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Insect galls of Restinga de Marambaia (Barra de Guaratiba, Rio de Janeiro, RJ)/ Galhas de insetos da Restinga de Marambaia (Barra de Guaratiba, Rio de Janeiro, RJ).

1. Introduction

Insect galls are characterized by abnormal growth of plant tissues and involve cell hypertrophy and/or hyperplasia (Mani, 1964). The galling insects have the ability to manipulate the development of plant tissue and promote its growth (Stone and Schonrogge, 2003) and the development of these structures has been an adaptive strategy of many insects for their food and even protection against predators (Mani, 1964; Stone and Schonrogge, 2003). Therefore, galls are considered the most sophisticated insect-plant interaction (Shorthouse et al., 2005).

In the State of Rio de Janeiro, several insect galls inventories have been published in restinga areas, in the following localities: Arraial do Cabo (APA de Massambaba, Monteiro et al., 1994 and Ilha do Cabo Frio, Maia and Souza, 2013), Jurubatiba (Monteiro et al., 2004), Carapebus and Marica (Maia, 2001), Grumari (Rio de Janeiro) (Oliveira and Maia, 2005), and Reserva Biologica Estadual da Praia do Sul (Ilha Grande, Angra dos Reis) (Maia and Oliveira, 2010). Furthermore, some records of insect galls are known from Parque Municipal da Boca da Barra (Cabo Frio, Rodrigues and Silva, 2011), and Paraty (Fernandes and Maia, 2011). These inventories indicate a great richness of insect galls in this ecosystem. Data on Restinga de Marambaia is still unknown. The objective of this work is to survey and characterize the insect galls of Restinga de Marambaia.

2. Material and Methods

The Restinga de Marambaia (Figure 1) has a total area of 81 [Km.sup.2] and spreads over three municipalities of Rio de Janeiro State: Rio de Janeiro, Itaguai, and Mangaratiba (CGCFN, 2015). It is separated from the continent by the Canal do Bacalhau (Figure 1). It is considered an area of special environmental interest (Rio de Janeiro, 2013), being under the control of the Brazilian Navy and Army. It is included in Atlantic Forest biome, and comprises three ecosystems: mangrove, restinga, and ombrophilous forest (Afonso et al., 2007). According to Koppen classification, the macroclimate is AW (rainy tropical).

[FIGURE 1 OMITTED]

The studied area is situated in the eastern portion of the Restinga da Marambaia, in the municipality of Rio de Janeiro, near Barra de Guaratiba. Twenty four sites were established along the pathway known as "line 1" (23[degrees] 02' 56" S, 43[degrees] 37' 51" W) at every 300 meters, totalizing 6.2 Km of surveyed area. Each site investigated for 30 minutes by two people, monthly, from January to May of 2012, totalizing 120 hours.

According to Afonso et al. (2007) the open shrubby formation of line 1 comprises 48 plant species in 43 genera and 24 families. They indicated the Fabaceae, Myrtaceae, Polygonaceae, Sapindaceae, and Sapotaceae as the richest families in number of species, and Coccoloba Vell. and Eugenia Casar. as the most speciose genera.

All plant organs were examined, except for the subterraneous roots. The plants were identified by the first author. All gall morphotypes were photographed, using a digital camera. Each morphotype was characterized based on shape (according to Isaias et al., 2013), plant organ, color, presence or absence of trichomes, and number of internal chambers. For each gall morphotype, previous records from other restinga inventories are provided.

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

3. Results

A total of 31 insect gall morphotypes and two flower damages were found in 16 families, 22 genera and 24 plant species in this inventory (Figures 2-37). The medium number of gall morphotypes and damages per plant species was 1.3. Three gall morphotypes were collected in magroves and 28 in the sandbank. Eugenia uniflora L. was observed in both ecosystems, hosting different gall morphotypes (conical on mangroves and circular on sandbanks) and, therefore, induced by different species of insects.

Fabaceae and Myrtaceae were the plant families with the greatest richness of gall (4 and 6 morphotypes, respectively), and the greatest number of galled plant species (four and three, respectively) (Table 1 ).

