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Papéis Avulsos de Zoologia

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

Pap. Avulsos Zool. vol.59  São Paulo  2019  Epub 25-Mar-2019

http://dx.doi.org/10.11606/1807-0205/2019.59.04 

Articles

Characterization of insect galls from a vegetation area in Altinópolis, São Paulo State, Brazil

Amanda das Neves Ribeiro1  4 
http://orcid.org/0000-0002-5970-6505

Maria Isabel Protti de Andrade Balbi2 
http://orcid.org/0000-0001-6092-3462

Maria Virginia Urso-Guimarães1  3  5 
http://orcid.org/0000-0003-3657-9379

1Universidade Federal de São Carlos (UFSCAR), Centro de Ciências Humanas e Biológicas (CCHB), Departamento de Biologia (DBio),Laboratório de Sistemática de Diptera. Sorocaba, SP, Brasil.

2Universidade de São Paulo (USP), Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto (FFCLRP), Departamento de Biologia, Laboratório de Morfologia e Evolução de Diptera (LMED). Ribeirão Preto, SP, Brasil. E-mail: mariaisabel.balbi@gmail.com

3Universidade de São Paulo (USP), Museu de Zoologia (MZUSP). São Paulo, SP, Brasil.

Abstract

Herein, we studied the occurrence of insect galls from natural vegetation around the Itambé Cave, Altinópolis, SP, Brazil. A sampling effort of 7.5 hours resulted in 41 gall morphotypes on 21 host plant species from 14 families. The richest families of host plants in morphotypes were Fabaceae (N = 11), Euphorbiaceae (N = 7), and Malpighiaceae (N = 5). Copaifera langsdorffii Desf. (N = 8), Croton floribundus Spreng. (N = 7), Diplopterys pubipetala (A. Juss.) W.R. Anderson & C.C. Davis (N = 5), and Bauhinia holophylla (Bong.) Steud. (N = 4) were the super host plant species. Among the gall makers obtained, cecidomyiids were reared in 81% of cases and Hemiptera (Diaspididae), Hymenoptera (Eurytomidae), Coleoptera (Apion sp./Apionidae), and Lepidoptera in 4.5% of cases, each. The parasitoids belong to the Chalcidoidea superfamily (Hymenoptera). One new species of Camptoneuromyiia (Cecidomyiidae) was found in Smilax oblongifolia Pohl ex Griseb. (Smilacaceae) as inquiline and a new species of Lestodiplosis in Diplopterys pubipetala (Malpighiaceae) was a predator. We also present the first register of Bauhinia holophylla as host plants of Cecidomyiidae. We also present the first register of Bauhinia holophylla as host plants of Cecidomyiidae, and we expand the occurrence of Rochadiplosis tibouchinae Tavares, Lopesia spinosa Maia and Couridiplosis vena Maia to São Paulo State. The results of this paper are a continuation of the description of gall morphotypes from the vegetation in Northeastern São Paulo State, and they also increase knowledge about the diversity of host plant and gall-maker associations in the Neotropical region.

Key-Words Biodiversity; Gall maker; Neotropical region; Northeastern São Paulo State; Plant-insect interaction

INTRODUCTION

Galls are vegetal structures produced by an abnormal increase of plant cells, tissues or organs in response to specific stimulation caused by an inductor agent, such as a virus, bacteria, nematodes or insects (Carneiro et al., 2009; Shorthouse et al., 2005; Shorthouse & Rohfritsch, 1992). Manipulation of the host plant can be so strong that the inducer assumes control of the gall tissue’s chemical composition, which is frequently quite different from the ungalled tissue (Scareli-Santos, 2001). It also involves two counteracting events: the insect stresses the host organ, and the host counters it with newly differentiated tissues and new physiological activities (Raman, 2007). Some authors affirm the high level of specificity of gall maker and host plant (species-specific) associations as a result of the interaction between two genotypes (Abrahamson & McCrea, 1986; Abrahamson & Weis, 1987; Stone & Schönrogge, 2003). Galls can be induced in any vegetal organ, but the highest frequency and diversity is found in leaves (Mani, 1964). Each inducer species produces galls that are anatomically and physiologically different from those induced by other related species (Stone & Schönrogge, 2003). In this study we describe qualitatively the insect gall morphotypes found in an area of Semideciduous Seasonal Forest in Altinópolis, which is a continuation of the description of gall morphotypes richness in the vegetation from Northeastern São Paulo State, Brazil (Saito & Urso-Guimarães, 2012; Urso-Guimarães & Scareli-Santos, 2006). The Semideciduous Seasonal Forest is an Atlantic Forest phytophysiognomy that is considered a priority area for conservation, due to its great biological richness and the degradation it has suffered in recent years (Martins et al., 2003). Currently, the vegetation is disturbed by anthropic action, mainly around the Itambé Cave.

