Insect galls of a protected remnant of the Atlantic Forest tableland from Rio de Janeiro State (Brazil)

ABSTRACT

Insect galls of a protected remnant of the Atlantic Forest tableland from Rio de Janeiro State (Brazil): Galling insects in Rio de Janeiro state are known by their great diversity, despite most of the surveys have been done in restinga. This paper investigated the insect galls from a remnant of Atlantic Forest located in São Francisco de Itabapoana municipality, Rio de Janeiro state, Brazil. The galling insect fauna was surveyed from March, 2013 to April, 2014 at the Estação Ecológica Estadual de Guaxindiba. 143 gall morphotypes were found in 31 plant families, 60 genera and 82 species. Fabaceae, Myrtaceae and Sapindaceae were the main host families, being Trichilia, Tontelea and Eugenia the main host genera. Most galls occured on leaves, with globose shape, green and glabrous. Diptera (Cecidomyiidae), Hemiptera, and Lepidoptera were the inducing orders and the associated fauna comprised parasitoids (Hymenoptera), inquilines (Lepidoptera, Coleoptera, and Hemiptera: Coccoidea), successors (Psocoptera, Collembola and Acari), and predators (Pseudoscorpiones). Three plant genera and nine plant species are recorded for the first time as host of galls in Brazil. All the records are new to the municipality, and the distribution of 15 galling species is extended to the North of the state of Rio de Janeiro.

Keywords:
Cecidomyiidae; Gall-inducing insects; Guaxindiba; Southeast Region

Introduction

The Atlantic Forest comprises several phytophysiognomies, one of them is the lowland semideciduous seasonal rainforest, also called “Tableland Forest” or “Tabuleiro Forest”. This physiognomy is distinguished from the other Atlantic Forest formation by occupying an extensive plain or coastal “tabuleiro” of Tertiary origin. The botanical species are distributed along a climatic gradient from the coast to the interior (Rizzini, 1979) and the interior generally presents low density of crawling vegetation and the occurrence of epiphyte species (Ruschi, 1950). The plants sclerophylly is other distinguishing characteristic (Rizzini, 1979).

Insect gall inventories have been developed in Atlantic Forest areas of the state of Rio de Janeiro (Maia, 2013a,b; Rodrigues et al., 2014), as well as in other Brazilian states of the Southeastern Region, such as São Paulo (Maia et al., 2008), Espírito Santo (Bregonci et al., 2010; Maia et al., 2014), and Minas Gerais (Maia, 2013b, 2014). These inventories focused mainly on restingas, but ombrophilous forest and altitude fields have been also investigated. The restinga inventories totaled 476 gall morphotypes, which are induced by Diptera, Lepidoptera, Hemiptera, Coleoptera, Thysanoptera, and Hymenoptera species, being Cecidomyiidae (Diptera) the most frequent galling taxon (Maia, 2013a). The ombrophilous forest and altitude fields together totaled 518 morphotypes and include the same galling insect taxa. No study has been performed in Tabuleiro Forest.

The galling insects are considered the one of the most sophisticated herbivores, as they are able to control and redirect the host plant to their advantage (Abrahamson and Weis, 1997; Shorthouse et al., 2005). They induce galls, abnormal increases in the number and/or size of plant cells resulting in the formation of a symmetrical structure(s) on one or more organs of a host plant (Mani, 1964; Raman, 2007).

The Estação Ecológica Estadual de Guaxindiba (EEEG) (21°24′28″S-41°5′33″W) is situated in the northeast portion of the state of Rio de Janeiro, in the municipality of São Francisco de Itabapoana, and is the biggest Tabuleiro Forest remnant of the state. The EEEG spreads over 3,260 hectares, but the forest is distributed along a stretch of 12,000 hectares. It hosts rare and typical plants of Tabuleiro Forest, such as Paratecoma peroba Kuhlm (Bignoniaceae), commonly known as “ipê peroba”, as well as plants of high economic value, namely, Aspidosperma polyneurum Müll. Arg. (Apocynaceae), Tabebuia spp.Gomes ex DC (Bignoniaceae), Copaifera lucens Dwyer (Fabaceae), and Cariniana legalis (Mart.) Kuntze (Lecythidaceae). It is internationally known as a world heritage site by UNESCO, being characterized as core area of Atlantic Forest Biosphere Reserve (Inea, 2015).

The present study represents the first contribution to the knowledge of the galling insect fauna from an area of Tabuleiro Forest.

Material and methods

The EEEG was investigated for insect galls during March, May, July, and September 2013, and April, 2014, totalizing five scientific expeditions. The vegetation of four trails was examined: Marcelo Trindade (S21° 24′55″-WO41° 04′38″), Colégio Agrícola (S21° 23′56.1″-WO4° 04′44.0″), Vera (S21° 24′26″-WO41° 04′59″), and Abelha (S21°24′40.7″-WO41°04′53.7″) in each expedition, as well as in the surrounding area of the Charco (S21°24′59.7″-W041°04′35.5″). Each trail and the Charco area were investigated by four hours per expedition. All plant organs were examined, except for the subterraneous roots. Galled plants were pressed for identification and preservation. Dried plants were deposited in the herbarium of the Universidade Federal Rural da Amazônia (UFRAM). The plants were identified by Dr. Gracialda Costa Ferreira (UFRAM), according to APGIII. All botanic names were updated based on the Lista de Espécies da Flora do Brasil (2015), and each species was classified as native or endemic of Brazil based on the same site. All gall morphotypes were photographed, using a digital camera. Each morphotype was characterized based on shape, plant organ, color, presence or absence of trichomes, number of internal chambers, and inducing insect, as in other Brazilian inventories (Maia, 2013b, 2014; Maia et al., 2014). For each gall morphotype, previous records from other Brazilian inventories are provided.

To obtain the galling insects, each gall morphotype was individually kept in labeled plastic pots layered at the bottom with damp cotton and covered by fine screening. All pots were checked daily for emergence. The specimens were preserved in 70% alcohol and later mounted on microscope slides following the method in Gagné (1994). The gall midges were identified by VCM based on the gall morphology, host plant and original descriptions. All material is deposited in the entomological collection of Museu Nacional/Universidade Federal do Rio de Janeiro (MNRJ).

Results and discussion

A total of 143 gall morphotypes were found in 31 plant families, 60 genera and 82 species. The average number of gall morphotypes per plant species was 1.74. In other Atlantic Forest inventories, the gall richness has ranged from 36 (Ilha Grande, Angra dos Reis, RJ) to 265 (Santa Teresa, ES), but similar values were recorded in Marambaia, RJ (n = 147) and São Tomé das Letras, MG (n = 152), the former comprises restinga areas and the latter forests and altitudinal fields. This range can be explained by different collecting efforts as well as by differences in plant richness.

Fabaceae was the botanical family with the greatest number of galled species (n = 12) and the highest richness of galls (n = 28), followed by Myrtaceae and Sapindaceae, both with 13 gall morphotypes in eight and four galled plant species, respectively. Bignoniaceae were the fourth family in number of galled species (n = 11), followed by Meliaceae (n = 9). The other families presented four or less galled species and nine or less gall morphotypes (Table 1).

Table 1
Richness of gall morphotypes by plant families in Estação Ecológica Estadual de Guaxindiba (São Francisco de Itabapoana, RJ, Brazil).

Galled families	Number of galled genera	Number of galled species	Number of gall morphotypes
Anacardiaceae	02	02	04
Annonaceae	01	01	01
Apocynaceae	01	01	01
Bignoniaceae	05	07	11
Boraginaceae	01	01	03
Burseraceae	01	01	04
Celastraceae	01	01	02
Chrysobalanaceae	01	01	01
Combretaceae	01	01	01
Erythroxylaceae	01	01	01
Euphorbiaceae	03	03	03
Fabaceae	12	12	28
Hippocrateaceae	01	02	07
Hypericaceae	01	01	01
Malpighiaceae	03	03	06
Malvaceae	01	01	02
Meliaceae	01	09	09
Moraceae	01	02	03
Myrtaceae	04	08	13
Nyctaginaceae	01	02	04
Ochnaceae	01	01	01
Olacaceae	01	01	02
Peraceae	01	01	01
Phyllantheaceae	01	01	02
Rubiaceae	01	01	01
Rutaceae	02	02	06
Salicaceae	01	03	03
Sapindaceae	03	04	13
Sapotaceae	02	03	05
Smilacaceae	01	01	01
Verbenaceae	01	02	01
Total	60	82	143

In several Brazilian inventories, Fabaceae and Myrtaceae have been indicated as the richest plant families in number of gall morphotypes (Santos et al., 2011b; Costa et al., 2014; Maia et al., 2014). Sapindaceae and Bignoniaceae are commonly present in these inventories, but not as super host families.

The genera with the highest gall richness were Trichilia P. Browne (Meliaceae) with nine morphotypes, Tontelea Miers (Hippocrateaceae), Eugenia L. (Myrtaceae), Serjania Mill. (Sapindaceae) each with seven morphotypes, Albizia Durazz. (Fabaceae) (Meliaceae) and Machaerium Pers. with six gall morphotypes. Among them, only Eugenia was already cited as super host genus in Brazilian inventories (Maia et al., 2014).

Protium heptaphyllum (Aubl.) Marchand (Burseraceae) presented the highest number of gall morphotypes (n = 4) among the identified plant species, but it cannot be considered as a super host, because four other plants (identified only at genus level) showed six or seven morphotypes.

Among the host plants, 11 are endemic of Brazil: Erythroxylum pauferrense Plowman (Erythroxylaceae), Eugenia bunchosiifolia Nied. (Myrtaceae), Manilkara subsericea (Mart.) Dubard. (Sapotaceae), Ouratea cuspidata (A. St.-Hil.) Engl. (Ochnaceae), Paullinia racemosa Wawra, Paullinia weinmanniifolia Mart., Matayba juglandifolia (Cambess.) Radlk. (Sapindaceae), Stigmaphyllon lalandianum A. Juss. (Malpighiaceae), Neoraputia alba (Nees & Mart.) Emmerich ex Kallunki (Rutaceae), Smilax kukrovii Griseb. (Smilacaceae), and Trichilia elegans A. Juss. (Meliaceae). The others are native. No exotic plant species was found as galls host in EEEG.

Among the endemic plants, T. elegans, P. racemosa, and P. weinmanniifolia have the widest geographical distribution in Brazil. The first has been recorded in Acre, Pará (North Region), Bahia, Ceará, Maranhão (Northeast Region), Distrito Federal, Goiás, Mato Grosso do Sul, Mato Grosso (Midwest Region), Espírito-Santo, Minas Gerais, Rio de Janeiro, São Paulo (Southeast Region), Paraná, Rio Grande do Sul, and Santa Catarina (South Region); the second in Pará (North Region), Alagoas, Bahia, Ceará, Maranhão, Paraíba, Pernambuco, Rio Grande do Norte (Northeast Region), Espírito Santo, Minas Gerais, Rio de Janeiro and São Paulo (Southeast Region); the third in Alagoas, Bahia, Paraíba, Pernambuco, Rio Grande do Norte and Sergipe (Northeast Region), Espírito Santo and Rio de Janeiro (Southeast Region). M. juglandifolia occurs in Bahia (Northeast Region), Goiás (Midwest Region), Minas Gerais, Rio de Janeiro and São Paulo (Southeast Region). N. alba is restricted to Bahia, Espírito Santo, Minas Gerais and Rio de Janeiro. E. bunchosiifolia occurs only in the Southeast (Rio de Janeiro and São Paulo) and South regions (Paraná); M. sericea too (in Espírito Santo, Minas Gerais, Rio de Janeiro, São Paulo, Paraná and Santa Catarina). S. lalandianum has a more restricted distribution, which includes only the Southeast Region, and E. pauferrense is restricted to a single state, Paraíba, in the Northeast Region (Lista de Espécies da Flora do Brasil, 2015). So, this is the first record of E. pauferrense in the Southeast Region.