The gall morphotypes characterization is presented in Table 2. About 77% of the galls occurred on leaves. Stem (10%), flower bud (7%), bud (3%) and fruit (3%) galls were also found. All gall morphotypes showed plant organ specifity, excepting the conical galls on Erythroxylum ovalifolium Peyr. (Erythroxylaceae), and the globoid galls on Byrsonima sericea DC. (Malpighiaceae), both occurring on leaves and stems (Table 3).

Besides the galling species, two free-living larvae were found, one on flowers of Asteraceae (not determined species), and the other, Clinodiplosisfloricola Novo-Guedes and Maia, 2008 on bud flowers of Heteropteris nitida Juss (Malpighiaceae).

We observed twelve different gall shapes (Table 4). Among these, the most frequent were discoid (23%), globoid (20%), and conical (16%).

Most galls are glabrous (97%), 87% were one-chambered, and 87% presented the same color of the galled organ, with four exceptions: the leaf galls of Clinodiplosis sp. on Erythroxylum ovalifolium Peyr. (Erythroxylaceae), the bud flower galls on Clitoria laurifolia Poir. (Fabaceae), the leaf galls of Dasineura globosa Maia, 1995 on Eugenia astringens Cambess. (Myrtaceae), and the leaf galls of Contarinia sp. on Ouratea cuspidata (St. Hil) Engl. (Ochnaceae). The galled organs were green, but the galls were light green, brown, yellow, and brown, respectively.

[FIGURES 2-37 OMITTED]

The galls were induced by three insect orders: Diptera (Cecidomyiidae), Hemiptera, and Lepidoptera. Cecidomyiidae (Diptera) were the most frequent gallers, inducing 81% of the morphotypes (Table 5).

4. Discussion

Thirty-one insect gall morphotypes and two flower damages were found in the studied area. Previous inventories in restinga areas of the State of Rio de Janeiro have reported values ranging from 101 (Maia, 2001) to 36 (Maia and Oliveira, 2010), but the sampling methods were not standardized: some restingas were surveyed for 12 months, whereas others for three. In spite of the restinga of Marambaia was surveyed for five months, new gall morphotypes were not found in the last three months, so we believe that the area was sufficiently investigated.

The great difference in the number of gall morphotypes between the two studied ecosystems (mangroove and sandbank) can be explained by the great difference in the diversity of plant species, being sandbanks much richer than mangrooves.

According to previous studies, the medium number of gall morphotypes in restinga areas of the State of Rio varies from 2.1 (Maia, 2001) to 1.5 (Maia and Souza, 2013). The value of the restinga de Marambaia is the lowest one (1.3), what can be related to the low number of botanical species along the investigated area (line 1): 48 species (Afonso et al., 2007).

The majority of the galls were induced by Cecidomyiidae (81%). As the Cecidomyiidae cause about 70% of all described galls in the world, these results were expected. Although galls of Coleoptera, Thysanoptera, and Hymenoptera have been recorded in other Brazilian restinga areas (Maia, 2013), they were not found in the investigated area of the Restinga of Marambaia.

There was a predominance of galls on Fabaceae and Myrtaceae (four and six morphotypes, respectively). Fabaceae and Myrtaceae showed a higher number of species plants with gall (four and three, respectively). Maia (2013) indicated the predominance of galls on Myrtaceae, Asteraceae and Fabaceae for restinga vegetation of the Southeastern region of Brazil, so this survey agreed with the previous data.

The plant genera with the greatest richness of galls were Eugenia L. (Myrtaceae) (n=5), Byrsonima Rich. ex Kunth (Malpighiaceae) (n=3), and Erythroxylum P. Browne (Erythroxylaceae) (n=3). Similar results were found in other restinga areas of the State of Rio de Janeiro, where Eugenia and Erythroxylum (Erythroxylaceae) were pointed out as super host plants (Maia, 2001; Oliveira and Maia, 2005). Although, Byrsonima is cited in this condition for the first time.

