Diversity of insect galls from Mato Grosso State, Brazil: Cerrado

Diversidade de galhas de insetos do Estado do Mato Grosso, Brasil: Cerrado

Abstract:

The Midwest region of Brazil possesses large areas dominated by the Cerrado that is poorly known concerning insect gall and their interactions. In this study, we inventory the gall morphology, host plants, and the gall makers from Parque Nacional da Chapada dos Guimarães, Mato Grosso State, in areas of natural vegetation from Cerrado, for the first time. Samplings occurred in two expeditions, July 2012 and January 2013. We characterized 295 morphotypes of insect galls in 140 host plant species, with 89 gall makers; the richest family in host plants was Fabaceae (16.7%), and the species was Protium heptaphyllum (Aubl.) Marchand (Burseraceae, 3.7%). Parque Nacional da Chapada dos Guimarães is the richest Brazilian cerrado area in gall morphotypes (295) and the second in average morphotypes/host plant species (2.1). Additionally, six genera and 38 species are new records as host plants; two of them, Bernardia similis Pax and K.Hoffm and Ormosia macrophylla Benth., are new occurrences for Mato Grosso State, and other two, Vochysia petraea Warm. and Talisia subalbens (Mart.) Radlk. are listed in the Red List of Threatened Species IUCN. This inventory data represents a testimony of insect-plant interactions in a Brazilian Cerrado area that was consumed by an unprecedented fire in the dry season of 2020.

Keywords:
Biodiversity; Brazilian savannah; gall makers; Neotropical region; insect-plant interaction

Resumo:

A região Centro-Oeste do Brasil possui grandes áreas dominadas pelo Cerrado nas quais insetos e suas interações são pouco conhecidos. Neste estudo, fizemos o inventário de galhas, plantas hospedeiras e galhadores do Parque Nacional da Chapada dos Guimarães, Mato Grosso, uma área de vegetação natural de Cerrado. As amostragens foram realizadas em duas expedições, em julho de 2012 e janeiro de 2013. Caracterizamos 295 morfotipos de galhas de insetos em 140 espécies de plantas hospedeiras; com identificação de 89 galhadores; a família de plantas com maior número de espécies hospedeiras de galhas foi Fabaceae (16,7%) e a espécie com maior número de galhas, Protium heptaphyllum (Aubl.) Marchand (Burseraceae, 3,7%). Esta é a área mais rica em morfotipos de galhas do cerrado brasileiro (295) e a segunda na média de morfotipos/espécie de planta hospedeira (2,1). Além disso, seis gêneros e 38 espécies são registros novos de ocorrência de plantas hospedeiras para galhas de insetos; duas delas, Bernardia similis Pax and K.Hoffm and Ormosia macrophylla Benth., são registros novos para o Estado do Mato Grosso e outras duas, Vochysia petraea Warm. and Talisia subalbens (Mart.) Radlk. estão listadas na Lista Vermelha de Espécies Ameaçadas IUCN. Os dados desse inventário representam um testemunho das interações inseto-planta para o Cerrado no Brasil, em uma área que foi consumida por um incêndio sem precedentes na estação seca de 2020.

Palavras-chave:
Biodiversidade; galhadores; interação inseto-planta; região Neotropical; savana brasileira

Introduction

Insect-plant interactions are among the most interesting subjects in science, and inventories of the association between host plants and insect gall makers are among the trend topics of studies in the scientific community dedicated to this theme in Brazil. In the last 30 years, more than 50 inventories focusing on insect galls were performed in all Brazilian biomes, with predominance in Atlantic Forest and Cerrado, with 23 and 22 inventories, respectively (Araújo et al. 2019).

The Cerrado from central Brazil harbors the most significant extent of savanna in the Neotropics (Bueno et al. 2018), and it is facing alarming record rates of deforestation (Russo et al. 2018), massively in the Southeast region (~60%), especially in the State of Minas Gerais (~33%). Depending on its geographic distribution, it is affected by innumerous environmental conditions, like soil fertility, water availability, and temperature. Regarding the composition of its phytophysiognomies, Cerrado is severely influenced by adjacent biomes (Bueno et al. 2018). The phytophysiognomies distributed in the states of Minas Gerais, São Paulo, Bahia, Piauí, Maranhão, and the eastern region of Tocantins and Goiás are influenced by the conditions of the Atlantic Forest and Caatinga biome. In contrast, the composition of the vegetation distributed in the States of Mato Grosso do Sul, Mato Grosso, western Goiás, and Tocantins are influenced by the environmental conditions of Amazon, Pantanal, and Chaco biomes. All these complexities make Cerrado the focus of many studies.

Although most of the inventories of the insect galls communities were done in the Cerrado environment, most were restricted to the States of Minas Gerais (41%), Goiás (28%), and Bahia (22%) (Cintra et al. 2020), portraying more the community of active researchers around the sampled areas than the representativeness of the areas in the Cerrado biome. The Midwest region of Brazil possess large areas dominated by the Cerrado, and it is poorly known concerning gall communities, since just about 15% of all studies on insect galls were done in this region (Araújo et al. 2019, Cintra et al. 2020), and none in areas located in the state of Mato Grosso.

Cintra et al. (2020) made an important compilation from insect galls communities sampled in 32 areas of the Cerrado Biome in Minas Gerais, Goiás, Bahia, São Paulo, and Mato Grosso do Sul States. The authorsregistered host plants of 505 species, 222 genera, and 67 families. Nine species threatened of extinction: Baccharis concinna G.M.Barroso (Asteraceae), Lychnophora ramosissima Gardner (Asteraceae), and Lychnophora tomentosa (Mart. ex DC.) Sch.Bip. (Asteraceae). In this study, we characterized gall morphology, identified host plants and the gall makers from Parque Nacional da Chapada dos Guimarães, Mato Grosso State, to contribute to the increase in the knowledge about host plant species and their gall morphotypes associated with gall-inducing insects in areas of natural vegetation from Cerrado. This inventory is the first record of insect-plant interactions in a region threatened by an unprecedented fire in the dry season of 2020 (Marengo et al. 2021). In this troubling scenario, our inventory represents a testimony of insect-plant interactions consumed by the fire and increases knowledge for the insect galls communities of Cerrado.

Material and Methods

1. Study site

The study was conducted during the expeditions of the “Rede Temática para Estudos de Diversidade, Sistemática e Limites Distribucionais de Diptera nos Estados do Mato Grosso, Mato Grosso do Sul e Rondônia (SISBIOTA-Diptera Brazil Program, Proc. Fapesp 10/52314-0; Proc. CNPq 563256/2010-9) in the Parque Nacional da Chapada dos Guimarães (PNCG), State of Mato Grosso, Brazil (Fig. 1), which is recognized internationally as a Biosphere Reserve.

Figure 1
A. Map of South America indicating the Mato Grosso State and Cerrado Biome extension in Brazil. B. Map of the main biomes of Mato Grosso State and the position of Parque Nacional da Chapada dos Guimarães in Mato Grosso State. C. Map of the sampling localities of Parque Nacional da Chapada dos Guimarães, Mato Grosso State, Brazil.

The PNCG is located in the Cerrado Biome. The climate is classified as Tropical Climate of Savana (Aw), with two well-defined seasons (hot and rainy in summer; dry and cold in winter). Two geological regions are found in the PNCG, the Cuiabana Depression, which altitude is 200 - 450 m and the Guimarães Plateau with altitudes 600 - 800 m (MMA, 2009). The sampling areas list, including the sampled phytophysiognomies (classified after Ribeiro & Walter 2008), are presented in Table 1.

Table 1
Sampling localities in Parque Nacional Chapada dos Guimarães - Mato Grosso State informing phytophysiognomy, geographical coordinates of the starting points and route length.

Localities	Phytophysiognomies	Geographical Coordinates	Route length
Vale do Rio Claro	Cerrado s.l.	15°19'37.1" S & 55°51'21.0" W	234 m
Cachoeira Véu da Noiva	Cerrado s.l.	15° 24' 33.6" S & 055° 49' 58.9" W	190 m
Cachoeira das Andorinhas	Cerrado s.l.	15° 24' 47.8" S & 055° 50' 34" W	174 m
Vale do Eco	Campo Cerrado	15° 20' 54.2" S & 055° 47' 59.9" W	149 m
Vale da Benção	Gallery forest	15° 26' 10" S & 055° 47' 23" W	47 m
Cidade de Pedra	Cerrado rupestre	15° 18' 00.4" S & 055° 50' 26.2" W	37.5 m

2. Sampling

We made the samples in two expeditions, in July 2012 and January 2013, with an effort of 30 minutes in each point in both, except for Cachoeira das Andorinhas sampled once in July 2012 and Vale do Rio Claro sampled once in January 2013, following Price et al. (1998). We sampled along the trails’ edges, and we measured each route’s length to dimension the sampled area following Urso-Guimarães et al. (2017). The total sampling effort in PNCH was 5 hours. Plant branches with galls were collected, labeled, stored in plastic bags and taken to the laboratory to document the galls’ morphotypes, following Araújo et al. (2021). We transferred part of the galls to plastic tubes for rearing the inducers. We identified gall makers and plant species using identification keys compared with type material, literature, and experts’ help. The voucher specimens were deposited in the Universidade Federal de São Carlos: plants in the Herbarium SORO and the insect material in the Laboratório de Sistemática de Diptera.

Results

We identified in the Parque Nacional da Chapada dos Guimarães 295 morphotypes of insect galls in 140 host plant species from 84 genera and 41 families (Table 2, Figs. 2-9). On average, we found 2.1 gall morphotypes per plant species (for comparisons with other inventories in Cerrado areas, see Table 3). Three host plants are identified only at a family level, and 11 are completely unidentified. The richest plant families in morphotypes of insect galls were Fabaceae (N=49, 16.7%), Bignoniaceae (N=16, 5.4%), Melastomataceae, and Myrtaceae (N=13, 4.4% each), Burseraceae, Malpighiaceae, and Vochysiaceae (N=12, 4.1% each). The richest plant genera in gall morphotypes were Andira Lam. (N=17; 5.8%), Myrcia DC., Davilla Vand. and Protium Burm.f. (N=11; 3.7%), and Protium heptaphyllum (Aubl.) Marchand (N=11, 3.7%), Qualea parviflora Mart (N=10, 3.4%), Davilla grandiflora A.St.-Hil. and Copaifera depilis Dwyer (N=8, 2.7% each) are the studied area’s super host species. The organ most affected were the leaves (N=250; 85%); the lenticular (N=104, 35.4%) and globoid gall shapes (N=96, 32.5%) were predominant, as the color green and its variations (N=129; 43.9%) and the glabrous galls (N=239; 81.3%).

Table 2
Characterization of insect galls recorded in Parque Nacional da Chapada dos Guimarães, MT, Brazil, by host plant. Figures refer to the picture of the gall morphotype.

