Insect Galls of Restinga Areas of Ilha Da Marambaia, Rio De Janeiro, Brazil

Revista Brasileira de Entomologia http://dx.doi.org/10.1590/S0085-56262014000200010

Insect galls of restinga areas of Ilha da Marambaia, Rio de Janeiro, Brazil

Alene Ramos Rodrigues1,2, Valéria Cid Maia1 & Márcia Souto Couri1

1Museu Nacional, Universidade Federal do Rio de Janeiro, Quinta da Boa Vista, São Cristóvão, 20940–040 Rio de Janeiro-RJ, Brazil [email protected]

ABSTRACT. Insect galls of restinga areas of Ilha da Marambaia, Rio de Janeiro, Brazil. This study carried out an insect gall inventory in restinga areas of Ilha da Marambaia, in the municipality of Mangaratiba, Rio de Janeiro, Brazil. Sampling was carried out monthly from April 2010 to March 2011 along the full extension of seven beaches. A total number of 147 gall morphotypes associated with 70 plant species were found, distributed in 33 plant families, and at least 54 genera. Myrtaceae was the botanical family with the highest richness of gall morphotypes and host species, followed by Bignoniaceae, Fabaceae, Asteraceae, Euphorbiaceae, Sapindaceae, and Malpighiaceae. Most of the gall morphotypes occurred in leaves (78 morphotypes), 38 in stems, 14 in flowers, eight in buds and fruits, and one in adventitious roots. The galling insects belong to the five orders: Diptera, Coleoptera, Hemiptera, Lepidoptera, and Thysanoptera. Cecidomyiidae (Diptera) was the most common galling taxon (78 morphotypes), represented by 87 species, being 78 gallers, seven inquilines and two predators. In addition to the gallers, parasitoids, inquilines, and predators were also found.

KEYWORDS. Cecidomyiidae; Diptera; Insecta; insect-plant interation; inventory.

Insect galls are pathological structures originated from localities of Rio de Janeiro State, little information is availa- new formations of vegetal tissues, resulting from mechanic ble. and/or chemical stimuli of insects (Bronner 1992). The in- The present study was conducted in Ilha da Marambaia ductors are usually specific in relation to plant species, in- (Mangaratiba municipality, in southern Rio de Janeiro State). ducing galls only in one species or on a small group of host The relevance of this work is based on the ecological impor- species (Carneiro et al. 2009). The gall insects are repre- tance of the galling insects, on the scarce knowledge of taxo- sented by the following orders: Coleoptera, Diptera, Hemi- nomic, biological and geographical distribution of gallers ptera, Hymenoptera, Lepidoptera, and Thysanoptera. Diptera, throughout all Brazilian territory and on the fact that the veg- represented mainly by Cecidomyiidae, is the main group of etation of Ilha da Marambaia includes one of the last re- galling insects (Mani 1964). serves of the Atlantic Florest in southeastern Rio de Janeiro. Many galling species of Cecidomyiidae may reach the Furthermore, among the published insect gall inventories in level of pest. In Brazil, species are recorded attacking plants the State of Rio de Janeiro, only one surveyed its southern of cassava, guava and pitanga (Fernandes 1987; Maia 2001; portion (Oliveira & Maia 2005). Ângelo & Maia 1999). Predator and galling larvae of Cecidomyiidae have been used as biological control and MATERIAL AND METHODS fungivorous larvae serve as indicators of soil conditions (Gagné 1994; Mamaev 1968). The Brazilian ecosystems more Sampling was carried out monthly from April 2010 to investigated in relation to composition of Cecidomyiidae March 2011 by two researchers along the entire extension of fauna and diversity of galling insects are the Cerrado and seven beaches of Ilha da Marambaia (Mangaratiba, RJ), to- Atlantic Florest (more specifically, restingas), but these stud- taling 16 hours per month for all the beaches: Kutuca ies still represent a small fraction of the total area of these (23º4’4.85”S 43º59’39.41”W – 23º3’59.17”S 43º59’33.59”W, biomes. In the Rio de Janeiro State, insect galls inventories 285 meters), Grande (23º3’57.34”S 43º59’31.01”W – were carried out in restinga areas of Angra dos Reis (Ilha 23º3’27.08”S 43º59’28.63”W, 990 meters), Suja (23º3’21.81”S Grande), Rio de Janeiro (Grumari), Maricá, Carapebus, and 43º58’51.35”W – 23º2’48.29”S 43º58’28.69”W, 1,350 meters), Arraial do Cabo (Maia & Oliveira 2010; Oliveira & Maia Caju (23º2’39.85”S 43º57’54.96”W – 23º2’33.64”S 43º57’ 2005; Maia 2001; Monteiro et al. 1994, 2004). In these stud- 46.12”W, 370 meters), João Manoel (23º2’34.17”S 43º57’ ies, the richness of insect galls was evidenced and 44.18”W – 23º2’34.89”S 43º57’35.75”W, 260 meters), Sítio Cecidomyiidae pointed as the most frequent galling taxo- (23º2’34.83”S 43º57’30.80”W – 23º4’4.85”S 43º59’39.41”W, nomic group. The number of galls induced by Cecidomyiidae 400 meters), and Armação (23º2’27.43”S 43º57’15,53”W – was 36, 43, 76, 68, 99, and 93, respectively, with a total of 65 23º3’38.64”S 43º54’9.10”W, 3,960 meters) (Fig. 1). The described new species (Maia & Oliveira 2010; Oliveira & beaches were chosen due to their conservation condition (few Maia 2005; Maia 2001; Monteiro et al. 1994, 2004). For other buildings and good vegetation cover).

Revista Brasileira de Entomologia 58(2): 173–197, June 2014 174 Rodrigues et al.

Fig. 1. Map of Ilha da Marambaia (Mangaratiba, RJ, Brazil); adapted from Pereira et al. (1990). Red lines indicate the investigated beaches in this work.

At each beach, along its entire length, herbaceous, shrubby and to present satisfactory results. The excedent specimens and arboreous plants (with up to two meters high, galled or remained in 70% ethanol. The Cecidomyiidae were identi- not) were surveyed for insect galls, representing a vegeta- fied to genus level using the keys of Gagné (1994) and to tion sampling effort of 100%. Only aerial organs were inves- species based on original descriptions. All the specimens were tigated. All gall morphotypes were photographed in the field. deposited in the Diptera collection of the MNRJ. The other Each morphotype was characterized by the plant organ of insects were identified by specialists and were deposited in occurrence, shape, presence or absence of trichomes, com- the collection of their institutions. plexity, color, number of internal chamber, and galling in- The average number of gall morphotypes per host plant sect. The gall shape was based on Isaias et al. (2013), and the species was calculated using simple arithmetic mean. The differentiation between complex gall (with formation of new plant species and genera were considered super-host when plant tissues) and simple gall (without formation of other bearing a high richness of insect galls, according Espírito- tissues) was based on Möhn (1962). Santo & Fernandes (2007). The richness of galling species Branches (whenever possible with flowers and fruits) were of each beach was evaluated qualitatively, based on the num- removed from each host plant, and pressed in the field for ber of gall morphotypes. According to temporal occurrence, preparation of exsiccates. They were examined by botanists the morphotypes were classified as constant (greater than or of Museu Nacional (MNRJ), Universidade Federal do Rio equal to 50%), accessory (between 25% and 50%) and acci- de Janeiro and Universidade do Estado do Rio de Janeiro dental (less than or equal to 25%) as proposed by Silveira (UERJ) for species identification. The botanical material was Neto et al. (1976). The formula used was C% = (p/n) * 100, deposited in the herbarium of MNRJ. Galled branches were where “p” is the number of months that the gall morphotype collected and transported to laboratory in closed and labeled was collected and “n” is the total number of collecting months. plastic bags. To obtain the adults, samples of each gall morphotype were separately conditioned in closed transpar- RESULTS ent plastic pots, labeled and lined with wet paper. In the case of larvae that leave the galls, the rearing pots received a layer In the restinga areas of the Ilha da Marambaia, 147 gall of approximately 10 cm of restinga soil. The pots were morphotypes were found in 70 plant species, distributed in 33 checked every day for newly emerged adults. When adults families and at least 54 genera. The average number of gall were found, the pots were placed in a refrigerator for some morphotypes per host plant species was 2.1 (Table I). Fifty hours, to induced insect lethargy. The adults were transferred two insect gall morphotypes were first recorded from Brazil- to tubes with 70% ethanol. To observe the internal chamber(s) ian restinga areas. Myrtaceae, Bignoniaceae, and Fabaceae and remove immatures, some galls were dissected, using a presented the highest richness of galls (20, 13, and 11 stylet. Samples of each gall morphotype were dried for preser- morphotypes, respectively) and largest number of host plant vation and incorporated in the gall collection of MNRJ. The species (9, 4, and 6 species, respectively), followed by gall midges (Cecidomyiidae) were mounted in microscopy Asteraceae, Euphorbiaceae, Sapindaceae, Malpighiaceae, and slides following the methodology of Gagné (1994), except Nyctaginaceae (with 10, 10, 9, 9, and 8 morphotypes, respec- for using butyl acetate instead of clove oil, to be less toxic tively, Table II).

Revista Brasileira de Entomologia 58(2): 173–197, June 2014 Insect galls of restinga areas of Ilha da Marambaia, Rio de Janeiro, Brazil 175

Table I. Data from literature on insect gall inventories in restingas of Rio de Janeiro State (Maia & Oliveira 2010; Oliveira & Maia 2005; Maia 2001; Monteiro et al. 1994, 2004). Data for Carapebus and Jurubatiba cannot be joined together, as the Parque Nacional da Restinga de Jurubatiba (PNRJ) includes three municipalities (Macaé, Carapebus, and Quissamã) and the collection sites were not provided in the inventory. Ilha da Arraial do Marambaia Ilha Grande Grumari Maricá Carapebus Jurubatiba Cabo Number of morphotypes 147 36 43 76 68 99 93 Number of host plant species 70 22 25 39 33 40 44 Average number of morphotypes per host plant species 2.10 1.64 1.72 1.95 2.06 2.48 2.11 Plant families with the highest richness of galls Myrtaceae Myrtaceae Myrtaceae Myrtaceae Myrtaceae Myrtaceae Myrtaceae Bignoniaceae Asteraceae Erythroxylaceae Malpighiaceae Burseraceae Fabaceae Nyctaginaceae Sapotaceae Clusiaceae Asteraceae Super-host plant genera Eugenia Mikania Eugenia Eugenia Eugenia Eugenia Eugenia Fridericia Guapira Erythroxylum Guapira Protium Protium Guapira Guapira Mikania Best represented Cecidomyiidae genera Asphondylia Bruggmannia Neolasioptera Clinodiplosis Asphondylia Lopesia Neolasioptera Liodiplosis Asphondylia Asphondylia Clinosiplosis Asphondylia Lopesia Neolasioptera Contarinia Neolasioptera Stephomyia Stephomyia

Table II. Distribution of insect gall morphotypes per host plants and in restinga areas of Ilha da Marambaia (Mangaratiba, RJ), according to the present study. Plant Families Plant Species Number of gall morphotypes Grande Kutuca Suja Caju João Manoel Sítio Armação Anacardiaceae Schinus terebinthifolius 01 01 Annonaceae Xylopia involucrata 01 01 Apocynaceae Aspidosperma pyricollum 03 01 02 Asteraceae Mikania argyraea 03 03 Mikania biformis 02 02 02 02 02 Mikania micrantha 02 02 Porophyllum ruderale 01 01 Vernonia rufogrisea 02 02 Bignoniaceae Adenocalymma comosum 02 02 Bignoniaceae sp. 02 02 Fridericia conjugata 03 02 01 01 01 01 01 03 Fridericia rego 04 04 01 01 Boraginaceae Tournefortia sp. 01 01 01 Burseraceae Protium brasiliense 02 01 01 02 Protium icicariba 03 03 03 01 03 Cactaceae Selenicereus setaceus 01 01 01 01 01 01 01 01 Celastraceae Maytenus obtusifolia 03 01 01 02 02 01 01 01 Convolvulaceae Convolvulaceae sp. 01 01 01 01 Dilleniaceae Davilla rugosa 02 02 Euphorbiaceae Alchornea triplinervia 01 01 Chaetocarpus sp. 03 01 03 Croton compressus 02 01 01 02 01 01 Croton floribundus 03 02 01 Gymnanthes gaudichaudii 01 01 Fabaceae Andira fraxinifolia 02 01 01 01 02 01 Clitoria sp. 02 01 01 02 Dalbergia ecastophylla 01 01 01 01 01 01 01 01 Inga sp. 03 02 02 01 01 Stylosanthes guianensis 01 01 Zollernia glabra 02 01 02 Lauraceae Ocotea notata 02 02 Loranthaceae Struthanthus concinnus 02 02 02 02 01 Malpighiaceae Byrsonima sericea 05 02 01 02 05 Heteropterys nitida 01 01 01 01 Peixotoa sp. 01 01 01 01 Stigmaphyllon ciliatum 01 01 Malpighiaceae sp. 01 01 01 01 Malvaceae Luehea divaricata 04 04 04 Sida sp. 01 01 01 01 Continues

Revista Brasileira de Entomologia 58(2): 173–197, June 2014 176 Rodrigues et al.