Most galls were observed on leaves (77%), a world pattern noted by Mani (1964), and confirmed by Maia (2013) for restinga areas and Goncalves-Alvim and Fernandes (2001) for cerrado vegetation. Maia (2001) argues that the leaves are the most frequently attacked vegetal organ in restingas as they represent a constant and abundant source. The second most attacked plant organ was the stem. Similar results were presented by Goncalves-Alvim and Fernandes (2001).

The plant organ specifity is confirmed, as suggested by Carneiro et al. (2009), as 92% of the gall morphotypes were recorded on a single organ.

The galls were classified into twelve different shapes, being the discoid, globoid and conical the most frequent. One-chambered galls (87%) predominated, as well as glabrous galls (97). In other inventories, globoid, one-chambered, and glabrous galls were also indicated as one of the most common (Maia and Souza, 2013; Malves and Freiro-Costa, 2012; Saito and Urso-Guimaraes, 2012; Bregonci et al., 2010, Santos et al., 2012), suggesting that these are the predominant morphologies of Brazilian galls.

Comparing the richness of each plant species among different restingas of the Southeastern region, we can realize that six botanical species showed the same number of gall morphotypes, 17 presented a smaller number, and three showed new records of gall morphotypes: Norantea brasiliensis Choisy (Marcgraviaceae), Clitoria ternatea L. and Clitoria laurifolia Poir (Fabaceae) (Table 6).

All records presented here are new, as this is the first survey of insect galls in the Restinga of Marambaia (RJ). Furthermore, Norantea brasiliensis Choisy (Marcgraviaceae), Clitoria ternatea L. and Clitoria laurifolia Poir (Fabaceae) are recorded as host plant of insect galls for the first time in restinga inventories.

5. Conclusion

The richness of insect galls in the Restinga de Marambaia was lower when compared to other restinga areas of the southeastern Brazil (Table 7). However, the majority of the host plant species showed similar number of gall morphotypes (Table 6). The Fabaceae and Myrtaceae are the plant families with the greatest number of galls, and Erythroxylum ovalifolium Peyr. (Erytrhoxylaceae) and Eugenia astringens Cambess. (Myrtaceae) are the super-host plant species.

The majority of the gall morphotypes are glabrous, one-chambered, occur on leaves, and present organ specificity.

The guild of galling insects in the Restinga de Marambaia includes only three orders: Diptera, Hemiptera, and Lepidoptera, being less diverse than in most other areas of restinga. The majority of the galls are induced by Cecidomyiidae (Diptera), as in any other place in the world.

All gall records are new for the Restinga de Marambaia, Rio de Janeiro (RJ) and Norantea brasiliensis, Clitoria ternatea, and Clitoria laurifolia are for the first time recorded as host plant species in restinga inventories.

http://dx.doi.org/10.1590/1519-6984.05314

Acknowledgements

We are grateful to Coronel Franco, Head of the Social Communication from CAEx (Army Center Reviews) by support during the field work, to Museu Nacional-UFRJ for logistical support, and to CNPq for financial support.

References

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STONE, G.N. and SCHONROGGE, K., 2003. The adaptive significance of insect gall morphology. Trends in Ecology & Evolution, vol. 18, no. 10, pp. 512-522. http://dx.doi.org/10.1016/ S0169-5347(03)00247-7.

V. C. Maia (a) * and L. O. Silva (a)

(a) Museu Nacional, Quinta da Boa Vista, Sao Cristovao, CEP 20940-040, Rio de Janeiro, RJ, Brazil

* e-mail: maiavcid@acd.ufrj.br

Received: April 16, 2015--Accepted: May 21, 2015--Distributed: August 31, 2016 (With 37 figures)
Table 1. Distribution of the number of morphotypes of insect
galls and damages per host plant and ecosystem in the Restinga
de Marambaia (Barra de Guaratiba, Rio de Janeiro, RJ).

Plant family       Plant species                    Number of galls
                                                       and damage
Acanthaceae        Avicennia schaueriana Stapf             1
                   and Leechm. ex Moldenke

Anacardiaceae      Anacardium occidentale L.               1
                   Schinus terebinthifolius                1
                   Raddi.

