Abstract

Understanding the diversity of insect galls is pivotal to the establishment of conservation planning in different Brazilian ecosystems. Here, we (1) characterize the insect galls found on plant host species, (2) identify the gall-inducing insects to the lowest possible taxonomic level, and (3) record the presence of gall-associated fauna. Our study was carried out monthly from August, 2017 to July, 2018 along nine trails in Serra da Bandeira, which is located in an area of Cerrado stricto sensu over a year. We found 48 distinct gall morphotypes, belonging to 12 botanical families. The most morphotypes commonly found were globoid (27.1%), lenticular (27.1%) and cylindrical (25%). The plant organs most affected by galling insects were the leaves (73%), followed by the stem (19%), flower (4%), inflorescence (2%) and fruits (2%). The host botanical families holding the highest number of galls were Fabaceae (26), Malpighiaceae (5) and Anacardiaceae, Combretaceae and Euphorbiaceae (3). We observed that the genus Copaifera Lindl. (Fabaceae) had the greatest diversity of gall morphotypes, harboring 19 morphotypes distributed in three species that occur sympatrically - Copaifera sabulicola J. Costa (Fabaceae), Copaifera depilis Dwyer (Fabaceae) and Copaifera luetzelburgii Harms (Fabaceae). For the first time in Brazil, we recorded the occurrence of galls on flowers of Manihot caerulescens (Euphorbiaceae), on inflorescences of Mimosa acutistipula (Fabaceae) and flower buds of Anacardium humile (Anacardiaceae), which were induced by Cecidomyiidae. Inducers of the order Diptera (Family Cecidomyiidae) were the most abundant, found in 14 morphotypes of galls. Regarding the associated fauna, we found insects primarily belonging the order Hymenoptera, and identified them as parasitoids. The information provided can be used highly by decision makers for conservation programs, as well as in other strategies for the conservation of biological diversity in the Brazilian Cerrado.

Keywords
Cerrado; Cecidomyiidae; Gall inducing insects; Galling insects; Insect-plant interaction

Resumo

Compreender a diversidade de galhas de insetos é fundamental para o estabelecimento de planos de conservação em diferentes ecossistemas brasileiros. Aqui, nós (1) caracterizamos as galhas de insetos encontradas em espécies de plantas hospedeiras, (2) identificamos os insetos indutores de galhas até o nível taxonômico mais baixo possível e (3) registramos a presença de fauna associada a galhas. Nosso estudo foi realizado mensalmente de agosto de 2017 a julho de 2018 ao longo de nove trilhas na Serra da Bandeira, que está localizada em uma área de Cerrado stricto sensu ao longo de um ano. Encontramos 48 morfotipos distintos de galhas, pertencentes a 12 famílias botânicas. Os morfotipos mais comumente encontrados foram globoide (27,1%), lenticular (27,1%) e cilíndrico (25%). Os órgãos vegetais mais afetados pelos insetos galhadores foram as folhas (73%), seguidas do caule (19%), flor (4%), inflorescência (2%) e frutos (2%). As famílias botânicas hospedeiras com maior número de galhas foram Fabaceae (26), Malpighiaceae (5) e Anacardiaceae, Combretaceae e Euphorbiaceae (3). Observamos que o gênero Copaifera Lindl. (Fabaceae) apresentou a maior diversidade de morfotipos de galhas, abrigando 19 morfotipos distribuídos em três espécies que ocorrem simpatriicamente – Copaifera sabulicola J. Costa (Fabaceae), Copaifera depilis Dwyer (Fabaceae) e Copaifera luetzelburgii Harms (Fabaceae). Pela primeira vez no Brasil, registramos a ocorrência de galhas em flores de Manihot caerulescens (Euphorbiaceae), em inflorescências de Mimosa acutistipula (Fabaceae) e em botões florais de Anacardium humile (Anacardiaceae), induzidas por Cecidomyiidae. Indutores da ordem Diptera (Família Cecidomyiidae) foram os mais abundantes, encontrados em 14 morfotipos de galhas. Em relação à fauna associada, encontramos insetos pertencentes principalmente à ordem Hymenoptera, e os identificamos como parasitóides. As informações fornecidas podem ser utilizadas por tomadores de decisão para programas de conservação, bem como em outras estratégias para a conservação da diversidade biológica no Cerrado brasileiro.

