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

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 et al., 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 et al., 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 et al., 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 et al., 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 et al., 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 et al., 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 et al., 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 et al., 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 et al., 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 et al., 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 et al., 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 et al., 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 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). N Title Year Journal 1 Biogeographical gradients in galling species richness - Tests of hypotheses 1988 Oecologia 2 Adaptive significance of insect gall distribution: survivorship of species in xeric and mesic habitats 1992 Oecologia 3 Utilization of Apion sp. (Coleoptera apionidae) galls by an ant community in southeastern brazil 1995 Tropical Zoology 4 Fire effects on a Palicourea rigida (rubiaceae) gall midge: A test of the plant vigor hypothesis 1996 Biotropica 5 Galling insects on neotropical species of Baccharis (Asteraceae) 1996 Tropical Zoology 6 The highest diversity of galling insects: Serra do Cipó, Brazil 1996 Biodiversity Letters 7 The ecological function of extrafloral nectaries: Herbivore deterrence by visiting ants and reproductive output in Caryocar brasiliense (Caryocaraceae) 1997 Functional Ecology 8 Global patterns in local number of insect galling species 1998 Journal of Biogeography 9 Hypersensitivity as a Phenotypic Basis of Plant Induced Resistance Against a Galling Insect (Diptera: Cecidomyiidae) 1998 Environmental Entomology 10 Natural history of a gall-inducing weevil Collabismus clitellae (Coleoptera: Curculionidae) and some effects on its host plant Solanum lycocarpum (Solanaceae) in southeastern Brazil 1998 Annals of the Entomological Society of America 11 Abundance and impact of a Lepidopteran gall on Macairea radula (Melastomataceae) in the Neotropics 1999 International Journal of Ecology and Environmental Sciences 12 The interplay between plant traits and herbivore attack: A study of a stem galling midge in the neotropics 1999 Ecological Entomology 13 Distance-limited recolonization of burned cerrado by leaf-miners and gallers in central Brazil 2000 Environmental Entomology 14 Biodiversity of galling insects: Historical, community and habitat effects in four neotropical savannas 2001 Biodiversity and Conservation 15 Galling insect diversity patterns: the resource synchronisation hypothesis 2001 Oikos 16 Host plant response and phenotypic plasticity of a galling weevil (Collabismus clitellae: Curculionidae) 2001 Austral Ecology 17 Leaf gall abundance on Avicennia germinans (Avicenniaceae) along an interstitial salinity gradient 2001 Biotropica 18 The occurrence and effectiveness of hypersensitive reaction against galling herbivores across host taxa 2001 Ecological Entomology 19 Vigour of a dioecious shrub and attack by a galling herbivore 2001 Ecological Entomology 20 Host plant effects on the development and survivorship of the galling insect Neopelma baccharidis (Homoptera: Psyllidae) 2002 Austral Ecology 21 Influence of host-plant sex and habitat on survivorship of insect galls within the geographical range of the host-plant 2002 Tropical Zoology 22 Tests of hypotheses on patterns of gall distribution along an altitudinal gradient 2002 Tropical Zoology 23 Complex interactions envolving a gall midge Myrciamyia maricaensis Maia (Diptera, Cecidomyiidae), phytophagous modifiers and parasitoids 2003 Revista Brasileira de Zoologia 24 Galling insects (Diptera: Cecidomyiidae) survive inundation during host plant flooding in Central Amazonia 2003 Biotropica 25 Hypersensitivity of Fagus sylvatica L. against leaf galling insects 2003 Trees 26 Occurrence and characterization of entomogen galls in plants from natural vegetation areas in Delfinópolis, MG, Brazil 2003 Brazilian Journal of Biology 27 A key to genera to Eriococcidae (Hemiptera: Coccoidea) from the Neotropical region and a revision of Pseudotectococcus Hempel (Eriococcidae), a gall inducing scale insect genus from Brazil, with a description of a new species 2004 Lundiana 28 Edge effect and species-area relationships in the gall-forming insect fauna of natural forest patches in the Brazilian Pantanal 2004 Biodiversity and Conservation 29 Effects of genetic variability and habitat of Qualea parviflora (Vochysiaceae) on herbivory by free-feeding and gall-forming insects 2004 Annals of Botany 30 Gall-inducing jumping plant-lice of the Neotropical genus Baccharopelma (Hemiptera, Psylloidea) associated with Baccharis (Asteraceae) 2004 Journal of Natural History 31 Insect galls from Serra de São José (Tiradentes, MG, Brazil) 2004 Brazilian Journal of Biology 32 Novas espécies de Prodecatoma (Hymenoptera, Eurytomidae) associadas a galhas em frutos de duas espécies de Psidium L. (Myrtaceae), com comentários sobre Prodecatoma spermophaga Costa-Lima 2004 Revista Brasileira de Entomologia 33 A new genus and species of gall midge (Diptera: Cecidomyiidae) associated with Waltheria indica L. (Sterculiaceae) 2005 Zootaxa 34 Convergence in the variation of local and regional galling species richness 2005 Neotropical Entomology 35 Insetos galhadores associados a duas espécies de plantas invasoras de áreas urbanas e peri-urbanas 2005 Revista Brasileira de Entomologia 36 Two new species of Asphondyliini (Diptera: Cecidomyiidae) associated with Bauhinia brevipes (Fabaceae) in Brazil 2005 Zootaxa 37 Distribution and frequency of galls induced by Anisodiplosis waltheriae Maia (Diptera: Cecidomyiidae) on the invasive plant Waltheria indica L. (Sterculiaceae) 2006 Neotropical Entomology 38 Diversity of galling arthropods and host plants in a subtropical forest of Porto Alegre, southern Brazil 2006 Neotropical Entomology 39 Effects of host plant architecture on colonization by galling insects 2006 Austral Ecology 40 Influence of Apion sp. (Brentidae, Apioninae) stem-galls on induced resistance and leaf area of Diospyros hispida (Ebenaceae) 2006 Revista Brasileira de Entomologia 41 Insect galls occurring in Miconia prasina (Melastomataceae) in remnants of Atlantic forest of northeastern Brazil 2006 Lundiana 42 Insetos fitófagos associados ao murici da praia, Byrsonima sericea (Malpighiaceae), na Restinga de Jurubatiba (RJ) 2006 Revista Brasileira de Entomologia 43 Processes driving ontogenetic succession of galls in a canopy tree 2006 Biotropica 44 Sex-mediated herbivory by galling insects on Baccharis concinna (Asteraceae) 2006 Revista Brasileira de Entomologia 45 A comunidade de insetos galhadores da RPPN Fazenda Bulcão, Aimorés, Minas Gerais, Brasil 2006 Lundiana 46 Caracterização e distribuição espacial de galhas em Clusia nemorosa G. Mey (Clusiaceae) em uma área de Floresta Atlântica, Igarassu, PE 2007 Lundiana 47 Ecology and impact of Allorhogas sp. (Hymenoptera: Braconidae) and Apion sp. (Coleoptera: Curculionoidea) on fruits of Miconia calvescens DC (Melastomataceae) in Brazil 2007 Biological Control 48 Effect of aib on quality and phytossanity of Caryocar brasiliense Camb (Caryocaraceae) air layering 2007 Revista Arvore 49 Galling insects as bioindicators of land restoration in an area of Brazilian Atlantic forest 2007 Lundiana 50 How Many Species of Gall-Inducing Insects Are There on Earth, and Where Are They? 2007 Annals of the Entomological Society of America 51 Impact of a gall midge Parkiamyia paraensis (Diptera, Cecidomyiidae) on the Amazonian plant Parkia pendula (Fabaceae) 2007 Revista Brasileira de Entomologia 52 Plant architecture and meristem dynamics as the mechanisms determining the diversity of gall-inducing insects 2007 Oecologia 53 Asphondylia gochnatiae, a new species of gall midge (Diptera, Cecidomyiidae) associated with Gochnatia polymorpha (Less.) Cabrera (Asteraceae) 2008 Zootaxa 54 Ocorrência e caracterização de galhas de insetos em áreas de restinga de Bertioga (São Paulo, Brasil) 2008 Biota Neotropica 55 Phytotoxicity of the extracts of Lonchocarpus muehlbergianus Hassl. (Fabaceae) leaflets and galls on seed germination and early development of lettuce 2008 Acta Botanica Brasilica 56 Plant organ abscission and the green island effect caused by gallmidges (Cecidomyiidae) on tropical trees 2008 Arthropod-Plant Interactions 57 Relationships between host plant architecture and gall abundance and survival 2008 Revista Brasileira de Entomologia 58 Species-specific changes in tissue morphogenesis induced by two arthropod leaf gallers in Lantana camara L. (Verbenaceae) 2008 Australian Journal of Botany 59 A new genus and species of gall midge (Diptera, Cecidomyiidae) associated with Myrcia retorta (Myrtaceae) 2009 Revista Brasileira de Entomologia 60 Are gall midge species (Diptera, Cecidomyiidae) host-plant specialists? 