MATERIAL AND METHODS

Studied area

The samples were carried out in the Itambé Touristic Complex area, located in Altinópolis, State of São Paulo, Brazil (47°23.0’W, 21°00.7’S, about 900 m altitude) (Fig. 1A). The Itambé Touristic Complex has an area of approximately 1.2 km² and includes two main attractions, the Itambé Cave and the Itambé Waterfall. Altinópolis presents Cwa climate (Köppen, 1948) and the vegetation is a mosaic of Riparian Forest, Seasonal Semideciduous Forest, and Cerrado phytophysiognomies, predominated by Seasonal Semideciduous Forest (Ponzoni & Moreira-Pessôa, 2015).

Figure 1 Aerial map of study area in Altinópolis, São Paulo State, Brazil. In the right corner, a map of Altinópolis in light green with the neighboring municipalities in grey, and in the upper right corner, Altinópolis’ location in the State of São Paulo (Sources: IBGE and CNES/Airbus. Digital Globe/Google). 

Sampling and analysis of the material

Five samplings were carried out in the area from March 2000 to August 2002 (15.iii.2000, 02.viii.2000, 04.x.2000, 28.v.2001, 12.viii.2002). Each sample consisted of an hour and a half walk on a 1.5 km trail, with a total sampling effort of 7.5 hours. To compare the similarity of the morphotypes in the host plant species found in Altinópolis and those from other areas of São Paulo State (Luiz Antônio, Santa Rita do Passa Quatro, and Sorocaba) we performed a binary similarity analysis using the Sorensen Similarity Coefficient (Ss = 2a / 2a + b + c, where a = total number of species in samples A and B, b = number of species present in sample B, but not in A, c = number of species present in sample A, but not in B). The branches of host plants with galls were collected, photographed; some galls were dissected to obtain immature, and other galls were placed in plastic pots to rear the adult forms of gall makers and associated fauna. All insects were preserved in 70% alcohol. The cecidomyiids were later mounted on microscope slides following the methodology outlined in Gagné (1994) and identified to genera based on the keys of Gagné (1994). After identifying the cecidomyiid genus, the obtained specimens (immature and/or adults) were compared to the original descriptions of Brazilian species from the genus. Other insects were sent to and identified by the specialists indicated in the acknowledgements. The nomenclature of galls follows Isaias et al. (2013). The exsiccates of host plants with fertile material are deposited in the Herbarium of FFCLRP/USP. The insects and galls are deposited in the Laboratório de Sistemática de Diptera/UFSCar.

RESULTS AND DISCUSSION

We found forty-one gall morphotypes on 21 host plant species from 14 different families. The morphotypes were obtained mostly from leaves (85%) followed by stems (15%), leaf buds (5%), and tendrils (3%). Our results corroborate other surveys conducted in drier environments (Mani, 1964; Maia, 2001; Urso-Guimarães et al., 2003; Fernandes & Negreiros, 2006; Maia et al., 2008) including those from Northeastern São Paulo State, Brazil (Urso-Guimarães & Scareli-Santos, 2006; Saito & Urso-Guimarães, 2012) where the percentage of leaf galls ranges from 75% to 90%. The most frequent shape of galls was globoid (37%) followed by lenticular (25%), fusiform (15%), cylindrical and amorphous (7% each), conical (5%), and convex and triangular (2.5% each). The most frequently sampled gall colors were brown (46%) and green (34%), followed by light yellow (22%), red (10%), black and yellow (2.5% each). In relation to the indumentum and internal chambers, most galls were glabrous (64%) and unilocular (93%) (for detailed discussion about presence/absence of trichomes, see Saito & Urso-Guimarães, 2012). Table 1 presents a detailed morphological description of the collected galls, and associated fauna from the samples. Plates with morphotypes are presented in Figs. 2A-L, 3A-L, 4A-N.

