes Aquidauana/Cerrado 175
Smilacaceae Smilax polyantha Griseb. Leaf Amorphous Green No Aquidauana/Cerrado 176
Smilacaceae Smilax sp. 1 Leaf Lenticular Brown No Bodoquena/Atlantic Forest 177
Smilacaceae Smilax sp. 2 Leaf Lenticular Brown No Corumbá/Pantanal 178
Solanaceae Cestrum strigilatum Ruiz & Pav. Leaf Lenticular White No Bodoquena/Atlantic Forest 179
Solanaceae Cestrum sp. Leaf Globoid Brown No Aquidauana/Cerrado 180
Solanaceae Solanum paniculatum L. Leaf Globoid Yellow Yes Bodoquena/Atlantic Forest 181
Solanaceae Solanaceae sp. 1 Leaf Lenticular Brown No Corumbá/Pantanal 182
Solanaceae Solanaceae sp. 2 Leaf Lenticular Green No Bodoquena/Atlantic Forest 183
Vochysiaceae Qualea grandiflora Mart. Leaf Lenticular Green No Aquidauana/Cerrado 184
Vochysiaceae Qualea multiflora Mart. Leaf Globoid Green No Aquidauana/Cerrado 185

Figs. 2-25.  Insect galls of Mato Grosso do Sul in host plants indicated. 2. Annona emarginata; 3 and 4. Duguetia furfuracea; 5. Annonaceae sp.; 6. Aspidosperma cylindrocarpon; 7 and 8. Aspidosperma olivaceum; 9. Aspidosperma subincanum; 10-13. Forsteronia rufa; 14. Forsteronia velloziana; 15. Asteraceae sp. 1; 16. Asteraceae sp. 2; 17. Mikania sp.; 18. Vernonia polyanthes; 19-22. Vernonanthura brasiliana; 23. Adenocalymma bracteatum; 24 and 25. Fridericia chica

Figs. 26-49.  Insect galls of Mato Grosso do Sul in host plants indicated. 26-29. Fridericia chica; 31. Fridericia caudigera; 32. Handroanthus chrysotrichus; 33 and 34. Handroanthus ochraceus; 35 and 36. Handroanthus heptaphyllus; 37. Tabebuia roseoalba; 38. Tanaecium pyramidatum; 39. Bignoniaceae sp.; 40. Protium heptaphyllum; 41 and 42. Celtis spinosa; 43. Caryocar brasiliense; 44. Terminalia argentea; 45. Terminalia cf. fagifolia; 46. Connarus cf. suberosus; 47. Connarus cf. suberosus; 48. Ipomoea alba; 49. Davilla elliptica

Figs. 50-73.  Insect galls of Mato Grosso do Sul in host plants indicated. 50. Erythroxylum suberosum; 51. Manihot tripartite; 52. Croton floribundus; 53. Croton sp. 1; 54 and 55; Croton sp. 2; 56. Sapium glandulosum; 57. Anadenanthera peregrina var. falcate; 58. Bauhinia mollis; 59. Bauhinia holophylla; 60 and 61. Bauhinia holophylla; 62. Bauhinia longifolia; 63-65. Bauhinia ungulate; 66 and 67. Copaifera langsdorffii; 68 and 69. Dipteryx alata; 70. Fabaceae sp.; 71. Galactia striata; 72 and 73. Guibourtia hymenaeifolia

Figs. 74-97.  Insect galls of Mato Grosso do Sul in host plants indicated. 74. Guibourtia hymenaeifolia; 75-78. Hymenaea stigonocarpa; 79-82. Inga vera; 83. Machaerium amplum; 84. Mimosa sp. 1; 85 and 86. Mimosa sp. 2; 87. Mimosa sp. 3; 88 and 89. Peltogyne confertiflora; 90. Senna velutina; 91. Hyptis brevipes; 92. Hyptis sp.; 93. Lauraceae sp.; 94. Persea sp.; 95. Strychnos parvifolia; 96 and 97. Amorimia pubiflora

