An overview of inventories of gall-inducing insects in Brazil: looking for patterns and identifying knowledge gaps

ARAÚJO, WALTER S. DE; FERNANDES, GERALDO W.; SANTOS, JEAN C.

doi:10.1590/0001-3765201920180162

Abstract

We compiled published Brazilian gall-inducing insect inventories aiming to understand trends and biases in this field research and to investigate the factors that potentially explain the diversity of gall-inducing insects among different sampling sites. A total of 51 studies with gall-inducing insect inventories were compiled for Brazil, which sampled 151 sites in 88 municipalities, 13 states and five regions. The number of papers published on gall-inducing insects per year has increased over the last 30 years, being Cecidomyiidae (Diptera) the main galling taxon, Fabaceae the main host-plant family and Protium heptaphyllum (Burseraceae) the most important super-host species in these inventories. We found a great bias in the geographical distribution of Brazilian inventories, with the majority of studies in the Southeast region, and Atlantic Forest and Cerrado biomes. The total richness of gall-inducing insects differed significantly among regions and biomes, with higher gall richnesses being recorded in the North region and Amazon biome. However, Brazilian regions and biomes did not vary in richness of gall-inducing insect morphotypes per plant species. According our results, sampling by cecidologists in less studied regions of Brazil is needed, particularly in the North and South regions and subsampled biomes such as the Amazon, Pampas and Pantanal.

Key words
Atlantic Forest; Cecidomyiidae; Cerrado; Fabaceae; gall-inducing insects

INTRODUCTION

Brazil is a mega-diverse country in terms of biodiversity (Lewinsohn and Prado 2005LEWINSOHN TM and PRADO PI. 2005. How many species are there in Brazil? Conserv Biol 19: 619-624.). Estimates suggest that Brazil possesses the richest flora of the world with about 40,000 species, almost 19,000 (46%) of which are endemic (Forzza et al. 2012FORZZA RC et al. 2012. New Brazilian Floristic List Highlights Conservation Challenges. BioScience 62: 39-45.). This high number of plant species represents a great diversity of potential niches for gall-inducing insects (Fernandes 1992, Mendonça 2007MENDONÇA JR MS. 2007. Plant diversity and galling arthropod diversity searching for taxonomic patterns in an animal-plant interaction in the Neotropics. Bol Soc Argent Bot 42: 347-357.). Galling insects are very specialized herbivores known to be highly specific to their host plants (Mani 2013MANI MS. 2013. Ecology of plant galls. New York, Springer, 434 p., Stone and Schönrogge 2003STONE GN and SCHÖNROGGE K. 2003. The adaptive significance of insect gall morphology. Trend Ecol Evol 18: 512-522.). Estimates of the global richness of gall-inducing insects point to approximately 133,000 species, with most of them occurring in the Neotropical region (Espírito-Santo and Fernandes 2007ESPÍRITO-SANTO MM and FERNANDES GW. 2007. How many species of gall-inducing insects are there on earth, and where are they? Ann Entomol Soci Am 100: 95-99.). The great richness of flora and number of gall-inducing insects that they can potentially host has resulted in a large number of studies inventorying insect gall diversity in Brazil in recent decades.

Inventories of gall-inducing insects have been performed in Brazil since the 1980’s. For example, in a pioneering study Fernandes et al. (1988)FERNANDES GW, COSTA-ARAUJO R, ARAUJO S, LOMBARDI JA, SILVA DE PAULA A, JÚNIOR RL and CORNELISSEN TG. 1997. Insect galls from savanna and rocky fields of the Jequitinhonha Valley, Minas Gerais, Brazil. Naturalia 22: 221-244. investigated the occurrence of gall-inducing insects in Cerrado vegetation of the Pampulha Campus in Minas Gerais State, recording 37 insect galling species on 22 host plant species. More recently, Urso-Guimarães et al. (2017)URSO-GUIMARÃES MV, CASTELLO ACD, KATAOKA EY and KOCH I. 2017. Characterization of entomogen galls from Mato Grosso do Sul, Brazil. Rev Bras Entomol 61: 25-42. performed inventories in four biomes in Mato Grosso do Sul State (Atlantic Forest, Cerrado, Chaco and Pantanal), recording a total of 186 insect galling species on 115 host plant species. These studies illustrate that during the last few decades many inventories have been published for several regions and biomes of Brazil. Inventories of gall-inducing insects performed in Brazil represent a good proportion of the scientific production about insect galls in Latin America (Grandez-Rios et al. 2015GRANDEZ-RIOS JM, GARCÍA-VILLACORTA R, CUEVAS-REYES P and ARAÚJO WS. 2015. Insectos inductores de agallas en América Latina: ecología, importancia y nuevas perspectivas. Rev Biol Neotrop 12: 92-103.).

Interest about gall-inducing insects has promoted great contributions to the ecological and evolutionary understanding of insect-plant interactions (Araújo et al. 2014aARAÚJO WS, SANTOS BB, GUILHERME FAG and SCARELI-SANTOS C, 2014a. Galling insects in the Brazilian Cerrado: Ecological patterns and perspectives. In: Santos JC, Fernandes GW (Eds), Neotropical Insect Galls, New York, Springer Netherlands. p. 257-272.), and also in applied areas such as agriculture, biological control and nature conservation (Grandez-Rios et al. 2015). Studies in galling insect ecology have clarified community structure throughout three trophic levels: host plants, herbivores as well as their natural enemies (Mendonça 2007MENDONÇA JR MS. 2007. Plant diversity and galling arthropod diversity searching for taxonomic patterns in an animal-plant interaction in the Neotropics. Bol Soc Argent Bot 42: 347-357., Araújo et al. 2014a). Research advances have also provided basic information for applied ecology, for example, in the agriculture and biological control due many gall-inducing insects attacks cultivated plants (Grandez-Rios et al. 2015) and in the conservation of natural areas, because galling insects can be used as biological indicators of habitat quality (Moreira et al. 2007MOREIRA RG, FERNANDES GW, ALMADA ED and SANTOS JC. 2007. Galling insects as bioindicators of land restoration in an area of Brazilian Atlantic Forest. Lundiana 8: 107-112., Araújo et al. 2014a).

Despite the growing number of gall-inducing insect inventories in Brazil, there is no compilation of the main trends and patterns of this research. Therefore, the aim of the present study was to understand the trends and biases among Brazilian galling insect inventories to better evaluate whether efforts have been well applied and to identify future challenges for Brazilian cecidologists. Thus, this study seeks to answer the following questions: (1) How are inventories distributed among Brazilian geographic regions and biomes? (2) Is there a temporal trend in the number of studies published on the topic? (3) Which taxa of host plants and galling insects are most frequently recorded among Brazilian inventories? (4) Do latitude and elevation affect the diversity of gall-inducing insects? and (5) Does gall-inducing insect diversity vary among Brazilian regions, biomes, and vegetation types?

MATERIALS AND METHODS

Gall-inducing insect inventories performed in Brazil were compiled from papers published between 1988 and 2017. Papers were considered inventories only if they possessed data collected in the field that included sampling of the community of host plants. Inventories were included in the compilation only when it was explicitly indicated that the study was fully or partially performed within the territory of Brazil. To give an overview of trends with Brazilian gall-inducing insect inventories, papers were classified by location (Brazilian region, state and city), habitat (biome and vegetation type), host plant taxa (super-host families and species) and gall-inducing insect taxa (proportion of gall-inducing insects induced by Cecidomyiidae), according to the content and descriptions provided by the cecidologists or taxonomists. Inventories carried out in more than two locations or habitats were included under each involved. All compiled inventories were performed in natural vegetation, but the vegetation sampled varied in the state of conservation.

The total richness of gall-inducing insects and the richness of gall morphotypes per plant species were used as variables of insect gall diversity. These variables were analyzed per sampling site (and not per paper) because many inventories were performed in several sample sites simultaneously (e.g., Fernandes et al. 2001FERNANDES GWA, TAMEIRÃO-NETO E and MARTINS RP. 1988. Ocorrência e caracterização de galhas entomógenas na vegetação do campus Pampulha da Universidade Federal de Minas Gerais. Rev Bras Zool 5: 11-29., Santos et al. 2011aSANTOS JC, ALMEIDA-CORTEZ JS and FERNANDES GW. 2011a. Diversity of gall-inducing insects in the high altitude wetland forests in Pernambuco, Northeastern Brazil. Braz J Biol 71: 47-56., Urso-Guimarães et al. 2017). Sampling sites were considered as different when it was explicitly indicated by the authors that sampling was done in distinct and discontinuous areas and/or distinct phytophysiognomies (from the availability of geographic coordinates), and also when the gall-inducing insects and the host plants were presented separately for each site. When it was indicated that different points were sampled within the same sampling area (e.g., conservation unit), and/or geographical coordinates that allowed the spatial differentiation of points were not provided, sampling was considered, for the purposes of this study, to have been performed at only one sampling site.

