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Papéis Avulsos de Zoologia

versión impresa ISSN 0031-1049versión On-line ISSN 1807-0205

Pap. Avulsos Zool. vol.58  São Paulo  2018  Epub 10-Jul-2018

http://dx.doi.org/10.11606/1807-0205/2018.58.24 

Articles

Insect galls of the Floresta da Cicuta (Volta Redonda, RJ, Brazil)

Ismael Cividini Flor1 
http://orcid.org/0000-0002-5173-4210

Jandira Chachá Ribeiro Flor2 

Paulo Sérgio do Nascimento Furtado3 

1Universidade Federal do Rio de Janeiro (UFRJ), Museu Nacional, Departamento de Entomologia. Rio de Janeiro, RJ, Brasil. E-mail: ismaelcflor@gmail.com

2Centro Universitário de Barra Mansa (UBM), Curso de Biologia. Barra Mansa, RJ, Brasil. E-mail: jandirachacha@gmail.com

3Universidade Federal do Rio de Janeiro (UFRJ), Centro de Educação a Distância do Estado do Rio de Janeiro (CEDERJ), Curso de Biologia. Volta Redonda, RJ, Brasil. E-mail: psnascimentofurtado@gmail.com

Abstract

Insect galls of the Floresta da Cicuta (Volta Redonda, RJ, Brazil). Galls are changes in the pattern of growth and development of plant tissues or organs in response to the action of an inducing organism, usually an insect. The goal of the present study was to inventory the insect galls of the Floresta da Cicuta (Volta Redonda, RJ, Brazil). The collections were carried out along all the trails, totaling 16 hours of sampling. Forty-three morphotypes of insect galls were found in 24 plant species (18 genera and 15 families). Sapindaceae and Euphorbiaceae were the most richness host plant families. Six new records of host plant species are presented: Senefeldera verticillata (Vell.) Croizat. (Euphorbiaceae), Inga acuminata (Fabaceae), Ocotea elegans (Lauraceae), Ouratea stipulata (Ochnaceae), Psychotria nuda (Rubiaceae) and Cestrum intermedium (Solanaceae). Most of the galls occurred on leaves (n = 21) and stems (n = 18), followed by buds (n = 2), two gall morphotypes occurred simultaneously on leaves and stems. One-chambered galls were more frequent (n = 31), as well as glabrous galls (n = 33). The gallers belong to three insect orders: Diptera (Cecidomyiidae), Hemiptera, and Lepidoptera. The associated fauna comprised parasitoids (Hymenoptera), inquilines (Hemiptera and Coleoptera) and successors (Isoptera and Acari).

Key-Words. Galling species; Host plant; Cecidomyiidae

INTRODUCTION

Insect galls are pathological structures that originating new formations in the plant tissues, as a result of mechanical and/or chemical stimulation of insects (Bronner, 1992). According to Mani (1964), galls are induced in any part of the plant, both in vegetative organs or reproductive organs, providing food and shelter for the larva until its adult stage. Although the entomogenous galls occur in any part of the plants, they are most common on leaves and branches (Fernandes et al., 1988).

Studies about insect galls and gallers have been performed in different plant species, mainly related to Cecidomyiidae (Diptera), the most important galling taxon. These studies cover aspects such as the description of new species (Maia, 1996a; Maia, 1996b); associations with parasitoids (Maia & Monteiro, 1999; Maia & Tavares, 2000); description of developmental stages (Maia, 1993) and patterns that influence the diversity of galls (Fernandes & Price, 1988; Fernandes et al., 1996; Fernandes et al., 1997a). However, other studies have focused on the description and characterization of galls from different localities (Fernandes et al., 1988; Fernandes et al., 1997b; Maia, 2001; Maia & Fernandes, 2004; Urso-Guimarães et al., 2003; Urso-Guimarães & Scareli-Santos, 2006).

The most investigated Brazilian ecosystems in relation to composition of the Cecidomyiidae fauna and diversity of galling insects are the Cerrado and the Atlantic Forest, but these studies still represent a small fraction of the total area of these biomes (Rodrigues et al., 2014).

