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ECOSYSTEMS • An. Acad. Bras. Ciênc. 93 (suppl 3) • 2021 • https://doi.org/10.1590/0001-3765202120201442 linkcopy

Open-access Insect galls and associated fauna in two areas of Cerrado sensu stricto in the State of Bahia, Brazil

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    Abstract

    This study inventoried and characterized the richness of galling insects based on gall morphotypes and their host plants in two Cerrado sensu stricto areas of Caetité municipality in Bahia State, Brazil, to aid the identification of galling insects and their host plants, as well as to contribute to the knowledge and conservation of local biodiversity. The survey was conducted in the Moita dos Porcos archaeological site and João Barroca Farm site, adopting the random walking methodology for sampling, during 12 months. We recorded 98 gall morphotypes on 42 plant species belonging to 36 genera and 22 families. Leguminosae, Malpighiaceae and Myrtaceae demonstrated the greatest richness of galls, and the Copaifera langsdorffii was the super-host species, with 16 gall morphotypes. Most galls occur on leaves, and may be globoid, glabrous, grouped, and are usually unilocular, and brown. The galling insects identified belonged to Coleoptera, Diptera, Lepidoptera, and Thysanoptera. Eight plant host species and eight gall morphotypes were recorded for the first time in Cerrado areas in Brazil. The areas surveyed demonstrated high richness of gall morphotypes and host plants, evidencing the importance of studying and preserving different areas of the same biome.

    Key words Copaifera galls; gall morphotypes; Malpighiaceae; savanna

    INTRODUCTION

    Brazilian Cerrado is a hostpost of biodiversity, which is formed by mosaic of different phytophysiognomy, demonstrating elevated levels of species richness. It hosts more than 12,330 plant species (BFG 2018, 2021) and one third of Brazilian biodiversity, with a high level of endemism, making it the most biodiverse savanna in the world (Klink & Machado 2005). In the state of Bahia, the Cerrado covers an area of approximately 9.1 million hectares (Faleiro 2015) distributed mainly in the western region of the state (Harley 1995). In addition, the Cerrado of Bahia is also distributed in higher regions forming small patches interspersed by Campos Rupestres, Caatinga and Seasonal Forests and transition areas, as occurs in Chapada Diamantina (Harley et al. 2005), and Serra Geral of the Caetité municipality (Bahia State, Brazil).

    The Brazilian Cerrado is also one of the most threatened biomes, due to continuing deforestation. It is estimated that 43% of its native vegetation has already been removed or transformed (MMA 2015). The Cerrado areas of the Caetité municipality have been subjected to constant environmental impacts (Rodrigues et al. 2017) due to iron ore and limestone rock extraction (DNPM 2014), the construction of wind farms (Prudente et al. 2017), and amethyst mining.

    Cerrado vegetation has several interactions among plants and herbivores (Ribeiro & Fernandes 2000, Furtado et al. 2003, Cintra et al. 2020). Among the different forms of herbivory, the endophytic habit of galling insects is by far the most sophisticated (Shorthouse et al. 2005). Galling insects are capable of inducing galls through disordered processes of hyperplasia, hypertrophy, and cellular differentiation in plant tissues (Ferreira & Isaias 2013). The structures resulting from those interactions provide shelter for the gall-inducing insect against abiotic and biotic factors, allowing its successful development, and energetic resources for nutrition of the inducers (Price et al. 1987, Stone & Schönrogge 2003).

    The Brazilian Cerrado has been the subject of in-depth studies on the richness of galls, mainly in state of Minas Gerais (e.g., Gonçalves-Alvim & Fernandes 2001, Urso-Guimarães et al. 2003, Carneiro et al. 2009a, Araújo & Guilherme 2012, Coelho et al. 2013, Cintra et al. 2020). The richness of gall studies in the Cerrado of Bahia State has been little studied; only five has yet been undertaken in the municipalities of Caetité (Nogueira et al. 2016, Vieira et al. 2018, Silva et al. 2018, Santana et al. 2020) and Barreiras (Lima & Calado 2018). These studies in the Cerrado of Bahia recorded a total of 144 different types of galls in 103 plant species.

    Studies of galling insect richness have demonstrated the usefulness of that insect guild as a measure of environmental conservation and quality (Santos et al. 2012, Santana & Isaias 2014, Brito et al. 2018). The entomofauna associated with galls responds to environmental disturbances, with resulting losses of species richness and abundance (which also impact their natural enemies) (Oliveira 2009). As such, inventories of gall-inducing insect richness can assistance in urban planning, design, and management (Julião et al. 2005) as well as for environmental monitoring and conservation activities (Santana & Isaias 2014, Melo-Júnior et al. 2018). Here, we realized an inventory of the richness of galling insects in two Cerrado sensu stricto areas of the Caetité municipality (Bahia) and a similarity analysis between areas based on gall morphotypes and their host plants to contribute to the knowledge and conservation of local biodiversity.