The endemic plants host 19 gall morphotypes. As the gallers are species-specific and monophagous, these 19 morphotypes can be considered as endemic too. Among them, only two morphotypes were already known (on P. weinmaniifolia and Ouratea cuspidata). The others (n = 17) represent new gall morphotypes.

Three plant genera and nine plant species are recorded for the first time as host of galls in Brazil: Albizia Durazz., Tontelea Miers. (Hippocrateaceae), Metrodorea A. St.-Hil. (Rutaceae), Martinella obovata (Kunth) Bureau & K. Schum (Bignoniaceae), Erythroxylum pauferrense Plown (Erythroxylaceae), Pachystroma longifolium (Nees.) I. M. Johnst (Euphorbiaceae), Chloroleucon acacioides (Ducke) Barneby & J. W. Grimes, Trichilia rubra C. DC. (Meliaceae), Eugenia bunchosiifolia Nied. (Myrtaceae), Neoraputia alba (Nees & Mart.) Emmerich ex Kallunki (Rutaceae), Matayba juglandifolia (Cambess.) Radlk. (Sapindaceae), and Smilax krukovii A. C. Sm. (Smilacaceae).

Galls were found on leaves (petiole, veins and leaf surface), stems, tendrils, buds, flower buds and inflorescence. Leaves comprised the greatest richness of gall morphotypes (n = 101) (Table 2). This result represents a global pattern pointed by Felt (1940) and confirmed in several inventories (Maia et al., 2014). The majority of the galls showed plant organ especificity (n = 134). This specificity is cited by several authors (Dreger-Jauffret and Shorthouse, 1992; Floate et al., 1996).

Table 2
Number of insect gall morphotypes per plant organs in Estação Ecológica Estadual de Guaxindiba (São Francisco de Itabapoana, RJ, Brazil).

Plant organs	Number of gall morphotypes
Leaf	101
Stem	17
Bud	13
Inflorescence or flower bud	02
Fruit	01
Tendril + leaf (vein)	01
Petiole + stem	02
Stem + tendril	01
Stem + leaf (vein)	01
Tendril + leaf (vein) + petiole + stem	04

The majority of the morphotypes were globose, glabrous and one-chambered, as in all other Brazilian inventories (Table 3) (Maia et al., 2014). Only 7% (n = 10) presented trichomes or micropubescence; 5.5% were multi-chambered (n = 8), two gall morphotypes (1.4%) had one or more internal chamber and a single morphotype was massive (without chamber) (probably the gall is still young). There was an evident predominance of green (n = 87) and brown (n = 46) galls, the colors of the most galled plant organs (leaves and stem, respectively). But, yellow (n = 2) and reddish (n = 3) galls were also found. In four morphotypes, the color varied (green, white or red) and this variation was not related to the gall maturity, as young and mature galls presented both colors. These colors are usually mentioned in Brazilian inventories, as well as the predominance of green and brown colors (Maia et al., 2014).

Table 3
Number of insect gall morphotypes per shapes in Estação Ecológica Estadual de Guaxindiba (São Francisco de Itabapoana, RJ, Brazil).

Shapes	Number of gall morphotypes
Globose	38
Fusiform	36
Conical	20
Circular	18
Roll	11
Cylindrical	11
Ovoid	04
Discoid	02
Circular-globose	01
Fold	01
Kidney-shaped	01

About 32% of the gallers (n = 46) were identified at least at order category. The remaining inducers were not identified by three reasons: (1) the galls were already empty, (2) two or more different dwellers were obtained from the same gall and their food habit could not be determined and (3) only parasitoid wasps were obtained. Among the identified gallers, three insect orders were represented: Diptera (Cecidomyiidae), Hemiptera, and Lepidoptera, with a clear predominance of the first (Table 4). Cecidomyiidae are in fact the main galling taxon throught the world (Felt, 1940).

Table 4
Number of insect gall morphotypes per galling insect order in Estação Ecológica Estadual de Guaxindiba (São Francisco de Itabapoana, RJ, Brazil).

Insect order	Number of gall morphotypes
Diptera	39
Hemiptera	06
Lepidoptera	01
Not determined	97

All gall records are new to São Francisco de Itabapoana and the geographical distribution of 15 galling species is extended to the North of the state of Rio de Janeiro: Calophya terebinthifoliiBurckhardt and Basset, 2000 (Psyllidae, Hemiptera), Asphondylia cf. cordiaeMöhn, 1959, Bruggmannia acaudataMaia, 2004a,b, Bruggmanniella byrsonimaeMaia and Couri, 1992, Bruggmannia elongataMaia and Couri, 1993, Bruggmanniella maytenuseMaia and Couri, 1992, Bruggmannia robustaMaia and Couri, 1993, Cordiamyia globosaMaia, 1996, Dactylodiplosis heptaphylliMaia, 2004a,b, Dasineura byrsonimaeMaia, 2010, Dasineura myrciariaeMaia, 1993, Iatrophobia brasiliensisRübsaamen, 1916, Mayteniella distincta Maia, 2001, Neolasioptera sp., and Paulliniamyia ampla Maia, 2001 (Cecidomyiidae).

The most common gall shapes were globose (n = 39) and fusiform (n = 36), as in other Brazilian inventories (Maia et al., 2014). But other shapes were verified, such as conical, cylindrical, circular, ovoid, among others.

The associated fauna comprised parasitoids (Hymenoptera), inquilines (Lepidoptera, Coleoptera and Hemiptera: Coccoidea), successors (Psocoptera, Collembola and Acari), and predators (Pseudoscorpiones) (Table 5). Hymenoptera were the most common, being obtained from 21 gall morphotypes, whereas the others were obtained from two or one morphotype only. All of these taxa have already been recorded as associated fauna (Maia, 2001a; Maia and Fernandes, 2004). Nevertheless, some of them are very rare, as pseudoscorpion in galls (Maia, 2001a). In Brazil, only three records of pseudoscorpions in galls are known: Novohorus sp. 1 (Olpiidae) in galls of Stephomyia rotundifoliorum Maia, 1994 (Cecidomyiidae) on Eugenia astringens Camb. (Myrtaceae) in Maricá (RJ), Novohorus sp. 2 in galls of Houardodiplosis rochae Tavares, 1925 (Cecidomyiidae) on Combretus leprosum Mart. (Combretaceae) in Fortaleza (Ceará), and a not determined species in stem galls of Myrcia tomentosa (Aubl.) DC. (Myrtaceae) in Caetité (Bahia) (Maia, 2001a, 2002; Costa et al., 2014).

Table 5
Arthropod fauna associated with insect galls in Estação Ecológica Estadual de Guaxindiba (São Francisco de Itabapoana, RJ, Brazil).

Family	Host Plant	Galler	Gall morphotype	Associated fauna	Guild	Figure
Anacardiaceae	Schinus terebinthifolius	Not determined	Globose stem gall	Acarina	successor	2
Bignoniaceae	Bignonia sp. 1	Cecidomyiidae	Stem, vein, petiole, tendril swelling	Hymenoptera	parasitoid	7
	Martinella obovata	Cecidomyiidae	Stem, vein, petiole, tendril swelling	Hymenoptera	parasitoid	11
	Pyrostegia sp.	Cecidomyiidae	Conical leaf gall	Hymenoptera	parasitoid	12
	Bignoniaceae sp. 1	Cecidomyiidae	Fusiform vein gall	Hymenoptera	parasitoid	14
Erythroxylaceae	Erytyhroxylum pauferrense	Not determined	Conical leaf gall	Hymenoptera	parasitoid	20
Fabaceae	Acacia sp.	Not determined	Stem swelling	Hymenoptera	parasitoid	25
	Acacia sp.	Not determined	Bud gall	Hymenoptera	parasitoid	26
	Albizia sp.	Cecidomyiidae	Circular leaf gall	Acarina	successor	29
	Machaerium sp.	Not determined	Globose leaf gall	Hymenoptera	parasitoid	43
	Machaerium sp.	Not determined	Bud gall	Hymenoptera	parasitoid	45
Hippocrateaceae	Tontelea sp. 1	Not determined	Stem swelling	Baridinae (Coleoptera, Curculionidae)	inquiline	56
Hypericaceae	Hypericaceae sp.	Not determined	Conical leaf gall	Hymenoptera	parasitoid	59
Meliaceae	Trichilia elegans	Not determined	Stem swelling	Hymenoptera	parasitoid	67
	Trichilia sp. 3	Not determined	Stem swelling	Hymenoptera	parasitoid	71
	Trichilia sp. 7	Not determined	Stem swelling	Hymenoptera	parasitoid	75
Moraceae	Ficus sp. 1	Not determined	Circular leaf gall	Hymenoptera	parasitoid	76
Myrtaceae	Eugenia bunchosiifolia	Cecidomyiidae	Marginal leaf roll	Hymenoptera	parasitoid	79
	Eugenia bunchosiifolia	Cecidomyiidae	Marginal leaf roll	Lepidoptera	inquiline	79
	Eugenia bunchosiifolia	Cecidomyiidae	Marginal leaf roll	Coccoidea (Hemiptera)	inquiline	79
	Eugenia bunchosiifolia	Cecidomyiidae	Marginal leaf roll	Psocoptera	successor	79
	Eugenia bunchosiifolia	Cecidomyiidae	Marginal leaf roll	Collembola	successor	79
	Eugenia sp. 1	Not determined	Conical leaf gall	Hemiptera	inquiline	82
	Eugenia sp. 3	Not determined	Globose leaf gall	Collembola	successor	84
	Eugenia sp. 3	Not determined	Globose leaf gall	Hymenoptera	parasitoid	84
Olacaceae	Olacaceae (not determined)	Not determined	Globose leaf gall	Pseudoscorpiones	predator	94
Salicaceae	Casearia sp. 3	Not determined	Bud gall	Hymenoptera	parasitoid	106
Sapindaceae	Serjania sp.	Not determined	Cylindrical leaf gall	Hymenoptera	parasitoid	114
	Serjania sp.	Cecidomyiidae	Stem,tendril, petiole, vein swelling	Hymenoptera	parasitoid	115
Sapotaceae	Pouteria sp. 2	Not determined	Bud gall	Hymenoptera	parasitoid	122
Verbenaceae	Lantana camara	Cecidomyiidae	Stem and petiole swelling	Hymenoptera	parasitoid	124

Data on insect galls are presented here under host plant families, genera and species in alphabetical order. They include gall morphological characterization, associated fauna and previous records in Brazil.

Anacardiaceae (n = 4)

Astronium sp. (native genus)

Leaf gall, globose, green, glabrous, one-chambered. Galler: Hemiptera. Trail: Charco (21/V/2013) and Marcelo Trindade (09/VII/2013) (Fig. 1).

Figs. 1–24
Insect galls of Guaxindiba. 1. Astronium sp., globose leaf gall; 2. Schinus terebinthifolius, globose stem gall; 3. Xylopia sp., conical leaf gall; 4. Aspidosperma sp., circular leaf gall; 5. Adenocalymma sp., fusiform vein/tendril gall; 6. Amphilophium sp., globose vein gall; 7. Bignonia sp. 1, fusiform vein gall; 8. Bignonia sp. 2, vein swelling; 9. Bignonia sp. 3, vein swelling; 10 and 11. Martinella obovata, 10: globose bud gall; 11: petiole/vein gall; 12 and 13. Pyrostegia sp., 12: conical leaf gall; 13: vein swelling; 14. Bignoniaceae sp. 1, vein swelling; 15. Bignoniaceae sp. 2, tendril/petiole swelling; 16 and 17. Protium heptaphyllum, 16: stem gall; 17: bud gall; 18. Licania sp., globose vein gall; 19. Buchenavia sp., marginal leaf roll; 20. Erythroxylum pauferrense, conical leaf gall; 21. Dodecastigma sp., vein swelling; 22. Manihot sp., cylindrical leaf gall; 23-24. Pachystroma longifolium, 23: marginal leaf roll; 24: conical leaf gall.