In the Southeast Region, insect galls inventories were carried out in restinga areas of the states of Espírito Santo (Parque Estadual Paulo César Vinha, Guarapari - Bregonci et al., 2010), São Paulo (Bertioga - Maia et al., 2008) and Rio de Janeiro, Ilha da Marambaia (Mangaratiba - Rodrigues et al., 2014), Marambaia (Maia & Silva, 2016), Parque Estadual da Costa do Sol Região (Região dos Lagos - Carvalho-Fernandes et al., 2016), and Reserva Particular do Patrimônio Natural Fazenda Caruara (São João da Barra - Carvalho-Fernandes et al., 2016).

The other physiognomies have been under studied as dry seasonal forest (Ilha do Cabo Frio, Arraial do Cabo, RJ - Maia & Souza, 2013), tableland forest (São Francisco de Itabapoana, RJ - Maia & Carvalho-Fernandes, 2016), altitudinal fields (Itamonte, MG - Maia, 2014) and ombrophilous forest (Santa Teresa, ES - Maia et al., 2014), all with a single inventory.

According to IBGE (1992), Floresta da Cicuta is classified as Semidecidual Seasonal Forest. Surveys of galls in this physiognomy are still scarce, according to the literature the following locations were investigated in Brazil: Goiânia, GO - Santos et al., 2010; Ilha do Cabo Frio, Arraial do Cabo, RJ - Maia & Souza, 2013; Telêmaco Borba, PR - Santos & Ribeiro, 2015; Maringá, PR - Carvalho et al., 2015; Bodoquena, MS - Urso-Guimarães et al., 2016.

In this context, the goal of the present study was to inventory the insect galls of the Area of Relevant Ecological Interest Floresta da Cicuta (Volta Redonda, RJ), contributing to the knowledge of the gall richness in semidecidual seasonal forest and in the State of Rio de Janeiro.

MATERIAL AND METHODS

Study area

The Floresta da Cicuta (22°33’20”S, 44°05’00”W) covers the municipalities of Volta Redonda and Barra Mansa. It is located in the south region of the State of Rio de Janeiro and has approximately 131,28 ha (Fig. 1A). It is a conservation unity area protected by Decree No. 90792 of January 9, 1985, framing on the Relevant Ecological Interest Area category (ARIE) (IBGE, 1992). According to Costa (2004), the Floresta da Cicuta is the last intact remaining Atlantic Forest in the Paraíba do Sul Valley (Fig. 1B). The climate is mesothermal - Cwa of Koppen - with dry winter and hot and rainy summer.

Figure 1 (A-B) Location of the Area of Relevant Ecological Interest Floresta da Cicuta (Volta Redonda, RJ, Brazil). (C) Aerial view of Floresta da Cicuta. (D) View of Trilha Principal where the collection of insect galls were carried out. 

Sampling

The collections were held in April and June 2015, along the trails: Trilha Principal (22°33’01.01”S, 44°05’23.88”W), Trilha da Velha (22°33’09.72”S, 44°05’20.03”W) and Trilha da Figueira (22°32’52.90”S, 44°05’16.61”W) of the Floresta da Cicuta, totaling 16 hours of sampling (Fig. 1C). All morphotypes were photographed in the field and characterized by shape (Isaias et al., 2013), color, host plant organ, indumentum, grouped or isolated occurrence, and number of internal chambers. Samples of each morphotype were dissected under stereomicroscope for observing the number of internal chambers and obtaining immature insects. Other samples were placed separately in plastic pots, sealed, labeled, lined with moistened paper and inspected daily to check the emergence of adults. All insects obtained were preserved in 70% alcohol. The cecidomyiids were mounted on microscope slides, following the methodology adopted by Gagné (1994).

Samples of the host plants were pressed and sent to the Jardim Botânico, RJ, experts, to identify at the lowest possible taxonomic level, according to APG III (2009). All botanic names were updated based on the Lista de Espécies da Flora do Brasil (2020), and each species was classified as native or endemic of Brazil based on the same site.

