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Biota Neotropica

Print version ISSN 1806-129XOn-line version ISSN 1676-0611

Biota Neotrop. vol.18 no.4 Campinas  2018  Epub July 16, 2018

http://dx.doi.org/10.1590/1676-0611-bn-2018-0523 

Article

Entomogen galls in a Seasonal Semideciduous Forest area in Sorocaba, Southeast of São Paulo State, Brazil

Galhas entomógenas em uma área de Mata Estacional Semidecidual em Sorocaba, Sudeste do Estado de São Paulo, Brasil

Leticia Salvioni Ansaloni1 

Julia Rodrigues Salmazo1 

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

1Universidade Federal de São Carlos, Sorocaba, SP, Brasil

Abstract:

In this paper we studied the occurrence of insect galls and gall makers in a Seasonal Semideciduous Forest area in Sorocaba Municipality, Southeast of São Paulo State, Brazil. One hundred and thirteen morphotypes of galls on 54 species of host plants of 24 different families were found. The families of host plants richer in gall morphotypes were Fabaceae (N = 26) and Malpighiaceae (N = 19); the super host plants species were Copaifera langsdorffii Desf. (Fabaceae) (N = 16), Stigmaphyllon lalandianum (Aubl.) Marchand (Malpighiaceae) (N = 11), Protium heptaphyllum A. Juss. (Burseraceae) (N = 10), Serjania lethalis A.St.-Hil. (Sapindaceae) (N = 5). Most of the galls were found empty, but insects of the family Cecidomyiidae (Diptera) were responsible for the induction of 92% (N = 11) of the galls and Hymenoptera (N = 1) for 8%. We registered insects of the order Hymenoptera (N = 11) as parasitoids and as successors Hemiptera (N = 8), Acari (N = 7), Psocoptera (N = 4), Hymenoptera (Formicidae, N = 2), Collembola and Thysanoptera (N = 1 each). Two species of Cecidomyiidae with inquiline habit were also obtained, Neolasioptera sp. and Trotteria sp. Five plant species were registered as hosts for cecidomyiids for the first time: Aloysia virgata (Ruiz & Pav.) Juss., Calliandra foliolosa Benth., Myrcia splendens (Sw.) DC., Serjania lethalis A.St.-Hil., and Tapirira guianiensis Aubl. This is the first study of gall characterization, gall makers and associated fauna of the Southeast of the State of São Paulo.

Keywords: Atlantic Forest Biome; biodiversity; gall makers; Neotropical region; plant-insect interaction

Resumo:

Neste trabalho, estudamos a ocorrência de galhas entomógenas e insetos galhadores em uma área de Mata Estacional Semidecidual em Sorocaba, Sudeste do Estado de São Paulo, Brasil. Cento e treze morfotipos de galhas em 54 espécies de plantas hospedeiras de 24 famílias distintas foram encontradas. As famílias de plantas hospedeiras mais ricas em morfotipos de galhas foram Fabaceae (N=26) e Malpighiaceae (N=19) e as espécies de plantas super hospedeiras foram Copaifera langsdorffii Desf. (Fabaceae) (N = 16), Stigmaphyllon lalandianum (Aubl.) Marchand (Malpighiaceae) (N = 11), Protium heptaphyllum A. Juss. (Burseraceae) (N = 10), Serjania lethalis A.St.-Hil. (Sapindaceae) (N = 5). A maioria das galhas foi encontrada vazia, mas insetos da família Cecidomyiidae (Diptera) foram responsáveis pela indução de 92% (N=11) das galhas e Hymenoptera (N = 1) por 8%. Nós registramos insetos da Ordem Hymenoptera (N = 11) como parasitoides e Hemiptera (N = 8), Acari (N = 7), Psocoptera (N = 4), Hymenoptera (Formicidae, N = 2), Collembola e Thysanoptera (N = 1 cada) como successores. Duas espécies de Cecidomyiidae com hábito inquilino também foram obtidas, Neolasioptera sp. e Trotteria sp. Cinco espécies de plantas foram registradas como hospedeiras para cecidomiídeos pela primeira vez: Aloysia virgata (Ruiz & Pav.) Juss., Calliandra foliolosa Benth., Myrcia splendens (Sw.) DC., Serjania lethalis A.St.-Hil. e Tapirira guianiensis Aubl. Este é o primeiro estudo de caracterização de galhas entomógenas, galhadores e fauna do Sudeste do Estado de São Paulo.