Palavras-chave
Cerrado; Cecidomyiidae; Insetos indutores de galhas; Insetos galhadores; Interação inseto-planta

Introduction

Galling insects are specialized herbivores that redirect plant resources in order to develop themselves during their cycle in host plants (Marini-Filho & Fernandes 2012MARINI-FILHO, O.J. & FERNANDES, G.W. 2012. Stem galls drain nutrients and decrease shoot performance in Diplusodon orbicularis (Lythraceae). Arthropod. Plant. Interact. 6(1):121–128., Gagné & Jaschhof 2017GAGNÉ, R.J. & JASCHHOF, M. 2017. A Catalog of the Cecidomyiidae (Diptera) of the World Fourth Edition Digital., Lima & Calado 2020LIMA, V.P. & CALADO, D.C. 2020. Mapping the habitat suitability of Andira humilis Mart. ex Benth. (Fabaceae) as a means to detect its associated galling species in Brazil. Acta Sci. Biol. Sci. 42(1):e48809.). Such development is an adaptive evolutionary strategy of certain groups for obtaining food and protection against predators (Gonçalves-Alvim & Fernandes 2001aGONÇALVES-ALVIM, S.J. & FERNANDES, G.W. 2001a. Biodiversity of galling insects: Historical, community and habitat effects in four neotropical savannas. Biodivers. Conserv. 10:79–98.). Insect galls are developed from tissue hyperplasia and cell hypertrophy (Martini et al. 2019MARTINI, V.C., MOREIRA, A.S.F.P., KUSTER, V.C. & OLIVEIRA, D.C. 2019. Galling insects as phenotype manipulators of cell wall composition during the development of galls induced on leaves of Aspidosperma tomentosum (Apocynaceae). South African J. Bot. 127226–233., Isaias et al. 2013ISAIAS, R.M.S., CARNEIRO, R.G.S., OLIVEIRA, D.C. & SANTOS, J.C. 2013. Illustrated and Annotated Checklist of Brazilian Gall Morphotypes. Neotrop. Entomol. 42(3):230–239., Mani 1964MANI, M.S. 1964. Ecology of Plant Galls. Springer Netherlands, Dordrecht.) due to abnormal differentiation in mechanical and chemical response of inducers, resulting in characteristic growth that harbor gall-inducing insects (Santos-Silva & Araujo 2020SANTOS-SILVA, J. & ARAUJO, T.J. 2020. Are Fabaceae the principal super-hosts of galls in Brazil? An. Acad. Bras. Cienc. 92(2):e20181115.). Currently, six orders of gall-inducing insects are known to science: Diptera, Hymenoptera, Thysanoptera, Coleoptera, Lepidoptera and Hemiptera (Maia & Monteiro 1999MAIA, V.C. & MONTEIRO, R.F. 1999. Espécies cecidógenas (Diptera, Cecidomyiidae) e parasitóides (Hymenoptera) associadas a Guapira opposita (Vell.) Reitz: (Nyctaginaceae) na Restinga da Barra de Maricá, Rio de Janeiro. Rev. Bras. Zool. 16(2):483–487.). Among Diptera, the Cecidomyiidae family is the main family of galling insects not only in the Neotropics, but also in other regions (Maia 2013a). To this date, 280 species and 103 genera have already been described belonging to the Cecidomyiidae family in Brazil (Maia 2023MAIA, V.C. 2023 http://fauna.jbrj.gov.br/ Retrieved October 13, 2023
http://fauna.jbrj.gov.br/... ).

Many species of galling insects are economically important, inducing galls on cultivated plants used daily as food, such as Anacardium humile A.St.Hil. (Anacardiaceae), and Caryocar brasiliense Cambess (Caryocaraceae), as well as other medicinal and ornamental plants (Fernandes & Price 1988FERNANDES, G.W. & PRICE, P.W. 1988. Biogeographical gradients in galling species richness - Tests of hypotheses. Oecologia. 76:161–167.). Galling insects are recognized as ecosystem engineers, as they can directly or indirectly modulate the availability of resources for other species, responsible for modifying, creating and maintaining microhabitats (Jones et al. 1994JONES, C.G., LAWTON, J.H. & SHACHAK, M. 1994. Organisms as Ecosystem Engineers. Oikos 69(3):373.). Furthermore, a large number of associated fauna (parasitoids, tenants, predators and successors) are regularly found in insect galls with great richness and abundance, thus increasing the ecological importance of galling insects (Maia & Monteiro 1999MAIA, V.C. & MONTEIRO, R.F. 1999. Espécies cecidógenas (Diptera, Cecidomyiidae) e parasitóides (Hymenoptera) associadas a Guapira opposita (Vell.) Reitz: (Nyctaginaceae) na Restinga da Barra de Maricá, Rio de Janeiro. Rev. Bras. Zool. 16(2):483–487., Santos et al. 2018SANTOS, I.M. dos, LIMA, V.P., SOARES, E.K.S., PAULA, M. de & CALADO, D.C. 2018. Insect galls in three species of Copaifera L. (Leguminosae, Caesalpinioideae) occurring sympatrically in a Cerrado area (Bahia, Brazil). Biota Neotrop. 18(1):e20170356., Soares et al. 2021SOARES, E.K.S., OLIVEIRA, A.B. de, LIMA, V.P. & CALADO, D. 2021. Insect galls associated with Copaifera sabulicola J.A.S Costa & L.P Queiroz (Fabaceae): Characterization and new records. Rev. Bras. Entomol. 65(4):e20210107., Lima & Calado 2018LIMA, V.P. & CALADO, D. 2018. Morphological characterization of insect galls and new records of associated invertebrates in a Cerrado area in Bahia State, Brazil. Brazilian J. Biol. 78(4):636–643., Maia 2013b).