Host plat family	Host plant species	Host plant organ	Gall shape	Gall color	Trichomes	Collection site	Phytophysiognomy	Figures
Anacardiaceae	Anacardium nannum A.St.-Hil.*	Leaf	Globoid	Green/Brown	No	Vale do Eco, Cidade de Pedra	Campo Cerrado, Cerrado rupestre	2a
Anacardiaceae	Tapirira guianensis Aubl.	Leaf	Globoid	Green	No	Vale do Eco, Cidade de Pedra	Campo Cerrado, Cerrado rupestre	2b
Annonaceae	Annona dioica A.St.-Hil.	Leaf	Lenticular	Green	No	Vale do Eco	Campo Cerrado	2c
Annonaceae	Annona tomentosa L.*	Leaf	Globoid	Green/red	No	Vale do Eco	Campo Cerrado	2d, 2e
Annonaceae	Duguetia flagellaris Huber*	Leaf	Globoid	Green/brown	No	Vale da Benção	Gallery forest	2f
Annonaceae	Duguetia flagellaris Huber*	Leaf	Globoid	Green	No	Vale da Benção	Gallery forest	2g
Annonaceae	Duguetia furfuracea (A.St.-Hil.) Saff.	Leaf	Globoid	Green/brown	No	Cachoeira Véu da Noiva	Cerrado s.l.	2h
Annonaceae	Duguetia furfuracea (A.St.-Hil.) Saff.	Leaf vein	Pocket shaped	Yellow	No	Vale do Eco	Campo Cerrado	2i
Annonaceae	Duguetia furfuracea (A.St.-Hil.) Saff.	Leaf	Cylindrical	Red	No	Vale do Eco	Campo Cerrado	2j
Annonaceae	Duguetia furfuracea (A.St.-Hil.) Saff.	Leaf	Globoid	Pink	No	Vale do Eco	Campo Cerrado	2k
Annonaceae	Guatteria ferruginea A.St.-Hil.*	Leaf	Lenticular	Black	No	Vale da Benção	Gallery forest	2l
Annonaceae	Guatteria ferruginea A.St.-Hil.*	Leaf	Globoid	Brown	No	Vale da Benção	Gallery forest	2m
Annonaceae	Unonopsis guatterioides (A.DC.) R.E.Fr.*	Leaf	Lenticular	Brown	No	Vale da Benção	Gallery forest	2n
Apocynaceae	Aspidosperma subincanum Mart.	Leaf	Lenticular	Green/grey	No	Vale do Eco	Campo Cerrado	2o
Apocynaceae	Aspidosperma tomentosum Mart.	Leaf	Globoid	Green	No	Cachoeira das Andorinhas	Cerrado s.l.	2p
Apocynaceae	Aspidosperma tomentosum Mart.	Leaf	Lenticular	Green/yellow	No	Cachoeira Véu da Noiva	Cerrado s.l.	2q
Apocynaceae	Aspidosperma verbascifolium Müll.Arg .*	Leaf	Lenticular	Green	No	Cachoeira Véu da Noiva	Cerrado s.l.	2r
Apocynaceae	Aspidosperma verbascifolium Müll.Arg .*	Leaf	Globoid	Green	No	Cachoeira Véu da Noiva	Cerrado s.l.	2s
Apocynaceae	Odontadenia lutea (Vell.) Markgr.*	Leaf	Fusiform	Green	Yes	Cidade de Pedra	Cerrado rupestre	2t
Araceae	Philodendron sp.	Leaf	Lenticular	Yellow/red	No	Cachoeira Véu da Noiva	Cerrado s.l.	2u
Araceae	Philodendron sp.	Leaf	Lenticular	Red/yellow	No	Cachoeira das Andorinhas	Cerrado s.l.	2v
Araliaceae	Schefflera morototoni (Aubl.) Maguire et al.	Leaf vein	Swelling	Yellow	Yes	Cachoeira Véu da Noiva	Cerrado s.l.	2w
Aristolochiaceae	Aristolochia sp.	Tendril	Fusiform	Green/brown	No	Vale da Benção	Gallery forest	2x
Aristolochiaceae	Aristolochia sp.	Stem	Globoid	Green	No	Vale da Benção	Gallery forest	2y
Asteraceae	Mikania sp.	Leaf, stem	Fusiform	Brown	Yes	Cachoeira Véu da Noiva	Cerrado s.l.	2z
Asteraceae	Mikania cf. micrantha Kunth	Leaf	Globoid	Green	No	Vale da Benção	Gallery forest	2za
Asteraceae	Mikania cf. micrantha Kunth	Leaf vein	Fusiform	Green	No	Vale da Benção	Gallery forest	2zb
Asteraceae	Mikania cf. micrantha Kunth	Leaf vein	Globoid	Green	No	Vale da Benção	Gallery forest	2zc
Asteraceae	Piptocarpha rotundifolia (Less.) Baker	Leaf	Lenticular	Grey	No	Cachoeira Véu da Noiva	Cerrado s.l.	2zd
Asteraceae	Piptocarpha rotundifolia (Less.) Baker	Leaf	Globoid	Yellow	Yes	Cachoeira Véu da Noiva	Cerrado s.l.	2ze
Asteraceae	Piptocarpha rotundifolia (Less.) Baker	Leaf	Globoid	Brown	Yes	Cachoeira Véu da Noiva	Cerrado s.l.	2zf
Bignoniaceae	Anemopaegma glaucum Mart. ex DC.*	Stem	Amorphous	Green	No	Vale da Benção	Campo Cerrado	2zg
Bignoniaceae	Anemopaegma glaucum Mart. ex DC.*	Leaf bud	Amorphous	Yellow	No	Cachoeira Véu da Noiva	Cerrado rupestre	2zh
Bignoniaceae	Anemopaegma glaucum Mart. ex DC.*	Stem	Fusiform	Green/brown	No	Cachoeira Véu da Noiva	Cerrado rupestre	2zi
Bignoniaceae	Anemopaegma glaucum Mart. ex DC.*	Leaf vein	Fusiform	Green	No	Vale da Benção	Campo Cerrado	2zj
Bignoniaceae	Anemopaegma glaucum Mart. ex DC.*	Leaf	Lenticular	Yellow/red	No	Vale da Benção	Campo Cerrado	3a
Bignoniaceae	Pleonotoma sp.	Stem	Fusiform	Brown	No	Vale da Benção	Gallery forest	3b
Bignoniaceae	Pleonotoma sp.	Stem	Fusiform	Green	No	Vale da Benção	Cerrado s.l.	3c
Bignoniaceae	Pleonotoma sp.	Stem	Globoid	Green	No	Vale da Benção	Cerrado s.l.	3c
Bignoniaceae	Bignoniaceae sp. 1	Tendril	Fusiform	Green	No	Cachoeira Véu da Noiva	Gallery forest	3d
Bignoniaceae	Bignoniaceae sp. 2	Stem	Globoid	Brown	No	Vale do Eco	Gallery forest	3e
Bignoniaceae	Bignoniaceae sp. 2	Leaf	Globoid	Brown	No	Vale do Rio Claro	Gallery forest	3f
Bignoniaceae	Bignoniaceae sp. 2	Leaf	Conical	Green	Yes	Vale da Benção	Gallery forest	3g
Bignoniaceae	Bignoniaceae sp. 3	Leaf vein	Globoid	Brown	No	Vale da Benção	Gallery forest	3h
Bignoniaceae	Bignoniaceae sp. 3	Stem	Globoid	Green/brown	No	Vale da Benção	Cerrado s.l.	3i
Bignoniaceae	Bignoniaceae sp. 4	Leaf vein	Globoid	Green/Red	No	Vale da Benção	Campo Cerrado	3j
Bignoniaceae	Bignoniaceae sp. 4	Leaf	Fusiform	Brown	No	Cachoeira Véu da Noiva	Cerrado s.s.	3k
Boraginaceae	Cordia sellowiana Cham.	Stem	Globoid	Grey	No	Cachoeira Véu da Noiva	Gallery forest	3l
Boraginaceae	Cordia sellowiana Cham.	Stem	Fusiform	Grey	No	Vale da Benção	Gallery forest	3l
Boraginaceae	Cordia sellowiana Cham.	Leaf	Globoid	Brown	No	Vale da Benção	Gallery forest	3m
Boraginaceae	Cordia sellowiana Cham.	Leaf	Globoid	Brown	Yes	Vale da Benção	Gallery forest	3n
Boraginaceae	Cordia sellowiana Cham.	Leaf	Globoid	Green	Yes	Vale da Benção	Gallery forest	3n
Boraginaceae	Cordia sellowiana Cham.	Leaf	Globoid	Grey	Yes	Vale da Benção	Gallery forest	3o
Burseraceae	cf. Tetragastris altissima (Aubl.) Swart	Leaf	Lenticular	Yellow	No	Cachoeira Véu da Noiva	Cerrado s.l.	3p
Burseraceae	Protium heptaphyllum (Aubl.) Marchand	Leaf	Globoid	Brown	No	Cidade de Pedra	Cerrado rupestre	3q
Burseraceae	Protium heptaphyllum (Aubl.) Marchand	Leaf margin	Swelling	Green	No	Vale do Eco	Campo Cerrado	3r
Burseraceae	Protium heptaphyllum (Aubl.) Marchand	Leaf	Lenticular (adax), globoid (abax)	Green	No	Vale do Eco	Campo Cerrado	3s
Burseraceae	Protium heptaphyllum (Aubl.) Marchand	Leaf	Conical	Green	No	Vale do Eco	Campo Cerrado	3t
Burseraceae	Protium heptaphyllum (Aubl.) Marchand	Stem	Fusiform	Brown	No	Vale do Eco	Campo Cerrado	3u
Burseraceae	Protium heptaphyllum (Aubl.) Marchand	Leaf	Globoid	Green/brown	No	Cidade de Pedra	Cerrado rupestre	3v
Burseraceae	Protium heptaphyllum (Aubl.) Marchand	Leaf	Lenticular	Green	No	Vale do Eco	Campo Cerrado	3w
Burseraceae	Protium heptaphyllum (Aubl.) Marchand	Leaf	Globoid	Brown	No	Vale da Benção	Gallery forest	3x
Burseraceae	Protium heptaphyllum (Aubl.) Marchand	Leaf	Globoid	Green/red	Yes	Vale da Benção	Gallery forest	3y
Burseraceae	Protium heptaphyllum (Aubl.) Marchand	Leaf	Globoid	Green/red	Yes	Cachoeira Véu da Noiva	Cerrado s.l.	3y
Burseraceae	Protium heptaphyllum (Aubl.) Marchand	Leaf, stem	Globoid	Green	No	Vale do Eco	Campo Cerrado	3z
Callophylaceae	Kielmeyera grandiflora (Wawra) Saddi	Leaf	Lenticular	Brown	No	Cachoeira Véu da Noiva	Cerrado s.l.	3za
Callophylaceae	Kielmeyera grandiflora (Wawra) Saddi	Leaf vein	Fusiform	Green/Brown	No	Cachoeira Véu da Noiva	Cerrado s.l.	3zb
Caryocaraceae	Caryocar brasiliense Camb.	Leaf	Lenticular	Green	Yes	Vale do Eco	Campo Cerrado	3zc
Celastraceae	Peritassa sp.	Leaf	Globoid	Red	Yes	Vale da Benção	Gallery forest	3zd
Celastraceae	Peritassa sp.	Leaf	Cylindrical	Brown	No	Vale da Benção	Gallery forest	3ze
Celastraceae	Peritassa sp.	Leaf	Lenticular	Brown	No	Vale da Benção	Gallery forest	3ze
Celastraceae	Peritassa sp.	Leaf	Globoid	Yellow/brown	No	Vale da Benção	Gallery forest	3zf
Celastraceae	Peritassa sp.	Leaf	Globoid	Brown	Yes	Vale da Benção	Gallery forest	3zg
Celastraceae	Pristimera celastroides (Kunth) A.C.Sm.*	Leaf vein	Fusiform	Brown	No	Vale da Benção	Gallery forest	3zh
Chrysobalanaceae	Chrysobalanaceae sp.	Leaf	Lenticular	Brown/black	No	Cidade de Pedra	Cerrado rupestre	3zi
Chrysobalanaceae	Parinari obtusifolia Hook.f.*	Leaf	Lenticular	Green	No	Vale do Eco	Campo Cerrado	4a
Chrysobalanaceae	Parinari obtusifolia Hook.f.*	Leaf	Globoid	Brown	Yes	Cidade de Pedra	Cerrado rupestre	4b
Chrysobalanaceae	Parinari obtusifolia Hook.f.*	Leaf	Globoid	Brown	Yes	Cidade de Pedra	Cerrado rupestre	4b
Chrysobalanaceae	Parinari obtusifolia Hook.f.*	Leaf	Globoid	Brown	Yes	Vale do Eco	Campo Cerrado	4b
Combretaceae	Combretum mellifluum Eichler*	Leaf	Lenticular	Brown	No	Cidade de Pedra	Cerrado rupestre	4c
Combretaceae	Combretum mellifluum Eichler*	Leaf	Globoid	Green	No	Cidade de Pedra	Cerrado rupestre	4d
Combretaceae	Combretum mellifluum Eichler*	Leaf	Globoid	Yellow	No	Cidade de Pedra	Cerrado rupestre	4e
Combretaceae	Combretum mellifluum Eichler*	Leaf	lenticular	Yellow	No	Cidade de Pedra	Cerrado rupestre	4e
Combretaceae	Terminalia fagifolia Mart.	Leaf	Lenticular	Green	No	Cidade de Pedra	Cerrado rupestre	4f
Combretaceae	Terminalia fagifolia Mart.	Leaf	Cylindrical	Brown	No	Cidade de Pedra	Cerrado rupestre	4g
Combretaceae	Terminalia fagifolia Mart.	Leaf	Conical	Brown	No	Cidade de Pedra	Cerrado rupestre	4h
Combretaceae	Terminalia glabrescens Mart.*	Leaf	Lenticular	Green	No	Cidade de Pedra	Cerrado rupestre	4i
Combretaceae	Terminalia glabrescens Mart.*	Leaf	Globoid	Green	Yes	Vale do Eco	Campo Cerrado	4i
Connaraceae	Connarus suberosus Planch.	Leaf	Globoid	Yellow/brown	No	Vale do Eco	Campo Cerrado	4j
Connaraceae	Rourea induta Planch.	Leaf	Lenticular	Green/brown	No	Cachoeira Véu da Noiva	Cerrado s.l.	4k
Connaraceae	Rourea induta Planch.	Leaf	Lenticular	Brown	No	Cidade de Pedra	Cerrado rupestre	4l
Connaraceae	Rourea induta Planch.	Leaf	Amorphous	Green	No	Cachoeira Véu da Noiva	Cerrado s.l.	4m
Dilleniaceae	Davilla grandiflora A.St.-Hil.*	Leaf	Lenticular	Brown	No	Cachoeira Véu da Noiva	Cerrado s.l.	4n
Dilleniaceae	Davilla grandiflora A.St.-Hil.*	Leaf	Lenticular	Brown	No	Cachoeira Véu da Noiva	Cerrado s.l.	4o
Dilleniaceae	Davilla grandiflora A.St.-Hil.*	Leaf	Lenticular	Grey	No	Cidade de Pedra	Cerrado rupestre	4p
Dilleniaceae	Davilla grandiflora A.St.-Hil.*	Fruit	Amorphous	Green	No	Cidade de Pedra	Cerrado rupestre	4q
Dilleniaceae	Davilla grandiflora A.St.-Hil.*	Leaf	Lenticular	Grey	No	Vale do Eco	Campo Cerrado	4r
