Revista Brasileira de Entomologia 58(2): 173–197, June 2014
Revista Brasileira de Entomologia
http://dx.doi.org/10.1590/S0085-56262014000200010
Insect galls are pathological structures originated from new formations of vegetal tissues, resulting from mechanic and/or chemical stimuli of insects (Bronner 1992). The ductors are usually specific in relation to plant species, in-ducing galls only in one species or on a small group of host species (Carneiro et al. 2009). The gall insects are repre-sented by the following orders: Coleoptera, Diptera, Hemi-ptera, HymenoHemi-ptera, LepidoHemi-ptera, and Thysanoptera. DiHemi-ptera, represented mainly by Cecidomyiidae, is the main group of galling insects (Mani 1964).
Many galling species of Cecidomyiidae may reach the level of pest. In Brazil, species are recorded attacking plants of cassava, guava and pitanga (Fernandes 1987; Maia 2001; Ângelo & Maia 1999). Predator and galling larvae of Cecidomyiidae have been used as biological control and fungivorous larvae serve as indicators of soil conditions (Gagné 1994; Mamaev 1968). The Brazilian ecosystems more investigated in relation to composition of Cecidomyiidae fauna and diversity of galling insects are the Cerrado and Atlantic Florest (more specifically, restingas), but these stud-ies still represent a small fraction of the total area of these biomes. In the Rio de Janeiro State, insect galls inventories were carried out in restinga areas of Angra dos Reis (Ilha Grande), Rio de Janeiro (Grumari), Maricá, Carapebus, and Arraial do Cabo (Maia & Oliveira 2010; Oliveira & Maia 2005; Maia 2001; Monteiro et al. 1994, 2004). In these stud-ies, the richness of insect galls was evidenced and Cecidomyiidae pointed as the most frequent galling taxo-nomic group. The number of galls induced by Cecidomyiidae was 36, 43, 76, 68, 99, and 93, respectively, with a total of 65 described new species (Maia & Oliveira 2010; Oliveira & Maia 2005; Maia 2001; Monteiro et al. 1994, 2004). For other
localities of Rio de Janeiro State, little information is availa-ble.
The present study was conducted in Ilha da Marambaia (Mangaratiba municipality, in southern Rio de Janeiro State). The relevance of this work is based on the ecological impor-tance of the galling insects, on the scarce knowledge of taxo-nomic, biological and geographical distribution of gallers throughout all Brazilian territory and on the fact that the veg-etation of Ilha da Marambaia includes one of the last re-serves of the Atlantic Florest in southeastern Rio de Janeiro. Furthermore, among the published insect gall inventories in the State of Rio de Janeiro, only one surveyed its southern portion (Oliveira & Maia 2005).
MATERIAL AND METHODS
Sampling was carried out monthly from April 2010 to March 2011 by two researchers along the entire extension of seven beaches of Ilha da Marambaia (Mangaratiba, RJ), to-taling 16 hours per month for all the beaches: Kutuca (23º4’4.85”S 43º59’39.41”W – 23º3’59.17”S 43º59’33.59”W, 285 meters), Grande (23º3’57.34”S 43º59’31.01”W – 23º3’27.08”S 43º59’28.63”W, 990 meters), Suja (23º3’21.81”S 43º58’51.35”W – 23º2’48.29”S 43º58’28.69”W, 1,350 meters), Caju (23º2’39.85”S 43º57’54.96”W – 23º2’33.64”S 43º57’ 46.12”W, 370 meters), João Manoel (23º2’34.17”S 43º57’ 44.18”W – 23º2’34.89”S 43º57’35.75”W, 260 meters), Sítio (23º2’34.83”S 43º57’30.80”W – 23º4’4.85”S 43º59’39.41”W, 400 meters), and Armação (23º2’27.43”S 43º57’15,53”W – 23º3’38.64”S 43º54’9.10”W, 3,960 meters) (Fig. 1). The beaches were chosen due to their conservation condition (few buildings and good vegetation cover).
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 2alenerodrigues@yahoo.com.br
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.
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At each beach, along its entire length, herbaceous, shrubby and arboreous plants (with up to two meters high, galled or not) were surveyed for insect galls, representing a vegeta-tion sampling effort of 100%. Only aerial organs were inves-tigated. All gall morphotypes were photographed in the field. Each morphotype was characterized by the plant organ of occurrence, shape, presence or absence of trichomes, com-plexity, color, number of internal chamber, and galling in-sect. The gall shape was based on Isaias et al. (2013), and the differentiation between complex gall (with formation of new plant tissues) and simple gall (without formation of other tissues) was based on Möhn (1962).
Branches (whenever possible with flowers and fruits) were removed from each host plant, and pressed in the field for preparation of exsiccates. They were examined by botanists
of Museu Nacional (MNRJ), Universidade Federal do Rio
de Janeiro and Universidade do Estado do Rio de Janeiro
(UERJ) for species identification. The botanical material was deposited in the herbarium of MNRJ. Galled branches were collected and transported to laboratory in closed and labeled plastic bags. To obtain the adults, samples of each gall morphotype were separately conditioned in closed transpar-ent plastic pots, labeled and lined with wet paper. In the case of larvae that leave the galls, the rearing pots received a layer of approximately 10 cm of restinga soil. The pots were checked every day for newly emerged adults. When adults were found, the pots were placed in a refrigerator for some hours, to induced insect lethargy. The adults were transferred to tubes with 70% ethanol. To observe the internal chamber(s) and remove immatures, some galls were dissected, using a stylet. Samples of each gall morphotype were dried for preser-vation and incorporated in the gall collection of MNRJ. The gall midges (Cecidomyiidae) were mounted in microscopy slides following the methodology of Gagné (1994), except for using butyl acetate instead of clove oil, to be less toxic
and to present satisfactory results. The excedent specimens remained in 70% ethanol. The Cecidomyiidae were identi-fied to genus level using the keys of Gagné (1994) and to species based on original descriptions. All the specimens were deposited in the Diptera collection of the MNRJ. The other insects were identified by specialists and were deposited in the collection of their institutions.
The average number of gall morphotypes per host plant species was calculated using simple arithmetic mean. The plant species and genera were considered super-host when bearing a high richness of insect galls, according Espírito-Santo & Fernandes (2007). The richness of galling species of each beach was evaluated qualitatively, based on the num-ber of gall morphotypes. According to temporal occurrence, the morphotypes were classified as constant (greater than or equal to 50%), accessory (between 25% and 50%) and acci-dental (less than or equal to 25%) as proposed by Silveira Neto et al. (1976). The formula used was C% = (p/n) * 100, where “p” is the number of months that the gall morphotype was collected and “n” is the total number of collecting months.
RESULTS
In the restinga areas of the Ilha da Marambaia, 147 gall morphotypes were found in 70 plant species, distributed in 33 families and at least 54 genera. The average number of gall morphotypes per host plant species was 2.1 (Table I). Fifty two insect gall morphotypes were first recorded from Brazil-ian restinga areas. Myrtaceae, Bignoniaceae, and Fabaceae presented the highest richness of galls (20, 13, and 11 morphotypes, respectively) and largest number of host plant species (9, 4, and 6 species, respectively), followed by Asteraceae, Euphorbiaceae, Sapindaceae, Malpighiaceae, and Nyctaginaceae (with 10, 10, 9, 9, and 8 morphotypes, respec-tively, Table II).