Table II. Continued. Plant Families Plant Species Number of gall morphotypes Grande Kutuca Suja Caju João Manoel Sítio Armação Melastomataceae Miconia cinnamomifolia 02 02 Meliaceae Guarea guidonia 03 03 01 01 01 Moraceae Ficus sp. 01 01 Myrtaceae Calyptranthes brasiliensis 01 01 Eugenia copacabanensis 02 02 Eugenia punicifolia 04 03 02 03 04 02 03 03 Eugenia adstringens 02 02 Eugenia uniflora 04 02 03 02 02 02 02 02 Myrcia acuminatissima 01 01 Myrcia splendens 04 03 02 Myrtaceae sp. 01 01 Psidium guajava 01 01 01 Nyctaginaceae Guapira opposita 08 02 02 02 02 02 07 08 Ochnaceae Ouratea cuspidata 02 02 Olacaceae Ximenia americana 01 01 01 01 01 01 01 Polygalaceae Securidaca sp. 03 03 Polygonaceae Coccoloba alnifolia 01 01 01 Rubiaceae Borreria verticillata 01 01 01 01 Rubiaceae sp. 03 01 02 02 Salicaceae Casearia sp. 01 01 Sapindaceae Matayba guianensis 03 03 Serjania sp. 1 03 03 Serjania sp. 2 03 01 03 01 Sapotaceae Pouteria caimito 01 01 Pouteria venosa 01 01 01 Sideroxylon obtusifolium 01 01 Smilacaceae Smilax rufescens 04 03 03 03 01 01 01 04 Solanaceae Solanum sp. 02 01 02 Verbenaceae Lantana camara 02 02 02 Lantana lilacina 02 01 01 Stachytarpheta sp. 01 01 01 Total 147 38 48 60 25 26 36 74

Eugenia L., Fridericia Mart., Guapira Aubl., and Mikania occurred in a unique plant organ, with three exceptions: the Willd. were the super-host genera, presenting, 12, 9, 8, and 7 fusiform galls on leaves of Fridericia conjugata (Vell.) L.G. morphotypes, respectively. Two plant genera were first recorded Lohmann (Bignoniaceae), the conical galls on leaves of as insect gall hosts: Sida L. (Malvaceae) and Securidaca L. Struthanthus concinnus Mart. (Loranthaceae), and the fusi- (Polygalaceae). Fifteen plant species were first recorded as in- form galls on leaves of a non identified species of Malpighia- sect gall hosts: Adenocalymma comosum (Cham.) DC. ceae, which also occurred on stems in the three species and (Bignoniaceae); Calyptranthes brasiliensis Spreng. (Myrtaceae); on tendrils of the first species as well. Chaetocharpus echinocarpus (Baill.) Ducke (Euphorbiaceae); Thirteen gall shapes were detected, predominating the Coccoloba alnifolia Casar. (Polygonaceae); Davilla rugosa Poir. fusiform (n = 44), globoid (n = 40), lenticular (n = 18), and (Dilleniaceae); Eugenia punicifolia (Kunt) DC. (Myrtaceae); conical (n = 15 morphotypes). Only one morphotype pre- Fridericia rego (Vell.) L.G. Lohmann (Bignoniaceae); Guarea sented shape variation: from conical to ovoid on Eugenia guidonia (L.) Sleumer (Meliaceae); Gymnanthes gaudichaudii uniflora L. (Myrtaceae), being the former the most com- Müll.Arg. (Euphorbiaceae); Myrcia acuminatissima O. Berg. mon. Eighty-nine gall morphotypes were classified as (Myrtaceae); Myrcia splendens (SW.) DC. (Myrtaceae); Psidium simple and 55 morphotypes as complex. The morphotypes guajava L. (Myrtaceae); Stigmaphyllon ciliatum (Lam.) A. Juss. were green, brown, yellow, red, pink, orange, white or black, (Malpighiaceae); Xylopia involucrata M. C. Dias & Kin.-Gouv. with predominance of green color (48%). Thirty-five (Annonaceae); and Zolernia glabra (Spreng.) Yakovlev morphotypes presented color variation associated with the (Fabaceae). Twenty plants (28% of the total) could not be iden- ontogenetic process. The majority of galls was one-cham- tified to species level, as the exsiccates comprised only non fer- bered (75%), often occupied by a unique galling larva, ex- tile material. cept for the leaf conical gall on Eugenia uniflora Galls were found in leaves (n = 78), stems (n = 38), flow- (Myrtaceae) with two larvae in some samples. The gall char- ers (inflorescences and flower buds) (n = 14), buds (n = 8), acterization (shape, color, number of internal chamber, pres- fruits (n = 8), adventitious root (n = 1), with predominance ence or absence of trichomes, vegetal organ of occurrence, of 53% of leaf galls. The majority of the gall morphotypes complexity and inducers) is presented in Table III. The ac-

Revista Brasileira de Entomologia 58(2): 173–197, June 2014 Insect galls of restinga areas of Ilha da Marambaia, Rio de Janeiro, Brazil 177 Number Figure Fig. 14 Fig. Continues Maia, 2002 30 Fig. Maia, 2001 17 Fig. Asphondylia Gagné, 2001 Gagné, Fig.10 Maia, 2001 Maia, 33 Fig. Rodrigues & Rodrigues Maia, 2010 27 Fig. Gagné, 2001 Gagné, 11 Fig. Rübsaamen, 1905Rübsaamen, 32 Fig. serrata icicaribae Maia, 2001 29 Fig.

cerei sp. 18 Fig.

distincta sp. 26 Fig. sp. 16 Fig.

cylindrica spherica

maricaensis simplex

Asphondylia Asphondylia Arrabidaeamyia Liodiplosis Liodiplosis Neolasioptera Lopesia Lopesia Dactylodiplosis Neolasioptera Mayteniella Galler Cecidomyiinae, CecidomyiidaeCecidomyiinae, 9 Fig. Number ofNumber Internal Chambers ), in restinga areas of Ilha da Marambaia (Mangaratiba, RJ), according to ), RJ), in (Mangaratiba, according restinga of da Marambaia areas present study. the Ilha al chamber, trichomes, galled plant organ, and inducing insects trichomes, plant organ, galled al chamber, bud rosette green-brown glabrous complex multi undeterminated 41 Fig. budbud fusiform rosette green green-brown glabrous glabrous complex complex multi one undeterminated undeterminated 35 Fig. 37 Fig. leaf lenticular green-yellow glabrous simple one undeterminated 40 Fig. leaf roll marginal green glabrous simple one leafleafinflorescence conical fusiform conical green green green glabrous glabrous complex simple glabrous one complex multi oneleafleaf species of undescribed Cecidomyiidae Cecidomyiinae, conical roll marginal green green 13 Fig. glabrous glabrous simple complex one one Cecidomyiidi 28 Fig. leafleafleafleafleafopening lenticular lenticular green roll marginal fusiform yellow green glabrous globoid simple glabrous green-brown glabrous one green-brown simple hairy simple hairy simple one one complex Psyllidae, Hemiptera one one undeterminated undeterminated undeterminated 4 Fig. 5 Fig. 6 Fig. 8 Fig. leaf globoidleaf, stem and tendril greenfruit fusiformleafleaf glabrous peduncle greenflower simple – fusiform conical glabrous one fusiform simple green green brown one green glabrous glabrous glabrous glabrous simple complex simple simple one one one oneCecidomyiidae Cecidomyiinae, undeterminated undeterminated undeterminated 23 Fig. 20 Fig. 19 Fig. 21 Fig. leaf conical green glabrous complex one leaf lenticular green glabrous simple one fruit globoid yellow-orange glabrous simple one Cecidomyiidae Cecidomyiinae, 38 Fig. leafleaf fusiform conical green green glabrous glabrous simple complex one one undeterminated leaf lenticular yellow-green glabrous simple one Psyllidae, Hemiptera 31 Fig. stemstem fusiform globoid brown green glabrous glabrous simple complex one one Lepidoptera undeterminated 2 Fig. 3 Fig. stem fusiform brown glabrous simple one undeterminated 39 Fig. stemstemstem conical fusiform globoid green brown glabrous yellow complex glabrous glabrous one simple complex one multi Cecidomyiidae Cecidomyiinae, Diptera Tephritidae, 12 Fig. 15 Fig. stem fusiform green hairy simple multi Cecidomyiidae Cecidomyiinae, 7 Fig. stemstem fusiform fusiform green green glabrous simple glabrous multi simple one Alycaulini undeterminated 22 Fig. 25 Fig. stem globoid green glabrous simple multi stem fusiform green glabrous simple multi undeterminated 34 Fig. stem fusiform green glabrous simple multi undeterminated sp. sp. fruit globoid green glabrous simple multi triplinervia

Xylopia involucrata Aspidosperma pyricollum Alchornea Adenocalymma comosum Adenocalymma Protium brasiliensis Protium Mikania biformis Mikania micrantha ruderale Porophyllum icicariba Protium Mikania argyraea Fridericia rego Fridericia Maytenus obtusifolia Maytenus Davilla rugosa Davilla Fridericia conjugata Fridericia Schinnus terebinthifolius Schinnus Selenicereus setaceus Selenicereus Bignoniaceae sp.Bignoniaceae leaf fusiform green glabrous simple multi undeterminated 24 Fig. Tournefortia Chaetocarpus Vernonia rufogrisea Vernonia Anacardiaceae Annonaceae Apocynaceae Asteraceae Burseraceae Boraginaceae Dilleniaceae Euphorbiaceae Bignoniaceae Celastraceae Convolvulaceae sp. Convolvulaceae stem fusiform green glabrous simple one Alycaulini 36 Fig. Cactaceae Plant Families Plant Species Occurrence organ Gall Shape Color Trichomes Complexity Table III. Gall characterization (shape, color, number of number intern (shape, color, III. Gall characterization Table

Revista Brasileira de Entomologia 58(2): 173–197, June 2014 178 Rodrigues et al. Continues Number Fig. 63 Fig. Fig. 58 Fig. Fig. 53 Fig. Fig. 49 Fig. Fig. 46 Fig. Figure 42 Fig. Figs. 71–72 Figs. Santos & Maia, 2008 56 Fig. &Maia Couri, 1992 64 Fig. Lopesia Bruggmanniella Dactylodiplosis Maia, 2005 Maia, Maia, 2001 Maia, sp. sp. 55 Fig. maricaensis byrsonimae

sp.

sp. 60–61 Figs. sp. byrsonimae sp. 51 Fig.

grandis sp. 50 Fig. Asphondylia Asphondylia Asphondylia Dasineura Neolasioptera Neolasioptera Lestodiplosis Lopesia Lopesia Galler Contarinia Clinodiplosis Number of Internal of Number Chambers bud rosette green-red-brown glabrous complex one species of undescribed inflorescenceinflorescence globoid fusiformleaf green brown lenticular glabrous glabrous complex brown-green simple one hairy one simple Lepidoptera one Cecidomyiidae Cecidomyiinae, Cecidomyiidae Cecidomyiinae, 66 Fig. 65 Fig. 69 Fig. inflorescence globoid brown glabrous simple one leaf lenticular brown hairy simple one leaf and stemleaf conical green glabrous complex one leaf fusiform green glabrous simple one Curculionidae, Coleoptera leafinflorescence – fusiform green – hairy – simple one – – leaf lineal green glabrous complex one leafleaf globoid globoid green green glabrous glabrous simple complex multi one Curculionidae, Coleoptera 52 Fig. leaf globoid green glabrous complex one inflorescence amorphic yellow glabrous complex multi undeterminated 44 Fig. leafleaf roll marginal globoid green-white green-white hairy simple hairy complex one one undeterminated 45 Fig. leaf globoid red glabrous complex one undeterminated 77 Fig. leafleaf globoidleaf roll marginal brownleaf green fusiform glabrous complex globoid glabrous brown-green simple one yellow glabrous one simple Cecidomyiidae Cecidomyiinae, glabrous one complex undeterminated one 73 Fig. Cecidomyiidae Cecidomyiinae, Cecidomyiidae Cecidomyiinae, 79 Fig. flower budflower – – – – – Coleoptera Curculionidae, 68 Fig. adventitious root fusiform brown glabrous simple one Cecidomyiidae Cecidomyiinae, 62 Fig. fruit globoid yellow glabrous simple one species of undescribed flower budflower – pink glabrous simple one Coleoptera Curculionidae, 57 Fig. fruit globoid orange glabrous simple one undeterminated 48 Fig. stem fusiform brown glabrous simple multi Cecidomyiidae Cecidomyiinae, 67 Fig. stem fusiform brown glabrous simple multi undeterminated 70 Fig. stem fusiform brown glabrous simple multi undeterminated 59 Fig. stem fusiform green hairy simple multi stem fusiform green hairy simple multi undeterminated 47 Fig. stem fusiform green glabrous simple one Lepidoptera 43 Fig. stem globoid brown glabrous complex one undeterminated 78 Fig. stemstem globoid globoidstem brown green fusiform glabrous complex glabrous complex brown-green one one glabrous simple Cecidomyiidae Cecidomyiinae, one undeterminated 74 Fig. Cecidomyiidae Cecidomyiinae, 75 Fig. ciliatum

ecastophylla

sp. divaricata sp. leaf fold leaf green glabrous simple one

sp. leaf fold leaf green-red glabrous simple one Thysanoptera 80 Fig. sp. leaf globoid yellow hairy complex one Cecidomyiidae Cecidomyiinae, 54 Fig. sp. stem fusiform brown glabrous simple one Cecidomyiidae Cecidomyiinae, 76 Fig. Andira fraxinifolia Andira Heteropterys nitida Heteropterys Peixotoa Byrsonima sericea Byrsonima Dalbergia Inga Miconia cinnamomifolia Luehea Ficus Stigmaphyllon Struthanthus concinnus Zollernia glabra Stylosanthes guianensis Sida Malpighiaceae sp.Malpighiaceae stem and leaf fusiform brown-green-yellow glabrous simple one-multi of species undescribed Ocotea notata Ocotea Clitoria Gymnanthes gaudichaudii Gymnanthes Croton compressus Croton floribundus Croton Guarea guidonia Guarea Malpighiaceae Loranthaceae Lauraceae Fabaceae Fabaceae Melastomataceae Malvaceae Meliaceae Moraceae Plant Families Plant Species Occurrence organ Gall Shape Color Trichomes Complexity Table III. Continued. Table