Table 1 Characterization of insect galls recorded in Altinópolis, Northeastern São Paulo State, Brazil by host plant. Figures refer to gall morphotype’s picture. 

Host family Host species Organ Shape Color Pubescence Occurrence Gall maker Associated fauna Figures
Anacardiaceae Tapirira guianensis Aubl. Leaf Globoid Green No unilocular Diptera (Cecidomyiidae, Cecidomyiinae, Cecidomyiidi) - 2a
Asteraceae Praxelis pauciflora (Kunth) R.M. King & H. Rob. Leaf Amorphous Green Yes unilocular empty gall - -
Asteraceae Moquiniastrum pulchrum (Cabrera) G. Sancho Leaf bud Amorphous Light yellow Yes unilocular Diptera (Cecidomyiidae, Cecidomyiinae, Cecidomyiini, Gen. nov., sp. nov.) Hymenoptera (Eulophidae, Pteromalidae, Torymidae) 2b
Asteraceae Moquiniastrum pulchrum Leaf/Stem Globoid Light yellow Yes unilocular Diptera (Cecidomyiidae, Cecidomyiinae, Cecidomyiidi) - 2c
Bignoniaceae Amphilophium elongatum (Vahl) L.G. Lohmann Tendril/Leaf midvein/Stem Fusiform Green No unilocular empty gall - 2d
Caryocaraceae Caryocar brasiliense Cambess. Leaf Lenticular Brown Yes unilocular Hemiptera (Diaspididae) Hymenoptera (Encyrtidae) 2e
Chrysobalanaceae Couepia grandiflora (Mart. & Zucc.) Benth. Leaf Lenticular Brown Yes unilocular Diptera (Cecidomyiidae, Cecidomyiinae, Cecidomyiidi) - 2f
Euphorbiaceae Croton floribundus Spreng. Leaf Cylindrical Brown Yes unilocular Diptera (Cecidomyiidae, Cecidomyiinae, Lopesiini, Lopesia spinosa Maia) - 2g, 2h
Euphorbiaceae Croton floribundus Leaf Lenticular Brown No unilocular Diptera (Cecidomyiidae/Cecidomyiinae) - 2i
Euphorbiaceae Croton floribundus Leaf Globoid hollow Light yellow Yes unilocular Diptera (Cecidomyiidae/Cecidomyiinae) - 2j
Euphorbiaceae Croton floribundus Leaf Globoid filled Light yellow Yes unilocular Diptera (Cecidomyiidae/Cecidomyiinae) - 2k
Euphorbiaceae Croton floribundus Leaf vein Fusiform Light yellow/Green Yes unilocular Diptera (Cecidomyiidae, Alycaulini, Couridiplosis vena Maia) - 2l
Euphorbiaceae Croton floribundus Stem Globoid Brown No unilocular Coleoptera (Apioninae, Apion sp.) - 3a
Euphorbiaceae Croton floribundus Stem Fusiform Brown No unilocular Lepidoptera - -
Fabaceae Bauhinia holophylla (Bong.) Steud. Leaf Conical Light yellow/Red Yes unilocular Diptera (Cecidomyiidae, Cecidomyiinae, Lasiopteridi) Hymenoptera (Rileynae/Eurytomidae) 3b, 3c
Fabaceae Bauhinia holophylla Leaf Globoid Brown No unilocular empty gall - -
Fabaceae Bauhinia holophylla Stem Fusiform Brown No plurilocular empty gall - 3d
Fabaceae Copaifera langsdorffii Desf. Leaf Convex Red No unilocular empty gall - 3e
Fabaceae Copaifera langsdorffii Leaf Globoid Brown No unilocular empty gall - 3f