175 Insect galls of restinga areas of Ilha da Marambaia, Rio de Janeiro, Brazil
Revista Brasileira de Entomologia 58(2): 173–197, June 2014
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 etal. 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
Marambaia Ilha Grande Grumari Maricá Carapebus Jurubatiba Arraial doCabo
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 IlhadaMarambaia (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
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Eugenia L., Fridericia Mart., Guapira Aubl.,and Mikania Willd.were the super-host genera, presenting, 12, 9, 8, and 7 morphotypes, respectively. Two plant genera were first recorded as insect gall hosts: Sida L. (Malvaceae) and Securidaca L. (Polygalaceae). Fifteen plant species were first recorded as in-sect gall hosts: Adenocalymma comosum (Cham.) DC. (Bignoniaceae); Calyptranthes brasiliensis Spreng. (Myrtaceae);
Chaetocharpus echinocarpus (Baill.) Ducke (Euphorbiaceae);
Coccolobaalnifolia Casar. (Polygonaceae); Davilla rugosa Poir. (Dilleniaceae); Eugenia punicifolia (Kunt) DC. (Myrtaceae); Fridericia rego (Vell.) L.G. Lohmann (Bignoniaceae); Guarea guidonia (L.) Sleumer (Meliaceae); Gymnanthes gaudichaudii Müll.Arg. (Euphorbiaceae); Myrcia acuminatissima O. Berg. (Myrtaceae); Myrcia splendens (SW.) DC. (Myrtaceae); Psidium guajava L. (Myrtaceae); Stigmaphyllon ciliatum (Lam.) A. Juss. (Malpighiaceae); Xylopia involucrata M. C. Dias & Kin.-Gouv. (Annonaceae); and Zolernia glabra (Spreng.) Yakovlev (Fabaceae). Twenty plants (28% of the total) could not be iden-tified to species level, as the exsiccates comprised only non fer-tile material.
Galls were found in leaves (n = 78), stems (n = 38), flow-ers (inflorescences and flower buds) (n = 14), buds (n = 8), fruits (n = 8), adventitious root (n = 1), with predominance of 53% of leaf galls. The majority of the gall morphotypes
occurred in a unique plant organ, with three exceptions: the fusiform galls on leaves of Fridericia conjugata (Vell.) L.G. Lohmann (Bignoniaceae), the conical galls on leaves of
Struthanthus concinnus Mart.(Loranthaceae), and the
fusi-form galls on leaves of a non identified species of Malpighia-ceae, which also occurred on stems in the three species and on tendrils of the first species as well.
Thirteen gall shapes were detected, predominating the fusiform (n = 44), globoid (n = 40), lenticular (n = 18), and conical (n = 15 morphotypes). Only one morphotype pre-sented shape variation: from conical to ovoid on Eugenia
uniflora L. (Myrtaceae), being the former the most
com-mon. Eighty-nine gall morphotypes were classified as simple and 55 morphotypes as complex. The morphotypes were green, brown, yellow, red, pink, orange, white or black, with predominance of green color (48%). Thirty-five morphotypes presented color variation associated with the ontogenetic process. The majority of galls was one-cham-bered (75%), often occupied by a unique galling larva, ex-cept for the leaf conical gall on Eugenia uniflora (Myrtaceae) with two larvae in some samples. The gall char-acterization (shape, color, number of internal chamber, pres-ence or abspres-ence of trichomes, vegetal organ of occurrpres-ence, complexity and inducers) is presented in Table III. The ac-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 Ficussp. 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 Securidacasp. 03 03
Polygonaceae Coccoloba alnifolia 01 01 01
Rubiaceae Borreria verticillata 01 01 01 01
Rubiaceae sp. 03 01 02 02
Salicaceae Caseariasp. 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
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Table III. Gall characterization (shape, color, number of internal chamber, trichomes, galled plant organ, and inducing insects), in restinga areas of Ilha da Marambaia (Mangaratiba, RJ), according to the present study.
Plant Families Plant Species Occurrence organ Gall Shape Color Trichomes Complexity Number of InternalChambers Galler FigureNumber Anacardiaceae Schinnus terebinthifolius stem fusiform brown glabrous simple one Lepidoptera Fig. 2 Annonaceae Xylopia involucrata stem globoid green glabrous complex one undeterminated Fig. 3 Apocynaceae Aspidosperma pyricollum leaf lenticular opening green glabrous simple one Psyllidae, Hemiptera Fig. 4 leaf lenticular yellow glabrous simple one undeterminated Fig. 5 leaf marginal roll green glabrous simple one undeterminated Fig. 6 Asteraceae Mikania argyraea stem fusiform green hairy simple multi Cecidomyiinae, Cecidomyiidae Fig. 7 leaf fusiform green-brown hairy simple one undeterminated Fig. 8 leaf globoid green-brown hairy complex one Cecidomyiinae, Cecidomyiidae Fig. 9 Mikania biformis leaf conical green glabrous complex one Liodiplosis cylindrica Gagné, 2001 Fig.10 leaf globoid green glabrous simple one Liodiplosis spherica Gagné, 2001 Fig. 11 Mikania micrantha stem conical green glabrous complex one Cecidomyiinae, Cecidomyiidae Fig. 12 leaf conical green glabrous complex one Cecidomyiinae, Cecidomyiidae Fig. 13 Porophyllum ruderale inflorescence fusiform green glabrous simple multi undescribed species of Asphondylia Fig. 14 Vernonia rufogrisea stem fusiform brown glabrous simple one Tephritidae, Diptera Fig. 15 stem globoid yellow glabrous complex multi Asphondylia sp. Fig. 16 Bignoniaceae Adenocalymma comosum stem fusiform green glabrous simple multi undeterminated
leaf fusiform green glabrous simple one undeterminated
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Table III. Continued.
Plant Families Plant Species Occurrence organ Gall Shape Color Trichomes Complexity ChambersNumber of Internal Galler FigureNumber bud rosette green-red-brown glabrous complex one undescribed species of Dactylodiplosis Fig. 42 Croton compressus stem fusiform green glabrous simple one Lepidoptera Fig. 43 inflorescence amorphic yellow glabrous complex multi undeterminated Fig. 44 Croton floribundus leaf marginal roll green-white hairy simple one undeterminated Fig. 45 leaf globoid green-white hairy complex one Clinodiplosis sp. Fig. 46 stem fusiform green hairy simple multi undeterminated Fig. 47 Gymnanthes gaudichaudii fruit globoid orange glabrous simple one undeterminated Fig. 48 Fabaceae Andira fraxinifolia leaf globoid green glabrous complex one Asphondylia sp. Fig. 49 leaf lineal green glabrous complex one Lopesia sp. Fig. 50 Clitoria sp. leaf leaf fold green glabrous simple one Contarinia sp. Fig. 51 leaf globoid green glabrous simple multi Curculionidae, Coleoptera Fig. 52 Dalbergia ecastophylla leaf globoid green glabrous complex one Lopesia grandis Maia, 2001 Fig. 53 Inga sp. leaf globoid yellow hairy complex one Cecidomyiinae, Cecidomyiidae Fig. 54
stem fusiform green hairy simple multi Neolasioptera sp.
leaf fusiform green hairy simple one Neolasioptera sp. Fig. 55 Fabaceae Stylosanthes guianensis inflorescence – – – – – Lestodiplosis maricaensis Santos & Maia, 2008 Fig. 56
Zollernia glabra leaf fusiform green glabrous simple one Curculionidae, Coleoptera
flower bud – pink glabrous simple one Curculionidae, Coleoptera Fig. 57 Lauraceae Ocotea notata fruit globoid yellow glabrous simple one undescribed species of Bruggmanniella Fig. 58 stem fusiform brown glabrous simple multi undeterminated Fig. 59 Loranthaceae Struthanthus concinnus leaf and stem conical green glabrous complex one Asphondylia sp. Figs. 60–61
adventitious root fusiform brown glabrous simple one Cecidomyiinae, Cecidomyiidae Fig. 62 Malpighiaceae Byrsonima sericea leaf lenticular brown hairy simple one Dasineura byrsonimae Maia, 2005 Fig. 63 inflorescence globoid brown glabrous simple one Asphondylia byrsonimae Maia & Couri, 1992 Fig. 64 inflorescence globoid green glabrous complex one Lepidoptera Fig. 65 inflorescence fusiform brown glabrous simple one Cecidomyiinae, Cecidomyiidae Fig. 66 stem fusiform brown glabrous simple multi Cecidomyiinae, Cecidomyiidae Fig. 67 Heteropterys nitida flower bud – – – – – Curculionidae, Coleoptera Fig. 68 Peixotoa sp. leaf lenticular brown-green hairy simple one Cecidomyiinae, Cecidomyiidae Fig. 69 Stigmaphyllon ciliatum stem fusiform brown glabrous simple multi undeterminated Fig. 70 Malpighiaceae sp. stem and leaf fusiform brown-green-yellow glabrous simple one-multi undescribed species of Lopesia Figs. 71–72 Malvaceae Luehea divaricata leaf globoid brown glabrous complex one Cecidomyiinae, Cecidomyiidae Fig. 73
stem globoid brown glabrous complex one Cecidomyiinae, Cecidomyiidae Fig. 74 stem globoid green glabrous complex one undeterminated Fig. 75 leaf marginal roll green glabrous simple one undeterminated
Sida sp. stem fusiform brown glabrous simple one Cecidomyiinae, Cecidomyiidae Fig. 76 Melastomataceae Miconia cinnamomifolia leaf globoid red glabrous complex one undeterminated Fig. 77 stem globoid brown glabrous complex one undeterminated Fig. 78 Meliaceae Guarea guidonia leaf fusiform brown-green glabrous simple one Cecidomyiinae, Cecidomyiidae
stem fusiform brown-green glabrous simple one Cecidomyiinae, Cecidomyiidae
leaf globoid yellow glabrous complex one Cecidomyiinae, Cecidomyiidae Fig. 79 Moraceae Ficus sp. leaf leaf fold green-red glabrous simple one Thysanoptera Fig. 80
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Table III. Continued.