Although several inventories of insect galls have been carried out in Cerrado areas, particularly in the states of Minas Gerais and Goiás (Araújo 2018ARAÚJO, W.S. de. 2018. 30 years of research on insect galls in Brazil: a scientometric review. Pap. Avulsos Zool. 58:e20185834.), few studies have covered the Cerrado of western Bahia (Lima & Calado 2018LIMA, V.P. & CALADO, D. 2018. Morphological characterization of insect galls and new records of associated invertebrates in a Cerrado area in Bahia State, Brazil. Brazilian J. Biol. 78(4):636–643.). Besides holding about 5% of the planet’s biological diversity, the Cerrado is one of the 25 world biodiversity hotspots, due to the high diversity of endemic species and extensive loss of habitats through anthropogenic actions (MMA 2017MMA. 2017. https://www.gov.br/mma/pt-br Retrieved October 13, 2023
https://www.gov.br/mma/pt-br... ). The vegetation of the Cerrado is diverse, presenting characteristics of forest, savannah and grassland formations. Among the various vegetation formations of the Cerrado, there is the Cerrado stricto sensu, which is characterized by trees randomly distributed on the ground in different densities, as well as by the presence of defined tree and shrub-herbaceous strata (Sano et al. 2008SANO, S.M.., ALMEIDA, S.P. de; & RIBEIRO, J.F. 2008. Cerrado: ecologia e flora. Brasília, DF: Embrapa Informação Tecnológica; Planaltina, DF: Embrapa Cerrados, 2008.). It is estimated that the invertebrate fauna of the Cerrado is approximately 90 thousand species. However, this fauna is still poorly known (Oliveira & Frizzas 2008OLIVEIRA, C.M. & FRIZZAS, M.R. 2008. Insetos de Cerrado: distribuição estacional e abundância. Planaltina- DF. In: Embrapa Cerrados, 2008.). Few efforts have sought to study the diversity of insects in Western Bahia, and these have been suffering significant declines mainly because of the destruction of their suitable habitats to meet the demand of agribusiness in the region (Soares et al. 2021SOARES, E.K.S., OLIVEIRA, A.B. de, LIMA, V.P. & CALADO, D. 2021. Insect galls associated with Copaifera sabulicola J.A.S Costa & L.P Queiroz (Fabaceae): Characterization and new records. Rev. Bras. Entomol. 65(4):e20210107., Lima & Calado 2018LIMA, V.P. & CALADO, D. 2018. Morphological characterization of insect galls and new records of associated invertebrates in a Cerrado area in Bahia State, Brazil. Brazilian J. Biol. 78(4):636–643.). Despite this chaotic scenario in the region, recent assessments in the region have characterized the ecology of galling species and described new species in heavily degraded areas (Garcia et al. 2017GARCIA, C. de A., LIMA, V.P., CALADO, D.C. & URSO-GUIMARÃES, M.V. 2017. New species of Lopesia Rübsaamen (Diptera: Cecidomyiidae) associated with Andira humilis Mart. ex Benth. (Fabaceae). Rev. Bras. Entomol. 61(3):239–242., Santos et al. 2018SANTOS, I.M. dos, LIMA, V.P., SOARES, E.K.S., PAULA, M. de & CALADO, D.C. 2018. Insect galls in three species of Copaifera L. (Leguminosae, Caesalpinioideae) occurring sympatrically in a Cerrado area (Bahia, Brazil). Biota Neotrop. 18(1):e20170356., Soares et al. 2021SOARES, E.K.S., OLIVEIRA, A.B. de, LIMA, V.P. & CALADO, D. 2021. Insect galls associated with Copaifera sabulicola J.A.S Costa & L.P Queiroz (Fabaceae): Characterization and new records. Rev. Bras. Entomol. 65(4):e20210107.).

Besides their important role as bioindicators of environmental quality (Santana & Isaias 2014SANTANA, A.P. & ISAIAS, R.M. dos S. 2014. Galling insects are bioindicators of environmental quality in a Conservation Unit. Acta Bot. Brasilica 28(4):594–608.), understanding the diversity of galling insects and the associated flora in tropical Brazilian ecosystems is extremely important to comprehend the patterns of distribution and occurrence of these herbivores in the Cerrado of Western Bahia, which effectively contributes as a tool for ecological study and conservation. Here, we (1) characterize the insect galls found on plant host species, (2) identify the gall-inducing insects to the lowest taxonomic level, and (3) record the presence of gall-associated fauna.

