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).
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).
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).
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.
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.
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.
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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: firstname.lastname@example.org
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|
|Date:||Jul 1, 2016|
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