30 years of research on insect galls in Brazil : a scientometric review

The first systematic studies on insect galls in Brazil date to the early 20th century, after which research on insect galls remained dormant in the country, with interest not reviving until the 1980s. The aim of this study was is to document historical trends in publications about insect galls in Brazil over the last 30 years. Papers about insect galls and galling species in Brazil published in peer-reviewed journals from 1988 to 2017 were compiled. A total of 1,378 papers were analyzed, of which 182 addressed insect galls in Brazil. The results showed that the number of publications on the subject has been increasing over the last 30 years, and especially in the last decade. The diversity of journals that published on the subject has also been increasing. The studies were concentrated on the following topics: ecology (94 papers), inventory (29) and taxonomy (27). Most of the insect gall inventories in Brazil took place in the Southeast Region (29 papers), followed by the Central-West and Northeast regions, with eight papers each. This study documents a trend toward increasing scientific production on insect galls in Brazil, but with significant geographical bias: the researchers involved are concentrated in the Southeast Brazilian region. Key-Words. Ecological interaction; Galling insects; Plant-insect interaction; Scientometry.


INTRODUCTION
Galling insects are very diverse, with some estimates indicating that there could be as many as 132,000 species on the planet (Espírito-Santo & Fernandes, 2007), and between 5,540 (Grandez-Rios et al., 2015) and 9,282 species (Araújo et al., 2014) in Brazil.Although reports on insect galls in Brazil have been published since the 19 th century, the first systematic studies involving them date to the early 20 th century (Moreira, 2006).From 1905 to 1925, important natural historians, such as J.S. Tavares (Portugal), E.H. Rübsaamen (Germany), and E.P. Felt (United States of America -USA), described a large number of galling insect species from Brazil (Maia, 2005).After this period, the study of insect galls in Brazil remained dormant, with interest in the group not reviving until the 1980s.Since then, studies on galling insects have been carried out in different regions of Brazil using a variety of approaches and focusing on topics such as anatomy, biology, ecology and taxonomy (Moreira, 2006).
Brazil is the current leader in scientific production regarding insect galls, together with Mexico and USA (Grandez-Rios et al., 2015).The aim of the present study was to identify historical trends in the research on insect galls in Brazil over the last 30 years.Publications from 1988 to 2017, available in different scientific journal databases, were compiled.The main features of the papers were described and historical trends assessed with regard to number of papers, journals publishing on the subject, quality of the publications, topics investigated and the most studied regions and states of Brazil.The evaluation of scientific production in natural sciences has been the topic of discussion in recent years (Brito et al., 2009;Nabout et al., 2012;Borges et al., 2015;Nabout et al., 2015;Vaz et al., 2015;Santos et al., 2017), and has become an important tool for identifying trends and biases in the scientific production of a given area of study (Drew et al., 2016).

MATERIALS AND METHODS
Papers about insect galls and galling species in Brazil published in peer-reviewed journals from 1988 to 2017 were compiled from papers indexed in the platform "Portal de Periódicos Capes" (www.periodicos.capes.gov.br).This platform includes several scientific databases such as SCOPUS and Scielo, which makes a more comprehensive search on the topic possible.The period analyzed in this study  begins in the 1980s, when gall studies were again becoming frequent in Brazil (Moreira, 2006).The search for papers was done in September of 2017 using the key-words "insect*" and "gall*" in the title, abstract or list.The resulting papers had their titles and abstracts (and when necessary the full text) inspected to filter out only studies on galling insects in Brazil.Thus, papers were included in the compilation only when it was explicitly indicated that the study was fully or partially performed within Brazil.
The selected papers were sorted by year and journal.The historical trend in the number of publications per year was evaluated using Pearson correlation (P < 0.05).The diversity of journals that published papers on the subject from 1988 to 2017 was evaluated using the Shannon-Wiener diversity index (H').This index is frequently used in ecological studies but has also been applied to estimate journal diversity over time in scientometric studies (e.g., Nabout et al., 2012;Vaz et al., 2015).Pearson correlation was then used to evaluate the relationship between the journal diversity index and year.Journals were ranked by importance according to the number of papers published on the subject.
All compiled papers were classified according to topic -the area(s) of knowledge they best matched -by inspecting the title and the abstract (or the full text if necessary).The topics included: agriculture (focusing on agricultural pests), botanical anatomy (anatomical, morphological and histochemical focus on galls), ecology (investigating ecological factors at population, community or biogeographical levels), genetics (genetic diversity), inventory (checklists of galls and host plants), taxonomy (focusing on systematics, descriptions and revisions of galling species) and reviews (compiling data from the literature or purely theoretical treatments).Papers that fit more than one topic were counted in each.The number of citations of each paper was also determined through the SCOPUS database (www.scopus.com),and compared among topics using ANOVA and among years using linear regression.
To give an overview of the distribution of papers identified as inventories, papers were classified by location (Brazilian region and state) according to the content and the description of the authors.This was done by obtaining data from the Portal de Periódicos Capes database and performing an additional search (through Google Scholar and bibliographies in the compiled papers).Papers were considered inventories only if they presented primary data and sampled the community of host plants.Studies that inventoried the diversity of insect galls of only one species of host plant were classified under the topic "ecology".Studies that compiled information on the occurrence of insect galls from secondary data (literature or museums) were considered under the topic "review".Inventories carried out in more than two Brazilian states were included under each state involved.