Figs. 98-121.  Insect galls of Mato Grosso do Sul in host plants indicated. 99. Amorimia pubiflora; 99. Byrsonima crassifolia; 100. Bunchosia paraguariensis; 101. Mascagnia cordifolia; 102. Mascagania sepium; 103. Malpighiaceae sp.; 104. Luehea divaricata; 105. Malvaceae sp.; 106. Byttneria dentata; 107. Waltheria indica; 108. Melastomataceae sp.; 109. Guarea guidonia; 110. Cissampelos pareira; 111. Brosimum gaudichaudii; 112. Campomanesia pubescens; 113. Eugenia bimarginata; 114-119. Eugenia florida; 120 and 121. Eugenia punicifolia

Figs. 122-145.  Insect galls of Mato Grosso do Sul in host plants indicated. 122 and 123. Eugenia punicifolia; 124 and 125. Myrcia sp.; 126. Psidium guajava; 127. Ludwigia longifolia; 128. Piper sp.; 129. Roupala montana; 130. Bathysa sp.; 131. Guettarda pohliana; 132-136. Psychotria carthagenensis; 137 and 138. Randia armata; 139. Rubiaceae sp. 1; 140. Rubiaceae sp. 2; 141-143. Zanthoxylum sp.; 144. Zanthoxylum riedelianum; 145. Casearia sp. 

Figs. 146-169.  Insect galls of Mato Grosso do Sul in host plants indicated. 146. Casearia gossypiosperma; 147-149. Casearia sylvestris; 150. Xylosma sp.; 151-153. Magonia pubescens; 154. Matayba guianensis; 155 and 156. Serjania cf. caracasana; 157 and 158. Serjania cf. crassifolia; 159-165. Serjania cf. glabrata; 166. Serjania sp. 1; 167-169. Serjania sp. 2. 

Figs. 170-185.  Insect galls of Mato Grosso do Sul in host plants indicated. 170 and 171. Serjania sp. 3; 172 and 173. Serjania sp. 4; 174. Chrysophyllum marginatum; 175. Pouteria torta; 176. Smilax polyantha; 177. Smilax sp. 1; 178. Smilax sp. 2; 179. Cestrum strigilatum; 180. Cestrum sp.; 181. Solanum paniculatum; 182. Solanaceae sp. 1; 183. Solanaceae sp. 2; 184. Qualea grandiflora; 185. Qualea multiflora

Table 3 Richness of insect galls in several localities of biomes of Atlantic Forest, Cerrado, Seasonally Tropical Dry Forests (STDF), and Dry Tropical Forests (DTF) of Brazil. 

Locality Number of gall morphotypes Number galled plant families Number galled plant genera Number galled plant species Average number of gall/host plant species Biome
Mato Grosso do Sul (this study) 186 35 73 115 1.6 Cerrado, Atlantic Forest, Pantanal, Chaco
Pantanal do Abobral, MS (Julião et al., 2002) 133 37 60 75 1.7 Pantanal
Goiânia, GO (Araújo et al., 2014) 97 24 37 55 1.8 Cerrado
Estação Ecológica do Jataí, Luiz Antônio, SP (Saito and Urso-Guimarães, 2012) 69 24 35 41 1.7 Cerrado
Parque Estadual de Vaçununga, Santa Rita do Passa Quatro, SP (Urso-Guimarães and Scarelli-Santos, 2006) 35 16 24 25 1.4 Cerrado
Delfinópolis, MG (Urso-Guimarães et al., 2003) 22 16 19 19 1.2 Cerrado, rupestrian fields (STDF), riparian forest
Reserva Biológica Boqueirão, Ingaí, MG (Malves and Frieiro-Costa, 2012) 36 14 18 26 1.4 Cerrado, rupestrian fields (STDF), riparian forest
Serra de São José, Tiradentes, MG (Maia and Fernandes, 2004) 137 47 30 73 1.8 Cerrado, rupestrian fields (STDF)
Serra do Cipó, MG (Coelho et al., 2009) 92 19 37 51 1.8 Rupestrian fields (STDF)
Cadeia do Espinhaço, MG (Carneiro et al., 2009b) 241 29 78 142 1.6 Rupestrian fields (STDF)
Serra do Caitité, BA (Nogueira et al., 2016) 49 13 18 27 1.8 Cerrado, Caatinga (TDF)
Pernambuco (Santos et al., 2011) 64 17 31 48 1.3 Caatinga (TDF)
Serra do Cabral, MG (Coelho et al., 2013) 47 21 32 39 1.2 Cerrado, rupestrian fields (STDF)