RESULTS

In the Floresta da Cicuta were found 43 gall morphotypes associated with 24 species of plants, distributed in at least 15 families and 18 genera (Figs. 2-4). The average number of gall morphotypes for host plant species was 1.79. Sapindaceae and Euphorbiaceae presented the greatest number of gall morphotypes (Table 1). The super host genera were Allophylus (with six gall morphotypes) and Croton (with five).

Figure 2 Insect galls of the Area of Relevant Ecological Interest Floresta da Cicuta (Volta Redonda, RJ, Brazil). (A-B) Asteraceae: (A) Chromolaena sp., leaf gall, (B) Vernonia sp., stem gall, (C) Berberidaceae: Berberis sp., stem gall. (D-F) Bignoniaceae: (D) Adenocalymma comosum, leaf/stem gall, (E) sp.1, stem gall, (F) sp.2, leaf gall. (G-H) Elaeocarpaceae: Sloanea guianensis, (G) leaf roll gall, (H) leaf parenchymal gall. (I-M) Euphorbiaceae: Croton sp. (I) leaf gall, (J) leaf gall, (K) leaf gall (L) leaf gall, (M) Senefeldera verticillata, leaf gall. Fabaceae: (N) Inga acuminate, bud gall, (O) Mimosa sp., stem gall, (P) sp.1, leaf gall. 

Figure 3 Insect galls of the Area of Relevant Ecological Interest Floresta da Cicuta (Volta Redonda, RJ, Brazil). (A) Lauraceae: Ocotea elegans, stem gall. (B-D) Malvaceae: Guazuma ulmifolia, (B) stem gall, (C) leaf gall, (D) Guazuma sp., leaf gall. (E) Ochnaceae: Ouratea stipulata, leaf gall. (F) Piperaceae: Piper amalago, leaf gall. (G) Proteaceae: Roupala montana var. brasiliensis, leaf/stem gall. (H) Rubiaceae: Psychotria nuda, leaf gall. (I) Sabiaceae: Meliosma sellowii, stem gall. 

Figure 4 Insect galls of the Area of Relevant Ecological Interest Floresta da Cicuta (Volta Redonda, RJ, Brazil). (A) Sapindaceae: Allophylus edulis, stem gall. Solanaceae: (B) Cestrum intermedium, leaf gall. (C) Cestrum sp., stem gall. (D-M) Not identified: (D) leaf gall, (E) stem gall, (F) stem gall, (G) leaf gall, (H) stem gall, (I) bud gall, (J) stem gall, (K) stem gall, (L) leaf gall (M) leaf gall. 

Table 1 Richness of gall morphotypes by plant families and host plant species in the Area of Relevant Ecological Interest Floresta da Cicuta (Volta Redonda, RJ, Brazil). 

Families Host plant Galls
Richness % Richness %
Asteraceae 2 5.9 2 4.7
Berberidaceae 1 2.9 1 2.3
Bignoniaceae 3 8.8 3 7
Elaeocarpaceae 2 5.9 2 4.7
Euphorbiaceae 2 5.9 5 11.6
Fabaceae 3 8.8 3 7
Lauraceae 1 2.9 1 2.3
Malvaceae 2 5.9 3 7
Ochnaceae 1 2.9 1 2.3
Piperaceae 1 2.9 1 2.3
Proteaceae 1 2.9 1 2.3
Rubiaceae 1 2.9 1 2.3
Sabiaceae 1 2.9 1 2.3
Sapindaceae 1 2.9 6 14
Solanaceae 2 5.9 2 4.7
Not determined 10 29.4 10 23.3
Total 34 100 43 100

Among the host plants, six are endemic of Brazil: Adenocalymma comosum (Cham.) DC., Senefeldera verticillata (Vell.) Croizat., Ocotea elegans Mez., Ouratea stipulata (Vell.) Sastre, Psychotria nuda (Cham. & Schltdl.) Wawra, and Meliosma sellowi Urb. The others are native. No exotic host plant species was found in the Floresta da Cicuta. As the gallers are species-specific and monophagous, these five morphotypes can be considered as endemic too (Flora do Brasil, 2020).

