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

Walter Santos de Araújo About the author

Abstract

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, 2007Espírito-Santo, M.M. & Fernandes, G.W. 2007. How many species of gall-inducing insects are there on earth, and where are they? Annals of the Entomological Society of America, 100(2): 95-99.), and between 5,540 (Grandez-Rios 2015Grandez-Rios, J.M.; García-Villacorta, R.; Cuevas-Reyes, P. & Araújo, W.S. 2015. Insectos inductores de agallas en América Latina: ecología, importancia y nuevas perspectivas. Revista de Biologia Neotropical, 12(2): 92-103.) and 9,282 species (Araújo 2014Araújo, W.S.; Santos, B.B.; Guilherme, F.A.G. & Scareli-Santos, C. 2014. Galling insects in the Brazilian Cerrado: ecological patterns and perspectives. In: Fernandes, G.W. & Santos, J.C. Eds.). Neotropical insect Galls. New York, Springer. p. 257-272.) in Brazil. Although reports on insect galls in Brazil have been published since the 19th century, the first systematic studies involving them date to the early 20th century (Moreira, 2006Moreira, G.R.P. 2006. Galhas entomógenas no Brasil: oportunidade de estudo sobre interação inseto-planta. In: Mariath, J.E. & Santos, R.P. (Orgs.). Os avanços da botânica no inicio do século XXI do 57º Congresso Nacional de Botânica. Porto Alegre, Sociedade de Botânica do Brasil. p. 532-537.). 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, 2005Maia, V.C. 2005. Catálogo dos Cecidomyiidae (Diptera) do estado do Rio de Janeiro. Biota Neotropica , 5(2): 189-203.). 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, 2006Moreira, G.R.P. 2006. Galhas entomógenas no Brasil: oportunidade de estudo sobre interação inseto-planta. In: Mariath, J.E. & Santos, R.P. (Orgs.). Os avanços da botânica no inicio do século XXI do 57º Congresso Nacional de Botânica. Porto Alegre, Sociedade de Botânica do Brasil. p. 532-537.).

Brazil is the current leader in scientific production regarding insect galls, together with Mexico and USA (Grandez-Rios 2015Grandez-Rios, J.M.; García-Villacorta, R.; Cuevas-Reyes, P. & Araújo, W.S. 2015. Insectos inductores de agallas en América Latina: ecología, importancia y nuevas perspectivas. Revista de Biologia Neotropical, 12(2): 92-103.). 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 2009Brito, D.; Oliveira, L.C.; Oprea, M. & Mello, M.A.R. 2009. An overview of Brazilian mammalogy: trends, biases and future directions. Zoologia, 26(1): 67-73.; Nabout 2012Nabout, J.C.; Carvalho, P.; Prado, M.U.; Borges, P.P.; Machado, K.B.; Haddad, K.B.; Michelan, T.S.; Cunha, H.F. & Soares, T.N. 2012. Trends and biases in global climate change literature. Natureza & Conservação, 10(1): 45-51.; Borges 2015Borges, P.P.; Andrade Oliveira, K.A.F.; Machado, K.B.; Vaz, Ú.L., Cunha, H.F. & Nabout, J.C. 2015. Trends and gaps of the scientific literature on the Cerrado biome: A scientometric analysis. Neotropical Biology and Conservation, 10(1): 2-8.; Nabout 2015Nabout, J.C.; Carneiro, F.M.; Borges, P.P.; Machado, K.B. & Huszar, V.L.M. 2015. Brazilian scientific production on phytoplankton studies: national determinants and international comparisons. Brazilian Journal of Biology , 75(1): 216-223.; Vaz 2015Vaz, U.L.; Cunha, H.F. & Nabout, J.C. 2015. Trends and biases in global scientific literature about ecological niche models. Brazilian Journal of Biology , 75(4): S17-S24.; Santos 2017Santos, D.; Sampronha, S. & Santos, C.H.D. 2017. Advances on dipterology in the 21st century and extinction rates. Papéis Avulsos de Zoologia , 57(33): 433-444.), and has become an important tool for identifying trends and biases in the scientific production of a given area of study (Drew 2016Drew, C.H.; Pettibone, K.G.; Finch 3rd, F.O.; Giles, D. & Jordan, P. 2016. Automated research impact assessment: a new bibliometrics approach. Scientometrics, 106(3): 987-1005.).