Material and Methods

Our study was carried out along trails in the Serra da Bandeira (–12° 05’ 29’S and –45° 02’ 23’W), located in the municipality of Barreiras (Figure 1). The area has a typical Cerrado vegetation with herbaceous and shrubby vegetation, predominance of subshrubs and shrubs, and great diversity of pioneer species in the secondary phase of succession (Cruz Ruggiero et al. 2002CRUZ RUGGIERO, P.G., BATALHA, M.A., PIVELLO, V.R. & MEIRELLES, S.T. 2002. Soil-vegetation relationships in cerrado (Brazilian savanna) and semideciduous forest, Southeastern Brazil. Plant Ecol. 160(1):1–16.). The region has a seasonal climate, with two well-defined seasons, a rainy one, lasting from October to March, and a dry one, which lasts from April to September. The average annual rainfall in this biome is 1,500mm and temperatures are generally mild throughout the year (Nascimento & Novais 2020NASCIMENTO, D.T.F. & NOVAIS, G.T. 2020. Clima do Cerrado: dinâmica atmosférica e características, variabilidades e tipologias climáticas. Élisée – Rev. Geogr. da UEG 9(2):e922021.).

Figure 1.
Study area. Location of the municipality of Barreiras, Bahia, Brazil depicted in blue. The west region of Bahia is highlighted in light green.

The study area was monthly sampled by the first author throughout one year, between August 2017 and July 2018, through walks between trails lasting 2 hours, which is a method commonly used in inventories of galling insects in Brazil (Soares et al. 2021SOARES, E.K.S., OLIVEIRA, A.B. de, LIMA, V.P. & CALADO, D. 2021. Insect galls associated with Copaifera sabulicola J.A.S Costa & L.P Queiroz (Fabaceae): Characterization and new records. Rev. Bras. Entomol. 65(4):e20210107., Lima & Calado 2018LIMA, V.P. & CALADO, D. 2018. Morphological characterization of insect galls and new records of associated invertebrates in a Cerrado area in Bahia State, Brazil. Brazilian J. Biol. 78(4):636–643., Bregonci et al. 2010BREGONCI, J. de M., POLYCARPO, P.V. & MAIA, V.C. 2010. Galhas de insetos do Parque Estadual Paulo César Vinha (Guarapari, ES, Brasil). Biota Neotrop. 10(1):265–274., Maia & Fernandes 2004MAIA, V.C. & FERNANDES, G.W. 2004. Insect galls from Serra de São José (Tiradentes, MG, Brazil). Brazilian J. Biol. 64(3):423–445.). All plant organs were inspected on the host plants from ground level to the top of the canopy for the presence of insect galls. We then photographed the galls found to better characterize the morphological characteristics such as shape, hairiness and distribution on the plant (Isaias et al. 2013ISAIAS, R.M.S., CARNEIRO, R.G.S., OLIVEIRA, D.C. & SANTOS, J.C. 2013. Illustrated and Annotated Checklist of Brazilian Gall Morphotypes. Neotrop. Entomol. 42(3):230–239.). Next, branches containing flowers and fruits were collected from the host plant for further identification of the species. Collected specimens were stored and transported them to the Laboratory of Invertebrate Zoology at the Federal University of Western Bahia (UFOB). The plant samples collected were stored in newspapers and cardboard containing 70% alcohol for subsequent assembly of specimens. These samples were sent to the BRBA Herbarium of UFOB for species identification by botanical taxonomists and incorporated into the collection under numbers from 7657 to 7676.

In the laboratory, part of the collected galls was dissected using tweezers and a stereomicroscope (Leica S8-APO) to look for the inducer and its associated fauna. The remains were kept in plastic containers containing cotton moistened with water and were stored in a BOD (SL-224) oven at a temperature of approximately 25 ^oC to obtain the insects in the adult phase. We monitored the containers daily for emergence of adult insects. The emerged adults’ insects were used to mount permanent slides following the methodology proposed by Gagné (1994), and later identification using dichotomous keys (Gagné 1994GAGNÉ, R.J. 1994. The gall midges of the Neotropical Region. University Pres, Ithaca.) and other descriptive studies of galling insects. The associated fauna was preserved in 70% alcohol and identified at the lowest possible taxonomic level using identification keys from the Insects from Brazil: Diversity and Taxonomy (Rafael et al. 2012RAFAEL, J.A., MELO, G.A.R., CARVALHO, C.J.B. de, CASARI, S.A. & CONSTANTINO, R. 2012. Insetos do Brasil: Diversidade e Taxonomia. Holos, Editora, Ribeirão Preto.) and Luz & Mendonça Júnior (2019)LUZ, F.A. & MENDONÇA JÚNIOR, M. de S. 2019. Guilds in Insect Galls: Who is Who. Florida Entomol. 102(1):207. as reference. Most of the associated fauna was obtained only at an immature stage and therefore we identified them only at the order level. Lastly, we summarized information on cecidomyids species, host plant species and associated fauna in a table.

