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

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.

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 , 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.

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).

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.

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.
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, 2006Maia 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.
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  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. 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) 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.
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).