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 (1988-2017) begins in the 1980s, when gall studies were again becoming frequent in Brazil (Moreira, 2006Moreira, G.R.P. 2006. Galhas entomógenas no Brasil: oportunidade de estudo sobre interação inseto-planta. In: Mariath, J.E. & Santos, R.P. (Orgs.). Os avanços da botânica no inicio do século XXI do 57º Congresso Nacional de Botânica. Porto Alegre, Sociedade de Botânica do Brasil. p. 532-537.). 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 2012Nabout, J.C.; Carvalho, P.; Prado, M.U.; Borges, P.P.; Machado, K.B.; Haddad, K.B.; Michelan, T.S.; Cunha, H.F. & Soares, T.N. 2012. Trends and biases in global climate change literature. Natureza & Conservação, 10(1): 45-51.; Vaz 2015Vaz, U.L.; Cunha, H.F. & Nabout, J.C. 2015. Trends and biases in global scientific literature about ecological niche models. Brazilian Journal of Biology , 75(4): S17-S24.). 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.

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

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 (1988Fernandes, G.W. & Price, P.W. 1988. Biogeographical gradients in galling species richness. Oecologia, 76(2): 161-167.) and Fernandes & Price (1992Fernandes, G.W. & Price, P.W. 1992. The adaptive significance of insect gall distribution: survivorship of species in xeric and mesic habitats. Oecologia, 90(1): 14-20.) 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.

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

Table 1
The most frequently cited papers about insect galls in Brazil published from 1988 to 2017 (from CAPES database).

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).

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.

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.

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 (2008-2017). 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 2012Nabout, J.C.; Carvalho, P.; Prado, M.U.; Borges, P.P.; Machado, K.B.; Haddad, K.B.; Michelan, T.S.; Cunha, H.F. & Soares, T.N. 2012. Trends and biases in global climate change literature. Natureza & Conservação, 10(1): 45-51.; Nabout 2015Nabout, J.C.; Carneiro, F.M.; Borges, P.P.; Machado, K.B. & Huszar, V.L.M. 2015. Brazilian scientific production on phytoplankton studies: national determinants and international comparisons. Brazilian Journal of Biology , 75(1): 216-223.; Vaz 2015Vaz, U.L.; Cunha, H.F. & Nabout, J.C. 2015. Trends and biases in global scientific literature about ecological niche models. Brazilian Journal of Biology , 75(4): S17-S24.). Scientometric analyses have also shown a significant increase in zoological scientific production, as has been demonstrated for mammalogy (Brito 2009Brito, D.; Oliveira, L.C.; Oprea, M. & Mello, M.A.R. 2009. An overview of Brazilian mammalogy: trends, biases and future directions. Zoologia, 26(1): 67-73.), carcinology (Nabout 2010Nabout, J.C.; Bini, L.M. & Diniz-Filho, J.A. 2010. Global literature of fiddler crabs, genus Uca (Decapoda, Ocypodidae): trends and future directions. Iheringia Série Zoologia, 100(4): 463-468.) and dipterology (Santos 2017Santos, D.; Sampronha, S. & Santos, C.H.D. 2017. Advances on dipterology in the 21st century and extinction rates. Papéis Avulsos de Zoologia , 57(33): 433-444.). Furthermore, recent scientometric studies have shown substantial growth in the scientific production of Latin American (e.g.,Garcia 2012Garcia, C.R.S.; Parodi, A.J. & Oliva, G. 2012. Growing Latin American science. Science, 338(6111): 1127.), which was also observed for publications on insect galls, mainly due to the large contribution of Brazilian studies (Grandez-Rios 2015Grandez-Rios, J.M.; García-Villacorta, R.; Cuevas-Reyes, P. & Araújo, W.S. 2015. Insectos inductores de agallas en América Latina: ecología, importancia y nuevas perspectivas. Revista de Biologia Neotropical, 12(2): 92-103.).