The temporal trend in the number of publications including gall-inducing insect inventories per year in Brazil was evaluated using Pearson correlation. Spearman rank correlations were used to relate gall-inducing insect variables (total richness of gall-inducing insects and the richness of gall morphotypes per plant species) with latitude and elevation of each sampling site. These variables were obtained from descriptions provided by the authors or, when absent, from the coordinates of the municipality where the sampling site was located. Coordinates were converted to decimal degrees using the online converter available at https://www.latlong.net/. Additionally, gall-inducing insect variables were contrasted among regions, biomes, and vegetation types using Kruskal-Wallis tests. For a better visualization of the results, data are presented in the text as mean ± SD (standard deviation).

RESULTS

A total of 51 studies on gall-inducing insect inventories were compiled for Brazil (Table I), which sampled 151 sites in 88 municipalities, 13 states and five regions (Figure 1). The number of papers published on gall-inducing insects per year has increased over the last 30 years (RP_earson = 0.628; N = 19; P < 0.01; Figure 2). Most Brazilian inventories were for the Southeast (58.8%), Midwest (15.6%) and Northeast (15.6%) regions, and for Minas Gerais (33.3%) and Rio de Janeiro (19.6%) states. The Atlantic Forest and Cerrado were the most studied Brazilian biomes, with 23 and 22 studies, respectively.

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TABLE I
Inventories of gall-inducing insects realized in Brazil between 1988 and 2017.

Figure 1
Distribution of sites where gall-inducing insects were sampled in different biomes and regions in Brazil. At this map scale some of sites are located so close to another that they are indistinguishable.

Figure 2
Temporal trends (1988-2017) in publications on gall-inducing insect inventories performed in Brazil.

The number of insect gall morphotypes ranged from 22 to 432 species (109.6 ± 75.7), and the number of host plants from 14 to 255 species (63.3 ± 47.7). The mean number of insect gall morphotypes per plant species was 1.72 (± 0.43), ranging between 1.16 and 3.50. The richness of gall-inducing Cecidomyiidae (Diptera) ranged from 5 to 301, and represented between 14.3% and 97.8% of the gall-inducing insects cited in the Brazilian insect gall inventories (Table I). Fabaceae was the most important plant family in the Brazilian inventories, appearing as a super-host in 68.6% of the studies, and as having the greatest gall-inducing insect richness in 22 studies (Table I). Myrtaceae and Asteraceae were also important host families, being super-hosts in 49.0% and 37.2% of the studies, and most diverse in eight studies each. The most frequent species listed as super-host plants were Protium heptaphyllum (Burseraceae) and Copaifera langsdorffii (Fabaceae), which were recorded in seven (13.7%) and six (11.7%) studies, respectively.

The total richness of gall-inducing insects and the richness of insect gall morphotypes per plant species were not influenced by latitude or elevation (all R_pearman values < 0.20 and P values > 0.05; Figure 3). On the other hand, the total richness of gall-inducing insects differed significantly among regions (H = 13.807; N = 74; P < 0.01), and biomes (H = 8.333; N = 87; P < 0.02). The highest gall richnesses were recorded in the North region (Figure 4a) and Amazon biome (Figure 4b), both with 181.2 (± 107.0) gall morphotypes. However, Brazilian regions and biomes did not vary in the richness of gall-inducing insect morphotypes per plant species (P values > 0.05; Figure 4c and 4d, respectively). Similarly, the gall-inducing insect variables did not differ among vegetation types (P > 0.05).

Figure 3
Effect of latitude and altitude on the gall-inducing insect richness total and per plant species.

Figure 4
Comparison of the gall-inducing insect richness total and per plant species between different regions and biomes in Brazil.

DISCUSSION

The results obtained from the compilation of Brazilian gall-inducing insect inventories reveal important trends and biases. First, there was a significant positive trend in the number of papers published in the country, especially over the last decade. This result is likely a direct consequence of the intensive effort of several researchers to gather data on the biodiversity of insect galls, mainly as a result of the establishment of the Brazilian Symposium on Galls and Gallers (in Portuguese: Simpósio Brasileiro sobre Galhas e Galhadores), which has been held biannually at the Brazilian Congress of Zoology (since 2012). These efforts have resulted in a broadening of gall-inducing insect sampling in different Brazilian regions, with almost all of the studies carried out in the Southeast region of Brazil being published in the last 10 years (see Table I). This large and growing number of insect gall inventories confirms the Brazil as the most important research center about gall-inducing insects in Latin America and one of the most important in the world. This result is in agreement with Grandez-Rios et al. (2015), which argue that Brazil is responsible for about 70% of Latin American scientific production on gall-inducing insects.

A significant geographical bias can be observed among the Brazilian gall-inducing insect inventories. Although inventories have been performed in all the five Brazilian regions, the greatest number has been in the Southeast region (30), with three times the number of studies in the Midwest and Northeast regions (eight studies each). This pattern is due to the Southeast region being the first (chronologically) to be sampled, while at the same time housing the first research centers focusing on gall-inducing insects in Brazil (Universidade Federal de Minas Gerais and Universidade Federal do Rio de Janeiro, respectively). This geographical bias is confirmed by the fact that 33.3% and 19.6% of the published inventories were performed in the states of Minas Gerais and Rio de Janeiro, respectively. The gall-inducing insect diversity of the North and South regions and several Brazilian states remains subsampled or completely unknown.

Most of the Brazilian gall-inducing insect inventories were performed in the Atlantic Forest and Cerrado biomes, which are relevant global biodiversity hotspots (Myers et al. 2000MYERS N, MITTERMEIER RA, MITTERMEIER CG, FONSECA GA and KENT J. 2000. Biodiversity hotspots for conservation priorities. Nature 403: 853-858.). Estimates indicate that more than 14,000 vascular plant species occur in the Atlantic Forest (Stehmann et al. 2009) and 12,000 in the Cerrado (Mendonça et al. 2008MENDONÇA RC, FELFILI JM, WALTER BMT, SILVA-JÚNIOR MC, REZENDE AV, FILGUEIRAS TS, NOGUEIRA PE and FAGG CW. 2008. Flora vascular do bioma cerrado: checklist com 12.356 espécies. In: Sano SM, Almeida SP and Ribeiro JF (Eds), Cerrado: ecologia e flora Volume 2, Brasília: Embrapa Cerrados, p. 422-442.), with these biomes also being considered hotspots of gall-inducing insect diversity (Araújo et al. 2014a, Santos et al. 2014SANTOS JC, COELHO MS, SOUZA DG and FERNANDES GW. 2014. Galls from Brazilian Atlantic Forest: Status of Knowledge and Perspectives. In: Santos JC and Fernandes GW (Eds), Neotropical Insect Galls, New York: Springer Netherlands. p. 363-376.). The Amazon, which is the largest biome in Brazil, had a small number of published studies (4). The same was observed for other Brazilian biomes (e.g., Caatinga, Pampas and Pantanal) that together sum only 12% of the gall-inducing insect inventories in Brazil. Thus, there are still many gaps in the knowledge of gall-inducing insects of Brazil considering both the political (i.e., regions and states) and the ecological (i.e., biomes) organization of the territory.

Cecidomyiidae (Diptera) was the most important gall-inducing group, producing an average of 63.9% of gall morphotypes of the Brazilian gall-inducing insect inventories. This pattern corroborates the study of Espírito-Santo and Fernandes (2007)FERNANDES SPC, CASTELO-BRANCO BP, ALBUQUERQUE FA, BRITO-RAMOS AB, FERREIRA ALN, BRAGA DVV and ALMEIDA-CORTEZ JS. 2009. Galhas entomógenas em um fragmento urbano de Mata Atlântica no centro de endemismo de Pernambuco. Rev Bras Bioc 7: 240-244., which estimated that 64% of gall-inducing insect species in the world belong to the family Cecidomyiidae. In spite of the preponderance of cecidomyiids in Brazilian inventories, they are usually not identified to the species level, either because of taxonomic uncertainties (i.e., difficulties researchers have in determining species) or because they have yet to be described and named (i.e., new species for science). Gagné and Jaschhof (2014)GAGNÉ RJ and JASCHHOF M. 2014. A Catalog of the Cecidomyiidae (Diptera) of the World. Digital version 2. ZooBank registration, 493 p., which created a worldwide catalog of cecidomyiids, hypothesize that the number of unidentified Cecidomyiidae species is inestimable, especially in the tropics. Due to the large floristic diversity of Brazilian grasslands, forests and savannas (Forzza et al. 2012), Brazilian biomes are likely to harbor the highest diversity of gall-inducing insects in the world (Espírito-Santo and Fernandes 2007). For this reason, in addition to making inventories, it is extremely important to refine the taxonomic understanding of galling insect groups. In this sense, there is an urgent need for investments to increase the number of taxonomists, particularly in Brazil where there is already a deficit of taxonomists specializing on galling insects.