Fabaceae Copaifera langsdorffii Leaf Globoid Orange/Red/Brown Yes unilocular empty gall - 3g
Fabaceae Copaifera langsdorffii Leaf Lenticular Light yellow No unilocular empty gall - 3h
Fabaceae Copaifera langsdorffii Leaf Triangular Brown No unilocular empty gall - 3i
Fabaceae Copaifera langsdorffii Leaf Globoid Red No unilocular empty gall - 3j
Fabaceae Copaifera langsdorffii Leaf Cylindrical Brown No unilocular empty gall - 3k
Fabaceae Copaifera langsdorffii Stem Globoid Brown No plurilocular Hymenoptera (Eulophidae) - 3l
Lauraceae Nectandra sp. Leaf Lenticular Green No unilocular Diptera (Cecidomyiidae/Cecidomyiinae) - 4a
Lauraceae Ocotea sp. Leaf Cylindrical Brown No unilocular empty gall - 4b
Malpighiaceae Diplopterys pubipetala (A. Juss.) W.R. Anderson & C.C. Davis Leaf Conical Green/Brown No unilocular Diptera (Cecidomyiidae, Cecidomyiinae, Clinodiplosini, Clinodiplosis bellum Urso-Guimarães & Carmo-Neto) Hymenoptera (Eulophinae, Entedoninae (Eulophidae), Torymidae) 4c
Malpighiaceae Diplopterys pubipetala Leaf Lenticular Green Yes unilocular Diptera (Cecidomyiidae, Cecidomyiinae, Dasineurini, Dasineura sp.) Diptera (Cecidomyiidae, Cecidomyiinae, Lestodiplosini, Lestodiplosis sp.) 4c
Malpighiaceae Diplopterys pubipetala Leaf Lenticular Yellow/Green/Brown No unilocular empty gall - 4d
Malpighiaceae Diplopterys pubipetala Leaf bud Globoid Brown No unilocular empty gall - 4e
Malpighiaceae Diplopterys pubipetala Stem Fusiform Brown No unilocular empty gall - -
Melastomataceae Miconia stenostachya DC. Leaf Globoid Light yellow Yes unilocular empty gall - 4f
Melastomataceae Tibouchina sp. Leaf Globoid Green Yes unilocular Diptera (Cecidomyiidae, Cecidomyiinae, Lopesiini, Rochadiplosis tibouchinae Tavares) Hymenoptera (Perilampidae) 4g
Meliaceae Guarea guidonia (L.) Sleumer Leaf midvein Fusiform Green No unilocular Diptera (Cecidomyiidae/Cecidomyiinae) - 4h
Myrtaceae Myrcia bella Cambess. Leaf Amorphous Green No plurilocular Hymenoptera (Eurytomidae) - 4i
Myrtaceae Eugenia punicifolia (Kunth) DC. Leaf Lenticular Black No unilocular empty gall - 4j
Myrtaceae Eugenia speciosa Cambess. Leaf Cylindrical with apical projection Light yellow No unilocular Diptera (Cecidomyiidae/Cecidomyiinae) - 4k
Myrtaceae Myrtaceae sp. Leaf Globoid Green No unilocular empty gall - 4l
Sapindaceae Serjania reticulata Cambess. Leaf Lenticular Green/Brown Yes unilocular Diptera (Cecidomyiidae/Cecidomyiinae) - 4m
Smilacaceae Smilax oblongifolia Pohl ex Griseb. Leaf Globoid Green No unilocular Diptera (Cecidomyiidae, Cecidomyiinae, Alycaulini, Alycaulus hexadentatus Urso-Guimarães) Hymenoptera (Eulophidae); Diptera (Cecidomyiidae, Cecidomyiinae, Camptoneuromyiini Camptoneuromyia sp.) 4n