Revista Brasileira de Entomologia 58(2): 173–197, June 2014 Insect galls of restinga areas of Ilha da Marambaia, Rio de Janeiro, Brazil 179 Number Fig. 112 Fig. Figure Fig. 83 Fig. Fig. 100 Fig. Fig. 102 Fig. Fig. 105 Fig. Continues Maia & Couri, 1993& Couri, Maia 103 Fig. Maia, 1993 89 Fig. Maia, 2004 Pisphondylia Maia & Couri, 1993& Couri, Maia 108 Fig. Maia & Couri, 1993 98 Fig. Rübsaamen, 1905 Rübsaamen, 113 Fig. Maia & Couri, 1993& Couri, Maia 99 Fig. Maia, 2005 Maia, 82 Fig. Maia, 2001 90 Fig. Maia, 1993 84 Fig. Maia, 1995 guapirae

eugeniae elongata robusta acaudata

profusa

sp.

borreriae communis

espiralis

sp. 85 Fig. marginalis globosa sp. 106 Fig.

sp. Asphondylia Asphondylia Lopesia Dasineura Dasineura Neolasioptera Bruggmannia Bruggmannia Bruggmannia Bruggmannia Proasphondylia Stephomyia Stephomyia Galler Clinodiplosis Contarinia Number of Internal Chambers bud conical green-brown glabrous complex multi undeterminated 81 Fig. bud globoid green-brown glabrous complex multi undeterminated 95 Fig. bud fusiform brown glabrous simple one leaf globoid green glabrous complex one undeterminated 116 Fig. inflorescence drop-like green glabrous complex one leafinflorescence globoid cylindrical green yellow-green glabrous complex glabrous complex one one undeterminated 110 Fig. leaf cylindrical yellow glabrous complex one Lestodiplosiini 119 Fig. leaf roll marginal green glabrous simple one leaf lenticular green glabrous simple one leaf spiral green-red glabrous complex one leafleaf lenticular cylindrical green yellow-green glabrous glabrous complex simple one one undeterminated leaf lenticular green-red glabrous simple one Cecidomyiidae Cecidomyiinae, 86 Fig. leaf lenticular green-black glabrous simple one leaf conical green-red glabrous complex one leafleafleaf fold leaf leaf globoid roll marginal leaf conical green lenticular green green glabrous simple glabrous yellow-green glabrous glabrous one simple complex green-red complex one one glabrous oneCecidomyiidae Cecidomyiinae, simple undeterminated undeterminated one undeterminated 91 Fig. 93 Fig. 94 Fig. leaf globoid red glabrous complex one leaf globoid brown glabrous complex one leafleaf globoid conical green green-red glabrous glabrous complex complex one one Cecidomyiidae Cecidomyiinae, 101 Fig. leafleaf withprojection apical cylindrical brown lenticular glabrous complex one green glabrous simple one Cecidomyiidae Cecidomyiinae, 107 Fig. fruit – green glabrous simple one undeterminated 115 Fig. fruit globoid red-yellow glabrous simple multi undeterminated 88 Fig. flower peduncleflower globoid green-red-brown glabrous complex one of species undescribed stem fusiform brown glabrous simple multi undeterminated 117 Fig. stem cylindrical green glabrous complex one undeterminated 111 Fig. stem fusiform brown glabrous simple multi undeterminated stem fusiform brown glabrous simple multi Lasiopteridi 87 Fig. stem fusiform brown glabrous simple multi undeterminated 96 Fig. stemstem fusiform globoid brown brown glabrous glabrous simple simple – multi undeterminated undeterminated 92 Fig. stem globoid brown glabrous simple multi stem globoid brown glabrous complex one undeterminated 104 Fig. sp. bud flower – – – – – Cecidomyiidae Cecidomyiinae, 109 Fig. sp. leaf conical brown glabrous simple one undeterminated 114 Fig. sp. 1 leaf fusiform green glabrous simple one Muscomorpha 118 Fig. Ximenia americana Ximenia Matayba guianensis Borreria verticillataBorreria Eugenia adstringensEugenia Eugenia copacabanensis Eugenia Eugenia punicifolia Eugenia Eugenia uniflora Eugenia Psidium guajava Myrcia acuminatissima Myrcia splendens Myrcia Serjania Securidaca Myrtaceae sp.Myrtaceae leaf lenticular green glabrous simple one undeterminated 97 Fig. Ouratea cuspidata Ouratea Casearia Coccoloba alnifolia Coccoloba Calyptranthes brasiliensis Calyptranthes Guapira opposita Guapira Nyctaginaceae Rubiaceae Polygalaceae Polygonaceae Myrtaceae Olacaceae Ochnaceae Sapindaceae Salicaceae Plant Families Plant Species Occurrence organ Gall Shape Color Trichomes Complexity Table III. Continued. Table

Revista Brasileira de Entomologia 58(2): 173–197, June 2014 180 Rodrigues et al.

cidental gall morphotypes predominated with 61% (90 morphotypes), followed by constant and accessory (with Number Fig. 134 Fig. Fig. 124 Fig. Figure 123 Fig. 37 and 20 morphotypes, respectively). The fusiform gall on Fridericia conjugata was constant on stems, accessory on tendrils, and accidental in leaf veins. Thirteen morphotypes were founded in all months, and 62 were founded only in a single month. Rübsaamen, 1907 Rübsaamen, Barnes, 1932 Barnes, 136 Fig. Möhn, 1975 Möhn, 125 Fig. The galling insects were distributed in five orders: Diptera Asphondylia Bruggmanniella

Maia, 2001 (n = 82), Coleoptera (n = 4), Lepidoptera (n = 4), Hemiptera lantanae Maia, 2001 Maia, (n = 3), and Thysanoptera (n = 1), being Cecidomyiidae candelariae

pouteriae (Diptera) the main galling group (n = 80), with 85% of the stachytarpheta

singularis total (Table IV). The inducers of 53 morphotypes (37% of

the total) were not identified, due to high rates of parasitism Asphodylia Lopesia Smilasioptera Schismatodiplosis Galler Youngomyia and to the fact that some collected galls were already unoc- cupied. In addition to gallers, other arthropods were associated with the galls: parasitoids, represented exclusively by Hymenoptera (in 54 morphotypes); inquilines, represented by Cecidomyiidae (Diptera), Lepidoptera, Curculionidae Number of Internal Chambers (Coleoptera), Thysanoptera, Sciaridae, Tephritidae (Diptera), and Aphididae (Hemiptera) (in 6, 5, 3, 3, 1, 1, and 1 morphotypes, respectively); and predators, represented by Cecidomyiidae (in two morphotypes) and Pseudoscorpiones (Arachnida) (in only one morphotype). Fifty-one species of gall midges were identified, distributed in at least 20 genera. The best represented genera were Asphondylia Loew, 1850, Lopesia Rübsaamen, 1908 and Neolasioptera Felt, 1908 (with at least 10, 7, and 5 species, respectively). Thirty-four other cecidomyiids were identified only to suprageneric levels (4 to tribe, 3 to supertribe, and 27 to subfamily), due to the scarcity of material (absence of one of the sexes and/or of immature specimens). Among the gall midges, 49 species were gallers, 6 inquilines and two predators.

Table IV. Distribution of the number of gall morphotypes per galling insect order in restinga areas of Ilha da Marambaia (Mangaratiba, RJ), according to the present study. Morphotypes of Galls Order of insects gallers Number Pecentage (%) Diptera 82 87 Cecidomyiidae 80 85 Tephritidae 1 1 Muscomorpha 1 1 Coleoptera 4 4 Lepidoptera 4 4 bud globoid brown glabrous complex one undeterminated 132 Fig. leaf cylindrical green hairy complex one undeterminated 135 Fig. leafleaf conical fusiform green green-red glabrous glabrous simple complex one one Hemiptera Cecidomyiidae Cecidomyiinae, 127 Fig. 126 Fig. leaf lenticular green-yellow-red glabrous simple one leaf lenticular green glabrous simple one leaf conical green glabrous complex one leaf petioleleaf fusiform lenticular green-yellow green-yellow glabrous glabrous simple simple one one undeterminated undeterminated 122 Fig. 121 Fig. leaf globoid green hairy complex one of species undescribed leaf globoid green hairy complex one fruit globoid green glabrous simple multi of species undescribed stem fusiform brown-green hairy simple one undeterminated 133 Fig. stem globoid green-red glabrous simple multi undeterminated 128 Fig. stemstem fusiform fusiformHemiptera green green hairy simple glabrous simple one multi3 undeterminated undeterminated 3 130 Fig. Thysanoptera 1 1 sp. inflorescence globoid green hairy complex one The Armação beach showed the greatest diversity of galls sp. leaf lenticular green glabrous simple one undeterminated 129 Fig. sp. 2 leaf fusiform green-yellow glabrous simpleand one host plants, Cecidomyiidae Cecidomyiinae, with 75 different 120 Fig. morphotypes in 38 host species, followed by the beaches Suja, Kutuca, Grande, Sítio, Pouteria caimito Pouteria Lantana lilacina Lantana camara Stachytarpheta Smilax rufescens Smilax Serjania Solanum Sideroxylon obtusifolium Sideroxylon Solanaceae sp.Solanaceae leaf lenticularJoão Manoel, and green Caju, with glabrous respectively simple one 60, 48, 38, Lepidoptera 36, 26 131 Fig. and 25 morphotypes, and 35, 33, 26, 21, 16 and 17 host plants (Table II). The majority of the galls occurred in a single beach (81 morphotypes); 29 in two beaches, 37 in three or more beaches, and only 5.4% occurred in all the investigated Verbenaceae Smilacaceae Sapotaceae Solanaceae Plant Families Plant Species Occurrence organ Gall Shape Color Trichomes Complexity Table III. Continued. Table beaches.

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Gall Characterization Gall (Fig. 9): on leaf, globoid, green-brown, hairy, complex, one-chambered. Galler: Cecidomyiinae (Diptera, Anacardiaceae Cecidomyiidae). Associated fauna: Hymenoptera parasitoid. Schinus terebintifolius Raddi Locality: Suja Beach. Occurrence period: December 2010. Temporal constancy: accidental. Previous records from Bra- Gall (Fig. 2): on stem, fusiform, brown, glabrous, simple, zilian restinga areas: Bertioga (Maia et al. 2008). one-chambered. Galler: Lepidoptera. Locality: Armação Beach. Occurrence period: December 2010. Temporal con- Mikania biformis DC. stancy: accidental. Previous records from Brazilian restinga areas: Cabo Frio, Bertioga and Grumari (Maia 2013; Maia et Gall (Fig. 10): on leaf, conical, green, glabrous, simple, al. 2008; Oliveira & Maia 2005). one-chambered. Galler: Liodiplosis cylindrica Gagné, 2001 (Diptera, Cecidomyiidae). Associated fauna: Hymenoptera Annonaceae parasitoid. Localities: Suja, João Manoel, Sítio and Armação Beaches. Occurrence period: April, December 2010, Janu- Xylopia involucrata M. C. Dias & Kin.-Gouv. ary and February 2011. Temporal constancy: accessory. Pre- vious records from Brazilian restinga areas: Bertioga (Maia Gall (Fig. 3): on stem, fusiform, green, glabrous, com- et al. 2008). plex, one-chambered. Galler: undetermined. Locality: Gall (Fig. 11): on leaf, globoid, green, glabrous, simple, Armação Beach. Occurrence period: September 2010. Tem- one-chambered. Galler: Liodiplosis spherica Gagné, 2001 poral constancy: accidental. (Diptera, Cecidomyiidae). Localities: Suja, João Manoel, Sítio This is the first record of insect galls in this plant species. and Armação Beaches. Occurrence period: May, December 2010, January and February 2011. Temporal constancy: ac- Apocynaceae cessory. Previous records from Brazilian restinga areas: Aspidosperma pyricollum Müll. Arg. Bertioga (Maia et al. 2008).

Gall (Fig. 4): on leaf, lenticular, permanently open, green, Mikania micrantha Kunt. glabrous, simple, one-chambered. Galler: Psyllidae (Hemi- ptera). Locality: João Manoel Beach. Occurrence period: Gall (Fig. 12): on stem, conical, green, glabrous, com- April, May, December 2010, February and March 2011. Tem- plex, one-chambered. Galler: Cecidomyiinae (Diptera, poral constancy: accessory. Previous records from Brazilian Cecidomyiidae). Locality: Armação Beach. Occurrence pe- restinga areas: Ilha Grande and Maricá (Maia & Oliveira riod: December 2010, January, February and March 2011. 2010; Maia 2001; Monteiro et al. 1994). Temporal constancy: accessory. No previous records from Gall (Fig. 5): on leaf, lenticular, yellow, glabrous, simple, Brazilian restinga areas. one-chambered. Galler: undetermined. Locality: Sítio Beach. Gall (Fig. 13): on leaf, conical, green, glabrous, complex, Occurrence period: November 2010. Temporal constancy: ac- one-chambered. Galler: Cecidomyiinae (Diptera, Cecidomyi- cidental. No previous records from Brazilian restinga areas. idae). Localities: Armação Beach. Occurrence period: Janu- Gall (Fig. 6): on leaf, marginal roll, green, glabrous, ary and February 2011. Temporal constancy: accidental. No simple, one-chambered. Galler: undetermined. Locality: João previous records from Brazilian restinga areas. Manoel Beach. Occurrence period: November 2010. Tem- poral constancy: accidental. No previous records from Bra- Porophyllum ruderale (Jack.) Cass. zilian restinga areas. Gall (Fig. 14): on inflorescence, fusiform, green, glabrous, Asteraceae simple, multi-chambered. Galler: undescribed species of Mikania argyreiae DC. Asphondylia (Diptera, Cecidomyiidae). Associated fauna: Trypanea sp. (Diptera, Tephritidae) inquiline. Locality: Gall (Fig. 7): on stem, fusiform, green, hairy, simple, Armação Beach. Occurrence period: December 2010, Janu- multi-chambered. Galler: Cecidomyiinae (Diptera, Ceci- ary, February and March 2011. Temporal constancy: acces- domyiidae). Locality: Suja Beach. Occurrence period: De- sory. No previous records from Brazilian restinga areas. cember 2010. Temporal constancy: accidental. Previous records from Brazilian restinga areas: Bertioga (Maia et al. Vernonia rufogrisea St. Hill. 2008). Gall (Fig. 8): on leaf vein, fusiform, green-brown, hairy, Gall (Fig. 15): on stem, fusiform, brown, glabrous, simple, simple, one-chambered. Galler: undetermined. Locality: Suja one-chambered. Galler: Tephritidae (Diptera). Locality: Beach. Occurrence period: December 2010. Temporal con- Grande Beach. Occurrence period: December 2010, Janu- stancy: accidental. No previous records from Brazilian ary and February 2011. Temporal constancy: accidental. No restinga areas. previous records from Brazilian restinga areas.