Previous records: Galls on Astronium spp. were recorded in Porto de Trombetas (Pará), Serra de São José (MG), and Maricá (RJ). Refs.: Almada and Fernandes (2011), Maia (2001a), Maia and Fernandes (2004).

Schinus terebinthifolius Raddi (native species)

Leaf gall, circular, green, glabrous, one-chambered. Galler: Calophya terebinthifoliiBurckhardt and Basset, 2000 (Psyllidae, Hemiptera). Trail: Marcelo Trindade (11/III/2013). Previous records: Cabo Frio (RJ), Maricá (RJ), Ilha Grande (Angra dos Reis, RJ), Paraty (RJ). Refs.: Fig. 3 in Maia and Oliveira (2010), Monteiro et al. (1994).

Stem swelling, globose, brown, glabrous, multi-chambered. Galler: not determined. Other dwellers: Acari (successors). Trail: Marcelo Trindade (12/III/2013). No previous record (Fig. 2).

Stem swelling, fusiform, brown, glabrous, one-chambered. Galler: Lepidoptera. Trail: Charco (21/V/2013). Previous records: Cabo Frio (RJ), Maricá (RJ), Ilha da Marambaia (Mangaratiba, RJ). Refs.: Maia (2006), Fig. 1 in Maia and Souza (2013), Rodrigues et al. (2014).

Annonaceae (n = 1)

Xylopia sp. (native genus)

Leaf gall, conical, green, glabrous, one-chambered. Galler: not determined. Trail: Abelha (22/V/2013) (Fig. 3).

Previous records: Galls on Xylopia spp. were recorded in the states of Minas Gerais, Rio de Janeiro, and São Paulo. Refs.: Fernandes et al. (1997), Gonçalves-Alvim and Fernandes (2001), Rodrigues et al. (2014), Saito and Urso-Guimarães (2012).

Apocynaceae (n = 1)

Aspidosperma sp. (native genus)

Leaf gall, circular, yellow, glabrous, one-chambered. Galler: Cecidomyiidae. Trail: Abelha (22/V/2013, 09/VII/2013), Colégio Agrícola (08/VII/2013, 11/IX/2013), Vera (11/III/2013, 11/IX/2013) (Fig. 4).

Previous records: Leaf galls on Aspidosperma spp. were recorded in the states of Pará, Goiás, Mato Grosso do Sul, Minas Gerais, and Rio de Janeiro. Refs.: Almada and Fernandes (2011), Araújo et al. (2011), Coelho et al. (2009), Fernandes et al. (1988, 1997), Maia (2014), Rodrigues et al. (2014).

Bignoniaceae (n = 11)

Adenocalymma sp. (native genus) (Memora sp.)

Tendril and vein swelling, fusiform, green, glabrous, one-chambered. Galler: not determined. Trail: Colégio Agrícola (11/IX/2013) (Fig. 5).

Previous records: Galls were recorded in Adenocalymma spp. (as Memora) in the state of Pará. Refs.: Almada and Fernandes (2011), Maia (2011a).

Amphilophium sp. (native genus)

Vein swelling, globose, green, glabrous, one-chambered. Galler: Cecidomyiidae. Trail: Abelha (13/III/2013, 22/V/2013, 29/IV/2014) (Fig. 6).

No previous record.

Bignonia sp. 1 (native genus)

Stem, tendril, vein and petiole swelling, fusiform, green, glabrous, one-chambered. Galler: Cecidomyiidae. Other dwellers: Hymenoptera (parasitoid). Trail: Abelha (22/V/2013), Colégio Agrícola (08/VII/2013), Marcelo Trindade (22/V/2013, 10/IX/2013), Vera (12/III/2013, 20/V/2013) (Fig. 7).

Bignonia sp. 2

Vein swelling, brown, glabrous, one-chambered. Galler: not determined. Trail: Marcelo Trindade (10/IX/2013) (Fig. 8).

Bignonia sp. 3

Vein swelling, brown, glabrous, one-chambered. Galler: not determined. Trail: Marcelo Trindade (10/IX/2013) (Fig. 9).

Previous records: A gall morphotype on stem was recorded on Bignonia sp. in Rio Grande do Sul. Ref.: Tavares (1909).

Martinella obovata (Kunth) Bureau & K. Schum (native species)

Bud gall, globose, with superficial grooves, green, rough, glabrous, one-chambered. Galler: not determined. Trail: Colégio Agrícola (08/VII/2013) (Fig. 10).

Stem, vein, petiole or tendril swelling, fusiform, green, glabrous, one-chambered. Galler: Cecidomyiidae. Other dwellers: Hymenoptera (parasitoid). Trail: Abelha (13/II/2013, 09/VII/2013, 10/IX/2013, 29/IV/2014), Colégio Agrícola (13/III/2013, 08.VII.2013, 29/IV/2014), Marcelo Trindade (22.V.2013), Vera (11-12/III/2013, 21/V/2013, 10/VII/2013, 11/IX/2013) (Fig. 11).

No previous record.

Pyrostegia sp. (native genus)

Leaf gall, conical, green, hairy, one-chambered. Galler: Cecidomyiidae. Other dwellers: Hymenoptera (parasitoid). Trail: Abelha (13/III/2013) (Fig. 12).

Stem or vein swelling, fusiform, green, glabrous, one-chambered. Galler: not determined. Trails: Colégio Agrícola (11/IX/2013), Marcelo Trindade (22/V/2013, 09/VII/2013), Vera (21/V/2013) (Fig. 13).

Previous records: A similar stem gall was recorded in Vale do Jequitinhonha (MG). Ref.: Fernandes et al. (1997).

Not determined Bignoniaceae sp. 1

Vein swelling, fusiform, green, glabrous, one-chambered. Galler: Cecidomyiidae. Other dwellers: Hymenoptera (parasitoid). Trails: Vera (12/III/2013, 21/V/2013, 11/IX/2013), Abelha (29/IV/2014) (Fig. 14).

Not determined Bignoniaceae sp. 2

Tendril and petiole swelling, fusiform, green, glabrous, one-chambered. Galler: Cecidomyiidae. Trails: Vera (12/III/2013), Abelha (09/VII/2013, 10/IX/2013), Colégio Agrícola (21/V/2013, 08/VII/2013) (Fig. 15).

Boraginaceae (n = 3)

Varronia curassavica Jacq. (native species)

Leaf gall, globose, green, hairy, one-chambered. Galler: Cordiamyia globosaMaia, 1996 (Cecidomyiidae). Trails: Charco (21/V/2013), Colégio Agrícola (13/III/2013, 08/VII/2013, 29/IV/2014), Marcelo Trindade (11/III/2013, 10/IX/2013), Vera (21/V/2013). Previous records: Jurubatiba (RJ), Carapebus (RJ), Cabo Frio (RJ), Belo Horizonte (MG), Guarapari (ES). Refs.: Bregonci et al. (2010), Fernandes et al. (1988), Maia (1996, 2001a), Fig. 30 in Maia et al. (2008), Monteiro et al. (1994, 2004).

Vein leaf gall, conical, green, hairy, one-chambered. Galler: Lopesiini (Cecidomyiidae). Trails: Charco (21/V/2013), Vera (21/V/2013), Colégio Agrícola (08/VII/2013, 11/IX/2013), Marcelo Trindade (11/III/2013, 10/IX/2013). Previous records: Cabo Frio (RJ), Maricá (RJ), Bertioga (SP). Refs.: Maia (2001a), Fig. 33 in Maia et al. (2008).

Inflorescence gall, ovoid, green, hairy, one-chambered. Galler: Asphondylia cfr. cordiaeMöhn, 1959 (Cecidomyiidae). Trails: Charco (21/V/2013), Marcelo Trindade (11/III/2013, 10/IX/2013), Vera (21/V/2013). Previous records: Jurubatiba (RJ), Cabo Frio (RJ), Maricá (RJ), Bertioga (SP). Refs.: Maia (2001a), Fig. 32 in Maia et al. (2008), Monteiro et al. (2004).

Burseraceae (n = 4)

Protium heptaphyllum (Aubl.) Marchand (native species)

Leaf gall, circular, green, glabrous, one-chambered. Galler: Psyllidae (Hemiptera). Trail: Marcelo Trindade (09/VII/2013). Previous records: Serra de São José (MG), São Tomé das Letras, Vale do Rio Doce (MG), Jurubatiba (RJ), Arraial do Cabo (RJ), Maricá (RJ). Refs.: Fig. 16 in Maia (2013b), Maia and Fernandes (2004), Monteiro et al. (1994, 2004).

Stem swelling, fusiform, brown, glabrous, one-chambered. Galler: not determined. Trail: Marcelo Trindade (09/VII/2013). No previous record (Fig. 16).

Bud gall, fusiform, brown, glabrous, one-chambered. Galler: not determined. Trail: Marcelo Trindade (09/VII/2013). No previous record (Fig. 17).

Leaf gall, conical, reddish, glabrous, one-chambered. Galler: Dactylodiplosis heptaphylliMaia, 2004a,b (Cecidomyiidae). Trail: Marcelo Trindade (09/VII/2013). Previous records: Pirineus (GO), Ingaí (MG), Serra de São José (MG), São Tomé das Letras (MG), Carapebus (RJ). Refs.: Araújo et al. (2011), Fig. 18 in Maia (2013b), Malves and Frieiro-Costa (2012), Narahara et al. (2004).

Celastraceae (n = 2)

Maytenus obtusifolia Mart. (native species)

Leaf gall, globose, thick and hard, green or red, glabrous, one-chambered. Galler: Mayteniella distincta Maia, 2001 (Cecidomyiidae). Trails: Charco (21/V/2013), Marcelo Trindade (11/III/2013, 22/V/2013, 09/VII/2013, 10/IX/2013), Vera (10/VII/2013). Previous records: Arraial do Cabo (RJ), Maricá (RJ), Grumari (Rio de Janeiro, RJ), Ilha da Marambaia (Mangaratiba, RJ). Refs.: Fig. 22 in Maia (2001a), Monteiro et al. (1994, 2004), Oliveira and Maia (2005), Rodrigues et al. (2014).

Fruit gall, ovoid, red, glabrous, one to three-chambered, externally not perceptible. Galler: Bruggmanniella maytenuse (Maia and Couri, 1992) (Cecidomyiidae). Trail: Marcelo Trindade (11/III/2013). Previous record: Maricá (RJ). Ref.: Maia (2001a).

Chrysobalanaceae (n = 1)

Licania sp. (native genus)

Vein swelling, globose, green, glabrous, one-chambered. Galler: not determined. Trail: Vera (12/III/2013) (Fig. 18).

Previous records: Galls on Licania spp. were recorded in the states of Pará, Goiás, Minas Gerais, and São Paulo. Refs.: Almada and Fernandes (2011), Araújo et al. (2014), Maia (2014), Maia and Fernandes (2004).

Combretaceae (n = 1)

Buchenavia sp. (native genus)

Marginal leaf roll, green, glabrous, one-chambered. Galler: not determined. Trail: Colégio Agrícola (13/III/2013) (Fig. 19).

Previous records: Leaf galls on Buchenavia sp. were recorded in the state of Pará. Ref.: Almada and Fernandes (2011).