Figure 2 Gall morphotypes in host plants from Altinópolis, São Paulo State, Brazil, (A) Leaf gall of Tapirira guianensis (Anacardiaceae); (B) Bud leaf convolute in a complex gall of Moquiniastrum pulchrum (Asteraceae); (C) Leaf gall of Moquiniastrum pulchrum (Asteraceae); (D) Leaf gall of Amphilophium elongatum (Bignoniaceae), arrow on gall; (E) Leaf gall of Caryocar brasiliense (Caryocaraceae), galls in higher magnification in the upper right corner; (F) Leaf gall of Couepia grandiflora (Chrysobalanaceae), arrow on gall; (G) Cylindrical leaf gall with star trichomes of Croton floribundus (Euphorbiaceae), galls in higher magnification in the upper right corner; (H) Exuvia of Cecidomyiidae emerging from previous gall; (I) Adaxial surface of lenticular leaf gall of Croton floribundus (Euphorbiaceae), galls in abaxial surface in the upper right corner; (J) Hollow globoid leaf gall with long trichomes of Croton floribundus (Euphorbiaceae), gall opened, with a larva in higher magnification in the upper right corner; (K) Filled globoid leaf gall of Croton floribundus (Euphorbiaceae); gall opened, with fungus associated in higher magnification in the upper right corner; (L) Leaf vein gall of Croton floribundus (Euphorbiaceae), exuvia leaving the gall in the upper left corner. (Pictures: Urso-Guimarães, M.V.). 

Figure 3 Gall morphotypes in host plants from Altinopolis, Sao Paulo State, Brazil. (A) Globoid and fusiform stem galls of Croton floribundus (Euphorbiaceae), arrow on both galls; (B) Immature leaf gall of Bauhinia holophylla (Fabaceae), arrow on gall; (C) Mature leaf gall of Bauhinia holophylla (Fabaceae), arrow on gall; (D) Stem gall of Bauhinia holophylla (Fabaceae); (E) Convex leaf gall of Copaifera langsdorffii (Fabaceae); (F) Globoid glabrous leaf gall of Copaifera langsdorffii (Fabaceae); (G) Globoid leaf gall with red and orange trichomes of Copaifera langsdorffii (Fabaceae); (H) Lenticular leaf gall of Copaifera langsdorffii (Fabaceae); (I) Triangular leaf gall of Copaifera langsdorffii (Fabaceae); (J) Globoid red leaf gall of Copaifera langsdorffii (Fabaceae); (K) Cylindrical leaf gall of Copaifera langsdorffii (Fabaceae); (L) Globoid stem gall of Copaifera langsdorffii (Fabaceae). (Pictures: Urso-Guimaraes, M.V.). 

Figure 4 Gall morphotypes in host plants from Altinopolis, Sao Paulo State, Brazil. (A) Leaf gall of Nectandra sp. (Lauraceae); (B) Leaf gall Ocotea sp. (Lauraceae); (C) Cylindrical and lenticular hairy leaf galls of Diplopterys pubipetala (Malpighiaceae); (D) Lenticular leaf gall of Diplopterys pubipetala (Malpighiaceae); (E) Bud leaf gall of Diplopterys pubipetala (Malpighiaceae); (F) Leaf gall of Miconia stenostachya (Melastomataceae); (G) Leaf hairy gall of Tibouchina sp. (Melastomataceae); (H) Leaf gall of Guarea guidonea (Meliaceae); (I) Leaf gall of Myrcia bella (Myrtaceae); (J) Leaf gall of Eugenia punicifolia (Myrtaceae), arrow on gall; (K) Leaf gall of Eugenia speciosa (Myrtaceae), arrow on gall; (L) Leaf gall of Myrtaceae sp., arrow on gall; (M) Leaf gall of Serjania reticulata (Sapindaceae); (N) Leaf gall of Smilax oblongifolia (Smilacaceae). (Pictures: Urso-Guimaraes, M.V.). 

In descending order, gall morphotypes appeared in Fabaceae (N = 11), followed by Euphorbiaceae (N = 7), Malpighiaceae (N = 5), Myrtaceae (N = 4), Asteraceae (N = 3), Lauraceae and Melastomataceae (N = 2). Information about morphotype richness of other families and species is given in Table 2. Our results indicated that the richer the host family, the richer their gall morphotypes, corroborating data previously obtained in the Neotropical region (Gagné, 1994; Araújo, 2011; Santana & Isaias, 2014). However, it’s important to highlight that of the 41 morphotypes sampled, 23 were found in the four host plant species: Copaifera langsdorffii, Croton floribundus, Diplopterys pubipetalum, and Bauhinia holophylla, with eight, seven, five and three morphotypes, respectively. Plants are referred to as super host plants when a single species presents a high number of different gall morphotypes caused by distinct inducers (Veldtman & McGeoch, 2003) and also increases the number of morphotypes per family as related by Araújo (2011).