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Gall (Fig. 16): stem, globoid, yellow, glabrous, complex, fauna: Hymenoptera parasitoid. Locality: Suja Beach. Oc- multi-chambered. Galler: Asphondylia sp. (Diptera, currence period: March 2011. Temporal constancy: acciden- Cecidomyiidae). Associated fauna: Sciaridae (Diptera) and tal. Resseliella sp. (Diptera, Cecidomyiidae) inquilines; and Hy- Gall (Fig. 21): on leaf vein, fusiform, green, glabrous, menoptera parasitoid. Locality: Grande Beach. Occurrence simple, one-chambered. Galler: undeterminated. Locality: period: December 2010, January and February 2011. Tem- Suja Beach. Occurrence period: February 2011. Temporal poral constancy: accidental. No previous records from Bra- constancy: accidental. zilian restinga areas. Gall (Fig. 22): on stem, fusiform, green, glabrous, simple, multi-chambered. Galler: Alycauliini (Diptera, Cecidomyiidae). Bignoniaceae Associated fauna: Hymenoptera parasitoid. Localities: Suja, Sítio Adenocalymma comosum (Cham.) DC. and Armação Beaches. Occurrence period: March 2011. Tem- poral constancy: accidental. Gall: on leaf vein, fusiform, green, glabrous, simple, one- Gall (Fig. 23): on flower peduncle, fusiform, green, gla- chambered. Galler: undeterminated. Locality: Suja Beach. Oc- brous, simple, one-chambered. Galler: Cecidomyiidae currence period: January 2011. Temporal constancy: accidental. (Diptera). Locality: Suja Beach. Occurrence period: Febru- Gall: on stem, fusiform, green, glabrous, simple, multi- ary and March 2011. Temporal constancy: accidental. chambered. Galler: undeterminated. Localities: Suja and This is the first record of insect galls in this plant species. Armação Beaches. Occurrence period: January 2011. Tem- poral constancy: accidental. Bignoniaceae sp. This is the first record of insect galls in this plant species. Gall (Fig. 24): on leaf vein, fusiform, green, glabrous, Fridericia conjugata (Vell.) L.G. Lohmann (= simple, one-chambered. Galler: undeterminated. Locality: Arrabidaea conjugata (Vell.) Mart.) Suja Beach. Occurrence period: March 2011. Temporal constancy: accidental. Gall (Fig. 17): on leaf, conical, green, glabrous, com- Gall (Fig. 25): on stem, fusiform, green, glabrous, simple, plex, one-chambered. Galler: Arrabidaeamyia serrata Maia, multi-chambered. Galler: undeterminated. Locality: Suja 2001 (Diptera, Cecidomyiidae). Localities: Grande and Beach. Occurrence period: March 2011. Temporal constancy: Armação Beaches. Occurrence period: April and May 2010. accidental. Temporal constancy: accidental. Previous records from Bra- zilian restinga areas: Grumari, Maricá, Arraial do Cabo, Boraginaceae Carapebus, and Jurubatiba (Oliveira & Maia 2005; Maia Tournefortia sp. 2001; Monteiro et al. 1994, 2004) Gall: on stem (Fig. 18), tendril and vein, fusiform, green, Gall (Fig. 26): on fruit, globoid, green, glabrous, simple, glabrous, simple, one or multi-chambered. Galler: Neolasiop- multi-chambered. Galler: Asphondylia sp. (Diptera, tera sp. (Diptera, Cecidomyiidae). Associated fauna: Cecidomyiidae). Associated fauna: Hymenoptera parasitoid. Lestodiplosis sp. (Cecidomyiidae, Diptera) and Cecidomyiidae Localities: Grande and Kutuca Beaches. Occurrence period: sp. inquilines of stem gall, and Hymenoptera parasitoid of stem December 2010, January February and March 2011. Tempo- and tendril galls. Localities: Grande, Kutuca, Suja, Caju, João ral constancy: accessory. No previous records from Brazil- Manoel, Sítio and Armação Beaches. Occurrence period: April, ian restinga areas. May, July, August, September, October, November, Decem- ber 2010, January and March 2011. Temporal constancy: con- Burseraceae stant on the stem, accessory on the tendril and accidental on the vein. Previous records from Brazilian restinga areas: Protium brasiliensis (Spr.) Engl. Grumari, Maricá, Carapebus, and Jurubatiba (Oliveira & Maia 2005; Maia 2001; Monteiro et al. 1994, 2004). Gall (Fig. 27): on leaf, marginal roll, green, glabrous, Gall (Fig. 19): on fruit, brown, glabrous, simple, one- simple, one-chambered. Galler: Lopesia maricaensis Ro- chambered. Galler: undeterminated. Associated fauna: Hy- drigues & Maia, 2010 (Diptera, Cecidomyiidae). Locality: menoptera parasitoid, Coleoptera and Lepidoptera inquilines. Suja Beach. Occurrence period: December 2010. Temporal Locatity: Armação Beach. Occurrence period: November constancy: accidental. Previous records from Brazilian 2010. Temporal constancy: accidental. No previous records restinga areas: Maricá (Maia 2001; Rodrigues & Maia 2010). from Brazilian restinga areas. Gall (Fig. 28): on leaf, conical, green, glabrous, complex, one-chambered. Galler: Cecidomyiidi (Diptera, Fridericia rego (Vell.) L.G. Lohmann Cecidomyiidae). Localities: Grande, Kutuca and Suja Beaches. Occurrence period: December 2010, January and Gall (Fig. 20): on leaf, conical, green, glabrous, com- March 2011. Temporal constancy: accidental. Previous plex, one-chambered. Galler: undeterminated. Associated records from Brazilian restinga areas: Maricá (Maia 2001).

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Figs. 2–29. Galls of restinga areas of Ilha da Marambaia (Mangaratiba, RJ, Brazil). 2, Schinus terebintifolius, stem gall. 3, Xylopia involucrata, globoid stem gall. 4–6, Aspidosperma pyricollum: 4, lenticular leaf gall; 5, yellow lenticular leaf gall; 6, marginal roll gall, arrow pointing to gall. 7–9, Mikania argyraea: 7, stem gall; 8, leaf vein gall; 9, globoid leaf gall. 10–11, Mikania biformis: 10, conical leaf gall; 11, globoid leaf gall. 12–13, Mikania micrantha: 12, conical stem gall; 13, conical leaf gall. 14, Porophyllum ruderale, gall on inflorescence. 15–16, Vernonia rufogrisea: 15, stem gall; 16, globoid stem gall. 17–19, Fridericia conjugata: 17, conical leaf gall; 18, stem gall, arrow pointing to gall; 19, gall on fruit. 20–23, Fridericia rego: 20, conical leaf gall; 21, leaf vein gall; 22, stem gall; 23, gall on flower peduncle. 24–25, Bignoniaceae sp.: 24, leaf vein gall; 25, stem gall. 26, Tournefortia sp., gall on fruit. 27–28, Protium brasiliensis: 27, marginal roll leaf; 28, conical leaf gall. 29, Protium icicariba, marginal roll leaf.

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Protium icicariba (DC.) Marchand period: February 2011. Temporal constancy: accidental. No previous records from Brazilian restinga areas. Gall (Fig. 29): on leaf, marginal roll, green, glabrous, Gall (Fig. 35): on bud, fusiform, green, glabrous, simple, simple, one-chambered. Galler: Lopesia simplex Maia, 2001 multi-chambered. Galler: undeterminated. Associated fauna: (Diptera, Cecidomyiidae). Localities: Grande, Kutuca, Suja Hymenoptera parasitoid. Locality: Suja Beach. Occurrence and Armação Beaches. Occurrence period: April, May, Oc- period: December 2010. Temporal constancy: accidental. No tober, December 2010, February and March 2011. Temporal previous records from Brazilian restinga areas. constancy: constant. Previous records from Brazilian restinga areas: Guarapari, Jurubatiba, and Carapebus (Bregonci et al. Convolvulaceae 2010; Monteiro et al. 2004; Maia 2001). Convolvulaceae sp. Gall (Fig. 30): on leaf, conical, green, glabrous, complex, one-chambered. Galler: Dactylodiplosis icicaribae Gall (Fig. 36): on stem, fusiform, green, glabrous, simple, Maia, 2002 (Diptera, Cecidomyiidae). Localities: Grande, one-chambered. Galler: Alycaulini (Diptera, Cecidomyiidae). Kutuca and Armação Beaches. Occurrence period: April, Locality: Grande, Suja, Sítio Beaches. Occurrence period: October, December 2010, February and March 2011. Tem- November, December 2010, January, February and March poral constancy: accessory. Previous records from Brazilian 2011. Temporal constancy: accessory. No previous records restinga areas: Jurubatiba, and Carapebus (Monteiro et al. from Brazilian restinga areas. 2004; Maia 2001) Gall (Fig. 31): on leaf, lenticular, green-yellow, glabrous, Dilleniaceae simple, one-chambered. Galler: Psyllidae (Hemiptera). Lo- Davilla rugosa Poir. calities: Grande, Kutuca and Armação Beaches. Occurrence period: April, May, July, Agust, Setember, October, Novem- Gall (Fig. 37): on bud, rosette, green-brown, hairy, com- ber, December 2010, January, February and March 2011. plex, one-chambered. Galler: undeterminated. Locality: Temporal constancy: constant. Previous records from Bra- Kutuca Beach. Occurrence period: June and October 2010. zilian restinga areas: Guarapari, and Jurubatiba (Bregonci et Temporal constancy: accidental. al. 2010; Monteiro et al. 2004). Gall (Fig. 38): on fruit, globoid, yellow-orange, simple, one-chambered. Galler: Cecidomyiidae (Diptera). Associated Cactaceae fauna: Hymenoptera parasitoid. Locality: Kutuca Beach. Selenicereus setaceus (SD) Berg Occurrence period: June, August, Setember, October and November 2010. Temporal constancy: accessory. Gall (Fig. 32): on stem, globoid, green, glabrous, simple, This is the first record of insect galls in this plant species. multi-chambered. Galler: Neolasioptera cerei Rübsaamen, 1905 (Diptera, Cecidomyiidae). Associated fauna: Hy- Euphorbiaceae menoptera parasitoid. Localities: Grande, Kutuca, Suja, Caju, Alchornea triplinervia (Spreng.) Müll. Arg. João Manoel, Sítio and Armação Beaches. Occurrence period: April 2010 to March 2011. Temporal constancy: con- Gall (Fig. 39): on stem, fusiform, brown, glabrous, simple, stant. Previous records from Brazilian restinga areas: Ilha multi-chambered. Galler: Cecidomyiidae (Diptera). Local- Grande, Jurubatiba, Maricá, and Carapebus (Maia & Oliveira ity: Suja Beach. Occurrence period: December 2010. Tem- 2010; Monteiro et al. 2004; Maia 2001). poral constancy: accidental. Previous records from Brazilian restinga areas: Bertioga (Maia et al. 2008). Celastraceae Maytenus obtusifolia Mart. Chaetocharpus echinocarpus (Baill.) Ducke

Gall (Fig. 33): on leaf, lenticular, green, glabrous, simple, Gall (Fig. 40): on leaf, lenticular, gree-yellow, glabrous, one-chambered. Galler: Mayteniella distincta Maia, 2001 simple, one-chambered. Galler: undeterminated. Locality: (Diptera, Cecidomyiidae). Associated fauna: Hymenoptera Armação Beach. Occurrence period: May 2010 and January parasitoid. Localities: Grande, Kutuca, Suja, Caju, João 2011. Temporal constancy: accidental. Manoel, Sítio and Armação Beaches. Occurrence period: Gall (Fig. 41): on bud, rosette, green-brown, glabrous, April 2010 to March 2011. Temporal constancy: constant. complex, multi-chambered. Galler: undeterminated. Asso- Previous records from Brazilian restinga areas: Grumari, ciated fauna: Hymenoptera parasitoid. Localities: Grande and Maricá, Carapebus, Arraial do Cabo, and Jurubatiba (Oliveira Armação Beaches. Occurrence period: August, October, & Maia 2005; Maia 2001; Monteiro et al. 1994, 2004). November, December 2010, January, February and March Gall (Fig. 34): on stem, fusiform, green, glabrous, simple, 2011. Temporal constancy: constant. multi-chambered. Galler: undeterminated. Associated fauna: Gall (Fig. 42): on bud, rosette, green-red-brown, glabrous, Hymenoptera parasitoid. Locality: Caju Beach. Occurrence complex, one-chambered. Galler: undescribed species of

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Figs. 30–57. Galls of restinga areas of Ilha da Marambaia (Mangaratiba, RJ, Brazil). 30–31, Protium icicariba: 30, conical leaf gall; 31, lenticular leaf gall. 32, Selenicereus setaceus, stem gall. 33–35, Maytenus obtusifolia: 33, lenticular leaf gall; 34, stem gall; 35, bud gall. 36, Convolvulaceae sp., stem gall. 37–38, Davilla rugosa: 37, rosette bud gall; 38, gall on fruit. 39, Alchornea triplinervia, stem gall, arrow pointing to gall. 40–42, Chaetocarpus echinocarpus: 40, lenticular leaf gall, arrow pointing to gall; 41–42, rosette bud galls. 43–44, Croton compressus: 43, stem gall; 44, gall on inflorescence. 45–47, Croton floribundus: 45, marginal roll leaf; 46, globoid leaf gall; 47, stem gall. 48, Gymnanthes gaudichaudii, gall on fruit. 49–50, Andira fraxinifolia: 49, globoid leaf gall; 50, lineal leaf gall. 51–52, Clitoria sp.: 51, leaf fold, arrow pointing to inducing larva; 52, globoid leaf gall. 53, Dalbergia ecastaphyllum, globoid leaf gall. 54–55, Inga sp.: 54, globoid leaf gall; 55, leaf vein gall. 56, Stylosanthes guianensis, inflorescence. 57, Zollernia glabra, gall on flower bud.