A consistent pattern observed among the inventories of gall-inducing insects in Brazil is that Fabaceae, Myrtaceae and Asteraceae are the most important host plant families. In virtually all compiled inventories at least one of these families appears in the top three most important families (see Table I). The importance of Fabaceae was found to be true for many Brazilian biomes, such as the Amazon (e.g., Almada et al. 2011ALMADA ED and FERNANDES GWA. 2011. Insetos indutores de galhas em florestas de terra firme e em reflorestamentos com espécies nativas na Amazônia Oriental, Pará, Brasil. Bol Mus Par Em Goeldi Ciênc Nat 6: 163-196., Araújo et al. 2012ARAÚJO WS. 2011. Size, age and composition: characteristics of plant taxa as diversity predictors of gall-midges (Diptera: Cecidomyiidae). Rev Biol Trop 59: 1599-1607.), Atlantic Forest (e.g., Fernandes and Negreiros 2006FERNANDES GW. 1992. Plant family size and age effects on insular gall-forming species richness. Glob Ecol Biogeog 2: 71-74., Maia and Carvalho-Fernandes 2016), Caatinga (e.g., Santos et al. 2011bSANTOS JC, ALMEIDA-CORTEZ JSD and FERNANDES GW. 2011b. Richness of gall-inducing insects in the tropical dry forest (caatinga) of Pernambuco. Rev Bras Entomol 55: 45-54., Costa et al. 2014COSTA EC, CARVALHO-FERNANDES SP and SANTOS-SILVA J. 2014. Galhas de insetos em uma área de transição caatinga-cerrado. Sitientibus Ser Ciênc Biol 14: 1-9.) and Cerrado (e.g., Maia and Fernandes 2004, Bergamini et al. 2017BERGAMINI BAR, BERGAMINI LL, SANTOS BB and ARAÚJO WS. 2017. Occurrence and characterization of insect galls in the Floresta Nacional de Silvânia, Brazil. Pap Avul Zool 57: 413-431.). Myrtaceae was found to be more important in Atlantic Forest inventories (e.g., Rodrigues et al. 2014, Carvalho-Fernandes et al. 2016CARVALHO-FERNANDES SP, ALMEIDA-CORTEZ JSD and FERREIRA ALN. 2012. The insect gall richness in preserved and anthropic areas of caatinga. Rev Árvore 36: 269-277., Maia and Silva 2016), while Asteraceae was found important in inventories of Atlantic Forest (e.g., Fernandes et al. 2001, Maia et al. 2014) and Cerrado (Carneiro et al. 2009, Coelho et al. 2013bCOELHO MS, CARNEIRO MAA, BRANCO C, BORGES RAX and FERNANDES GW. 2013a. Gall-inducing insects from Campos de Altitude, Brazil. Biota Neotrop 13: 139-151.). The main reason for the great importance of Fabaceae, Myrtaceae and Asteraceae as super-hosts of gall-inducing insects is the high number of species they encompass (Araújo 2011). These families are listed among the top ten richest families of Brazil with nearly 2,700 species in Fabaceae, 1,900 in Asteraceae and 920 in Myrtaceae (BFG 2015BFG. 2015. Growing knowledge: an overview of Seed Plant diversity in Brazil. Rodriguésia 66: 1085-1113.). The most important super-host species were Protium heptaphyllum (Burseraceae) and Copaifera langsdorffii (Fabaceae). Both these species are widely distributed throughout Brazil (Lorenzi 1992LORENZI H. 1992. Árvores Brasileiras, Vol 1, Nova Odessa: Instituto Plantarum, 368 p.), which can be explained by the high number of local gall morphospecies recorded by each particular gall-inducing insect inventory (i.e., alpha diversity) as well as regional richness (i.e., beta diversity) (Araújo et al. 2013ARAÚJO WS, SCARELI-SANTOS C, GUILHERME FAG and CUEVAS-REYES P. 2013. Comparing galling insect richness among Neotropical savannas: effects of plant richness, vegetation structure and super-host presence. Biodivers Conserv 22: 1083-1094.). Other factors, such as architecture, phenology and release of natural enemies, can also explain the importance of these plant species to host galling insects (Araújo et al. 2013).

Another interesting pattern obtained from the inventories of insect galls in Brazil is that the total richness of gall-inducing insects differs among sampling sites of different Brazilian regions and biomes, but the same is not true for the number of gall morphotypes per plant species. The gross number of gall-inducing insects recorded at the sampling sites in the North region and Amazon biome were much higher than at other Brazilian sites. This result can be explained by the high plant species richness in tropical rain forests and the great environmental stress on the forest canopy (Julião et al. 2014JULIÃO GR, VENTICINQUE EM, FERNANDES GW and PRICE PW. 2014. Unexpected high diversity of galling insects in the Amazonian upper canopy: the savanna out there. PloS ONE 9: e114986.), in addition to sampling factors (i.e., different sampling efforts and methodologies). On the other hand, when controlling for differences in host plant richness (and, consequently, sampling differences too) by using the number of gall-inducing insects per host plant species, these differences disappear. This result confirms previous studies that pointed out that local and regional difference in the plant species richness are the main factors that explain the richness of galling insects (Cuevas-Reyes et al. 2004CUEVAS-REYES P, QUESADA M, HANSON P, DIRZO R and OYAMA K. 2004. Diversity of gall-inducing insects in a Mexican tropical dry forest: the importance of plant species richness, life-forms, host plant age and plant density. J Ecol 92: 707-716., Araújo et al. 2014bARAÚJO WS, CUEVAS-REYES P and GUILHERME FAG. 2014b. Local and regional determinants of galling-insect richness in Neotropical savanna. J Trop Ecol 30: 269-272., Araújo 2017ARAÚJO WS. 2017. Plant species richness mediates the effects of vegetation structure, but not soil fertility, on insect gall richness in a savanna in Brazil. J Trop Ecol 33: 197-204.). The number of gall-inducing insect morphotypes per plant species varied relatively little, being on average 1.72 (± 0.43) gall morphotypes per plant species in Brazilian inventories. Other possible explanatory factors, such as latitude, elevation and vegetation type, were not found to influence the diversity of gall-inducing insects in Brazil. This absence of effects may be due to other non-controlled characteristics of the sampling sites, such as vegetation structure and conservation status.

This study represents the first systematic compilation of inventories of gall-inducing insects in Brazil. Given the growing interest in this line of research, as evidenced by the recent significant increase in the number of publications on the subject, this study identifies the main trends and gaps in the knowledge of gall-inducing insects in Brazil. Based on the results obtained, it is clear that sampling efforts by cecidologists are needed in less studied regions of Brazil, especially the North and South regions and subsampled biomes such as Amazon, Caatinga, Pampas and Pantanal. Furthermore, investment in the production of new taxonomists specializing on galling insects is urgently needed, particularly for Cecidomyiidae, in order to improve the taxonomic resolution of the surveys that have been carried out. Finally, the results presented herein emphasize the importance for cecidologists to publish their inventories in scientific journals. In addition to the acquisition of basic knowledge related to the description of group diversity, these surveys are vital to applied research, such as serving as indicator species or being used in testing ecological hypotheses.

ACKNOWLEGMENTS

The authors would like to Erik Wild for revising the English and to Pablo Cuevas-Reyes and one anonymous reviewer for important suggestions to the manuscript. This work was prepared as a presentation in the “IV Simpósio Brasileiro Sobre Galhas e Galhadores” of the “XXXII Congresso Brasileiro de Zoologia”.