Most galls were induced on leaves (n = 21), stems (n = 18), buds (n = 2) and two morphotypes occurred both on leaves and stems. Eight different gall shapes were found in this study the most common were fusiform (44%) and globoid (30%) (Table 2). The morphotypes were green (n = 21), brown (n = 21) and white (n = 1). In relation to the indumentum and internal chambers, most galls were glabrous (n = 33) and one-chambered (n = 31).

Table 2 Number of gall morphotypes of different shapes in the Area of Relevant Ecological Interest Floresta da Cicuta (Volta Redonda, RJ, Brazil). 

Shapes Number of gall morphotypes %
Fusiform 19 44
Globoid 13 30
Midvein swelling 3 7
Discoid 3 7
Conical 2 5
Spheroid 1 2
Leaf roll 1 2
Circular 1 2

The gallers of ten morphotypes were determined. They belong to three insect orders: Diptera (Cecidomyiidae), Hemiptera, and Lepidoptera. The former mentioned was the most frequent galling taxa, being responsible for eight morphotypes, followed by Hemiptera, and Lepidoptera both with one. The gallers of 33 morphotypes cannot be determined, because the galls were already empty when collected or occupied by two or more different dwellers and their food habit could not be determined. Three galling insects were identified at tribe level: Lopesiini sp.1 (Diptera, Cecidomyiidae) on Bignoniaceae, Lopesiini sp.2 on Guazuma ulmifolia Lam. (Malvaceae) and Alycaulini sp. on an undetermined host plant species.

The associated fauna comprised parasitoids, inquilines and successors. This fauna was found in seven, two and two of galls morphotypes, respectively. Parasitoids, represented by Hymenoptera, were found in galls on Bignoniaceae, Euphorbiaceae, Sapindaceae, Solanaceae and an unidentified plant. Inquilines represented by Hemiptera and Coleoptera, were obtained from galls on two unidentified plants. Successors represented by Isoptera and mites (Acari) were observed on Senefeldera verticillata (Euphorbiaceae) and Bignoniaceae, respectively. This is the first record of Isoptera as successors in insect galls (Table 3).

Table 3 Arthropod fauna associated with insect galls in the Area of Relevant Ecological Interest Floresta da Cicuta (Volta Redonda, RJ, Brazil). 

Host Plan Gall morphotype Associated fauna Guild
Adenocalymma comosum Leaf/stem gall, fusiform, brown, glabrous and one-chambered Acari Successor
Bignoniaceae Stem gall, fusiform, brown, glabrous and multi-chambered Hymenoptera Parasitoid
Croton sp. Leaf gall, globoid, green, glabrous and one-chambered Hymenoptera Parasitoid
Allophylus edulis Stem gall, fusiform, brown, hairy and one-chambered Pteromalidae, Hymenoptera Parasitoid
Stem gall, fusiform, green, glabrous and one-chambered Hymenoptera Parasitoid
Stem gall, globoid, brown, hairy and multi-chambered Hymenoptera Parasitoid
Cestrum sp. Stem gall, globoid, green, glabrous and multi-chambered Hymenoptera Parasitoid
Senefeldera verticillata Leaf gall, globoid, green, glabrous and one-chambered Isoptera Successor
Not identified Leaf gall, midvein swelling, green, glabrous and one-chambered Hemiptera Inquiline
Not identified Stem gall, fusiform, brown, glabrous and multi-chambered Coleoptera Inquiline
Not identified Leaf gall, globoid, green, hairy and one-chambered Hymenoptera Parasitoid

Data on insect galls are presented here under host plant families, genera and species in alphabetical order. They include gall morphological characterization, associated fauna and previous records in Brazil.

Asteraceae

Chromolaena sp. (native genus)

Leaf gall, conical, green, hairy and one-chambered (Fig. 2A).

Previous records: Galls on Chromolaena spp. were recorded in Pará.

Galler: Clinodiplosis eupatorii Felt, 1911 (Toma & Maia, 2012).