Erythroxylaceae (n = 1)

Erythroxylum pauferrense Plowman (endemic species of Brazil)

Leaf gall, conical, green, glabrous, one-chambered. Galler: not determined. Trails: Charco (21/V/2013), Marcelo Trindade (12/III/2013, 10/IX/2013). Other dwellers: Hymenoptera (parasitoid) (Fig. 20).

No previous record.

Euphorbiaceae (n = 4)

Dodecastigma sp. (native genus)

Vein swelling, fusiform, green, glabrous, one-chambered. Galler: not determined. Trail: Vera (12/III/2013) (Fig. 21).

This plant genus was previously recorded in the North (Acre, Amazonas, Amapá, and Pará) and Northeast (Maranhão) regions of Brazil. This is the first record in the Southeast Region.

No previous record of galls.

Manihot sp. (native genus)

Leaf gall, cylindrical, green or red, glabrous, one-chambered. Galler: Iatrophobia brasiliensisRübsaamen, 1916 (Cecidomyiidae). Trail: Colégio Agrícola (11/III/2013, 20/V/2013, 08/VII/2013, 29/IV/2014) (Fig. 22).

Previous records: Similar galls on Manihot spp. were recorded in Goiás, Minas Gerais, and São Paulo. Refs.: Araújo et al. (2011), Carneiro et al. (2009), Maia et al. (2008), Saito and Urso-Guimarães (2012).

Pachystroma longifolium (Nees) I. M. Johnst. (native species)

Marginal roll, green, glabrous, one-chambered. Galler: not determined. Trails: Abelha (10/IX/2013), Colégio Agrícola (11/IX/2013) (Fig. 23).

Leaf gall, conical, green, glabrous, one-chambered. Galler: Hemiptera. Trails: Abelha (13/III/2013, 10/IX/2013), Colégio Agrícola (08/VII/2013), Vera (29/IV/2014) (Fig. 24).

No previous record.

Fabaceae (n = 35)

Acacia sp. (native genus)

Stem swelling, fusiform, brown, glabrous, multi-chambered. Galler: not determined. Other dwellers: Hymenoptera (parasitoid). Trail: Vera (12/III/2013, 21/V/2013) (Fig. 25).

Bud gall, globose, brown, glabrous, one-chambered. Galler: not determined. Other dwellers: Hymenoptera (parasitoid). Trail: Vera (12/III/2013) (Fig. 26).

Figs. 25–48
Insect galls of Guaxindiba. 25 and 26. Acacia sp., 25: fusiform stem gall; 26: globose bud gall; 27–32. Albizia sp., 27: globose bud gall; 28: fusiform bud gall; 29: circular leaf gall; 30: vein swelling; 31: marginal leaf roll; 32: globose leaf gall; 33. Bauhinia sp., cylindrical leaf gall; 34–36. Chloroleucon acacioides, 34: conical gall on folioles; 35: conical petiole gall; 36: globose bud gall; 37. Copaifera sp., cylindrical leaf gall; 38 and 39. Inga laurina, 38: globose leaf gall; 39: vein swelling; 40–45. Machaerium sp., 40: circular leaf gall; 41: fusiform stem gall; 42: marginal leaf roll; 43: circular leaf gall; 44: conical leaf gall; 45: globose bud gall; 46. Ormosia sp., vein swelling; 47. Pterodon sp., globose stem gall; 48. Senegalia sp., globose bud gall.

Previous records: Galls were recorded on this plant genus in the states of Pará, Pernambuco and Minas Gerais Refs.: Almada and Fernandes (2011), Coelho et al. (2009), Fernandes and Negreiros (2006), Fernandes et al. (1997), Santos et al. (2011a).

Albizia sp. (native genus)

Apical bud gall, globose, brown, glabrous, one-chambered. Galler: not determined. Trail: Abelha (29/IV/2014) (Fig. 27).

Apical bud gall, fusiform, brown, glabrous, multi-chambered. Galler: not determined. Trail: Abelha (22/V/2013) (Fig. 28).

Leaf gall, circular, green, glabrous, one-chambered. Galler: Cecidomyiidae. Other dwellers: Acari (successors). Trail: Abelha (13/III/2013, 22/V/2013, 10/IX/2013), Colégio Agrícola (13/III/2013), Vera (12/III/2013, 21/V/2013) (Fig. 29).

Vein swelling, fusiform, green, glabrous, multi-chambered. Galler: not determined. Trail: Abelha (22/V/2013) (Fig. 30).

Marginal roll, green, glabrous, one-chambered. Galler: not determined. Trail: Abelha (22/V/2013) (Fig. 31).

Leaf gall, globose, brown, glabrous, one-chambered. Galler: Cecidomyiidae. Trail: Abelha (13/III/2013) (Fig. 32).

No previous record.

Bauhinia sp. (native genus)

Leaf gall, cylindrical, brown, glabrous, one-chambered. Galler: not determined. Trail: Marcelo Trindade (10/IX/2013) (Fig. 33).

Previous records: Several galls were recorded on Bauhinia spp. in many Brazilian states: Amazonas, Pernambuco, Goiás, Mato Grosso do Sul, Minas Gerais, Espírito Santo, Rio de Janeiro, São Paulo. Refs.: Carneiro et al. (2009), Coelho et al. (2009), Fernandes et al. (1988), Fernandes et al. (2001), Julião et al. (2002), Maia et al. (2014), Rübsaamen (1907), Santos et al. (2010), Saito and Urso-Guimarães (2012), Santos et al. (2011b), Tavares (1920), Urso-Guimarães and Scarelli-Santos (2006), Urso-Guimarães et al. (2003).

Chloroleucon acacioides (Ducke) Barneby & J.W. Grimes (native species)

Leaf gall, formed by the coalescence of two folioles, conical, brown, glabrous, one-chambered. Galler: Cecidomyiidae. Trails: Colégio Agrícola (13/III/2013), Marcelo Trindade (12/III/2013), Vera (11/III/2013, 21/V/2013) (Fig. 34).

Petiole or stem swelling, conical, glabrous, brown, one-chambered. Galler: not determined. Trail: Abelha (10.IX.2013), Colégio Agrícola (21/V/2013) (Fig. 35).

Bud gall, globose, brown, glabrous, one-chambered. Galler: not determined. Trail: Vera (10/VII/2013) (Fig. 36).

No previous record.

Copaifera sp. (native genus)

Leaf gall, circular-globose, green, glabrous, one-chambered. Galler: not determined. Trail: Vera (29/IV/2014).

Leaf gall, cylindrical, green, glabrous, one-chambered. Galler: not determined. Trail: Marcelo Trindade (22/V/2013) (Fig. 37).

Previous records: Galls on Copaifera spp. were recorded in the states of Pernambuco, Minas Gerais, Espírito Santo, Rio de Janeiro, and São Paulo. Refs.: Maia and Souza (2013), Maia and Fernandes (2004), Maia et al. (2014).

Inga laurina (Sw.) Willd (native species)

Leaf gall, globose, green, glabrous, one-chambered. Galler: not determined. Trails: Marcelo Trindade (10/IX/2013), Vera (21/V/2013). Previous records: Porto Trombetas (PA). Ref.: Almada and Fernandes (2011) (Fig. 38).

Vein swelling, fusiform, green, glabrous, one-chambered. Galler: Neolasioptera sp. (Cecidomyiidae). Trail: Marcelo Trindade (08/VII/2013, 10/IX/2013). Previous records: Maricá (RJ), Porto Trombetas (PA). Refs.: Almada and Fernandes (2011), Maia et al. (2002) (Fig. 39).

Machaerium sp. (native genus)

Leaf gall, circular, green, glabrous, one-chambered. Galler: not determined. Trails: Abelha (22/V/2013), Marcelo Trindade (22/V/2013), Vera (10/VII/2013, 29/IV/2014) (Fig. 40).

Stem swelling, fusiform, brown, glabrous, one-chambered. Galler: not determined. Trail: Vera (21/V/2013) (Fig. 41).

Marginal leaf roll, green, glabrous, one-chambered. Galler: not determined. Trails: Abelha (13/III/2013, 22/V/2013, 29/IV/2014), Colégio Agrícola (13/II/2013, 22/V/2013, 08/VII/2013), Marcelo Trindade (22/V/2013, 09/VII/2013), Vera (12/III/2013, 21/V/2013, 10/VII/2013) (Fig. 42).

Leaf gall (foliole), circular, green, glabrous, one-chambered. Galler: not determined. Dwellers: Hymenoptera (parasitoid). Trails: Abelha (13/III/2013, 09/VII/2013), Colégio Agrícola (13/III/2013) (Fig. 43).

Leaf gall, conical, green, glabrous, one-chambered. Galler: not determined. Trail: Colégio Agrícola (21/V/2013). (Fig. 44)

Bud gall, globose, green, glabrous, one-chambered. Galler: not determined. Dwellers: Hymenoptera (parasitoid). Trails: Abelha (13.III.2013) (Fig. 45).

Previous records: Several galls were recorded on Machaerium spp. in the states of Pará, Minas Gerais, Espírito Santo, Rio de Janeiro, São Paulo, and Santa Catarina. Refs.: Almada and Fernandes (2011), Fernandes and Negreiros (2006), Fernandes et al. (1988), Fernandes et al. (2001), Gagné (1994), Maia et al. (2008), Maia et al. (2014), Malves and Frieiro-Costa (2012), Rübsaamen (1907), Tavares (1916, 1920).

Ormosia sp. (native genus)

Vein swelling, fusiform, green, glabrous, one-chambered. Galler: not determined. Trails: Colégio Agrícola (20/V/2013), Marcelo Trindade (12/III/2013, 09/VII/2013, 29/IV/2014) (Fig. 46).

Previous records: Other leaf gall morphotype was recorded on Ormosia paraensis Ducke in Porto de Trombetas (Pará). Ref: Almada and Fernandes (2011).

Pterodon sp. (native genus)

Stem swelling, globose, brown, glabrous, multi-chambered. Galler: not determined. Trail: Vera (21/V/2013) (Fig. 47).

No previous record.

Senegalia sp. (native genus)

Bud gall, globose, green, glabrous, one-chambered. Galler: not determined. Trail: Abelha (22/V/2013), Marcelo Trindade (09/VII/2013), Vera (29/IV/2014, 20/V/2013) (Fig. 48).

Previous records: Similar gall was recorded on Senegalia polyphylla (DC.) Britton & Rose in Cabo Frio (RJ). Ref.: Maia and Souza (2013).

Senna sp. (native genus)

Marginal leaf roll, green, glabrous, one-chambered. Galler: not determined. Trails: Colégio Agrícola (21/V/2013, 11/IX/2013), Marcelo Trindade (12/III/2013) (Fig. 49).

Figs. 49–72
Insect galls of Guaxindiba. 49 and 50. Senna sp., 49:marginal leaf roll; 50: globose leaf gall; 51. Zollernia ilicifolia, circular leaf gall; 52–57. Tontelea sp. 1, 52: conical leaf gall; 53: globose stem gall; 54: discoid leaf gall; 55: globose leaf gall; 56: fusiform stem gall; 57: marginal leaf roll; 58. Tontelea sp. 2, circular leaf gall; 59. Hypericaceae sp., conical leaf gall; 60–62. Byrsonima sericea, 60: globose stem gall; 61: circular leaf gall; 62: fower bud gall; 63: Mascagnia sp., globose leaf gall; 64–65. Stigmaphyllon lalandianum, 64: conical leaf gall; 65. globose leaf gall; 66. Sidastrum micranthum, globose leaf gall; 67. Trichilia elegans, fusiform stem gall; 68. Trichilia rubra, cylindrical leaf gall; 69. Trichilia sp. 1, marginal leaf roll; 70. Trichilia sp. 2, vein swelling; 71. Trichilia sp. 3, fusiform stem gall; 72. Trichilia sp. 4, cylindrical leaf gall.