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FERNANDES GWA, TAMEIRÃO-NETO E and MARTINS RP. 1988. Ocorrência e caracterização de galhas entomógenas na vegetação do campus Pampulha da Universidade Federal de Minas Gerais. Rev Bras Zool 5: 11-29.
FERNANDES GW, JULIÃO GR, ARAÚJO R, ARAÚJO S, LOMBARDIM JA, NEGREIROS D and CARNEIRO M. 2001. Distribution and morphology of insect galls of the Rio Doce Valley, Brazil. Naturalia 26: 211-244.
FERNANDES SPC, CASTELO-BRANCO BP, ALBUQUERQUE FA, BRITO-RAMOS AB, FERREIRA ALN, BRAGA DVV and ALMEIDA-CORTEZ JS. 2009. Galhas entomógenas em um fragmento urbano de Mata Atlântica no centro de endemismo de Pernambuco. Rev Bras Bioc 7: 240-244.
FORZZA RC et al. 2012. New Brazilian Floristic List Highlights Conservation Challenges. BioScience 62: 39-45.
GAGNÉ RJ and JASCHHOF M. 2014. A Catalog of the Cecidomyiidae (Diptera) of the World. Digital version 2. ZooBank registration, 493 p.
GONÇALVES-ALVIM SJ and FERNANDES GW. 2001. Comunidades de insetos galhadores (Insecta) em diferentes fisionomias do cerrado em Minas Gerais, Brasil. Rev Bras Zool 18: 289-305.
GRANDEZ-RIOS JM, GARCÍA-VILLACORTA R, CUEVAS-REYES P and ARAÚJO WS. 2015. Insectos inductores de agallas en América Latina: ecología, importancia y nuevas perspectivas. Rev Biol Neotrop 12: 92-103.
JULIÃO GR, AMARAL M and FERNANDES G. 2002. Galhas de insetos e suas plantas hospedeiras no Pantanal sul-mato-grossense. Naturalia 27: 47-74.
JULIÃO GR, VENTICINQUE EM, FERNANDES GW and PRICE PW. 2014. Unexpected high diversity of galling insects in the Amazonian upper canopy: the savanna out there. PloS ONE 9: e114986.
JULIÃO GR, ALMADA ED, COSTA FRC, CARNEIRO MAA and FERNANDES GW. 2017. Understory host plant and insect gall diversity changes across topographic habitats differing in nutrient and water stress in the Brazilian Amazon rainforest. Acta Amazon 47: 237-246.
LEWINSOHN TM and PRADO PI. 2005. How many species are there in Brazil? Conserv Biol 19: 619-624.
LORENZI H. 1992. Árvores Brasileiras, Vol 1, Nova Odessa: Instituto Plantarum, 368 p.
LUZ GR, FERNANDES GW, SILVA JO, NEVES FS and FAGUNDES M. 2012. Insect galls in xeric and mesic habitats in a Cerrado-Caatinga transition in northern Minas Gerais, Brazil. Neotrop Biol Conserv 7: 171-187.
MAIA VC. 2001. The gall midges (Diptera, Cecidomyiidae) from three restingas of Rio de Janeiro State, Brazil. Rev Bras Zool 18: 583-629.
MAIA VC. 2011. Characterization of insect galls, gall makers, and associated fauna of Platô Bacaba (Porto de Trombetas, Pará, Brazil). Biota Neotrop 11: 37-53.
MAIA VC. 2013. Insect galls of São Tomé das Letras (MG, Brazil). Biota Neotrop 13: 164-189.
MAIA VC and CARVALHO-FERNANDES SP. 2016. Insect galls of a protected remnant of the Atlantic Forest tableland from Rio de Janeiro State (Brazil). Rev Bras Entomol 60: 40-56.
MAIA VC and FERNANDES GW. 2004. Insect galls from Serra de São José (Tiradentes, MG, Brazil). Braz J Biol 64: 423-445.
MAIA VC and MASCARENHAS B. 2017. Insect Galls of the Parque Nacional do Itatiaia (Southeast Region, Brazil). An Acad Bras Cienc 89: 505-575. http://dx.doi.org/10.1590/0001-3765201720160877.
MAIA VC and OLIVEIRA J. 2010. Galhas de insetos da Reserva Biológica Estadual da Praia do Sul (Ilha Grande, Angra dos Reis, RJ). Biota Neotrop 10: 227-238.
MAIA VC and SILVA LO. 2016. Insect galls of Restinga de Marambaia (Barra de Guaratiba, Rio de Janeiro, RJ). Braz J Biol 76: 787-795.
MAIA VC, MAGENTA MAG and MARTINS SE. 2008. Occurrence and characterization of insect galls at restinga areas of Bertioga (São Paulo, Brazil). Biota Neotrop 8: 167-197.
MAIA VC, CARDOSO LJT and BRAGA JMA. 2014. Insect galls from Atlantic Forest areas of Santa Teresa, Espírito Santo, Brazil: characterization and occurrence. Bol Mus Biol Mello Leitão 33: 47-129.
MALVES K and FRIEIRO-COSTA FA. 2012. List of plants with galls induced by insects from the UNILAVRAS/Boqueirão Biological Reserve, Ingaí, State of Minas Gerais, Brazil. Check List 8: 426-431.
MANI MS. 2013. Ecology of plant galls. New York, Springer, 434 p.
MENDONÇA RC, FELFILI JM, WALTER BMT, SILVA-JÚNIOR MC, REZENDE AV, FILGUEIRAS TS, NOGUEIRA PE and FAGG CW. 2008. Flora vascular do bioma cerrado: checklist com 12.356 espécies. In: Sano SM, Almeida SP and Ribeiro JF (Eds), Cerrado: ecologia e flora Volume 2, Brasília: Embrapa Cerrados, p. 422-442.
MENDONÇA JR MS. 2007. Plant diversity and galling arthropod diversity searching for taxonomic patterns in an animal-plant interaction in the Neotropics. Bol Soc Argent Bot 42: 347-357.
MOREIRA RG, FERNANDES GW, ALMADA ED and SANTOS JC. 2007. Galling insects as bioindicators of land restoration in an area of Brazilian Atlantic Forest. Lundiana 8: 107-112.
MYERS N, MITTERMEIER RA, MITTERMEIER CG, FONSECA GA and KENT J. 2000. Biodiversity hotspots for conservation priorities. Nature 403: 853-858.
OLIVEIRA JD and MAIA VC. 2005. Ocorrência e caracterização de galhas de insetos na restinga de Grumari (Rio de Janeiro, RJ, Brasil). Arq Mus Nac 63: 669-675.
RODRIGUES AR, MAIA VC and COURI MS. 2014. Insect galls of restinga areas of Ilha da Marambaia, Rio de Janeiro, Brazil. Rev Bras Entomol 58: 173-197.
SAITO VS and URSO-GUIMARÃES MV. 2012. Characterization of galls, insect galls and associated fauna of Ecological Station of Jataí (Luiz Antônio, SP). Biota Neotrop 12: 99-107.
SANTOS BB, FERREIRA HD and ARAÚJO WS. 2010. Ocorrência e caracterização de galhas entomógenas em uma área de floresta estacional semidecídua em Goiânia, Goiás, Brasil. Acta Bot Bras 24: 243-249.
SANTOS JC, ALMEIDA-CORTEZ JS and FERNANDES GW. 2011a. Diversity of gall-inducing insects in the high altitude wetland forests in Pernambuco, Northeastern Brazil. Braz J Biol 71: 47-56.
SANTOS JC, ALMEIDA-CORTEZ JSD and FERNANDES GW. 2011b. Richness of gall-inducing insects in the tropical dry forest (caatinga) of Pernambuco. Rev Bras Entomol 55: 45-54.
SANTOS BB, RIBEIRO BA, SILVA TM and ARAÚJO W. 2012a. Galhas de insetos em uma área de cerrado sentido restrito na região semi-urbana de Caldas Novas (Goiás, Brasil). Rev Bras Bioc 10: 439.
SANTOS JC, ALMEIDA-CORTEZ JSD and FERNANDES GW. 2012b. Gall-inducing insects from Atlantic forest of Pernambuco, Northeastern Brazil. Biota Neotrop 12: 196-212.
SANTOS JC, COELHO MS, SOUZA DG and FERNANDES GW. 2014. Galls from Brazilian Atlantic Forest: Status of Knowledge and Perspectives. In: Santos JC and Fernandes GW (Eds), Neotropical Insect Galls, New York: Springer Netherlands. p. 363-376.
SILVA TM, ARAÚJO WS and SANTOS BB. 2015. Ocorrência e caracterização de galhas de insetos em um fragmento de mata semicaducifólia do Câmpus Samambaia, Goiânia, GO, Brasil. Rev Biol Neotrop 12: 26-38.
STEHMANN JR, FORZZA RC, SALINO A, SOBRAL M, COSTA DP and KAMINO LHY. 2009. Plantas da Floresta Atlântica. Rio de Janeiro: Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, 505 p.
STONE GN and SCHÖNROGGE K. 2003. The adaptive significance of insect gall morphology. Trend Ecol Evol 18: 512-522.
TOMA TSP and MENDONÇA JR MS. 2013. Gall-inducing insects of an Araucaria Forest in southern Brazil. Rev Bras Entomol 57: 225-233.
URSO-GUIMARÃES MV, CASTELLO ACD, KATAOKA EY and KOCH I. 2017. Characterization of entomogen galls from Mato Grosso do Sul, Brazil. Rev Bras Entomol 61: 25-42.
URSO-GUIMARÃES MV and SCARELI-SANTOS C. 2006. Galls and gall makers in plants from the Pé-de-Gigante Cerrado Reserve, Santa Rita do Passa Quatro, SP, Brazil. Braz J Biol 66: 357-369.
URSO-GUIMARÃES MV, SCARELI-SANTOS C and BONIFÁCIO-SILVA AC. 2003. Occurrence and characterization of entomogen galls in plants from natural vegetation areas in Delfinópolis, MG, Brazil. Braz J Biol 63: 705-715.