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 regionalism 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 2015Nabout, J.C.; Carneiro, F.M.; Borges, P.P.; Machado, K.B. & Huszar, V.L.M. 2015. Brazilian scientific production on phytoplankton studies: national determinants and international comparisons. Brazilian Journal of Biology , 75(1): 216-223.). 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 (1988Fernandes, G.W. & Price, P.W. 1988. Biogeographical gradients in galling species richness. Oecologia, 76(2): 161-167.), 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, 2007Espírito-Santo, M.M. & Fernandes, G.W. 2007. How many species of gall-inducing insects are there on earth, and where are they? Annals of the Entomological Society of America, 100(2): 95-99.; Araújo 2014Araújo, W.S.; Santos, B.B.; Guilherme, F.A.G. & Scareli-Santos, C. 2014. Galling insects in the Brazilian Cerrado: ecological patterns and perspectives. In: Fernandes, G.W. & Santos, J.C. Eds.). Neotropical insect Galls. New York, Springer. p. 257-272.; Grandez-Rios 2015Grandez-Rios, J.M.; García-Villacorta, R.; Cuevas-Reyes, P. & Araújo, W.S. 2015. Insectos inductores de agallas en América Latina: ecología, importancia y nuevas perspectivas. Revista de Biologia Neotropical, 12(2): 92-103.), 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, 1994Gagné, R. 1994. The Gall Midges of the Neotropical Region. Ithaca, Cornell University Press. 360 p.).

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 concentrated 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) regarding 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 research 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, 2014Fernandes, G.W. & Santos, J.C. (Eds.). 2014. Neotropical insect galls (Vol. 550). Dordrecht, Springer. 550 p.). 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, 2007Espírito-Santo, M.M. & Fernandes, G.W. 2007. How many species of gall-inducing insects are there on earth, and where are they? Annals of the Entomological Society of America, 100(2): 95-99.; Grandez-Rios 2015Grandez-Rios, J.M.; García-Villacorta, R.; Cuevas-Reyes, P. & Araújo, W.S. 2015. Insectos inductores de agallas en América Latina: ecología, importancia y nuevas perspectivas. Revista de Biologia Neotropical, 12(2): 92-103.), 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.

ACKNOWLEDGEMENTS

The author would like to thank Jean Carlos Santos, Charles Morphy D. Santos and one anonymous reviewer for suggestions on the manuscript and Erik Wild for English revision. This work was prepared as a presentation in the “IV Simpósio Brasileiro Sobre Galhas e Galhadores” of the “XXXII Congresso Brasileiro de Zoologia”.