Apocynaceae        Aspidosperma pyricollum M.              1
                   Arg.

Asteraceae         Not determined                          1

Bignoniaceae       Fridericia conjugata (Vell.)            2
                   Mart.

Celastraceae       Maytenus obtusifolia Mart.              1

Convolvulaceae     Jacquemontia holosericea                1
                   (Weinm.) O'Donell.

Erythroxylaceae    Erythroxylum ovalifolium Peyr.          3

Fabaceae           Clitoria laurifolia Poir.               1
                   Clitoria ternatea L. Dalbergia          1
                   ecastophylla L. Taub Inga               1
                   maritima Benth.                         1

Malpighiaceae      Byrsonima sericea DC.                   3
                   Heteropterys nitida Juss.               1

Marcgraviaceae     Norantea brasiliensis Choisy.           1

Myrtaceae          Eugenia astringens Cambess.             3
                   Eugenia uniflora L.                     2

                   Neomitranthes obscura (DC) N.           1
                   Silveira

Nyctaginaceae      Guapira opposita (Vell.)                2
                   Reitz.

Ochnaceae          Ouratea cuspidata (St. Hil)             1
                   Engl.

Sapotaceae         Manilkara subsericea (Mart.)            1
                   Dubard. Pouteria venosa                 1
                   (Mart.) Baehni.

Smilacaceae        Smilax rufescens Griseb                 1

Plant family       Plant species                     Ecosystem

Acanthaceae        Avicennia schaueriana Stapf        Mangrove
                   and Leechm. ex Moldenke

Anacardiaceae      Anacardium occidentale L.          Restinga
                   Schinus terebinthifolius           Restinga
                   Raddi.

Apocynaceae        Aspidosperma pyricollum M.         Restinga
                   Arg.

Asteraceae         Not determined                     Mangrove

Bignoniaceae       Fridericia conjugata (Vell.)       Restinga
                   Mart.

Celastraceae       Maytenus obtusifolia Mart.         Restinga

Convolvulaceae     Jacquemontia holosericea           Restinga
                   (Weinm.) O'Donell.

Erythroxylaceae    Erythroxylum ovalifolium Peyr.     Restinga

Fabaceae           Clitoria laurifolia Poir.          Restinga
                   Clitoria ternatea L. Dalbergia     Restinga
                   ecastophylla L. Taub Inga          Mangrove
                   maritima Benth.                    Restinga

Malpighiaceae      Byrsonima sericea DC.              Restinga
                   Heteropterys nitida Juss.          Restinga

Marcgraviaceae     Norantea brasiliensis Choisy.      Restinga

Myrtaceae          Eugenia astringens Cambess.        Restinga
                   Eugenia uniflora L.              Mangrove and
                                                      Restinga
                   Neomitranthes obscura (DC) N.      Restinga
                   Silveira

Nyctaginaceae      Guapira opposita (Vell.)           Restinga
                   Reitz.

Ochnaceae          Ouratea cuspidata (St. Hil)        Restinga
                   Engl.

Sapotaceae         Manilkara subsericea (Mart.)       Restinga
                   Dubard. Pouteria venosa            Restinga
                   (Mart.) Baehni.

Smilacaceae        Smilax rufescens Griseb            Restinga

Table 2. Characterization of insect galls of the Restinga of
Marambaia (Barra de Guaratiba, Rio de Janeiro, RJ).

                                     Gall color /
Plant species          Gall shape     Plant organ    Trichomes

A. schaueriana        Intralaminar   Green / Leaf     Absent
                        globoid

A. occidentale          Discoid      Green / Leaf     Absent

S. terebinthifolius     Fusiform        Brown /       Absent
                                         Stem

A. pyricollum           Discoid      Green / Leaf     Absent

Asteraceae             Free larva      - / Fower         -

F. conjugata            Conical      Green / Leaf     Absent

                        Globoid      Green / Fruit    Absent

M. obtusifolia        Intralaminar   Green / Leaf     Absent
                       lenticular

J. holosericea          Globoid       Green / Bud     Absent
                        discrete        flower

E. ovalifolium          Conical      Green / Leaf     Absent

                        Marginal     Light green /    Absent
                       Leaf roll         Leaf