    MATERIALS AND METHODS

    Study area

    The study was carried out in two localities of Cerrado sensu stricto vegetation in the municipality of Caetité, Bahia State, Brazil: João Barroca Farm (JB) (14°19’23.96” S and 42°33’’7.91” W) situated about 40 km of Caetité’s center, and the Moita dos Porcos archaeological site (MP) (14°10’1.52” S and 42°31’’16.05” W) approximately 15 km from the city center. The areas studied were selected on the basis of accessibility for sampling, the distance from previously sampled areas, and the presence of preserved vegetation (Costa et al. 2014a, b, Nogueira et al. 2016, Vieira et al. 2018, Silva et al. 2018, Santana et al. 2020). The JB comprises approximately 105 hectares of preserved area at 950 m elevation, while the MP covers approximately 300 hectares of preserved area at 920 m elevation. The vegetation is composed of many herbaceous and woody species, with a palm (Syagrus werdermannii Burret, Arecaceae) and sparse trees from 2 to 3 m tall (e.g., Hymenaea courbaril L., Leguminosae). The soil is sandy to sandy with rock outcrops on the higher elevation sites (Alves 2008). The regional climate is Aw (Alvares et al. 2013), with a mean annual temperature of 21.4°C and mean annual rainfall of 862 mm (IBGE 2015).

    Sampling method

    The Cerrado vegetation was examined during 12 months, between May 2016 to April 2017 throughout the MP site and between August 2017 to July 2018 at the JB site, adopting the random walking methodology for sampling (Julião et al. 2002, Oliveira & Maia 2005, Coelho et al. 2009). In these areas, the galls and the host plants were collected once a month by two people working for four person-hours along pre-existing trails, totaling 96 hours of total collecting efforts. All plant architectural types (herbaceous, shrub, arboreal, tree and vines) up to 2 m tall were inspected. Each gall morphotype was photographed in field, and characterized based on shape, color, presence or absence of trichomes, number of internal chambers (Isaias et al. 2013). Specimens of the host plants were collected, pressed, and deposited in the Caetité Collection of the HUNEB herbarium. The plants were identified by consulting the taxonomic literature and contacting botanical specialists, and by comparisons with herbarium collections at the Universidade do Estado da Bahia (HUNEB, Caetité collection) and the Universidade Estadual de Feira de Santana (HUEFS). Plant nomenclature was verified in the Flora do Brasil 2020 (www.floradobrasil.jbrj.gov.br) and, the names are presented in alphabetical order by family, following APG IV (2016). The circumscription of the Leguminosae family was based on classification proposed by LPWG (2017).

    The samples of each gall morphotypes collected in the field were analyzed in laboratory. Galls were dissected under a stereomicroscope to retrieve any larvae of the gall-inducing insects and/or associated fauna, as well as observation the number of larval chamber. To obtain adults, samples of each gall morphotype were held separately in labeled plastic containers (lined with paper) and inspected daily. All of the insects obtained were conserved in 70% alcohol and sent to be identified at the Diptera Laboratory of the National Museum at the Universidade Federal do Rio de Janeiro.

    Statistical Analysis

    Sørensen’s similarity index (S= 2c/a+b) (Sørensen 1948) was used to compare the two localities in relation to the host plants (c = number of host plant species common to JB and MP, a = number of species in JB and b = number of species in MP) and gall morphotypes (c= number of gall morphotypes common to JB and MP, a = number of gall morphotypes in JB and b = number of gall morphotypes in MP).

    RESULTS

    We recorded 98 gall morphotypes on 42 plant species belonging to 36 genera and 22 families (Table I; Figures 1-5). Galls were recorded for the first time on the plant species Alchornea tiliifolia (Benth.) Müll. Arg. (Euphorbiaceae, Fig. 1m), Byrsonima correifolia A. Juss. (Malpighiaceae, Fig. 4c), Dalbergia acuta Benth. (Leguminoseae-Papilionoideae, Fig. 3m), Erythroxylum stipulosum Plowman (Erythoxylaceae, Fig. 1l), Eugenia lucidifolia Barb. Rodr. (Myrtaceae, Fig. 5b), Pseudobrickellia brasiliensis (Spreng.) R. M. King & Rob. (Asteraceae, Fig. 1h), Senna cana (Nees & Mart.) H. S. Irwin & Barneby var. cana (Leguminoseae- Caesalpinioideae, Fig. 2f), and Lippia origanoides Kunth (Verbenaceae, Fig. 5p).