REFERENCES

  • Alcântara, J.A.; Souza, E.B. & Braga, P.E.T. 2017. Ocorrência e caracterização de galhas em duas áreas do noroeste do Ceará, Brasil. Natureza On-Line, 15(1): 33-40.
  • Almada, E.D. & Fernandes, G.W.A. 2011. Insetos indutores de galhas em florestas de terra firme e em reflorestamentos com espécies nativas na Amazônia Oriental, Pará, Brasil. Boletim do Museu Paraense Emílio Goeldi Ciências Naturais, 6(2): 163-196.
  • Araújo, W.S.; Santos, B.B. & Gomes-Klein, V.L. 2011. Insect galls from Serra dos Pireneus, GO, Brazil. Biota Neotropica, 11(2): 357-365.
  • Araújo, W.S.; Santos, B.B.; Guilherme, F.A.G. & Scareli-Santos, C. 2014. Galling insects in the Brazilian Cerrado: ecological patterns and perspectives. In: Fernandes, G.W. & Santos, J.C. Eds.). Neotropical insect Galls. New York, Springer. p. 257-272.
  • Bergamini, B.A.R.; Bergamini, L.L.; Santos, B.B. & Araújo, W.S. 2017. Occurrence and characterization of insect galls in the Floresta Nacional de Silvânia, Brazil. Papéis Avulsos de Zoologia, 57(32): 413-431.
  • Borges, P.P.; Andrade Oliveira, K.A.F.; Machado, K.B.; Vaz, Ú.L., Cunha, H.F. & Nabout, J.C. 2015. Trends and gaps of the scientific literature on the Cerrado biome: A scientometric analysis. Neotropical Biology and Conservation, 10(1): 2-8.
  • Bregonci, J.D.M.; Polycarpo, P.V. & Maia, V.C. 2010. Insect galls of the Parque Estadual Paulo César Vinha (Guarapari, ES, Brazil). Biota Neotropica , 10(1): 265-274.
  • Brito, D.; Oliveira, L.C.; Oprea, M. & Mello, M.A.R. 2009. An overview of Brazilian mammalogy: trends, biases and future directions. Zoologia, 26(1): 67-73.
  • Carneiro, M.A.A.; Branco, C.S.; Braga, C.E.; Almada, E.D.; Costa, M.; Maia, V.C. & Fernandes, G.W. 2009. Are gall midge species (Diptera, Cecidomyiidae) host-plant specialists? Revista Brasileira de Entomologia, 53(3): 365-378.
  • Carvalho-Fernandes, S.P.; Almeida-Cortez, J.S.D. & Ferreira, A.L.N. 2012. The insect gall richness in preserved and anthropic areas of caatinga. Revista Árvore, 36(2): 269-277.
  • Carvalho-Fernandes, S.P.; Ascendino, S.; Maia, V.C. & Couri, M.S. 2016. Diversity of insect galls associated with coastal shrub vegetation in Rio de Janeiro, Brazil. Anais da Academia Brasileira de Ciências, 88(3): 1407-1418.
  • Carvalho-Fernandes, S.P.; Castelo-Branco, B.P.; Albuquerque, F.A.; Brito-Ramos, A.B.; Ferreira, A.L.N.; Braga, D.V.V. & Almeida-Cortez, J.S. 2009. Galhas entomógenas em um fragmento urbano de Mata Atlântica no centro de endemismo de Pernambuco. Revista Brasileira de Biociências, 7(3): 240-244.
  • Coelho, M.S.; Almada, E.D.; Fernandes, G.W.; Carneiro, M.A.A.; Santos, R.M.D.; Quintino, A.V. & Sanchez-Azofeifa, A. 2009. Gall inducing arthropods from a seasonally dry tropical forest in Serra do Cipó, Brazil. Revista Brasileira de Entomologia , 53(3): 404-414.
  • Coelho, M.S.; Carneiro, M.A.A.; Branco, C.; Borges, R.A.X. & Fernandes, G.W. 2013. Gall-inducing insects from Campos de Altitude, Brazil. Biota Neotropica , 13(4): 139-151.
  • Costa, E.C.; Carvalho-Fernandes, S.P. & Santos-Silva, J. 2014. Galhas de insetos em uma área de transição caatinga-cerrado no Nordeste do Brasil. Sitientibus, Série Ciências Biológicas, 14(1): 1-9.
  • Drew, C.H.; Pettibone, K.G.; Finch 3rd, F.O.; Giles, D. & Jordan, P. 2016. Automated research impact assessment: a new bibliometrics approach. Scientometrics, 106(3): 987-1005.