2009 Revista Brasileira de Entomologia 61 Asphondylia fructicola, a new species of Cecidomyiidae (Diptera) associated with Solanum sp. (Solanaceae) from Brazil 2009 Revista Brasileira de Entomologia 62 Efeitos da sazonalidade e do tamanho da planta hospedeira na abundância de galhas de Cecidomyiidae (Diptera) em Piper arboreum (Piperaceae) 2009 Revista Brasileira de Entomologia 63 Gall inducing arthropods from a seasonally dry tropical forest in Serra do Cipó, Brazil 2009 Revista Brasileira de Entomologia 64 Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, Minas Gerais, Brasil 2009 Revista Brasileira de Entomologia 65 Gall midge attack intensity and host-plant response in a Neotropical coastal ecosystem 2009 Revista Brasileira de Entomologia 66 Grape phylloxera in Brazil 2009 Acta Horticulturae 67 Influence of leaflet age in anatomy and possible adaptive values of the midrib gall of Copaifera langsdorffii (Fabaceae: Caesalpinioideae) 2009 Revista de Biologia Tropical 68 Intra-specific phenotypic variations in Lantana camara leaves affect host selection by the gall maker Aceria lantanae 2009 Biochemical Systematics and Ecology 69 Complexidade estrutural e diversidade de insetos galhadores em Styrax pohlii Fritsch (Styracaceae) 2009 Bioscience Journal 70 Two new gall-inducing genera and species of Eriococcidae (Hemiptera) on Malvaceae and Anacardiaceae from the Neotropics 2009 Lundiana 71 Within tree distribution of a gall-inducing Eurytoma (Hymenoptera, Eurytomidae) on Caryocar brasiliense (Caryocaraceae) 2009 Revista Brasileira de Entomologia 72 Description of the female, pupa and gall of Pisphondylia brasiliensis Couri and Maia, 1992 (Diptera: Cecidomyiidae, Schizomyiina) with new records 2010 Brazilian Journal of Biology 73 First record of galls in hog plum (Spondias mombim L.) panicles caused by Clinodiplosis (Diptera: Cecidomyiidae) and evaluation of genotypes in the State of Piauí 2010 Revista Brasileira de Fruticultura 74 Gall midges (Diptera, Cecidomyiidae) associated with Aldina heterophylla spr. ex Benth. (Fabaceae) from Brazil 2010 Biota Neotropica 75 Gall-inducing insect species richness as indicators of forest age and Health 2010 Environmental Entomology 76 Insect galls of the Parque Estadual Paulo César Vinha (Guarapari, ES, Brazil) 2010 Biota Neotropica 77 Ocorrência e caracterização de galhas entomógenas em uma área de floresta estacional semidecídua em Goiânia, Goiás, Brasil 2010 Acta Botanica Brasilica 78 Pattern of attack of a galling insect reveals an unexpected preference-performance linkage on medium-sized resources 2010 Revista Brasileira de Entomologia 79 Photosynthetic efficiency of Clusia arrudae leaf tissue with and without Cecidomyiidae galls 2010 Brazilian Journal of Biology 80 Redifferentiation of leaflet tissues during midrib gall development in Copaifera langsdorffii (Fabaceae) 2010 South African Journal of Botany 81 Two new species of Lopesia Rübsaamen (Diptera, Cecidomyiidae) from Brazil, with an identification key of species 2010 Biota Neotropica 82 A new genus and species of gall midge (Diptera, Cecidomyiidae) associated with Microgramma vacciniifolia (Langsd. & Fisch.) Copel. (Polypodiaceae) from Brazil 2011 Revista Brasileira de Entomologia 83 Abundance of gall-inducing insect species in sclerophyllous savanna: Understanding the importance of soil fertility using an experimental approach 2011 Journal of Tropical Ecology 84 Burseramyia braziliensis, a new species of gall midge (Diptera, Cecidomyiidae, Asphondyliini) associated with Swartzia langsdorffii Raddi (Fabaceae) 2011 Biota Neotropica 85 Calophya latiforceps, a new species of jumping plant lice (Hemiptera: Calophyidae) associated with Schinus terebinthifolius (Anacardiaceae) in Brazil 2011 Florida Entomologist 86 Can host plant richness be used as a surrogate for galling insect diversity? 2011 Tropical Conservation Science 87 Characterization of insect galls, gall makers, and associated fauna of Platô Bacaba (Porto de Trombetas, Pará, Brazil) 2011 Biota Neotropica 88 Cytological and histochemical gradients on two Copaifera langsdorffii Desf. (Fabaceae)-Cecidomyiidae gall systems 2011 Protoplasma 89 Differential female attack and larval performance of a galling cecidomyiid on the host, Astronium fraxinifolium (Anacardiaceae), in contrasting habitats 2011 Entomological News 90 Distribution of a leaf vein gall in Caryocar Brasiliense (Caryocaraceae) tree 2011 Revista Caatinga 91 Diversity of gall-inducing insects in the high altitude wetland forests in Pernambuco, Northeastern Brazil 2011 Brazilian Journal of Biology 92 Diversity of galling insects in Styrax pohlii (Styracaceae): Edge effect and use as bioindicators 2011 Revista de Biologia Tropical 93 Fire increases insect herbivory in a neotropical savanna 2011 Biotropica 94 Herbivory, pathogens, and epiphylls in araucaria forest and ecologically-managed tree monocultures 2011 Forest Ecology and Management 95 Insect galls from Serra dos Pireneus, GO, Brazil Galhas de insetos da Serra dos Pireneus, GO, Brasil 2011 Biota Neotropica 96 Insect herbivores associated with Baccharis dracunculifolia (Asteraceae): Responses of gall-forming and free-feeding insects to latitudinal variation 2011 Revista de Biologia Tropical 97 Richness of gall-inducing insects in the tropical dry forest (caatinga) of Pernambuco 2011 Revista Brasileira de Entomologia 98 Size, age and composition: Characteristics of plant taxa as diversity predictors of gall-midges (Diptera: Cecidomyiidae) 2011 Revista de Biologia Tropical 99 Spatial distribution of a spherical gall (Hymenoptera, Eulophidae) on Caryocar brasiliense (Caryocaraceae) 2011 Revista Brasileira de Entomologia 100 Two new species of gall midges (Diptera, Cecidomyiidae) associated with Erythroxylum ovalifolium Peyr. (Erythroxylaceae) from the barra de Maricá restinga, Maricá, Rio de Janeiro, Brazil 2011 Brazilian Journal of Biology 101 Characterization of galls, insect galls and associated fauna of Ecological Station of Jataí (Luiz Antônio, SP) 2012 Biota Neotropica 102 Edge effect benefits galling insects in the Brazilian Amazon 2012 Biodiversity and Conservation 103 Eugeniamyia dispar in Surinam cherry: Associated parasitoids, population dynamics and distribution of plant galls 2012 Revista Brasileira de Fruticultura 104 Gall-inducing insects from Atlantic forest of Pernambuco, Northeastern Brazil 2012 Biota Neotropica 105 Distribuição de insetos galhadores em diferentes formações vegetais e paisagens do cerrado brasileiro 2012 Bioscience Journal 106 Herbivory among habitats on the Neotropical tree Cnidoscolus quercifolius Pohl. in a seasonally deciduous forest 2012 Brazilian Journal of Biology 107 Galhas de insetos em habitats xérico e mésico em região de transição Cerrado-Caatinga no norte de Minas Gerais, Brasil 2012 Neotropical Biology and Conservation 108 List of plants with galls induced by insects from the UNILAVRAS/Boqueirão Biological Reserve, Ingaí, state of Minas Gerais, Brazil 2012 Check List 109 Mutualism from the inside: Coordinated development of plant and insect in an active pollinating fig wasp 2012 Arthropod-Plant Interactions 110 Population ecology of the multivoltine Neotropical gall midge Eugeniamyia dispar (Diptera, Cecidomyiidae) 2012 Iheringia Série Zoologia 111 Population structure and genetic diversity analysis in Gynaikothrips uzeli (Zimerman, 1909) (Thysanoptera: Phlaeothripidae) by RAPD markers 2012 Bulletin of Entomological Research 112 Relationship between host plant diversity and gall-inducing insect’s richness in the Brazilian Cerrado 2012 Neotropical Biology and Conservation 113 Richness of hymenopterous galls from South America 2012 Papéis Avulsos de Zoologia 114 Seasonal variation of natural mortality factors of the guava psyllid Triozoida limbata 2012 Bulletin of Entomological Research 115 Source-sink relationship and photosynthesis in the horn-shaped gall and its host plant Copaifera langsdorffii Desf. (Fabaceae) 2012 South African Journal of Botany 116 Stem galls drain nutrients and decrease shoot performance in Diplusodon orbicularis (Lythraceae) 2012 Arthropod-Plant Interactions 117 A new gall-inducing genus and species of Eriococcidae (Hemiptera: Sternorrhyncha: Coccoidea) on Sapindaceae from Brazil 2013 Zootaxa 118 A new genus and species of Lasiopteridi (Diptera, Cecidomyiidae) associated with