Checklist of host plants of insect galls in the state of Goiás in the Midwest Region of Brazil

Abstract Background Surveys of host plants of insect galls have been performed in different regions of Brazil. The knowledge of species of host plants of insect galls is fundamental to further studies of plant-galling insect interactions. However, a list of host plant species of gall-inducing insects has not yet been compiled for the flora of the Midwest Region of Brazil. New information We provide a compilation of the plant species reported to host insect galls in the Cerrado of the state of Goiás in the Midwest Region of Brazil. Altogether we found records for 181 species of 47 families of host plants, which hosted 365 distinct gall morphotypes.


Introduction
Insect galls are structures formed by the development of larvae or nymphs in the interior of plant tissues (Mani 1964, Rohfritsch 1982, Stone and Schönrogge 2003. Galls develop by hypertrophy and hyperplasia of the plant cells, which changes all of the structure of the attacked plant organ (Moura et al. 2008). Because of the intimate level of interaction between gall-inducing insects and their host plants at histological and cellular scale, these insects are considered the most specialized guild of herbivores (Stone and Schönrogge 2003, Carneiro et al. 2009, Fernandes and Santos 2014. Due to this high degree of specialization, knowledge regarding the identity of host plant species is fundamental to studies of plant-galling insect interactions. It is already known that there exists a high diversity of insect galls in the Neotropics (Gagné 1994, Fernandes andSantos 2014), mainly in the savannas located in central Brazil (Araújo et al. 2014b). A likely explanation for this is the great diversity of plants in the region (Espírito-Santo and Fernandes 2007), since richness of host plants is an important factor in explaining the distribution patterns of insect galls (Araújo et al. 2014b). Considering that each species of plant is a potential host for galling, a greater local and regional diversity of plant species implies greater galling species richness (Mendonça 2007). Several studies in Brazil have produced local and regional lists of host plant species and their associated galls, especially in the South and Southeast regions (e.g. Gonçalves-Alvim and Fernandes 2001, Maia and Fernandes 2004, Mendonça 2007, Maia et al. 2008, Bregonci et al. 2010, while in other regions, such as the Midwest, surveys are still scarce (Araújo et al. 2013). In the present work, we provide a compilation of plant species that have been recorded to host insect galls in the state of Goiás in the Midwest Region of Brazil.

Material and methods
We compiled data from different surveys of plant species that are hosts of insect galls from several locations in the state of Goiás in the Midwest Region of Brazil (Fig. 1). We also included data from the Distrito Federal, which is a separate political entity, but is surrounded by the state of Goiás. All records of hosts and galls were collected between 2005 and 2013 in different types of vegetation that comprise the Cerrado biome (Table 1). We included data published in local checklists (e.g. Santos et al. 2010, Araújo et al. 2011, Araújo et al. 2014a) as well as unpublished data. The identification of the plants was made by comparison with the collections of Universidade Federal de Goiás, herbarium, literature, as well as consultation with specialists. We checked the synonymy using The Plant List database (www.theplantlist.org). In addition to the list of host plants, we provide a short morphological characterization of gall morphotypes (plant organ, gall form and gall color) associated with each host plant species. The use of gall morphotypes is a commonly used and reliable parameter because evidence indicates that each gall morphospecies (examples in Fig. 2) is unique to a particular gall-inducing insect (Stone and Schönrogge 2003), and each galling species is specific to a particular host plant (Abrahamson et al. 1998). Insect galls can be differentiated from galls induced by other organisms, such as mites and nematodes, because they form an internal chamber where the immature insect develops (see Fig. 2f). Furthermore, insect galls are relatively large structures (in cm scale) and usually closed (internal chamber has no opening to the outside), unlike other galls induced by animals. Insect galls were collected and taken to laboratory where they were dissected to obtain the immature and adults gall-inducing insects. It was not our objective to list the species (or taxa) of the gall-inducing insects responsible for the galls observed in the plants of our survey. For details about galling insect taxa associated with each host plant species the original studies should be consulted.

Results
We recorded a total of 181 species of 47 families of plants that host insect galls in the state of Goiás (Table 2). Seventy-three (40.3%) plant species are registered as gall hosts for the first time to Goiás. Associated with plant species were 365 gall morphotypes, of which 192

Discussion
We have systematically compiled the results of studies on plant species that host insect galls in the Cerrado of the state of Goiás for the first time, which resulted in new records of 73 (40.3%) plant species and 173 (47.4%) gall morphospecies. Our results corroborate previous studies that indicate Fabaceae as the plant family that hosts the greatest diversity of galling insects in the Neotropical Region (Gagné 1994, Maia and Fernandes 2004, Araújo et al. 2014b, Fernandes and Santos 2014. Local studies in different regions of Brazil found the same pattern (Gonçalves-Alvim and Fernandes 2001, Santos et al. 2010, Araújo et al. 2011, Araújo et al. 2013, Araújo et al. 2014a. Fabaceae is the most diverse plant family of the Cerrado with nearly 800 species, and so it is not surprising that it hosts the highest diversity of insect galls (Araújo et al. 2014b).
We found that Byrsonima, Qualea and Myrcia were the genera hosting the greatest number of gall morphotypes. These results differ from that observed in other regions of Brazil. For example, Mendonça 2007] found the genera Mikania (Asteraceae), Eugenia (Myrtaceae) and Guapira (Nyctaginaceae) to host the greatest diversity of galls in the state of Rio Grande do Sul in Southern Brazil. In the Brazilian Southeast, the genera Myrcia (Myrtaceae), Ocotea (Lauraceae) and Paullinia (Sapindaceae) hosted the most diversity of galls in the state of São Paulo (Maia et al. 2008), while Baccharis (Asteraceae) hosted the greatest richness of galls in state of Minas Gerais (Fernandes et al. 1996). With regards to host plant species, some species stand out as super-hosts of insect galls in Goiás, such as Byrsonima pachyphylla, Protium heptaphyllum, Qualea parviflora and Styrax pohlii. In a previous study, Maia and Fernandes 2004]  To maintain this high gall diversity it is essential that the remaining fragments of Cerrado are preserved and retain a high diversity of native plants (Araújo et al. 2014b). In the state of Goiás, areas of native vegetation are very small and the majority is widely fragmented (Cunha et al. 2007). Given the eminent risk of destruction of the remaining vegetation, inventories of host plants and their associated insect galls are urgently needed to provide a foundation for further understanding these interactions. We hope that this compilation can serve as an important tool for gall inventories and provide a theoretical reference for new studies in the state of Goiás and in all of Brazil.

Author contributions
WSA, BAR, TMS, ECS, FAGG, CSS and BBS collect data in field and help in data compilation. WSA created the map and formated the figures. WSA and EDPJ wrote the manuscript. All authors read the manuscript and contributed with suggestions.