Publication Dates

Publication in this collection
21 Mar 2019
Date of issue
2019

History

Received
21 Feb 2018
Accepted
26 May 2018

This is an open-access article distributed under the terms of the Creative Commons Attribution License

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[7] ARAÚJO WS, SANTOS BBD and GOMES-KLEIN VL. 2011. Insect galls from Serra dos Pireneus, GO, Brazil. Biota Neotrop 11: 357-365.

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[24] FERNANDES GW and NEGREIROS D. 2006. A comunidade de insetos galhadores da RPPN fazenda Bulcão, Aimorés, Minas Gerais, Brasil. Lundiana 7: 111-120.

[25] FERNANDES GW, COSTA-ARAUJO R, ARAUJO S, LOMBARDI JA, SILVA DE PAULA A, JÚNIOR RL and CORNELISSEN TG. 1997. Insect galls from savanna and rocky fields of the Jequitinhonha Valley, Minas Gerais, Brazil. Naturalia 22: 221-244.

[26] FERNANDES GWA, TAMEIRÃO-NETO E and MARTINS RP. 1988. Ocorrência e caracterização de galhas entomógenas na vegetação do campus Pampulha da Universidade Federal de Minas Gerais. Rev Bras Zool 5: 11-29.

[27] FERNANDES GW, JULIÃO GR, ARAÚJO R, ARAÚJO S, LOMBARDIM JA, NEGREIROS D and CARNEIRO M. 2001. Distribution and morphology of insect galls of the Rio Doce Valley, Brazil. Naturalia 26: 211-244.

[28] FERNANDES SPC, CASTELO-BRANCO BP, ALBUQUERQUE FA, BRITO-RAMOS AB, FERREIRA ALN, BRAGA DVV and ALMEIDA-CORTEZ JS. 2009. Galhas entomógenas em um fragmento urbano de Mata Atlântica no centro de endemismo de Pernambuco. Rev Bras Bioc 7: 240-244.

[29] FORZZA RC et al. 2012. New Brazilian Floristic List Highlights Conservation Challenges. BioScience 62: 39-45.

[30] GAGNÉ RJ and JASCHHOF M. 2014. A Catalog of the Cecidomyiidae (Diptera) of the World. Digital version 2. ZooBank registration, 493 p.

[31] GONÇALVES-ALVIM SJ and FERNANDES GW. 2001. Comunidades de insetos galhadores (Insecta) em diferentes fisionomias do cerrado em Minas Gerais, Brasil. Rev Bras Zool 18: 289-305.

[32] GRANDEZ-RIOS JM, GARCÍA-VILLACORTA R, CUEVAS-REYES P and ARAÚJO WS. 2015. Insectos inductores de agallas en América Latina: ecología, importancia y nuevas perspectivas. Rev Biol Neotrop 12: 92-103.

[33] JULIÃO GR, AMARAL M and FERNANDES G. 2002. Galhas de insetos e suas plantas hospedeiras no Pantanal sul-mato-grossense. Naturalia 27: 47-74.

[34] JULIÃO GR, VENTICINQUE EM, FERNANDES GW and PRICE PW. 2014. Unexpected high diversity of galling insects in the Amazonian upper canopy: the savanna out there. PloS ONE 9: e114986.

[35] JULIÃO GR, ALMADA ED, COSTA FRC, CARNEIRO MAA and FERNANDES GW. 2017. Understory host plant and insect gall diversity changes across topographic habitats differing in nutrient and water stress in the Brazilian Amazon rainforest. Acta Amazon 47: 237-246.

[36] LEWINSOHN TM and PRADO PI. 2005. How many species are there in Brazil? Conserv Biol 19: 619-624.

[37] LORENZI H. 1992. Árvores Brasileiras, Vol 1, Nova Odessa: Instituto Plantarum, 368 p.

[38] LUZ GR, FERNANDES GW, SILVA JO, NEVES FS and FAGUNDES M. 2012. Insect galls in xeric and mesic habitats in a Cerrado-Caatinga transition in northern Minas Gerais, Brazil. Neotrop Biol Conserv 7: 171-187.

[39] MAIA VC. 2001. The gall midges (Diptera, Cecidomyiidae) from three restingas of Rio de Janeiro State, Brazil. Rev Bras Zool 18: 583-629.

[40] MAIA VC. 2011. Characterization of insect galls, gall makers, and associated fauna of Platô Bacaba (Porto de Trombetas, Pará, Brazil). Biota Neotrop 11: 37-53.

[41] MAIA VC. 2013. Insect galls of São Tomé das Letras (MG, Brazil). Biota Neotrop 13: 164-189.

[42] MAIA VC and CARVALHO-FERNANDES SP. 2016. Insect galls of a protected remnant of the Atlantic Forest tableland from Rio de Janeiro State (Brazil). Rev Bras Entomol 60: 40-56.

[43] MAIA VC and FERNANDES GW. 2004. Insect galls from Serra de São José (Tiradentes, MG, Brazil). Braz J Biol 64: 423-445.

[44] MAIA VC and MASCARENHAS B. 2017. Insect Galls of the Parque Nacional do Itatiaia (Southeast Region, Brazil). An Acad Bras Cienc 89: 505-575. http://dx.doi.org/10.1590/0001-3765201720160877.

[45] MAIA VC and OLIVEIRA J. 2010. Galhas de insetos da Reserva Biológica Estadual da Praia do Sul (Ilha Grande, Angra dos Reis, RJ). Biota Neotrop 10: 227-238.

[46] MAIA VC and SILVA LO. 2016. Insect galls of Restinga de Marambaia (Barra de Guaratiba, Rio de Janeiro, RJ). Braz J Biol 76: 787-795.

[47] MAIA VC, MAGENTA MAG and MARTINS SE. 2008. Occurrence and characterization of insect galls at restinga areas of Bertioga (São Paulo, Brazil). Biota Neotrop 8: 167-197.

[48] MAIA VC, CARDOSO LJT and BRAGA JMA. 2014. Insect galls from Atlantic Forest areas of Santa Teresa, Espírito Santo, Brazil: characterization and occurrence. Bol Mus Biol Mello Leitão 33: 47-129.

[49] MALVES K and FRIEIRO-COSTA FA. 2012. List of plants with galls induced by insects from the UNILAVRAS/Boqueirão Biological Reserve, Ingaí, State of Minas Gerais, Brazil. Check List 8: 426-431.

[50] MANI MS. 2013. Ecology of plant galls. New York, Springer, 434 p.

[51] MENDONÇA RC, FELFILI JM, WALTER BMT, SILVA-JÚNIOR MC, REZENDE AV, FILGUEIRAS TS, NOGUEIRA PE and FAGG CW. 2008. Flora vascular do bioma cerrado: checklist com 12.356 espécies. In: Sano SM, Almeida SP and Ribeiro JF (Eds), Cerrado: ecologia e flora Volume 2, Brasília: Embrapa Cerrados, p. 422-442.

[52] MENDONÇA JR MS. 2007. Plant diversity and galling arthropod diversity searching for taxonomic patterns in an animal-plant interaction in the Neotropics. Bol Soc Argent Bot 42: 347-357.

[53] MOREIRA RG, FERNANDES GW, ALMADA ED and SANTOS JC. 2007. Galling insects as bioindicators of land restoration in an area of Brazilian Atlantic Forest. Lundiana 8: 107-112.

[54] MYERS N, MITTERMEIER RA, MITTERMEIER CG, FONSECA GA and KENT J. 2000. Biodiversity hotspots for conservation priorities. Nature 403: 853-858.

[55] OLIVEIRA JD and MAIA VC. 2005. Ocorrência e caracterização de galhas de insetos na restinga de Grumari (Rio de Janeiro, RJ, Brasil). Arq Mus Nac 63: 669-675.