Vernonia sp. (native genus)

Stem gall, fusiform, brown, glabrous and one-chambered (Fig. 2B).

Previous records: Galls on Vernonia spp. were recorded in Rio Grande do Sul state (Mendonça et al., 2014), Bertioga (SP) (Maia et al., 2008), Carapebus and Jurubatiba (RJ) (Monteiro et al., 2004), Belo Horizonte (MG) (Fernandes et al., 1988), Santa Teresa, (ES) (Maia et al., 2014), Serra de São José (MG) (Maia & Fernandes, 2004), Tiradentes (MG) (Maia, 2014), Vale do Jequitinhonha (MG) (Fernandes et al., 1997b).

Berberidaceae

Berberis sp.

Stem gall, fusiform, brown, glabrous and one-chambered (Fig. 2C).

Previous records: Galls on Berberis spp. were recorded in Rio Grande do Sul state (Mendonça et al., 2014).

Bignoniaceae

Adenocalymma comosum (Cham.) DC. (endemic species)

Leaf/stem gall, fusiform, brown, glabrous and one-chambered (Fig. 2D).

Previous records: Galls on A. comosum were recorded in Ilha da Marambaia (RJ) (Rodrigues et al., 2014).

Associated fauna: Acari (successor).

Bignoniaceae sp.1

Stem gall, fusiform, brown, glabrous and multi-chambered (Fig. 2E).

Associated fauna: Hymenoptera (parasitoid).

Bignoniaceae sp.2

Leaf gall, globoid, brown, hairy and one-chambered (Fig. 2F).

Galler: Lopesiini (Cecidomyiidae).

Elaeocarpaceae

Sloanea guianensis (Aubl.) Benth.

Leaf gall, roll, green, glabrous, and multi-chambered (Fig. 2G).

Previous records: The same gall has been recorded in Bertioga (SP) (Maia et al., 2008).

Galler: Clinodiplosis sp. (Cecidomyiidae).

Leaf gall, discoid, green, glabrous and one-chambered (Fig. 2H).

Previous records: The same gall has been recorded in Bertioga (SP) (Maia et al., 2008).

Galler: Lasiopteridi (Cecidomyiidae).

Euphorbiaceae

Croton sp.

Leaf gall, globoid, green, glabrous and one-chambered (Fig. 2I).

Galler: Cecidomyiidae.

Associated fauna: Hymenoptera (parasitoid).

Leaf gall, spheroid, white, hairy and one-chambered (Fig. 2J).

Galler: Cecidomyiidae.

Previous records: The same gall has been recorded on Croton floribundus in Tiradentes (MG) (Maia & Fernandes, 2004).

Galler: Clinodiplosis sp. (Cecidomyiidae).

Associated fauna: Hymenoptera (parasitoid) and Lepidoptera (inquilinous).

Leaf gall, midvein swelling, green, glabrous and one-chambered (Fig. 2K).

Previous records: The same gall has been recorded on Croton floribundus in Tiradentes (MG) (Maia & Fernandes, 2004).

Galler: Lasiopteridi (Cecidomyiidae).

Associated fauna: Hymenoptera (parasitoid).

Leaf gall, circular, green glabrous and one-chambered (Fig. 2L).

Previous records: Galls on Croton spp. were recorded in Ilha da Marambaia (RJ) (Rodrigues et al., 2014), Pará (Almada & Fernandes, 2011), Catimbau Valley National Park (PE) (Silva et al., 2011), Tiradentes (MG) (Maia & Fernandes, 2004). Maia & Fernandes (2004) compiled the records of galls for five host plant species, four galls induced by cecidomiids and one induced by Eriophyidae (Acari), found by other authors for the genus Croton (Gagné, 1994; Rübsaamen, 1905; Tavares, 1922; Houard, 1933; Tavares, 1925; Tavares, 1915).

Senefeldera verticillata (Vell.) Croizat. (endemic species)

Leaf gall, globoid, green, glabrous and one-chambered (Fig. 2M). This is the first record of gall on S. verticillata.

Associated fauna: Isoptera (successors). This is the first record of Isoptera as successors in insect galls.

