Characterization of entomogen galls from Mato Grosso do Sul, 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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Publication Dates

• Publication in this collection
  Jan-Mar 2017

History

• Received
  13 May 2016
• Reviewed
  19 Aug 2016
• Accepted
  04 Sept 2016