Plant Families Plant Species Occurrence organ Gall Shape Color Trichomes Complexity ChambersNumber of InternalGaller FigureNumber Myrtaceae Calyptranthes brasiliensis bud conical green-brown glabrous complex multi undeterminated Fig. 81
Eugenia adstringens leaf marginal roll green glabrous simple one Dasineura marginalis Maia, 2005 Fig. 82 leaf lenticular green glabrous simple one Dasineura globosa Maia, 1995 Fig. 83 Eugenia copacabanensis leaf spiral green-red glabrous complex one Stephomyia espiralis Maia, 1993 Fig. 84
leaf lenticular green glabrous simple one undeterminated
Eugenia punicifolia leaf cylindrical yellow-green glabrous complex one Stephomyia sp. Fig. 85 leaf lenticular green-red glabrous simple one Cecidomyiinae, Cecidomyiidae Fig. 86 stem fusiform brown glabrous simple multi Lasiopteridi Fig. 87 fruit globoid red-yellow glabrous simple multi undeterminated Fig. 88 Eugenia uniflora leaf lenticular green-black glabrous simple one Neolasioptera eugeniae Maia, 1993 Fig. 89 leaf conical green-red glabrous complex one Clinodiplosis profusa Maia, 2001 Fig. 90 leaf leaf fold green glabrous simple one Cecidomyiinae, Cecidomyiidae Fig. 91 stem fusiform brown glabrous simple – undeterminated
Myrcia acuminatissima stem globoid brown glabrous simple multi undeterminated Fig. 92 Myrcia splendens leaf globoid green glabrous complex one undeterminated Fig. 93 leaf marginal roll green glabrous simple one undeterminated Fig. 94 bud globoid green-brown glabrous complex multi undeterminated Fig. 95 leaf conical yellow-green glabrous complex one undeterminated
Psidium guajava stem fusiform brown glabrous simple multi undeterminated Fig. 96 Myrtaceae sp. leaf lenticular green glabrous simple one undeterminated Fig. 97 Nyctaginaceae Guapira opposita leaf lenticular green-red glabrous simple one Bruggmannia elongata Maia & Couri, 1993 Fig. 98 leaf globoid red glabrous complex one Bruggmannia robusta Maia & Couri, 1993 Fig. 99 leaf globoid brown glabrous complex one Bruggmannia sp. Fig. 100 leaf globoid green glabrous complex one Cecidomyiinae, Cecidomyiidae Fig. 101 leaf conical green-red glabrous complex one Bruggmannia acaudata Maia, 2004 Fig. 102 stem globoid brown glabrous simple multi Proasphondylia guapirae Maia & Couri, 1993 Fig. 103 stem globoid brown glabrous complex one undeterminated Fig. 104 flower peduncle globoid green-red-brown glabrous complex one undescribed species of Pisphondylia Fig. 105 Ochnaceae Ouratea cuspidata leaf cylindrical with apical projection brown glabrous complex one Contarinia sp. Fig. 106 leaf lenticular green glabrous simple one Cecidomyiinae, Cecidomyiidae Fig. 107 Olacaceae Ximenia americana bud fusiform brown glabrous simple one Asphondylia communis Maia & Couri, 1993 Fig. 108 Polygalaceae Securidaca sp. flower bud – – – – – Cecidomyiinae, Cecidomyiidae Fig. 109 leaf cylindrical green glabrous complex one undeterminated Fig. 110 stem cylindrical green glabrous complex one undeterminated Fig. 111 Polygonaceae Coccoloba alnifolia inflorescence globoid yellow-green glabrous complex one Lopesia sp. Fig. 112 Rubiaceae Borreria verticillata inflorescence drop-like green glabrous complex one Asphondylia borreriae Rübsaamen, 1905 Fig. 113 Salicaceae Casearia sp. leaf conical brown glabrous simple one undeterminated Fig. 114 Sapindaceae Matayba guianensis fruit – green glabrous simple one undeterminated Fig. 115 leaf globoid green glabrous complex one undeterminated Fig. 116 stem fusiform brown glabrous simple multi undeterminated Fig. 117 Serjania sp. 1 leaf fusiform green glabrous simple one Muscomorpha Fig. 118 leaf cylindrical yellow glabrous complex one Lestodiplosiini Fig. 119 stem fusiform brown glabrous simple multi undeterminated
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cidental gall morphotypes predominated with 61% (90 morphotypes), followed by constant and accessory (with 37 and 20 morphotypes, respectively). The fusiform gall
on Fridericia conjugata was constant on stems, accessory
on tendrils, and accidental in leaf veins. Thirteen morpho-types were founded in all months, and 62 were founded only in a single month.
The galling insects were distributed in five orders: Diptera (n = 82), Coleoptera (n = 4), Lepidoptera (n = 4), Hemiptera (n = 3), and Thysanoptera (n = 1), being Cecidomyiidae (Diptera) the main galling group (n = 80), with 85% of the total (Table IV). The inducers of 53 morphotypes (37% of the total) were not identified, due to high rates of parasitism and to the fact that some collected galls were already unoc-cupied. In addition to gallers, other arthropods were associ-ated with the galls: parasitoids, represented exclusively by Hymenoptera (in 54 morphotypes); inquilines, represented by Cecidomyiidae (Diptera), Lepidoptera, Curculionidae (Coleoptera), Thysanoptera, Sciaridae, Tephritidae (Diptera), and Aphididae (Hemiptera) (in 6, 5, 3, 3, 1, 1, and 1 morpho-types, 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.