                        Conical       Brown / Bud     Absent

C. laurifolia           Conical       Brown / Bud     Present
                                        flower

C. ternatea             Globoid      Green / Leaf     Absent

D. ecastophylla         Discoid      Green / Leaf     Absent

I. maritima              Pocket      Green / Leaf     Absent
                         shaped

B. sericea              Discoid        Green or       Absent
                                     yellow / Leaf

                        Globoid         Brown /       Absent
                                         Stem

                        Globoid      Green / Leaf     Absent

H. nitida              Free larva       - / Bud
                                        flower

N. brasiliensis       Intralaminar   Green / Leaf     Absent
                       lenticular

E. astringens           Clavate      Green / Leaf     Absent

                                       Yellow /
                        Globoid          Leaf         Absent

                        Marginal     Green / Leaf     Absent
                       Leaf roll

E. uniflora             Conical      Green / Leaf     Absent

                        Circular     Green / Leaf     Absent

N. obscura              Marginal     Green / Leaf     Absent
                       Leaf roll

G. opposita           Intralaminar   Green / Leaf     Absent
                       lenticular

                                        Brown /
                        Globoid          Stem         Absent

                      Cylindrical
O. cuspidata          with apical    Brown / Leaf     Absent
                       projection

M. subsericea           Discoid      Green / Leaf     Absent

P. venosa               Discoid      Green / Leaf     Absent

S. rufescens            Discoid      Green / Leaf     Absent

                                      Number
Plant species          Gall shape    internal          Galler
                                     chamber

A. schaueriana        Intralaminar      1       Cecidomyiidae
                        globoid

A. occidentale          Discoid         1       Cecidomyiidae

S. terebinthifolius     Fusiform        1       Lepidoptera

A. pyricollum           Discoid         1       Psyllidae
                                                (Hemiptera)

Asteraceae             Free larva       -       Not determined

                                                Arrabidaeamyia
F. conjugata            Conical         1       serrata Maia, 2001
                                                Cecidomyiidae

                        Globoid      Several    Neolasioptera sp.
                                                Cecidomyiidae

                                                Mayteniella
M. obtusifolia        Intralaminar      1       distincta Maia, 2001
                       lenticular               Cecidomyiidae

                                                Schizomyia santosi
J. holosericea          Globoid         1       Maia and Araujo,
                        discrete                2009 Cecidomyiidae

                                                Dasineura
E. ovalifolium          Conical         1       ovalifoliae Maia
                                                and Fernandes, 2011
                                                Cecidomyiidae

                        Marginal        1       Clinodiplosis sp.
                       Leaf roll                Cecidomyiidae

                                                Lopesia erythroxyli
                        Conical         1       Rodrigues and Maia
                                                (2010)

C. laurifolia           Conical         1       Not determined

C. ternatea             Globoid         1       Not determined

                                                Lopesia grandis
D. ecastophylla         Discoid         1       Maia, 2001a
                                                Cecidomyiidae

                                                Neolasioptera
I. maritima              Pocket         1       ingae Mohn, 1964a
                         shaped                 Cecidomyiidae

                                                Dasineura
B. sericea              Discoid         1       byrsonimae Maia,
                                                2010 Cecidomyiidae

                                                Bruggmanniella
                        Globoid      Several    byrsonimae Maia
                                                and Couri, 1992
                                                Cecidomyiidae

                        Globoid         1       Lepidoptera

                                                Clinodiplosis
H. nitida              Free larva               floricola Novo-
                                                Guedes and Maia,
                                                2008 Cecidomyiidae

N. brasiliensis       Intralaminar      1       Not determined
                       lenticular

                                                Stephomyia clavata
E. astringens           Clavate         1       Tavares, 1920
                                                Cecidomyiidae

                                                Dasineura globosa
                        Globoid         1       Maia, 1995
                                                Cecidomyiidae

                                                Dasineura
                        Marginal        1       marginalis
                       Leaf roll                Maia, 2005a
                                                Cecidomyiidae