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Dactylodiplosis (Diptera, Cecidomyiidae). Locality: Armação accessory. Previous records from Brazilian restinga areas: Beach. Occurrence period: November 2010, January and Bertioga (Maia et al. 2008). February 2011. Temporal constancy: accidental. Gall (Fig. 50): on leaf, lineal, green, glabrous, complex, This is the first record of insect galls in this plant species. one-chambered. Galler: Lopesia sp. (Diptera, Cecidomyi- idae). Associated fauna: Cecidomyiinae sp. (Diptera, Croton compressus Lam. Cecidomyiidae) inquiline and Hymenoptera parasitoid. Lo- calities: Grande, Kutuca, Suja, Sítio and Armação Beaches. Gall (Fig. 43): on stem, fusiform, green, hairy, simple, Occurrence period: April 2010 to March 2011. Temporal one-chambered. Galler: Lepidoptera. Localities: Kutuca, constancy: constant. Previous records from Brazilian restinga Suja, Sítio and Armação Beaches. Occurrence period: De- areas: Bertioga (Maia et al. 2008). cember 2010 and January 2011. Temporal constancy: accidental. Previous records from Brazilian resting areas: Cabo Clitoria sp. Frio (Maia 2013). Gall (Fig. 44): on inflorescence, amorphic, yellow, hairy, Gall (Fig. 51): on leaf fold, green, glabrous, simple, one- complex, multi-chambered. Galler: undeterminated. Asso- chambered. Galler: Contarinia sp. (Diptera, Cecidomyiidae). ciated fauna: Curculionidae (Coleoptera) inquiline and Hy- Locality: Armação Beach. Occurrence period: October, No- menoptera parasitoid. Localities: Grande and Suja Beaches. vember 2010 and March 2011. Temporal constancy: acci- Occurrence period: January and February 2011. Temporal dental. No previous records from Brazilian restinga areas. constancy: accidental. No previous records from Brazilian Gall (Fig. 52): on leaf, globoid, green, glabrous, simple, restinga areas. multi-chambered. Galler: Curculionidae (Coleoptera). Asso- ciated fauna: Hymenoptera parasitoid. Localities: Grande, Croton floribundus Spreng. Suja and Armação Beaches. Occurrence period: December 2010 and March 2010. Temporal constancy: accidental. No Gall (Fig. 45): on leaf, marginal roll, green-white, hairy, previous records from Brazilian restinga areas. simple, one-chambered. Galler: undeterminated. Locality: Kutuca Beach. Occurrence period: March 2011. Temporal Dalbergia ecastaphyllum L. Taub. constancy: accidental. No previous records from Brazilian restinga areas. Gall (Fig. 53): on leaf, globoid, green, glabrous, com- Gall (Fig. 46): on leaf, globoid, green-white, hairy, complex, one-chambered. Galler: Lopesia grandis Maia, 2001 plex, one-chambered. Galler: Clinodiplosis sp. (Diptera, (Diptera, Cecidomyiidae). Associated fauna: Hymenoptera Cecidomyiidae). Locality: Kutuca Beach. Occurrence pe- parasitoid. Localities: Grande, Kutuca, Suja, Caju, João riod: January, February and March 2011. Temporal con- Manoel, Sítio and Armação Beaches. Occurrence period: stancy: accidental. No previous records from Brazilian April 2010 to March 2011. Temporal constancy: constant. restinga areas. Previous records from Brazilian restinga areas: Ilha Grande, Gall (Fig. 47): on stem, fusiform, green, hairy, simple, Jurubatiba, Maricá, and Carapebus (Maia & Oliveira 2010; multi-chambered. Galler: undeterminated. Locality: Armação Monteiro et al. 2004; Maia 2001). Beach. Occurrence period: January 2011. Temporal constancy: accidental. No previous records from Brazilian Inga sp. restinga areas. Gall (Fig. 54): on leaf, globoid, yellow, hairy, complex, Gymnanthes gaudichaudii Müll.Arg. one-chambered. Galler: Cecidomyiinae (Diptera, Cecidomyi- idae). Associated fauna: Hymenoptera parasitoid. Localities: Gall (Fig. 48): on fruit, globoid, orange, glabrous, simple, Caju and Armação Beaches. Occurrence period: December one-chambered. Galler: undeterminated. Locality: Kutuca 2010 and February 2011. Temporal constancy: accidental. Beach. Occurrence period: December 2010. Temporal con- No previous records from Brazilian restinga areas. stancy: accidental. Gall (Fig. 55): on leaf vein, fusiform, green-brown, hairy, This is the first record of insect galls in this plant species. simple, one-chambered. Galler: Neolasioptera sp. (Diptera, Cecidomyiidae). Localities: Suja, Caju and Sítio Beaches. Fabaceae Occurrence period: December 2010 and January 2011. Tem- Andira fraxinifolia Benth. poral constancy: accidental. No previous records from Bra- zilian restinga areas. Gall (Fig. 49): on leaf, globoid, green, glabrous, com- Gall: on stem, fusiform, green-brown, hairy, simple, one- plex, one-chambered. Galler: Asphondylia sp. (Diptera, chambered. Galler: Neolasioptera sp. (Diptera, Cecidomyi- Cecidomyiidae). Associated fauna: Hymenoptera parasitoid. idae). Associated fauna: Lepidoptera inquiline. Locality: Suja Locality: Sítio Beach. Occurrence period: December 2010, Beach. Occurrence period: March 2011. Temporal constancy: January, February and March 2011. Temporal constancy: accidental. No previous records from Brazilian restinga areas.

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Stylosanthes guianensis Sw. Malpighiaceae Byrsonima sericea DC. Inflorescence (Fig. 56) with free-life larvae of Lestodip- losis sp. (Diptera, Cecidomyiidae). Associated fauna: Lepi- Gall (Fig. 63): on leaf, lenticular, brown, hairy, simple, doptera. Locality: Armação Beach. Occurrence period: one-chambered. Galler: Dasineura byrsonimae Maia, 2010 December 2010. Temporal constancy: accidental. Previous (Diptera, Cecidomyiidae). Associated fauna: Hymenoptera records from Brazilian restinga areas: Jurubatiba, Maricá, parasitoid. Localities: Grande, Kutuca, Suja and Armação and Carapebus (Monteiro et al. 2004; Maia 2001). Beaches. Occurrence period: April, May, June, July, Septem- ber, October, November, December 2010, January, February Zollernia glabra (Spreng.) Yakovlev and March 2011. Temporal constancy: constant. Previous records from Brazilian restinga areas: Ilha Grande, Guarapari, Gall: on leaf vein, fusiform, green, glabrous, simple, one- Grumari, Jurubatiba, Maricá, and Carapebus (Maia & chambered. Galler: Curculionidae (Coleoptera). Locality: Oliveira 2010; Bregonci et al. 2010; Oliveira & Maia 2005; João Manoel Beach. Occurrence period: April, May, June Monteiro et al. 2004; Maia 2001). and July 2010. Temporal constancy: accessory. Gall (Fig. 64): on inflorescence, globoid, brown, glabrous, Closed flower (Fig. 57) with Curculionidae (Coleoptera). simple, one-chambered. Galler: Bruggmanniella byrsonimae Localities: Caju and João Manoel Beaches. Occurrence pe- (Maia & Couri, 1992) (Diptera, Cecidomyiidae). Locality: riod: July 2010. Temporal constancy: accidental. Armação Beach. Occurrence period: April, May, July, Sep- This is the first record of insect galls in this plant species. tember, December 2010, January and February 2011. Tem- poral constancy: constant. Previous records from Brazilian Lauraceae restinga areas: Maricá, Carapebus, and Jurubatiba (Maia Ocotea notota (Nees & Mart.) Mez 2001; Monteiro et al. 1994, 2004). Gall (Fig. 65): on inflorescence, globoid, green, glabrous, Gall (Fig. 58): on fruit, globoid, yellow, simple, one-cham- complex, one-chambered. Galler: Lepidoptera. Locality: bered. Galler: undescribed species of Bruggmanniella Grande and Armação Beaches. Occurrence period: July 2010 (Diptera, Cecidomyiidae). Locality: Armação Beach. Occur- to January 2011. Temporal constancy: accidental. Previous rence period: October, November and December 2010. Tem- records from Brazilian restinga areas: Maricá, Arraial do poral constancy: accessory. No previous records from Cabo, and Jurubatiba (Monteiro et al. 1994, 2004). Brazilian restinga areas. Gall (Fig. 66): on floral peduncle, fusiform, brown, gla- Gall (Fig. 59): on stem, fusiform, brown, glabrous, simple, brous, simple, one-chambered. Galler: Cecidomyiinae multi-chambered. Galler: undeterminated. Locality: Armação (Diptera, Cecidomyiidae). Locality: Armação Beach. Occur- Beach. Occurrence period: October, November, December rence period: February 2011. Temporal constancy: acciden- 2010 and February 2011. Temporal constancy: accessory. tal. No previous records from Brazilian restinga areas. Previous records from Brazilian restinga areas: Maricá, Gall (Fig. 67): on stem, fusiform, brown, glabrous, simple, Jurubatiba (Monteiro et al. 1994, 2004). multi-chambered. Galler: Cecidomyiinae (Diptera, Cecido- myiidae). Localities: Suja and Armação Beach. Occurrence pe- Loranthaceae riod: April, May, September, October, November, December Struthanthus concinnus Mart. 2010 and January 2011. Temporal constancy: constant. Previ- ous records from Brazilian restinga areas: Ilha Grande, Gall: on leaf (Fig. 60) and stem (Fig. 61), conical, green, Guarapari, Grumari, Maricá, Carapebus, Arraial do Cabo, and glabrous, complex, one-chambered. Galler: Asphondylia sp. Jurubatiba (Maia & Oliveira 2010; Bregonci et al. 2010; Oliveira (Diptera, Cecidomyiidae). Associated fauna: Camptoneuriini & Maia 2005; Maia 2001; Monteiro et al. 1994, 2004). (Diptera, Cecidomyiidae) inquiline of leaf gall, Cecidomyi- inae sp. (Diptera, Cecidomyiidae), Thysanoptera inquilines Heteropterys nitida Kunth of stem gall, and Hymenoptera parasitoid of both. Locali- ties: Grande, Kutuca, Suja and Caju Beaches. Occurrence Closed flower (Fig. 68) with Curculionidae (Coleoptera). period: April 2010 to March 2011. Temporal constancy: con- Localities: Kutuca, Caju and Sítio Beaches. Occurrence pe- stant. No previous records from Brazilian restinga areas. riod: April, June and December 2010. Temporal constancy: Gall (Fig. 62): on adventice root, fusiform, brown, gla- accidental. Previous records from Brazilian restinga areas: brous, simple, one-chambered. Galler: Cecidomyiinae Maricá (Maia 2001). (Diptera, Cecidomyiidae). Associated fauna: Hymenoptera parasitoid. Locality: Grande, Kutuca and Suja Beaches. Oc- Peixotoa sp. currence period: April, May, June, August and November 2010. Temporal constancy: accessory. No previous records Gall (Fig. 69): on leaf, lenticular, green-brown, hairy, from Brazilian restinga areas. simple, one-chambered. Galler: Cecidomyiinae (Diptera,

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Cecidomyiidae). Localities: Grande, Kutuca and João Manoel Occurrence period: December 2010, January and February Beaches. Occurrence period: April, May, June, August and 2011. Temporal constancy: accidental. December 2010. Temporal constancy: constant. No previous This is the first record of insect galls in this plant genus. records from Brazilian restinga areas. Melastomataceae Stigmaphyllon ciliatum (Lam.) A. Juss. Miconia cinnamomifolia (DC.) Naudin