Results

We found and characterized 48 distinct gall morphotypes, belonging to 12 plant families (Figures 2, 3 and 4, Table 1). Insect galls showed different morphotypes such as globoid, cylindrical, lenticular, conical, fusiform and marginal leaf fold. The most commonly found were globoid (27.1%), lenticular (27.1%) and cylindrical (25%), followed by conical (12.5%) and fusiform (6.2%). The least abundant shape was marginal leaf fold (2.1%) (Figure 5). We observed insect galls developed on leaves, stems, flowers, inflorescences and fruits. The plant organs most affected by galling insects in the Serra da Bandeira were the leaves (73%), followed by the stem (19%), flower (4%), inflorescence (2%) and fruits (2%) (Figure 6). Green was the most frequent color found among the morphotypes (32), followed by brown (25) and red (11) (Table 1).

Figure 2.
Insect galls found in the Serra da Bandeira (Barreiras, Bahia, Brazil). a. Anacardium humile – Globoid, b. Anacardium humile – Conical, c. Anacardium humile – Globoid, d. Bignoniaceae – Conical, e. Caryocar brasiliense – Globoid, f. Terminalia fagifolia – Conical, g. Terminalia sp. – Cylindrical, h. Combretaceae R. – Conical, i. Erythroxylum sp. – Globoid, j. Manihot caerulescens – Cylindrical, k. Manihot caerulescens – Cylindrical, l. Manihot caerulescens – Cylindrical, m. Copaifera sabulicola – Lenticular, n. Copaifera sabulicola – Lenticular, o. Copaifera sabulicola – Lenticular, p. Copaifera sabulicola – Globoid, q. Copaifera sabulicola – Globoid, r. Copaifera sabulicola – Lenticular, s. Copaifera sabulicola – Lenticular and t. Copaifera sabulicola – Marginal Leaf Fold.

Figure 3.
Insect galls found in the Serra da Bandeira (Barreiras, Bahia, Brazil). a. Copaifera sabulicola – Globoid, b. Copaifera sabulicola – Lenticular, c. Copaifera depilis – Lenticular, d. Copaifera depilis – Globoid, e. Copaifera depilis – Cylindrical, f. Copaifera depilis – Lenticular, g. Copaifera depilis – Globoid, h. Copaifera luetzelburgii – Cylindrical, i. Copaifera luetzelburgii – Lenticular, j. Copaifera luetzelburgii – Lenticular, k. Mimosa sericantha – Cylindrical, l. Mimosa sericantha – Cylindrical, m. Caliandra sp. – Globoid, n. Caliandra sp. – Fusiform, o. Mimosa acutistipula – Cylindrical, p. Fabaceae – Fusiform, q. Bauhinia sp1 – Globoid, r. Bauhinia sp2 – Fusiform, s. Diplopterys sp. – Conical and t. Diplopterys sp. – Globoid.

Figure 4.
Insect galls found in the Serra da Bandeira (Barreiras, Bahia, Brazil). a. Byrsonima sp. – Lenticular, b. Malpighiaceae sp1 – Lenticular, c. Malpighiaceae sp2 – Conical, d. Malvaceae – Cylindrical, e. Eugenia sp. – Cylindrical, f. Eugenia sp. – Cylindrical, g. Ouratea sp. – Lenticular and h. Verbenaceae – Globoid.

Figure 5.
Percentage of gall morphotypes found in the Serra da Bandeira (Barreiras, Bahia, Brazil).

Figure 6.
Percentage of plant organs affected by galling insects in the Serra da Bandeira (Barreiras, Bahia, Brazil).

The host plant families with the highest number of gall morphotypes in Serra da Bandeira were Fabaceae (26), Malpighiaceae (5) and Anacardiaceae, Combretaceae and Euphorbiaceae (3) (Figure 7, Table 1). Furthermore, we found that the genus Copaifera Lindl. (Fabaceae) had the greatest diversity of gall morphotypes, harboring 19 morphotypes distributed in three species that occur sympatrically – Copaifera sabulicola J. Costa (Fabaceae), Copaifera depilis Dwyer (Fabaceae) and Copaifera luetzelburgii Harms (Fabaceae) (Table 1). Here, for the first time in Brazil, we recorded the occurrence of galls on flowers of Manihot caerulescens (Euphorbiaceae), on inflorescences of Mimosa acutistipula (Fabaceae) and flower buds of Anacardium humile (Anacardiaceae), which were induced by Cecidomyiidae. Galls on flowers of Manihot caerulescens Pohl (Euphorbiaceae) was induced by the species Iatrophobia brasiliensis (Rübsaamen, 1908).

Figure 7.
Distribution of insect galls in host plant families found in Serra da Bandeira (Barreiras, Bahia, Brazil).

Cecidomyiidae were found inducing galls in 14 morphotypes. Out of 48 morphotypes found in our study, inducers were not determined for 32 morphotypes. Additionally, we found Hymenoptera in 24 gall morphotypes, Lepidoptera in 2 gall morphotypes and Acari and Pseudoscorpiones in only one gall morphotype (Table 1).