In our survey, the richest plant families in terms of gall morphotypes were Fabaceae (N = 34), Sapindaceae (N = 24), Bignoniaceae (N = 17), and Myrtaceae (N = 15), corroborating the hypothesis that families with the highest number of plant species also have the highest number of gall-forming species ( Fernandes, 1992 ; Mendonça, 2007). As previously stated, local gall-forming species richness is closely related to the diversity of plant species (Butterill and Novotný, 2015). Fabaceae and Myrtaceae are among the ten most diversified families in Brasil (BFG, 2015) and studies of plant diversity in several vegetation types in Mato Grosso do Sul pointed out Fabaceae as the most species-rich family ( Pott and Pott, 1999; Damasceno et al., 2005 ; Frison, 2007). The same applies to the Cerrado (Mendonça et al., 2008), the Atlantic Forest (Baptista-Maria et al., 2009), in forest patches of the Pantanal (Frison, 2007), and the Chaco (Freitas et al., 2013). Despite the different sampling effort, this average is closer to other studies in Cerrado, seasonally dry tropical forests, and dry tropical forests of Brazil (Table 3). Families and species with the highest number of morphotypes for Mato Grosso do Sul are presented in Table 4, which also contain the results for each biome in this study and the Julião et al. (2002) results. Although our aim was not to verify the hygrothermal hypothesis, the collections were conducted in biomes with marked differences in humidity. When the results of different biomes of MS were compared, we did not find increased gall richness in low-humidity environments as stated by Price et al. (1998), Fernandes and Price (1991), Julião et al. (2014) (Table 4), reinforcing the richness hypothesis to the MS environments ( Fernandes, 1992 ; Mendonça, 2007).

Table 4 Richness of insect galls per biomes in Mato Grosso do Sul. 

Locality/Biome Richest plant families Super host genera Super host species Total of galls
Mato Grosso do Sul (this study) Fabaceae (34) Sapindaceae (24) Bignoniaceae (17) Myrtaceae (15) Serjania (20) Eugenia (11) Bauhinia (8) Fridericia (8) Fridericia chica (7) Serjania cf. glabrata (7) Eugenia florida (6) 186
Aquidauana/Cerrado (this study) Fabaceae (20) Sapindaceae (8) Myrtaceae (7) Serjania (6) Bauhinia (4) Eugenia (4) Hymenaea (4) Hymenaea stigonocarpa (4) Guibourtia hymenaeifolia (3) 68
Atlantic Forest (this study) Bignoniaceae (9) Asteraceae (8) Rubiaceae (8) Fridericia (8) Casearia (5) Serjania (5) Fridericia chica (7) Serjania cf. glabrata (5) 65
Corumbá/Pantanal (this study) Sapindaceae (9) Apocynaceae (3) Serjania (9) Serjania sp. 7 (4) 32
Porto Murtinho/Chaco (this study) Fabaceae (9) Bauhinia (4) Mimosa (3) Bauhinia ungulata (2) Eugenia punicifolia (2) Forsteronia rufa (2) Magonia pubescens (2) Mimosa sp. 3 (2) 21
Pantanal do Abobral/Pantanal (Julião et al., 2002) Bignoniaceae (18) Fabaceae (13) Sapindaceae (11) Hippocrateaceae (7) Serjania (12) Hippocratea (6) Hippocratea volubilis (6) Inga vera (5) 133

The plant genera with the highest gall diversity in all biomes were Serjania Mill. (N = 20, Sapindaceae), Eugenia L. (N = 11, Myrtaceae), Bauhinia L. (N = 8, Fabaceae), and Fridericia Mart. (N = 8, Bignoniaceae). The composition of plant species, genera and families also highlights the specificities of each biome. Despite Fabaceae, Sapindaceae, Bignoniaceae, and Myrtaceae being the richest families in all biomes of MS ( Pott and Pott, 1999; Damasceno et al., 2005 ; Frison, 2007), in the Atlantic Forest the richest families also included Asteraceae and Rubiaceae; and Apocynaceae in Pantanal and Chaco.