Ta bl e I II . C ontinued. P la nt F ami lie s P lant Spec ies O cc ur re nc e or ga n G all Shape C olor T richome s C om ple xi ty N um ber o f I nt er nal Ch am be rs G alle r Fi gur e Number Se rj ani a s p. 2 leaf fu si fo rm gr ee n-ye llo w glabr ous si mple one C ec idom yiinae, C ec idom yiidae Fi g. 120 leaf lenticular gr ee n-ye llo w glabr ous si mple one undete rm inated Fi g. 121 leaf petiol e fus if or m gr ee n-ye llo w glabr ous si mple one undete rm inated Fi g. 122 S apot ace ae P oute ria c a im ito leaf conic al gr een glabr ous comple x one Y oung om yia pouter iae M ai a, 2001 Fi g. 123 leaf lenticular gr ee n glabr ous si mple one Lopes ia si ngular is M aia, 2001 Sider o xylon obtus if olium fr uit globoid gr een glabr ous si mple multi undes cr ibe d s pecies of B ruggm anniella Fi g. 124 S m il ac ace ae S m il a x ru fe sce n s le af le ntic ula r gr ee n-y ello w -re d gla brous si mple one Smilas iopter a cande lar iae M öhn, 1975 Fi g. 125 leaf conic al gr een glabr ous comple x one Hemipter a Fig. 126 leaf fu si fo rm gr ee n-re d glabr ous si mple one C ec idom yiinae, C ec idom yiidae Fi g. 127 st em globoid gr een-red glabr ous si mple multi undete rm inated Fi g. 128 S ol anace ae Solanum s p. leaf lenticular gr ee n glabr ous si mple one undete rm inated Fi g. 129 st em fu si fo rm gr ee n hair y si mple one undete rm inated Fi g. 130 Sol anace ae s p. leaf lenticular gr ee n glabr ous si mple one L epi dopte ra Fig. 131 bud globoid br ow n glabr ous comple x one undete rm inated Fi g. 132 st em fus if or m gr ee n glabr ous si mple multi undete rm inated V er benac eae L antana camar a leaf globoid gr een hair y comple x one Sc his m atodiplos is lantanae R übs aa m en, 1907 st em fu si fo rm br ow n-gr een hair y simple one undete rm inated Fi g. 133 L antana li lac ina leaf globoid gr een hair y comple x one undes cr ibe d s pecies of A sphondylia Fi g. 134 leaf cy lindr ic al gr ee n hair y comple x one undete rm inated Fi g. 135 Stac h ytar pheta s p. inf lor es cence globoid gr een hair y comple x one A sphody li a st achy ta rp h et a B ar nes , 1932 Fi g. 136
Table IV. Distribution of the number of gall morphotypes per galling insect order in restinga areas of IlhadaMarambaia (Mangaratiba, RJ), according to the present study.
Order of insects gallers Morphotypes of Galls Number Pecentage (%)
Diptera 82 87
Cecidomyiidae 80 85
Tephritidae 1 1
Muscomorpha 1 1
Coleoptera 4 4
Lepidoptera 4 4
Hemiptera 3 3
Thysanoptera 1 1
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Gall Characterization
Anacardiaceae
Schinus terebintifolius Raddi
Gall (Fig. 2): on stem, fusiform, brown, glabrous, simple, one-chambered. Galler: Lepidoptera. Locality: Armação Beach. Occurrence period: December 2010. Temporal con-stancy: accidental. Previous records from Brazilian restinga areas: Cabo Frio, Bertioga and Grumari (Maia 2013; Maia et al. 2008; Oliveira & Maia 2005).
Annonaceae
Xylopia involucrata M. C. Dias & Kin.-Gouv.
Gall (Fig. 3): on stem, fusiform, green, glabrous, com-plex, one-chambered. Galler: undetermined. Locality: Armação Beach. Occurrence period: September 2010. Tem-poral constancy: accidental.
This is the first record of insect galls in this plant species.
Apocynaceae
Aspidosperma pyricollum Müll. Arg.
Gall (Fig. 4): on leaf, lenticular, permanently open, green, glabrous, simple, one-chambered. Galler: Psyllidae (Hemi-ptera). Locality: João Manoel Beach. Occurrence period: April, May, December 2010, February and March 2011. Tem-poral constancy: accessory. Previous records from Brazilian restinga areas: Ilha Grande and Maricá (Maia & Oliveira 2010; Maia 2001; Monteiro et al. 1994).
Gall (Fig. 5): on leaf, lenticular, yellow, glabrous, simple, one-chambered. Galler: undetermined. Locality: Sítio Beach. Occurrence period: November 2010. Temporal constancy: ac-cidental. No previous records from Brazilian restinga areas.
Gall (Fig. 6): on leaf, marginal roll, green, glabrous, simple, one-chambered. Galler: undetermined. Locality: João Manoel Beach. Occurrence period: November 2010. Tem-poral constancy: accidental. No previous records from Bra-zilian restinga areas.
Asteraceae
Mikania argyreiae DC.
Gall (Fig. 7): on stem, fusiform, green, hairy, simple, multi-chambered. Galler: Cecidomyiinae (Diptera, Ceci-domyiidae). Locality: Suja Beach. Occurrence period: De-cember 2010. Temporal constancy: accidental. Previous records from Brazilian restinga areas: Bertioga (Maia et al. 2008).
Gall (Fig. 8): on leaf vein, fusiform, green-brown, hairy, simple, one-chambered. Galler: undetermined. Locality: Suja Beach. Occurrence period: December 2010. Temporal con-stancy: accidental. No previous records from Brazilian restinga areas.
Gall (Fig. 9): on leaf, globoid, green-brown, hairy, com-plex, one-chambered. Galler: Cecidomyiinae (Diptera, Cecidomyiidae). Associated fauna: Hymenoptera parasitoid. Locality: Suja Beach. Occurrence period: December 2010. Temporal constancy: accidental. Previous records from Bra-zilian restinga areas: Bertioga (Maia et al. 2008).
Mikania biformis DC.
Gall (Fig. 10): on leaf, conical, green, glabrous, simple, one-chambered. Galler: Liodiplosis cylindrica Gagné, 2001 (Diptera, Cecidomyiidae). Associated fauna: Hymenoptera parasitoid. Localities: Suja, João Manoel, Sítio and Armação Beaches. Occurrence period: April, December 2010, Janu-ary and FebruJanu-ary 2011. Temporal constancy: accessory. Pre-vious records from Brazilian restinga areas: Bertioga (Maia et al. 2008).
Gall (Fig. 11): on leaf, globoid, green, glabrous, simple, one-chambered. Galler: Liodiplosis spherica Gagné, 2001 (Diptera, Cecidomyiidae). Localities: Suja, João Manoel, Sítio and Armação Beaches. Occurrence period: May, December 2010, January and February 2011. Temporal constancy: ac-cessory. Previous records from Brazilian restinga areas: Bertioga (Maia et al. 2008).
Mikania micrantha Kunt.
Gall (Fig. 12): on stem, conical, green, glabrous, com-plex, one-chambered. Galler: Cecidomyiinae (Diptera, Cecidomyiidae). Locality: Armação Beach. Occurrence pe-riod: December 2010, January, February and March 2011. Temporal constancy: accessory. No previous records from Brazilian restinga areas.
Gall (Fig. 13): on leaf, conical, green, glabrous, complex, one-chambered. Galler: Cecidomyiinae (Diptera, Cecidomyi-idae). Localities: Armação Beach. Occurrence period: Janu-ary and FebruJanu-ary 2011. Temporal constancy: accidental. No previous records from Brazilian restinga areas.
Porophyllum ruderale (Jack.) Cass.
Gall (Fig. 14): on inflorescence, fusiform, green, glabrous, simple, multi-chambered. Galler: undescribed species of
Asphondylia (Diptera, Cecidomyiidae). Associated fauna:
Trypanea sp. (Diptera, Tephritidae) inquiline. Locality:
Armação Beach. Occurrence period: December 2010, Janu-ary, February and March 2011. Temporal constancy: acces-sory. No previous records from Brazilian restinga areas.
Vernonia rufogrisea St. Hill.
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Gall (Fig. 16): stem, globoid, yellow, glabrous, complex, multi-chambered. Galler: Asphondylia sp. (Diptera, Cecidomyiidae). Associated fauna: Sciaridae (Diptera) and Resseliella sp. (Diptera, Cecidomyiidae) inquilines; and Hy-menoptera parasitoid. Locality: Grande Beach. Occurrence period: December 2010, January and February 2011. Tem-poral constancy: accidental. No previous records from Bra-zilian restinga areas.
Bignoniaceae
Adenocalymma comosum (Cham.) DC.
Gall: on leaf vein, fusiform, green, glabrous, simple, one-chambered. Galler: undeterminated. Locality: Suja Beach. Oc-currence period: January 2011. Temporal constancy: accidental. Gall: on stem, fusiform, green, glabrous, simple, multi-chambered. Galler: undeterminated. Localities: Suja and Armação Beaches. Occurrence period: January 2011. Tem-poral constancy: accidental.