Leaf gall, globose, brown, hairy, one-chambered. Galler: not determined. Trail: Marcelo Trindade (12/III/2013) (Fig. 50).

Previous records: Galls on this host plant genus were recorded in the states of Rio de Janeiro, Minas Gerais and São Paulo. Refs.: Carneiro et al. (2009), Maia et al. (1992), Saito and Urso-Guimarães (2012).

Zollernia ilicifolia (Brongn.) Vogel (native species)

Leaf gall, circular, green, glabrous, one-chambered. Galler: not determined. Trail: Marcelo Trindade (10/IX/2013) (Fig. 51).

Previous records: Coleopteran galls were recorded on Z. glabra (Spreng.) Yakovlev in Ilha da Marambaia (Mangaratiba, RJ). Ref.: Rodrigues et al. (2014).

Hippocrateaceae (n = 7)

Tontelea sp. 1 (native genus)

Leaf gall, conical, green, glabrous, one-chambered. Galler: not determined. Trail: Abelha (10/IX/2013) (Fig. 52).

Stem swelling, globose, reddish, glabrous, one-chambered. Galler: not determined. Trail: Abelha (10/IX/2013) (Fig. 53).

Leaf gall, discoid, brown, glabrous, one-chambered. Galler: not determined. Trail: Abelha (09/VII/2013, 10/IX/2013) (Fig. 54).

Leaf gall, globose, green, glabrous, one-chambered. Galler: not determined. Trail: Abelha (13/III/2013) (Fig. 55).

Stem swelling, fusiform, green, glabrous, one-chambered. Galler: not determined. Dwellers: Baridinae (Coleoptera, Curculionidae). Trail: Abelha (13/III/2013) (Fig. 56).

Marginal roll, green, glabrous, one-chambered. Galler: not determined. Trail: Abelha (13/II/2013, 10/IX/2013) (Fig. 57).

Tontelea sp 2

Leaf gall, circular, green, glabrous, one-chambered. Galler: not determined. Trail: Vera (11/IX/2013) (Fig. 58).

No previous record.

Hypericaceae (n = 1)

Not determined Hypericaeae

Leaf gall, conical, green, glabrous, one-chambered. Galler: not determined. Dwellers: Hymenoptera (parasitoid). Trail: Vera (20/V/2013) (Fig. 59).

Malpighiaceae (n = 6)

Byrsonima sericea DC. (native species)

Stem swelling, globose, brown, glabrous, one-chambered. Galler: Cecidomyiidae. Trail: Marcelo Trindade (22/V/2013, 08-09/VII/2013, 10/IX/2013, 29/IV/2014). Previous records: Pernambuco, Ilha Grande (Angra dos Reis, RJ), Ilha da Marambaia (Mangaratiba, RJ), Guarapari (ES), Jurubatiba (RJ), Carapebus (RJ), Arraial do Cabo (RJ), Maricá (RJ), Grumari (Rio de Janeiro, RJ), Vale do Jequitinhonha (MG). Refs.: Bregonci et al. (2010), Fernandes et al. (1997), Maia (2001a), Maia and Oliveira (2010), Monteiro et al. (1994, 2004), Oliveira and Maia (2005), Rodrigues et al. (2014), Santos et al. (2011b) (Fig. 60).

Leaf gall, circular, brown, glabrous, one-chambered. Galler: Dasineura byrsonimaeMaia, 2010 (Cecidomyiidae). Trails: Charco (21/V/2013), Marcelo Trindade (12/III/2013, 09/VII/2013, 10/IX/2013). Previous records: Guarapari (ES), Jurubatiba (RJ), Carapebus (RJ), Maricá (RJ), Grumari (Rio de Janeiro, RJ), Ilha da Marambaia (Mangaratiba, RJ), Ilha Grande (Angra dos Reis, RJ), Vale do Jequitinhonha (MG). Refs.: Bregonci et al. (2010), Fernandes et al. (1997), Maia (2001a, 2010), Maia and Oliveira (2010), Monteiro et al. (2004), Oliveira and Maia (2005), Rodrigues et al. (2014) (Fig. 61).

Flower bud gall, ovoid, brown, glabrous, multi-chambered. Galler: Bruggmanniella byrsonimae (Maia and Couri, 1992) (Cecidomyiidae). Trails: Charco (21/V/2013), Marcelo Trindade (08/VII/2013, 10/IX/2013). Previous records: Jurubatiba (RJ), Carapebus (RJ), Maricá (RJ), Ilha da Marambaia (Mangaratiba, RJ). Refs.: Maia (1999, 2001a), Monteiro et al. (1994, 2004), Rodrigues et al. (2014) (Fig. 62).

Mascagnia sp.

Leaf gall, globose, green, glabrous, one-chambered. Galler: not determined. Trail: Colégio Agrícola (11/IX/2013) (Fig. 63).

Previous records: Two gall morphotypes were recorded on this plant genus in the state of Espírito Santo and Minas Gerais. Refs.: Maia (2013b), Maia et al. (2014).

Stigmaphyllon lalandianum A. Juss. (endemic species of Brazil)

Leaf gall, conical, green, glabrous, one-chambered. Galler: Cecidomyiidae. Trails: Abelha (13/III/2013, 20/V/2013), Colégio Agrícola (29/IV/2014), Marcelo Trindade (11/III/2013) (Fig. 64).

Leaf gall, globose, green, glabrous, one-chambered. Galler: not determined. Trail: Colégio Agrícola (08/VII/2013, 11/IX/2013) (Fig. 65).

Previous record: An elongate-ovoid leaf gall was recorded in Minas Gerais on this same plant species. Ref.: Fernandes et al. (1988).

Malvaceae (n = 2)

idastrum micranthum S(A. St.-Hil.) Fryxell (= Sida micrantha A. St.-Hil.) (native species)

Stem swelling, fusiform, brown, glabrous, one-chambered. Galler: not determined. Trail: Marcelo Trindade (10/IX/2013).

Leaf gall, globose, yellow, hairy, one-chambered. Galler: not determined. Trail: Colégio Agrícola (08/VII/2013, 11/IX/2013) (Fig. 66).

Previous records: Galls on Sidastrum spp. (as Sida) were recorded in the states of Rio de Janeiro and Minas Gerais. Refs.: Coelho et al. (2009), Fernandes et al. (1997), Rodrigues et al. (2014).

Meliaceae (n = 9)

Trichilia elegans A. Juss. (endemic species of Brazil)

Stem swelling, fusiform, brown, glabrous, one-chambered. Galler: not determined. Dwellers: Hymenoptera (parasitoid). Trails: Colégio Agrícola (08/VII/2013), Vera (10/VII/2013, 11/IX/2013) (Fig. 67).

Trichilia rubra C.DC. (native species)

Leaf gall, cylindrical, brown, glabrous, one-chambered. Galler: not determined. Trail: Vera (12/III/2013, 11/IX/2013) (Fig. 68).

Trichilia sp. 1

Marginal leaf roll, green, glabrous, one-chambered. Galler: Cecidomyiidae. Trails: Abelha (13/III/2013, 22/V/2013, 09/VII/2013, 10/IX/2013), Vera (11-12/III/2013, 10/VII/2013, 11/IX/2013) (Fig. 69).

Trichilia sp. 2

Vein swelling, fusiform, brown, glabrous, one-chambered. Galler: Cecidomyiidae. Trail: Marcelo Trindade (12/III/2013, 22/V/2013) (Fig. 70).

Trichilia sp. 3

Stem swelling, fusiform, brown, glabrous, multi-chambered. Galler: not determined. Dwellers: Hymenoptera (parasitoid) (Fig. 71).

Trichilia sp. 4

Leaf gall, cylindrical (tubular), green, glabrous, one-chambered. Galler: not determined. Trail: Abelha (13/III/2013) (Fig. 72).

Trichilia sp. 5

Leaf gall, globose, green, glabrous, one or multi-chambered. Galler: Cecidomyiidae. Trail: Vera (12/III/2013, 21/V/2013) (Fig. 73).

Figs. 73–96
Insect galls of Guaxindiba. 73. Trichilia sp. 5, globose leaf gall; 74. Trichilia sp. 6, vein swelling; 75. Trichilia sp. 7, fusiform stem gall; 76. Ficus sp. 1, circular leaf gall; 77. Ficus sp. 2, globose leaf gall.; 78. Ficus sp. 2, conical leaf gall; 79–80. Eugenia bunchosiifolia, 79: marginal leaf roll; 80: conical leaf gall; 81–82. Eugenia sp. 1, 81: conical leaf gall; 82: cylindrical leaf gall; 83. Eugenia sp. 2, cylindrical leaf gall; 84. Eugenia sp. 3, globose leaf gall; 85. Eugenia sp. 4, discoid leaf gall; 86. Marlierea sp., gobose leaf gall; 87–90. Myrcia sp., 87: globose leaf gall; 88: ovoid leaf gall; 89: fusiform stem gall; 90: fusiform bud gall; 91. Myrciaria floribunda, marginal leaf roll; 92. Guapira sp., globose bud gall; 93–94. Olacaceae not determined, 93: tendril swelling; 94: globose leaf gall; 95. Pera glabrata, conical leaf gall; 96. Phyllanthus sp., circular leaf gall.

Trichilia sp. 6

Vein swelling, fusiform, brown, glabrous, one-chambered. Galler: not determined. Trail: Marcelo Trindade (10/IX/2013) (Fig. 74).

Trichilia sp. 7

Stem swelling, fusiform, brown, glabrous, one-chambered. Galler: not determined. Dwellers: Hymenoptera (parasitoid). Trail: Vera (11/IX/2013) (Fig. 75).

No previous record.

Moraceae (n = 3)

Ficus sp. 1 (native genus)

Leaf gall, circular, green or red, glabrous, one-chambered. Galler: not determined. Dwellers: Hymenoptera (parasitoid). Trail: Marcelo Trindade (12/III/2013, 10/IX/2013) (Fig. 76).

Leaf gall, globose, green or white, hairy, one-chambered. Galler: not determined. Trails: Charco (21/V/2013), Marcelo Trindade (12/III/2013, 10/IX/2013) (Fig. 77).

Ficus sp. 2

Leaf gall, conical, green, glabrous, one-chambered. Galler: Cecidomyiidae. Trail: Colégio Agrícola (21/V/2013) (Fig. 78).

Previous records: Galls on Ficus sp. were recorded in the states of Pará, Mato Grosso do Sul and Rio de Janeiro. Refs.: Almada and Fernandes (2011), Julião et al. (2002), Rodrigues et al. (2014).

Myrtaceae (n = 13)

Eugenia bunchosiifolia Nied. (= Eugenia santensis Kiaersk.) (endemic species of Brazil)

Marginal roll, green, glabrous, one-chambered. Galler: Cecidomyiidae. Other dwellers: Coccoidea, catterpilars (Lepidoptera) (inquilines), Psocoptera (successors), Hymenoptera (parasitoid). Trails: Charco (21/V/2013), Colégio Agrícola (11/IX/2013), Marcelo Trindade (11/III/2013, 12/III/2013, 22/V/2013, 09/VII/2013),Vera (11/IX/2013) (Fig. 79).

Leaf gall, conical, green, glabrous, one-chambered. Galler: not determined. Trails: Colégio Agrícola (11/IX/2013), Vera (11/IX/2013) (Fig. 80).

No previous record.

Eugenia sp. 1

Leaf gall, cylindrical, green, glabrous, one-chambered. Galler: not determined. Trail: Vera (11/IX/2013) (Fig. 81).