Serjania, with 20 morphotypes in MS, was recorded with 12 galls in Pantanal (Julião et al., 2002), and six gall morphotypes in rocky areas of Serra do Cipó, MG (Coelho et al., 2009). Eugenia, recorded with 11 morphotypes in MS, is most commonly found in restinga with 12 morphotypes (Maia et al., 2014). Bauhinia, with eight morphotypes in MS, appeared with ten galls in Serra do Cipó, MG ( Coelho et al., 2009), three galls in the Cerrado of Santa Rita do Passa Quatro, SP (Urso-Guimarães and Scarelli-Santos, 2006), two in the Cerrado of Delfinópolis, MG (Urso-Guimarães et al., 2003) and two in the Caatinga of Pernambuco (Santos et al., 2011). The same occurs with Fridericia, with eight morphotypes in MS, also found in restinga with seven morphotypes ( Maia et al., 2014). In addition, no survey of the Cerrado or Atlantic Forest presented Eugenia or Fridericia as superhost species before ( Table 5).

Table 5 Richness of gall morphotypes in host plants in several localities of dry vegetation of Brazil. STDF, Seasonally Tropical Dry Forest; TDF, Tropical Dry Forest. 

Locality Biomes Richest families Richest genera (superhosts) Richest species (superhosts)
Mato Grosso do Sul (this study) Cerrado, Atlantic Forest, Pantanal, Chaco Fabaceae (34) Sapindaceae (24) Bignoniaceae (17) Myrtaceae (15) Serjania (20) Eugenia (11) Bauhinia (8) Fridericia (8) Fridericia chica (7) Serjania cf. glabrata (7) Eugenia florida (6)
Pantanal do Abobral, MS (Julião et al., 2002) Pantanal Bignoniaceae (18) Fabaceae (13) Sapindaceae (11) Hyppocrateaceae (7) Serjania (12) Hippocratea (6) Hippocratea volubilis (6) Inga vera (5)
Goiânia, GO (Araújo et al., 2014) Cerrado Myrtaceae (17) Fabaceae (14) Myrcia (10) Qualea (10) Andira cujabensis (4) Myrcia guianensis (4)
Estação Ecológica do Jataí, Luiz Antônio, SP (Saito and Urso-Guimarães, 2012) Cerrado Annonaceae (10) Malpighiaceae (9) Fabaceae (6) Byrsonima (6) Duguetia (5) Byrsonima cf. intermedia (6) Duguetia furfuracea (5)
Parque Estadual de Vaçununga, Santa Rita do Passa Quatro, SP (Urso-Guimarães and Scarelli-Santos, 2006) Cerrado Myrtaceae (5) Fabaceae (5) Myrcia (4) Bauhinia (3) Myrcia bella (3) Bauhinia rufa (3)
Delfinópolis, MG (Urso-Guimarães et al., 2003) Cerrado, rupestrian fields (STDF), riparian forest Fabaceae (5) Bauhinia (2) Chomelia (2) Qualea (2) Bauhinia ungulata (2) Chomelia pohliana (2) Qualea parviflora (2)
Reserva Biológica Boqueirão, Ingaí, MG (Malves and Frieiro-Costa, 2012) Cerrado, rupestrian fields (STDF), riparian forest Asteraceae (6) Myrtaceae (5) Melastomataceae (3) Miconia (5) Eugenia (5) Croton sp. (4)
Serra de São José, Tiradentes, MG (Maia and Fernandes, 2004) Cerrado, rupestrian fields (STDF) Fabaceae (20) Myrtaceae (18) Asteraceae (16) Melastomataceae (14) Protium (7) Baccharis (6) Copaifera (6) Myrcia (6) Protium heptaphyllum (7) Copaifera langsdorffii (6) Myrcia sp. (6) Croton floribundus (5) Miconia theaezans (5)
Serra do Cipó, MG (Coelho et al., 2009) Rupestrian fields (STDF) Fabaceae (22) Myrtaceae (11) Asteraceae (8) Bauhinia (10) Myrcia (7) Baccharis (6) Celtis (6) Serjania (6) Baccharis dracunculifolia (5) Celtis brasiliensis (5)
Cadeia do Espinhaço, MG (Carneiro et al., 2009b) Rupestrian fields (STDF) Asteraceae (39) Melastomataceae (26) Malpighiaceae (22) Fabaceae (21) Baccharis (92) Byrsonima (17) Microlicia (10) Lessingianthus (10) Lychnophora (10) Baccharis pseudomyriocephala (10) Byrsonima coccolobifolia (8)
Serra do Caitité, BA (Nogueira et al., 2016) Cerrado, Caatinga (TDF) Fabaceae (22) Malpighiaceae (10) Copaifera (10) Bauhinia (6) Mimosa (4) Copaifera langsdorffii (9) Bauhinia acuruana (5)
Pernambuco (Santos et al., 2011) Caatinga (TDF) Fabaceae (15) Euphorbiaceae (9) Boraginaceae (4) Malpighiaceae (4) Myrtaceae (4) Croton (4) Cnidoscolus (3) Bauhinia (2) Byrsonima (2) Bauhinia cheilantha (4)
Serra do Cabral, MG (Coelho et al., 2013) Cerrado, rupestrian fields (STDF) Asteraceae (70) Malpighiaceae (17) Fabaceae (17) Byrsonima (27) Lessingianthus (17) Byrsonima guilleminiana (3)