Myrciaria delicatula (Myrtaceae) from Brazil, with identification keys of tribes and unplaced genera 2013 Biota Neotropica 119 Biology and systematics of gall-inducing triozids (Hemiptera: Psylloidea) associated with Psidium spp. (Myrtaceae) 2013 Zootaxa 120 Comparing galling insect richness among Neotropical savannas: Effects of plant richness, vegetation structure and super-host presence 2013 Biodiversity and Conservation 121 Gall-inducing insects from Campos de Altitude, Brazil Insetos indutores de galhas de Campos de Altitude, Brazil 2013 Biota Neotropica 122 Gall-inducing insects from Serra do Cabral, Minas Gerais, Brazil 2013 Biota Neotropica 123 Gall-inducing insects of an araucaria forest in southern Brazil 2013 Revista Brasileira de Entomologia 124 Host plants of insect-induced galls in areas of cerrado in the state of Goiás, Brazil 2013 Acta Botanica Brasilica 125 Insect galls from restingas of Southeastern Brazil, with new records 2013 Biota Neotropica 126 Insect galls of São Tomé das Letras (MG, Brazil) 2013 Biota Neotropica 127 Insect galls of the xeric vegetation of Ilha do Cabo Frio (Arraial do Cabo, RJ, Brazil) 2013 Biota Neotropica 128 Seasonal abundance of galling insects (Hymenoptera) on Caryocar brasiliense (Malpighiales: Caryocaraceae) trees in the cerrado 2013 Florida Entomologist 129 Synchronism between Aspidosperma macrocarpon (Apocynaceae) resources allocation and the establishment of the gall inducer Pseudophacopteron sp.(Hemiptera: Psylloidea) 2013 Revista de Biologia Tropical 130 The effect of fluctuating asymmetry and leaf nutrients on gall abundance and survivorship 2013 Basic and Applied Ecology 131 The genus Dasineura Rondani, 1840 (Diptera, Cecidomyiidae) in Brazil 2013 Brazilian Journal of Biology 132 Water stress and phenological synchronism between Copaifera langsdorffii (Fabaceae) and multiple galling insects: Formation of seasonal patterns 2013 Journal of Plant Interactions 133 Confirmation bias leads to overestimation of losses of woody plant foliage to insect herbivores in tropical regions 2014 PeerJ 134 Galling insects are bioindicators of environmental quality in a conservation unit 2014 Acta Botanica Brasilica 135 Habitat conversion and galling insect richness in tropical rainforests under mining effect 2014 Journal of Insect Conservation 136 Insect galls of Itamonte (Minas Gerais, Brazil): Characterization and occurrence 2014 Biota Neotropica 137 Insect galls of restinga areas of Ilha da Marambaia, Rio de Janeiro, Brazil 2014 Revista Brasileira de Entomologia 138 Insect galls of the Parque Nacional das Emas (Mineiros, GO, Brazil) 2014 Check List 139 Leptocybe invasa (Hymenoptera: Eulophidae), an exotic pest of Eucalyptus, in minas Gerais state, Brazil 2014 Florida Entomologist 140 Local and regional determinants of galling-insect richness in neotropical savanna 2014 Journal of Tropical Ecology 141 Native range density, host utilisation and life history of Calophya latiforceps (Hemiptera: Calophyidae): An herbivore of Brazilian Peppertree (Schinus terebinthifolia) 2014 Biocontrol Science and Technology 142 Patterns of cell elongation in the determination of the final shape in galls of Baccharopelma dracunculifoliae (Psyllidae) on Baccharis dracunculifolia DC (Asteraceae) 2014 Protoplasma 143 Redescription of Japanagromyza inferna Spencer, first recorded from Brazil, and a key to the Neotropical species of Japanagromyza Sasakawa (Diptera, Agromyzidae) 2014 ZooKeys 144 Same but different: Larval development and gall-inducing process of a non-pollinating fig wasp compared to that of pollinating fig-wasps 2014 Acta Oecologica 145 Senescent stem-galls in trees of Eremanthus erythropappus as a resource for arboreal ants 2014 Revista Brasileira de Entomologia 146 Structure of floral galls of Byrsonima sericea (Malpighiaceae) induced by Bruggmanniella byrsonimae (Cecidomyiidae, Diptera) and their effects on host plants 2014 Plant Biology 147 Temporal Variation in the Sex Ratio of a Natural Population of a Multivoltine Gall-Inducing Braconid Wasp 2014 Journal of Insect Behavior 148 The insect gall collection of the museu nacional/universidade federal do rio de janeiro: Biome cerrado, rupestrian fields 2014 Brazilian Journal of Biology 149 Unexpected high diversity of galling insects in the Amazonian upper canopy: The savanna out there 2014 PLoS ONE 150 Checklist of host plants of insect galls in the state of Goiás in the Midwest Region of Brazil 2015 Biodiversity Data Journal 151 Cytological cycles and fates in Psidium myrtoides are altered towards new cell metabolism and functionalities by the galling activity of Nothotrioza myrtoidis 2015 Protoplasma 152 Descriptions of two new Pseudophacopteron species (Hemiptera: Psylloidea: Phacopteronidae) inducing galls on Aspidosperma (Apocynaceae) in Brazil 2015 Acta Entomologica Musei Nationalis Pragae 153 Detection and distribution of cell growth regulators and cellulose microfibrils during the development of Lopesia sp. galls on Lonchocarpus cultratus (Fabaceae) 2015 Botany 154 Multivesicular bodies differentiate exclusively in nutritive fast-dividing cells in Marcetia taxifolia galls 2015 Protoplasma 155 New Species Diversity Revealed from Molecular and Morphological Characterization of Gall-Inducing Calophya spp. (Hemiptera: Calophyidae) from Brazilian Peppertree 2015 Florida Entomologist 156 Phenotypic plasticity and similarity among gall morphotypes on a superhost, Baccharis reticularia (Asteraceae) 2015 Plant Biology 157 Population dynamics of the gall inducer Eriogallococcus isaias (Hemiptera: Coccoidea: Eriococcidae) on Pseudobombax grandiflorum (Malvaceae) 2015 Journal of Natural History 158 Questioning the environmental stress hypothesis for gall diversity of restinga vegetation on dunes 2015 Revista de Biologia Tropical 159 The imbalance of redox homeostasis in arthropod-induced plant galls: Mechanisms of stress generation and dissipation 2015 Biochimica et biophysica acta. G, General subjects 160 Clinodiplosis agerati (Diptera, Cecidomyiidae), a new galling species associated with Ageratum conyzoides (Asteraceae) from Brazil 2016 Brazilian Journal of Biology 161 Galling Insect Species Richness and Leaf Herbivory in an Abrupt Transition between Cerrado and Tropical Dry Forest 2016 Annals of the Entomological Society of America 162 Galls in Schinus polygamus (Anacardiaceae): effects of forest structure on infestation intensity 2016 Brazilian Journal of Botany 163 Galls induced by Calophya latiforceps (Hemiptera: Calophyidae) reduce leaf performance and growth of Brazilian peppertree 2016 Biocontrol Science and Technology 164 Holopothrips molzi sp. n. (Thysanoptera, Phlaeothripidae): Natural history and interactions in Myrtaceae galls 2016 Zootaxa 165 How detrimental are seed galls to their hosts? Plant performance, germination, developmental instability and tolerance to herbivory in Inga laurina, a leguminous tree 2016 Plant Biology 166 Insect galls from Serra Geral, Caetité, Ba, Brazil 2016 Biota Neotropica 167 Insect galls of a protected remnant of the Atlantic Forest tableland from Rio de Janeiro State (Brazil) 2016 Revista Brasileira de Entomologia 168 Insect galls of Restinga de Marambaia (Barra de Guaratiba, Rio de Janeiro, RJ) 2016 Brazilian Journal of Biology 169 Insect galls on Mikania glomerata (Asteraceae) in an area of atlantic forest in Viçosa (Minas Gerais, Brazil) 2016 Check List 170 Manipulation of host plant cells and tissues by gall-inducing insects and adaptive strategies used by different feeding guilds 2016 Journal of Insect Physiology 171 Shifts in Plant Assemblages Reduce the Richness of Galling Insects Across Edge-Affected Habitats in the Atlantic Forest 2016 Environmental Entomology 172 The gall inducing insect community on Baccharis concinna (Asteraceae): The role of shoot growth rates and seasonal variations 2016 Lundiana 173 Where host plant goes, galls go too: New records of the Neotropical galling Cecidomyiidae (Diptera) associated with Calophyllum brasiliense Cambess. (Calophyllaceae) 2016 Check List 174 Cecidonius pampeanus, gen. et sp. n.: an overlooked and rare, new gall-inducing micromoth associated with Schinus in southern Brazil (Lepidoptera, Cecidosidae) 2017 ZooKeys 175 Characterization of entomogen galls from Mato Grosso do Sul, Brazil 2017 Revista Brasileira de Entomologia 176 Differences in leaf nutrients and developmental instability in relation to induced resistance to a gall midge 2017 Arthropod-Plant Interactions 177 Experimentally reducing species abundance indirectly affects food web structure and robustness 2017 Journal of Animal Ecology 178 Neolasioptera pantaneira, a new species of cecidomyiidae (Diptera) associated with Aeschynomene denticulata (Fabaceae) from Brazil 2017 Brazilian Journal of Biology 179 Patterns gall infestation in Heteropterys byrsonimifolia A. Juss. in a forest-savannah ecotone 2017 Revista Ceres 180 Plant species richness mediates the effects of vegetation structure, but not soil fertility, on insect gall richness in a savanna in Brazil 2017 Journal of Tropical Ecology 181 The role of senescent stem-galls over arboreal ant communities structure in Eremanthus erythropappus (DC.) MacLeish (Asteraceae) trees 2017 Sociobiology 182 Understory host plant and insect gall diversity changes across topographic habitats differing in nutrient and water stress in the Brazilian Amazon rainforest 2017 Acta Amazonica ). 