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

Department of general Biology, Center of Biological Sciences and Health, Universidade estadual de Montes Claros, C.P. 126, 39401-089 Montes Claros, Mg, Brazil Department of general Biology, Institute of Biological Sciences, Universidade Federal de Minas gerais, C.P. 486, 31270-901 Belo Horizonte, Mg, Brazil Institute of Biology, Universidade Federal de Uberlândia, C.P. 593, 38400-462 Uberlândia, Mg, Brazil


INTRODUCTION
Brazil is a mega-diverse country in terms of biodiversity (lewinsohn and Prado 2005).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. 2012).This high number of plant species represents a great diversity of potential niches for gall-inducing insects (Fernandes 1992, Mendonça 2007).galling insects are very specialized herbivores known to be highly specific to their host plants (Mani 2013, Stone andSchönrogge 2003).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 2007).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) 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) 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. 2015).
Interest about gall-inducing insects has promoted great contributions to the ecological and evolutionary understanding of insect-plant interactions (Araújo et al. 2014a), 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 2007, 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. 2007, 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 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. 2001, Santos et al. 2011a, 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 (R Pearson = 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.
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 gallinducing 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 Spearman values < 0.20 and P values > 0.05; Figure 3).On the other hand, the total richness of gall-inducing insects differed significantly among An Acad Bras Cienc (2019) 91(1)  e20180162 4 | 19  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).

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.
An Acad Bras Cienc (2019) 91(1) e20180162 5 | 19         (Myers et al. 2000).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. 2008), with these biomes also being considered hotspots of gall-inducing insect diversity (Araújo et al. 2014a, Santos et al. 2014).The Amazon, which is the largest biome in Brazil, had a small number of published studies (4).The same was observed  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), 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), 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 2004, Bergamini et al. 2017).Myrtaceae was found to be more important in Atlantic Forest inventories (e.g., Rodrigues et al. 2014, Carvalho-Fernandes et al. 2016, 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. 2013b).The main reason for the great importance of Fabaceae, Myrtaceae and Asteraceae as superhosts 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 2015).The most important super-host species were Protium heptaphyllum (Burseraceae) and Copaifera langsdorffii (Fabaceae).Both these species are widely distributed throughout Brazil (lorenzi 1992), which can be explained by the high number of local gall morphospecies recorded by each particular gall-inducing insect inventory (i.e., 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. 2011, Araújo et al. 2012), Atlantic Forest (e.g., Fernandes and Negreiros 2006, Maia and Carvalho-Fernandes 2016), Caatinga (e.g., Santos et al. 2011b, Costa et al. 2014) and Cerrado (e.g., Maia and Fernandes alpha diversity) as well as regional richness (i.e., beta diversity) (Araújo et al. 2013).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. 2014), 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 gallinducing 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. 2004, Araújo et al. 2014b, Araújo 2017).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 gallinducing 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.

Figure 1 -
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.
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 gallinducing insects of Brazil considering both the political (i.e., regions and states) and the ecological (i.e., biomes) organization of the territory.

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

TABLE I Inventories of gall-inducing insects realized in Brazil between 1988 and 2017.
WAlTeR S. De ARAÚJO, geRAlDO W. FeRNANDeS and JeAN C. SANTOS AN OVeRVIeW OF INSeCT gAll INVeNTORIeS IN BRAZIl An Acad Bras Cienc (2019) 91(1) e20180162 6 | 19

TABLE I
(continuation) An Acad Bras Cienc (2019) 91(1) e20180162 13 | 19 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