This is the first record of insect galls in this plant species.
Fridericia conjugata (Vell.) L.G. Lohmann (=
Arrabidaea conjugata (Vell.) Mart.)
Gall (Fig. 17): on leaf, conical, green, glabrous, com-plex, one-chambered. Galler: Arrabidaeamyia serrata Maia, 2001 (Diptera, Cecidomyiidae). Localities: Grande and Armação Beaches. Occurrence period: April and May 2010. Temporal constancy: accidental. Previous records from Bra-zilian restinga areas: Grumari, Maricá, Arraial do Cabo, Carapebus, and Jurubatiba (Oliveira & Maia 2005; Maia 2001; Monteiro et al. 1994, 2004)
Gall: on stem (Fig. 18), tendril and vein, fusiform, green, glabrous, simple, one or multi-chambered. Galler:
Neolasiop-tera sp. (Diptera, Cecidomyiidae). Associated fauna:
Lestodiplosis sp. (Cecidomyiidae, Diptera) and Cecidomyiidae sp. inquilines of stem gall, and Hymenoptera parasitoid of stem and tendril galls. Localities: Grande, Kutuca, Suja, Caju, João Manoel, Sítio and Armação Beaches. Occurrence period: April, May, July, August, September, October, November, Decem-ber 2010, January and March 2011. Temporal constancy: con-stant on the stem, accessory on the tendril and accidental on the vein. Previous records from Brazilian restinga areas: Grumari, Maricá, Carapebus, and Jurubatiba (Oliveira & Maia 2005; Maia 2001; Monteiro et al. 1994, 2004).
Gall (Fig. 19): on fruit, brown, glabrous, simple, one-chambered. Galler: undeterminated. Associated fauna: Hy-menoptera parasitoid, Coleoptera and Lepidoptera inquilines. Locatity: Armação Beach. Occurrence period: November 2010. Temporal constancy: accidental. No previous records from Brazilian restinga areas.
Fridericia rego (Vell.) L.G. Lohmann
Gall (Fig. 20): on leaf, conical, green, glabrous, com-plex, one-chambered. Galler: undeterminated. Associated
fauna: Hymenoptera parasitoid. Locality: Suja Beach. Oc-currence period: March 2011. Temporal constancy: acciden-tal.
Gall (Fig. 21): on leaf vein, fusiform, green, glabrous, simple, one-chambered. Galler: undeterminated. Locality: Suja Beach. Occurrence period: February 2011. Temporal constancy: accidental.
Gall (Fig. 22): on stem, fusiform, green, glabrous, simple, multi-chambered. Galler: Alycauliini (Diptera, Cecidomyiidae). Associated fauna: Hymenoptera parasitoid. Localities: Suja, Sítio and Armação Beaches. Occurrence period: March 2011. Tem-poral constancy: accidental.
Gall (Fig. 23): on flower peduncle, fusiform, green, gla-brous, simple, one-chambered. Galler: Cecidomyiidae (Diptera). Locality: Suja Beach. Occurrence period: Febru-ary and March 2011. Temporal constancy: accidental.
This is the first record of insect galls in this plant species.
Bignoniaceae sp.
Gall (Fig. 24): on leaf vein, fusiform, green, glabrous, simple, one-chambered. Galler: undeterminated. Locality: Suja Beach. Occurrence period: March 2011. Temporal con-stancy: accidental.
Gall (Fig. 25): on stem, fusiform, green, glabrous, simple, multi-chambered. Galler: undeterminated. Locality: Suja Beach. Occurrence period: March 2011. Temporal constancy: accidental.
Boraginaceae Tournefortia sp.
Gall (Fig. 26): on fruit, globoid, green, glabrous, simple, multi-chambered. Galler: Asphondylia sp. (Diptera, Cecidomyiidae). Associated fauna: Hymenoptera parasitoid. Localities: Grande and Kutuca Beaches. Occurrence period: December 2010, January February and March 2011. Tempo-ral constancy: accessory. No previous records from Brazil-ian restinga areas.
Burseraceae
Protium brasiliensis (Spr.) Engl.
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Protium icicariba (DC.) Marchand
Gall (Fig. 29): on leaf, marginal roll, green, glabrous, simple, one-chambered. Galler: Lopesia simplex Maia, 2001 (Diptera, Cecidomyiidae). Localities: Grande, Kutuca, Suja and Armação Beaches. Occurrence period: April, May, Oc-tober, December 2010, February and March 2011. Temporal constancy: constant. Previous records from Brazilian restinga areas: Guarapari, Jurubatiba, and Carapebus (Bregonci et al. 2010; Monteiro et al. 2004; Maia 2001).
Gall (Fig. 30): on leaf, conical, green, glabrous, com-plex, one-chambered. Galler: Dactylodiplosis icicaribae Maia, 2002 (Diptera, Cecidomyiidae). Localities: Grande, Kutuca and Armação Beaches. Occurrence period: April, October, December 2010, February and March 2011. Tem-poral constancy: accessory. Previous records from Brazilian restinga areas: Jurubatiba, and Carapebus (Monteiro et al. 2004; Maia 2001)
Gall (Fig. 31): on leaf, lenticular, green-yellow, glabrous, simple, one-chambered. Galler: Psyllidae (Hemiptera). Lo-calities: Grande, Kutuca and Armação Beaches. Occurrence period: April, May, July, Agust, Setember, October, Novem-ber, December 2010, January, February and March 2011. Temporal constancy: constant. Previous records from Bra-zilian restinga areas: Guarapari, and Jurubatiba (Bregonci et al. 2010; Monteiro et al. 2004).
Cactaceae
Selenicereus setaceus (SD) Berg
Gall (Fig. 32): on stem, globoid, green, glabrous, simple, multi-chambered. Galler: Neolasioptera cerei Rübsaamen, 1905 (Diptera, Cecidomyiidae). Associated fauna: Hy-menoptera parasitoid. Localities: Grande, Kutuca, Suja, Caju, João Manoel, Sítio and Armação Beaches. Occurrence pe-riod: April 2010 to March 2011. Temporal constancy: con-stant. Previous records from Brazilian restinga areas: Ilha Grande, Jurubatiba, Maricá, and Carapebus (Maia & Oliveira 2010; Monteiro et al. 2004; Maia 2001).
Celastraceae
Maytenus obtusifolia Mart.
Gall (Fig. 33): on leaf, lenticular, green, glabrous, simple, one-chambered. Galler: Mayteniella distincta Maia, 2001 (Diptera, Cecidomyiidae). Associated fauna: Hymenoptera parasitoid. Localities: Grande, Kutuca, Suja, Caju, João Manoel, Sítio and Armação Beaches. Occurrence period: April 2010 to March 2011. Temporal constancy: constant. Previous records from Brazilian restinga areas: Grumari, Maricá, Carapebus, Arraial do Cabo, and Jurubatiba (Oliveira & Maia 2005; Maia 2001; Monteiro et al. 1994, 2004).
Gall (Fig. 34): on stem, fusiform, green, glabrous, simple, multi-chambered. Galler: undeterminated. Associated fauna: Hymenoptera parasitoid. Locality: Caju Beach. Occurrence
period: February 2011. Temporal constancy: accidental. No previous records from Brazilian restinga areas.
Gall (Fig. 35): on bud, fusiform, green, glabrous, simple, multi-chambered. Galler: undeterminated. Associated fauna: Hymenoptera parasitoid. Locality: Suja Beach. Occurrence period: December 2010. Temporal constancy: accidental. No previous records from Brazilian restinga areas.
Convolvulaceae Convolvulaceae sp.
Gall (Fig. 36): on stem, fusiform, green, glabrous, simple, one-chambered. Galler: Alycaulini (Diptera, Cecidomyiidae). Locality: Grande, Suja, Sítio Beaches. Occurrence period: November, December 2010, January, February and March 2011. Temporal constancy: accessory. No previous records from Brazilian restinga areas.
Dilleniaceae Davilla rugosa Poir.