Leaf gall, conical, green, glabrous, one-chambered. Galler: not determined. Dwellers: Hemiptera (successors). Trails: Abelha (10/IX/2013), Colégio Agrícola (12/III/2013), Vera (20/V/2013, 10/VII/2013, 29/IV/2014) (Fig. 82).

Eugenia sp. 2

Leaf gall, cylindrical (tubular), green, glabrous, one-chambered. Galler: not determined. Trail: Abelha (13/III/2013) (Fig. 83).

Eugenia sp. 3

Leaf gall, globose, green, glabrous, one-chambered. Galler: not determined. Dwellers: Hymenoptera (parasitoid) and Collembola (successor). Trails: Abelha (29/IV/2014), Charco (21/V/2013), Colégio Agrícola (29/IV/2014), Marcelo Trindade (11/III/2013, 12/III/2013, 22/V/2013, 09/VII/2013) (Fig. 84).

Eugenia sp. 4

Leaf gall, discoid, brown, glabrous, one-chambered. Galler: not determined. Trail: Marcelo Trindade (10/IX/2013) (Fig. 85).

Marlierea sp. (native genus)

Leaf gall, globose, brown, glabrous, massive. Galler: not determined. Trail: Marcelo Trindade (10/IX/2013) (Fig. 86).

Previous records: Five different gall morphotypes are recorded on this host plant genus in Minas Gerais. Ref.: Maia (2014).

Myrcia sp.

Leaf gall (vein), globose, brown, glabrous, one-chambered. Galler: not determined. Trail: Marcelo Trindade (10/IX/2013) (Fig. 87).

Leaf gall (vein), ovoid, brown, glabrous, one-chambered. Galler: not determined. Trail: Marcelo Trindade (10/IX/2013) (Fig. 88).

Stem swelling, fusiform, brown, glabrous, one-chambered. Galler: not determined. Trail: Abelha (09/VII/2013, 10/IX/2013) (Fig. 89).

Bud gall, fusiform, brown, glabrous, one-chambered. Galler: not determined. Trail: Abelha (22/V/2013) (Fig. 90).

Previous records: Galls on Myrcia spp. were recorded in Goiás, Pernambuco, Minas Gerais, Espírito Santo, Rio de Janeiro, São Paulo, and Rio Grande do Sul. Refs.: Araújo et al. (2014), Maia (2013a,b), Maia (2014), Maia et al. (2014), Toma and Mendonça (2013).

Myrciaria floribunda (West ex Willdenow) Berg. (native species)

Marginal roll, green, glabrous, one-chambered. Galler: Dasineura myrciariaeMaia, 1993 (Cecidomyiidae). Trail: Abelha (10/IX/2013, 29/IV/2014). Previous records: Guarapari (ES), Santa Teresa (ES), Jurubatiba (RJ), Carapebus (RJ), Maricá (RJ). Refs.: Bregonci et al. (2010), Maia (1993), Maia et al. (2014), Monteiro et al. (1994, 2004) (Fig. 91).

Nyctaginaceae (n = 4)

Guapira opposita (Vell.) Reitz (native species)

Leaf gall, globose, red or green, hairy, one-chambered. Galler: Bruggmannia robustaMaia and Couri, 1993 (Cecidomyiidae). Trail: Marcelo Trindade (12/III/2013, 09/VII/2013, 10/IX/2013). Previous records: Jurubatiba (RJ), Arraial do Cabo (RJ), Maricá (RJ), Ilha Grande (Angra dos Reis, RJ), Ilha da Marambaia (Mangaratiba, RJ), Bertioga (SP). Refs.: Maia and Couri (1993), Maia (2001a), Fig. 29 in Maia and Oliveira (2010), Maia et al. (2008), Monteiro et al. (2004), Rodrigues et al. (2014).

Leaf gall, conical, green, glabrous, one-chambered. Galler: Bruggmannia acaudataMaia, 2004a (Cecidomyiidae). Trail: Vera (21/V/2013). Previous records: Santa Teresa (ES), Jurubatiba (RJ), Carapebus (RJ), Maricá (RJ), Ilha Grande (Angra dos Reis, RJ). Refs.: Maia (2001a, 2004a), Fig. 30 in Maia and Oliveira (2010), Maia et al. (2014), Monteiro et al. (2004), Rodrigues et al. (2014).

Leaf gall, circular, green, glabrous, one-chambered. Galler: Bruggmannia elongataMaia and Couri, 1993 (Cecidomyiidae). Trail: Marcelo Trindade (22/V/2013). Previous records: Bertioga (SP), Jurubatiba (RJ), Carapebus (RJ), Arraial do Cabo (RJ), Maricá (RJ), Ilha da Marambaia (Mangaratiba, RJ), Ilha Grande (Angra dos Reis, RJ). Refs.: Maia (2001a), Maia and Couri (1993), Fig. 28 in Maia and Oliveira (2010), Maia et al. (2008), Monteiro et al. (1994), Rodrigues et al. (2014).

Guapira sp.

Bud gall, globose, green, glabrous, one-chambered. Galler: Cecidomyiidae. Trail: Abelha (22/V/2013) (Fig. 92).

Ochnaceae (n = 1)

Ouratea cuspidata (A. St.-Hil.) Engl. (endemic species of Brazil)

Leaf gall, cylindrical, brown, glabrous, one-chambered. Galler: Contarinia (Cecidomyiidae). Trail: Abelha (09/VII/2013). Previous records: Grumari (Rio de Janeiro, RJ), Ilha Grande (Angra dos Reis, RJ), Maricá (RJ), Jurubatiba (RJ), Guarapari (ES). Refs.: Bregonci et al. (2010), Maia (2001a), Fig. 33 in Maia and Oliveira (2010), Monteiro et al. (2004), Oliveira and Maia (2005).

Olacaceae (n = 2)

Not determined species

Stem and tendril swelling, fusiform, brown, glabrous, one-chambered. Galler: not determined. Trails: Colégio Agrícola (21/V/2013), Marcelo Trindade (12/III/2013, 22/V/2013) (Fig. 93).

Leaf gall, globose, green, glabrous, one-chambered. Galler: not determined. Other dwellers: Pseudoscorpiones (predator). Trail: Colégio Agrícola (13/III/2013) (Fig. 94).

Peraceae (n = 1)

Pera glabrata (Schott) Poepp. ex Baill. (native species)

Leaf gall, conical, green, glabrous, one-chambered. Galler: not determined. Trail: Abelha (22/V/2013) (Fig. 95).

Previous records: A gall morphotype on buds was recorded on this same plant species in Minas Gerais. Refs.: Maia (2011b).

Phyllanthaceae (n = 2)

Phyllanthus sp. (native genus)

Leaf gall, circular, green, glabrous, one-chambered. Galler: not determined. Trails: Abelha (29/IV/2014), Vera (11/IX/2013) (Fig. 96).

Leaf gall, globose (kidney-shaped), green, glabrous, one-chambered. Galler: Cecidomyiidae. Trails: Abelha (13/III/2013) (Fig. 97).

Figs. 97–120
Insect galls of Guaxindiba. 97. Phyllanthus sp., globose leaf gall; 98. Psychotria sp., fusiform stem gall; 99–100. Metrodorea sp., 99. circular leaf gall; 100. vein swelling; 101–103. Neoraputia alba, 101: globose leaf gall; 102: fusiform leaf gall at petiole basis; 103: vein swelling; 104. Casearia sp. 1, cylindrical leaf gall; 105. Casearia sp. 2, leaf roll; 106. Casearia sp. 3, globose bud gall; 107–108. Matayba juglandifolia, 107: conical leaf gall; 108: globose leaf gall; 109–110. Paullinia racemosa, 109: midvein swelling; 110: circular leaf gall; 111–117. Serjania sp., 111: vein swelling; 112: fusiform bud gall; 113: circular leaf gall; 114: cylindrical leaf gall; 115: tendril swelling; 116: midvein swelling; 117: globose leaf gall; 118–119. Manilkara subsericea, 118: circular leaf gall; 119: globose stem gall; 120. Pouteria sp. 1, circular leaf gall.

Previous records: A similar globose gall was recorded on this plant genus in Santa Teresa (ES). Refs.: Maia et al. (2014).

Rubiaceae (n = 1)

Psychotria sp. (native genus)

Stem swelling, fusiform, brown, glabrous, one-chambered. Galler: not determined. Trail: Vera (21/V/2013) (Fig. 98).

Previous records: Several galls on Psychotria spp. were recorded in Pernambuco, Mato Grosso do Sul, Minas Gerais, Rio de Janeiro, São Paulo, and Rio Grande do Sul. Refs.: Maia (2014), Maia et al. (2014).

Rutaceae (n = 6)

Metrodorea sp. (native genus)

Marginal roll, green, glabrous, one-chambered. Galler: not determined. Trails: Colégio Agrícola (29/IV//2014), Vera (10/VII/2013, 11/IX/2013)

Leaf gall, circular, green, glabrous, one-chambered. Galler: Hemiptera. Trails: Abelha (22/V/2013, 10/IX/2013, 29/IV/2014), Colégio Agrícola (13/III/2013, 11/IX/2013, 29/IV/2014), Marcelo Trindade (12/III/2013, 22/V/2013), Vera (12/III/2013, 20-21/V/2013, 10/VII/2013, 29/IV/2014) (Fig. 99).

Vein swelling, fusiform, green, glabrous, one-chambered. Galler: not determined. Trails: Abelha (13/III/2013, 10/IX/2013, 29/IV/2014), Colégio Agrícola (13.III.2013, 21/V/2013, 11/IX/2013), Marcelo Trindade (12/III/2013, 22/V/2013, 29/IV/2014), Vera (11-12/III/2013, 20/V/2013, 10/VII/2013, 11/IX/2013, 29/IV/2014) (Fig. 100).

No previous record.

Neoraputia alba (Nees & Mart.) Emmerich ex Kallunki (endemic species of Brazil)

Leaf gall, globose, brown, glabrous, one-chambered. Galler: not determined. Trail: Vera (11/IX/2013) (Fig. 101).

Leaf gall, at petiole basis, fusiform, green, glabrous, one-chambered. Galler: not determined. Trail: Abelha (22/V/2013) (Fig. 102).

Vein swelling, fusiform, green, glabrous, one-chambered. Galler: not determined. Trails: Abelha (13/III/2013, 22/V/2013), Colégio Agrícola (13/III/2013), Vera (12/III/2014, 21/V/2013, 10/VII/2013) (Fig. 103).

No previous record.

Salicaceae (n = 3)

Casearia sp. 1 (native genus)

Leaf gall, cylindrical, green, glabrous, one-chambered. Galler: Hemiptera. Trails: Abelha (09/VII/2013), Marcelo Trindade (12/III/2013, 22/V/2013, 29/IV/2014) (Fig. 104).

Casearia sp. 2

Leaf roll, green, glabrous, one-chambered. Galler: not determined. Trail: Vera (21/V/2013, 10/VII/2013) (Fig. 105).

Casearia sp. 3

Bud gall, globose, spongy, brown, micropubescent, one-chambered. Galler: not determined. Dwellers: Hymenoptera (parasitoid). Trail: Abelha (22/V/2013) (Fig. 106).

Previous records: Galls on Casearia spp. were recorded in the states of Pará, Goiás, Pernambuco, Minas Gerais, and Rio de Janeiro. Refs.: Araújo et al. (2014), Maia et al. (2014), Rodrigues et al. (2014).

Sapindaceae (n = 13)

Matayba juglandifolia (Cambess.) Radlk. (endemic species of Brazil)

Leaf gall, conical, green, glabrous, one-chambered. Galler: not determined. Trail: Marcelo Trindade (10/IX/2013) (Fig. 107).