The highest gall richness on plant species in MS were found in Fridericia chica (Bonpl.) L.G.Lohmann (N = 7, Bignoniaceae), Serjania cf. glabrata Kunth (N = 7, Sapindaceae), and Eugenia florida DC. (N = 6, Myrtaceae). There were no reports of Fridericia chica as superhost in the literature. Eugenia florida was recorded in studies in Southern Brazil ( Mendonça et al., 2014) and Serjania glabrata in one leaf gall from Pernambuco ( Santos et al., 2011).

In specific biomes the results were slightly different. The families and species with more morphotypes in Cerrado are Fabaceae and Hymenaea stigonocarpa Mart. ex Hayne, in Atlantic Forest are Bignoniaceae and Friedericia chica, in Pantanal are Sapindaceae and Serjania sp. 7, and in Chaco, Fabaceae and Bauhinia ungulata L. are the richest, followed by Eugenia punicifolia (Kunth) DC., Forsteronia rufa Müll.Arg., Magonia pubescens A.St.-Hil., and Mimosa sp. (details in Table 4).

Another pattern recovered in our results is the organ more frequent to gall occurrence: leaves (Mani, 1964). Eighty-five percent of galls occurred in leaves, leaflets or leaf veins, 14% in stems, and the other 2% in tendrils and inflorescences. Galls on fruits or aerial roots were not found. Only one morphotype occurred simultaneously in two plant organs: stem and leaf. The most common morphotypes of galls were lenticular (35%), corroborating the pattern found by Fernandes and Negreiros (2006), Bregonci et al. (2010), Santos et al. (2011), Saito and Urso-Guimarães (2012), followed by globoid (30%), and fusiform (17%); 80% of the galls were glabrous, corroborating the findings of Urso-Guimarães et al. (2003), which refuted the idea of trichomes as a defense against immature gall-makers (Table 6).

Table 6 Description of predominant gall morphotypes recorded in the Mato Grosso do Sul (Brazil) and in each biome. 