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 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. N Author Title Year Journal 1 Fernandes et al., 1988 Ocorrência e caracterização de galhas entomógenas na vegetação do campus Pampulha da Universidade Federal de Minas Gerais 1988 Revista Brasileira de Zoologia 2 Fernandes et al., 1997 Insect-galls from savanna and rocky fields of the Jequitinhonha valley, Minas Gerais, Brazil 1997 Naturalia 3 Gonçalves-Alvim & Fernandes, 2001 Comunidades de insetos galhadores (Insecta) em diferentes fisionomias do cerrado em Minas Gerais, Brasil 2001 Revista Brasileira de Zoologia 4 Fernandes et al., 2001 Distribution and morphology ofinsect galls of the Rio Doce Valley, Brazil 2001 Naturalia 5 Maia, 2001 The gall midges (Diptera, Cecidomyiidae) from three restingas of Rio de Janeiro State, Brazil 2001 Revista Brasileira de Zoologia 6 Julião et al., 2002 Galhas de insetos e suas plantas hospedeiras no Pantanal sul-mato-grossense 2002 Naturalia 7 Urso-Guimarães et al., 2003 Occurrence and characterization of entomogen galls in plants from natural vegetation areas in Delfinópolis, MG, Brazil 2003 Brazilian Journal of Biology 8 Maia & Fernandes, 2004 Insect galls from Serra de São José (Tiradentes, MG, Brazil) 2004 Brazilian Journal of Biology 9 Oliveira & Maia, 2005 Ocorrência e Caracterização de Galhas de Insetos na Restinga de Grumari (Rio de Janeiro, RJ, Brasil) 2005 Arquivos do Museu Nacional 10 Urso-Guimarães & Scareli-Santos, 2006 Galls and gall makers in plants from the Pé de Gigante Cerrado Reserve, Santa Rita do Passa Quatro, SP, Brazil 2006 Brazilian Journal of Biology 11 Fernandes & Negreiros, 2006 A comunidade de insetos galhadores da RPPN Fazenda Bulcão, Aimorés, Minas Gerais, Brasil 2006 Lundiana 12 Moreira et al., 2007 Galling insects as bioindicators of land restoration in an areaof Brazilian Atlantic Forest 2007 Lundiana 13 Maia et al., 2008 Ocorrência e caracterização de galhas de insetos em áreas de restinga de Bertioga (São Paulo, Brasil) 2008 Biota Neotropica 14 Carvalho-Fernandes et al., 2009 Galhas entomógenas em um fragmento urbano de Mata Atlântica no centro de endemismo de Pernambuco 2009 Revista Brasileira de Biociências 15 Coelho et al., 2009 Gall inducing arthropods from a seasonally dry tropical forest in Serra do Cipó, Brazil 2009 Revista Brasileira de Entomologia 16 Carneiro et al., 2009 Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, Minas Gerais, Brasil 2009 Revista Brasileira de Entomologia 17 Maia & Oliveira, 2010 Galhas de insetos da Reserva Biológica Estadual da Praia do Sul (Ilha Grande, Angra dos Reis, RJ) 2010 Biota Neotropica 18 Bregonci et al., 2010 Galhas de insetos do Parque Estadual Paulo CéSar Vinha (Guarapari, ES, Brasil) 2010 Biota Neotropica 19 Santos et al., 2010 Ocorrência e caracterização de galhas entomógenas em uma área de floresta estacional semidecídua em Goiânia, Goiás, Brasil 2010 Acta Botanica Brasilica 20 Maia, 2011 Characterization of insect galls, gall makers, and associated fauna of Platô Bacaba (Porto de Trombetas, Pará, Brazil) 2011 Biota Neotropica 21 Santos et al., 2011 Diversity of gall-inducing insects in the high altitude wetland forests in Pernambuco, Northeastern Brazil 2011 Brazilian Journal of Biology 22 Araújo et al., 2011 Insect galls from Serra dos Pireneus, GO, Brazil 2011 Biota Neotropica 23 Almada & Fernandes, 2011 Insetos indutores de galhas em florestas de terra firme e em reflorestamentos com espécies nativas na Amazônia Oriental, Pará, Brasil 2011 Boletim do Museu Paranaense Emílio Goeldi de Ciências Naturais 24 Santos et al., 2011 Richness of gall-inducing insects in the tropical dry forest (caatinga) of Pernambuco 2011 Revista Brasileira de Entomologia 25 Saito & Urso-Guimarães, 2012 Characterization of galls, insect galls and associated fauna of Ecological Station of Jataí (Luiz Antônio, SP) 2012 Biota Neotropica 26 Santos et al., 2012 Galhas de insetos em uma área de cerrado sentido restrito na região semi-urbana de Caldas Novas (Goiás, Brasil) 2012 Revista Brasileira de Biociências 27 Santos et al., 2012 Gall-inducing insects from Atlantic forest of Pernambuco, Northeastern Brazil 2012 Biota Neotropica 28 Luz et al., 2012 Galhas de insetos em habitats xérico e mésico em região de transição Cerrado-Caatinga no norte de Minas Gerais, Brasil 2012 Neotropical Biology and Conservation 29 Malves & Friero-Costa, 2012 List of plants with galls induced by insects from the UNILAVRAS/Boqueirão Biological Reserve, Ingaí, State of Minas Gerais, Brazil 2012 Check List 30 Carvalho-Fernandes et al., 2012 The insect gall richness in preserved and anthropic areas of caatinga 2012 Revista Árvore 31 Coelho et al., 2013 Gall-inducing insects from Campos de Altitude, Brazil 2013 Biota Neotropica 32 Coelho et al., 2013 Gall-inducing insects from Serra do Cabral, Minas Gerais, Brazil 2013 Biota Neotropica 33 Toma & Mendonça Jr., 2013 Gall-inducing insects of an araucaria forest in southern Brazil 2013 Revista Brasileira de Entomologia 34 Maia, 2013 Insect galls of São Tomé das Letras (MG, Brazil) 2013 Biota Neotropica 35 Maia & Souza, 2013 Insect galls of the xeric vegetation of Ilha do Cabo Frio (Arraial do Cabo, RJ, Brazil) 2013 Biota Neotropica 36 Costa et al., 2014 Galhas de insetos em uma área de transição caatinga-cerrado no Nordeste do Brasil 2014 Sitientibus série Ciências Biológicas 37 Maia et al., 2014 Insect galls from Atlantic Forest areas of Santa Teresa, Espírito Santo, Brazil: characterization and occurrence 2014 Boletim do Museu de Biologia Mello Leitão 38 Maia, 2014 Insect galls of Itamonte (Minas Gerais, Brazil): Characterization and occurrence 2014 Biota Neotropica 39 Rodrigues et al., 2014 Insect galls of restinga areas of Ilha da Marambaia, Rio de Janeiro, Brazil 2014 Revista Brasileira de Entomologia 40 Araújo et al., 2014 Insect galls of the Parque Nacional das Emas (Mineiros, GO, Brazil) 2014 Check List 41 Silva et al., 2015 Ocorrência e caracterização de galhas de insetos em um fragmento de mata semicaducifólia do Campus Samambaia, Goiânia, GO, Brasil 2015 Revista de Biologia Neotropical 42 Alcântara et al., 2017 Ocorrência e caracterização de galhas em duas áreas do noroeste do Ceará, Brasil 2015 Natureza on line 43 Carvalho-Fernandes et al., 2016 Diversity of insect galls associated with coastal shrub vegetation in Rio de Janeiro, Brazil 2016 Anais da Academia Brasileira de Ciências 44 Carvalho-Fernandes et al., 2016 Insect galls from Serra Geral, Caetité, Ba, Brazil [Galhas de insetos da Serra Geral, Caetité, Bahia, Brasil] 2016 Biota Neotropica 45 Maia & Carvalho-Fernandes, 2016 Insect galls of a protected remnant of the Atlantic Forest tableland from Rio de Janeiro State (Brazil) 2016 Revista Brasileira de Entomologia 46 Maia & Silva, 2016 Insect galls of Restinga de Marambaia (Barra de Guaratiba, Rio de Janeiro, RJ) [Galhas de insetos da Restinga de Marambaia (Barra de Guaratiba, Rio de Janeiro, RJ)] 2016 Brazilian Journal of Biology 47 Urso-Guimarães et al., 2017 Characterization of entomogen galls from Mato Grosso do Sul, Brazil 2017 Revista Brasileira de Entomologia 48 Bergamini et al., 2017 Occurrence and characterization of insect galls in the Floresta Nacional de Silvânia, Brazil 2017 Papéis Avulsos de Zoologia ). 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 et al., 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 et al., 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 et al., 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 et al., 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 et al., 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 et al., 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 et al., 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 et al., 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 et al., 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 et al., 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 et al., 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 et al., 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”.