Discussion

Inventories of gall-inducing insects in Brazil indicate Fabaceae as the most common host plant family for galling insects (Marinho et al. 2023MARINHO, R.A., MAIA, V.C. & BARBOSA, M.R. de V. 2023. Entomogenous galls and their associated fauna in deciduous dry forest and woodland vegetation remnants (Caatinga) in the Northern Depressão Sertaneja, Brazil. Biota Neotrop. 23(1):e20221428., Maia 2013a, Lima & Calado 2018LIMA, V.P. & CALADO, D. 2018. Morphological characterization of insect galls and new records of associated invertebrates in a Cerrado area in Bahia State, Brazil. Brazilian J. Biol. 78(4):636–643., Araujo et al. 2019ARAUJO, W.S., FERNANDES, G.W. & SANTOS, J.C. 2019. An overview of inventories of gall-inducing insects in Brazil: looking for patterns and identifying knowledge gaps. An. Acad. Bras. Cienc. 91(1):e20180162.), which confirms the richness hypothesis (Southwood 1960SOUTHWOOD, T.R.E. 1960. The abundance of the Hawaiian trees and the number of their associated insect species. Proc. Hawaiian Entomol. Soc. 17299–303.), also recorded in other studies carried out in the Cerrado (Gonçalves-Alvim & Fernandes 2001bGONÇALVES-ALVIM, S.J. & FERNANDES, G.W. 2001b. Comunidades de insetos galhadores (Insecta) em diferentes fisionomias do cerrado em Minas Gerais, Brasil. Rev. Bras. Zool. 18(1):289–305., Santana & Isaias 2014SANTANA, A.P. & ISAIAS, R.M. dos S. 2014. Galling insects are bioindicators of environmental quality in a Conservation Unit. Acta Bot. Brasilica 28(4):594–608.). Among the Fabaceae family, Copaifera Lindl. (Fabaceae) had a great diversity of gall morphotypes, a result found by Santos et al. (2018)SANTOS, I.M. dos, LIMA, V.P., SOARES, E.K.S., PAULA, M. de & CALADO, D.C. 2018. Insect galls in three species of Copaifera L. (Leguminosae, Caesalpinioideae) occurring sympatrically in a Cerrado area (Bahia, Brazil). Biota Neotrop. 18(1):e20170356., in the same area with three species of the Copaifera (C. sabulicola C. depilis and C. luetzelburgii). Furthermore, Nogueira et al. (2016)NOGUEIRA, R.M., COSTA, E.C., CARVALHO-FERNANDES, S.P. & SANTOS-SILVA, J. 2016. Insect galls from Serra Geral, Caetité, BA, Brazil. Biota Neotrop. 16(1):e20150035., in a study in Serra Geral in the city of Caetité, Bahia, characterized ten morphotypes for Copaifera langsdorffii Desf. (Fabaceae) in transition areas between Cerrado and Caatinga. Therefore, our study contributes to scientific knowledge on insect galls by reinforcing that Copaifera species are super hosts of insect galls.