[56] RODRIGUES AR, MAIA VC and COURI MS. 2014. Insect galls of restinga areas of Ilha da Marambaia, Rio de Janeiro, Brazil. Rev Bras Entomol 58: 173-197.

[57] SAITO VS and URSO-GUIMARÃES MV. 2012. Characterization of galls, insect galls and associated fauna of Ecological Station of Jataí (Luiz Antônio, SP). Biota Neotrop 12: 99-107.

[58] SANTOS BB, FERREIRA HD and ARAÚJO WS. 2010. Ocorrência e caracterização de galhas entomógenas em uma área de floresta estacional semidecídua em Goiânia, Goiás, Brasil. Acta Bot Bras 24: 243-249.

[59] SANTOS JC, ALMEIDA-CORTEZ JS and FERNANDES GW. 2011a. Diversity of gall-inducing insects in the high altitude wetland forests in Pernambuco, Northeastern Brazil. Braz J Biol 71: 47-56.

[60] SANTOS JC, ALMEIDA-CORTEZ JSD and FERNANDES GW. 2011b. Richness of gall-inducing insects in the tropical dry forest (caatinga) of Pernambuco. Rev Bras Entomol 55: 45-54.

[61] SANTOS BB, RIBEIRO BA, SILVA TM and ARAÚJO W. 2012a. Galhas de insetos em uma área de cerrado sentido restrito na região semi-urbana de Caldas Novas (Goiás, Brasil). Rev Bras Bioc 10: 439.

[62] SANTOS JC, ALMEIDA-CORTEZ JSD and FERNANDES GW. 2012b. Gall-inducing insects from Atlantic forest of Pernambuco, Northeastern Brazil. Biota Neotrop 12: 196-212.

[63] SANTOS JC, COELHO MS, SOUZA DG and FERNANDES GW. 2014. Galls from Brazilian Atlantic Forest: Status of Knowledge and Perspectives. In: Santos JC and Fernandes GW (Eds), Neotropical Insect Galls, New York: Springer Netherlands. p. 363-376.

[64] SILVA TM, ARAÚJO WS and SANTOS BB. 2015. Ocorrência e caracterização de galhas de insetos em um fragmento de mata semicaducifólia do Câmpus Samambaia, Goiânia, GO, Brasil. Rev Biol Neotrop 12: 26-38.

[65] STEHMANN JR, FORZZA RC, SALINO A, SOBRAL M, COSTA DP and KAMINO LHY. 2009. Plantas da Floresta Atlântica. Rio de Janeiro: Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, 505 p.

[66] STONE GN and SCHÖNROGGE K. 2003. The adaptive significance of insect gall morphology. Trend Ecol Evol 18: 512-522.

[67] TOMA TSP and MENDONÇA JR MS. 2013. Gall-inducing insects of an Araucaria Forest in southern Brazil. Rev Bras Entomol 57: 225-233.

[68] URSO-GUIMARÃES MV, CASTELLO ACD, KATAOKA EY and KOCH I. 2017. Characterization of entomogen galls from Mato Grosso do Sul, Brazil. Rev Bras Entomol 61: 25-42.

[69] URSO-GUIMARÃES MV and SCARELI-SANTOS C. 2006. Galls and gall makers in plants from the Pé-de-Gigante Cerrado Reserve, Santa Rita do Passa Quatro, SP, Brazil. Braz J Biol 66: 357-369.

[70] URSO-GUIMARÃES MV, SCARELI-SANTOS C and BONIFÁCIO-SILVA AC. 2003. Occurrence and characterization of entomogen galls in plants from natural vegetation areas in Delfinópolis, MG, Brazil. Braz J Biol 63: 705-715.