Vein swelling, fusiform, green, glabrous, one-chambered. Galler: not determined. Trail: Colégio Agrícola (20/V/2013)

Leaf gall, globose, green, glabrous, one-chambered. Galler: not determined. Trails: Charco (21/V/2013), Marcelo Trindade (10/IX/2013) (Fig. 108).

No previous record.

Paullinia racemosa Wawra (endemic species of Brazil)

Midvein swelling, fusiform, brown, glabrous, one-chambered. Galler: not determined. Trails: Colégio Agrícola (11/IX/2013), Marcelo Trindade (10/IX/2013) (Fig. 109).

Leaf gall, circular, green, glabrous, one-chambered. Galler: not determined. Trails: Abelha (10/IX/2013), Vera (20/V/2013, 11/IX/2013) (Fig. 110).

Previous records: Clavate leaf galls were recorded in Cabo Frio (RJ) and petiole galls in Pernambuco on this host plant genus. Refs.: Maia and Souza (2013), Santos et al. (2011b).

Paullinia weinmanniifolia Mart. (endemic species of Brazil)

Leaf gall, conical, green, glabrous, one-chambered. Galler: Paulliniamyia ampla Maia, 2001 (Cecidomyiidae). Trails: Marcelo Trindade (12/III/2013, 10/IX/2013), Vera (20/V/2013). Previous records: Jurubatiba (RJ), Arraial do Cabo (RJ), Maricá (RJ). Refs.: Fig. 86 in Maia (2001a), Maia (2001b), Monteiro et al. (1994, 2004).

Serjania sp. (native genus)

Vein swelling, fusiform, little evident, green, glabrous, one-chambered. Galler: not determined. Trail: Vera (10/VII/2013) (Fig. 111).

Bud gall, fusiform, brown, glabrous, one-chambered. Galler: not determined. Trail: Vera (21/V/2013) (Fig. 112).

Leaf gall (vein), circular, green, glabrous, one-chambered. Galler: not determined. Trails: Abelha (13/III/2013, 29/IV/2014), Colégio Agrícola (21/V/2013), Marcelo Trindade (12/III/2013, 20-21/V/2013, 10/IX/2013), Vera (12/III/2013, 20-21/V/2013, 10/VII/2013, 11/IX/2013) (Fig. 113).

Leaf gall, cylindrical, green, glabrous, one-chambered. Galler: not determined. Dwellers: Hymenoptera (parasitoid). Trails: Colégio Agrícola (13/III/2013, 21/V/2013, 08/VII/2013), Marcelo Trindade (13/III/2013, 21/V/2013, 08/VII/2013, 10/IX/2013), Vera (12/III/2013, 11/IX/2013) (Fig. 114).

Stem, tendril, petiole, vein swelling, globose, brown, glabrous, one-chambered. Galler: Cecidomyiidae. Other dwellers: Hymenoptera (parasitoid). Trails: Abelha (22/V/2013, 10/IX/2013, 29/IV/2014), Colégio Agrícola (13/III/2013), Marcelo Trindade (12/III/2013, 22/V/2013), Vera (21/V/2013) (Fig. 115).

Midvein swelling (causing leaf fold), fusiform, green, glabrous, one-chambered. Galler: not determined. Trail: Colégio Agrícola (13/III/2013) (Fig. 116).

Leaf gall, globose, green, glabrous, one-chambered. Galler: not determined. Trail: Colégio Agrícola (13/III/2013) (Fig. 117).

Previous records: Several galls were recorded on Serjania spp. in Amazonas, Pará, Goiás, Mato Grosso do Sul, Pernambuco, Minas Gerais, Espírto Santo, Rio de Janeiro, and São Paulo. Refs.: Maia (2013a,b), Maia (2014), Maia et al. (2014), Rodrigues et al. (2014).

Sapotaceae (n = 5)

Manilkara subsericea (Mart.) Dubard. (endemic species of Brazil)

Leaf gall, circular, green, glabrous, one-chambered. Galler: not determined. Trail: Marcelo Trindade (09/VII/2013, 10/IX/2013) (Fig. 118).

Stem swelling, globose, brown, glabrous, one-chambered. Galler: not determined. Trails: Charco (21/V/2013), Marcelo Trindade (11/III/2013, 29/IV/2014, 22/V/2013, 09/VII/2013, 10/IX/2013) (Fig. 119).

Previous records: Some galls were recorded in this plant species in the states of Espírito Santo and Rio de Janeiro. Refs.: (Maia, 2014).

Pouteria sp. 1 (native genus)

Leaf gall, circular, green, glabrous, one-chambered. Galler: Cecidomyiidae. Trails: Abelha (10/IX/2013), Colégio Agrícola (13/III/2013, 084/VII/2013, 29/IV/2014), Vera (11-12/III/2013, 20/V/2013, 10/VII/2013) (Fig. 120).

Pouteria sp. 2

Stem swelling, globose, brown, glabrous, one-chambered. Galler: not determined. Trails: Abelha (09/07/2013), Vera (11/IX/2013) (Fig. 121).

Figs. 121–125
Insect galls of Guaxindiba. 121 and 122. Pouteria sp. 2, 121: globose stem gall; 122: globose bud gall; 123. Smilax krukovii, conical leaf gall; 124. Lantana camara, fusiform stem gall; 125. Lantana sp., cylindrical leaf gall.

Bud gall, globose, brown, glabrous, multi-chambered. Galler: not determined. Dwellers: Hymenoptera (parasitoid). Trails: Abelha (22/V/2013, 10/IX/2013), Vera (20/V/2013) (Fig. 122).

Previous records: Several galls on Pouteria spp. were recorded in the states of Pará, Goiás, Mato Grosso do Sul, Minas Gerais, Espírito Santo, Rio de Janeiro and São Paulo. Refs.: Araújo et al. (2014), Maia (2014), Maia et al. (2014).

Smilacaceae (n = 1)

Smilax krukovii A. C. Sm. (endemic species of Brazil)

Leaf gall, conical, green, glabrous, one-chambered. Galler: Hemiptera. Trails: Charco (21/V/2013), Marcelo Trindade (22/V/2013, 09/07/2013, 10/IX/2013) (Fig. 123).

No previous records.

Verbenaceae (n = 2)

Lantana camara L. (native species)

Stem and petiole swelling, fusiform, green, glabrous, one-chambered. Galler: Cecidomyiidae. Other dwellers: Hymenoptera (parasitoid). Trail: Colégio Agrícola (13/III/2013, 21/V/2013, 08/VII/2013) (Fig. 124). Previous records: Vale do Rio Doce (MG). Ref.: Fernandes et al. (2001).

Lantana sp.

Leaf gall, cylindrical (tubular), green, micropubescent, one-chambered. Galler: Cecidomyiidae. Trails: Colégio Agrícola (13/III/2013, 08/VII/2013), Marcelo Trindade (09/VII/2013),Vera (20/V/2013) (Fig. 125).

Conclusions

The only surveyed area of Tabuleiro Forest in Brazil presented a great richness of insect galls. The most galled botanical taxa and plant organs, the most frequent galler taxon, the most common gall morphology (shape, color and indumentary) and the composition of the associated fauna confirm the known patterns of Brazil and Atlantic Forest.

Acknowledgments

We are grateful to Barbara Proença and Sharlene Ascendino (Museu Nacional) for helping in the field work, and to CNPq (VCM, Proc. 371848/2013-0; SPCF, Proc. 140344/2011-0) and FAPERJ (Proc. E-26/111.40/2012) for financial support.