Locality/Biome Number of morphotypes Organ more afected Shape more frequent Pubescence Predominant color of galls
Mato Grosso do Sul 186 Leaf (85%) Lenticular (35%), globoid (30%), fusiform (17%) 20% Green (47%)
Aquidauana/Cerrado 68 Leaf (93%) Lenticular (38%), globoid (30%), fusiform (12%) 35% Green (48%)
Bodoquena/Atlantic Forest 65 Leaf (77%) Lenticular (37%), globoid (30%), fusiform (18.5%) 11% Green (46%)
Corumbá/Pantanal 32 Leaf (94%) Lenticular (41%), globoid (28%), fusiform (9%) 16% Green (44%)
Porto Murtinho/Chaco 21 Leaf (71%) Fusiform (43%), globoid (33%), lenticular (13%) 9.5% Green (52%)

In the biomes, the numbers were slightly different (Table 6). Leaf remains as the most frequent organ attacked by galls, but the percentages ranged from 71% to 93%. Lenticular gall shape was the most common in Pantanal (41%), Cerrado (38%), and Atlantic Forest (38%), but not in Chaco, where the shape most commonly found was fusiform (43%). Chaco is a very dry biome, and the fusiform and globoid shapes are often the swelling of plant tissue, resulting in galls with thicker walls. In our opinion, those swollen galls are the less susceptible to desiccation of immatures than any other gall shape, which can explain the high number of them in a dry environment. The absence of trichomes in galls predominated in all vegetation types, with presence ranging only between 9.5% and 35%.

We obtained and identified the inducers of 50 morphotypes of galls in 38 host plants (20%), 78% of which belongs to Diptera (Cecidomyiidae), 10% to Hymenoptera, and the other 12% are divided among Hemiptera, Thysanoptera, Coleoptera, and Lepidoptera (Table 7). The gall makers of 136 morphotypes could not be determined, because gall samples were collected empty, old, or senescent.

Table 7 Gall makers and associated fauna in galls of Mato Grosso do Sul biomes. 

Associated fauna Number of morphotypes obtained Percentual
Diptera 39 78%
Hymenoptera 5 10%
Hemiptera 2 4%
Thysanoptera 2 4%
Coleoptera 1 2%
Lepidoptera 1 2%

The Cecidomyiidae was the dominant family in Diptera. We identified five species of Cecidomyiidae present in galls, the gall makers Contarinia sp. And Youngomyia pouteriaeMaia, 2004, and the inquilines Trotteria quadridentataMaia, 2004, Camptoneuromyia sp 1, and Camptoneuromyia sp 2. The hymenopterans obtained were from four morphotypes, Mononeuron duguetiae Fischer, 1981 (Braconidae), associated with leaf galls of Duguetia furfuracea (A.St.-Hil.) Saff., and three parasitoid species from the Chalcidoidea superfamily. Additional information about associated fauna is presented in Table 8.

Table 8 Insect fauna obtained in the galls sampled in the Mato Grosso do Sul environments and their habits. Figures refer to gall morphotype's image. 