Here, we describe for the first time the occurrence of insect gall on flowers of Manihot caerulescens Pohl (Euphorbiaceae), which had not been observed in other studies carried out in different Brazilian ecosystems (Carneiro, Borges, et al. 2009CARNEIRO, M.A.A., BORGES, R.A.X., ARAÚJO, A.P.A. & FERNANDES, G.W. 2009. Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, Minas Gerais, Brasil. Rev. Bras. Entomol. 53(4):570–592., Araújo et al. 2011ARAÚJO, W.S. de, SANTOS, B.B. dos & GOMES-KLEIN, V.L. 2011. Insect galls from Serra dos Pireneus, GO, Brazil. Biota Neotrop. 11(2):357–365., Maia 2013a, Scareli-Santos et al. 2018SCARELI-SANTOS, C., SILVA, P.C., CARNEIRO, A.S. & DANTAS, S.P. 2018. Galhas em Manihot esculenta Crantz (Euphorbiaceae): Avaliação dos impactos na arquitetura e na produtividade da planta Hospedeira. Rev. Desafios 5(2):51–59., Saito & Urso-Guimarães 2012SAITO, V.S. & URSO-GUIMARÃES, M.V. 2012. Characterization of galls, insect galls and associated fauna of Ecological Station of Jataí (Luiz Antônio, SP). Biota Neotrop. 12(3):99–107.). Many studies have observed the occurrence of galls exclusively on leaves for the genus Manihot and the inducing insect has been identified as belonging to the genus Iatrophobia (Rübsaamen, 1915) (Diptera, Cecidomyiidae). The occurrence of the species Iatrophobia brasiliensis (Rübsaamen, 1908) in several species of the genus Manihot can be explained by the fact that the species is oligophagous. Carneiro et al. (2009)CARNEIRO, M.A.A., BRANCO, C.S.A., BRAGA, C.E.D., ALMADA, E.D., COSTA, M.B.M., MAIA, V.C. & FERNANDES, G.W. 2009. Are gall midge species (Diptera, Cecidomyiidae) host-plant specialists? Rev. Bras. Entomol. 53(3):365–378. investigated the level of specificity of inducers and identified that about 5.6% of the 196 galling species studied are oligophagous, inducing galls on more than one host plant species of the same genus. Another new record is the occurrence of cylindrical and glabrous galls in the inflorescence of Mimosa acutistipula (Fabaceae), whose inducer is an undetermined species of Cecidomyiidae. Many studies have reported the occurrence of insect galls in species of the genus Mimosa on leaves and stems (Nogueira et al. 2018NOGUEIRA, R.M., COSTA, E.C., SILVA, J.S. & ISAIAS, R.M. dos S. 2018. Structural and histochemical profile of Lopesia sp. Rübsaamen 1908 pinnula galls on Mimosa tenuiflora (Willd.) Poir. in a Caatinga environment. Hoehnea 45(2):314–322., Vieira et al. 2018VIEIRA, L.G., NOGUEIRA, R.M., COSTA, E.C., CARVALHO-FERNANDES, S.P. & SILVA, J.S. 2018. Insect galls in Rupestrian field and Cerrado stricto sensu vegetation in Caetité, Bahia, Brazil. Biota Neotrop. 18(2):e20170402., Nogueira et al. 2016NOGUEIRA, R.M., COSTA, E.C., CARVALHO-FERNANDES, S.P. & SANTOS-SILVA, J. 2016. Insect galls from Serra Geral, Caetité, BA, Brazil. Biota Neotrop. 16(1):e20150035., Costa et al. 2014COSTA, E.C., CARVALHO-FERNANDES, S.P. & SANTOS-SILVA, J. 2014. Galhas de insetos em uma área de transição caatinga-cerrado no Nordeste do Brasil. Sitientibus série Ciências Biológicas. 14:10.13102/scb481
https://doi.org/10.13102/scb481... , Coelho et al. 2013COELHO, M.S., CARNEIRO, M.A.A., BRANCO, C.A. & FERNANDES, G.W. 2013. Gall-inducing insects from Serra do Cabral, Minas Gerais, Brazil. Biota Neotrop. 13(3):102–109.), however, none for the species Mimosa acutistipula. Thus, this is the first record of the insect gall on this plant species, which is rare in field.

Furthermore, we found an unprecedented record of galls on flower buds, induced by a cecidomyiids on Anacardium humile (Anacardiaceae), a species popularly known as cajuí or cajuzinho do Cerrado. The record of galls in the Anacardium genus is very common in leaves (Vieira et al. 2018VIEIRA, L.G., NOGUEIRA, R.M., COSTA, E.C., CARVALHO-FERNANDES, S.P. & SILVA, J.S. 2018. Insect galls in Rupestrian field and Cerrado stricto sensu vegetation in Caetité, Bahia, Brazil. Biota Neotrop. 18(2):e20170402., Araújo et al. 2011ARAÚJO, W.S. de, SANTOS, B.B. dos & GOMES-KLEIN, V.L. 2011. Insect galls from Serra dos Pireneus, GO, Brazil. Biota Neotrop. 11(2):357–365.). Such occurrence on flowers is relevant due to the economic importance, since the insect galls caused deformities in the flower buds, preventing the opening of the flowers and, consequently, the formation of the accessory fruit and the fruit (chestnut). According to ethnobotanical studies, o cajuzinho do Cerrado creates income, serves as food for local communities and consequently improves people’s livelihoods (Vieira et al. 2016VIEIRA, R.F., CAMILLO, J. & CORADIN, L. 2016. Espécies Nativas da Flora Brasileira de Valor Econômico Atual ou Potencial Plantas para o Futuro – Região Centro – Oeste. Ministério do Meio Ambiente, Brasília, DF.). In this context, investigations on the phenology of the plant, aiming at a better understanding of the incidence of the infection, as well as the damage caused in fruits and pseudofruits, are fundamental.