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  • 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.
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  • 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.
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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).

N Title Year Journal 1 Biogeographical gradients in galling species richness - Tests of hypotheses 1988 Oecologia 2 Adaptive significance of insect gall distribution: survivorship of species in xeric and mesic habitats 1992 Oecologia 3 Utilization of Apion sp. (Coleoptera apionidae) galls by an ant community in southeastern brazil 1995 Tropical Zoology 4 Fire effects on a Palicourea rigida (rubiaceae) gall midge: A test of the plant vigor hypothesis 1996 Biotropica 5 Galling insects on neotropical species of Baccharis (Asteraceae) 1996 Tropical Zoology 6 The highest diversity of galling insects: Serra do Cipó, Brazil 1996 Biodiversity Letters 7 The ecological function of extrafloral nectaries: Herbivore deterrence by visiting ants and reproductive output in Caryocar brasiliense (Caryocaraceae) 1997 Functional Ecology 8 Global patterns in local number of insect galling species 1998 Journal of Biogeography 9 Hypersensitivity as a Phenotypic Basis of Plant Induced Resistance Against a Galling Insect (Diptera: Cecidomyiidae) 1998 Environmental Entomology 10 Natural history of a gall-inducing weevil Collabismus clitellae (Coleoptera: Curculionidae) and some effects on its host plant Solanum lycocarpum (Solanaceae) in southeastern Brazil 1998 Annals of the Entomological Society of America 11 Abundance and impact of a Lepidopteran gall on Macairea radula (Melastomataceae) in the Neotropics 1999 International Journal of Ecology and Environmental Sciences 12 The interplay between plant traits and herbivore attack: A study of a stem galling midge in the neotropics 1999 Ecological Entomology 13 Distance-limited recolonization of burned cerrado by leaf-miners and gallers in central Brazil 2000 Environmental Entomology 14 Biodiversity of galling insects: Historical, community and habitat effects in four neotropical savannas 2001 Biodiversity and Conservation 15 Galling insect diversity patterns: the resource synchronisation hypothesis 2001 Oikos 16 Host plant response and phenotypic plasticity of a galling weevil (Collabismus clitellae: Curculionidae) 2001 Austral Ecology 17 Leaf gall abundance on Avicennia germinans (Avicenniaceae) along an interstitial salinity gradient 2001 Biotropica 18 The occurrence and effectiveness of hypersensitive reaction against galling herbivores across host taxa 2001 Ecological Entomology 19 Vigour of a dioecious shrub and attack by a galling herbivore 2001 Ecological Entomology 20 Host plant effects on the development and survivorship of the galling insect Neopelma baccharidis (Homoptera: Psyllidae) 2002 Austral Ecology 21 Influence of host-plant sex and habitat on survivorship of insect galls within the geographical range of the host-plant 2002 Tropical Zoology 22 Tests of hypotheses on patterns of gall distribution along an altitudinal gradient 2002 Tropical Zoology 23 Complex interactions envolving a gall midge Myrciamyia maricaensis Maia (Diptera, Cecidomyiidae), phytophagous modifiers and parasitoids 2003 Revista Brasileira de Zoologia 24 Galling insects (Diptera: Cecidomyiidae) survive inundation during host plant flooding in Central Amazonia 2003 Biotropica 25 Hypersensitivity of Fagus sylvatica L. against leaf galling insects 2003 Trees 26 Occurrence and characterization of entomogen galls in plants from natural vegetation areas in Delfinópolis, MG, Brazil 2003 Brazilian Journal of Biology 27 A key to genera to Eriococcidae (Hemiptera: Coccoidea) from the Neotropical region and a revision of Pseudotectococcus Hempel (Eriococcidae), a gall inducing scale insect genus from Brazil, with a description of a new species 2004 Lundiana 28 Edge effect and species-area relationships in the gall-forming insect fauna of natural forest patches in the Brazilian Pantanal 2004 Biodiversity and Conservation 29 Effects of genetic variability and habitat of Qualea parviflora (Vochysiaceae) on herbivory by free-feeding and gall-forming insects 2004 Annals of Botany 30 Gall-inducing jumping plant-lice of the Neotropical genus Baccharopelma (Hemiptera, Psylloidea) associated with Baccharis (Asteraceae) 2004 Journal of Natural History 31 Insect galls from Serra de São José (Tiradentes, MG, Brazil) 2004 Brazilian Journal of Biology 32 Novas espécies de Prodecatoma (Hymenoptera, Eurytomidae) associadas a galhas em frutos de duas espécies de Psidium L. (Myrtaceae), com comentários sobre Prodecatoma spermophaga Costa-Lima 2004 Revista Brasileira de Entomologia 33 A new genus and species of gall midge (Diptera: Cecidomyiidae) associated with Waltheria indica L. (Sterculiaceae) 2005 Zootaxa 34 Convergence in the variation of local and regional galling species richness 2005 Neotropical Entomology 35 Insetos galhadores associados a duas espécies de plantas invasoras de áreas urbanas e peri-urbanas 2005 Revista Brasileira de Entomologia 36 Two new species of Asphondyliini (Diptera: Cecidomyiidae) associated with Bauhinia brevipes (Fabaceae) in Brazil 2005 Zootaxa 37 Distribution and frequency of galls induced by Anisodiplosis waltheriae Maia (Diptera: Cecidomyiidae) on the invasive plant Waltheria indica L. (Sterculiaceae) 2006 Neotropical Entomology 38 Diversity of galling arthropods and host plants in a subtropical forest of Porto Alegre, southern Brazil 2006 Neotropical Entomology 39 Effects of host plant architecture on colonization by galling insects 2006 Austral Ecology 40 Influence of Apion sp. (Brentidae, Apioninae) stem-galls on induced resistance and leaf area of Diospyros hispida (Ebenaceae) 2006 Revista Brasileira de Entomologia 41 Insect galls occurring in Miconia prasina (Melastomataceae) in remnants of Atlantic forest of northeastern Brazil 2006 Lundiana 42 Insetos fitófagos associados ao murici da praia, Byrsonima sericea (Malpighiaceae), na Restinga de Jurubatiba (RJ) 2006 Revista Brasileira de Entomologia 43 Processes driving ontogenetic succession of galls in a canopy tree 2006 Biotropica 44 Sex-mediated herbivory by galling insects on Baccharis concinna (Asteraceae) 2006 Revista Brasileira de Entomologia 45 A comunidade de insetos galhadores da RPPN Fazenda Bulcão, Aimorés, Minas Gerais, Brasil 2006 Lundiana 46 Caracterização e distribuição espacial de galhas em Clusia nemorosa G. Mey (Clusiaceae) em uma área de Floresta Atlântica, Igarassu, PE 2007 Lundiana 47 Ecology and impact of Allorhogas sp. (Hymenoptera: Braconidae) and Apion sp. (Coleoptera: Curculionoidea) on fruits of Miconia calvescens DC (Melastomataceae) in Brazil 2007 Biological Control 48 Effect of aib on quality and phytossanity of Caryocar brasiliense Camb (Caryocaraceae) air layering 2007 Revista Arvore 49 Galling insects as bioindicators of land restoration in an area of Brazilian Atlantic forest 2007 Lundiana 50 How Many Species of Gall-Inducing Insects Are There on Earth, and Where Are They? 2007 Annals of the Entomological Society of America 51 Impact of a gall midge Parkiamyia paraensis (Diptera, Cecidomyiidae) on the Amazonian plant Parkia pendula (Fabaceae) 2007 Revista Brasileira de Entomologia 52 Plant architecture and meristem dynamics as the mechanisms determining the diversity of gall-inducing insects 2007 Oecologia 53 Asphondylia gochnatiae, a new species of gall midge (Diptera, Cecidomyiidae) associated with Gochnatia polymorpha (Less.) Cabrera (Asteraceae) 2008 Zootaxa 54 Ocorrência e caracterização de galhas de insetos em áreas de restinga de Bertioga (São Paulo, Brasil) 2008 Biota Neotropica 55 Phytotoxicity of the extracts of Lonchocarpus muehlbergianus Hassl. (Fabaceae) leaflets and galls on seed germination and early development of lettuce 2008 Acta Botanica Brasilica 56 Plant organ abscission and the green island effect caused by gallmidges (Cecidomyiidae) on tropical trees 2008 Arthropod-Plant Interactions 57 Relationships between host plant architecture and gall abundance and survival 2008 Revista Brasileira de Entomologia 58 Species-specific changes in tissue morphogenesis induced by two arthropod leaf gallers in Lantana camara L. (Verbenaceae) 2008 Australian Journal of Botany 59 A new genus and species of gall midge (Diptera, Cecidomyiidae) associated with Myrcia retorta (Myrtaceae) 2009 Revista Brasileira de Entomologia 60 Are gall midge species (Diptera, Cecidomyiidae) host-plant specialists? 