Dilleniaceae	Davilla grandiflora A.St.-Hil.*	Leaf	Rosette	Brown	No	Cidade de Pedra	Cerrado rupestre	4s
Dilleniaceae	Davilla grandiflora A.St.-Hil.*	Leaf bud	Rosette	Green	No	Vale do Rio Claro	Cerrado s.s.	4t
Dilleniaceae	Davilla grandiflora A.St.-Hil.*	Stem	Swelling	Brown	No	Cachoeira Véu da Noiva	Cerrado s.l.	4u
Dilleniaceae	Davilla lacunosa Mart.*	Leaf	Lenticular	Grey/brown	No	Cachoeira Véu da Noiva	Cerrado s.l.	4v
Dilleniaceae	Davilla lacunosa Mart.*	Leaf	Lenticular	Grey	No	Cachoeira Véu da Noiva	Cerrado s.l.	4w
Dilleniaceae	Davilla lacunosa Mart.*	Leaf	Lenticular	Yellow	No	Cachoeira das Andorinhas	Cerrado s.l.	4x
Elaeocarpaceae	Sloanea sp.	Leaf	Cylindrical	Green	No	Vale da Benção	Gallery forest	4y
Elaeocarpaceae	Sloanea sp.	Leaf	Cylindrical	Brown	No	Vale da Benção	Gallery forest	4z
Erythroxylaceae	Erythroxylum cf. pruinosum O.E.Schulz*	Fruit	Amorphous	Green	No	Cachoeira Véu da Noiva	Cerrado s.l.	4za
Erythroxylaceae	Erythroxylum campestre A.St.-Hil.	Leaf	Lenticular	Green/brown	No	Cachoeira Véu da Noiva	Cerrado s.l.	4zb
Erythroxylaceae	Erythroxylum citrifolium A.St.-Hil.	Leaf	Lenticular	Brown	No	Cachoeira das Andorinhas	Cerrado s.l.	4zc
Erythroxylaceae	Erythroxylum citrifolium A.St.-Hil.	Leaf	Lenticular	Yellow	No	Cachoeira das Andorinhas	Cerrado s.l.	4zc
Erythroxylaceae	Erythroxylum daphnites Mart.	Leaf	Star shaped	Brown	Yes	Cachoeira Véu da Noiva	Cerrado s.l.	4zd
Erythroxylaceae	Erythroxylum daphnites Mart.	Stem	Piriformis	Brown	No	Cachoeira Véu da Noiva	Cerrado s.l.	4ze
Erythroxylaceae	Erythroxylum daphnites Mart.	Leaf	Lenticular	Grey	No	Cachoeira Véu da Noiva	Cerrado s.l.	4ze
Erythroxylaceae	Erythroxylum daphnites Mart.	Leaf	Globoid	Yellow	Yes	Cachoeira Véu da Noiva	Cerrado s.l.	4zf
Erythroxylaceae	Erythroxylum daphnites Mart.	Leaf	Lenticular	Brown	No	Cidade de Pedra	Cerrado rupestre	4zg
Euphorbiaceae	Bernardia similis Pax & K.Hoffm.*	Leaf	Lenticular	Black	No	Cidade de Pedra	Cerrado rupestre	4zh
Euphorbiaceae	Mabea sp.	Leaf	Conical	Yellow	No	Vale da Benção	Gallery forest	4zi
Euphorbiaceae	Manihot tripartita (Spreng.) Müll.Arg.	Leaf	Globoid	Green/red	No	Cidade de Pedra	Cerrado rupestre	5a
Euphorbiaceae	Manihot tripartita (Spreng.) Müll.Arg.	Leaf	Cylindrical	Green	No	Cidade de Pedra	Cerrado rupestre	5b
Euphorbiaceae	Manihot tripartita (Spreng.) Müll.Arg.	Leaf	Lenticular	Brown	No	Cidade de Pedra	Cerrado rupestre	5b
Euphorbiaceae	Manihot tripartita (Spreng.) Müll.Arg.	Leaf	Lenticular	Black	No	Cidade de Pedra	Cerrado rupestre	5b
Euphorbiaceae	Manihot tripartita (Spreng.) Müll.Arg.	Leaf	Cylindrical	Green/red	No	Vale do Rio Claro	Cerrado s.s.	5c
Euphorbiaceae	Jatropha sp.	Leaf	Cylindrical	Green	No	Vale do Eco	Campo Cerrado	5d
Euphorbiaceae	Jatropha sp.	Leaf	Cylindrical	Green/red	No	Vale do Eco	Campo Cerrado	5e
Euphorbiaceae	Maprounea guianensis Aubl.	Stem	Globoid	Green/brown	No	Vale da Benção	Gallery forest	5f
Euphorbiaceae	Maprounea guianensis Aubl.	Stem	Fusiform	Green/brown	No	Cachoeira Véu da Noiva	Cerrado s.l.	5g
Fabaceae	Ancistrotropis firmula (Mart. ex Benth.) A. Delgado*	Leaf	Lenticular	Yellow	No	Cidade de Pedra	Cerrado rupestre	5h
Fabaceae	Andira cujabensis Benth.	Leaf	Amorphous	Yellow	No	Vale do Eco	Campo Cerrado	5i
Fabaceae	Andira cujabensis Benth.	Leaf	Lenticular	Yellow	Yes	Cachoeira das Andorinhas	Cerrado s.l.	5j
Fabaceae	Andira cujabensis Benth.	Leaf	Lenticular	Yellow/red	No	Cachoeira Véu da Noiva	Cerrado s.l.	5k
Fabaceae	Andira cujabensis Benth.	Leaf	Lenticular	Yellow	No	Cachoeira Véu da Noiva	Cerrado s.l.	5l
Fabaceae	Andira cujabensis Benth.	Leaf	Lenticular	Green	No	Cachoeira Véu da Noiva	Cerrado s.l.	5m
Fabaceae	Andira cujabensis Benth.	Leaf	Lenticular	Yellow	No	Vale do Rio Claro	Cerrado s.s.	5n
Fabaceae	Andira humilis Mart. ex Benth.	Leaf	Globoid	Green	No	Vale do Eco	Campo Cerrado	5o
Fabaceae	Andira surinamensis (Bondt) Splitg. ex Amshoff	Leaf	Globoid	Brown	No	Cidade de Pedra	Cerrado rupestre	5p
Fabaceae	Andira surinamensis (Bondt) Splitg. ex Amshoff	Leaf vein	Fusiform	Yellow/red	No	Cidade de Pedra	Cerrado rupestre	5q
Fabaceae	Andira surinamensis (Bondt) Splitg. ex Amshoff	Leaf	Globoid	Yellow	No	Cidade de Pedra	Cerrado rupestre	5q
Fabaceae	Andira surinamensis (Bondt) Splitg. ex Amshoff	Leaf	Globoid	Green/red	No	Vale do Eco	Campo Cerrado	5r
Fabaceae	Andira surinamensis (Bondt) Splitg. ex Amshoff	Leaf	Lenticular	Brown	No	Vale do Eco	Campo Cerrado	5r
Fabaceae	Andira surinamensis (Bondt) Splitg. ex Amshoff	Leaf	Globoid	Yellow	No	Vale do Rio Claro	Cerrado s.s.	5s
Fabaceae	Andira surinamensis (Bondt) Splitg. ex Amshoff	Leaf	Kidney shape	Green	No	Vale do Eco	Campo Cerrado	5t
Fabaceae	Andira vermifuga (Mart.) Benth.	Leaf	Globoid	Green	No	Vale do Eco	Campo Cerrado	5u
Fabaceae	Andira vermifuga (Mart.) Benth.	Leaf	Conical	Green	No	Vale do Rio Claro	Cerrado s.s.	5v
Fabaceae	Andira vermifuga (Mart.) Benth.	Leaf	Kidney shape	Green	No	Vale do Rio Claro	Cerrado s.s.	5w
Fabaceae	Bauhinia sp. 1	Leaf	Lenticular	Brown	No	Vale da Benção	Gallery forest	5x
Fabaceae	Bauhinia sp. 1	Leaf vein	Triangular	Green	No	Vale da Benção	Gallery forest	5x
Fabaceae	Bauhinia sp. 2	Leaf vein	Fusiform	Green	No	Vale do Eco	Campo Cerrado	5y
Fabaceae	Bauhinia sp. 3	Leaf	Lenticular	Grey	No	Cachoeira Véu da Noiva	Cerrado s.l.	5z
Fabaceae	Bauhinia sp. 4	Leaf	Globoid	Green	No	Vale do Eco	Campo Cerrado	5za
Fabaceae	Calliandra sp.	Stem	Fusiform	Brown	No	Vale do Eco	Campo Cerrado	5zb
Fabaceae	Chamaecrista sp.	Leaf	Lenticular	Brown	No	Cachoeira Véu da Noiva	Cerrado s.l.	5zc
Fabaceae	Copaifera depilis Dwyer	Leaf	Lenticular	Brown	No	Vale do Eco	Campo Cerrado	5zd
Fabaceae	Copaifera depilis Dwyer	Leaf	Lenticular	Green	No	Vale do Eco	Campo Cerrado	5ze
Fabaceae	Copaifera depilis Dwyer	Leaf	Globoid	Yellow	No	Vale do Eco	Campo Cerrado	5ze
Fabaceae	Copaifera depilis Dwyer	Leaf	Globoid	Brown	Yes	Vale do Eco	Campo Cerrado	5zf
Fabaceae	Copaifera depilis Dwyer	Leaf, stem	Globoid	Yellow	No	Vale do Eco	Campo Cerrado	5zg
Fabaceae	Copaifera depilis Dwyer	Leaf	Lenticular convex	Brown/pink	No	Vale do Eco	Campo Cerrado	5zh
Fabaceae	Copaifera depilis Dwyer	Leaf	Globoid	Brown	Yes	Vale do Eco	Campo Cerrado	5zi
Fabaceae	Copaifera depilis Dwyer	Leaf bud	Globoid	Brown	Yes	Vale do Eco	Campo Cerrado	6a
Fabaceae	Hymenaea courbaril L.	Leaf	Lenticular	Yellow	No	Vale da Benção	Gallery forest	6b
Fabaceae	Hymenaea courbaril L.	Leaf	Lenticular	Yellow	No	Vale da Benção	Gallery forest	6c
Fabaceae	Hymenaea courbaril L.	Leaf	Lenticular	Green	No	Vale da Benção	Gallery forest	6d
Fabaceae	Inga disticha Benth.	Leaf	Globoid	Yellow	Yes	Cachoeira Véu da Noiva	Cerrado s.l.	6e
Fabaceae	Inga disticha Benth.	Leaf	Globoid	Yellow	No	Cachoeira Véu da Noiva	Cerrado s.l.	6e
Fabaceae	Inga leiocalycina Benth.*	Leaf	Marginal roll	Green	No	Vale da Benção	Gallery forest	6f
Fabaceae	Inga vera Willd.	Leaf vein	Fusiform	Yellow	No	Cachoeira Véu da Noiva	Cerrado s.l.	6g
Fabaceae	Machaerium sp.	Leaf	Cylindrical	Green	No	Vale da Benção	Gallery forest	6h
Fabaceae	Ormosia macrophylla Benth.*	Leaf	Lenticular	Grey	No	Vale da Benção	Gallery forest	6i
Fabaceae	Senegalia sp.	Leaf	Globoid	Brown	No	Vale da Benção	Gallery forest	6j
Fabaceae	Stryphnodendron adstringens (Mart.) Coville	Leaf	Lenticular	Brown	No	Cidade de Pedra	Cerrado rupestre	6k
Fabaceae	Stryphnodendron adstringens (Mart.) Coville	Stem	Globoid	Brown	No	Cidade de Pedra	Cerrado rupestre	6l
Fabaceae	Stryphnodendron adstringens (Mart.) Coville	Stem	Fusiform	Brown	No	Vale do Eco	Campo Cerrado	6m
Fabaceae	Tachigali rubiginosa (Mart. ex Tul.) Oliveira-Filho*	Leaf	Lenticular	Green /brown	Yes	Cachoeira Véu da Noiva	Cerrado s.l.	6n
Fabaceae	Tachigali rubiginosa (Mart. ex Tul.) Oliveira-Filho*	Leaf	Globoid (adax), lenticular (abax)	Green/brown	Yes	Cachoeira Véu da Noiva	Cerrado s.l.	6o, 6p
Fabaceae	Tachigali subvelutina (Benth.) Oliveira-Filho*	Leaf, stem	Cylindrical	Green	Yes	Vale do Eco	Campo Cerrado	6q
Lauraceae	Aiouea saligna Meisn.*	Leaf	Globoid	Green/brown	No	Vale do Eco	Campo Cerrado	6r
Lauraceae	Aiouea saligna Meisn.*	Ovary	Swelling	Green/red	No	Vale do Eco	Campo Cerrado	6s
Malpighiaceae	Alicia macrodisca (Triana & Planch.) W.R.Anderson*	Stem	Fusiform	Green/brown	Yes	Vale da Benção	Gallery forest	6t
Malpighiaceae	Byrsonima coccolobifolia Kunth.	Leaf vein	Swelling	Brown	No	Cachoeira Véu da Noiva	Cerrado s.l.	6u
Malpighiaceae	Byrsonima sericea DC.	Stem	Fusiform	Brown	No	Cachoeira Véu da Noiva	Cerrado s.l.	6v
Malpighiaceae	Byrsonima sericea DC.	Leaf	Lenticular	Green	No	Cidade de Pedra	Cerrado rupestre	6w
Malpighiaceae	Diplopterys pubipetala (A.Juss.) W.R.Anderson & C.C.Davis	Leaf	Conical	Green	No	Vale do Eco	Campo Cerrado	6x
Malpighiaceae	Heteropterys cf. coriacea A. Juss.*	Leaf bud	Amorphous	Green	No	Cidade de Pedra	Cerrado rupestre	6y
Malpighiaceae	Heteropterys cf. coriacea A. Juss.*	Leaf	Lenticular	Brown	No	Cidade de Pedra	Cerrado rupestre	6z
Malpighiaceae	Heteropterys cf. coriacea A. Juss.*	Leaf	Lenticular	Green /brown	No	Cidade de Pedra	Cerrado rupestre	6za
Malpighiaceae	Heteropterys cf. coriacea A. Juss.*	Leaf	Lenticular	Brown	No	Cachoeira das Andorinhas	Cerrado s.l.	6zb
Malpighiaceae	Heteropterys cf. coriacea A. Juss.*	Leaf	Lenticular	Green /brown	No	Cachoeira das Andorinhas	Cerrado s.l.	6zc
Malpighiaceae	Heteropterys cf. coriacea A. Juss.*	Leaf	Lenticular	Green /brown	No	Cidade de Pedra	Cerrado rupestre	6zd
Malpighiaceae	Heteropterys cf. coriacea A. Juss.*	Leaf	Lenticular	Yellow	No	Vale do Rio Claro	Cerrado s.s.	6ze
Melastomataceae	Macairea radula (Bonpl.) DC.	Stem	Globoid	Green	Yes	Cachoeira Véu da Noiva	Cerrado s.l.	6zf
Melastomataceae	Miconia albicans (Sw.) Triana	Leaf	Globoid	Brown	Yes	Cachoeira Véu da Noiva	Cerrado s.l.	6zg
Melastomataceae	Miconia albicans (Sw.) Triana	Leaf	Amorphous	Yellow	No	Cachoeira das Andorinhas	Cerrado s.l.	6zh
Melastomataceae	Miconia rubiginosa (Bonpl.) DC.*	Leaf	Lenticular	Brown	No	Cachoeira Véu da Noiva	Cerrado s.l.	6zi
Melastomataceae	Miconia sp. 1	Leaf	Lenticular	Yellow	No	Cachoeira Véu da Noiva	Cerrado s.l.	7a
Melastomataceae	Miconia sp. 1	Leaf	Globoid	Yellow/pink	Yes	Cachoeira Véu da Noiva	Cerrado s.l.	7b