Gall (Fig. 70): on stem, fusiform, brown, glabrous, simple, Gall (Fig. 77): on leaf, globoid, red, glabrous, complex, multi-chambered. Galler: undeterminated. Locality: Suja one-chambered. Galler: undeterminated. Locality: Armação Beach. Occurrence period: December 2010. Temporal con- Beach. Occurrence period: August 2010. Temporal constancy: stancy: accidental. accidental. No previous records from Brazilian restinga ar- This is the first record of insect galls in this plant species. eas. Gall (Fig. 78): on stem, globoid, brown, glabrous, com- Malpighiaceae sp. plex, one-chambered. Galler: undeterminated. Locality: Armação Beach. Occurrence period: August 2010. Tempo- Gall: on stem (Fig. 71) and leaf vein (Fig. 72), fusiform, ral constancy: accidental. No previous records from Brazil- brown-green-yellow, glabrous, simple, one and multi-cham- ian restinga areas. bered. Galler: undescribed species of Lopesia (Diptera, Cecidomyiidae). Locality: Grande, Kutuca and Suja Beaches. Meliaceae Occurrence period: April 2010 to March 2011. Temporal con- Guarea guidonia (L.) Sleumer stancy: constant. Gall (Fig. 79): on leaf, globoid, yellow, glabrous, com- Malvaceae plex, one-chambered. Galler: Cecidomyiinae (Diptera, Luehea divaricata Mart. Cecidomyiidae). Associated fauna: Hymenoptera parasitoid. Localities: Suja, Caju, Sítio and Armação Beaches. Occur- Gall (Fig. 73): on leaf, globoid, brown, hairy, complex, rence period: April, June, August, September, October, De- one-chambered. Galler: Cecidomyiinae (Diptera, Cecidomyi- cember 2010, February and March 2011. Temporal constancy: idae). Localities: João Manoel and Sítio Beaches. Occurrence constant. period: May, November, December 2010, January, February Gall: on leaf vein, fusiform, green-brown, glabrous, and March 2011. Temporal constancy: constant. No previ- simple, one-chambered. Galler: Cecidomyiinae (Diptera, ous records from Brazilian restinga areas. Cecidomyiidae). Associated fauna: Hymenoptera parasitoid. Gall: on leaf, marginal roll, green, hairy, simple, one- Locality: Suja Beach. Occurrence period: April and August chambered. Galler: undeterminated. Localities: João Manoel 2010. Temporal constancy: accidental. and Sítio Beaches. Occurrence period: April, May, June, Gall: on stem, fusiform, green-brown, glabrous, simple, December 2010 and January 2011. Temporal constancy: con- one-chambered. Galler: Cecidomyiinae (Diptera, Cecidomyi- stant. No previous records from Brazilian restinga areas. idae). Associated fauna: Hymenoptera parasitoid. Locality: Gall (Fig. 74): on stem, globoid, brown, glabrous, com- Suja Beach. Occurrence period: April 2010. Temporal con- plex, one-chambered. Galler: Cecidomyiinae (Diptera, stancy: accidental. Cecidomyiidae). Associated fauna: Olcella sp. (Diptera, Chlo- This is the first record of insect galls in this plant species. ropidae) inquiline and Hymenoptera parasitoid. Localities: João Manoel and Sítio Beaches. Occurrence period: April, Moraceae May, June, July, October, December 2010, January, Febru- Ficus sp. ary and March 2011. Temporal constancy: constant. No previous records from Brazilian restinga areas. Gall (Fig. 80): on leaf fold, green-red, glabrous, simple, Gall (Fig. 75): on stem, globoid with apical spine, green, one-chambered. Galler: Thysanoptera. Locality: Suja Beach. glabrous, complex, one-chambered. Galler: undeterminated. Occurrence period: April 2010. Temporal constancy: acci- Localities: João Manoel and Sítio Beaches. Occurrence pe- dental. No previous records from Brazilian restinga areas. riod: April, May, June, November, December 2010, January and February 2011. Temporal constancy: constant. No pre- Myrtaceae vious records from Brazilian restinga areas. Calyptranthes brasiliensis Spreng.

Sida sp. Gall (Fig. 81): on bud, conical, green-brown, glabrous, complex, multi-chambered. Galler: undeterminated. Locality: Gall (Fig. 76): on stem, fusiform, brown, glabrous, simple, Armação Beach. Occurrence period: December 2010, Janu- one-chambered. Galler: Cecidomyiinae (Diptera, Cecidomyi- ary and February 2011. Temporal constancy: accidental. idae). Localities: Kutuca, João Manoel and Sítio Beaches. This is the first record of insect galls in this plant species.

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Figs. 58–85. Galls of restinga areas of Ilha da Marambaia (Mangaratiba, RJ, Brazil). 58–59, Ocotea notata: 58, gall on fruit; 59, stem gall. 60–62, Struthanthus concinnus: 60, leaf gall; 61, stem gall; 62, adventitious root gall. 63–67, Byrsonima sericea: 63, lenticular leaf gall; 64–66, galls on inflorescence; 67, stem gall. 68, Heteropterys nitida, flower bud. 69, Peixotoa sp., lenticular leaf gall. 70, Stigmaphyllon ciliatum, stem gall. 71–72, Malpighiaceae sp.: 71, stem gall; 72, leaf vein gall. 73–75, Luehea divaricata: 73, leaf gall; 74, globoid stem gall; 75, globoid stem gall with projection. 76, Sida sp., stem gall. 77–78, Miconia cinnamomifolia: 77, globoid leaf gall; 78, globoid stem gall. 79, Guarea guidonia, globoid leaf gall. 80, Ficus sp., leaf fold gall. 81, Calyptranthes brasiliensis, bud gall. 82–83, Eugenia adstringens: 82, marginal roll gall; 83, lenticular leaf gall, arrow pointing to gall. 84, Eugenia copacabanensis, spiral leaf gall. 85, Eugenia punicifolia, cylindrica leaf gall.

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Eugenia adstringens Cambess. (= Eugenia rotundifolia Associated fauna: Curculionidae (Coleoptera) inquiline and Casar and E. umbelliflora O. Berg) Hymenoptera parasitoid. Localities: Grande, Suja, Caju, João Manoel, Sítio and Armação Beaches. Occurrence period: Gall (Fig. 82): on leaf, marginal roll, green, glabrous, September, October and November 2010. Temporal con- simple, one-chambered. Galler: Dasineura marginalis Maia, stancy: accidental. 2005 (Diptera, Cecidomyiidae). Associated fauna: Hy- This is the first record of insect galls in this plant species. menoptera parasitoid. Locality: Armação Beach. Occurrence period: April, May, July, August, September, October, Novem- Eugenia uniflora L. ber, December 2010, January, February and March 2011. Tem- Gall (Fig. 89): on leaf, lenticular, green-black, glabrous, poral constancy: constant. Previous records from Brazilian simple, one-chambered. Galler: Neolasioptera eugeniae restinga areas: Grumari, Jurubatiba, Carapebus, and Maricá Maia, 1993 (Diptera, Cecidomyiidae). Associated fauna: (Oliveira & Maia 2005; Monteiro et al. 2004; Maia 2001). Hymenoptera parasitoid. Localities: Grande, Kutuca, Suja, Gall (Fig. 83): on leaf, lenticular, green, glabrous, simple, Caju, João Manoel, Sítio and Armação Beaches. Occurrence one-chambered. Galler: Dasineura globosa Maia, 1995 (Diptera, period: April 2010 to March 2011. Temporal constancy: con- Cecidomyiidae). Locality: Armação Beach. Occurrence period: stant. Previous records from Brazilian restinga areas: Paraty, May, July, August, September, November, December 2010, Cabo Frio, Ilha Grande, Grumari, Jurubatiba, Arraial do Cabo, January, February and March 2011. Temporal constancy: con- and Maricá (Maia 2013; Maia & Oliveira 2010; Oliveira & stant. Previous records from Brazilian restinga areas: Bertioga, Maia 2005; Monteiro et al. 2004; Maia 2001). Grumari, Jurubatiba, Carapebus, and Maricá (Maia et al. 2008; Gall (Fig. 90): on leaf, conical, green-red, glabrous, com- Oliveira & Maia 2005; Monteiro et al. 2004; Maia 2001). plex, one-chambered. This gall presents variation in shape, being globoid in some samples; and with occurrence of one Eugenia copacabanensis Kiaersk. or two larvae in the internal chamber. Galler: Clinodiplosis profusa Maia, 2001 (Diptera, Cecidomyiidae). Associated Gall (Fig. 84): on leaf, spiral, red-green, glabrous, com- fauna: Gynaikothrips uzeli (Zimerman, 1909) (Thysanoptera, plex, one-chambered. Galler: Stephomyia espiralis Maia, Phlaeothripidae) inquilines and Hymenoptera parasitoid. 1993 (Diptera, Cecidomyiidae). Associated fauna: Hy- Localities: Grande, Kutuca, Suja, Caju, João Manoel and Sítio menoptera parasitoid. Locality: Armação Beach. Occurrence Beaches. Occurrence period: July 2010 to February 2011. period: May 2010. Temporal constancy: accidental. Previ- Temporal constancy: constant. Previous records from Bra- ous records from Brazilian restinga areas: Jurubatiba, and zilian restinga areas: Cabo Frio, Grumari, Jurubatiba, Arraial Maricá (Monteiro et al. 2004; Maia 2001). do Cabo, and Maricá (Maia 2013; Oliveira & Maia 2005; Gall: on leaf, lenticular, green, glabrous, simple, one-cham- Monteiro et al. 2004; Maia 2001). bered. Galler: undeterminated. Locality: Armação Beach. Gall (Fig. 91): on leaf roll, green, glabrous, simple, one- Occurrence period: May 2010. Temporal constancy: acciden- chambered. Galler: Cecidomyiinae (Diptera, Cecidomyiidae). tal. No previous records from Brazilian restinga areas. Locality: Kutuca Beach. Occurrence period: November 2010. Temporal constancy: accidental. No previous records from Eugenia punicifolia (Kunt) DC. Brazilian restinga areas. Gall: on stem, fusiform, brown, glabrous, simple. Galler: Gall (Fig. 85): on leaf, cylindrical, green-red, glabrous, undeterminated. Locality: Armação Beach. Occurrence pe- complex, one-chambered. Galler: Stephomyia sp. (Diptera, riod: August 2010. Temporal constancy: accidental. Previ- Cecidomyiidae). Associated fauna: Hymenoptera parasitoid. ous records from Brazilian restinga areas: Ilha Grande (Maia Localities: Grande, Kutuca, Suja, Caju, João Manoel, Sítio & Oliveira 2010). and Armação Beaches. Occurrence period: April 2010 to March 2011. Temporal constancy: constant. Myrcia acuminatissima O. Berg. Gall (Fig. 86): on leaf, lenticular, green-red, glabrous, simple, one-chambered. Galler: Cecidomyiinae (Diptera, Gall (Fig. 92): on stem, globoid, brown, glabrous, simple, Cecidomyiidae). Locality: Caju Beach. Occurrence period: multi-chambered. Galler: undeterminated. Locality: Kutuca August 2010. Temporal constancy: accidental. Beach. Occurrence period: October and November 2010. Gall (Fig. 87): on stem, fusiform, brown, glabrous, simple, Temporal constancy: accidental. multi-chambered. Galler: Lasiopteridi (Diptera, Cecidomyi- This is the first record of insect galls in this plant species. idae). Associated fauna: Hymenoptera parasitoid. Localities: Grande, Kutuca, Suja, Caju, Sítio and Armação Beaches. Myrcia splendens (SW.) DC. Occurrence period: April 2010 to February 2011. Temporal constancy: constant. Gall (Fig. 93): on leaf, globoid, green, glabrous, com- Gall (Fig. 88): on fruit, globoid, green-red-yellow, gla- plex, one-chambered. Galler: undeterminated. Associated brous, simple, multi-chambered. Galler: undeterminated. fauna: Hymenoptera parasitoid. Localities: Kutuca and Caju