  • Espírito-Santo, M.M. & Fernandes, G.W. 2007. How many species of gall-inducing insects are there on earth, and where are they? Annals of the Entomological Society of America, 100(2): 95-99.
  • Fernandes, G.W. 1998. Hypersensitivity as a phenotypic basis of plant induced resistance against a galling insect (Diptera: Cecidomyiidae). Environmental Entomology, 27(2): 260-267.
  • Fernandes, G.W. & Negreiros, D. 2006. A comunidade de insetos galhadores da RPPN fazenda bulcão, Aimorés, Minas Gerais, Brasil. Lundiana, 7(2): 111-120.
  • Fernandes, G.W. & Negreiros, D. 2008. The occurrence and effectiveness of hypersensitive reaction against galling herbivores across host taxa. Ecological Entomology, 26(1): 46-55.
  • Fernandes, G.W. & Price, P.W. 1988. Biogeographical gradients in galling species richness. Oecologia, 76(2): 161-167.
  • Fernandes, G.W. & Price, P.W. 1992. The adaptive significance of insect gall distribution: survivorship of species in xeric and mesic habitats. Oecologia, 90(1): 14-20.
  • Fernandes, G.W. & Santos, J.C. (Eds.). 2014. Neotropical insect galls (Vol. 550). Dordrecht, Springer. 550 p.
  • Fernandes, G.W.; Araújo, R.C.; Araújo, S.C.; Lombardi, J.A.; Silva De Paula, A.; Júnior, R.L. & Cornelissen, T.G. 1997. Insect galls from savanna and rocky fields of the Jequitinhonha Valley, Minas Gerais, Brazil. Naturalia, 22(1): 221-244.
  • Fernandes, G.W.; Carneiro, M.A.A.; Lara, A.C.F.; Allain, L.R.; Andrade, G.I.; Julião, G.R.; Reis, T.R. & Silva, I.M. 1996. Galling insects on neotropical species of Baccharis (Asteraceae). Tropical Zoology, 9(2): 315-332.
  • Fernandes, G.W.; Julião, G.R.; Araújo, R.C.; Araújo, S.C.; Lombardi, J.A.; Negreiros, D. & Carneiro, M.A.A. 2001. Distribution and morphology of insect galls of the Rio Doce Valley, Brazil. Naturalia, 26(1): 211-244.
  • Fernandes, G.W.A.; Tameirão-Neto, E. & Martins, R.P. 1988. Ocorrência e caracterização de galhas entomógenas na vegetação do campus Pampulha da Universidade Federal de Minas Gerais. Revista Brasileira de Zoologia, 5(1): 11-29.
  • Gagné, R. 1994. The Gall Midges of the Neotropical Region. Ithaca, Cornell University Press. 360 p.
  • Garcia, C.R.S.; Parodi, A.J. & Oliva, G. 2012. Growing Latin American science. Science, 338(6111): 1127.
  • Gonçalves-Alvim, S.J. & Fernandes, G.W. 2001. Biodiversity of galling insects: historical, community and habitat effects in four neotropical savannas. Biodiversity & Conservation, 10(1): 79-98.
  • Grandez-Rios, J.M.; García-Villacorta, R.; Cuevas-Reyes, P. & Araújo, W.S. 2015. Insectos inductores de agallas en América Latina: ecología, importancia y nuevas perspectivas. Revista de Biologia Neotropical, 12(2): 92-103.
  • Julião, G.R.; Amaral, M. & Fernandes, G.W. 2002. Galhas de insetos e suas plantas hospedeiras no Pantanal sul-mato-grossense. Naturalia, 27(1): 47-74.
  • Luz, R.G.; Fernandes, G.W.; Silva, J.O.; Neves, F.S. & Fagundes, M. 2012. Galhas de insetos em habitats xérico e mésico em região de transição Cerrado-Caatinga no norte de Minas Gerais, Brasil. Neotropical Biology & Conservation, 7(3): 171-187.
  • Maia, V. & Oliveira, J. 2010. Galhas de insetos da Reserva Biológica Estadual da Praia do Sul (Ilha Grande, Angra dos Reis, RJ). Biota Neotropica , 10(4): 227-238.
  • Maia, V.C. 2001. The gall midges (Diptera, Cecidomyiidae) from three restingas of Rio de Janeiro State, Brazil. Revista Brasileira de Zoologia , 18(2): 583-629.