Host family Host species Insects Habit Figure
Annonaceae Annona emarginata Diptera (Phoridae, adult) inquiline 2
Annonaceae Duguetia furfuracea Hymenoptera (Braconidae, Doryctinae, adult) parasitoid 3
Annonaceae Duguetia furfuracea Diptera (Cecidomyiidae, Cecidomyiidi, larva) gall maker 4
Asteraceae Asteraceae sp.2 Thysanoptera (adult) gall maker 16
Bignoniaceae Fridericia chica Diptera (Cecidomyiidae, Cecidomyiinae, larva) gall maker 28
Bignoniaceae Fridericia chica Diptera (Cecidomyiidae, Cecidomyiinae, larva) gall maker 28
Bignoniaceae Handroanthus cf. ochraceus Diptera (Cecidomyiidae, Cecidomyiinae, larva) gall maker 33
Cannabaceae Celtis spinosa Diptera (Cecidomyiidae, Cecidomyiinae, larva) gall maker 41
Cannabaceae Celtis spinosa Lepidoptera (exuvia, adult) inquiline 42
Caryocaraceae Caryocar brasiliense Hemiptera (Diaspididae, adult) gall maker 43
Combretaceae Terminalia cf. fagifolia Diptera (Cecidomyiidae, Cecidomyiinae, larva) gall maker 45
Convolvulaceae Ipomoea alba Diptera (Cecidomyiidae, Cecidomyiinae, larva) gall maker 48
Dilleniaceae Davilla elliptica Diptera (Cecidomyiidae, Cecidomyiinae, larva) gall maker 49
Erythroxylaceae Erythroxylum suberosum Diptera (Cecidomyiidae, Cecidomyiinae, larva) gall maker 50
Euphorbiaceae Manihot tripartita Diptera (Cecidomyiidae, Cecidomyiinae, larva) gall maker 51
Euphorbiaceae Manihot tripartita Diptera (Cecidomyiidae, Camptoneuromyia, adult) inquiline 51
Euphorbiaceae Croton floribundus Diptera (Cecidomyiidae, Cecidomyiinae, larva) gall maker 52
Euphorbiaceae Croton floribundus Hymenoptera (Chalcidoidea, adult) parasitoid 52
Fabaceae Guibourtia hymenaeifolia Diptera (Cecidomyiidae, Cecidomyiinae, larva) gall maker 72
Fabaceae Guibourtia hymenaeifolia Diptera (Cecidomyiidae, Cecidomyiinae, larva) gall maker 74
Fabaceae Hymenaea stigonocarpa Hymenoptera (Chalcidoidea, adult) inquiline 75
Fabaceae Inga vera Diptera (Cecidomyiidae, Cecidomyiinae, larva) gall maker 79
Fabaceae Inga vera Diptera (Cecidomyiidae, Cecidomyiinae, larva) gall maker 80
Fabaceae Inga vera Diptera (Cecidomyiidae, Cecidomyiinae, larva) gall maker 81
Fabaceae Inga vera Coleoptera (larva) inquiline 81
Fabaceae Inga vera Diptera (Cecidomyiidae, Cecidomyiinae, larva) gall maker 82
Fabaceae Inga vera Diptera (Cecidomyiidae, Camptoneuromyia, larva, exuvia, adult) inquiline 82
Fabaceae Inga vera Diptera (Cecidomyiidae, Cecidomyiinae, larva) gall maker 82
Fabaceae Mimosa sp.2 Diptera (Cecidomyiidae, Cecidomyiinae, larva) gall maker 85
Fabaceae Mimosa sp.3 Diptera (Cecidomyiidae, Cecidomyiinae, larva) gall maker 87
Lamiaceae Hyptis brevipes Hymenoptera (Chalcidoidea, adult) parasitoid 91
Loganiaceae Strychnos parvifolia Diptera (Cecidomyiidae, Contarinia, larva) gall maker 95
Malpighiaceae Amorimia pubiflora Diptera (Cecidomyiidae, Cecidomyiinae, larva) gall maker 96
Malpighiaceae Amorimia pubiflora Diptera (Cecidomyiidae, Cecidomyiinae, larva) gall maker 97
Malpighiaceae Amorimia pubiflora Diptera (Cecidomyiidae, Cecidomyiinae, larva) gall maker 98
Malpighiaceae Amorimia pubiflora Diptera (Cecidomyiidae, Cecidomyiinae, larva) inquiline 98
Malpighiaceae Mascagnia cordifolia Diptera (Cecidomyiidae, Cecidomyiinae, larva) gall maker 101
Malpighiaceae Mascagnia cordifolia Diptera (Cecidomyiidae, Cecidomyiinae, larva) inquiline 101
Malvaceae Waltheria indica Diptera (Cecidomyiidae, Cecidomyiinae, larva) gall maker 107
Meliaceae Guarea guidonia Diptera (Cecidomyiidae, Cecidomyiinae, larva) gall maker 109
Myrtaceae Psidium guajava Thysanoptera (adult) gall maker 126
Sapindaceae Magonia pubescens Hymenoptera (Chalcidoidea, adult) parasitoid 151
Sapindaceae Serjania cf. glabrata Diptera (Cecidomyiidae, Cecidomyiinae, larva) gall maker 160
Sapotaceae Pouteria torta Cecidomyiidae (Youngomyia pouteriae, larva) gall maker 175
Sapotaceae Pouteria torta Cecidomyiidae (Trotteria quadridentata, pupa, adult) inquiline 175
Solanaceae Cestrum sp. Diptera (Cecidomyiidae, Cecidomyiinae, larva) gall maker 180
Solanaceae Cestrum sp. Hemiptera (Physilidae, nymph) inquiline 180
Solanaceae Solanum paniculatum Diptera (Cecidomyiidae, Cecidomyiinae, larva) gall maker 181
Solanaceae Solanaceae sp.2 Diptera (Cecidomyiidae, Cecidomyiinae, larva) gall maker 183
Vochysiaceae Qualea grandiflora Diptera (Cecidomyiidae, Cecidomyiinae, larva) gall maker 184

