Revista Brasileira de Entomologia Revista Brasileira de Entomologia
Rev Bras Entomol 2017;61:25-42 - Vol. 61 Núm.1 DOI: 10.1016/j.rbe.2016.08.002
Biology, Ecology and Diversity
Characterization of entomogen galls from Mato Grosso do Sul, Brazil
Maria Virginia Urso-Guimarãesa,, , Ana Carolina Devides Castellob, Eric Yasuo Kataokaa, Ingrid Kochc
a Universidade Federal de São Carlos, Departamento de Biologia, Sorocaba, SP, Brazil
b Universidade Estadual de São Paulo, Programa de Pós Graduação em Ciências Biológicas (Botânica), Botucatu, SP, Brazil
c Universidade de Campinas, Departamento de Biologia Vegetal, Campinas, SP, Brazil
Recebido 13 Maio 2016, Aceitaram 19 Agosto 2016
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, 1917, 1918, 1920, 1922, 1925), Houard (1933), and Occhioni (1979, 1981), some biomes remain poorly sampled, such as the Pantanal, Caatinga and the Amazonian forest (Julião et al., 2002, 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 methodsStudy areas

Mato Grosso do Sul State has an approximate area of 358km2, 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 200m to 700m (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 1500mm (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.
(0.26MB).

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
Cerrado  Aquidauana/Distrito de Camisão  S 20° 26′ 58.1″,
W 055° 38′ 16.9″ 
300
Atlantic Forest  Bodoquena/Sede Fazenda Califórnia  S 20° 42′ 18.9″,
W 56° 51′ 17.4″ 
320
Atlantic Forest  Bodoquena/Trilha da Gruta  S 20° 41′ 55.9″,
W 56° 52′ 49.4″ 
517
Pantanal  Corumbá/Base de Estudos do Pantanal  S 19° 34′ 20.09″,
W 057° 00′ 57.09″ 
400
Pantanal  Corumbá/Fazenda São Bento  S 19° 28′ 09.1″,
W 057° 01′ 49.9″ 
110
Chaco  Porto Murtinho/Trilha Fazenda Retiro Conceição  S 21° 41′ 07.6″,
W 57° 45′ 09.0″ 
662
Chaco  Porto Murtinho/Trilha Fazenda Campo Florido  S 21° 38′ 18.3″,
W 57° 42′ 22.7″ 
550

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. 2–185) 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 
Annonaceae  Duguetia furfuracea (A.St.-Hil.) Saff.  Leaf  Globoid  Yellow  Yes  Aquidauana/Cerrado 
Annonaceae  Duguetia furfuracea (A.St.-Hil.) Saff.  Leaf  Lenticular  Yellow  No  Aquidauana/Cerrado 
Annonaceae  Annonaceae sp.  Stem  Globoid  Green  No  Bodoquena/Atlantic Forest 
Apocynaceae  Aspidosperma cylindrocarpon Müll.Arg.  Leaf  Lenticular  Brown  No  Corumbá/Pantanal 
Apocynaceae  Aspidosperma olivaceum Müll.Arg.  Leaf  Globoid  Yellow  No  Bodoquena/Atlantic Forest 
Apocynaceae  Aspidosperma olivaceum Müll.Arg.  Leaf  Triangular  Green  No  Bodoquena/Atlantic Forest 
Apocynaceae  Aspidosperma subincanum Mart.  Leaf  Lenticular  Yellow  No  Bodoquena/Atlantic Forest 
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.
(0.93MB).

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.
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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.
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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.
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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.
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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.
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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.
(0.73MB).

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.
(0.55MB).

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., 2002133  37  60  75  1.7  Pantanal 
Goiânia, GO (Araújo et al., 201497  24  37  55  1.8  Cerrado 
Estação Ecológica do Jataí, Luiz Antônio, SP (Saito and Urso-Guimarães, 201269  24  35  41  1.7  Cerrado 
Parque Estadual de Vaçununga, Santa Rita do Passa Quatro, SP (Urso-Guimarães and Scarelli-Santos, 200635  16  24  25  1.4  Cerrado 
Delfinópolis, MG (Urso-Guimarães et al., 200322  16  19  19  1.2  Cerrado, rupestrian fields (STDF), riparian forest 
Reserva Biológica Boqueirão, Ingaí, MG (Malves and Frieiro-Costa, 201236  14  18  26  1.4  Cerrado, rupestrian fields (STDF), riparian forest 
Serra de São José, Tiradentes, MG (Maia and Fernandes, 2004137  47  30  73  1.8  Cerrado, rupestrian fields (STDF) 
Serra do Cipó, MG (Coelho et al., 200992  19  37  51  1.8  Rupestrian fields (STDF) 
Cadeia do Espinhaço, MG (Carneiro et al., 2009b241  29  78  142  1.6  Rupestrian fields (STDF) 
Serra do Caitité, BA (Nogueira et al., 201649  13  18  27  1.8  Cerrado, Caatinga (TDF) 
Pernambuco (Santos et al., 201164  17  31  48  1.3  Caatinga (TDF) 
Serra do Cabral, MG (Coelho et al., 201347  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., 2002Bignoniaceae (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., 2002Pantanal  Bignoniaceae (18)
Fabaceae (13)
Sapindaceae (11)
Hyppocrateaceae (7) 
Serjania (12)
Hippocratea (6) 
Hippocratea volubilis (6)
Inga vera (5) 
Goiânia, GO (Araújo et al., 2014Cerrado  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, 2012Cerrado  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, 2006Cerrado  Myrtaceae (5)
Fabaceae (5) 
Myrcia (4)
Bauhinia (3) 
Myrcia bella (3)
Bauhinia rufa (3) 
Delfinópolis, MG (Urso-Guimarães et al., 2003Cerrado, 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, 2012Cerrado, 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, 2004Cerrado, 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., 2009Rupestrian 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., 2009bRupestrian 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., 2016Cerrado, Caatinga (TDF)  Fabaceae (22)
Malpighiaceae (10) 
Copaifera (10)
Bauhinia (6)
Mimosa (4) 
Copaifera langsdorffii (9)
Bauhinia acuruana (5) 
Pernambuco (Santos et al., 2011Caatinga (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., 2013Cerrado, 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  10% 
Hemiptera  4% 
Thysanoptera  4% 
Coleoptera  2% 
Lepidoptera  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 pouteriae Maia, 2004, and the inquilines Trotteria quadridentata Maia, 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 
Annonaceae  Duguetia furfuracea  Hymenoptera (Braconidae, Doryctinae, adult)  parasitoid 
Annonaceae  Duguetia furfuracea  Diptera (Cecidomyiidae, Cecidomyiidi, larva)  gall maker 
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).

Conflicts of interest

The authors declare no conflicts of interest.

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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Copyright © 2016. Sociedade Brasileira de Entomologia
Rev Bras Entomol 2017;61:25-42 - Vol. 61 Núm.1 DOI: 10.1016/j.rbe.2016.08.002