Melastomataceae	Miconia sp. 1	Leaf	Globoid	Yellow	Yes	Cachoeira Véu da Noiva	Cerrado s.l.	7c
Melastomataceae	Miconia sp. 1	Leaf bud	Amorphous	Green	Yes	Cachoeira Véu da Noiva	Cerrado s.l.	7d
Melastomataceae	Miconia sp. 2	Leaf	Globoid	Green	Yes	Cachoeira das Andorinhas	Cerrado s.l.	7e, 7f
Melastomataceae	Mouriri elliptica Mart.*	Leaf	Lenticular	Brown	No	Cidade de Pedra	Cerrado rupestre	7g
Melastomataceae	Tibouchina sp.	Stem	Fusiform	Brown	No	Cidade de Pedra	Cerrado rupestre	7h
Melastomataceae	Tibouchina sp.	Stem	Globoid	Brown	No	Cidade de Pedra	Cerrado rupestre	7i
Melastomataceae	Tococa sp	Leaf	Lenticular	Brown	No	Cachoeira Véu da Noiva	Cerrado s.l.	7j
Melastomataceae	Tococa sp	Leaf vein	Fusiform	Brown	No	Cachoeira Véu da Noiva	Cerrado s.l.	7j
Meliaceae	Guarea guidonia (L.) Sleumer	Leaf vein	Fusiform	Brown	No	Vale da Benção	Gallery forest	7k
Meliaceae	Guarea guidonia (L.) Sleumer	Leaf	Globoid	Yellow	No	Vale da Benção	Gallery forest	7l
Meliaceae	Guarea guidonia (L.) Sleumer	Leaf	Globoid	Yellow	No	Vale da Benção	Gallery forest	7m
Meliaceae	Guarea macrophylla subsp. spiciflora (A.Juss.) T.D.Penn.*	Leaf	Globoid	Yellow	Yes	Cachoeira Véu da Noiva	Cerrado s.l.	7n
Monimiaceae	Mollinedia sp.	Leaf	Lenticular	Green/yellow	No	Cachoeira Véu da Noiva	Cerrado s.l.	7o
Moraceae	Brosimum lactescens (S.Moore) C.C.Berg	Leaf	Cylindrical	Green/brown	No	Cachoeira Véu da Noiva	Cerrado s.l.	7p
Moraceae	Ficus sp. 1	Leaf	Lenticular	Green	No	Cachoeira das Andorinhas	Cerrado s.l.	7q
Moraceae	Ficus sp. 2	Leaf	Globoid	Green/red	No	Cachoeira Véu da Noiva	Cerrado s.l.	7r
Moraceae	Ficus sp. 2	Leaf	Lenticular	Green /brown	No	Cachoeira Véu da Noiva	Cerrado s.l.	7s
Moraceae	Ficus sp. 2	Leaf	Lenticular	Yellow/red	No	Cachoeira Véu da Noiva	Cerrado s.l.	7t
Myrtaceae	Eugenia punicifolia (Kunth)	Stem	Globoid	Brown	No	Cachoeira Véu da Noiva	Cerrado s.l.	7u
Myrtaceae	Eugenia sp.	Leaf	Lenticular	Yellow/red	No	Vale do Rio Claro	Cerrado s.s.	7v
Myrtaceae	Myrcia bella Cambess.	Leaf	Lenticular	Yellow/brown	No	Vale do Eco	Campo Cerrado	7w
Myrtaceae	Myrcia bella Cambess.	Leaf	Globoid	Green/red	No	Vale do Eco	Campo Cerrado	7x
Myrtaceae	Myrcia bella Cambess.	Leaf bud	Amorphous	Green	No	Vale do Rio Claro	Cerrado s.s.	7y
Myrtaceae	Myrcia guianensis (Aubl.) DC.	Leaf	Lenticular	Green/brown	No	Cachoeira Véu da Noiva	Cerrado s.l.	7z
Myrtaceae	Myrcia guianensis (Aubl.) DC.	Leaf	Lenticular	Brown	No	Cachoeira Véu da Noiva	Cerrado s.l.	7za
Myrtaceae	Myrcia sp.	Leaf	Lenticular	Brown	No	Cachoeira Véu da Noiva	Cerrado s.l.	7zb
Myrtaceae	Myrcia splendens (Sw.) DC.	Leaf	Globoid	Green	No	Vale da Benção	Gallery forest	7zc
Myrtaceae	Myrcia splendens (Sw.) DC.	Leaf	Globoid	Green	Yes	Vale da Benção	Gallery forest	7zd
Myrtaceae	Myrcia splendens (Sw.) DC.	Leaf	Lenticular	Brown	No	Cachoeira das Andorinhas	Cerrado s.l.	7ze
Myrtaceae	Myrcia splendens (Sw.) DC.	Leaf	Globoid	Red	Yes	Cachoeira Véu da Noiva	Cerrado s.l.	7zf
Myrtaceae	Myrcia variabilis DC.	Leaf	Lenticular	Brown	No	Cachoeira das Andorinhas	Cerrado s.l.	7zg
Ochnaceae	Ouratea castaneifolia (DC.) Engl.	Leaf	Lenticular	Green	No	Vale da Benção	Gallery forest	7zh
Ochnaceae	Ouratea nana (A.St.-Hil.) Engl.*	Leaf	Lenticular	Grey	No	Cidade de Pedra	Cerrado rupestre	7zi
Ochnaceae	Ouratea nana (A.St.-Hil.) Engl.*	Leaf	Lenticular	Green/brown	No	Cidade de Pedra	Cerrado rupestre	7zi
Ochnaceae	Ouratea nana (A.St.-Hil.) Engl.*	Leaf	Lenticular	Green/brown	No	Cachoeira das Andorinhas	Cerrado s.l.	8a
Ochnaceae	Ouratea riedeliana Engl.*	Leaf	Lenticular	Green/brown	No	Cidade de Pedra	Cerrado rupestre	8b
Piperaceae	cf. Piper dilatatum Rich.	Leaf, stem	Cylindrical	Green	Yes	Vale da Benção	Gallery forest	8c
Polygonaceae	Coccoloba cujabensis Wedd.	Leaf, stem	Lenticular	Brown	No	Cidade de Pedra	Cerrado rupestre	8d
Proteaceae	Roupala montana Aubl.	Leaf	Lenticular	Brown	No	Cachoeira das Andorinhas	Cerrado s.l.	8e
Rubiaceae	Cordiera myrciifolia (K.Schum.) C.H.Perss. and Delprete*	Leaf	Lenticular	Brown	No	Cachoeira das Andorinhas	Cerrado s.l.	8f
Rubiaceae	Cordiera myrciifolia (K.Schum.) C.H.Perss. and Delprete*	Leaf vein	Fusiform	Green	No	Cachoeira das Andorinhas	Cerrado s.l.	8f
Rubiaceae	Cordiera obtusa (K.Schum.) Kuntze*	Leaf	Lenticular	Brown	No	Cidade de Pedra	Cerrado rupestre	8g
Rubiaceae	Rubiaceae sp.	Stem	Fusiform	Brown	No	Vale da Benção	Gallery forest	8h
Sapindaceae	Matayba guianensis Aubl.	Leaf	Cylindrical	Green	Yes	Cachoeira Véu da Noiva	Cerrado s.l.	8i
Sapindaceae	Matayba sp. 1	Leaf vein	Fusiform	Green	No	Vale da Benção	Gallery forest	8j
Sapindaceae	Matayba sp. 2	Leaf	Lenticular	Grey	No	Vale do Eco	Campo Cerrado	8k
Sapindaceae	Serjania caracasana (Jacq.) Willd.	Leaf	Cylindrical	Green/Red	Yes	Vale da Benção	Gallery forest	8l
Sapindaceae	Serjania matogrossensis Ferrucci & Acev.-Rodr.*	Tendril	Fusiform	Green/brown	No	Vale da Benção	Gallery forest	8m
Sapindaceae	Serjania sp.	Leaf	Lenticular	Brown	No	Cachoeira Véu da Noiva	Cerrado s.l.	8n
Sapindaceae	Talisia subalbens (Mart.) Radlk.*	Leaf	Lenticular	Yellow	No	Cachoeira das Andorinhas	Cerrado s.l.	8o
Sapotaceae	Ecclinusa ramiflora Mart.*	Leaf	Wrinkle	Green	No	Vale da Benção	Gallery forest	8p
Sapotaceae	Pouteria ramiflora (Mart.) Radlk.	Leaf	Lenticular	Brown	No	Cachoeira Véu da Noiva	Cerrado s.l.	8q
Sapotacae	Pouteria torta (Mart.) Radlk.	Leaf	Cylindrical	Green/brown	Yes	Vale do Rio Claro	Cerrado s.s.	8r
Sapotaceae	Pouteria torta (Mart.) Radlk.	Stem	Fusiform	Brown	No	Vale do Eco	Campo Cerrado	8s
Sapotaceae	Pouteria torta (Mart.) Radlk.	Leaf	Conical	Green	Yes	Vale do Eco	Campo Cerrado	8t
Sapotaceae	Pouteria torta (Mart.) Radlk.	Leaf	Lenticular	Green	Yes	Vale do Eco	Campo Cerrado	8u
Sapotaceae	Pouteria sp. 1	Leaf	Lenticular	Brown	No	Vale do Eco	Campo Cerrado	8v
Sapotaceae	Pouteria sp. 1	Stem	Fusiform	Brown	No	Vale do Eco	Campo Cerrado	8v
Sapotaceae	Pouteria sp. 2	Leaf	Globoid	Green	No	Vale do Eco	Campo Cerrado	8w
Simaroubaceae	Simarouba versicolor A.St.-Hil.*	Leaf	Globoid	Green/red	No	Cachoeira Véu da Noiva	Cerrado s.l.	8x
Simaroubaceae	Simarouba versicolor A.St.-Hil.*	Leaf	Lenticular (adax), conical (abax)	Green	No	Cachoeira Véu da Noiva	Cerrado s.l.	8y, 8z
Simaroubaceae	Simarouba versicolor A.St.-Hil.*	Leaf	Cylindrical	Green	No	Cachoeira das Andorinhas	Cerrado s.l.	8za
Simplocaceae	Symplocos cf. nitens (Pohl) Benth.*	Stem	Fusiform	Brown	No	Cachoeira Véu da Noiva	Cerrado s.l.	8zb
Siparunaceae	Siparuna guianensis Aubl.	Leaf	Cylindrical	Yellow/brown	Yes	Cachoeira Véu da Noiva	Cerrado s.l.	8zc
Siparunaceae	Siparuna guianensis Aubl.	Stem	Globoid	Green	No	Cachoeira Véu da Noiva	Cerrado s.l.	8zd
Siparunaceae	Siparuna guianensis Aubl.	Leaf vein	Globoid	Brown	No	Vale da Benção	Gallery forest	8ze
Siparunaceae	Siparuna guianensis Aubl.	Leaf	Globoid	Grey	No	Vale da Benção	Gallery forest	8zf
Siparunaceae	Siparuna guianensis Aubl.	Leaf	Lenticular	Green	Yes	Cachoeira Véu da Noiva	Cerrado s.l.	8zg, 8zh
Siparunaceae	Siparuna sp.	Leaf vein	Fusiform	Green	Yes	Vale da Benção	Gallery forest	8zi
Smilacaceae	Smilax brasiliensis Spreng.	Stem	Amorphous	Green	No	Vale do Eco	Campo Cerrado	9a
Smilacaceae	Smilax brasiliensis Spreng.	Leaf vein	Globoid	Green/brown	No	Vale do Eco	Campo Cerrado	9b
Smilacaceae	Smilax fluminensis Steud.	Leaf vein	Lenticular (addax.), globoid (abax.)	Green	No	Vale da Benção	Gallery forest	9c
Smilacaceae	Smilax fluminensis Steud.	Leaf	Lenticular	Green	No	Vale da Benção	Gallery forest	9d
Styracaceae	Styrax sp.	Leaf	Lenticular	Black	No	Cachoeira Véu da Noiva	Cerrado s.l.	9e
Styracaceae	Styrax sp.	Stem	Fusiform	Brown	No	Cachoeira Véu da Noiva	Cerrado s.l.	9f
Styracaceae	Styrax sp.	Stem	Fusiform	Brown	No	Cachoeira Véu da Noiva	Cerrado s.l.	9g
Styracaceae	Styrax sp.	Leaf	Lenticular	Brown	No	Cachoeira Véu da Noiva	Cerrado s.l.	9g
Vochysiaceae	Qualea parviflora Mart	Leaf	Lenticular	Brown	No	Cidade de Pedra	Cerrado rupestre	9h
Vochysiaceae	Qualea parviflora Mart	Leaf	Lenticular	Black	No	Cidade de Pedra	Cerrado rupestre	9i
Vochysiaceae	Qualea parviflora Mart	Leaf	Globoid	Yellow	No	Cidade de Pedra	Cerrado rupestre	9j, 9k
Vochysiaceae	Qualea parviflora Mart	Leaf	Lenticular	Yellow/brown	No	Vale do Eco	Campo Cerrado	9l
Vochysiacece	Qualea parviflora Mart	Leaf	Globoid (addax.), conical (abax.)	Green/yellow	Yes	Cidade de Pedra	Cerrado rupestre	9m, 9n
Vochysiacece	Qualea parviflora Mart	Leaf	Globoid	Yellow	No	Vale do Rio Claro	Cerrado s.s.	9o
Vochysiacece	Qualea parviflora Mart	Leaf	Globoid	Yellow/red	Yes	Vale do Rio Claro	Cerrado s.s.	9p
Vochysiacece	Qualea parviflora Mart	Leaf	Fusiform	Green	No	Vale do Rio Claro	Cerrado s.s.	9q
Vochysiacece	Qualea parviflora Mart	Stem	Amorphous	Brown	Yes	Cachoeira Véu da Noiva	Cerrado s.l.	9r
Vochysiacece	Qualea parviflora Mart	Leaf	Globoid	Yellow/red	Yes	Cachoeira Véu da Noiva	Cerrado s.l.	9s
Vochysiacece	Vochysia petraea Warm.*	Leaf	Lenticular	Green	No	Cidade de Pedra	Cerrado rupestre	9t
Vochysiaceae	Vochysia petraea Warm.*	Leaf	Globoid	Yellow	Yes	Vale do Eco	Campo Cerrado	9u
Unidentified	Unidentified sp. 1	Leaf	Amorphous	Yellow	No	Cachoeira Véu da Noiva	Cerrado s.l.	9v
Unidentified	Unidentified sp. 2	Leaf	Globoid	Green	No	Cidade de Pedra	Cerrado rupestre	9w
Unidentified	Unidentified sp. 3	Stem	Globoid	Yellow	No	Cidade de Pedra	Cerrado rupestre	9x
Unidentified	Unidentified sp. 4	Leaf vein	Fusiform	Green	No	Cidade de Pedra	Cerrado rupestre	9y
Unidentified	Unidentified sp. 5	Leaf	Cylindrical	Brown	No	Cidade de Pedra	Cerrado rupestre	9z
Unidentified	Unidentified sp. 5	Leaf	Globoid	Yellow	No	Cidade de Pedra	Cerrado rupestre	9z
Unidentified	Unidentified sp. 6	Leaf	Conical	Yellow	Yes	Cidade de Pedra	Cerrado rupestre	9za
Unidentified	Unidentified sp. 7	Stem	Fusiform	Brown	No	Vale do Eco	Campo Cerrado	9zb
Unidentified	Unidentified sp. 7	Leaf	Cylindrical	Green	Yes	Vale do Eco	Campo Cerrado	9zc, 9zd
Unidentified	Unidentified sp. 8	Leaf vein	Fusiform	Green	No	Vale do Eco	Campo Cerrado	9ze
Unidentified	Unidentified sp. 9	Leaf	Globoid	Green	Yes	Vale da Benção	Gallery forest	9zf
Unidentified	Unidentified sp. 10	Stem	Globoid	Red	No	Cachoeira Véu da Noiva	Cerrado s.l.	9zg
Unidentified	Unidentified sp. 11	Stem	Globoid	Brown	No	Cachoeira Véu da Noiva	Cerrado s.l.	9zh