Palavras-chave: Bioma Mata Atlântica; biodiversidade; galhador; região Neotropical; interação ineto-planta

Introduction

Studies on the occurrence and characterization of galls in Brazil have increased significantly in the last 30 years, especially in Cerrado Biome (Fernandes et al. 1988, Fernandes et al. 1997, Urso-Guimarães et al. 2003, Maia & Fernandes 2004, Scareli-Santos et al. 2005, Urso-Guimarães & Scareli-Santos 2006, Maia et al. 2008, Saito & Urso-Guimarães 2012, Carneiro et al. 2009, Coelho et al. 2009, Malves & Frieiro-Costa 2012, Maia 2012, Araújo et al. 2013, Bergamini et al. 2017), Restinga and Ombrophilous Forest from Atlantic Forest Biome (Maia et al. 2008, Bregonci et al. 2010, Maia 2013a, Maia 2013b, Rodrigues et al. 2014, Maia et al. 2014, Maia & Carvalho-Fernandes 2016).

However, environments such as Pantanal (Julião et al. 2002, Urso-Guimarães et al. 2017), Caatinga (Carvalho-Fernandes et al. 2012, Santos et al. 2011), Amazonic Forest (Julião et al. 2015) and Seasonal Semideciduous Forest of Atlantic Forest Biome (Santos et al. 2010, Carvalho et al. 2015) are considered little sampled and their biodiversity is still poorly understood. Particularly, the Seasonal Semideciduous Forest is considered priority area for conservation in Atlantic Forest Biome due to two factors: the biological richness and the fast degradation in recent years to economic activities in the Southeast region of Brazil (Martins et al. 2003).

Considering that gall morphotypes are used as a surrogate for species of gall-inducing insects because of the host-specificity of insect and host plant species (Carneiro et al. 2009, Bergamini et al. 2017), we described in this study the gall morphotypes with the register of the association between gall maker and their host plant species in a Seasonal Semideciduous Forest area in Sorocaba Municipality, the first survey to the Southeast region of São Paulo State, Brazil.

Material and Methods

1. Study area

The Seasonal Semideciduous Forest fragment of the sampling area is located on the campus of the Universidade Federal de São Carlos (UFSCar), located in the municipality of Sorocaba (47º 31 '28 "W and 23º 34' 53" S), Southeast region of São Paulo State, 580 m altitude and climate Cwa-Köppen classification. This area is located in the transition between the Planalto Atlântico and the São Paulo State Peripheral Depression. Among forest remnants, Cerrado elements are found in the flatter areas and Seasonal Semideciduous Forest in the areas closest to water bodies or slopes (Corrêa et al. 2014). The Sorocaba campus of UFSCar is 700,000 m² in size and has a vegetative mosaic composed by two typical phytophysiognomies of the region, the Seasonal Semideciduous Forest and the Cerrado, remaining of continuous forest before its exploration for economic activities (Fig. 1).

Figure 1 A. Localization of the Sorocaba Municipality in Southeast of São Paulo State; B. Aerial view of the Sorocaba campus of Universidade de São Carlos, Southeast of São Paulo State, Brazil, with reference of the fragments of the area sampled (FL, F1, F2, F3, F4, F5, F6). (Source: Google Earth, 2017). 

2. Sampling

The samplings of this study were carried out between the years 2014 to 2016, with seasonal frequency (trimonthly), in twelve samplings of four hour each, totalizing 48 hours of sampling effort. Branches of the host plants with galls were collected, pictured and placed for rearing in labeled plastic pots to obtain the adults of the associated fauna. All individuals obtained were preserved in 80% alcohol.

