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

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.

Sampling and analysis of the material
Five samplings were carried out in the area from March 2000to 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
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).
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.
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.
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.
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.

Figure 1 .
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).

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

Table 3 .
Richness of gall morphotypes from localities with Seasonal Semideciduous Forest and Cerrado phytophysiognomies in Northeastern São Paulo State.
Carvalho et al., 20152015were 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.

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

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.