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Beaches. Occurrence period: May and December 2010. Tem- (Arachinida) predator and Hymenoptera parasitoid. Locali- poral constancy: accidental. ties: João Manoel, Sítio and Armação Beaches. Occurrence Gall: on leaf, conical, yellow-green, glabrous, complex, period: April 2010 to March 2011. Temporal constancy: con- one-chambered. Galler: undeterminated. Associated fauna: stant. No previous records from Brazilian restinga areas. Hymenoptera parasitoid. Locality: Caju Beach. Occurrence Gall (Fig. 101): on leaf, globoid, green, glabrous, com- period: December 2010. Temporal constancy: accidental. plex, one-chambered. Galler: Cecidomyiinae (Diptera, Gall (Fig. 94): on leaf, marginal roll, green, glabrous, Cecidomyiidae). Localities: Sítio and Armação Beaches. simple, one-chambered. Galler: undeterminated. Locality: Occurrence period: April, May, June, October, Nevember and Kutuca Beach. Occurrence period: February 2011. Tempo- December 2010. Temporal constancy: constant. Previous ral constancy: accidental. records from Brazilian restinga areas: Guarapari, and Bertioga Gall (Fig. 95): on bud, globoid, green-brown, glabrous, (Bregonci et al. 2010; Maia et al. 2008). complex, multi-chambered. Galler: undeterminated. Local- Gall (Fig. 102): on leaf, conical, green-red, glabrous, com- ity: Kutuca Beach. Occurrence period: June 2011. Temporal plex, one-chambered. Galler: Bruggmannia acaudata Maia, constancy: accidental. 2004 (Diptera, Cecidomyiidae). Locaities: Sítio and Armação This is the first record of insect galls in this plant species. Beaches. Occurrence period: May, July, September, Octo- ber, November, December 2010, January, February and Psidium guajava L. March 2011. Temporal constancy: constant. Previous records from Brazilian restinga areas: Ilha Grande, Maricá, Gall (Fig. 96): on stem, fusiform, brown, glabrous, simple, Jurubatiba, and Carapebus (Maia & Oliveira 2010; Monteiro multi-chambered. Galler: undeterminated. Localities: Suja et al. 2004; Maia 2001). and Armação Beaches. Occurrence period: April, May, June, Gall (Fig. 103): on stem, globoid, brown, glabrous, com- September, November 2010 and February 2011. Temporal plex, multi-chambered. Galler: Proasphondylia guapirae constancy: constant. Maia & Couri, 1993. Localities: Grande, Kutuca, Suja, Caju, This is the first record of insect galls in this plant species. Sítio and Armação Beaches. Occurrence period: May, Au- gust, September, October, December 2010, January, Febru- Myrtaceae sp. ary and March 2011. Temporal constancy: constant. Previous records from Brazilian restinga areas: Ilha Grande, Bertioga, Gall (Fig. 97): on leaf, lenticular, green, glabrous, simple, Jurubatiba, Maricá, and Carapebus (Maia et al. 2008; Maia one-chambered. Galler: undeterminated. Locality: Kutuca & Oliveira 2010; Monteiro et al. 2005; Maia 2001). Beach. Occurrence period: June 2010. Temporal constancy: Gall (Fig. 104): on stem, globoid, brown, glabrous, com- accidental. plex, one-chambered. Galler: undeterminated. Locality: Armação Beach. Occurrence period: October 2010. Tempo- Nyctaginaceae ral constancy: accidental. No previous records from Brazil- Guapira opposita (Vell.) Reitz. ian restinga areas. Gall (Fig. 105): on flower peduncle, globoid, green- Gall (Fig. 98): on leaf, lenticular, green-red, glabrous, brown-red, glabrous, complex, one-chambered. Galler: simple, one-chambered. Galler: Bruggmannia elongata Maia undescribed species of Pisphondylia (Diptera, Cecidomyi- & Couri, 1993 (Diptera, Cecidomyiidae). Localities: Grande, idae). Associated fauna: Lepidoptera inquiline and Hy- Kutuca, Suja, Caju, João Manoel, Sítio and Armação Beaches. menoptera parasitoid. Localities: Sítio and Armação Beaches. Occurrence period: April 2010 to March 2011. Temporal Occurrence period: September, October and November 2010. constancy: constant. Previous records from Brazilian restinga Temporal constancy: accidental. No previous records from areas: Ilha Grande, Bertioga, Jurubatiba, Arraial do Cabo, Brazilian restinga areas. Maricá, and Carapebus (Maia & Oliveira 2010; Maia et al. 2008; Monteiro et al. 2004; Maia 2001). Ochnaceae Gall (Fig. 99): on leaf, globoid, red, glabrous, complex, Ouratea cuspidata (St. Hil.) Engl. one-chambered. Galler: Bruggmannia robusta Maia & Couri, 1993 (Diptera, Cecidomyiidae). Localities: Sítio and Armação Gall (Fig. 106): on leaf, cylindrical with apical projection, Beaches. Occurrence period: April 2010 to March 2011. brown, glabrous, complex, one-chambered. Galler: Contarinia Temporal constancy: constant. Previous records from Bra- sp. (Diptera, Cecidomyiidae). Locality: Armação Beach. Oc- zilian restinga areas: Ilha Grande, Bertioga, Jurubatiba, currence period: April, May and September 2010. Temporal Arraial do Cabo, Maricá, and Carapebus (Maia & Oliveira constancy: accidental. Previous records from Brazilian restinga 2010; Maia et al. 2008; Monteiro et al. 2004; Maia 2001). areas: Ilha Grande, Guarapari, Grumari, Maricá, and Jurubatiba Gall (Fig. 100): on leaf, globoid, brown, glabrous, com- (Maia & Oliveira 2010; Bregonci et al. 2010; Oliveira & Maia plex, one-chambered. Galler: undescribed species of 2005; Maia 2001; Monteiro et al. 1994, 2004). Bruggmannia (Diptera, Cecidomyiidae). Associated fauna: Gall (Fig. 107): on leaf, lenticular, green, glabrous, simple, Aphididae (Hemiptera) inquiline, Pseudoscorpiones one-chambered. Galler: Cecidomyiinae (Diptera, Cecidomyi-

Revista Brasileira de Entomologia 58(2): 173–197, June 2014 192 Rodrigues et al. idae). Locality: Armação Beach. Occurrence period: April areas: Arraial do Cabo, Jurubatiba, Maricá, and Carapebus 2010. Temporal constancy: accidental. No previous records (Monteiro et al. 1994, 2004; Maia 2001). from Brazilian restinga areas. Salicaceae Olacaceae Casearia sp. Ximenia americana L. Gall (Fig. 114): on leaf petiole, fusiform, brown, glabrous, Gall (Fig. 108): on bud, fusiform, brown, glabrous, simple, simple, one-chambered. Galler: undeterminated. Locality: one-chambered. Galler: Asphondylia communis Maia & Suja Beach. Occurrence period: March 2011. Temporal con- Couri, 1993 (Cecidomyiidae, Diptera). Associated fauna: stancy: accidental. No previous records from Brazilian Hymenoptera parasitoid. Localities: Grande, Suja, Caju, João restinga areas. Manoel, Sítio and Armação Beaches. Occurrence period: April 2010 to February 2011. Temporal constancy: constant. Sapindaceae Previous records from Brazilian restinga areas: Maricá (Maia Matayba guianensis Aubl. 2001; Monteiro et al. 1994). Gall (Fig. 115): on fruit, globoid, green, glabrous, simple, Polygalaceae one-chambered. Galler: undeterminated. Locality: Armação Securidaca sp. Beach. Occurrence period: September 2010. Temporal constancy: accidental. No previous records from Brazilian Closed flower (Fig. 109) with larvae of Cecidomyiidae restinga areas. (Diptera). Associated fauna: Muscomorpha (Diptera) in- Gall (Fig. 116): on leaf, globoid, green, glabrous, com- quiline and Hymenoptera parasitoid. Locality: Armação plex, one-chambered. Galler: undeterminated. Locality: Beach. Occurrence period: October 2010. Temporal con- Armação Beach. Occurrence period: May 2010. Temporal stancy: accidental. constancy: accidental. No previous records from Brazilian Gall (Fig. 110): on leaf, cylindrical, green, glabrous, com- restinga areas. plex, one-chambered. Galler: undeterminated. Locality: Gall (Fig. 117): on stem, fusiform, brown, glabrous, Armação Beach. Occurrence period: September 2010. Tem- simple, multi-chambered. Galler: undeterminated. Locality: poral constancy: accidental. Armação Beach. Occurrence period: December 2010. Tem- Gall (Fig. 111): on stem, cylindrical, green, glabrous, poral constancy: accidental. No previous records from Bra- complex, one-chambered. Galler: undeterminated. Locality: zilian restinga areas. Armação Beach. Occurrence period: September 2010. Tem- poral constancy: accidental. Serjania sp. 01 This is first record of insect galls in this plant genus. Gall (Fig. 118): on leaf central vein, fusiform, green, glabrous, simple, one-chambered. Galler: Muscomorpha Polygonaceae (Diptera). Associated fauna: Hymenoptera parasitoid. Local- Coccoloba alnifolia Casar ity: Armação Beach. Occurrence period: May, August, De- cember 2010, January and February 2011. Temporal constancy: Gall (Fig. 112): on inflorescence, globoid, yellow-green, accessory. glabrous, complex, one-chambered. Galler: Lopesia sp. Gall (Fig. 119): on leaf, cylindrical, yellow, glabrous, (Diptera, Cecidomyiidae). Associated fauna: Lepidoptera complex, one-chambered. Galler: undeterminated. Associ- inquiline. Localities: Grande and Armação Beaches. Occur- ated fauna: Lestodiplosiini (Diptera, Cecidomyiidae) preda- rence period: April, May and June 2010. Temporal constancy: tor. Locality: Armação Beach. Occurrence period: July and accidental. December 2010. Temporal constancy: accidental. This is the first record of insect galls in this plant species. Gall: on stem, fusiform, brown, glabrous, simple, one- chambered. Galler: undeterminated. Associated fauna: Hy- Rubiaceae menoptera parasitoid. Locality: Armação Beach. Occurrence Borreria verticillata G. Mey. period: December 2010 and January 2011. Temporal constancy: accidental. Gall (Fig. 113): on inflorescence, drop-like, green, glabrous, complex, one-chambered. Galler: Asphondylia Serjania sp. 02 borreriae Rübsaamen, 1905 (Diptera, Cecidomyiidae). Lo- calities: Grande, Kutuca and Suja Beaches. Occurrence pe- Gall (Fig. 120): on leaf vein, fusiform, green-yellow, gla- riod: April, May, June, July, August, September, October, brous, simple, one-chambered. Galler: Cecidomyiinae November, December 2010 and February 2011. Temporal (Diptera, Cecidomyiidae). Associated fauna: Hymenoptera constancy: constant. Previous records from Brazilian restinga parasitoid. Locality: João Manoel and Sítio Beaches. Occur-

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Figs. 86–113. Galls of restinga areas of Ilha da Marambaia (Mangaratiba, RJ, Brazil). 86–88, Eugenia punicifolia: 86, lenticular leaf gall; 87, stem gall; 88, gall on fruit. 89–91, Eugenia uniflora: 89, lenticular leaf gall; 90, conical leaf gall; 91, roll leaf. 92, Myrcia acuminatissima, stem gall. 93–95, Myrcia splendens: 93, globoid leaf gall; 94, marginal roll leaf gall; 95, bud gall. 96, Psidium guajava, stem gall. 97, Myrtaceae sp., lenticular leaf gall. 98–105, Guapira opposita: 98, lenticular leaf gall; 99, red globoid leaf gall; 100, brown globoid leaf gall; 101, green globoid leaf gall; 102, conical leaf gall; 103, stem gall; 104, globoid stem gall; 105, globoid gall on flower peduncle. 106–107, Ouratea cuspidata: 106, cylindrica leaf gall with apical projection; 107, lenticular leaf gall. 108, Ximenia americana, bud gall. 109–111, Securidaca sp.: 109, flower buds; 110, cylindrical leaf gall; 111, cylindrical stem gall. 112, Coccoloba alnifolia, gall on inflorescence. 113, Borreria verticillata, gall on inflorescence.

Revista Brasileira de Entomologia 58(2): 173–197, June 2014 194 Rodrigues et al. rence period: December 2010, January and March 2011. Tem- Carapebus (Oliveira & Maia 2005; Monteiro et al. 2004; Maia poral constancy: accidental. 2001). Gall (Fig. 121): on leaf, lenticular, green-yellow, glabrous, Gall (Fig. 126): on leaf, conical, green, glabrous, com- simple, one-chambered. Galler: undeterminated. Locality: plex, one-chambered. Galler: Hemiptera. Locality: Armação Kutuca and João Manoel Beach. Occurrence period: April Beach. Occurrence period: April, May, July, August, Sep- 2010. Temporal constancy: accidental. tember, October, November, December 2010, January, Feb- Gall (Fig. 122): on leaf petiole, fusiform, green-yellow, ruary and March 2011. Temporal constancy: constant. glabrous, simple, one-chambered. Galler: undeterminated. Previous records from Brazilian restinga areas: Guarapari, Locality: João Manoel Beach. Occurrence period: March Ilha Grande, Maricá, and Arraial do Cabo (Bregonci et al. 2011. Temporal constancy: accidental. No previous records 2010; Maia & Oliveira 2010; Monteiro et al. 1994). from Brazilian restinga areas. Gall (Fig. 127): on leaf vein, fusiform, green-red, glabrous, simple, one-chambered. Galler: Cecidomyiinae Sapotaceae (Diptera, Cecidomyiidae). Associated fauna: Hymenoptera Pouteria caimito (R. & P.) Radlk. parasitoid. Localities: Grande, Kutuca, Suja and Armação Beaches. Occurrence period: April, May, June July, August, Gall (Fig. 123): on leaf, conical, green, glabrous, com- October 2010, February and March 2011. Temporal con- plex, one-chambered. Galler: Youngomyia pouteriae Maia, stancy: constant. Previous records from Brazilian restinga 2001 (Diptera, Cecidomyiidae). Locality: Armação Beach. areas: Grumari, Jurubatiba, Maricá, and Carapebus (Oliveira Occurrence period: December 2010. Temporal constancy: & Maia 2005; Monteiro et al. 2004; Maia 2001). accidental. Previous records from Brazilian restinga areas: Gall (Fig. 128): on stem, globoid, green-red, glabrous, Grumari, Maricá, and Arraial do Cabo (Oliveira & Maia 2005; simple, multi-chambered. Galler: undeterminated. Associated Maia 2001; Monteiro et al. 1994). fauna: Hymenoptera parasitoid. Localities: Grande, Kutuca, Suja and Armação Beaches. Occurrence period: April, May, Pouteria venosa (Mart.) Baehni July, August, December 2010 and February 2011. Temporal constancy: constant. No previous records from Brazilian Gall: on leaf, lenticular, green, glabrous, simple, one- restinga areas. chambered. Galler: Lopesia singularis Maia, 2001 (Diptera, Solanaceae Cecidomyiidae). Locality: Kutuca and Caju Beaches. Occur- rence period: April, May and December 2010. Temporal con- Solanum sp. stancy: accidental. Previous records from Brazilian restinga Gall (Fig. 129): on leaf, lenticular, green, glabrous, simple, areas: Bertioga, Maricá, and Arraial do Cabo (Maia et al. one-chambered. Galler: undeterminated. Locality: Suja 2008; Maia 2001; Monteiro et al. 1994). Beach. Occurrence period: December 2010. Temporal constancy: accidental. No previous records from Brazilian Sideroxylon obtusifolium (Roem. & Schult.) T. D. restinga areas. Penn. (= Bumelia obtusifolia Roem. & Schult.) Gall (Fig. 130): on stem, fusiform, green, hairy, simple, one-chambered. Galler: undeterminated. Localities: Kutuca Gall (Fig. 124): on fruit, globoid, green, glabrous, simple, and Suja Beaches. Occurrence period: December 2010 and multi-chambered. Galler: undescribed species of Bruggman- January 2011. Temporal constancy: accidental. No previous niella (Diptera, Cecidomyiidae). Associated fauna: records from Brazilian restinga areas. Cecidomyiinae sp. (Diptera, Cecidomyiidae) inquiline and Hymenoptera parasitoid. Locality: Caju Beach. Occurrence Solanaceae sp. period: June, July, August, October and November 2010. Tem- poral constancy: accessory. No previous records from Bra- Gall (Fig. 131): on leaf, lenticular, green, glabrous, simple, zilian restinga areas. one-chambered. Galler: Lepidoptera. Associated fauna: Hy- menoptera parasitoid. Localities: Kutuca and Suja Beaches. Smilacaceae Occurrence period: October and December 2010. Temporal Smilax rufescens Griseb constancy: accidental. Gall (Fig. 132): on lateral bud, globoid, brown, glabrous, Gall (Fig. 125): on leaf, lenticular, green-yellow-red, gla- complex, one-chambered. Galler: undeterminated. Localities: brous, simple, one-chambered. Galler: Smilasioptera Grande and Kutuca Beach. Occurrence period: May 2010. candelariae Möhn, 1975 (Diptera, Cecidomyiidae). Locali- Temporal constancy: accidental. ties: Grande, Kutuca, Suja, Caju, João Manoel, Sítio and Gall: stem, fusiform, green-brown, glabrous, simple, Armação Beaches. Occurrence period: April 2010 to March multi-chambered. Galler: undeterminated. Associated fauna: 2011. Temporal constancy: constant. Previous records from Hymenoptera parasitoid. Locality: Suja Beach. Occurrence Brazilian restinga areas: Grumari, Jurubatiba, Maricá, and period: June 2010. Temporal constancy: accidental.