3. Treatment of the samples

The gall midges were mounted later on microscope slides following Gagné (1994) methodology. The cecidomyiids were identified using keys of Gagné (1994). Other arthropods and host plant species were sent to specialists for identification. The gall morphotypes were characterized according Isaías et al. (2013). The specimens of the associated fauna are deposited in the Laboratório de Sistemática de Diptera/UFSCar and the exsiccates of host plants with reproductive material will be deposited in Herbário UFSCar Sorocaba (SORO).

Results and Discussion

A total of 113 gall morphotypes were found in 54 species of 24 host family families in the remnants of Seasonal Semideciduous Forest in the Southeast of São Paulo State. The average of gall morphotypes per plant species is 2.1, a high average when compared with other areas with the same phytophysiognomy (Table 1) and comparable to dry environments (see Urso-Guimarães et al. 2017 for detailed discussion). The morphotypes are characterized in Table 2 and are presented in Figures 2 to 6.

Table 1 Richness of gall morphotypes in localities with Seasonal Semideciduous Forest phytophysiognomy. 

Locality Richness of gall morphotypes Richness of host plant species Average number of gall/host plant species
Sorocaba/Southeast SP (this study) 113 54 2.1
Altinópolis, SP (Ribeiro et al. – submitted Papéis Avulsos de Zoologia) 41 21 1.95
Serra da Bodoquena, MS
(Urso-Guimarães et al. 2017) 65 39 1.6
Maringá, PR (Carvalho et al. 2015)* 40 35 1.2
Goiânia, GO (Santos et al. 2010) 34 20 1.7

*In Carvalho et al. *(2015) the plant species were not identified and the morphotypes were not characterized, however we chose to include these data because it is one of the few works in the area of Seasonal Semideciduous Forest phytophysiognomy.

Table 2 Characterization of insect galls recorded in Sorocaba, Southeast of São Paulo State, Brazil by host plant. “Figure” refers to gall morphotype’s picture, and “-” refers to no pictured morphotypes. 