Table 2 Richness of gall morphotypes in plant host family and species from vegetation around Itambé Cave, Altinópolis, São Paulo State, Brazil. 

Host Plant Families (N = 14) Number of species (N = 21) Gall Morphotypes (N = 41)
Fabaceae 2 11
Euphorbiaceae 1 7
Malpighiaceae 1 5
Myrtaceae 4 4
Asteraceae 2 3
Lauraceae 2 2
Melastomataceae 2 2
Anacardiaceae 1 1
Bignoniaceae 1 1
Caryocaraceae 1 1
Chrysobalanaceae 1 1
Meliaceae 1 1
Sapindaceae 1 1
Smilacaceae 1 1

Prior to this study, only four surveys have been performed in areas with Seasonal Semideciduous Forest (SSF):, Maringá/PR (Carvalho et al., 2015), Goiânia/GO (Santos et al., 2010), Serra da Bodoquena/MS (Urso-Guimarães et al., 2017), and Sorocaba/SP (Ansaloni et al., 2018), which were compared to Altinópolis (this study). Table 3 shows the compared richness of gall morphotypes in these areas, as well as from nearby areas of Cerrado vegetation from Northeastern São Paulo State. The average 1.95 morphotypes per plant species in Altinópolis is comparable to the average found in other dry environments (see also Table 3 in Urso-Guimarães et al., 2017) and is higher than those found in areas with the same vegetation in Goiânia/GO (1.7), Serra da Bodoquena/MS (1.6), and Maringá/PR (1.2). This average is only comparable to the Seasonal Semideciduous Forest area in Sorocaba in Southeastern São Paulo State (2.1), where the sampling effort was 48 hours and it is higher than the Cerrado areas in Luiz Antônio (1.7) and Santa Rita do Passa Quatro (1.4), both nearby areas in the State of São Paulo.

Table 3 Richness of gall morphotypes from localities with Seasonal Semideciduous Forest and Cerrado phytophysiognomies in Northeastern São Paulo State. 

Locality Richness of gall morphotypes Richness of host plant species Average number of gall/host plant species Total sampling effort
Sorocaba, SP (Ansaloni et al., 2018) 113 54 2.1 48h
Altinópolis, SP (this study) 41 21 1.95 7.5h
Estação Ecológica do Jataí, Luiz Antônio, SP (Saito & Urso-Guimarães, 2012) 69 41 1.7 15h
Goiás, GO (Santos et al., 2010) 34 20 1.7 not informed
Serra da Bodoquena, MS (Urso-Guimarães et al., 2017) 65 39 1.6 2h
Santa Rita do Passa Quatro, SP (Urso-Guimarães & Scareli-Santos, 2006) 35 25 1.4 not informed
Maringá, PR (Carvalho et al., 2015)* 40 35 1.2 not informed

* In Carvalho et al., 2015 were not identified all morphospecies and morphotypes are not characterized, even so we chose to include these data because it is one of the few works in the area of Seasonal Semideciduous Forest phytophysiognomy.

Comparing morphotypes of the host plant species found in Altinópolis with those from other areas, we found low similarity among them, with the Sorensen Coefficient (Ss) varying from 0.01 to 0.28 (Table 4). The highest similarity was found between Altinópolis (SSF) and Santa Rita do Passa Quatro (Cerrado Pé-de-Gigante) with Ss = 0.28, even though they have different phytophysiognomies and are not the closest areas (122 km). Two factors influenced such result, the first was the presence of eleven similar gall morphotypes in eight host plant species with wide distribution, which are Amphilophium elongatum (Vahl) L.G. Lohmann, Caryocar brasiliense Cambess, Copaifera langsdorffii Desf., Diplopterys pubipetala (A. Juss.) W.R. Anderson & C.C. Davis, Miconia stenostachya DC., Moquiniastrum pulchrum (Cabrera) G. Sancho, Myrcia bella Cambess, and Tapirira guianensis Aubl.; the second factor was the presence of three super host plant species, Copaifera langsdorffii, Diplopterys pubipetala, and Moquiniastrum pulchrum, responsible for six of the eleven similar gall morphotypes.

