Insect gall occurrence in savanna and forest remnant sites of Hidrolândia , GO , Brazil Central

In this study we perform an inventory of the insect galls in savanna and forest sites of Hidrolândia, Goiás, Brazil. We found 150 insect gall morphotypes, distributed on 39 botanical families and 104 plant species. Among the insect galls, 81 gall morphotypes were recorded in the savanna site and 73 in the forest site. The plant taxa richest in insect galls were the family Fabaceae with 22 gall morphotypes, the genus Bauhinia (Fabaceae) with 15, and the species Siparuna guianensis (Siparuna‐ ceae) with seven gall morphotypes. We found gall‐inducing insects belonging to orders Diptera, Coleoptera, Lepidoptera and Thysanoptera. The galling insects of family Cecidomyiidae (Diptera) were the most common inducing 48.1% of the gall mor‐ photypes. This is the first systematic survey of insect galls realized in the city of Hidrolândia, being this the site with the higher insect gall diversity already cataloged to the Central region of Brazil. Key-Words. Cerrado; Fabaceae; Host plants; Insect galls; Plant‐insect interaction.


INTRODUCTION
Galls are abnormal modifications in the vegetal tissues induced mainly by galling insects, and characterized by hypertrophy and hyperplasia of plant cells (Mani, 1964;Shorthouse & Rohfritsch, 1992).From an evolutionary point of view, insect galls are extended phenotypes of the gall-inducers (Stone & Schönrogge, 2003), which leads to each species of galling insect induces a specific morphotype of gall on their host plant (Carneiro et al., 2009a).Galls and galling insects are widely distributed around the globe, especially in the Neotropical region (Espírito-Santo & Fernandes, 2007).In the Neotropics stand out Amazon (Julião et al., 2014), Atlantic Forest (Santos et al., 2014) and Cerrado (Araújo et al., 2014a) as hotspots of insect gall diversity.
The Brazilian Cerrado is composed by a wide variety of vegetation types (Ribeiro & Walter, 2008), and one of the richest floras of Brazil and in the world (Klink & Machado, 2005;Mendonça et al., 2008).This great structural and floristic diversity is one of the main explanations for the high insect gall diversity in the Cerrado (Araújo et al., 2014a).In this sense, although the number of insect gall studies in the Cerrado has been growing in the recent years (Araújo et al., 2014a), evidence points that there are still temporal and spatial gaps in the group sampling (e.g., Araújo, 2011;Maia et al., 2014).
To the Central Brazil, insect gall inventories have been published only to the following localities: Caldas Novas (Santos et al., 2012), Goiânia (Santos et al., 2010;Silva et al., 2015), Parque Estadual da Serra dos Pireneus (Araújo et al., 2011), and Parque Nacional das Emas (Araújo et al., 2014b).Given these gaps in knowledge of insect galls in the Central Brazil, in the present study we perform an inventory of the insect galls and their host plants in sites of savanna and forest in Hidrolândia, Goiás, Central Brazil.

MATERIALS AND METHODS
The study was realized in the Escola Agrícola (EA) of the Centro de Formação Agroecológico de Hidrolândia (CEFAEH) in the city of Hidrolândia, State of Goiás, Central Brazil (17°00'56"S, 49°12'00"W; Fig. 1).The climate of region is classified as Aw of Köppen, being humid tropical with wet summer and dry winter.EA-CEFAEH has an area of approximately 40 hectares, most covered by natural vegetation with some level of human disturbance.The area is under Cerrado domain being characterized by several vegetation types, such as grasslands (e.g., Rocky Field), savannas (e.g., Cerrado Sensu Stricto or Neotropical savanna) and forests (e.g., Semidecidual Forest and Gallery Forest) (Ribeiro & Walter, 2008).
The sampling was done monthly between September 2011 and May 2012 in two vegetation remnants being one of Cerrado Sensu Stricto (hereafter called savanna; 17°01'05"S; 49°11'49"W) and other of Semidecidual Forest (hereafter called forest; 17°00'42"S; 49°12'04"W).We performed the collect of insect galls along two transects (one in each vegetation type) sampled by two hours (Araújo et al., 2011).All host plants had their epigeous parts inspected and all observed insect galls were registered.Samples of each insect galls were photographed, collected and transported individually in labeled plastic bags.
The collected insect galls were taken to the laboratory of Universidade Federal de Goiás (UFG) and packed in plastic container with moistened paper.Insect galls were identified in morphotypes using the host plant species and the gall characteristics (organ of occurrence, form, color, pubescence, and size).In laboratory, the galls were daily observed to verify the emergence of adult insects or dissected to obtainment of immature insects.All obtained insects were fixed in 70% alcohol and identified using the insect gall literature to Neotropics and Brazil (e.g., Gagné, 1994;Maia & Fernandes, 2004, Araújo et al., 2011).The identification of the host plant species was made by comparison with the collection of UFG herbarium.We checked plant species nomenclature and synonymy using The Plant List (http://theplantlist.org).