Host plant family Host plant species Organ Shape Color Pube-scence Figure
Anacardiaceae Lithraea molleoides (Vell.) Engl. Leaf Globoid Pink/Red/Green/Brown No 2A
Lithraea molleoides Stem Globoid Brown No 2B
Tapirira guianensis Aubl. Stem Globoid Cream No 2C
Tapirira guianensis Leaf Lenticular Green No 2D
Schinus terebinthifolia Raddi Leaf Marginal roll Red No 2E
Annonaceae Annona dioica A.St.-Hil. Leaf Globoid Cream No 2F
Duguetia furfuracea (A.St.-Hil.) Saff. Leaf Globoid Green Yes 2G
Apocynaceae Oxypetalum banksii R.Br. ex Schult. Leaf Lenticular Green/Brown No 2H
Condylocarpon sp. Stem Globoid Cream No 2I
Asteraceae Chromolaena laevigata (Lam.) R.M.King & H.Rob. Leaf Lenticular Brown No 2J
Bidens segetum Mart. ex Colla Leaf Lenticular Yellowish No 2K
Calea pinnatifida (R.Br.) Less. Stem Fusiform Green No 2L
Mikania sp. Leaf Globoid Green No 2M
Mikania sp. Leaf Lenticular Green No 2N
Moquiniastrum polymorphum (Less.) G. Sancho Leaf Lenticular Green/Yellowish/Brown No 2O
Moquiniastrum polymorphum Stem Fusiform Green/Brown No 2P
Bignoniaceae Bignoniaceae sp. Leaf Lenticular White No 2Q
Burseraceae Protium heptaphyllum (Aubl.) Marchand Leaf Conical Brown Yes 2R
Protium heptaphyllum Leaf Lenticular Brown No 2S
Protium heptaphyllum Leaf Globoid Brown Yes 2T
Protium heptaphyllum Leaf Globoid Green/Brown No 3A
Protium heptaphyllum Leaf Globoid Green No 3B
Protium heptaphyllum Leaf vein Fusiform Brown No 3C
Protium heptaphyllum Leaf vein Cylindrical with apical projection Brown No 3D
Protium heptaphyllum Stem Globoid Brown No -
Protium heptaphyllum Stem Fusiform Brown No 3E
Protium heptaphyllum Leaf/Stem Fusiform Green/Brown No 3F
Cannabaceae Celtis iguanaea (Jacq.) Sarg. Leaf Conical Green No 3G
Celtis iguanaea Stem Fusiform Brown No 3H
Celtis iguanaea Leaf Globoid Green No 3I
Caryocaraceae Caryocar brasiliense Cambess. Leaf Globoid Green No 3J
Celastraceae Hippocratea volubilis L. Leaf Lenticular Brown Yes 3K
Convolvulaceae Ipomoea sp. Stem Globoid Cream No 3L
Fabaceae Andira humilis Mart. ex Benth. Leaf Globoid Green No 3M
Bauhinia sp. Leaf Fusiform Green No -
Bauhinia forficata Link Stem Fusiform Brown No 3N
Bauhinia holophylla (Bong.) Steud. Leaf Globoid Green No 3O
Bauhinia holophylla Stem Fusiform Green No 3P
Bauhinia longifolia (Bong.) Steud. Leaf Globoid Green No 3Q
Bauhinia longifolia Stem Fusiform Brown No 3R
Calliandra foliolosa Benth. Stem Globoid Brown No 3S
Calliandra foliolosa Stem Fusiform Brown No 3T
Copaifera langsdorffii Desf. Leaf Lenticular Green/Yellowish/Brown No 4A
Copaifera langsdorffii Leaf Cylindrical Pink/Green/Brown No 4B
Copaifera langsdorffii Leaf Conical Brown No -
Copaifera langsdorffii Leaf Globoid White/Pink No -
Copaifera langsdorffii Leaf Globoid Black No 4C
Copaifera langsdorffii Leaf Globoid Green No -
Copaifera langsdorffii Leaf Globoid Green/Brown No -
Copaifera langsdorffii Leaf Globoid Cream Yes -
Copaifera langsdorffii Leaf Globoid Green No 4D
Copaifera langsdorffii Leaf vein/ Stem Globoid Brown No -
Copaifera langsdorffii Stem Fusiform Cream No -
Copaifera langsdorffii Stem Globoid Green No -
Copaifera langsdorffii Stem Globoid Green No -