Table 3
Richness of gall morphotypes and plant super-hosts families and species from localities in Brazilian Cerrado areas.

Inventories	Locality, Brazilian State, Brazilian Region	Biome	Richness				Super-host
			Gall morphotypes	Plant species	Plant family	Average morphotypes/ plant species	Families	Species
Urso-Guimarães, Koch & Castello (present study)	Parque Nacional da Chapada dos Guimarães, MT, Midwest	Gallery Forest, Cerrado	295	139	40	2.1	Fabaceae (49), Bignoniaceae (16), Myrtaceae (13), Malpighiaceae (12), Melastomataceae (11)	Protium heptaphyllum (10), Qualea parviflora (10), Davilla grandiflora (8), Copaifera depilis (8)
Carneiro et al. (2009)	Cadeia do Espinhaço, MG, Southeast	Rupestrian fields	241	142	29	1.7	Asteraceae (86), Melastomataceae (22), Malpighiaceae (18)	Baccharis pseudomyriocephala (10), Byrsonima coccolobifolia (8), Baccharis platypoda (7)
Fernandes et al. (1997)	Jequitinhonha Valley, MG, Southeast	Rupestrian fields	236	134	27	1.76	Fabaceae (34), Malpighiaceae (32), Asteraceae (32)	Sida urens (6)
Bergamini et al. (2017)	Floresta Nacional de Silvania, GO, Midwest	Gallery Forest, Cerrado	186	61	35	3.05	Fabaceae (18), Asteraceae (17), Sapindaceae (16)	Protium heptaphyllum (14), Siparuna guianensis (12), Serjania sp. (12)
Silva et al. (2018)	Hidrolândia, GO, Midwest	SEF, Cerrado	150	104	39	1.44	Fabaceae (22), Malpighiaceae (13), Sapindaceae (11), Erythroxylaceae (8), Myrtaceae (9)	Siparuna guianensis (7), Bauhinia brevipes (6), Erythroxylum sp. (5)
Maia & Fernandes (2004)	Serra de São José, Tiradentes, MG, Southeast	Rupestrian fields	137	73	30	1.88	Fabaceae (20), Myrtaceae (18), Asteraceae (16)	Protium heptaphyllum (7), Copaifera langsdorffii (6), Myrcia sp. (6)
Luz et al. (2012)	APA Rio Pandeiros, MG, Southeast	Caatinga, Cerrado	98	70	20	1.4	Fabaceae (19), Myrtaceae (6), Sapindaceae (4)	Copaifera langsdorffii (11), Calophyllum brasiliense (5), Bauhinia brevipes (4)
Araújo et al. (2014)	Parque Nacional das Emas, Mineiros, GO, Midwest	Cerrado	97	55	24	1.76	Myrtaceae (17), Fabaceae (14), Vochysiaceae (9)	Andira cujabensis (4), Myrcia guianensis (4)
Coelho et al. (2013a)	Serra da Mantiqueira, MG, Southeast	Cerrado , Atlantic Forest	93	50	21	1.86	Asteraceae (52), Melastomataceae (17), Euphorbiaceae (5)	Baccharis platypoda (8), Baccharis salzmanii (6)
Gonçalves-Alvim & Fernandes (2001)	Estação Ecológica de Pirapitinga, Três Marias, MG, Southeast	Cerrado	92	62	28	1.48	Fabaceae (13), Asteraceae (5), Malpighiaceae (5)	Byrsonima coccolobifolia (4) Andira sp. (4), Myrcia sp. (4)
Saito & Urso-Guimarães (2012)	Estação Ecológica de Jataí, Luiz Antônio, SP, Southeast	Cerrado	69	41	24	1.68	Malpighiaceae (9), Annonaceae (7), Myrtaceae (7)	Byrsonima intermedia (6), Duguetia furfuracea (5), Arrabidaea sp. (4)
Urso-Guimarães et al. (2017)	Morro do Camisão, Aquidauana, MS, Midwest	Cerrado	68	50	23	1.36	Fabaceae (20), Sapindaceae (8), Myrtaceae (7)	Hymenaea stigonocarpa (4), Guibourtia hymenaeifolia (3), Amorimia pubiflora (3)
Araújo et al. (2011)	Parque Estadual da Serra dos Pireneus, Pirenópolis, GO, Midwest	Gallery Forest, SEF, Cerrado, Rocky Savanna	62	51	28	1.22	Fabaceae (8), Styracaceae (6), Malpighiaceae (5)	Styrax pohlii (5) &ira paniculata (3), Qualea parviflora (3), Davilla elliptica (2)
Malves & Friero-Costa (2012)	Lavras, MG, Southeast	Rupestrian Fields, Riparian Forest, Cerrado	57	43	18	1.33	Asteraceae (6), Myrtaceae (5), Melastomataceae (3)	Croton sp. (4), Eugenia sp.2 (3)
Santos et al. (2012)	Caldas Novas, GO, Midwest	Cerrado	56	34	21	1.65	Fabaceae (9), Styracaceae (6), Ulmaceae (4)	Styrax pohlii (6), Inga cylindrica (3), Serjania obtusidentata (3), Trema micrantha (3)
Nogueira et al. (2016)	Serra Geral, Caitité, BA, Northeast	Caatinga, Cerrado	49	14	13	3.5	Fabaceae (22), Malpighiaceae (10)	Copaifera langsdorffii (10), Bauhinia acuruana (5), Mimosa gemmulata (4)
Vieira et al. (2018)	Caitité, BA, Northeast	Rupestrian fields, Cerrado	48	37	21	1.3	Fabaceae (10), Malpighiaceae (8), Myrtaceae (4)	Copaifera sabulicola (5)
Coelho et al. (2013b)	Serra do Cabral, MG, Southeast	Rupestrian Fields, Cerrado	47	39	21	1.21	Asteraceae (12), Malpighiaceae (9), Fabaceae (4)	Byrsonima guilleminiana (3)
Costa et al. (2014)	Caitité, BA, Northeast	Caatinga, Cerrado	43	33	17	1.3	Fabaceae (15), Myrtaceae (5)	Bauhinia pulchella (3)
Silva et al. (2015)	Campus Samambaia - UFG, GO, Midwest	Cerrado	42	22	20	1.91	Styracaceae (7), Burseraceae (7), Fabaceae (5)	Styrax pohlii (7), Protium heptaphyllum (7), Siparuna guianensis (4)
Fernandes et al. (1988)	Campus UFMG, Belo Horizonte, MG, Southeast	Cerrado	37	22	11	1.68	Fabaceae (15), Boraginaceae (5)	Copaifera langsdorffii (7), Cordia sellowiana (4)
Urso-Guimarães & Scareli-Santos (2006)	Santa Rita do Passa Quatro, SP, Southeast	Cerrado	36	26	15	1.38	Fabaceae (7), Myrtaceae (5), Annonaceae (4)	Duguetia furfuracea (3), Myrcia bella (3)
Urso-Guimarães et al. (2003)	Delfinópolis, MG, Southeast	Rupestrian fields, Gallery Forest, Cerrado	22	19	16	1.16	Fabaceae (5), Rubiaceae (2),Vochysiaceae (2)	Bauhinia ungulata (2), Chomelia pohliana (2), Qualea parviflora (2)