                                                Clinodiplosis
E. uniflora             Conical         1       profusa Maia, 2001a
                                                Cecidomyiidae

                                                Neolasioptera
                        Circular        1       eugeniae Maia, 1993
                                                Cecidomyiidae

N. obscura              Marginal        1       Clinodiplosis sp.
                       Leaf roll                Cecidomyiidae

                                                Bruggmannia
G. opposita           Intralaminar      1       elongata Maia
                       lenticular               and Couri, 1993
                                                Cecidomyiidae

                                                Proasphondylia
                        Globoid      Several    guapirae
                                                Maia, 1994a
                                                Cecidomyiidae

                      Cylindrical
O. cuspidata          with apical       1       Contarinia sp.
                       projection               Cecidomyiidae

                                                Manilkaramyia
M. subsericea           Discoid        1-2      notabilis Maia, 2001
                                                Cecidomyiidae

                                                Lopesia singularis
P. venosa               Discoid         1       Maia, 2001
                                                Cecidomyiidae

                                                Smilasioptera
S. rufescens            Discoid         1       candelariae Mohn,
                                                1975 Cecidomyiidae

                                     Previous
Plant species          Gall shape    records

A. schaueriana        Intralaminar   BER and
                        globoid      CF

A. occidentale          Discoid      AMA

S. terebinthifolius     Fusiform     BER, GRU
                                     and CF

A. pyricollum           Discoid      IG and
                                     MAR

Asteraceae             Free larva    -

                                     GRU,
F. conjugata            Conical      MAR, AC,
                                     CAR and
                                     JU

                        Globoid      GRU, AR,
                                     CAR and
                                     JU

                                     GRU,
M. obtusifolia        Intralaminar   MAR and
                       lenticular    AC

J. holosericea          Globoid      MAR
                        discrete

                                     GRU
E. ovalifolium          Conical      MAR, CAR
                                     and JU

                        Marginal     IG, MAR,
                       Leaf roll     CAR and
                                     JU

                                     IG, GRU,
                        Conical      MAR, AC,
                                     CAR and
                                     JU

C. laurifolia           Conical      -

C. ternatea             Globoid      -

                                     IG, MAR,
D. ecastophylla         Discoid      CAR and
                                     JU

I. maritima              Pocket      GRU and
                         shaped      MAR

                                     IG, GRU
B. sericea              Discoid      MAR,
                                     CAR, JU
                                     and GUA

                        Globoid      MAR, CAR
                                     and JU

                        Globoid      MAR and AC

H. nitida              Free larva    MAR

N. brasiliensis       Intralaminar   -
                       lenticular

E. astringens           Clavate      CAR and
                                     JU

                                     GRU,
                        Globoid      MAR, CAR
                                     and JU

                                     GRU,
                        Marginal     MAR, AC,
                       Leaf roll     CAR and
                                     JU

                                     GRU,
E. uniflora             Conical      MAR, AC,
                                     CF, CAR
                                     and JU

                                     PA, IG,
                                     GRU,
                        Circular     MAR, CF
                                     and AC

N. obscura              Marginal     MAR,
                       Leaf roll     CAR, JU
                                     and GUA

                                     BER, IG,
G. opposita           Intralaminar   MAR, AC,
                       lenticular    CAR and
                                     JU

                                     BER, IG,
                        Globoid      MAR, CAR
                                     and JU

                      Cylindrical    IG, GRU,
O. cuspidata          with apical    MAR, JU
                       projection    and GUA

                                     CAR, JU
M. subsericea           Discoid      and GUA

                                     BER, MAR
P. venosa               Discoid      and AC

                                     GRU,
S. rufescens            Discoid      MAR, CAR
                                     and JU

AC = Arraial do Cabo (RJ) (Monteiro et al., 1994); BER = Bertioga
(SP) (Maia et al., 2008); CAR = Carapebus (RJ) (Maia, 2001); CF =
Cabo Frio (RJ) (Rodrigues and Silva, 2011; Maia and Souza, 2013);
GRU = Grumari (RJ) (Oliveira and Maia, 2005); GUA = Guarapari
(ES) (Bregonci et al., 2010); IG = Ilha Grande (RJ) (Maia and
Oliveira, 2010); JU = Jurubatiba (RJ); MAR = Marica (RJ) (Maia,
2001); PA = Paraty (RJ) (Fernandes and Maia, 2011).