The geographic distribution of gall morphotypes associated with the cecidomyiids Youngomyia pouteriae and Trotteria quadridentata, and the wasp Mononeuron duguetiae were expanded to the localities sampled in Mato Grosso do Sul. In MS, the host plant of Youngomyia pouteriae is Pouteria torta, as opposed to the originally described host plant (Pouteria caimito) in the restinga.

All occurrences of Cecidomyiidae in Mato Grosso do Sul localities are new records. We identified four new records of host plant genera: Byttneria, Galactia, Guibourtia, Tanaecium; and 24 new records of host plant species: Adenocalymma bracteatum, Annona emarginata, Aspidosperma olivaceum, Aspidosperma subincanum, Bauhinia mollis, Brosimum gaudichaudii, Byttneria dentata, Casearia gossypiosperma, Celtis spinosa, Cestrum strigilatum, Forsteronia rufa, Forsteronia velloziana, Galactia striata, Guettarda pohliana, Guibourtia hymenaeifolia, Hymenaea martiana, Ipomoea alba, Mascagnia cordifolia, Peltogyne confertiflora, Smilax polyantha, Solanum paniculatum, Strychnos parvifolia, Tanaecium pyramidatum and Zanthoxylum riedelianum.

Our most relevant findings include the survey of 186 gall morphotypes in MS; leaves remain as the organ most frequently attacked by galls, and the most common gall shape was lenticular in Pantanal (41%), Cerrado (38%), and Atlantic Forest (38%), and fusiform (43%) in Chaco. The galls were found in 115 plant species, with host families and species richness varying according to the biome: Cerrado - Fabaceae and Hymenaea stigonocarpa; Atlantic Forest: Bignoniaceae and Friedericia chica; Pantanal: Sapindaceae and Serjania sp. 7; and Chaco: Fabaceae and Bauhinia ungulata. Although we did not aim to verify the hygrothermal hypothesis, our surveys were conducted in biomes with marked differences in humidity. As supplementary information, when different biomes of MS were compared, we did not find an increase in gall richness in low-humidity environments as stated by Price et al. (1998), Fernandes and Price (1991), Julião et al. (2014) (Table 4), reinforcing the richness hypothesis ( Fernandes, 1992 ; Mendonça, 2007). In addition, we presented four new records of host plant genera, with Eugenia and Fridericia described as superhost species for the first time. The gall makers are mostly represented by Diptera, mainly Cecidomyiidae species recorded for the first time in Mato Grosso do Sul. We also found that Youngomyia pouteriae is no longer a monophagous species, since we found this gall-maker in Pouteria torta rather than in the originally described host plant (Pouteria caimito).

Acknowledgements

The MVUG thanks the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Proc. No. 563256/2010-9) and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (Proc. No. 2010/52314-0) for the support to the SISBIOTA - Diptera Brasil Program. The authors thank J. Semir (IB/UNICAMP), G.H. Shimizu (IB/UNICAMP) and R.B. Pinto (IB/UNICAMP) for invaluable help in plant species identification.

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Received: May 13, 2016; Revised: August 19, 2016; Accepted: September 04, 2016

* Corresponding author. E-mail: virginia@ufscar.br (M.V. Urso-Guimarães).

Conflicts of interest The authors declare no conflicts of interest.

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