Figure 2
Insect galls of Parque Nacional da Chapada dos Guimarães, Mato Grosso State, Brazil in host plants indicated. Anacardiaceae. a. Anacardium nannum, b. Tapirira guianensis. Annonaceae. c. Annona dioica, d–e. Annona tomentosa, f–g. Duguetia flagellaris, h–k. Duguetia furfuracea, l–m. Guatteria ferruginea, n. Unonopsis guatterioides. Apocynaceae. o. Aspidosperma subincanum, p–q. Aspidosperma tomentosum, r–s. Aspidosperma verbascifolium, t. Odontadenia lutea. Araceae. u–v. Philodendron sp. Araliaceae. w. Schefflera morototoni. Aristolochiaceae. x–y. Aristolochia sp. Asteraceae. z. Mikania sp., za–zc. Mikania cf. micrantha, zd–zf. Piptocarpha rotundifolia. Bignoniaceae. zg–zi. Anemopaegma glaucum.

Figure 3
Insect galls of Parque Nacional da Chapada dos Guimarães, Mato Grosso State, Brazil in host plants indicated. Bignoniaceae. a. Anemopaegma glaucum. b–c. Pleonotoma sp., d. Bignoniaceae sp. 1, e–g. Bignoniaceae sp. 2, h–i. Bignoniaceae sp. 3, j–k. Bignoniaceae sp. 4. Boraginaceae. l–o. Cordia sellowiana. Burseraceae. p. cf. Tetragastris altissima, q–z. Protium heptaphyllum. Callophylaceae. za–zb. Kielmeyera grandiflora. Caryocaraceae. zc. Caryocar brasiliense. Celastraceae. zd–zg. Peritassa sp. zh. Pristimera celastroides. Chrysobalanaceae. zi. Chrysobalanaceae sp.

Figure 4
Insect galls of Parque Nacional da Chapada dos Guimarães, Mato Grosso State, Brazil in host plants indicated. Chrysobalanaceae. a–b. Parinari obtusifolia. Combretaceae. c–e. Combretum mellifluum, f–h. Terminalia fagifolia, i. Terminalia glabrescens. Connaraceae. j. Connarus suberosus, k–m. Rourea induta. Dilleniaceae n–u. Davilla grandiflora, v–x. Davilla lacunosa. Elaeocarpaceae. y–z. Sloanea sp. Erythroxylaceae. za. Erythroxylum cf. pruinosum. zb. Erythroxylum campestre, zc. Erythroxylum citrifolium, zd–zg. Erythroxylum daphnites. Euphorbiaceae. zh. Bernardia similis, zi. Mabea sp.

Figure 5
Insect galls of Parque Nacional da Chapada dos Guimarães, Mato Grosso State, Brazil in host plants indicated. Euphorbiaceae. a–c. Manihot tripartita, d–e. Jatropha sp., f–g. Maprounea guianensis. Fabaceae. h. Ancistrotropis formula, i–n. Andira cujabensis, o. Andira humilis, p–t. Andira surinamensis, u–w. Andira vermifuga, x. Bauhinia sp. 1, y. Bauhinia sp. 2, z. Bauhinia sp. 3, za. Bauhinia sp. 4, zb. Calliandra sp., zc. Chamaecrista sp., zd–zi. Copaifera depilis.

Figure 6
Insect galls of Parque Nacional da Chapada dos Guimarães, Mato Grosso State, Brazil in host plants indicated. Fabaceae. a. Copaifera depilis, b–d. Hymenaea courbaril, e. Inga disticha, f. Inga leiocalycina, g. Inga vera, h. Machaerium sp., i. Ormosia macrophylla, j. Senegalia sp., k–m. Stryphnodendron adstringens, n–p. Tachigali rubiginosa, q. Tachigali subvelutina. Lauraceae. r–s. Aiouea saligna. Malpighiaceae. t. Alicia macrodisca, u. Byrsonima coccolobifolia, v–w. Byrsonima sericea, x. Diplopterys pubipetala, y–ze. Heteropterys cf. coriacea. Melastomataceae. zf. Macairea radula, zg–zh. Miconia albicans, zi. Miconia rubiginosa.