Gall (Fig. 37): on bud, rosette, green-brown, hairy, com-plex, one-chambered. Galler: undeterminated. Locality: Kutuca Beach. Occurrence period: June and October 2010. Temporal constancy: accidental.
Gall (Fig. 38): on fruit, globoid, yellow-orange, simple, one-chambered. Galler: Cecidomyiidae (Diptera). Associated fauna: Hymenoptera parasitoid. Locality: Kutuca Beach. Occurrence period: June, August, Setember, October and November 2010. Temporal constancy: accessory.
This is the first record of insect galls in this plant species.
Euphorbiaceae
Alchornea triplinervia (Spreng.) Müll. Arg.
Gall (Fig. 39): on stem, fusiform, brown, glabrous, simple, multi-chambered. Galler: Cecidomyiidae (Diptera). Local-ity: Suja Beach. Occurrence period: December 2010. Tem-poral constancy: accidental. Previous records from Brazilian restinga areas: Bertioga (Maia et al. 2008).
Chaetocharpus echinocarpus (Baill.) Ducke
Gall (Fig. 40): on leaf, lenticular, gree-yellow, glabrous, simple, one-chambered. Galler: undeterminated. Locality: Armação Beach. Occurrence period: May 2010 and January 2011. Temporal constancy: accidental.
Gall (Fig. 41): on bud, rosette, green-brown, glabrous, complex, multi-chambered. Galler: undeterminated. Asso-ciated fauna: Hymenoptera parasitoid. Localities: Grande and Armação Beaches. Occurrence period: August, October, November, December 2010, January, February and March 2011. Temporal constancy: constant.
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Dactylodiplosis (Diptera, Cecidomyiidae). Locality: Armação Beach. Occurrence period: November 2010, January and February 2011. Temporal constancy: accidental.
This is the first record of insect galls in this plant species.
Croton compressus Lam.
Gall (Fig. 43): on stem, fusiform, green, hairy, simple, one-chambered. Galler: Lepidoptera. Localities: Kutuca, Suja, Sítio and Armação Beaches. Occurrence period: De-cember 2010 and January 2011. Temporal constancy: acci-dental. Previous records from Brazilian resting areas: Cabo Frio (Maia 2013).
Gall (Fig. 44): on inflorescence, amorphic, yellow, hairy, complex, multi-chambered. Galler: undeterminated. Asso-ciated fauna: Curculionidae (Coleoptera) inquiline and Hy-menoptera parasitoid. Localities: Grande and Suja Beaches. Occurrence period: January and February 2011. Temporal constancy: accidental. No previous records from Brazilian restinga areas.
Croton floribundus Spreng.
Gall (Fig. 45): on leaf, marginal roll, green-white, hairy, simple, one-chambered. Galler: undeterminated. Locality: Kutuca Beach. Occurrence period: March 2011. Temporal constancy: accidental. No previous records from Brazilian restinga areas.
Gall (Fig. 46): on leaf, globoid, green-white, hairy, com-plex, one-chambered. Galler: Clinodiplosis sp. (Diptera, Cecidomyiidae). Locality: Kutuca Beach. Occurrence pe-riod: January, February and March 2011. Temporal con-stancy: accidental. No previous records from Brazilian restinga areas.
Gall (Fig. 47): on stem, fusiform, green, hairy, simple, multi-chambered. Galler: undeterminated. Locality: Armação Beach. Occurrence period: January 2011. Temporal con-stancy: accidental. No previous records from Brazilian restinga areas.
Gymnanthesgaudichaudii Müll.Arg.
Gall (Fig. 48): on fruit, globoid, orange, glabrous, simple, one-chambered. Galler: undeterminated. Locality: Kutuca Beach. Occurrence period: December 2010. Temporal con-stancy: accidental.
This is the first record of insect galls in this plant species.
Fabaceae
Andira fraxinifolia Benth.
Gall (Fig. 49): on leaf, globoid, green, glabrous, com-plex, one-chambered. Galler: Asphondylia sp. (Diptera, Cecidomyiidae). Associated fauna: Hymenoptera parasitoid. Locality: Sítio Beach. Occurrence period: December 2010, January, February and March 2011. Temporal constancy:
accessory. Previous records from Brazilian restinga areas: Bertioga (Maia et al. 2008).
Gall (Fig. 50): on leaf, lineal, green, glabrous, complex, one-chambered. Galler: Lopesia sp. (Diptera, Cecidomyi-idae). Associated fauna: Cecidomyiinae sp. (Diptera, Cecidomyiidae) inquiline and Hymenoptera parasitoid. Lo-calities: Grande, Kutuca, Suja, Sítio and Armação Beaches. Occurrence period: April 2010 to March 2011. Temporal constancy: constant. Previous records from Brazilian restinga areas: Bertioga (Maia et al. 2008).
Clitoria sp.
Gall (Fig. 51): on leaf fold, green, glabrous, simple, one-chambered. Galler: Contarinia sp. (Diptera, Cecidomyiidae). Locality: Armação Beach. Occurrence period: October, No-vember 2010 and March 2011. Temporal constancy: acci-dental. No previous records from Brazilian restinga areas.
Gall (Fig. 52): on leaf, globoid, green, glabrous, simple, multi-chambered. Galler: Curculionidae (Coleoptera). Asso-ciated fauna: Hymenoptera parasitoid. Localities: Grande, Suja and Armação Beaches. Occurrence period: December 2010 and March 2010. Temporal constancy: accidental. No previous records from Brazilian restinga areas.
Dalbergia ecastaphyllum L. Taub.
Gall (Fig. 53): on leaf, globoid, green, glabrous, com-plex, one-chambered. Galler: Lopesia grandis Maia, 2001 (Diptera, Cecidomyiidae). Associated fauna: Hymenoptera parasitoid. Localities: Grande, Kutuca, Suja, Caju, João Manoel, Sítio and Armação Beaches. Occurrence period: April 2010 to March 2011. Temporal constancy: constant. Previous records from Brazilian restinga areas: Ilha Grande, Jurubatiba, Maricá, and Carapebus (Maia & Oliveira 2010; Monteiro et al. 2004; Maia 2001).
Inga sp.
Gall (Fig. 54): on leaf, globoid, yellow, hairy, complex, one-chambered. Galler: Cecidomyiinae (Diptera, Cecidomyi-idae). Associated fauna: Hymenoptera parasitoid. Localities: Caju and Armação Beaches. Occurrence period: December 2010 and February 2011. Temporal constancy: accidental. No previous records from Brazilian restinga areas.
Gall (Fig. 55): on leaf vein, fusiform, green-brown, hairy, simple, one-chambered. Galler: Neolasioptera sp. (Diptera, Cecidomyiidae). Localities: Suja, Caju and Sítio Beaches. Occurrence period: December 2010 and January 2011. Tem-poral constancy: accidental. No previous records from Bra-zilian restinga areas.
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Stylosanthes guianensis Sw.
Inflorescence (Fig. 56) with free-life larvae of Lestodip-losis sp. (Diptera, Cecidomyiidae). Associated fauna: Lepi-doptera. Locality: Armação Beach. Occurrence period: December 2010. Temporal constancy: accidental. Previous records from Brazilian restinga areas: Jurubatiba, Maricá, and Carapebus (Monteiro et al. 2004; Maia 2001).
Zollernia glabra (Spreng.) Yakovlev
Gall: on leaf vein, fusiform, green, glabrous, simple, one-chambered. Galler: Curculionidae (Coleoptera). Locality: João Manoel Beach. Occurrence period: April, May, June and July 2010. Temporal constancy: accessory.
Closed flower (Fig. 57) with Curculionidae (Coleoptera). Localities: Caju and João Manoel Beaches. Occurrence pe-riod: July 2010. Temporal constancy: accidental.
This is the first record of insect galls in this plant species.
Lauraceae
Ocotea notota (Nees & Mart.) Mez
Gall (Fig. 58): on fruit, globoid, yellow, simple, one-cham-bered. Galler: undescribed species of Bruggmanniella (Diptera, Cecidomyiidae). Locality: Armação Beach. Occur-rence period: October, November and December 2010. Tem-poral constancy: accessory. No previous records from Brazilian restinga areas.