  • Maia, V.C. 2005. Catálogo dos Cecidomyiidae (Diptera) do estado do Rio de Janeiro. Biota Neotropica , 5(2): 189-203.
  • Maia, V.C. 2011. Characterization of insect galls, gall makers, and associated fauna of Platô Bacaba (Porto de Trombetas, Pará, Brazil). Biota Neotropica , 11(4): 37-53.
  • Maia, V.C. 2013. Insect galls of São Tomé das Letras (MG, Brazil). Biota Neotropica , 13(4): 164-189.
  • Maia, V.C. 2014. Insect galls of Itamonte (Minas Gerais, Brazil): characterization and occurrence. Biota Neotropica , 14(1): e20133839.
  • Maia, V.C. & Carvalho-Fernandes, S.P. 2016. Insect galls of a protected remnant of the Atlantic Forest tableland from Rio de Janeiro State (Brazil). Revista Brasileira de Entomologia , 60(1): 40-56.
  • Maia, V.C. & Fernandes, G.W. 2004. Insect galls from Serra de São José (Tiradentes, MG, Brazil). Brazilian Journal of Biology, 6(3a): 423-445.
  • Maia, V.C. & Silva, L.O. 2016. Insect galls of Restinga de Marambaia (Barra de Guaratiba, Rio de Janeiro, RJ). Brazilian Journal of Biology , 76(3): 787-795.
  • Maia, V.C. & Souza, M.C. 2013. Insect galls of the xeric vegetation of Ilha do Cabo Frio (Arraial do Cabo, RJ, Brazil). Biota Neotropica , 13(3): 278-288.
  • Maia, V.C.; Cardoso, L.J.T. & Braga, J.M.A. 2014. Insect galls from Atlantic Forest areas of Santa Teresa, Espírito Santo, Brazil: characterization and occurrence. Boletim do Museu de Biologia Mello Leitão, 33(1): 47-129.
  • Maia, V.C.; Galvão-Magenta, M.A. & Martins, E.S. 2008. Ocorrência e caracterização de galhas de insetos em áreas de restinga de Bertioga (São Paulo, Brasil). Biota Neotropica , 8(1): 167-197.
  • Malves, K. & Frieiro-Costa, F.A. 2012. List of plants with galls induced by insects from the UNILAVRAS/Boqueirão Biological Reserve, Ingaí, State of Minas Gerais, Brazil. Check List, 8(3): 426-431.
  • Moreira, G.R.P. 2006. Galhas entomógenas no Brasil: oportunidade de estudo sobre interação inseto-planta. In: Mariath, J.E. & Santos, R.P. (Orgs.). Os avanços da botânica no inicio do século XXI do 57º Congresso Nacional de Botânica. Porto Alegre, Sociedade de Botânica do Brasil. p. 532-537.
  • Moreira, R.G.; Fernandes, G.W.; Almada, E.D. & Santos, J.C. 2007. Galling insects as bioindicators of land restoration in an area of Brazilian Atlantic Forest. Lundiana, 8(2): 107-112.
  • Nabout, J.C.; Bini, L.M. & Diniz-Filho, J.A. 2010. Global literature of fiddler crabs, genus Uca (Decapoda, Ocypodidae): trends and future directions. Iheringia Série Zoologia, 100(4): 463-468.
  • Nabout, J.C.; Carneiro, F.M.; Borges, P.P.; Machado, K.B. & Huszar, V.L.M. 2015. Brazilian scientific production on phytoplankton studies: national determinants and international comparisons. Brazilian Journal of Biology , 75(1): 216-223.
  • Nabout, J.C.; Carvalho, P.; Prado, M.U.; Borges, P.P.; Machado, K.B.; Haddad, K.B.; Michelan, T.S.; Cunha, H.F. & Soares, T.N. 2012. Trends and biases in global climate change literature. Natureza & Conservação, 10(1): 45-51.
  • Oliveira, J.D. & Maia, V.C. 2005. Ocorrência e caracterização de galhas de insetos na restinga de Grumari (Rio de Janeiro, RJ, Brasil). Arquivos do Museu Nacional, 63(4): 669-675.
  • Oliveira, P.S. 1997. The ecological function of extrafloral nectaries: herbivore deterrence by visiting ants and reproductive output in Caryocar brasiliense (Caryocaraceae). Functional Ecology, 11(3): 323-330.