Figure 7
Insect galls of Parque Nacional da Chapada dos Guimarães, Mato Grosso State, Brazil in host plants indicated. Melastomataceae. a–d. Miconia sp. 1, e–f. Miconia sp. 2, g. Mouriri elliptica, h–i. Tibouchina sp. 1, j. Tococa sp. Meliaceae. k–m. Guarea guidonia, n. Guarea macrophylla subsp. spiciflora. Monimiaceae. o. Mollinedia sp. Moraceae. p. Brosimum lactescens, q. Ficus sp. 1, r–t. Ficus sp. 2. Myrtaceae. u. Eugenia punicifolia, v. Eugenia sp., w–y. Myrcia bella, z–za. Myrcia guianensis, zb. Myrcia sp., zc–zf. Myrcia splendens, zg. Myrcia variabilis. Ochnaceae. zh. Ouratea castaneifolia, zi. Ouratea nana.

Figure 8
Insect galls of Parque Nacional da Chapada dos Guimarães, Mato Grosso State, Brazil in host plants indicated. Ochnaceae. a. Ouratea nana, b. Ouratea riedeliana. Piperaceae. c. cf. Piper dilatatum. Polygonaceae. d. Coccoloba cujabensis. Proteaceae. e. Roupala montana. Rubiaceae. f. Cordiera myrciifolia, g. Cordiera obtusa. h. Rubiaceae sp. Sapindaceae. i. Matayba guianensis, j. Matayba sp. 1, k. Matayba sp. 2, l. Serjania caracasana, m. Serjania matogrossensis, n. Serjania sp., o. Talisia subalbens. Sapotaceae. p. Ecclinusa ramiflora, q. Pouteria ramiflora, r–u. Pouteria torta, v. Pouteria sp. 1, w. Pouteria sp. 2. Simaroubaceae. x–za. Simarouba versicolor. Symplocaceae. zb. Symplocos cf. nitens. Siparunaceae. zc–zh. Siparuna guianensis. zi. Siparuna sp.

Figure 9
Insect galls of Parque Nacional da Chapada dos Guimarães, Mato Grosso State, Brazil in host plants indicated. Smilacaceae. a–b. Smilax brasiliensis, c–d. Smilax fluminensis. Styracaceae. e–g. Styrax sp. Vochysiaceae. h–s. Qualea parviflora, t–u. Vochysia petraea. Unidentified. v. Unidentified sp. 1, w. Unidentified sp. 2, x. Unidentified sp. 3, y. Unidentified sp. 4, z. Unidentified sp. 5, za. Unidentified sp. 6, zb–zd. Unidentified sp. 7, ze. Unidentified sp. 8, zf. Unidentified sp. 9, zg. Unidentified sp. 10, zh. Unidentified sp. 11.

From the insect galls, 91 (30%) of the gall inducers were obtained and identified in 66 host plant species. The gall makers of 218 morphotypes are undetermined because the material collected were empty. In 11 cases the specimens obtained were damaged or with insufficient information to the identification. Among the insect gall inducers, 51% belong to Diptera (N=45), 22.5% to Hymenoptera (N=20), followed by far by Coleoptera (N=6, 6.7%), Hemiptera (N=4, 4.5%) and Thysanoptera (N=2, 2.2%) and Lepidoptera (N=1, 1%). We identified eleven species of Cecidomyiidae: nine gall makers - three species of Lopesia Rübsaamen, two species of Asphondylia Loew and one species of each genus Bruggmannia Tavares, Dasineura Rondani, Stephomyia Tavares and Youngomyia Felt, and two species of the inquiline genus Trotteria Kieffer. Associated fauna and other details are in Table 4. One supplementary gall in Miconia albicans (Sw.) Triana (Melastomataceae) (Fig. 9G) was induced by fungus.

Table 4
Gall makers and associated fauna in galls of Parque Nacional da Chapada dos Guimarães, Mato Grosso, Brazil.

Host plat family	Host plant species	Gall inducers	Associated Fauna
Anacardiaceae	Anacardium nannum A.St.-Hil.*	Diptera, Cecidomyiidae, Asphondyliini, Bruggmannia sp.	not observed
Anacardiaceae	Tapirira guianensis Aubl.	Diptera, Cecidomyiidae, Cecidomyiinae	not observed
Annonaceae	Duguetia furfuracea (A.St.-Hil.) Saff.	Diptera, Cecidomyiidae, Cecidomyiinae	not observed
Annonaceae	Duguetia furfuracea (A.St.-Hil.) Saff.	Hemiptera	not observed
Annonaceae	Duguetia furfuracea (A.St.-Hil.) Saff.	Hymenoptera, Chalcidoidea	not observed
Apocynaceae	Aspidosperma tomentosum Mart.	Unidentified	not observed
Apocynaceae	Aspidosperma verbascifolium Müll.Arg .*	Hemiptera	not observed
Asteraceae	Mikania sp.	Coleoptera	not observed
Asteraceae	Mikania cf. micrantha Kunth	Hymenoptera	not observed
Asteraceae	Mikania cf. micrantha Kunth	Hymenoptera, Chalcidoidea	not observed
Asteraceae	Piptocarpha rotundifolia (Less.) Baker	Diptera, Cecidomyiidae, Cecidomyiinae	Hymenoptera
Asteraceae	Piptocarpha rotundifolia (Less.) Baker	Hymenoptera, Chalcidoidea	not observed
Bignoniaceae	Anemopaegma glaucum Mart. ex DC.*	Coleoptera	not observed
Bignoniaceae	Pleonotoma sp.	not observed	Hymenoptera
Bignoniaceae	Pleonotoma sp.	Thysanoptera, Phlaeothripidae	not observed
Bignoniaceae	Bignoniaceae sp. 1	Unidentified	not observed
Bignoniaceae	Bignoniaceae sp. 2	Diptera, Cecidomyiidae, Cecidomyiinae	Hymenoptera
Bignoniaceae	Bignoniaceae sp. 3	Hymenoptera, Chalcidoidea	not observed
Bignoniaceae	Bignoniaceae sp. 3	Coleoptera	Hymenoptera, Chalcidoidea
Bignoniaceae	Bignoniaceae sp. 4	Diptera, Cecidomyiidae, Cecidomyiinae	Hymenoptera
Bignoniaceae	Bignoniaceae sp. 4	Diptera, Cecidomyiidae, Cecidomyiinae	not observed
Boraginaceae	Cordia sellowiana Cham.	Diptera, Cecidomyiidae, Asphondyliini, Asphondylia sp.2	Hymenoptera, Chalcidoidea
Burseraceae	Protium heptaphyllum (Aubl.) Marchand	Diptera, Cecidomyiidae, Cecidomyiinae	Hymenoptera
Burseraceae	Protium heptaphyllum (Aubl.) Marchand	Diptera, Cecidomyiidae, Cecidomyiinae	not observed
Burseraceae	Protium heptaphyllum (Aubl.) Marchand	Diptera, Cecidomyiidae, Cecidomyiinae	Hymenoptera, Encyrtidae
Burseraceae	Protium heptaphyllum (Aubl.) Marchand	Hymenoptera, Chalcididae	not observed
Celastraceae	Peritassa sp.	Diptera, Cecidomyiidae, Cecidomyiinae	Diptera, Cecidomyiidae, Trotteria sp.1
Celastraceae	Peritassa sp.	Hymenoptera, Chalcidoidea	Psocoptera
Celastraceae	Peritassa sp.	Hymenoptera, Chalcidoidea	not observed
Celastraceae	Peritassa sp.	Hymenoptera, Chalcidoidea	not observed
Chrysobalanaceae	Parinari obtusifolia Hook.f.*	Diptera, Cecidomyiidae, Cecidomyiinae	not observed
Chrysobalanaceae	Parinari obtusifolia Hook.f.*	Diptera, Cecidomyiidae, Cecidomyiinae, Lasiopteridi	Hymenoptera
Combretaceae	Terminalia glabrescens Mart.*	Diptera, Cecidomyiidae, Cecidomyiinae	Hymenoptera
Connaraceae	Rourea induta Planch.	Diptera, Cecidomyiidae, Cecidomyiinae	Hemiptera
Dilleniaceae	Davilla grandiflora A.St.-Hil.*	Diptera, Cecidomyiidae, Cecidomyiinae	not observed
Dilleniaceae	Davilla lacunosa Mart.*	Diptera, Cecidomyiidae, Cecidomyiinae	not observed
Elaeocarpaceae	Sloanea sp.	Unidentified	not observed
Erythroxylaceae	Erythroxylum daphnites Mart.	Diptera, Cecidomyiidae, Cecidomyiinae	not observed
Euphorbiaceae	Manihot tripartita (Spreng.) Müll.Arg.	Diptera, Cecidomyiidae, Cecidomyiinae	not observed
Euphorbiaceae	Maprounea guianensis Aubl.	Diptera, Cecidomyiidae, Cecidomyiinae	not observed
Fabaceae	Andira cujabensis Benth.	Hymenoptera	not observed
Fabaceae	Andira humilis Mart. ex Benth.	Diptera, Cecidomyiidae, Lopesiini, Lopesia andira Garcia et al., 2017	not observed
Fabaceae	Andira surinamensis (Bondt) Splitg. ex Amshoff	Unidentified	not observed
Fabaceae	Andira surinamensis (Bondt) Splitg. ex Amshoff	Unidentified	not observed
Fabaceae	Andira vermifuga (Mart.) Benth.	Diptera, Cecidomyiidae, Cecidomyiinae	Hymenoptera, Chalcidoidea
Fabaceae	Andira vermifuga (Mart.) Benth.	Diptera, Cecidomyiidae, Lopesiini, Lopesia chapadensis Garcia & Urso-Guimarães, 2018	not observed
Fabaceae	Bauhinia sp. 4	Unidentified	not observed
Fabaceae	Calliandra sp.	Unidentified	Unidentified
Fabaceae	Copaifera depilis Dwyer	Diptera, Cecidomyiidae, Cecidomyiinae	Hymenoptera, Chalcidoidea
Fabaceae	Copaifera depilis Dwyer	Diptera, Cecidomyiidae, Cecidomyiinae	not observed
Fabaceae	Copaifera depilis Dwyer	Hymenoptera	not observed
Fabaceae	Copaifera depilis Dwyer	Unidentified	Unidentified
Fabaceae	Hymenaea courbaril L.	Diptera, Cecidomyiidae, Cecidomyiinae	not observed
Fabaceae	Inga disticha Benth.	Diptera, Cecidomyiidae, Cecidomyiinae	Hymenoptera, Chalcidoidea
Fabaceae	Inga leiocalycina Benth.*	Hemiptera, Cicadelidae	not observed
Fabaceae	Ormosia macrophylla Benth.*	Hymenoptera, Chalcidoidea	not observed
Fabaceae	Tachigali subvelutina (Benth.) Oliveira-Filho*	Diptera, Cecidomyiidae, Cecidomyiinae	Thysanoptera
Malpighiaceae	Alicia macrodisca (Triana & Planch.) W.R.Anderson*	Diptera, Cecidomyiidae, Cecidomyiinae	not observed
Malpighiaceae	Byrsonima sericea DC.	Unidentified	not observed
Malpighiaceae	Diplopterys pubipetala (A.Juss.) W.R.Anderson & C.C.Davis	Diptera, Cecidomyiidae, Cecidomyiinae	not observed
Malpighiaceae	Heteropterys cf. coriacea A. Juss.*	Diptera, Cecidomyiidae, Cecidomyiinae	not observed
Malpighiaceae	Heteropterys cf. coriacea A. Juss.*	Hymenoptera, Pteromalidae	Psocoptera
Melastomataceae	Miconia sp. 1	Diptera, Cecidomyiidae, Cecidomyiinae	not observed
Melastomataceae	Macairea radula (Bonpl.) DC.	Lepidoptera, Coleophoridae, Palaeomystella oligophaga Becker & Adamski, 2008	not observed
Melastomataceae	Tibouchina sp.	Unidentified	not observed
Meliaceae	Guarea guidonia (L.) Sleumer	Hymenoptera, Chalcidoidea	not observed
Moraceae	Ficus sp. 2	Coleoptera	not observed
Myrtaceae	Myrcia guianensis (Aubl.) DC.	Hymenoptera, Chalcidoidea	not observed
Myrtaceae	Myrcia splendens (Sw.) DC.	Diptera, Cecidomyiidae, Cecidomyiinae	not observed
Piperaceae	cf. Piper dilatatum Rich.	Hymenoptera, Chalcidoidea	not observed
Rubiaceae	Rubiaceae sp.	Hymenoptera, Chalcidoidea	not observed
Sapindaceae	Serjania caracasana (Jacq.) Willd.	Diptera, Cecidomyiidae, Dasineurini, Dasineura sp.	not observed
Sapindaceae	Serjania matogrossensis Ferrucci & Acev.-Rodr.*	Diptera, Cecidomyiidae, Cecidomyiinae	not observed
Sapindaceae	Matayba guianensis Aubl.	Diptera, Cecidomyiidae,Lopesiini, Lopesia mataybae Garcia & Urso-Guimarães, 2018	not observed
Sapotacae	Pouteria torta (Mart.) Radlk.	Diptera, Cecidomyiidae, Youngomyia matogrossensis Proença & Maia, 2019	not observed
Sapotaceae	Pouteria torta (Mart.) Radlk.	Diptera, Cecidomyiidae, Asphondyliini, Stephomyia sp.	Diptera, Cecidomyiidae, Trotteria sp.2
Simaroubaceae	Simarouba versicolor A.St.-Hil.*	Coleoptera, Curculionidae, Scolytinae	not observed
Simplocaceae	Symplocos cf. nitens (Pohl) Benth.*	Diptera, Cecidomyiidae, Cecidomyiinae	not observed
Siparunaceae	Siparuna guianensis Aubl.	Diptera, Cecidomyiidae, Asphondyliini, Asphondylia sp.1	not observed
Siparunaceae	Siparuna guianensis Aubl.	Thysanoptera, Phlaeothripidae	Coleoptera, Curculionidae
Smilacaceae	Smilax brasiliensis Spreng.	Diptera, Cecidomyiidae, Cecidomyiinae	not observed
Smilacaceae	Smilax fluminensis Steud.	Unidentified	Diptera, Phoridae
Styracaceae	Styrax sp.	Hymenoptera, Chalcidoidea, Pteromalidae	not observed
Vochysiacece	Qualea parviflora Mart	Diptera, Cecidomyiidae, Cecidomyiinae	not observed
Vochysiacece	Qualea parviflora Mart	Diptera, Cecidomyiidae, Cecidomyiinae	not observed
Vochysiacece	Qualea parviflora Mart	Hymenoptera	not observed
Unidentified	Unidentified sp. 1	Hemiptera	not observed
Unidentified	Unidentified sp. 4	Hymenoptera	not observed
Unidentified	Unidentified sp. 10	Diptera, Cecidomyiidae, Cecidomyiinae	not observed
Unidentified	Unidentified sp. 11	Coleoptera	not observed