References

• Abrahamson, W.G., Weis, A.E., 1997. Evolutionary Ecology Across Three Trophic Levels: Goldenrods, Gallmakers and Natural Enemies. Princeton University Press, New Jersey.
• Almada, E.D., Fernandes, G.W., 2011. Insetos indutores de galhas em florestas de terra firme e em reflorestamentos com espécies nativas na Amazônia Oriental, Pará. Brasil. Bol. Mus. Para. Emilio Goeldi 6, 163-196.
• Araújo, W.S., Santos, B.B., Gomes-Klein, V.L., 2011. Insect galls from Serra dos Pireneus, GO, Brazil. Biota Neotrop. 11, 357-365.
• Araújo, W.S., Sobral, F.L., Maracahipes, L., 2014. Insect galls of the Parque Nacional das Emas (Mineiros, GO, Brazil). Check List 10, 1445-1451.
• Bregonci, J.M., Polycarpo, P.V., Maia, V.C., 2010. Galhas de insetos do Parque Estadual Paulo César Vinha (Guarapari, ES, Brasil). Biota Neotrop. 10, 227-238.
• Burckhardt, D., Basset, Y., 2000. The jumping plant-lice (Hemiptera, Psylloidea) associated with Schinus (Anacardiaceae); systematics, biogeography and host plant relationships. J. Nat. Hist. 34, 57-155.
• Carneiro, M.A.A., Borges, R.A.X., Araújo, A.P.A., Fernandes, G.W., 2009. Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, MG, Brasil. Rev. Bras. Entomol. 53, 570-592.
• Coelho, M.S., Almada, E.D., Fernandes, G.W., Carneiro, M.A.A., Santos, R.M., Sanchez-Azofeifa, A., 2009. Gall inducing arthropods from a seasonally dry tropical Forest in Serra do Cipó, Brazil. Rev. Bras. Entomol. 53, 404-414.
• Costa, E.C., Carvalho-Fernandes, S.P., Santos-Silva, J., 2014. Galhas de insetos de uma área de transição caatinga-cerrado no Nordeste do Brasil. Sitientibus Ser. Ci. Biol. 14, 1-9.
• Dreger-Jauffret, F., Shorthouse, J.D., 1992. Diversity of gall-inducing insects and their galls. In: Shorthouse, J.D., Rohfritsch, O. (Eds.), Biology of Insect-Induced Galls. Oxford, Oxford University Press, pp. 8–33.
• Felt, E.P., 1940. Plant Galls and Gall Makers, Ithaca, N.Y.
• Fernandes, G.W., Negreiros, D., 2006. A comunidade de insetos galhadores da RPPN Fazenda Bulcão, Aimorés, Minas Gerais, Brasil. Lundiana 7, 111-120.
• Fernandes, G.W., Tameirão-Neto, E., Martins, R.P., 1988. Ocorrência e caracterização de galhas entomógenas na vegetação do campus Pampulha da Universidade Federal de Minas Gerais. Rev. Bras. Zool. 5, 11-29.
• Fernandes, G.W., Araújo, R.C., Araújo, S.C., Lombardi, J.A., Paula, A.S., Loyolla Jr., R.R., Cornelissen, T.G., 1997. Insect galls from savanna and rocky fields of the Jequitinhonha Valley, Minas Gerais, Brazil. Naturalia 22, 221-224.
• Fernandes, G.W., Julião, G.R., Araújo, R.C., Araújo, S.C., Lombardi, J.A., Negreiros, D., Varneiro, M.A.A., 2001. Distribution and morphology of insect galls of the Rio Doce Valley, Brazil. Naturalia 26, 221-244.
• Floate, K.D., Fernandes, G.W., Nilsson, J.A., 1996. Distinguishing intrapopulacional categories of plants by their insect faunas: galls on rabbitbrush. Oecologia 105, 221-229.
• Gagné, R., 1994. The Gall Midges of the Neotropical Region. Cornell University Press, Ithaca.
• Gonçalves-Alvim, S.J., Fernandes, G.W., 2001. Comunidades de insetos galhadores (Insecta) em diferentes fisionomias do cerrado em Minas Gerais, Brasil. Rev. bras. Zool. 18, 289-305.
• Inea, 2015. Estação Ecológica de Guaxindiba, Available from: http://www.inea.rj.gov.br/Portal/Agendas/BIODIVERSIDADEEAREASPROTEGIDAS/UnidadesdeConservacao/INEA_008607 (accessed 02.03.15).
  » http://www.inea.rj.gov.br/Portal/Agendas/BIODIVERSIDADEEAREASPROTEGIDAS/UnidadesdeConservacao/INEA_008607
• Julião., G.R., Amaral, M.E.C., Fernandes, G.W., 2002. Galhas de insetos de suas plantas hospedeiras do Pantanal sul-mato-grossense. Naturalia 27, 47-74.
• Lista de Espécies da Flora do Brasil, 2015. Jardim Botânico do Rio de Janeiro, Available from: http://floradobrasil.jbrj.gov.br/ (accessed 20.03.15).
  » http://floradobrasil.jbrj.gov.br/
• Maia, V.C., 1993. Três espécies novas de Dasineura Rondani (Diptera, Cecidomyiidae) associadas a Myrtaceae na Restinga da Barra de Maricá, Rio de Janeiro. Rev. Bras. Zool. 12, 1001-1008.
• Maia, V.C., 1996. Cordiamyia globosa, n. gen. E n. sp. (Diptera, Cecidomyiidae) associado com Cordia verbenacea (Boraginaceae), na Restinga da Barra de Maricá (R.J.). Rev. Bras. Zool. 13, 579-583.
• Maia, V.C., 1999. Descrição de imaturos de quatro espécies de Asphondyliini neotropicais e nota taxonômica sobre Asphondylia maytenuse Maia & Couri (Diptera, Cecidomyiidae). Rev. Bras. Zool. 16, 775-778.
• Maia, V.C., 2001a. The gall midges (Diptera, Cecidomyiidae) from three restingas of Rio de Janeiro State, Brazil. Rev. Bras. Zool. 18, 583-629.
• Maia, V.C., 2001b. New genera and species of gall midges (Diptera, Cecidomyiidae) from three restingas of Rio de Janeiro State, Brazil. Rev. Bras. Zool. 18, 1-32.
• Maia, V.C., 2002. Description of the larva of Houardodiplosis rochae Tavares, 1925 (Diptera, Cecidomyiidae, Clinodiplosini) and new record of pseudoscorpions in galls. Rev. Bras. Entomol. 46, 81-82.
• Maia, V.C., 2004a. Description of a new species of Bruggmannia Tavares (Diptera, Cecidomyiidae) associated with Guapira opposita (Vell.) Reitz. (Nyctaginaceae) from Brazil. Rev. Bras. Zool. 21, 761-764.
• Maia, V.C., 2004b. Pp. 485–489. In: Narahara, K.L., Maia, V.C., Monteiro, R.F. (Eds.), Two new species of gall midges (Diptera, Cecidomyiidae) associated with Protium heptaphyllum (Aubl.) Marchand in Brazil. Rev. Bras. Entomol. 48, 485–490.
• Maia, V.C., 2006. Galls of Hemiptera, Lepidoptera and Thysanoptera from Central and South America. Publ. Avulsas Mus. Nac. 110, 3-22.
• Maia, 2010. A new species of Dasineura Rondani, 1840 (Diptera, Cecidomyiidae) associated with Byrsonima sericea (Malpighiaceae). Rev. Bras. Bioci. 8, 377-380.
• Maia, V.C., 2011a. Characterization of insect galls, gall makers, and associated fauna of Platô Bacaba (Porto de Trombetas, Pará, Brazil). Biota Neotrop. 11, 37-53.
• Maia, V.C., 2011b. Galhas de insetos do Parque Nacional do Ibitipoca (Minas Gerais, Brasil). X Congresso de Ecologia do Brasil, www.sebecologia.org.br/xceb/resumos/53.pdf
  » www.sebecologia.org.br/xceb/resumos/53.pdf
• Maia, V.C., 2013a. Galhas de insetos em restingas da região sudeste do Brasil com novos registros. Biota Neotrop. 13, 183-209.
• Maia, V.C., 2013b. Insect galls of São Tomé das Letras (MG, Brazil). Biota Neotrop. 13, 164-189.
• Maia, V.C., 2014. Insect galls of Itamonte (Minas Gerais, Brazil): characterization and occurrence. Biota Neotrop. 14, 1-17.
• Maia, V.C., Couri, M.S., 1993. Descrição de três espécies de Bruggmannia Tavares, 1915 (Diptera, Cecidomyiidae, Asphondyliidi) do Brasil, associadas com Guapira opposita (Nyctaginaceae). Rev. Bras. Biol. 53, 209-215.
• Maia, V.C., Couri, M.S., 1992. Pp. 655–660. In: Maia, V.C., Couri, M.S., Monteiro, R.F. (Eds.), Sobre seis espécies de Asphondylia Loew, 1850 do Brasil (Diptera, Cecidomyiidae). Rev. Bras. Entomol. 36, 653–661.
• Maia, V.C., Fernandes, G.W., 2004. Insect galls from Serra de São José (Tiradentes, MG, Brazil). Braz. J. Biol. 64(3a), 423-445.
• Maia, V.C., Oliveira, J.C., 2010. Galhas de insetos da Reserva Biológica Estadual da Praia do Sul (Ilha Grande, Angra dos Reis, RJ). Biota Neotrop. 10, 227-238.
• Maia, V.C., Souza, M.C., 2013. Insect galls of the xeric vegetation of Ilha do Cabo Frio (Arraial do Cabo, RJ, Brazil). Biota Neotrop. 13, 278-288.
• Maia, V.C., Couri, M.S., Monteiro, R.F., 1992. Sobre seis espécies de Asphondylia Loew, 1850 do Brasil (Diptera, Cecidomyiidae). Rev. Bras. Entomol. 36, 653-661.
• Maia, V.C., Azevedo, M.A.P., Couri, M.S., 2002. New contribution to the knowledge of the gall midges (Diptera, Cecidomyiidae) from the restinga of Barra de Maricá (Rio de Janeiro, Brazil). Stud. Dipterol. 9, 447-452.
• Maia, V.C., Magenta, M.A.G., Martins, S.E., 2008. Ocorrência e caracterização de galhas de insetos em áreas de restinga de Bertioga (São Paulo, Brasil). Biota Neotrop. 8, 167-197.
• Mani, M.S., 1964. The Ecology of Plant Galls. Dr. Junk, The Hague, xii+434.
• Maia, V.C., Cardoso, L.J.T., Braga, J.M.A., 2014. Insect galls from Atlantic Forest areas of Santa Teresa, Espírito Santo, Brazil: characterization and occurrence. Boletim do MBML (N. Sér.) 33, 47-129.
• Malves, K., Frieiro-Costa, F.A., 2012. List of plants with galls induced by insects from the UNILAVRAS/Boqueirão Biological Reserve, Ingaí, State of Minas Gerais, Brazil. Check List 8, 426-431.
• Möhn, E., 1959. Gallmücken (Diptera, Itonididae) aus El Salvador. 1. Teil. Senckenbergiana Biologica 40, 297-368.
• Monteiro, R.F., Ferraz, F.F.F., Maia, V.C., Azevedo, M.A.P., 1994. Galhas entomógenas em restingas: uma abordagem preliminar. An. ACIESP 3, 210-220.
• Monteiro, R.F., Oda, R.A.M., Narahara, K.L., Constantino, P.A.L., 2004. Galhas: Diversidade, Especificidade e Distribuição. In: Rocha, C.F.D., Esteves, F.A., Scarano, F.R. (Eds.), Pesquisa de Longa Duração na Restinga de Jurubatiba: Ecologia, História Natural e Conservação. RiMa Editora, São Carlos, pp. 127–141.
• Narahara, K.L., Maia, V.C., Monteiro, R.F., 2004. Two new species of gall midges (Diptera, Cecidomyiidae) associated with Protium heptaphyllum (Aubl.) Marchand (Burseraceae) in Brazil. Rev. Bras. Entomol. 48, 485-490.
• Oliveira, J.C., Maia, V.C., 2005. Ocorrência e caracterização de galhas de insetos na restinga de Grumari (Rio de Janeiro, RJ, Brasil). Arq. Mus. Nac. 63, 669-676.
• Raman, A., 2007. Insect-induced plant galls of India: unresolved questions. Curr. Sci. 92, 748-757.
• Rizzini, C.T., 1979. Tratado de Fotogeografia do Brasil, Hucitec. v.2, São Paulo.
• Rodrigues, A.R., Maia, V.C., Couri, M.S., 2014. Insect galls of restinga areas of Ilha da Marambaia, Rio de Janeiro, Brazil. Rev. Bras. Entomol. 58, 173-197.
• Rübsaamen, E.H., 1907. Beitrage zur Kenntnis aussereuropaischer Zoocecidien. Ill. Beitrag: Gallen aus Brazilien und Peru. Marcellia 6, 110-173.
• Rübsaamen, E.H., 1916. Beitrag zur Kenntnis aussereuropäischer Gallmücken. Sitzungsberichte der Gesellschaft Naturforschender Freunde zu Berlin 1915., pp. 431–481.
• Ruschi, A., 1950. Fitogeografia do Estado do Espírito Santo. v.l.Considerações gerais sobre a distribuição da flora do Estado do Espírito Santo. Boletim do MBML. Sér. Botânica 1, 1-353.
• Saito, V.S., Urso-Guimarães, M.V., 2012. Characterization of galls, insect galls and associated fauna of Ecological Station of Jataí (Luiz Antônio, SP). Biota Neotrop. 12, 99-107.
• Santos, B.B., Ferreira, H.D., Araújo, W.S., 2010. Ocorrência e caracterização de galhas entomógenas em uma área de floresta estacional semidecídua em Goiânia, Goiás, Brasil. Acta Bot. Bras. 24, 243-249.
• Santos, J.C., Almeida-Cortez, J.S., Fernandes, G.W., 2011a. Diversity of gall-inducing insects in the high altitude wetland forests in Pernambuco, Northeastern, Brazil. Braz. J. Biol. 71, 47-56.
• Santos, J.C., Almeida-Cortez, J.S., Fernandes, G.W., 2011b. Richness of gall-inducing insects in the tropical dry forest (caatinga) of Pernambuco. Rev. Bras. Entomol. 55, 45-54.
• Shorthouse, J.D., Wool, D., Raman, A., 2005. Gall-inducing insects – nature's most sophisticated herbivores. Basic Appl. Ecol. 6, 407-411.
• Tavares, J.S., 1909. Contribution prima ad cognitionem cecidologiae Braziliae. Brotéria 5, 5-28.
• Tavares, J.S., 1916. Cecidomyias novas do Brazil. Brotéria 14, 36-57.
• Tavares, J.S., 1920. Cecidologia brazileira. Cecídias que se criam em plantas das famílias das Leguminosae, Sapotaceae, Lauraceae, Myrtaceae, Punicaceae, Aurantiaceae, Malpighiaceae, Sapindaceae, Umbelliferae, Loranthaceae, Apocynaceae, Urticaceae, Salicaceae e Graminae. Brotéria 18, 82-125.
• Toma, T.S.P., Mendonça, M.S., 2013. Gall-inducing insects of an Araucaria Forest in southern Brazil. Rev. Bras. Entomol. 57, 225-233.
• Urso-Guimarães, M.V., Scarelli-Santos, C., 2006. Galls and gall makers in plants from the Pé-de-Gigante Cerrado Reserve, Santa Rita do Passa Quatro, SP, Brazil. Braz. J. Biol. 66, 357-369.
• Urso-Guimarães, M.V., Scarelli-Santos, C., Bonifácio-Silva, A.C., 2003. Occurrence and characterization of entomogen galls in plants from natural vegetation areas in Delfinópolis, MG, Brazil. Braz. J. Biol. 63, 705-715.

Publication Dates

• Publication in this collection
  Jan-Mar 2016

History

• Received
  11 June 2015
• Accepted
  15 Sept 2015