Table 4 Sorensen Similarity Coefficient (Ss) comparing Altinópolis gall morphotypes per host plant species from Semideciduous Seasonal Forest (SSF) in the States of Mato Grosso do Sul and Southeastern São Paulo and with Cerrado in Northeastern São Paulo State. 

Locality Ss
Altinópolis X Santa Rita do Passa Quatro (Urso-Guimarães & Scareli-Santos, 2006) 0,28
Altinópolis x Sorocaba (Ansaloni et al., 2018) 0,15
Altinópolis X Luiz Antônio (Saito & Urso-Guimarães, 2012) 0,10
Altinópolis x Serra da Bodoquena, MS (Urso-Guimarães et al., 2017) 0,01

Of the associated gall fauna from Altinópolis, we recorded eighteen species of Diptera (Cecidomyiidae) (81.8%), two species of Hymenoptera (Eulophidae and Eurytomidae) (9.1%), and one species of Hemiptera (Diaspididae), Coleoptera (Apion sp./Apionidae) and Lepidoptera (4.5% each).

Of the eighteen species of cecidomyiids found, five species were known: Rochadiplosis tibouchinae Tavares associated with Tibouchina sp. (Tavares, 1917) from Rio de Janeiro State (Tavares, 1917), and Lopesia spinosa Maia and Couridiplosis vena Maia associated with Croton floribundus (Euphorbiaceae) from Minas Gerais State (Maia & Fernandes, 2004), and Clinodiplosis bellum Urso-Guimarães and Carmo-Neto found in conical leaf galls of Diplopterys pubipetala (Urso-Guimarães & Carmo-Neto, 2015) and Alycaulus hexadentatus found on leaf galls in Smilax oblongifolia Pohl ex Grisebach (Smilacaceae) in Altinópolis/São Paulo State (Urso-Guimarães, 2018). The other thirteen species of Cecidomyiidae (78%) are probably new species, four of which are going to be described in other papers, as well as the previously unknown larvae of L. spinosa. L. spinosa and C. vena associated with C. floribundus (Euphorbiaceae) are registered in the São Paulo State for the first time.

Parasitoids were found in 15% of the sampled galls (Table 1) and belong to Hymenptera families Encyrtidae, Eulophidae (Entedoninae, Eulophinae), Eurytomidae (Rileynae), Pteromalidae, Perilampidae, and Torymidae. When compared to other environments as the Cerrado in Minas Gerais State (34%, Maia & Fernandes, 2004), Restinga in São Paulo State (24%, Maia et al., 2008), and especially the Restinga in Rio de Janeiro State (95%, Maia & Azevedo, 2009) such result is relatively low.

Herein, Bauhinia holophylla (Bong.) Steud is registered as host plant of Cecidomyiidae for the first time. The results of this work help increase knowledge about the diversity of the host plant and gall-maker associations in the Neotropical region, which, despite researchers’ efforts, still presents large information gaps.

ACKNOWLEDGMENTS

The authors thank Dr. Dalton de Souza Amorim (FFCLRP/USP) for infrastructure support and identification of the Diaspididae (Hemiptera), Dr. Helena Carolina Onody for identification of the Chalcidoidea (Hymenoptera), Dr. Alessandra Tomaselli Fidélis (UNESP/Rio Claro), Dr. Ana Carolina Bonifácio Caboni (ICMBio), Dr. Olga Kotchetkoff-Henriques (PMRP), and Dr. Ricardo Barosela (FFCLRP/USP) for identification of botanical species,. This study was supported by FAPESP (Proc. #99/01429-1).

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Published with the financial support of the Committee of "Programa de Apoio às Publicações Científicas Periódicas da USP" (SIBi-USP)

Recibido: 22 de Noviembre de 2017; Aprobado: 29 de Enero de 2019

4E-mail: amanda_nribeiro@hotmail.com

5E-mail: mvirginiaurso@gmail.com

Edited by: Carlos José Einicker Lamas

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