Table 3. Number of insect galls by galled plant organ in the
Restinga of Marambaia (Barra de Guaratiba, Rio de Janeiro, RJ).

Plant organ       Number of gall morphotypes
                            (N=31)
Leaf          24 ([approximately equal to] 77%)
Stem           3 ([approximately equal to] 10%)
Bud flower     2 ([approximately equal to] 7%)
Bud            1 ([approximately equal to] 3%)
Fruit          1 ([approximately equal to] 3%)

Table 4. Number of insect galls by gall shape in the Restinga of
Marambaia (Barra de Guaratiba, Rio de Janeiro, RJ).

Gall shape                   Number of gall morphotypes
                                       (N=31)

Discoid                   7 ([approximately equal to] 23%)
Globoid                   6 ([approximately equal to] 20%)
Conical                   5 ([approximately equal to] 16%)
Marginal leaf roll        3 ([approximately equal to] 10%)
Intralaminar lenticular   3 ([approximately equal to] 10%)
Fusiform                   1 ([approximately equal to] 3%)
Intralaminar globoid       1 ([approximately equal to] 3%)
Circular                   1 ([approximately equal to] 3%)
Clavate                    1 ([approximately equal to] 3%)
Pocket shaped              1 ([approximately equal to] 3%)
Globoid discrete           1 ([approximately equal to] 3%)
Cylindrical with apical    1 ([approximately equal to] 3%)
projection

Table 5. Number of insect galls by galling insect in the Restinga
of Marambaia (Barra de Guaratiba, Rio de Janeiro, RJ).

Galling insect                      Number of gall
                                  morphotypes (N=31)

Diptera (Cecidomyiidae)   25 ([approximately equal to] 81%)
Not determined             3 ([approximately equal to] 10%)
Lepidoptera                2 ([approximately equal to] 6%)
Hemiptera                  1 ([approximately equal to] 3%)

Table 6. Distribution of the total number of morphotypes
of insect galls in restinga areas of the Southeastern region
and number of morphotypes recorded from the Restinga de
Marambaia), Rio de Janeiro, RJ.

                            Total        Number of
                          number of     morphotypes
Host-plant               morphotypes    reported to
                          of insects    Restinga de
                            galls        Marambaia
Anacardium                    01            01
occidentale
Aspidosperma                  01            01
pyricollum
Byrsonima sericea             04            03
Clitoria laurifolia           0             01
Clitoria ternatea             0             01
Dalbergia                     01            01
ecastophylla
Erythroxylum                  05            03
ovalifolium
Eugenia astringens            07            03
Eugenia uniflora              06            02
Heteropteris nitida           03            01
Fridericia conjugata          03            02
Guapira opposita              10            02
Inga maritima                 01            01
Jacquemontia                  01            01
holosericea
Manilkara subsericea          07            01
Maytenus obtusifolia          02            01
Neomitranthes                 06            01
obscura
Norantea brasiliensis         0             01
Ouratea cuspidata             03            01
Pouteria venosa               01            01
Schinnus                      02            01
terebinthifolius
Smilax rufescens              06            01

Table 7. Distribution of the number of morphotypes of insect
galls in restinga areas of the Southeastern region of Brazil.
Restinga de Marambaia, Barra de Guaratiba, Rio de Janeiro (RJ).

Localities                    Number of gall
                               morphotypes

Bertioga, SP                       233
Marica, RJ                          72
Carapebus, RJ                       62
Grumari, RJ                         43
Arraial do Cabo, RJ                 41
PEPCV, ES                           38
RBEPS, RJ                           36
Restinga de Marambaia, RJ           31
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Title Annotation:Original Article
Author:Maia, V.C.; Silva, L.O.
Publication:Brazilian Journal of Biology
Article Type:Report
Date:Jul 1, 2016
Words:4309
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