Copaifera langsdorffii Stem Globoid Brown No -
Copaifera langsdorffii Stem Globoid Cream No 4E
Copaifera langsdorffii Stem Globoid Brown No 4F
Inga edulis Mart. Flower Amorphous Green No 4G
Lauraceae Nectandra grandiflora Ness Stem Globoid Cream No 4H
Persea sp. Leaf Globoid Green No 4I
Persea willdenovii Kosterm. Leaf Globoid Green No 4J
Malpighiaceae Diplopterys pubipetala (A.Juss.) W.R.Anderson & C.C.Davis Leaf Conical Green No 4K
Diplopterys pubipetala Leaf Lenticular Brown No 4L
Diplopterys pubipetala Stem Fusiform Brown No 4M
Byrsonima intermedia A.Juss. Leaf Lenticular Brown No 4N
Byrsonima intermedia Stem Globoid Cream No 4O
Janusia guaranitica (A.St.-Hil.) A.Juss. Leaf Globoid Green Yes 4P
Janusia guaranitica Stem Fusiform Brown No 4Q
Niedenzuella multiglandulosa (A.Juss.) W.R.Anderson Leaf Lenticular Green No -
Stigmaphyllon lalandianum A.Juss. Leaf Fusiform Brown No 4R
Stigmaphyllon lalandianum Leaf Conical Green No -
Stigmaphyllon lalandianum Leaf Conical Green No -
Stigmaphyllon lalandianum Leaf Concave Green No 4S
Stigmaphyllon lalandianum Leaf Lenticular Green No 4T
Stigmaphyllon lalandianum Leaf Lenticular Green No -
Stigmaphyllon lalandianum Leaf Lenticular Yellowish No -
Stigmaphyllon lalandianum Stem Fusiform Cream No -
Stigmaphyllon lalandianum Stem Fusiform Red No -
Stigmaphyllon lalandianum Stem Fusiform Brown No 5A
Stigmaphyllon lalandianum Stem Fusiform Green No 5B
Melastomataceae Miconia sp. Leaf vein Conical Brown No 5C
Miconia sp. Leaf Globoid Green No 5D
Miconia sp. Leaf Lenticular Cream No 5E
Miconia sp. Stem Globoid Brown No 5F
Meliaceae Trichilia sp. Leaf Lenticular Green/Brown No 5G
Myrtaceae Myrtaceae sp.1 Leaf Lenticular Brown No -
Myrtaceae sp.2 Stem Globoid Brown No 5H
Campomanesia sp. Leaf Lenticular Yellowish/Red/Brown No 5I
Eugenia bimarginata DC. Leaf Lenticular Brown/Red No 5J
Eugenia bimarginata Leaf Globoid Green No 5K
Eugenia pluriflora DC. Flower/Fruit Amophous Green No 5L
Eugenia pluriflora Leaf Cylindrical Cream/Red/Brown No 5M
Myrcia sp. Leaf Globoid Red No 5N
Myrcia sp. Leaf Marginal roll Green No -
Myrcia splendens (Sw.) DC. Leaf vein Globoid Green No 5O
Myrcia splendens Leaf Conical Green No 5P
Passifloraceae Passiflora pohlii Mast. Leaf Lenticular Green No 5Q
Passiflora crassifolia Killip Leaf Lenticular Green No -
Peraceae Pera glabrata (Schott) Poepp. ex Baill. Leaf Lenticular Green No 5R
Piperaceae Piper sp. Leaf Lenticular Green No 5S
Primulaceae Myrsine umbellata Mart. Leaf Globoid Brown No 5T
Myrsine umbellata Leaf Lenticular Green No 6A
Myrsine coriacea (Sw.) R.Br. ex Roem. & Schult. Stem Globoid Brown No 6B
Rutaceae Zanthoxylum riedelianum Engl. Leaf Lenticular Yellowish No 6C
Sapindaceae Serjania lethalis A.St.-Hil. Tendril Fusiform Green/Brown No 6D
Serjania lethalis Leaf Concave Green Yes 6E
Serjania lethalis Leaf Linear Green No 6F
Serjania lethalis Leaf Globoid Green No 6G
Serjania lethalis Leaf Lenticular Green/Brown/Black No 6H
Smilacaceae Smilax quinquenervia Vell. Leaf Globoid Green No 6I
Smilax cf. fluminensis Steud. Leaf Lenticular Green No 6J
Verbenaceae Aloysia virgata (Ruiz & Pav.) Juss. Leaf Globoid Green No 6K