About 65% of the inducer species have not yet been determined, due to the absence of individuals in the adult (male and female), pupa and larva stages. Maia (2013)MAIA, V.C. 2013. Galhas de insetos em restingas da região sudeste do Brasil com novos registros. Biota Neotrop. 13(1):183–209. highlights the need to obtain gallers at each stage of the life cycle, as this is the only way to describe new species. Inducers of the order Diptera (Family Cecidomyiidae) were the most abundant, found in 14 morphotypes of galls. Cecidomyiidae is the main family of gall-inducing insects throughout Brazil and the Neotropics (Gagné & Jaschhof 2017GAGNÉ, R.J. & JASCHHOF, M. 2017. A Catalog of the Cecidomyiidae (Diptera) of the World Fourth Edition Digital., Fernandes et al. 1988FERNANDES, G.W.A., TAMEIRÃO NETO, E. & MARTINS, R.P. 1988. Ocorrência e caracterização de galhas entomógenas na vegetação do campus pampulha da Universidade Federal de Minas Gerais. Rev. Bras. Zool. 5(1):11–29.). The distribution of gallers in the different orders of insects and their host plants, observed in this study, has also been detected by other authors (Carneiro et al. 2009CARNEIRO, M.A.A., BRANCO, C.S.A., BRAGA, C.E.D., ALMADA, E.D., COSTA, M.B.M., MAIA, V.C. & FERNANDES, G.W. 2009. Are gall midge species (Diptera, Cecidomyiidae) host-plant specialists? Rev. Bras. Entomol. 53(3):365–378., Araújo et al. 2011ARAÚJO, W.S. de, SANTOS, B.B. dos & GOMES-KLEIN, V.L. 2011. Insect galls from Serra dos Pireneus, GO, Brazil. Biota Neotrop. 11(2):357–365., Maia 2013a, Scareli-Santos et al. 2018SCARELI-SANTOS, C., SILVA, P.C., CARNEIRO, A.S. & DANTAS, S.P. 2018. Galhas em Manihot esculenta Crantz (Euphorbiaceae): Avaliação dos impactos na arquitetura e na produtividade da planta Hospedeira. Rev. Desafios 5(2):51–59., Saito & Urso-Guimarães 2012SAITO, V.S. & URSO-GUIMARÃES, M.V. 2012. Characterization of galls, insect galls and associated fauna of Ecological Station of Jataí (Luiz Antônio, SP). Biota Neotrop. 12(3):99–107.), confirming that the cecidomyids are the main group of galling insects in the Cerrado.

We showed that the leaf was the organ with the highest number of registered galls as shown in other inventories in the Cerrado (Marinho et al. 2023MARINHO, R.A., MAIA, V.C. & BARBOSA, M.R. de V. 2023. Entomogenous galls and their associated fauna in deciduous dry forest and woodland vegetation remnants (Caatinga) in the Northern Depressão Sertaneja, Brazil. Biota Neotrop. 23(1):e20221428., Maia 2013a). Such preference has been justified due to the availability of resources in the leaves being constantly abundant (Maia 2001MAIA, V.C. 2001. New genera and species of gall midges (Diptera, Cecidomyiidae) from three restingas of Rio de Janeiro State, Brazil. Rev. Bras. Zool. 18(1):1–32.). For this study, the globoid and cylindrical morphotypes were the most expressive, similar to studies conducted by Maia (2014)MAIA, V.C. 2014. Insect galls of Itamonte (Minas Gerais, Brazil): characterization and occurrence. Biota Neotrop. 14(1):e20133839.. Bregonci et al. (2010)BREGONCI, J. de M., POLYCARPO, P.V. & MAIA, V.C. 2010. Galhas de insetos do Parque Estadual Paulo César Vinha (Guarapari, ES, Brasil). Biota Neotrop. 10(1):265–274. found that the majority of galls had the same color as the plant organ, with a predominance of green color as in the leaves. Here, we observe my pattern and that the coloration of some morphotypes can vary over time. Regarding the associated fauna, we found insects primarily belonging the order Hymenoptera, and identified them as parasitoids. According to Gagné (1994)GAGNÉ, R.J. 1994. The gall midges of the Neotropical Region. University Pres, Ithaca., hymenoptera are the main natural enemies of the Cecidomyiidae family. Further, the presence of these parasitoids has been considered a problem for obtaining insect galls at different stages of development and subsequent description (Maia 2013MAIA, V.C. 2013. Galhas de insetos em restingas da região sudeste do Brasil com novos registros. Biota Neotrop. 13(1):183–209.). Although we noticed a pseudoscorpion in the conical morphotype on Diplopterys sp. A. Juss, the occurrence of pseudoscorpions in Brazilian inventories seems to be scarce. Nogueira et al. 2016NOGUEIRA, R.M., COSTA, E.C., CARVALHO-FERNANDES, S.P. & SANTOS-SILVA, J. 2016. Insect galls from Serra Geral, Caetité, BA, Brazil. Biota Neotrop. 16(1):e20150035. also observed the presence of pseudoscorpions in a single gall morphotype and highlighted this likely scarcity.

In short, we characterized the insect galls found on plant host species, identified the gall-inducing insects to the lowest taxonomic level, and recorded the presence of gall-associated fauna. The information provided can be used highly by decision makers for conservation programs, as well as in other strategies for the conservation of biological diversity in the Brazilian Cerrado.

Acknowledgments

We thank the Federal University of Western Bahia (UFOB) for the structure provided and the Bahia State Research Support Foundation (FAPESB) for the master’s scholarship (Term of grant BOL0374/2020).

Data Availability

Codes are available on https://doi.org/10.5281/zenodo.8104868

References

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