2009 Revista Brasileira de Entomologia 61 Asphondylia fructicola, a new species of Cecidomyiidae (Diptera) associated with Solanum sp. (Solanaceae) from Brazil 2009 Revista Brasileira de Entomologia 62 Efeitos da sazonalidade e do tamanho da planta hospedeira na abundância de galhas de Cecidomyiidae (Diptera) em Piper arboreum (Piperaceae) 2009 Revista Brasileira de Entomologia 63 Gall inducing arthropods from a seasonally dry tropical forest in Serra do Cipó, Brazil 2009 Revista Brasileira de Entomologia 64 Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, Minas Gerais, Brasil 2009 Revista Brasileira de Entomologia 65 Gall midge attack intensity and host-plant response in a Neotropical coastal ecosystem 2009 Revista Brasileira de Entomologia 66 Grape phylloxera in Brazil 2009 Acta Horticulturae 67 Influence of leaflet age in anatomy and possible adaptive values of the midrib gall of Copaifera langsdorffii (Fabaceae: Caesalpinioideae) 2009 Revista de Biologia Tropical 68 Intra-specific phenotypic variations in Lantana camara leaves affect host selection by the gall maker Aceria lantanae 2009 Biochemical Systematics and Ecology 69 Complexidade estrutural e diversidade de insetos galhadores em Styrax pohlii Fritsch (Styracaceae) 2009 Bioscience Journal 70 Two new gall-inducing genera and species of Eriococcidae (Hemiptera) on Malvaceae and Anacardiaceae from the Neotropics 2009 Lundiana 71 Within tree distribution of a gall-inducing Eurytoma (Hymenoptera, Eurytomidae) on Caryocar brasiliense (Caryocaraceae) 2009 Revista Brasileira de Entomologia 72 Description of the female, pupa and gall of Pisphondylia brasiliensis Couri and Maia, 1992 (Diptera: Cecidomyiidae, Schizomyiina) with new records 2010 Brazilian Journal of Biology 73 First record of galls in hog plum (Spondias mombim L.) panicles caused by Clinodiplosis (Diptera: Cecidomyiidae) and evaluation of genotypes in the State of Piauí 2010 Revista Brasileira de Fruticultura 74 Gall midges (Diptera, Cecidomyiidae) associated with Aldina heterophylla spr. ex Benth. (Fabaceae) from Brazil 2010 Biota Neotropica 75 Gall-inducing insect species richness as indicators of forest age and Health 2010 Environmental Entomology 76 Insect galls of the Parque Estadual Paulo César Vinha (Guarapari, ES, Brazil) 2010 Biota Neotropica 77 Ocorrência e caracterização de galhas entomógenas em uma área de floresta estacional semidecídua em Goiânia, Goiás, Brasil 2010 Acta Botanica Brasilica 78 Pattern of attack of a galling insect reveals an unexpected preference-performance linkage on medium-sized resources 2010 Revista Brasileira de Entomologia 79 Photosynthetic efficiency of Clusia arrudae leaf tissue with and without Cecidomyiidae galls 2010 Brazilian Journal of Biology 80 Redifferentiation of leaflet tissues during midrib gall development in Copaifera langsdorffii (Fabaceae) 2010 South African Journal of Botany 81 Two new species of Lopesia Rübsaamen (Diptera, Cecidomyiidae) from Brazil, with an identification key of species 2010 Biota Neotropica 82 A new genus and species of gall midge (Diptera, Cecidomyiidae) associated with Microgramma vacciniifolia (Langsd. & Fisch.) Copel. (Polypodiaceae) from Brazil 2011 Revista Brasileira de Entomologia 83 Abundance of gall-inducing insect species in sclerophyllous savanna: Understanding the importance of soil fertility using an experimental approach 2011 Journal of Tropical Ecology 84 Burseramyia braziliensis, a new species of gall midge (Diptera, Cecidomyiidae, Asphondyliini) associated with Swartzia langsdorffii Raddi (Fabaceae) 2011 Biota Neotropica 85 Calophya latiforceps, a new species of jumping plant lice (Hemiptera: Calophyidae) associated with Schinus terebinthifolius (Anacardiaceae) in Brazil 2011 Florida Entomologist 86 Can host plant richness be used as a surrogate for galling insect diversity? 2011 Tropical Conservation Science 87 Characterization of insect galls, gall makers, and associated fauna of Platô Bacaba (Porto de Trombetas, Pará, Brazil) 2011 Biota Neotropica 88 Cytological and histochemical gradients on two Copaifera langsdorffii Desf. (Fabaceae)-Cecidomyiidae gall systems 2011 Protoplasma 89 Differential female attack and larval performance of a galling cecidomyiid on the host, Astronium fraxinifolium (Anacardiaceae), in contrasting habitats 2011 Entomological News 90 Distribution of a leaf vein gall in Caryocar Brasiliense (Caryocaraceae) tree 2011 Revista Caatinga 91 Diversity of gall-inducing insects in the high altitude wetland forests in Pernambuco, Northeastern Brazil 2011 Brazilian Journal of Biology 92 Diversity of galling insects in Styrax pohlii (Styracaceae): Edge effect and use as bioindicators 2011 Revista de Biologia Tropical 93 Fire increases insect herbivory in a neotropical savanna 2011 Biotropica 94 Herbivory, pathogens, and epiphylls in araucaria forest and ecologically-managed tree monocultures 2011 Forest Ecology and Management 95 Insect galls from Serra dos Pireneus, GO, Brazil Galhas de insetos da Serra dos Pireneus, GO, Brasil 2011 Biota Neotropica 96 Insect herbivores associated with Baccharis dracunculifolia (Asteraceae): Responses of gall-forming and free-feeding insects to latitudinal variation 2011 Revista de Biologia Tropical 97 Richness of gall-inducing insects in the tropical dry forest (caatinga) of Pernambuco 2011 Revista Brasileira de Entomologia 98 Size, age and composition: Characteristics of plant taxa as diversity predictors of gall-midges (Diptera: Cecidomyiidae) 2011 Revista de Biologia Tropical 99 Spatial distribution of a spherical gall (Hymenoptera, Eulophidae) on Caryocar brasiliense (Caryocaraceae) 2011 Revista Brasileira de Entomologia 100 Two new species of gall midges (Diptera, Cecidomyiidae) associated with Erythroxylum ovalifolium Peyr. (Erythroxylaceae) from the barra de Maricá restinga, Maricá, Rio de Janeiro, Brazil 2011 Brazilian Journal of Biology 101 Characterization of galls, insect galls and associated fauna of Ecological Station of Jataí (Luiz Antônio, SP) 2012 Biota Neotropica 102 Edge effect benefits galling insects in the Brazilian Amazon 2012 Biodiversity and Conservation 103 Eugeniamyia dispar in Surinam cherry: Associated parasitoids, population dynamics and distribution of plant galls 2012 Revista Brasileira de Fruticultura 104 Gall-inducing insects from Atlantic forest of Pernambuco, Northeastern Brazil 2012 Biota Neotropica 105 Distribuição de insetos galhadores em diferentes formações vegetais e paisagens do cerrado brasileiro 2012 Bioscience Journal 106 Herbivory among habitats on the Neotropical tree Cnidoscolus quercifolius Pohl. in a seasonally deciduous forest 2012 Brazilian Journal of Biology 107 Galhas de insetos em habitats xérico e mésico em região de transição Cerrado-Caatinga no norte de Minas Gerais, Brasil 2012 Neotropical Biology and Conservation 108 List of plants with galls induced by insects from the UNILAVRAS/Boqueirão Biological Reserve, Ingaí, state of Minas Gerais, Brazil 2012 Check List 109 Mutualism from the inside: Coordinated development of plant and insect in an active pollinating fig wasp 2012 Arthropod-Plant Interactions 110 Population ecology of the multivoltine Neotropical gall midge Eugeniamyia dispar (Diptera, Cecidomyiidae) 2012 Iheringia Série Zoologia 111 Population structure and genetic diversity analysis in Gynaikothrips uzeli (Zimerman, 1909) (Thysanoptera: Phlaeothripidae) by RAPD markers 2012 Bulletin of Entomological Research 112 Relationship between host plant diversity and gall-inducing insect’s richness in the Brazilian Cerrado 2012 Neotropical Biology and Conservation 113 Richness of hymenopterous galls from South America 2012 Papéis Avulsos de Zoologia 114 Seasonal variation of natural mortality factors of the guava psyllid Triozoida limbata 2012 Bulletin of Entomological Research 115 Source-sink relationship and photosynthesis in the horn-shaped gall and its host plant Copaifera langsdorffii Desf. (Fabaceae) 2012 South African Journal of Botany 116 Stem galls drain nutrients and decrease shoot performance in Diplusodon orbicularis (Lythraceae) 2012 Arthropod-Plant Interactions 117 A new gall-inducing genus and species of Eriococcidae (Hemiptera: Sternorrhyncha: Coccoidea) on Sapindaceae from Brazil 2013 Zootaxa 118 A new genus and species of Lasiopteridi (Diptera, Cecidomyiidae) associated with Myrciaria delicatula (Myrtaceae) from Brazil, with identification keys of tribes and unplaced genera 2013 Biota Neotropica 119 Biology and systematics of gall-inducing triozids (Hemiptera: Psylloidea) associated with Psidium spp. (Myrtaceae) 2013 Zootaxa 120 Comparing galling insect richness among Neotropical savannas: Effects of plant richness, vegetation structure and super-host presence 2013 Biodiversity and Conservation 121 Gall-inducing insects from Campos de Altitude, Brazil Insetos indutores de galhas de Campos de Altitude, Brazil 2013 Biota Neotropica 122 Gall-inducing insects from Serra do Cabral, Minas Gerais, Brazil 2013 Biota Neotropica 123 Gall-inducing insects of an araucaria forest in southern Brazil 2013 Revista Brasileira de Entomologia 124 Host plants of insect-induced galls in areas of cerrado in the state of Goiás, Brazil 2013 Acta Botanica Brasilica 125 Insect galls from restingas of Southeastern Brazil, with new records 2013 Biota Neotropica 126 Insect galls of São Tomé das Letras (MG, Brazil) 2013 Biota Neotropica 127 Insect galls of the xeric vegetation of Ilha do Cabo Frio (Arraial do Cabo, RJ, Brazil) 2013 Biota Neotropica 128 Seasonal abundance of galling insects (Hymenoptera) on Caryocar brasiliense (Malpighiales: Caryocaraceae) trees in the cerrado 2013 Florida Entomologist 129 Synchronism between Aspidosperma macrocarpon (Apocynaceae) resources allocation and the establishment of the gall inducer Pseudophacopteron sp.