RESULTS
A total of 1,378 papers were recovered for the period of 1988 to 2017, 182 of which dealt with insect galls in Brazil (Supplementary Material 1).The number of publications was found to have increased over the last 30 years (r = 0.82, p < 0.001), and especially in the last decade (Fig. 1a).A significant increase in the diversity of journals that published on the subject was also found (r = 0.90, p < 0.05, Fig. 1b).The publications came from 67 different journals, with the ten most important having published 48.35% of all the papers (Fig. 2).The top three journals, Revista Brasileira de Entomologia (24 papers), Biota Neotropica (17) and Brazilian Journal of Biology (11), represented 28.57% of all the publications.
The compiled papers comprise a variety of different topics (Fig. 3a).The most common topic was ecology (94 papers), followed by inventory (29) and taxonomy (27), which together represented 82.41% of all the publications.The topics of the remaining papers were anatomy (15), review (9), agriculture (7) and genetics (2).Among the subtopics of ecology (Fig. 3b), there were papers on community ecology (47), population ecology (46) and biogeography (2).The top ten most cited papers of the 182 compiled studies are presented in Table 1, among which Fernandes & Price (1988) and Fernandes & Price (1992) stand out.The average number of total citations per paper was 16.05 (± 27.66).There were no differences among papers on different topics in the average number of total citations (F₍₇₁₇₄₎ = 1.39; p = 0.21), but as expected older papers were cited more than more recent papers (r² = 0.43; p < 0.001).Considering the yearly rate of citation, 60.98% of the papers had less than two citations per year and 36.81% had less than one citation per year.Forty-eight papers were inventories (Supplementary Material 2).Most of the insect gall inventories were located in Southeast Brazil (29 papers), followed by the Central-West and Northeast regions, with eight papers each (Fig. 4a).The North and South regions were the least studied, with two and one papers, respectively.Inventories of insect galls in Brazil were performed in 13 of the 27 Brazilian states (including the Federal District) (Fig. 5a), although the states of origin of most of the first authors represented only eight states, and were usually in Southeast Brazil (Fig. 5b).Among Brazilian states, Minas Gerais led in number of papers ( 16), followed by Rio de Janeiro (9) and Goiás (6) (Fig. 4b).