Figure 2 Gall morphotypes of Sorocaba, Southeast of São Paulo State, Brazil by host plant. Anacardiaceae: A-B. Lithraea molleoides, C-D. Tapirira guianiensis, E. Schinus terebinthifolius. Annonaceae: F. Annona dioica, G. Duguetia furfuracea. Apocynaceae: H. Oxypetalum banksii, I. Condylocarpon sp. Asteraceae: J. Chromolaena laevigata, K. Bidens segetum, L. Calea pinnatifida, M-N. Mikania sp., O-P. Moquiniastrum polymorphum. Bignoniaceae: Q. Bignoniaceae sp. Burseraceae: R-T. Protium heptaphyllum. (Pictures: Ansaloni, L. S. and Salmazo, J. R.). 

Figure 3 Gall morphotypes of Sorocaba, Southeast of São Paulo State, Brazil by host plant. Burseraceae: A-F. Protium heptaphyllum. Cannabaceae: G-I. Celtis iguanaea. Caryocaraceae: J. Caryocar brasiliense. Celastraceae: K. Hippocratea volubilis, L. Ipomoea sp. Fabaceae: M. Andira humilis, N. Bauhinia forficata, O-P. Bauhinia holophylla, Q-R. Bauhinia longifolia, S-T. Calliandra foliosa. (Pictures: Ansaloni, L. S. and Salmazo, J. R.). 

Figure 4 Gall morphotypes of Sorocaba, Southeast of São Paulo State, Brazil by host plant. Fabaceae: A-F. Copaifera langsdorffii. G. Inga edulis. Lauraceae: H. Nectandra grandiflora, I. Persea sp., J. Persea willdenovii. Malpighiaceae: K-M. Diplopterys pubipetala, N-O. Byrsonima intermedia, P-Q. Janusia guaranitica, R-T. Stigmaphyllon lalandianum. (Pictures: Ansaloni, L. S. and Salmazo, J. R.). 

Figure 5 Gall morphotypes of Sorocaba, Southeast of São Paulo State, Brazil by host plant. Malpighiaceae: A-B. Stigmaphyllon lalandianum. Melastomataceae: C-F. Miconia sp. Meliaceae: G. Trichilia sp. Myrtaceae: H. Myrtaceae sp. 2, I. Campomanesia sp., J-K. Eugenia bimaginata, L-M. Eugenia pluriflora, N. Myrcia sp., O-P. Myrcia splendens. Passifloraceae: Q. Passiflora pohlii. Peraceae: R. Pera glabrata. Piperaceae; S. Piper sp. Primulaceae: T. Myrsine umbellata (Pictures: Ansaloni, L. S. and Salmazo, J. R.). 

Figure 6 Gall morphotypes of Sorocaba, Southeast of São Paulo State, Brazil by host plant. Primulaceae: A. Myrsine umbellata, B. Myrsine coriacea, Rutaceae: C. Zanthxylum riedelianum, Sapindaceae: D-H. Serjania lethalis. Smilacaceae: I. Smilax quinquenervia, J. Smilax cf. fluminensis. Verbenaceae: K. Aloysia virgata. (Pictures: Ansaloni, L. S. and Salmazo, J. R.). 

The morphotypes were obtained most frequently in leaves (70%) followed by stems (30%), flower bud (2%), tendril and fruit (1%). Three morphotypes occurred in more than one vegetal organ; the fusiform morphotypes on leaf and stem of Protium heptaphyllum, the globoid morphotype on leaf vein and stem of Copaifera langsdorffii, and the amorphous morphotype on flower and fruit of Eugenia pluriflora. Our results are slightly lower than other surveys conducted in different environments (Maia, 2001, Urso-Guimarães et al. 2003, Fernandes & Negreiros, 2006 Maia et al. 2008, Saito & Urso-Guimarães 2012, Maia & Carvalho-Fernandes 2016, Bergamini et al. 2017, Urso-Guimarães et al. 2017) where the percentage of leaf galls ranges from 75 to 90%. The shape of galls more frequent was globoid (42%) followed by lenticular (26%), fusiform (18%), conical (7%), cylindrical (3%), amorphous, concave and marginal roll (2% each), and linear (1%). The color more frequently sampled in galls were green (42%) and brown (27%), followed by cream (10%), red and yellow (3% each) with other colors appearing in less than 1%. Frequently there are changes of color along the development of gall and as observed in the most galls, it passes from green to brown. In Campomanesia sp., Eugenia pluriflora, Copaifera langsdorffii, Moquiniastrum polymorphum, and Serjania lethalis it was observed changing in three different colors during maturation process. Lithraea molleoides presented the largest color variation found on galls in this study: four different colors - pink, red, green, and brown. In relation to the pubescence and internal chambers, most galls were glabrous (94%) and unilocular (100%) (for detailed discussion about presence/absence of trichomae, see Saito & Urso-Guimarães, 2012). In the Table 2 are presented a detailed morphological description of the collected galls.