Aiouea Aubl., Alicia W.R.Anderson, Ancistrotropis A. Delgado, Bernardia Houst. ex Mill., Peritassa Miers, Pleonotoma Miers, Pristimera Miers are new records as a host plant for insect galls. The same occurs with 38 host plant species (Table 2). Two host plant species are listed in the Red List of Threatened Species of the International Union for Conservation of Nature in the category “Threatened”: Vochysia petraea Warm. as “Endangered” and Talisia subalbens (Mart.) Radlk. as “Vulnerable”.

Additionally, Bernardia similis Pax and K.Hoffm and Ormosia macrophylla Benth. are registered for the first time in Mato Grosso State’s flora (Flora do Brasil 2020).

Discussion

Even though comparisons of this study with others are hampered both, by the diversity of sampling methods used and by the presence of other phytophysiognomies than Cerrado strict sensu, our results allow us to state that the Parque Nacional da Chapada dos Guimarães harbors the highest number of gall morphotypes and the second-highest gall morphotypes average per plant species found in the Cerrado hitherto (Araújo et al. 2019, Cintra et al. 2020). The number of morphotypes (295) and the average of morphotypes per plant species (2.1) are comparable with those found in the Parque Nacional de Silvania (GO) (Bergamini et al. 2017), with similar phytophysiognomies sampled (Gallery Forest and Cerrado strict sensu). These authors found 186 gall morphotypes and an average of 3.0 gall morphotypes per species, representing the highest average recorded in the Cerrado Biome (Bergamini et al. 2017). A similar pattern was found in studies conducted in Campos Rupestres (rupestrian grasslands) in the Cadeia do Espinhaço (Carneiro et al. 2009) and in the Vale do Rio Jequitinhonha (Fernandes et al. 1997) (both in Minas Gerais State), with 241 and 236 gall morphotypes, respectively and an average of 1.7 morphotypes per species each.

Our results corroborate the hypothesis that environmental stress (Fernandes & Price 1988) would justify the high richness of gall morphotypes in these phytophysiognomies. Indeed, considering that gall morphotypes are extended phenotypes of their inducers (Abrahamson & McCrea 1986), it also justifies gall makers’ high richness in scleromorphic vegetation. The plants of practically all phytophysiognomies in Cerrado have adaptations to soil poverty and hydric stress, recognized in high concentrations of defense compounds, especially tannins. This higher concentration of chemical compounds provides the galls inducers defense against predators and pathogens (Fernandes & Price 1992). Allied to this, manipulating the nutritional resources in very young vegetable tissue (Fernandes et al. 2011) allows the gallers larvae access to nutrients inaccessible to other herbivores.

Fabaceae, Bignoniaceae, Melastomataceae, Myrtaceae, Burseraceae, Malpighiaceae, and Vochysiaceae are the richer families in species in the Parque Nacional da Chapada dos Guimarães, which corroborates in part the hypothesis of the predominance of gall morphotypes in the families with the most remarkable species richness (Southwood 1960, 1961, Santos-Silva & Araújo 2020). Also confirm the predominance of these families in the data compiled by Cintra et al. (2020). Fabaceae is among the five richest families in gall morphotypes in 20 of the 22 studies in Cerrado phytophysiognomies, Myrtaceae in 11, and Malpighiaceae in 10 (Araújo et al. 2019). On the other hand, Vochysiaceae is a super host family case because, in just two species, we found a high number of morphotypes (12), contributing to increasing the total number of gall morphotypes in the sampled area. This family was also mentioned as a super host in an area of Cerrado in Goiás state (Araújo 2011). Bignoniaceae was referred to as a rich family in gall morphotypes in Pantanal (Julião et al. 2002; Urso-Guimarães et al. 2017), but it is among the super host families in the Cerrado for the first time. In the compilation of 32 areas of Cerrado, Cintra et al. (2020) found 20 gall morphotypes against 16 morphotypes found in this study. These results may be related to the fact that all Bignoniaceae species sampled in this study are climbing plants, which are not frequently sampled in studies about galling insects. It shows the importance of sampling all vegetation strata to understand the galling insects’ distribution in their hosts.

From the richest plant genera in gall morphotypes found in Parque Nacional da Chapada dos Guimarães, Andira Lam. and Myrcia DC. are richer in species, and Davilla Vand. and Protium Burm.f. are super host species (Table 3). Myrcia appears as one of the richest genera in the Cerrado records in Cintra et al. (2020). But Andira, Davilla, and Protium are referred as morphotype richest genera for the first time to Cerrado biome.

Protium heptaphyllum (Aubl.) Marchand, Qualea parviflora Mart, Davilla grandiflora A.St.-Hil. and Copaifera depilis Dwyer were the richest host species in the studied area (Table 3), being D. grandiflora reported as super host of gall morphotypes for the first time.

Leaves are the most abundant resource in any biome. The scleromorphic plants in the Cerrado biome have low leaf abscission rates (Fernandes & Price 1988; Price et al. 1998; Cuevas-Reyes et al. 2004), so it is natural that most galls occurred on leaves. The shapes more common, lenticular and globoid, are predominant because they favor the reduction of water loss, mainly on leaf galls, compared to more bulky shapes such as cylindrical and conical. Together with the color green and glabrous galls, these predominant characteristics are a pattern also found in precedent surveys in Cerrado phytophysiognomies (Araújo et al. 2019).

The Cecidomyiidae was the predominant family among the gall inducers, as found in surveys worldwide (Espírito-Santo & Fernandes 2007).

All plant species are new as host to insect galls to the state of Mato Grosso, except for Andira cujabensis Benth., A. vermifuga (Mart.) Benth., Matayba guianensis Aubl. (Garcia et al. 2017, Garcia & Urso-Guimarães 2018) and Pouteria torta (Mart.) Radlk. (Proença & Maia 2019). Eight percent of the 84 genera found in this inventory are new records as a host plant for insect galls, and 27% of the total host plant species sampled in Parque Nacional da Chapada dos Guimarães are new as host for galls. Among the new registers, Bernardia similis Pax & K.Hoffm and Ormosia macrophylla Benth., also are registered for the first time in the flora of Mato Grosso State (Flora do Brasil 2020). That reinforces the importance of multidisciplinary studies like this, founding new points of occurrence for plant species and the associated fauna.

The two species classified as threatened, Vochysia petraea Warm. and Talisia subalbens (Mart.) Radlk., are endemic of Cerrado in Mato Grosso State (Shimizu et al. 2020, Acevedo-Rodríguez 2015). Currently, the state is one of Brazil’s agricultural frontiers to soybean plantation areas, meaning that both plant species and their interactions (e.g., galls and associated fauna) are also threatened with extinction.

Studies like this collaborate to increase the knowledge about a rich and undescribed fauna. This fauna begins to be documented from its extended phenotype - the gall - which remains on the host plant even after the emergence of the galler. The taxonomic studies’ continuity in the areas registered here is fundamental to identify and describe the inducers and the associated fauna. Before the SISBIOTA - Diptera Brasil Program (2010-2015), this study is part, only two species of Cecidomyiidae, the principal inducer of galls in the world, had the occurrence registered in this Mato Grosso State, Termitomastus leptoproctus Silvestri, 1901 and Asphondylia tuiuiu Urso-Guimarães & Amorim, 2002. Currently, four new species found in this survey have been described - Lopesia andiraeGarcia et al., 2017, L. chapadensis Garcia & Urso-Guimarães, 2018, L. mataybae Garcia & Urso-Guimarães, 2018, and Youngomyia matogrossensisProença & Maia, 2019. Another five are under the description (Asphondylia spp., Bruggmannia sp., Dasineura sp. and Stephomyia sp.). Even with the efforts addressed during this period, gall inducers’ fauna remains poorly known because they are highly diversified. More investigation focused on finding all stages of the life cycle of gall morphotypes documented in this study is necessary to understand this fauna’s richness, including the other insects from the associated guild.

Acknowledgements

MVUG acknowledges the Conselho Nacional de Desenvolvimento Científico e Tecnológico (Proc. CNPq 563256/2010-9) and Fundação de Amparo à Pesquisa do Estado de São Paulo (Proc. FAPESP 10/52314-0) for the support to the field works under the SISBIOTA - Diptera Brasil Program. The authors also thank J. Semir - in memorian, J. Tamashiro, G.H. Shimizu, A. F. Versiane and A.V. Scatigna (IB/UNICAMP), R.B. Pinto (UFG) and M. Monge (UFU) for invaluable help in plant species identification.

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Publication Dates

• Publication in this collection
  19 July 2021
• Date of issue
  2021

History

• Received
  08 Jan 2021
• Reviewed
  09 June 2021
• Accepted
  11 June 2021