Fabaceae

Inga acuminata Benth.

Bud gall, globoid, green, hairy and one-chambered (Fig. 2N). This is the first record of gall on I. acuminata.

Mimosa sp.

Stem gall, globoid, brown, glabrous and one-chambered (Fig. 2O).

Galler: Lepidoptera.

Previous records: Galls on Mimosa spp. were recorded in Caetité (BA) (Nogueira et al., 2016), Paramirim (PE) (Maia et al., 2010), Xingó (Northeast region) (Carvalho-Fernandes et al., 2012), Ceará (Gagné & Jaschhof, 2014), Rio Grande do Sul (Mendonça et al., 2014), Grumari (RJ) (Oliveira & Maia, 2005).

Fabaceae sp.1

Leaf gall, fusiform, brown, glabrous and one-chambered (Fig. 2P).

Lauraceae

Ocotea elegans Mez. (endemic species)

Stem gall, fusiform, brown, glabrous and multi-chambered (Fig. 3A). This is the first record of gall on O. elegans.

Malvaceae

Guazuma ulmifolia Lam.

Stem gall, fusiform, green, hairy and one-chambered (Fig. 3B).

Leaf gall, globoid, green, hairy and one-chambered.

Galler: Lopesiini (Cecidomyiidae) (Fig. 3C).

Previous records: Galls on G. ulmifolia were recorded in Serra do Cipó (MG) (Coelho et al., 2009).

Guazuma sp.

Leaf gall, conical, green, glabrous and one-chambered (Fig. 3D).

Galler: Hemiptera.

Ochnaceae

Ouratea stipulata (Vell.) Engl. (endemic species)

Leaf gall, discoid, green, glabrous and one-chambered (Fig. 3E). This is the first record of gall on O. stipulata.

Piperaceae

Piper amalago L.

Leaf gall, discoid, green, glabrous and one-chambered (Fig. 3F).

Previous records: Galls on P. amalago were recorded in Grumari (RJ) (Oliveira & Maia, 2005).

Proteaceae

Roupala montana var. brasiliensis (Klotzsch) K.S. Edwards

Leaf/stem gall, globoid, brown, glabrous and one-chambered (Fig. 3G).

Galler: Cecidomyiidae.

Previous records: Galls on R. montana were recorded in Caldas Novas (GO) (Santos et al., 2012), Ecological Station of Jataí (SP) (Saito & Urso-Guimarães, 2012), Serra dos Pireneus (GO) (Araújo et al., 2011), Rio Grande do Sul (Toma & Mendonça, 2013).

Rubiaceae

Psychotria nuda (Cham. & Schltdl.) Wawra (endemic species)

Leaf gall, globoid, brown, hairy and one-chambered (Fig. 3H). This is the first record of gall on P. nuda.

Sabiaceae

Meliosma sellowii Urb. (endemic species)

Stem gall, fusiform, brown, glabrous and multi-chambered (Fig. 3I). This is the first record of gall on M. sellowii.

Sapindaceae

Allophylus edulis (A. St.-Hil. et al.) Hieron. ex Niederl.

Stem gall, fusiform, brown, hairy and one-chambered (Fig. 3J).

Associated fauna: Pteromalidae (Hymenoptera) (parasitoid).

Leaf gall, midvein swelling, green, glabrous and one-chambered (Fig. 3K).

Stem gall, globoid, brown, glabrous and multi-chambered (Fig. 3L).

Stem gall, fusiform, green, glabrous and one-chambered (Fig. 3M).

Associated fauna: Hymenoptera (parasitoid).

Stem gall, fusiform, brown, glabrous and multi-chambered (Fig. 3N).

Stem gall, globoid, brown, hairy and multi-chambered (Fig. 4A).

Associated fauna: Hymenoptera (parasitoid).

Previous records: Galls on A. edulis were recorded in São Francisco de Paula (RS) - Araucaria Forest (Toma & Mendonça, 2013).

Solanaceae

Cestrum intermedium Sendtn.

