Insect galls of Restinga de Marambaia ( Barra de Guaratiba , Rio de Janeiro , RJ )

Thirty-one morphotypes of insect galls and two flower damages were found on 16 families, 22 genera and 24 plant species in Restinga de Marambaia (Barra de Guaratiba, Rio de Janeiro, RJ). Fabaceae and Myrtaceae were the plant families with the greatest richness of insect galls (4 and 6 morphotypes, respectively), and the greatest number of galled plants (four and three species, respectively). Galls were mostly found on leaves and stems (77% and 10%, respectively). The galling insects are represented by Diptera, Lepidoptera, and Hemiptera. The majority of the galls (81%) were induced by gall midges (Cecidomyiidae: Diptera).


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 Schönrogge, 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 Schönrogge, 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 andIlha do Cabo Frio, Maia andSouza, 2013), Jurubatiba (Monteiro et al., 2004), Carapebus and Maricá (Maia, 2001), Grumari (Rio de Janeiro) (Oliveira and Maia, 2005), and Reserva Biológica 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.

Material and Methods
The Restinga de Marambaia (Figure 1) has a total area of 81 Km 2 and spreads over three municipalities of Rio de Janeiro State: Rio de Janeiro, Itaguaí, 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 Köppen classification, the macroclimate is AW (rainy tropical).
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° 02' 56" S, 43° 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 (Gagné, 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).

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

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
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 Gonçalves-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 Gonçalves-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.
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.

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.

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).

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

species Gall shape Gall color / Plant organ Trichomes Number internal chamber Galler Previous records
AC = Arraial do Cabo (RJ)

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

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

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

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).

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.