DISCUSSION
The results showed a significant increase in the number of papers published on insect galls in Brazil over the past 30 years, and especially over the last decade (2008)(2009)(2010)(2011)(2012)(2013)(2014)(2015)(2016)(2017).The growing number of publications on this topic follows a global trend of exponential growth in the number of scientific publications over recent decades (Nabout et al., 2012;Nabout et al., 2015;Vaz et al., 2015).Scientometric analyses have also shown a significant increase in zoological scientific production, as has been demonstrated for mammalogy (Brito et al., 2009), carcinology (Nabout et al., 2010) and dipterology (Santos et al., 2017).Furthermore, recent scientometric studies have shown substantial growth in the scientific production of Latin American (e.g., Garcia et al., 2012), which was also observed for publications on insect galls, mainly due to the large contribution of Brazilian studies (Grandez-Rios et al., 2015).
A large number of scientific journals (67) published papers about Brazilian insect galls, but the three most important in terms of number of publications were Brazilian journals (i.e., Revista Brasileira de Entomologia, Biota Neotropica and Brazilian Journal of Biology).On the other hand, the ten most cited papers on the subject were almost all published in international journals (such as Oecologia, Journal of Biogeography and Functional Ecology).These results indicate a great degree of region-alism in the scientific production on insect galls in Brazil, since most of papers were published in regional journals (frequently in Portuguese) usually with low impact factors.Consequently, the number of citations per study and per year is generally low, which is relatively common for publications of Latin American authors (Nabout et al., 2015).An increase in the diversity of journals that publish on the subject was also found, which indicates that over the last few years a greater variety of aspects of insect gall diversity has been studied in Brazil.
Considering the topics that studies on insect galls in Brazil have focused on, approximately 50% of the publications were classified under ecology, i.e., investigations on the biology of galling species or the tests of ecological hypothesis.For example, Fernandes & Price (1988), the most cited paper about insect galls in Brazil, tested several ecological hypotheses with emphasis on the hypotheses of hygrothermal stress and plant species richness, which remain the most frequently tested hypotheses in such studies.Two other important topics of insect gall studies in Brazil were inventory and taxonomy.Inventories represented 15.9% of the compiled papers and focused on the occurrence and morphological characterization of insect galls of different Brazilian sites.Inventory papers are important for describing insect gall diversity at different sites and provide information necessary for the development of other types of studies.Taxonomic studies, in turn, represented 14.8% of all the publications.Based on previous studies that estimated the potential number of galling species from Brazil as being much higher than the number of described species (Espírito-Santo & Fernandes, 2007;Araújo et al., 2014;Grandez-Rios et al., 2015), taxonomic studies are very important for describing gall-inducer diversity, particularly of Cecidomyiidae, the most important gall-inducing insect group in the Neotropical region (Gagné, 1994).
Regarding the distribution of insect gall inventories among the geographical regions of Brazil, it is clear that there is a significant bias for studies in Southeast Brazil, which represents 60.4% of the publications (see Figs. 4 and 5).A similar pattern was also found for the states of origin of the first author, which are also concen-     search center has been dedicated to ecological research over the past three decades, while the latter has focused on taxonomic studies and faunistic inventories since the 1990s.Despite the increasing number of insect gall inventories in Brazil, the results show that there have been no papers published on the occurrence of insect galls in 51.8% of the states of Brazil.This result can be attributed to the lack of professionals in this area of study in most Brazilian states, which may indicate a problem in the training of scientists in Brazil, which tends to be concentrated in the Southeast region of the country.

CONCLUSIONS
The present study documents an increase in scientific production regarding insect galls in Brazil.Some well-studied topics, especially ecology, inventory and taxonomy, have contributed to the description and elucidation of patterns of the diversity of these insects in the Neotropical region (Fernandes & Santos, 2014).On the other hand, there is great geographical bias among insect gall studies in Brazil, with most of the data acquired, and researchers involved, being concentrated in the Southeast region of the country.This spatial bias, along with estimates that suggest an enormous diversity of galling insects in Brazil (Espírito-Santo & Fernandes, 2007;Grandez-Rios et al., 2015), make it clear that much remains to be done with regard to galls and galling insects in Brazil.A future challenge for researchers conducting studies about Brazilian insect galls is to increase the rate of publication in international journals with higher impact factors and, consequently, increase the average number of citations per study.

Figure 1 .
Figure 1.Historical trends (1988-2017) in publications on insect galls in Brazil (from CAPES database): (a) number of publications per year; and (b) diversity indexes of journals that published on the subject.

Figure 2 .
Figure2.Main journals that published on insect galls in Brazil (from CAPES database).

Figure 5 .
Figure 5. Geographic distribution of insect gall inventories among Brazilian states (from CAPES and additional databases): (a) the distribution of study area locations; and (b) distribution of the state of origin of the first author.

Figure 3 .
Figure 3. Number of publications about insect galls in Brazil (from CAPES database): (a) by topics (knowledge areas); and (b) by subtopics of ecology.

Figure 4 .
Figure 4. Number of inventories of insect galls in Brazil (CAPES and additional databases): (a) number of publications for Brazilian regions; and (b) number of publications for Brazilian states.

Table 1 .
The most frequently cited papers about insect galls in Brazil published from 1988 to 2017 (from CAPES database).trated in Southeast Brazil.These biases are due to the states of Minas Gerais and Rio de Janeiro, which have historically been the most important Brazilian research centers (both in article publishing and in staff training) re-garding galls and galling insects, in particular the laboratories of G.W. Fernandes (Universidade Federal de Minas Gerais) and V.C. Maia (Museu Nacional, Universidade Federal do Rio de Janeiro), respectively.The former re-