Gall (Fig. 59): on stem, fusiform, brown, glabrous, simple, multi-chambered. Galler: undeterminated. Locality: Armação Beach. Occurrence period: October, November, December 2010 and February 2011. Temporal constancy: accessory. Previous records from Brazilian restinga areas: Maricá, Jurubatiba (Monteiro et al. 1994, 2004).
Loranthaceae
Struthanthus concinnus Mart.
Gall: on leaf (Fig. 60) and stem (Fig. 61), conical, green, glabrous, complex, one-chambered. Galler: Asphondylia sp. (Diptera, Cecidomyiidae). Associated fauna: Camptoneuriini (Diptera, Cecidomyiidae) inquiline of leaf gall, Cecidomyi-inae sp. (Diptera, Cecidomyiidae), Thysanoptera inquilines of stem gall, and Hymenoptera parasitoid of both. Locali-ties: Grande, Kutuca, Suja and Caju Beaches. Occurrence period: April 2010 to March 2011. Temporal constancy: con-stant. No previous records from Brazilian restinga areas.
Gall (Fig. 62): on adventice root, fusiform, brown, gla-brous, simple, one-chambered. Galler: Cecidomyiinae (Diptera, Cecidomyiidae). Associated fauna: Hymenoptera parasitoid. Locality: Grande, Kutuca and Suja Beaches. Oc-currence period: April, May, June, August and November 2010. Temporal constancy: accessory. No previous records from Brazilian restinga areas.
Malpighiaceae
Byrsonima sericea DC.
Gall (Fig. 63): on leaf, lenticular, brown, hairy, simple, one-chambered. Galler: Dasineura byrsonimae Maia, 2010 (Diptera, Cecidomyiidae). Associated fauna: Hymenoptera parasitoid. Localities: Grande, Kutuca, Suja and Armação Beaches. Occurrence period: April, May, June, July, Septem-ber, OctoSeptem-ber, NovemSeptem-ber, December 2010, January, February and March 2011. Temporal constancy: constant. Previous records from Brazilian restinga areas: Ilha Grande, Guarapari, Grumari, Jurubatiba, Maricá, and Carapebus (Maia & Oliveira 2010; Bregonci et al. 2010; Oliveira & Maia 2005; Monteiro et al. 2004; Maia 2001).
Gall (Fig. 64): on inflorescence, globoid, brown, glabrous, simple, one-chambered. Galler: Bruggmanniella byrsonimae (Maia & Couri, 1992) (Diptera, Cecidomyiidae). Locality: Armação Beach. Occurrence period: April, May, July, Sep-tember, December 2010, January and February 2011. Tem-poral constancy: constant. Previous records from Brazilian restinga areas: Maricá, Carapebus, and Jurubatiba (Maia 2001; Monteiro et al. 1994, 2004).
Gall (Fig. 65): on inflorescence, globoid, green, glabrous, complex, one-chambered. Galler: Lepidoptera. Locality: Grande and Armação Beaches. Occurrence period: July 2010 to January 2011. Temporal constancy: accidental. Previous records from Brazilian restinga areas: Maricá, Arraial do Cabo, and Jurubatiba (Monteiro et al. 1994, 2004).
Gall (Fig. 66): on floral peduncle, fusiform, brown, gla-brous, simple, one-chambered. Galler: Cecidomyiinae (Diptera, Cecidomyiidae). Locality: Armação Beach. Occur-rence period: February 2011. Temporal constancy: acciden-tal. No previous records from Brazilian restinga areas.
Gall (Fig. 67): on stem, fusiform, brown, glabrous, simple, multi-chambered. Galler: Cecidomyiinae (Diptera, Cecido-myiidae). Localities: Suja and Armação Beach. Occurrence pe-riod: April, May, September, October, November, December 2010 and January 2011. Temporal constancy: constant. Previ-ous records from Brazilian restinga areas: Ilha Grande, Guarapari, Grumari, Maricá, Carapebus, Arraial do Cabo, and Jurubatiba (Maia & Oliveira 2010; Bregonci et al. 2010; Oliveira & Maia 2005; Maia 2001; Monteiro et al. 1994, 2004).
Heteropterys nitida Kunth
Closed flower (Fig. 68) with Curculionidae (Coleoptera). Localities: Kutuca, Caju and Sítio Beaches. Occurrence pe-riod: April, June and December 2010. Temporal constancy: accidental. Previous records from Brazilian restinga areas: Maricá (Maia 2001).
Peixotoa sp.
188 Rodrigues et al.
Revista Brasileira de Entomologia 58(2): 173–197, June 2014
Cecidomyiidae). Localities: Grande, Kutuca and João Manoel Beaches. Occurrence period: April, May, June, August and December 2010. Temporal constancy: constant. No previous records from Brazilian restinga areas.
Stigmaphyllon ciliatum (Lam.) A. Juss.
Gall (Fig. 70): on stem, fusiform, brown, glabrous, simple, multi-chambered. Galler: undeterminated. Locality: Suja Beach. Occurrence period: December 2010. Temporal con-stancy: accidental.
This is the first record of insect galls in this plant species.
Malpighiaceae sp.
Gall: on stem (Fig. 71) and leaf vein (Fig. 72), fusiform, brown-green-yellow, glabrous, simple, one and multi-cham-bered. Galler: undescribed species of Lopesia (Diptera, Cecidomyiidae). Locality: Grande, Kutuca and Suja Beaches. Occurrence period: April 2010 to March 2011. Temporal con-stancy: constant.
Malvaceae
Luehea divaricata Mart.
Gall (Fig. 73): on leaf, globoid, brown, hairy, complex, one-chambered. Galler: Cecidomyiinae (Diptera, Cecidomyi-idae). Localities: João Manoel and Sítio Beaches. Occurrence period: May, November, December 2010, January, February and March 2011. Temporal constancy: constant. No previ-ous records from Brazilian restinga areas.
Gall: on leaf, marginal roll, green, hairy, simple, one-chambered. Galler: undeterminated. Localities: João Manoel and Sítio Beaches. Occurrence period: April, May, June, December 2010 and January 2011. Temporal constancy: con-stant. No previous records from Brazilian restinga areas.
Gall (Fig. 74): on stem, globoid, brown, glabrous, com-plex, one-chambered. Galler: Cecidomyiinae (Diptera, Cecidomyiidae). Associated fauna: Olcella sp. (Diptera, Chlo-ropidae) inquiline and Hymenoptera parasitoid. Localities: João Manoel and Sítio Beaches. Occurrence period: April, May, June, July, October, December 2010, January, Febru-ary and March 2011. Temporal constancy: constant. No pre-vious records from Brazilian restinga areas.
Gall (Fig. 75): on stem, globoid with apical spine, green, glabrous, complex, one-chambered. Galler: undeterminated. Localities: João Manoel and Sítio Beaches. Occurrence pe-riod: April, May, June, November, December 2010, January and February 2011. Temporal constancy: constant. No pre-vious records from Brazilian restinga areas.
Sida sp.
Gall (Fig. 76): on stem, fusiform, brown, glabrous, simple, one-chambered. Galler: Cecidomyiinae (Diptera, Cecidomyi-idae). Localities: Kutuca, João Manoel and Sítio Beaches.
Occurrence period: December 2010, January and February 2011. Temporal constancy: accidental.
This is the first record of insect galls in this plant genus.
Melastomataceae
Miconia cinnamomifolia (DC.) Naudin
Gall (Fig. 77): on leaf, globoid, red, glabrous, complex, one-chambered. Galler: undeterminated. Locality: Armação Beach. Occurrence period: August 2010. Temporal constancy: accidental. No previous records from Brazilian restinga ar-eas.
Gall (Fig. 78): on stem, globoid, brown, glabrous, com-plex, one-chambered. Galler: undeterminated. Locality: Armação Beach. Occurrence period: August 2010. Tempo-ral constancy: accidental. No previous records from Brazil-ian restinga areas.