In a decreasing order of occurrence of galls morphotypes appear the Fabaceae (N = 26), followed by Malpighiaceae (N = 19), Myrtaceae (N = 11), Burseraceae (N = 10), Asteraceae (N = 7), Anacardiaceae and Sapindaceae (N = 5 each).

Information about richness of morphotypes of other families and species is given in Table 3. This study corroborates others in the Neotropical region that indicates the richest families as the richer in number of gall morphotypes (Gagné 1994, Araújo 2011, Santana & Isaias 2014). It's important to highlight the high number of morphotypes found in the same plant species (the super host plants sensu Veldtman & McGeoch 2003). The presence of super hosts increase the counting of morphotypes per family in the studied area, as related by Araújo (2011) to Goiânia (GO, Brazil) and Ribeiro et al. (submitted Papéis Avulsos de Zoologia) to Altinópolis (SP, Brazil). The presence of Copaifera langsdorffii with 16 morphotypes, Stigmaphyllon lalandianum with 11, Protium heptaphyllum with 10, and Serjania lethalis with five morphotypes in this study are examples of it. Protium heptaphyllum was referred before as super host in Maia & Fernandes (2004) and Copaifera langsdorffii in Oliveira et al. (2008), Fernandes et al. (1988) and Drummond et al. (2008), both from cerrado areas in Minas Gerais State.

Table 3 Richness of gall morphotypes in plant host family and species in Sorocaba, Southeast of São Paulo State, Brazil. 

Host Plant Families (N = 24) Morphotypes (N = 113) Number of species (N = 54)
Fabaceae 26 8
Malpighiaceae 19 6
Myrtaceae 11 7
Burseraceae 10 1
Asteraceae 7 5
Anacardiaceae 5 3
Sapindaceae 5 1
Melastomataceae 4 1
Cannabaceae 3 1
Lauraceae 3 3
Primulaceae 3 1
Annonaceae 2 2
Apocynaceae 2 2
Passifloraceae 2 2
Smilacaceae 2 2
Bignoniaceae 1 1
Caryocaraceae 1 1
Celastraceae 1 1
Convolvulaceae 1 1
Meliaceae 1 1
Peraceae 1 1
Piperaceae 1 1
Rutaceae 1 1
Verbenaceae 1 1

Most of the galls were found empty. Although only 12% of gall makers were obtained (Table 4), insects of the family Cecidomyiidae (Diptera) were responsible for the induction of 92% of galls (N = 11) and the order Hymenoptera (N = 1) for 8%. The other insects associated with galls (30%, N = 34) were considered parasitoids, successors or inquilines. As parasitoids were registered insects of the order Hymenoptera (N = 11) and as successors, the orders Hemiptera (N = 8), Acari (N = 7, Iphiseiodes zuluagai Denmark & Muma, Iphiseiodes saopaulus Denmark & Muma), Psocoptera (N = 4), Hymenoptera (Formicidae, N = 2), Collembola and Thysanoptera (N = 1 each). Two species of Cecidomyiidae with inquiline habit were also obtained, Neolasioptera sp. and Trotteria sp.

Table 4 Gall makers and associated fauna found in gall morphotypes in host plants from Sorocaba, Southeast of São Paulo State, Brazil. 