Leaf gall, fusiform, green, glabrous and one-chambered (Fig. 4B).

Cestrum sp.

Stem gall, globoid, green, glabrous and multi-chambered (Fig. 4C).

Associated fauna: Hymenoptera (parasitoid).

Previous records: Galls on Cestrum were recorded in Bertioga (SP) (Maia et al., 2008), Santa Teresa, (ES) (Maia et al., 2014), Mato Grosso do Sul (Urso-Guimarães et al., 2016). Maia et al. (2008) compiled the records of galls for four host plant species, three galls induced by Aphidae (Hemiptera) and one induced by cecidomyiidae (Diptera), found by other authors for the genus Cestrum (Tavares, 1909; Tavares, 1915; Houard, 1933).

Not identified

Leaf gall, midvein swelling, green, glabrous and one-chambered (Fig. 4D).

Galler: Alycaulini (Cecidomyiidae).

Associated fauna: Hemiptera (inquiline).

Stem gall, fusiform, brown, glabrous and multi-chambered (Fig. 4E).

Stem gall, fusiform, brown, glabrous and multi-chambered (Fig. 4F).

Leaf gall, globoid, green, glabrous and one-chambered (Fig. 4G).

Stem gall, fusiform, brown, glabrous and multi-chambered (Fig. 4H).

Galler: Cecidomyiidae.

Associated fauna: Coleoptera (inquiline).

Bud gall, fusiform, brown, glabrous and one-chambered (Fig. 4I).

Stem gall, fusiform, brown, glabrous and one-chambered (Fig. 4J).

Stem gall, fusiform, brown, glabrous and multi-chambered (Fig. 4K).

Leaf gall, fusiform, green, glabrous and one-chambered (Fig. 4L).

Leaf gall, globoid, green, hairy and one-chambered (Fig. 4M).

Associated fauna: Hymenoptera (parasitoid).

DISCUSSION

The gall richness values found in the present study are similar for some studies performed in the Semidecidual Seasonal Forest, for example in Telêmaco Borba, PR (Santos & Ribeiro, 2015) and Ilha do Cabo Frio, Arraial do Cabo, RJ (Maia & Souza, 2013), lower values were recorded in Goiânia, GO (Santos et al., 2010), and Maringá, PR (Carvalho et al., 2015). Urso-Guimarães et al. (2016) with 65 morphotypes recorded the greatest richness of galls for this physiognomy. However, it is worth mentioning that the sample effort in the different works cited was not performed in the same way thus hindering the direct comparison of the results (Table 4). The average number of gall morphotypes for host plant species was 1.79. In Brazilian inventories, the average ranges from 1.0 to 2.1 (Maia et al., 2014). Similar values were found for all other areas already studied in the Semideciduous Seasonal Forest (Santos et al., 2010; Maia & Souza, 2013; Carvalho et al., 2015; Santos & Ribeiro, 2015; Urso-Guimarães et al., 2016). This fact is interesting, because suggest a limitation in the number of galling species supported by host plant species (Maia & Oliveira, 2010).

Table 4 Data from literature on insect gall inventories in Semidecidual Seasonal Forest of Brazil (Goiânia, GO - Santos et al., 2010; Ilha do Cabo Frio, Arraial do Cabo, RJ - Maia & Souza, 2013; Telêmaco Borba, PR - Santos & Ribeiro, 2015; Maringá, PR - Carvalho et al., 2015; Bodoquena, MS - Urso-Guimarães et al., 2016). 

Cicuta Bodoquena Telêmaco Borba Goiânia Cabo Frio Maringá
Number of morphotypes 43 65 41 34 45 35
Number of host plant species 24 38 32 20 29 -
Average number of morphotypes/host plant species 1.79 1.71 1.28 1.7 1.55 -
Sampling effort 16 hs 8 hs 10 hs:30min - 24 hs Plots
Richest plant families Euphorbiaceae Bignoniaceae Asteraceae Leguminosae Asteraceae Sapindaceae
Sapindaceae Asteraceae Euphorbiaceae Styracaceae Myrtaceae -
- Rubiaceae Solanaceae Ulmaceae - -
Super-host plant genera Allophylus Fridericia Croton Bauhinia Eugenia -
Croton Casearia - Inga Guapira -
- Serjania - Myrcia Lantana -