RESULTS AND DISCUSSION
We found 150 insect gall morphotypes distributed on 39 botanical families and 104 plant species in the EA-CE-FAEH (Table 1).Previous studies that inventoried the insect gall diversity in the Cerrado sites ranged from 22 (Urso- Guimarães et al., 2003) to 241 (Carneiro et al., 2009b) gall morphotypes.The insect gall richness recorded in the present study is almost twice of 86.8 morphotypes, which is the average number of gall morphotypes recorded in the different surveys performed in the Brazilian Cerrado (review in Araújo et al., 2014a).For studies in Central region of Brazil, the insect gall richness in the EA-CEFAEH exceeds all previously cataloged sites (Table 2), as for example, the Parque Nacional das Emas that had 97 gall morphotypes recorded (Araújo et al., 2014b).Additionally, the average number of gall morphotypes per host plant species was of 1.44 in the present study, which was very similar to mean of 1.5 listed to Cerrado (Araújo et al., 2014a).These variations in the number of insect gall morphotypes and galls per plant species can be explained by differences in the sampling efforts and number of sampled host plants in the different inventories.
The plant families richest in insect galls were Fabaceae, with 22 gall morphotypes, Malpighiaceae with 13, Sapindaceae with 11, and Erythroxylaceae and Myrtaceae with nine gall morphotypes each (Table 1).Our results are according to previous studies that point Fabaceae as the most important host family of insect galls in the Cerrado (e.g., Maia & Fernandes, 2004;Santos et al., 2010;Araújo et al., 2011;Santos et al., 2012;Silva et al., 2015).The main explanation for the high insect gall richness hosted by Fabaceae in the Cerrado is its high species number (Southwood, 1960(Southwood, , 1961;;Araújo et al., 2014a) of nearly 800 (Mendonça et al., 2008).Malpighiaceae and Myrtaceae also frequently appear in the ranking of insect gall host families most important of Cerrado (Araújo et al., 2014a).
In this study we found gall-inducing insects belonging to orders Diptera, Coleoptera, Lepidoptera and Thysanoptera (Table 4).The Figs. 2-8 illustrates the gall morphotypes induced by galling insects.The most common galling taxon was Cecidomyiidae (Diptera), which induced 48.1% of the insect gall morphotypes.Galling insects of other taxonomic groups were much less frequent (only 7.2%), while from 44.7% of the insect gall morphotypes we did not find taxa of gall-inducers.Our results corroborate previous studies in the Brazilian savannas that point the dominance of Cecidomyiidae (Maia & Fernandes, 2004;Santos et al., 2010;Araújo et al., 2011), which is considered the main galling insect group of world (Gagné, 2010).The high cecidomyiid diversity in the Cerrado is hypothesized to be due to richest flora and the strongly opportunistic adaptive radiation of group (Araújo et al., 2014a).Besides of gall-inducing insects, we also record several hymenopteran parasitoids from families Braconidae, Encyrtidae, Eulophidae, Eurytomidae, Pteromalidae and Torymidae.Hymenopteran parasitoids are very frequently in Neotropical insect galls (Fernandes & Santos, 2014) and are the main natural enemies of Cecidomyiidae (Maia & Azevedo, 2009).
Of the 150 insect gall morphotypes recorded in our study, 81 were recorded in the savanna site and 73 in the forest site.Only the globoid gall morphotype (Gall 18) recorded on Caryocar brasiliense (Caryocaraceae), the conical gall morphotype (Gall 76) of Diplopterys Table 1.Number of host plant species and insect gall morphotypes in the host plant families recorded in EA-CEFAEH, Hidrolândia, Goiás, Brazil.     in mesics (although it was not the objective of the work to test statistically these differences).Among the possible explanations to this pattern are that in xeric environments the plants are more nutritive to galling insects and the attack frequency of natural enemies (e.g., parasitoids) is lower as compared to mesic habitats, as predicted by hydrothermal stress hypothesis at community level (Fleck & Fonseca, 2007;Araújo et al., 2014a).

CONCLUSIONS
This is the first systematic survey of insect galls realized in the EA-CEFAEH and region of Hidrolândia city.Although the study area is relatively anthropized and little fragments, the sampled sites presented great insect gall richness as compared to other sites cataloged to the Central region of Brazil.The EA-CEFAEH area had more insect gall morphotypes than the Parque Estadual da Serra dos Pireneus (62, Araújo et al., 2011) and Parque Nacional das Emas (97, Araújo et al., 2014b).Despite the possible effects of sampling effort differences between these studies, as previously discussed, our results show that any vegetation fragment can be a potential shelter to conserve insect galls.Finally, the observed results about host plant taxa, galling insect groups, gall morphology and occurrence between vegetation types confirm the known patterns of Brazilian Cerrado.

Table 2 .
Comparison between the insect gall surveys performed in different areas of Brazil Central.