Host plant family Host plant species Gall maker Associated fauna Figure
Anacardiaceae Tapirira guianiensis Cecidomyiidae - 2D
Annonaceae Annona dioica Contarinia sp. or Prodiplosis sp. (Cecidomyiidae) Hemiptera 2F
Annonaceae Duguetia furfuracea Hymenoptera - 2G
Asteraceae Calea pinnatifida - Hymenoptera 2L
Asteraceae Mikania sp. - Hemiptera 2M
Asteraceae Moquiniastrum polymorphum - Hymenoptera/Acari 2O
Bignoniaceae Bignoniaceae sp. Cecidomyiinae (larva) Acari 2Q
Burseraceae Protium heptaphyllum - Psocoptera 2R
Burseraceae Protium heptaphyllum - Hemiptera 2T
Fabaceae Bauhinia longifolia Cecidomyiidae (larva) Psocoptera 3R
Fabaceae Callindra foliolosa Contarinia sp. (Cecidomyiidae) Hymenoptera 3T
Fabaceae Copaifera langsdorffii - Psocoptera/Hemiptera/Hymenoptera (Formicidae)/Acari 4D
Lauraceae Persea willdenovii - Hemiptera 4J
Malpighiaceae Byrsonima intermedia Asphondylia sp. (Cecidomyiidae) Hemiptera/Hymenoptera 4N
Malpighiaceae Stigmaphyllon lalandianum Contarinia (Cecidomyiidae) Hymenoptera/Collembola/Neolasioptera (Cecidomyiidae) 4S
Melastomataceae Miconia sp. Bruggmanniella sp. (Cecidomyiidae) Thysanoptera/Hemiptera/Hymenoptera 5C
Myrtaceae Myrtaceae sp.1 - Psocoptera -
Myrtaceae Eugenia pluriflora Cecidomyiinae Hymenoptera/Acari 5L
Myrtaceae Myrcia splendens Dasineura sp. (Cecidomyiidae) Hymenoptera 5O
Primulaceae Myrsine coriacea - Acari 6B
Sapindaceae Serjania lethalis - Trotteria (Cecidomyiidae)/Hymenoptera/Acari 6D
Smilacaceae Smilax quinquenervia - Hymenoptera/Acari 6I
Verbenaceae Aloysia virgata Cecidomyiidae Hemiptera 6K

This is the first survey of the association of gall, gall makers, host plants and associated fauna in Seasonal Semidecidual Forest to the Southeast of the State of São Paulo. In addition to the associations, five plant species were registered as hosts for cecidomyiids for the first time: Aloysia virgata, Calliandra foliolosa, Myrcia splendens, Serjania lethalis and Tapirira guianiensis. In the Southeast of the State of São Paulo there are several areas preserved in Conservation Units (UC), but the majority is dedicated to the protection of Dense Ombrophylous Forest vegetation. Few fragments of Seasonal Semideciduous Forest are included in that Conservation Units. Studies like this are still essential for the registration of host plants that may be at risk of extinction as well as the entire trophic network dependent on them in Seasonal Semideciduous Forest environments, a priority area for conservation in Atlantic Forest Biome, due to the biological richness and the fast degradation in recent years to economic activities in the Southeast region of Brazil, as stated to Martins et al. (2003).

Acknowledgments

The authors acknowledge Dr. Ingrid Koch (Unicamp), MSc. Ana Carolina Devides Castello (Unesp/Botucatu) and MSc. Ana Laura Scudeler (Unesp/Botucatu) for the identification of botanical species, Dr. Gilberto José de Moraes (Esalq/USP) for the identification of Acari species, and CNPq by scientific initiation grant of Leticia Salvioni Ansaloni (PIBIC/CNPq Proc. #102480/2015-0) and Julia Rodrigues Salmazo (PIBIC/CNPq Proc. #101881/2015-0).

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Received: February 04, 2018; Revised: April 05, 2018; Accepted: June 21, 2018

*Corresponding author: Maria Virginia Urso Guimarães, e-mail: mvirginiaurso@gmail.com

Author Contributions

Leticia Salvioni Ansaloni - Contribution in the: concept of the study; data collection; data analysis and interpretation; manuscript preparation, contribution to critical revision, adding intellectual content.

Julia Rodrigues Salmazo - Contribution in the: data collection; data analysis and interpretation; contribution to critical revision.

Maria Virginia Urso Guimarães - Contribution in the: concept and design of the study; data collection; data analysis and interpretation; manuscript preparation, contribution to critical revision, adding intellectual content.

Conflicts of interest

The authors declare that they have no conflict of interest related to the publication of this manuscript.

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