Sapindaceae and Euphorbiaceae were the families with the highest number of galls. In the Brazil, some studies also recorded these families as the richest in insect galls (Santos & Ribeiro, 2015; Carvalho et al., 2015 and Maia & Carvalho-Fernandes, 2016). However, we do not corroborate the results found in other studies where the Asteraceae family is recorded as richier in insect galls (Maia & Souza, 2013; Santos & Ribeiro, 2015; Urso-Guimarães et al., 2016). Regarding the genera of host plants, the results confirm other studies where Croton is considered a super host, accumulating nine different galls morphotypes (Teixeira & Isaias, 2013). These results can be explained by the fact that the species Allophylus edulis and Croton sp. presented a high richness of insect galls. Some host plants have few associated insect species (Hawkins & Compton, 1992). In contrast, other plants support a high level of richness of galling insects, such as the species Baccharis pseudomyriocephala Teodoro (Asteraceae) (Araújo et al., 2003), Guapira opposita (Vell.) Reitz. (Nyctaginaceae) (Maia et al., 2008) and Mikania glomerata Spreng. (Asteraceae) (Maia & Proença, 2016) in the Neotropical Region. The presence of these plants, called “super-hosts” (Veldtman & McGeoch, 2003), can cause a dramatic increase in the local accumulation of galling insect species (Carneiro et al., 2009).

Leaf galls predominated. This is observed in all other Brazilian biomes and all biogeographical regions, probably because leaves represent an abundant and frequently renewable resource, with undifferentiated meristematic cells that are essential to gall growth (Maia, 2011). Green and brown were the predominant colors. These colors are usually mentioned in Brazilian inventories (Maia et al., 2014). The majority of the galls were glabrous and one-chambered as in all other Brazilian galls inventories, excepting by Delfinópolis, where hairy galls were more frequent than glabrous (54% and 46%, respectively) (Urso-Guimarães et al., 2003).

Cecidomyiidae (Diptera) was the most frequent galling insect, followed by Hemiptera and Lepidoptera. Cecidomyiidae are the most speciose and frequent galling insects in all zoogeographic regions (Gagné & Jaschhof, 2014). Hemiptera and Lepidoptera are also important gallers. In the Neotropical region, they are the second and third most frequent galling insects (Maia, 2006). Coleoptera is the fourth (Maia, 2012), but they were not found in the searched area.

Hymenoptera are the most important natural enemies of Cecidomyiidae (Diptera). They are frequently found in galls induced by these midges mostly acting as parasitoids, and in some cases as phytophagous able to modify the structure and morphology of the gall (Maia & Azevedo, 2009).

CONCLUSIONS

The Floresta da Cicuta was the third area in richness of insect galls compared to the other areas of Semidecidual Seasonal Forest physiognomy. The present study registered the Euphorbiaceae and Sapindaceae as the plant families with the highest morphotypes of galls in the studied physiognomy. The distribution of the galls in the plant organs followed the pattern already known in other studies, with predominance of leaf galls and the stems followed by buds. Most of the galls presented the following morphological characteristics: same coloration of the occurrence organ, a single internal chamber, and glabrous, also predominant in other studies. Three orders of galling insects were found: Diptera (Cecidomyiidae), Lepidoptera and Hemiptera, with clear predominance of Cecidomyiidae.

ACKNOWLEDGEMENTS

We would like to thank Valéria Cid Maia for a careful first reading of the manuscript and identification of the gall inducers, and the whole team at the ICMBIO - Floresta da Cicuta (Sandro Leonardo Alves, Glaucia Alves Viana de Oliveira, Vanessa Martins de Nazareth, José Henrique de Oliveira) for support and readiness during the execution of the study. We thank the anonymous reviewers for suggestions on earlier versions of the manuscript.

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Recibido: 30 de Noviembre de 2016; Aprobado: 15 de Mayo de 2018

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