(Hemiptera: Psylloidea) 2013 Revista de Biologia Tropical 130 The effect of fluctuating asymmetry and leaf nutrients on gall abundance and survivorship 2013 Basic and Applied Ecology 131 The genus Dasineura Rondani, 1840 (Diptera, Cecidomyiidae) in Brazil 2013 Brazilian Journal of Biology 132 Water stress and phenological synchronism between Copaifera langsdorffii (Fabaceae) and multiple galling insects: Formation of seasonal patterns 2013 Journal of Plant Interactions 133 Confirmation bias leads to overestimation of losses of woody plant foliage to insect herbivores in tropical regions 2014 PeerJ 134 Galling insects are bioindicators of environmental quality in a conservation unit 2014 Acta Botanica Brasilica 135 Habitat conversion and galling insect richness in tropical rainforests under mining effect 2014 Journal of Insect Conservation 136 Insect galls of Itamonte (Minas Gerais, Brazil): Characterization and occurrence 2014 Biota Neotropica 137 Insect galls of restinga areas of Ilha da Marambaia, Rio de Janeiro, Brazil 2014 Revista Brasileira de Entomologia 138 Insect galls of the Parque Nacional das Emas (Mineiros, GO, Brazil) 2014 Check List 139 Leptocybe invasa (Hymenoptera: Eulophidae), an exotic pest of Eucalyptus, in minas Gerais state, Brazil 2014 Florida Entomologist 140 Local and regional determinants of galling-insect richness in neotropical savanna 2014 Journal of Tropical Ecology 141 Native range density, host utilisation and life history of Calophya latiforceps (Hemiptera: Calophyidae): An herbivore of Brazilian Peppertree (Schinus terebinthifolia) 2014 Biocontrol Science and Technology 142 Patterns of cell elongation in the determination of the final shape in galls of Baccharopelma dracunculifoliae (Psyllidae) on Baccharis dracunculifolia DC (Asteraceae) 2014 Protoplasma 143 Redescription of Japanagromyza inferna Spencer, first recorded from Brazil, and a key to the Neotropical species of Japanagromyza Sasakawa (Diptera, Agromyzidae) 2014 ZooKeys 144 Same but different: Larval development and gall-inducing process of a non-pollinating fig wasp compared to that of pollinating fig-wasps 2014 Acta Oecologica 145 Senescent stem-galls in trees of Eremanthus erythropappus as a resource for arboreal ants 2014 Revista Brasileira de Entomologia 146 Structure of floral galls of Byrsonima sericea (Malpighiaceae) induced by Bruggmanniella byrsonimae (Cecidomyiidae, Diptera) and their effects on host plants 2014 Plant Biology 147 Temporal Variation in the Sex Ratio of a Natural Population of a Multivoltine Gall-Inducing Braconid Wasp 2014 Journal of Insect Behavior 148 The insect gall collection of the museu nacional/universidade federal do rio de janeiro: Biome cerrado, rupestrian fields 2014 Brazilian Journal of Biology 149 Unexpected high diversity of galling insects in the Amazonian upper canopy: The savanna out there 2014 PLoS ONE 150 Checklist of host plants of insect galls in the state of Goiás in the Midwest Region of Brazil 2015 Biodiversity Data Journal 151 Cytological cycles and fates in Psidium myrtoides are altered towards new cell metabolism and functionalities by the galling activity of Nothotrioza myrtoidis 2015 Protoplasma 152 Descriptions of two new Pseudophacopteron species (Hemiptera: Psylloidea: Phacopteronidae) inducing galls on Aspidosperma (Apocynaceae) in Brazil 2015 Acta Entomologica Musei Nationalis Pragae 153 Detection and distribution of cell growth regulators and cellulose microfibrils during the development of Lopesia sp. galls on Lonchocarpus cultratus (Fabaceae) 2015 Botany 154 Multivesicular bodies differentiate exclusively in nutritive fast-dividing cells in Marcetia taxifolia galls 2015 Protoplasma 155 New Species Diversity Revealed from Molecular and Morphological Characterization of Gall-Inducing Calophya spp. (Hemiptera: Calophyidae) from Brazilian Peppertree 2015 Florida Entomologist 156 Phenotypic plasticity and similarity among gall morphotypes on a superhost, Baccharis reticularia (Asteraceae) 2015 Plant Biology 157 Population dynamics of the gall inducer Eriogallococcus isaias (Hemiptera: Coccoidea: Eriococcidae) on Pseudobombax grandiflorum (Malvaceae) 2015 Journal of Natural History 158 Questioning the environmental stress hypothesis for gall diversity of restinga vegetation on dunes 2015 Revista de Biologia Tropical 159 The imbalance of redox homeostasis in arthropod-induced plant galls: Mechanisms of stress generation and dissipation 2015 Biochimica et biophysica acta. G, General subjects 160 Clinodiplosis agerati (Diptera, Cecidomyiidae), a new galling species associated with Ageratum conyzoides (Asteraceae) from Brazil 2016 Brazilian Journal of Biology 161 Galling Insect Species Richness and Leaf Herbivory in an Abrupt Transition between Cerrado and Tropical Dry Forest 2016 Annals of the Entomological Society of America 162 Galls in Schinus polygamus (Anacardiaceae): effects of forest structure on infestation intensity 2016 Brazilian Journal of Botany 163 Galls induced by Calophya latiforceps (Hemiptera: Calophyidae) reduce leaf performance and growth of Brazilian peppertree 2016 Biocontrol Science and Technology 164 Holopothrips molzi sp. n. (Thysanoptera, Phlaeothripidae): Natural history and interactions in Myrtaceae galls 2016 Zootaxa 165 How detrimental are seed galls to their hosts? Plant performance, germination, developmental instability and tolerance to herbivory in Inga laurina, a leguminous tree 2016 Plant Biology 166 Insect galls from Serra Geral, Caetité, Ba, Brazil 2016 Biota Neotropica 167 Insect galls of a protected remnant of the Atlantic Forest tableland from Rio de Janeiro State (Brazil) 2016 Revista Brasileira de Entomologia 168 Insect galls of Restinga de Marambaia (Barra de Guaratiba, Rio de Janeiro, RJ) 2016 Brazilian Journal of Biology 169 Insect galls on Mikania glomerata (Asteraceae) in an area of atlantic forest in Viçosa (Minas Gerais, Brazil) 2016 Check List 170 Manipulation of host plant cells and tissues by gall-inducing insects and adaptive strategies used by different feeding guilds 2016 Journal of Insect Physiology 171 Shifts in Plant Assemblages Reduce the Richness of Galling Insects Across Edge-Affected Habitats in the Atlantic Forest 2016 Environmental Entomology 172 The gall inducing insect community on Baccharis concinna (Asteraceae): The role of shoot growth rates and seasonal variations 2016 Lundiana 173 Where host plant goes, galls go too: New records of the Neotropical galling Cecidomyiidae (Diptera) associated with Calophyllum brasiliense Cambess. (Calophyllaceae) 2016 Check List 174 Cecidonius pampeanus, gen. et sp. n.: an overlooked and rare, new gall-inducing micromoth associated with Schinus in southern Brazil (Lepidoptera, Cecidosidae) 2017 ZooKeys 175 Characterization of entomogen galls from Mato Grosso do Sul, Brazil 2017 Revista Brasileira de Entomologia 176 Differences in leaf nutrients and developmental instability in relation to induced resistance to a gall midge 2017 Arthropod-Plant Interactions 177 Experimentally reducing species abundance indirectly affects food web structure and robustness 2017 Journal of Animal Ecology 178 Neolasioptera pantaneira, a new species of cecidomyiidae (Diptera) associated with Aeschynomene denticulata (Fabaceae) from Brazil 2017 Brazilian Journal of Biology 179 Patterns gall infestation in Heteropterys byrsonimifolia A. Juss. in a forest-savannah ecotone 2017 Revista Ceres 180 Plant species richness mediates the effects of vegetation structure, but not soil fertility, on insect gall richness in a savanna in Brazil 2017 Journal of Tropical Ecology 181 The role of senescent stem-galls over arboreal ant communities structure in Eremanthus erythropappus (DC.) MacLeish (Asteraceae) trees 2017 Sociobiology 182 Understory host plant and insect gall diversity changes across topographic habitats differing in nutrient and water stress in the Brazilian Amazon rainforest 2017 Acta Amazonica

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.