Inventories	Brazilian regions	Brazilian states	Biomes	Gall-inducing insect richness	Plant species richness	Plant family richness	Number of gall morphotypes per plant species	Super-host families (number of insect gall morphotypes)	Super-host species (number of insect gall morphotypes)	Richness of Cecidomyiidae	% of Cecidomyiidae
Alcântara et al. 2017ALCÂNTARA JA, SOUZA EB and BRAGA PET. 2017. Ocorrência e caracterização de galhas em duas áreas do noroeste do Ceará, Brasil. Natureza on line 15: 33-40.	Northeast	CE	Caatinga-Atlantic forest	48	19	17	2.53	Burseraceae (16), Euphorbiaceae (8), Myrtaceae (3)	Protium heptaphyllum (16), Croton sonderianus (8)	NI	NI
Almada et al. 2011	North	PA	Amazon	309	255	45	1.21	Fabaceae (87), Chrysobalanaceae (12), Burseraceae (18)	Tapirira guianensis (6), Vismia latifolia (5), Endopleura uchi (4)	301	97.4
Araújo et al. 2011ARAÚJO WS, SANTOS BBD and GOMES-KLEIN VL. 2011. Insect galls from Serra dos Pireneus, GO, Brazil. Biota Neotrop 11: 357-365.	Midwest	GO	Cerrado	62	51	28	1.22	Fabaceae (8), Styracaceae (6), Malpighiaceae (5)	Andira paniculata (3), Qualea parviflora (3)	22	35.5
Araújo et al. 2012ARAÚJO WS, JÚNIOR ÉDP, JORGE VA and ESPÍRITO-SANTO FILHO K. 2012. Plantas hospedeiras e galhas entomógenas em sub-bosques de florestas tropicais do Pará, Brasil. INSULA Rev Bot 41: 59-72.	North	PA	Amazon	112	65	33	1.72	Fabaceae (18), Bignoniaceae (14), Lauraceae (12)	Adenocalymma neoflavidum (9), Ocotea sp. (6), Inga sp. (5)	NI	NI
Araújo et al. 2014cARAÚJO WS, SOBRAL FL and MARACAHIPES L. 2014c. Insect galls of the Parque Nacional das Emas (Mineiros, GO, Brazil). Check List 10: 1445-1451.	Midwest	GO	Cerrado	97	55	24	1.76	Myrtaceae (17), Fabaceae (14), Vochysiaceae (9)	Andira cujabensis (4), Myrcia guianensis (4)	37	38.1
Bergamini et al. 2017	Midwest	GO	Cerrado	186	61	35	3.05	Fabacewwae (18), Asteraceae (17), Sapindaceae (16)	Protium heptaphyllum (14), Siparuna guianensis (12), Serjania sp. (12)	64	34.4
Bregonci et al. 2010BREGONCI JDM, POLYCARPO PV and MAIA VC. 2010. Insect galls of the Parque Estadual Paulo César Vinha (Guarapari, ES, Brazil). Biota Neotrop 10: 265-274.	Southeast	ES	Atlantic Forest	38	21	17	1.81	Nyctaginaceae (7), Myrtaceae (5), Sapotaceae (4)	Manilkara subsericea (4), Andira nitida (3), Myrciaria floribunda (3)	32	84.2
Carneiro et al. 2009CARNEIRO MAA, BORGES RA, ARAÚJO A and FERNANDES GW. 2009. Gall inducing insects from southern portion of the Espinhaço Range, Minas Gerais, Brazil. Rev Bras Entomol 53: 570-592.	Southeast	MG	Cerrado	241	142	29	1.70	Asteraceae (86), Melastomataceae (22), Malpighiaceae (18)	Baccharis pseudomyriocephala (10), Byrsonima coccolobifolia (8), Baccharis platypoda (7)	205	85.1
Carvalho-Fernandes et al. 2012	Northeast	AL, BA, SE	Caatinga	25	18	8	1.39	Fabaceae (11), Euphorbiaceae (4), Boraginaceae (3)	Caesalpinia pyramidalis (4)	10	40.0
Carvalho-Fernandes et al. 2016CARVALHO-FERNANDES SP, ASCENDINO S, MAIA VC and COURI MS. 2016. Diversity of insect galls associated with coastal shrub vegetation in Rio de Janeiro, Brazil. An Acad Bras Cienc 88: 1407-1418. http://dx.doi.org/10.1590/0001-3765201620150658.	Southeast	RJ	Atlantic Forest	151	82	34	1.84	Myrtaceae (36), Fabaceae (14), Rubiaceae (9)	Eugenia copacabanensis (9)	95	62.9
Coelho et al. 2009COELHO MS, ALMADA ED, FERNANDES GW, CARNEIRO MAA, SANTOS RMD, QUINTINO AV and SANCHEZ-AZOFEIFA A. 2009. Gall inducing arthropods from a seasonally dry tropical forest in Serra do Cipó, Brazil. Rev Bras Entomol 53: 404-414.	Southeast	MG	Cerrado	92	51	17	1.80	Fabaceae (22), Myrtaceae (11), Asteraceae (8)	Baccharis dracunculifolia (5), Cordia trichotoma (5), Celtis brasiliensis (5)	70	76.1
Coelho et al. 2013aCOELHO MS, CARNEIRO MAA, BRANCO C, BORGES RAX and FERNANDES GW. 2013a. Gall-inducing insects from Campos de Altitude, Brazil. Biota Neotrop 13: 139-151.	Southeast	ES, MG, RJ	Cerrado, Atlantic Forest	93	50	13	1.86	Asteraceae (52), Melastomataceae (17), Euphorbiaceae (5)	Baccharis platypoda (8), Baccharis salzmanii (6)	91	97.8
Coelho et al. 2013bCOELHO MS, CARNEIRO MAA, BRANCO CA and FERNANDES GW. 2013b. Gall-inducing insects from Serra do Cabral, Minas Gerais, Brazil. Biota Neotrop 13: 102-109.	Southeast	MG	Cerrado	47	39	21	1.21	Asteraceae (12), Malpighiaceae (9), Fabaceae (4)	Byrsonima guilleminiana (3)	44	93.6
Costa et al. 2014	Northeast	BA	Caatinga-Cerrado	43	33	17	1.30	Fabaceae (15), Myrtaceae (5)	Bauhinia pulchella (3)	15	34.9
Fernandes and Negreiros 2006FERNANDES GW and NEGREIROS D. 2006. A comunidade de insetos galhadores da RPPN fazenda Bulcão, Aimorés, Minas Gerais, Brasil. Lundiana 7: 111-120.	Southeast	MG	Atlantic Forest	30	25	12	1.20	Fabaceae (6), Euphorbiaceae (4)	Cordia sellowiana (3)	28	93.3
Fernandes et al. 1988FERNANDES GWA, TAMEIRÃO-NETO E and MARTINS RP. 1988. Ocorrência e caracterização de galhas entomógenas na vegetação do campus Pampulha da Universidade Federal de Minas Gerais. Rev Bras Zool 5: 11-29.	Southeast	MG	Cerrado	37	22	11	1.68	Fabaceae (15), Boraginaceae (5)	Copaifera langsdorffii (7), Cordia sellowiana (4)	21	56.8
Fernandes et al. 1997	Southeast	MG	Cerrado	236	134	27	1.76	Fabaceae (34), Malpighiaceae (32), Asteraceae (32)	Sida urens (6)	195	82.6
Fernandes et al. 2001FERNANDES GW, JULIÃO GR, ARAÚJO R, ARAÚJO S, LOMBARDIM JA, NEGREIROS D and CARNEIRO M. 2001. Distribution and morphology of insect galls of the Rio Doce Valley, Brazil. Naturalia 26: 211-244.	Southeast	MG	Atlantic Forest	273	139	40	1.96	Asteraceae (17), Myrtaceae (16), Bignoniaceae (16)	Myrcia multiflora (9), Vernonia polyanthes (9), Eremanthus sp. (8)	225	82.4
Fernandes et al. 2009	Northeast	PE	Atlantic Forest	32	16	13	2.00	Burseraceae (5), Lecythidaceae (5)	Protium heptaphyllum (5)	5	15.6
Gonçalves-Alvim and Fernandes 2001GONÇALVES-ALVIM SJ and FERNANDES GW. 2001. Comunidades de insetos galhadores (Insecta) em diferentes fisionomias do cerrado em Minas Gerais, Brasil. Rev Bras Zool 18: 289-305.	Southeast	MG	Cerrado	92	62	28	1.48	Fabaceae (13), Asteraceae (5), Malpighiaceae (5)	Byrsonima coccolobifolia (4), Andira sp. (4), Myrcia sp. (4)	69	75.0
Julião et al. 2002JULIÃO GR, AMARAL M and FERNANDES G. 2002. Galhas de insetos e suas plantas hospedeiras no Pantanal sul-mato-grossense. Naturalia 27: 47-74.	Midwest	MS	Pantanal	133	75	37	1.77	Bignoniaceae (10), Fabaceae (6), Sapindaceae (6)	Hippocratea volubis (6), Inga vera (5)	130	97.7
Julião et al. 2017JULIÃO GR, ALMADA ED, COSTA FRC, CARNEIRO MAA and FERNANDES GW. 2017. Understory host plant and insect gall diversity changes across topographic habitats differing in nutrient and water stress in the Brazilian Amazon rainforest. Acta Amazon 47: 237-246.	North	AM	Amazon	228	169	38	1.35	Burseraceae (28), Fabaceae (28), Chrysobalanaceae (21)	Protium pilosissimum (5)	NI	NI
Luz et al. 2012LUZ GR, FERNANDES GW, SILVA JO, NEVES FS and FAGUNDES M. 2012. Insect galls in xeric and mesic habitats in a Cerrado-Caatinga transition in northern Minas Gerais, Brazil. Neotrop Biol Conserv 7: 171-187.	Southeast	MG	Cerrado-Caatinga	98	70	20	1.40	Fabaceae (19), Myrtaceae (6), Sapindaceae (4)	Copaifera langsdorffii (11), Calophyllum brasiliense (5), Bauhinia brevipes (4)	59	60.2
Maia and Carvalho-Fernandes 2016MAIA VC and CARVALHO-FERNANDES SP. 2016. Insect galls of a protected remnant of the Atlantic Forest tableland from Rio de Janeiro State (Brazil). Rev Bras Entomol 60: 40-56.	Southeast	RJ	Atlantic Forest	143	82	31	1.74	Fabaceae (28), Myrtaceae (13), Sapindaceae (13)	Protium heptaphyllum (4)	39	27.3
Maia and Fernandes 2004MAIA VC and FERNANDES GW. 2004. Insect galls from Serra de São José (Tiradentes, MG, Brazil). Braz J Biol 64: 423-445.	Southeast	MG	Cerrado	137	73	30	1.88	Fabaceae (20), Myrtaceae (18), Asteraceae (16)	Protium heptaphyllum (7), Copaifera langsdorffii (6), Myrcia sp. (6)	101	73.7