  • Price, P.W.; Fernandes, G.W.; Lara, A.C.F.; Brawn, J.; Barrios, H.; Wright, M.G.; Ribeiro, S.P. & Rothcliff, N. 1998. Global patterns in local number of insect galling species. Journal of Biogeography, 25(3): 581-591.
  • Rodrigues, A.R.; Maia, V.C. & Couri, M.S. 2014. Insect galls of restinga areas of Ilha da Marambaia, Rio de Janeiro, Brazil. Revista Brasileira de Entomologia , 58(2): 173-197.
  • Saito, V.S. & Urso-Guimarães, M.V. 2012. Characterization of galls, insect galls and associated fauna of Ecological Station of Jataí (Luiz Antônio, SP). Biota Neotropica , 12(3): 99-107.
  • Santos, B.B.; Ferreira, H.D. & de Araújo, W.S. 2010. Ocorrência e caracterização de galhas entomógenas em uma área de floresta estacional semidecídua em Goiânia, Goiás, Brasil. Acta Botânica Brasilica, 24(1): 243-249.
  • Santos, B.B.; Ribeiro, B.A.; Silva, T.M. & Araújo, W. 2012. Galhas de insetos em uma área de cerrado sentido restrito na região semi-urbana de Caldas Novas (Goiás, Brasil). Revista Brasileira de Biociências , 10(4): 439-445.
  • Santos, D.; Sampronha, S. & Santos, C.H.D. 2017. Advances on dipterology in the 21st century and extinction rates. Papéis Avulsos de Zoologia , 57(33): 433-444.
  • Santos, J.C.; Almeida-Cortez, J.S. & Fernandes, G.W. 2011. Diversity of gall-inducing insects in the high altitude wetland forests in Pernambuco, Northeastern Brazil. Brazilian Journal of Biology , 71(1): 47-56.
  • Silva, T.M.; Araújo, W.S. & Santos, B.B. 2015. Ocorrência e caracterização de galhas de insetos em um fragmento de mata semicaducifólia do Campus Samambaia, Goiânia, GO, Brasil. Revista de Biologia Neotropical , 12(1): 26-38.
  • Toma, T.S.P. & Mendonça Jr., M.S. 2013. Gall-inducing insects of an Araucaria Forest in southern Brazil. Revista Brasileira de Entomologia , 57(2): 225-233.
  • Urso-Guimarães, M.V. & Scareli-Santos, C. 2006. Galls and gall makers in plants from the Pé-de-Gigante Cerrado reserve, Santa Rita do Passa Quatro, SP, Brazil. Brazilian Journal of Biology , 66(1B): 357-369.
  • Urso-Guimarães, M.V.; Castello, A.C.D.; Kataoka, E.Y. & Koch, I. 2017. Characterization of entomogen galls from Mato Grosso do Sul, Brazil. Revista Brasileira de Entomologia , 61(1): 25-42.
  • Urso-Guimarães, M.V.; Scareli-Santos, C. & Bonifácio-Silva, A.C. 2003. Occurrence and characterization of entomogen galls in plants from natural vegetation areas in Delfinópolis, MG, Brazil. Brazilian Journal of Biology , 63(4): 705-715.
  • Vaz, U.L.; Cunha, H.F. & Nabout, J.C. 2015. Trends and biases in global scientific literature about ecological niche models. Brazilian Journal of Biology , 75(4): S17-S24.

SUPPLEMENTARY MATERIAL 1

List of papers about insect galls and galling species in Brazil published in peer-reviewed journals between 1988 and 2017 compiled from papers indexed in the platform “Portal de Periódicos Capes” (www.periodicos.capes.gov.br).

SUPPLEMENTARY MATERIAL 2

List of inventory papers about insect galls in Brazil compiled from papers indexed in the platform “Portal de Periódicos Capes” (www.periodicos.capes.gov.br), Google Scholar and in the references of the compiled papers.

Publication Dates

  • Publication in this collection
    16 Aug 2018
  • Date of issue
    2018

History

  • Received
    13 Nov 2017
  • Accepted
    24 May 2018
Museu de Zoologia da Universidade de São Paulo Av. Nazaré, 481, Ipiranga, 04263-000 São Paulo SP Brasil, Tel.: (55 11) 2065-8133 - São Paulo - SP - Brazil
E-mail: einicker@usp.br