Meliaceae
Guarea guidonia (L.) Sleumer
Gall (Fig. 79): on leaf, globoid, yellow, glabrous, com-plex, one-chambered. Galler: Cecidomyiinae (Diptera, Cecidomyiidae). Associated fauna: Hymenoptera parasitoid. Localities: Suja, Caju, Sítio and Armação Beaches. Occur-rence period: April, June, August, September, October, De-cember 2010, February and March 2011. Temporal constancy: constant.
Gall: on leaf vein, fusiform, green-brown, glabrous, simple, one-chambered. Galler: Cecidomyiinae (Diptera, Cecidomyiidae). Associated fauna: Hymenoptera parasitoid. Locality: Suja Beach. Occurrence period: April and August 2010. Temporal constancy: accidental.
Gall: on stem, fusiform, green-brown, glabrous, simple, one-chambered. Galler: Cecidomyiinae (Diptera, Cecidomyi-idae). Associated fauna: Hymenoptera parasitoid. Locality: Suja Beach. Occurrence period: April 2010. Temporal con-stancy: accidental.
This is the first record of insect galls in this plant species.
Moraceae Ficus sp.
Gall (Fig. 80): on leaf fold, green-red, glabrous, simple, one-chambered. Galler: Thysanoptera. Locality: Suja Beach. Occurrence period: April 2010. Temporal constancy: acci-dental. No previous records from Brazilian restinga areas.
Myrtaceae
Calyptranthes brasiliensis Spreng.
Gall (Fig. 81): on bud, conical, green-brown, glabrous, complex, multi-chambered. Galler: undeterminated. Locality: Armação Beach. Occurrence period: December 2010, Janu-ary and FebruJanu-ary 2011. Temporal constancy: accidental.
189 Insect galls of restinga areas of Ilha da Marambaia, Rio de Janeiro, Brazil
190 Rodrigues et al.
Revista Brasileira de Entomologia 58(2): 173–197, June 2014
Eugenia adstringens Cambess. (= Eugenia rotundifolia
Casar and E. umbelliflora O. Berg)
Gall (Fig. 82): on leaf, marginal roll, green, glabrous, simple, one-chambered. Galler: Dasineura marginalis Maia, 2005 (Diptera, Cecidomyiidae). Associated fauna: Hy-menoptera parasitoid. Locality: Armação Beach. Occurrence period: April, May, July, August, September, October, Novem-ber, December 2010, January, February and March 2011. Tem-poral constancy: constant. Previous records from Brazilian restinga areas: Grumari, Jurubatiba, Carapebus, and Maricá (Oliveira & Maia 2005; Monteiro et al. 2004; Maia 2001).
Gall (Fig. 83): on leaf, lenticular, green, glabrous, simple, one-chambered. Galler: Dasineura globosa Maia, 1995 (Diptera, Cecidomyiidae). Locality: Armação Beach. Occurrence period: May, July, August, September, November, December 2010, January, February and March 2011. Temporal constancy: con-stant. Previous records from Brazilian restinga areas: Bertioga, Grumari, Jurubatiba, Carapebus, and Maricá (Maia et al. 2008; Oliveira & Maia 2005; Monteiro et al. 2004; Maia 2001).
Eugenia copacabanensis Kiaersk.
Gall (Fig. 84): on leaf, spiral, red-green, glabrous, com-plex, one-chambered. Galler: Stephomyia espiralis Maia, 1993 (Diptera, Cecidomyiidae). Associated fauna: Hy-menoptera parasitoid. Locality: Armação Beach. Occurrence period: May 2010. Temporal constancy: accidental. Previ-ous records from Brazilian restinga areas: Jurubatiba, and Maricá (Monteiro et al. 2004; Maia 2001).
Gall: on leaf, lenticular, green, glabrous, simple, one-cham-bered. Galler: undeterminated. Locality: Armação Beach. Occurrence period: May 2010. Temporal constancy: acciden-tal. No previous records from Brazilian restinga areas.
Eugenia punicifolia (Kunt) DC.
Gall (Fig. 85): on leaf, cylindrical, green-red, glabrous, complex, one-chambered. Galler: Stephomyia sp. (Diptera, Cecidomyiidae). Associated fauna: Hymenoptera parasitoid. Localities: Grande, Kutuca, Suja, Caju, João Manoel, Sítio and Armação Beaches. Occurrence period: April 2010 to March 2011. Temporal constancy: constant.
Gall (Fig. 86): on leaf, lenticular, green-red, glabrous, simple, one-chambered. Galler: Cecidomyiinae (Diptera, Cecidomyiidae). Locality: Caju Beach. Occurrence period: August 2010. Temporal constancy: accidental.
Gall (Fig. 87): on stem, fusiform, brown, glabrous, simple, multi-chambered. Galler: Lasiopteridi (Diptera, Cecidomyi-idae). Associated fauna: Hymenoptera parasitoid. Localities: Grande, Kutuca, Suja, Caju, Sítio and Armação Beaches. Occurrence period: April 2010 to February 2011. Temporal constancy: constant.
Gall (Fig. 88): on fruit, globoid, green-red-yellow, gla-brous, simple, multi-chambered. Galler: undeterminated.
Associated fauna: Curculionidae (Coleoptera) inquiline and Hymenoptera parasitoid. Localities: Grande, Suja, Caju, João Manoel, Sítio and Armação Beaches. Occurrence period: September, October and November 2010. Temporal con-stancy: accidental.
This is the first record of insect galls in this plant species.
Eugenia uniflora L.
Gall (Fig. 89): on leaf, lenticular, green-black, glabrous, simple, one-chambered. Galler: Neolasioptera eugeniae Maia, 1993 (Diptera, Cecidomyiidae). Associated fauna: Hymenoptera parasitoid. Localities: Grande, Kutuca, Suja, Caju, João Manoel, Sítio and Armação Beaches. Occurrence period: April 2010 to March 2011. Temporal constancy: con-stant. Previous records from Brazilian restinga areas: Paraty, Cabo Frio, Ilha Grande, Grumari, Jurubatiba, Arraial do Cabo, and Maricá (Maia 2013; Maia & Oliveira 2010; Oliveira & Maia 2005; Monteiro et al. 2004; Maia 2001).
Gall (Fig. 90): on leaf, conical, green-red, glabrous, com-plex, one-chambered. This gall presents variation in shape, being globoid in some samples; and with occurrence of one or two larvae in the internal chamber. Galler: Clinodiplosis
profusa Maia, 2001 (Diptera, Cecidomyiidae). Associated
fauna: Gynaikothrips uzeli (Zimerman, 1909) (Thysanoptera, Phlaeothripidae) inquilines and Hymenoptera parasitoid. Localities: Grande, Kutuca, Suja, Caju, João Manoel and Sítio Beaches. Occurrence period: July 2010 to February 2011. Temporal constancy: constant. Previous records from Bra-zilian restinga areas: Cabo Frio, Grumari, Jurubatiba, Arraial do Cabo, and Maricá (Maia 2013; Oliveira & Maia 2005; Monteiro et al. 2004; Maia 2001).
Gall (Fig. 91): on leaf roll, green, glabrous, simple, one-chambered. Galler: Cecidomyiinae (Diptera, Cecidomyiidae). Locality: Kutuca Beach. Occurrence period: November 2010. Temporal constancy: accidental. No previous records from Brazilian restinga areas.
Gall: on stem, fusiform, brown, glabrous, simple. Galler: undeterminated. Locality: Armação Beach. Occurrence pe-riod: August 2010. Temporal constancy: accidental. Previ-ous records from Brazilian restinga areas: Ilha Grande (Maia & Oliveira 2010).
Myrcia acuminatissima O. Berg.
Gall (Fig. 92): on stem, globoid, brown, glabrous, simple, multi-chambered. Galler: undeterminated. Locality: Kutuca Beach. Occurrence period: October and November 2010. Temporal constancy: accidental.
This is the first record of insect galls in this plant species.
Myrcia splendens (SW.) DC.