N Author Title Year Journal 1 Fernandes et al., 1988 Ocorrência e caracterização de galhas entomógenas na vegetação do campus Pampulha da Universidade Federal de Minas Gerais 1988 Revista Brasileira de Zoologia 2 Fernandes et al., 1997 Insect-galls from savanna and rocky fields of the Jequitinhonha valley, Minas Gerais, Brazil 1997 Naturalia 3 Gonçalves-Alvim & Fernandes, 2001 Comunidades de insetos galhadores (Insecta) em diferentes fisionomias do cerrado em Minas Gerais, Brasil 2001 Revista Brasileira de Zoologia 4 Fernandes et al., 2001 Distribution and morphology ofinsect galls of the Rio Doce Valley, Brazil 2001 Naturalia 5 Maia, 2001 The gall midges (Diptera, Cecidomyiidae) from three restingas of Rio de Janeiro State, Brazil 2001 Revista Brasileira de Zoologia 6 Julião et al., 2002 Galhas de insetos e suas plantas hospedeiras no Pantanal sul-mato-grossense 2002 Naturalia 7 Urso-Guimarães et al., 2003 Occurrence and characterization of entomogen galls in plants from natural vegetation areas in Delfinópolis, MG, Brazil 2003 Brazilian Journal of Biology 8 Maia & Fernandes, 2004 Insect galls from Serra de São José (Tiradentes, MG, Brazil) 2004 Brazilian Journal of Biology 9 Oliveira & Maia, 2005 Ocorrência e Caracterização de Galhas de Insetos na Restinga de Grumari (Rio de Janeiro, RJ, Brasil) 2005 Arquivos do Museu Nacional 10 Urso-Guimarães & Scareli-Santos, 2006 Galls and gall makers in plants from the Pé de Gigante Cerrado Reserve, Santa Rita do Passa Quatro, SP, Brazil 2006 Brazilian Journal of Biology 11 Fernandes & Negreiros, 2006 A comunidade de insetos galhadores da RPPN Fazenda Bulcão, Aimorés, Minas Gerais, Brasil 2006 Lundiana 12 Moreira et al., 2007 Galling insects as bioindicators of land restoration in an areaof Brazilian Atlantic Forest 2007 Lundiana 13 Maia et al., 2008 Ocorrência e caracterização de galhas de insetos em áreas de restinga de Bertioga (São Paulo, Brasil) 2008 Biota Neotropica 14 Carvalho-Fernandes et al., 2009 Galhas entomógenas em um fragmento urbano de Mata Atlântica no centro de endemismo de Pernambuco 2009 Revista Brasileira de Biociências 15 Coelho et al., 2009 Gall inducing arthropods from a seasonally dry tropical forest in Serra do Cipó, Brazil 2009 Revista Brasileira de Entomologia 16 Carneiro et al., 2009 Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, Minas Gerais, Brasil 2009 Revista Brasileira de Entomologia 17 Maia & Oliveira, 2010 Galhas de insetos da Reserva Biológica Estadual da Praia do Sul (Ilha Grande, Angra dos Reis, RJ) 2010 Biota Neotropica 18 Bregonci et al., 2010 Galhas de insetos do Parque Estadual Paulo CéSar Vinha (Guarapari, ES, Brasil) 2010 Biota Neotropica 19 Santos et al., 2010 Ocorrência e caracterização de galhas entomógenas em uma área de floresta estacional semidecídua em Goiânia, Goiás, Brasil 2010 Acta Botanica Brasilica 20 Maia, 2011 Characterization of insect galls, gall makers, and associated fauna of Platô Bacaba (Porto de Trombetas, Pará, Brazil) 2011 Biota Neotropica 21 Santos et al., 2011 Diversity of gall-inducing insects in the high altitude wetland forests in Pernambuco, Northeastern Brazil 2011 Brazilian Journal of Biology 22 Araújo et al., 2011 Insect galls from Serra dos Pireneus, GO, Brazil 2011 Biota Neotropica 23 Almada & Fernandes, 2011 Insetos indutores de galhas em florestas de terra firme e em reflorestamentos com espécies nativas na Amazônia Oriental, Pará, Brasil 2011 Boletim do Museu Paranaense Emílio Goeldi de Ciências Naturais 24 Santos et al., 2011 Richness of gall-inducing insects in the tropical dry forest (caatinga) of Pernambuco 2011 Revista Brasileira de Entomologia 25 Saito & Urso-Guimarães, 2012 Characterization of galls, insect galls and associated fauna of Ecological Station of Jataí (Luiz Antônio, SP) 2012 Biota Neotropica 26 Santos et al., 2012 Galhas de insetos em uma área de cerrado sentido restrito na região semi-urbana de Caldas Novas (Goiás, Brasil) 2012 Revista Brasileira de Biociências 27 Santos et al., 2012 Gall-inducing insects from Atlantic forest of Pernambuco, Northeastern Brazil 2012 Biota Neotropica 28 Luz et al., 2012 Galhas de insetos em habitats xérico e mésico em região de transição Cerrado-Caatinga no norte de Minas Gerais, Brasil 2012 Neotropical Biology and Conservation 29 Malves & Friero-Costa, 2012 List of plants with galls induced by insects from the UNILAVRAS/Boqueirão Biological Reserve, Ingaí, State of Minas Gerais, Brazil 2012 Check List 30 Carvalho-Fernandes et al., 2012 The insect gall richness in preserved and anthropic areas of caatinga 2012 Revista Árvore 31 Coelho et al., 2013 Gall-inducing insects from Campos de Altitude, Brazil 2013 Biota Neotropica 32 Coelho et al., 2013 Gall-inducing insects from Serra do Cabral, Minas Gerais, Brazil 2013 Biota Neotropica 33 Toma & Mendonça Jr., 2013 Gall-inducing insects of an araucaria forest in southern Brazil 2013 Revista Brasileira de Entomologia 34 Maia, 2013 Insect galls of São Tomé das Letras (MG, Brazil) 2013 Biota Neotropica 35 Maia & Souza, 2013 Insect galls of the xeric vegetation of Ilha do Cabo Frio (Arraial do Cabo, RJ, Brazil) 2013 Biota Neotropica 36 Costa et al., 2014 Galhas de insetos em uma área de transição caatinga-cerrado no Nordeste do Brasil 2014 Sitientibus série Ciências Biológicas 37 Maia et al., 2014 Insect galls from Atlantic Forest areas of Santa Teresa, Espírito Santo, Brazil: characterization and occurrence 2014 Boletim do Museu de Biologia Mello Leitão 38 Maia, 2014 Insect galls of Itamonte (Minas Gerais, Brazil): Characterization and occurrence 2014 Biota Neotropica 39 Rodrigues et al., 2014 Insect galls of restinga areas of Ilha da Marambaia, Rio de Janeiro, Brazil 2014 Revista Brasileira de Entomologia 40 Araújo et al., 2014 Insect galls of the Parque Nacional das Emas (Mineiros, GO, Brazil) 2014 Check List 41 Silva et al., 2015 Ocorrência e caracterização de galhas de insetos em um fragmento de mata semicaducifólia do Campus Samambaia, Goiânia, GO, Brasil 2015 Revista de Biologia Neotropical 42 Alcântara et al., 2017 Ocorrência e caracterização de galhas em duas áreas do noroeste do Ceará, Brasil 2015 Natureza on line 43 Carvalho-Fernandes et al., 2016 Diversity of insect galls associated with coastal shrub vegetation in Rio de Janeiro, Brazil 2016 Anais da Academia Brasileira de Ciências 44 Carvalho-Fernandes et al., 2016 Insect galls from Serra Geral, Caetité, Ba, Brazil [Galhas de insetos da Serra Geral, Caetité, Bahia, Brasil] 2016 Biota Neotropica 45 Maia & Carvalho-Fernandes, 2016 Insect galls of a protected remnant of the Atlantic Forest tableland from Rio de Janeiro State (Brazil) 2016 Revista Brasileira de Entomologia 46 Maia & Silva, 2016 Insect galls of Restinga de Marambaia (Barra de Guaratiba, Rio de Janeiro, RJ) [Galhas de insetos da Restinga de Marambaia (Barra de Guaratiba, Rio de Janeiro, RJ)] 2016 Brazilian Journal of Biology 47 Urso-Guimarães et al., 2017 Characterization of entomogen galls from Mato Grosso do Sul, Brazil 2017 Revista Brasileira de Entomologia 48 Bergamini et al., 2017 Occurrence and characterization of insect galls in the Floresta Nacional de Silvânia, Brazil 2017 Papéis Avulsos de Zoologia

Publication Dates

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

History

  • Received
    13 Nov 2017
  • Accepted
    24 May 2018
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