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Figs. 114–136. Galls of restinga areas of Ilha da Marambaia (Mangaratiba, RJ, Brazil). 114, Casearia sp., leaf petiole. 115–117, Matayba guianensis: 115, gall on fruit; 116, globoid leaf gall; 117, stem gall. 118–119, Serjania sp. 01: 118, leaf vein gall; 119, cylindrical leaf gall. 120–122, Serjania sp. 02: 120, leaf vein gall; 121, lenticular leaf gall; 122, leaf petiole. 123, Pouteria caimito, conical leaf gall. 124, Sideroxylon obtusifolium, gall on fruit. 125–128, Smilax rufescens: 125, lenticular leaf gall; 126, conical leaf gall; 127, leaf vein gall; 128, stem gall. 129–130, Solanum sp.: 129, lenticular leaf gall; 130, stem gall. 131–132, Solanaceae sp.: 131, lenticular leaf gall; 132, globoid stem gall. 133, Lantana camara, stem gall. 134–135, Lantana lilacina: 134, globoid leaf gall; 135, cylindrical leaf gall. 136, Stachytarpheta sp., gall on inflorescence.

Verbenaceae Occurrence period: June, August and September 2010. Tem- Lantana camara L. poral constancy: accidental. Previous records from Brazilian restinga areas: Maricá (Maia 2001; Monteiro et al. 1994). Gall: on leaf, globoid, green, hairy, complex, one-cham- Gall (Fig. 133): on stem, fusiform, green-brown, hairy, bered. Galler: Schismatodiplosis lantanae Rübsaamen, 1907 simple, one-chambered. Galler: undeterminated. Associated (Diptera, Cecidomyiidae). Localities: Kutuca and Suja Beaches. fauna: Hymenoptera parasitoid. Localities: Kutuca and Suja

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Beach. Occurrence period: December 2010. Temporal constancy: (Maia & Oliveira 2010; Oliveira & Maia 2005; Maia 2001, 2006; accidental. No previous records from Brazilian restinga areas. Monteiro et al. 1994, 2004). Regarding lepidopteran galls, each morphotype developed on a different plant organ: stem, leaf Lantana lilacina Desf. and flower. Galls on these organs have already been recorded in other restingas of the State (Maia & Oliveira 2010; Oliveira & Gall (Fig. 134): on leaf, globoid, green, hairy, complex, Maia 2005; Maia 2001, 2006; Monteiro et al. 1994, 2004), oc- one-chambered. Galler: Asphondylia sp. (Diptera, Cecidomyi- curring, however, preferentially on stems. In restingas, the co- idae). Associated fauna: Hymenoptera parasitoid. Locality: leopteran galls have been recorded on leaves and stems (Maia Suja Beach. Occurrence period: January, February and March & Oliveira 2004; Maia 2001). In this work, coleopteran galls 2011. Temporal constancy: accidental. No previous records are recorded for the first time on flower bud. It is also provided from Brazilian restinga areas. the first record of coleopteran flower bud galls in Brazil (in Gall (Fig. 135): on leaf, cylindrical, green, hairy, com- South America, there is a single previous record for Argentina) plex, one-chambered. Galler: undeterminated. Associated (Maia & Oliveira 2004). Although hymenopteran galls have been fauna: Hymenoptera parasitoid. Locality: Kutuca Beach. recorded in Maricá and Carapebus (Maia 2001), none was found Occurrence period: December 2010. Temporal constancy: in the present study. In restingas, the number of Hymenoptera accidental. No previous records from Brazilian restinga areas. gall morphotypes is very low, varying from 0 to 2 (Maia 2013). In Jurubatiba, RJ (Monteiro et al. 2004); Ilha Grande, Angra Stachytarpheta sp. dos Reis, RJ (Maia & Oliveira 2010) and Guarapari, ES (Bregonci et al. 2010), hymenopteran galls were not founded, Gall (Fig. 136): on inflorescence, globoid, green, hairy, com- well as in the Ilha de Marambaia. Therefore, the result of this plex, one-chambered. Galler: Schizomyia stachytarphetae study fits in the context of low richness of galls, suggesting low Barnes, 1932 (Diptera, Cecidomyiidae). Associated fauna: adaptability of this insect order to the restinga environment. Haplothrips gowdeyi (Franklin, 1908) (Thysanoptera, Phlaeo- Cecidomyiidae was the most diverse and abundant gall- thripidae) inquiline and Hymenoptera parasitoid. Localities: ing group, with 84% of the occurrence. The most represented Grande and Kutuca Beaches. Occurrence period: May, Decem- genera, Asphondylia, Neolasioptera and Lopesia, were also ber 2010, January and February 2011. Temporal constancy: ac- pointed out in other restingas of the State (Maia & Oliveira cessory. No previous records from Brazilian restinga areas. 2010; Oliveira & Maia 2005; Maia 2001; Monteiro et al. 1994, 2004), confirming their high representation in this DISCUSSION ecosystem. Asphondylia and Neolasioptera are genera with many species, the first being cosmopolitan and the second Among the studied restingas of Rio de Janeiro State, Ilha recorded only for the Nearctic and Neotropical regions. Dif- da Marambaia stands out for presenting the greatest richness fering from them, Lopesia has few species, being distributed of insect gall morphotypes and host plant species, followed of in the Nearctic, Neotropical, Afrotropical and Australasia Jurubatiba and Arraial do Cabo (Maia & Oliveira 2010; regions (Gagné 2010). Oliveira & Maia 2005; Maia 2001; Monteiro et al. 1994, 2004). Other Cecidomyiidae were found as inquilines, predators Conde et al. (2005) cited Fabaceae, Myrtaceae, Orchidaceae, and free living, besides Hymenoptera, Lepidoptera, Co- Rubiaceae, and Sapindaceae as the most diversified families leoptera, Hemiptera, Thysanoptera, other Diptera and in number of species, and Eugenia, Ocotea, Ficus, Myrcia, Pseudoscorpiones founded as inquilines, predators and para- and Psychotria as the best represented genera in Marambaia sitoids. The study in the restinga of Maricá also recorded (Conde et al. 2005). Among them, in the present study, Hymenoptera, Lepidoptera and other Diptera as inquilines, Myrtaceae and Fabaceae stood out for the greatest richness of and Pseudoscorpiones as predator (Maia 2001). Hymenoptera gall morphotypes, and Eugenia as the super-host genus, while was the most represented insect order as parasitoid, this same Ocotea, Ficus and Myrcia presented few morphotypes, and pattern also recorded in Maricá and Arraial do Cabo (Maia Psychotria none. Concerning Eugenia, the results agreed with 2001; Monteiro et al. 1994). the hypothesis that plant taxa with the highest species richness Most gall morphotypes were accidental. In other restinga have equally a highest gall richness (Fleck & Fonseca 2007). surveys, the galls were not classified according to their fre- The most galled organs were the leaves, with predomi- quency. This is the first inventory that provides this informa- nance of 54% of occurrences. This same result was found in tion. Therefore, we cannot make comparisons with other other surveys in Rio de Janeiro State (Maia & Oliveira 2010; studied areas. The large number of accidental morphotypes Oliveira & Maia 2005; Maia 2001; Monteiro et al. 1994, explains the large proportion of undetermined inducers and 2004), and according with Felt (1940) this is a worldwide identifications only to suprageneric categories. pattern. Maia (2001) argued that the leaves are the most fre- Among the investigated beaches, Armação (with the larg- quently attacked vegetal organ in restingas as they represent est extension) presented the greatest richness of gall a constant and abundant source. morphotypes and host species, possibly due to the high num- Hemipteran and thysanopteran galls were found on leaves, ber of plant species, as proposed by the hypothesis of plant as recorded in other studies in restingas of Rio de Janeiro State richness (Fleck & Fonseca 2007).

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CONCLUSIONS tural da Marambaia. Seropédica, Editora da Universidade Federal Rural do Rio de Janeiro. 288 p. Espírito-Santo, M.M. & Fernandes, G.W. 2007. How many species of gall- Based on the present investigation and the results obtained inducing insects are there on Earth, and where are they? Annals of we can conclude that Ilha da Marambaia presents the greatest the Entomological Society of America 100: 95–99. number of insect gall morphotypes and of host plant species Felt, E. P. 1940. Plant Galls and Gall Makers. Ithaca, Comstock, 364 p. among the already studied restingas of the State of Rio de Fernandes, G.W. 1987. Gall forming insects: their economic importance Janeiro. Among the plant families investigated, Myrtaceae and control. Revista Brasileira de Entomologia 31: 379–398. Fleck, T. & Fonseca, C.R. 2007. Hipóteses sobre riqueza de insetos galhadores: proved to be the one with the highest gall richness and number uma revisão considerando os níveis intra-específico, interespecífico e de of galled species. We also concluded that Eugenia, Fridericia, comunidade. Neotropical Biology and Conservation 2: 36–45. Guapira and Mikania are super-host genera in this restinga, Gagné, R.J. 1994. The gall midges of the Neotropical region. Ithaca, and the leaf the most galled plant organ. Among the insects, Cornell University Press, 352 p. Diptera was the most representative galler order, standing out Gagné, R.J. 2010. Update for a catalog of the Cecidomyiidae (Diptera) of the world. Digital version 1. http://www.ars.usda.gov/SP2UserFiles/ the Cecidomyiidae, with Asphondylia, Lopesia and Neolasiop- Place/12754100/Gagne_2010_World_Catalog_Cecidomyiidae.pdf tera showing the highest species richness. Concerning other (accessed 24 October 2013). insects, Hymenoptera was pointed as the unique order of para- Isaias R.M.S., Carneiro, R.G.S., Oliveira, D.C. & Santos, J.C. 2013. sitoids, while inquiline insects were represented by five or- Illustrated and annotated checklist of Brazilian gall morphotypes. ders and predators were represented by Cecidomyiidae and Neotropical Entomology 42: 230–239. Maia, V.C. 2001. The gall midges (Diptera, Cecidomyiidae) from three pseudoscorpions. Finally, Armação Beach presented the larg- restingas of Rio de Janeiro State, Brazil. Revista Brasileira de Zoo- est richness of gall morphotypes and host plant species. logia 18: 305–656. Maia, V.C. 2006. Galls of Hemiptera, Lepidoptera and Thysanoptera from ACKNOWLEDGEMENTS Central and South America. Publicações Avulsas do Museu Nacio- nal 110: 1–22. We wish to thank Dr. Roberto de Xerez (UFRRJ) and Centro Maia, V.C. 2013. Galhas de insetos em restingas da região sudeste do Brasil com novos registros. Biota Neotropica 13: 183–209. de Avalição da Ilha da Marambaia (CADIM – Marinha do Maia, V.C. & Oliveira, J.C. 2004. Coleoptera associated with galls from South Brasil) for granting access to the study areas and for providing America with new records. Arquivos do Museu Nacional 62: 179–184. information and infrastructure; to the botanists Dr. Marcelo Maia, V.C. & Oliveira, J.C. 2010. Galhas de insetos da Reserva Biológica Souza (MNRJ), Dr. Débora Medeiros (MNRJ), Dr. Roberto Estadual da Praia do Sul (Ilha Grande, Angra dos Reis, RJ). Biota Esteves (UERJ) and Dr. Luiz Pinto (UERJ) for host plant iden- Neotropica 10: 227–237. Maia, V.C., Magenta, M.A.G. & Martins, S.E. 2008. Ocorrência e caracteri- tification; to Dr. Sérgio Vanin (USP) and Dr. Adriano Cavalleri zação de galhas de insetos em áreas de restinga de Bertioga (São Paulo, (UFRS) for Curculionidae (Coleoptera) and Thysanoptera Brasil). 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