Maia and Mascarenhas 2017MAIA VC and MASCARENHAS B. 2017. Insect Galls of the Parque Nacional do Itatiaia (Southeast Region, Brazil). An Acad Bras Cienc 89: 505-575. http://dx.doi.org/10.1590/0001-3765201720160877.	Southeast	ES, MG, RJ	Atlantic Forest	432	145	47	2.97	Asteraceae (93), Melastomataceae (66), Fabaceae (29)	Mikania glomerata (8), Mikania sp. (8), Myrcia sylvatica (8)	152	64.9
Maia and Oliveira 2010MAIA VC and OLIVEIRA J. 2010. Galhas de insetos da Reserva Biológica Estadual da Praia do Sul (Ilha Grande, Angra dos Reis, RJ). Biota Neotrop 10: 227-238.	Southeast	RJ	Atlantic Forest	36	22	16	1.64	Myrtaceae (9), Asteraceae (5) e Nyctaginaceae (4)	Mikania sp. (4), Guapira opposita (4)	27	75.0
Maia and Silva 2016MAIA VC and SILVA LO. 2016. Insect galls of Restinga de Marambaia (Barra de Guaratiba, Rio de Janeiro, RJ). Braz J Biol 76: 787-795.	Southeast	RJ	Atlantic Forest	31	24	16	1.29	Myrtaceae (6), Fabaceae (4), Malpighiaceae (4)	Eugenia adstringens (3), Erythroxylum ovalifolium (3), Byrsonima sericea (3)	25	80.6
Maia and Souza 2013MAIA VC. 2013. Insect galls of São Tomé das Letras (MG, Brazil). Biota Neotrop 13: 164-189.	Southeast	RJ	Atlantic Forest	45	29	18	1.55	Asteraceae (7), Myrtaceae (6)	Guapira opposita (4), Tournefortia membranacea (3), Eugenia uniflora (3)	23	51.1
Maia 2001MAIA VC. 2001. The gall midges (Diptera, Cecidomyiidae) from three restingas of Rio de Janeiro State, Brazil. Rev Bras Zool 18: 583-629.	Southeast	RJ	Atlantic Forest	108	53	32	2.04	Myrtaceae (24), Burseraceae (8), Nyctaginaceae (5)	Eugenia multiflora (6), Guapira opposita (5)	94	87.0
Maia 2011MAIA VC. 2011. Characterization of insect galls, gall makers, and associated fauna of Platô Bacaba (Porto de Trombetas, Pará, Brazil). Biota Neotrop 11: 37-53.	North	PA	Amazon	76	38	22	2.00	Burseraceae (23), Fabaceae (11) e Melastomataceae (6)	Protium sagotianum (7), Tetragastris panamensis (6), Miconia stenostachya (5)	25	32.9
Maia 2013MAIA VC. 2013. Insect galls of São Tomé das Letras (MG, Brazil). Biota Neotrop 13: 164-189.	Southeast	MG	Atlantic Forest	152	94	37	1.62	Fabaceae (20), Melastomataceae (18), Myrtaceae (17)	Copaifera langsdorfii (10), Myrcia sylvatica (7), Calophyllum brasiliense (6)	82	53.9
Maia 2014MAIA VC, CARDOSO LJT and BRAGA JMA. 2014. Insect galls from Atlantic Forest areas of Santa Teresa, Espírito Santo, Brazil: characterization and occurrence. Bol Mus Biol Mello Leitão 33: 47-129.	Southeast	MG	Atlantic Forest	101	63	23	1.60	Melastomataceae (29), Asteraceae (18), Myrtaceae (11)	Asteraceae sp. 2 (6), Marlierea sp. (5)	51	50.5
Maia et al. 2008MAIA VC, MAGENTA MAG and MARTINS SE. 2008. Occurrence and characterization of insect galls at restinga areas of Bertioga (São Paulo, Brazil). Biota Neotrop 8: 167-197.	Southeast	SP	Atlantic Forest	233	123	48	1.89	Myrtaceae (31), Asteraceae (29), Melastomataceae (18)	Myrcia fallax (7), Paullinia sp. (7), Guapira opposita (6)	135	57.9
Maia et al. 2014	Southeast	ES	Atlantic Forest	265	141	49	1.88	Asteraceae (36), Fabaceae (32), Myrtaceae (27)	Inga sp.1 (10), Myrcia sp.1 (8), Guapira opposita (8)	129	48.7
Malves and Friero-Costa 2012MALVES K and FRIEIRO-COSTA FA. 2012. List of plants with galls induced by insects from the UNILAVRAS/Boqueirão Biological Reserve, Ingaí, State of Minas Gerais, Brazil. Check List 8: 426-431.	Southeast	MG	Cerrado	57	43	18	1.33	Asteraceae (6), Myrtaceae (5), Melastomataceae (3)	Croton sp. (4), Eugenia sp.2 (3)	14	24.6
Moreira et al. 2007	Southeast	MG	Atlantic Forest	50	41	15	1.22	Fabaceae (8), Bignoniaceae (7), Asteraceae (7)	Vernonia polyanthes (3), Bignoniaceae Sp. 1 (3)	44	88.0
Oliveira and Maia 2005OLIVEIRA JD and MAIA VC. 2005. Ocorrência e caracterização de galhas de insetos na restinga de Grumari (Rio de Janeiro, RJ, Brasil). Arq Mus Nac 63: 669-675.	Southeast	RJ	Atlantic Forest	43	25	19	1.72	Myrtaceae (7), Erythroxylaceae (5)	Erythroxyllum ovalifolium (5)	39	90.7
Nogueira et al. 2016	Northeast	BA	Cerrado-Caatinga	49	14	13	3.50	Fabaceae (22), Malpighiaceae (10)	Copaifera langsdorffii (10), Bauhinia acuruana (5), Mimosa gemmulata (4)	9	18.4
Rodrigues et al. 2014RODRIGUES AR, MAIA VC and COURI MS. 2014. Insect galls of restinga areas of Ilha da Marambaia, Rio de Janeiro, Brazil. Rev Bras Entomol 58: 173-197.	Southeast	RJ	Atlantic Forest	147	70	33	2.10	Myrtaceae (20), Bignoniaceae (13), Fabaceae (11)	Guapira opposita (8), Byrsonima sericea (5)	80	54.4
Saito and Urso-Guimarães 2012	Southeast	SP	Cerrado	69	41	24	1.68	Malpighiaceae (9), Annonaceae (7), Myrtaceae (7)	Byrsonima intermedia (6), Duguetia furfuracea (5), Arrabidaea sp. (4)	23	33.3
Santos et al. 2010SANTOS BB, FERREIRA HD and ARAÚJO WS. 2010. Ocorrência e caracterização de galhas entomógenas em uma área de floresta estacional semidecídua em Goiânia, Goiás, Brasil. Acta Bot Bras 24: 243-249.	Midwest	GO	Cerrado	34	20	12	1.70	Fabaceae (9), Styracaceae (6), Ulmaceae (4)	Styrax pohlii (6), Inga cylindrica (3), Serjania obtusidentata (3)	13	38.2
Santos et al. 2011aSANTOS JC, ALMEIDA-CORTEZ JS and FERNANDES GW. 2011a. Diversity of gall-inducing insects in the high altitude wetland forests in Pernambuco, Northeastern Brazil. Braz J Biol 71: 47-56.	Northeast	PE	Atlantic Forest	80	49	28	1.63	Nyctaginaceae (15), Fabaceae (10), Meliaceae (8)	Guapira sp. 1 (7), Guapira sp. 2 (7), Guarea macrophylla (6)	65	81.3
Santos et al. 2011bSANTOS JC, ALMEIDA-CORTEZ JSD and FERNANDES GW. 2011b. Richness of gall-inducing insects in the tropical dry forest (caatinga) of Pernambuco. Rev Bras Entomol 55: 45-54.	Northeast	PE	Caatinga	64	48	17	1.33	Fabaceae (15), Euphorbiaceae (9)	Bauhinia cheilantha (4)	57	89.1
Santos et al. 2012aSANTOS BB, RIBEIRO BA, SILVA TM and ARAÚJO W. 2012a. Galhas de insetos em uma área de cerrado sentido restrito na região semi-urbana de Caldas Novas (Goiás, Brasil). Rev Bras Bioc 10: 439.	Midwest	GO	Cerrado	56	34	21	1.65	Fabaceae (14), Vochysiaceae (8), Malpighiaceae (5)	Andira paniculata (5)	18	32.1
Santos et al. 2012bSANTOS JC, ALMEIDA-CORTEZ JSD and FERNANDES GW. 2012b. Gall-inducing insects from Atlantic forest of Pernambuco, Northeastern Brazil. Biota Neotrop 12: 196-212.	Northeast	PE	Atlantic Forest	136	79	35	1.72	Lecythidaceae (9), Myrtaceae (9), Nyctaginaceae (9)	Guapira opposita (9), Eschweilera ovata (6), Protium heptaphyllum (6)	129	94.9
Silva et al. 2015SILVA TM, ARAÚJO WS and SANTOS BB. 2015. Ocorrência e caracterização de galhas de insetos em um fragmento de mata semicaducifólia do Câmpus Samambaia, Goiânia, GO, Brasil. Rev Biol Neotrop 12: 26-38.	Midwest	GO	Cerrado	42	22	20	1.91	Styracaceae (7), Burseraceae (7), Fabaceae (5)	Styrax pohlii (7), Protium heptaphyllum (7), Siparuna guianensis (4)	6	14.3
Toma and Mendonça Jr 2013TOMA TSP and MENDONÇA JR MS. 2013. Gall-inducing insects of an Araucaria Forest in southern Brazil. Rev Bras Entomol 57: 225-233.	South	RS	Pampas	57	43	18	1.33	Myrtaceae (20), Asteraceae (8), Melastomataceae (5)	Siphoneugena reitzii (4), Myrcia guianensis (3), Ilex microdonta (3)	31	54.4
Urso-Guimarães and Scareli-Santos 2006URSO-GUIMARÃES MV and SCARELI-SANTOS C. 2006. Galls and gall makers in plants from the Pé-de-Gigante Cerrado Reserve, Santa Rita do Passa Quatro, SP, Brazil. Braz J Biol 66: 357-369.	Southeast	SP	Cerrado	36	26	15	1.39	Fabaceae (7), Myrtaceae (5), Annonaceae (4)	Duguetia furfuracea (3), Myrcia bella (3)	19	52.8
Urso-Guimarães et al. 2003URSO-GUIMARÃES MV, SCARELI-SANTOS C and BONIFÁCIO-SILVA AC. 2003. Occurrence and characterization of entomogen galls in plants from natural vegetation areas in Delfinópolis, MG, Brazil. Braz J Biol 63: 705-715.	Southeast	MG	Cerrado	22	19	16	1.16	Fabaceae (5)	No super-host	12	54.5
Urso-Guimarães et al. 2017	Midwest	MS	Cerrado, Atlantic Forest, Pantanal and Chaco	186	115	35	1.62	Fabaceae (34), Sapindaceae (24), Bignoniaceae (17)	Fridericia chica (7), Serjania cf. glabrata (7), Eugenia florida (6)	39	21.0