    Figure 1
    Insect galls in two areas of Cerrado sensu stricto vegetation in Caetité, Bahia State, Brazil. a-b. Anacardium humile; c. Annonaceae Indet. d. Annona leptopetala; e-f.Duguetia furfuracea; g. Moquiniastrum paniculatum; h. Pseudobrickellia brasiliensis; i. Maytenus sp.; j. Combretum leprosum; k. Erythroxylum suberosum; l. Erythroxylum stipulosum; m. Alchornea tiliifolia; n. Manihot tripartita; o. Ocotea lancifolia;p-r. Calliandra dysantha; s. Calliandra macrocalyx; t. Mimosa gemmulata.
    Figure 2
    Insect galls in two areas of Cerrado sensu stricto vegetation in Caetité, Bahia State, Brazil. a-d. Mimosa gemmulata; e. Senegalia langsdorffii; f. Senna cana var. cana; g-i. Bauhinia acuruana; j-l. Bauhinia pulchella; m-t. Copaifera langsdorffii.
    Figure 3
    Insect galls in two areas of Cerrado sensu stricto vegetation in Caetité, Bahia State, Brazil. a-h. Copaifera langsdorffii; i. Copaifera luetzelburgii; j-k. Hymenaea courbaril; l. Andira parvifolia; m. Dalbergia acuta; n. Dalbergia miscolobium; o. Struthanthus sp.; p-q. Malpighiaceae Indet. 1; r. Malpighiaceae Indet. 2; s. Malpighiaceae Indet. 3.; t. Malpighiaceae Indet. 4.
    Figure 4
    Insect galls in two areas of Cerrado sensu stricto vegetation in Caetité, Bahia State, Brazil. a-b. Banisteriopsis malifolia; c. Byrsonima correifolia; d-e. Byrsonima gardneriana; f-h. Byrsonima sericea; i. Byrsonima sp.; j. Diospyros sp. k. Diplopterys pubipetala; l. Stigmaphyllon paralias; m. Helicteres sp.; n-o. Moraceae Indet. 1.; p. Myrtaceae Indet. 1; q. Myrtaceae Indet. 2; r. Myrtaceae Indet. 3; s. Eugenia sp.; t. Eugenia dysenterica.
    Figure 5
    Insect galls in two areas of Cerrado sensu stricto vegetation in Caetité, Bahia State, Brazil. a. Eugenia dysenterica; b. Eugenia lucidifolia; c-e. Eugenia punicifolia; f-g. Myrcia tomentosa; h. Guapira laxa; i-j. Ouratea semiserrata; k. Ouratea sp.; l. Turnera harleyi; m. Roupala montana; n. Rubiaceae Indet.; o. Trigonia nivea; p. Lippia origanoides; q-r. Qualea parviflora.
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    Table I
    Insect galls of areas of Cerrado sensu stricto vegetation in the municipality of Caetité, Bahia State, Brazil. Abbreviations: JB, the João Barroca farm; MP, the Moita dos Porcos Archaeological Site.

    A total of 73 gall morphotypes were found on the JB farm on 35 plant species belonging to 31 genera and 20 families (Table I). The species of the families Leguminosae, Malpighiaceae and Myrtaceae hosted the greatest gall richness, with 31, nine, and nine morphotypes, respectively. The plant genera with the greatest richness of gall morphotypes were Copaifera L. (Leguminosae-Detarioideae) (n = 13, n = 2 host species) and Byrsonima Rich. ex Kunth (Malpighiaceae) (n = 7, n = 4 host species). The super-host species with the greatest richness of gall morphotypes was Copaifera langsdorffii Desf (n = 12 gall morphotypes; Figs. 2m-o, 2q-t, 3a-e).

    On the MP archaeological site, 40 gall morphotypes were found on 29 plant species belonging to 18 genera and 13 families (Table I). The plant families that hosted the greatest richness of gall morphotypes were Leguminosae and Malpighiaceae (n = 16 and n = 8, respectively). The plant genera with the greatest richness of galls were Copaifera L. (n = 10 gall morphotypes, n = 2 host species) and Byrsonima Rich. ex Kunth (n = 5 gall morphotypes, n = 3 host species). The super-host species with the greatest richness of gall morphotypes was Copaifera langsdorffii (n = 9 gall morphotypes; Figs. 2m-n, p, r, t, 3a, f-h).

    The galls were found only on vegetative organs: leaves (n = 88, 57 in JB and 32 in MP), stems (n = 23, 15 in JB and eight in MP), and buds (n = 4 in JB). Most gall morphotypes occurred on a single plant organ; only one gall morphotype induced on Moquiniastrum paniculatum (Less.) G. Sancho (Asteraceae) was observed on both stems and leaves (Table I, Fig. 1g).

    The most frequent gall shapes were globoid (n = 54, 32 in JB and 22 in MP), lenticular (n = 23, 15 in JB and 8 in MP), and fusiform (n = 12, 7 in JB and 5 in MP). Most galls were glabrous (n = 101, 67 in JB and 34 in MP), unilocular (n = 94, 64 in JB and 30 in MP), and solitary (n = 58, 41 in JB and 17 in MP) or grouped (n = 55, 32 in JB and 23 in MP). Gall color were green, brown, red, yellow, orange, gray, white, black or purple, being the brown color the most frequent (n = 44, 26 in JB and 18 in MP). The globoid leaf galls of Combretum leprosum Mart. (Combretaceae) could be green, yellow (Fig. 1j) red, or brown.

    The inducer insects that emerged (from only 33 gall morphotypes) belonged to the orders Diptera, Cecidomyiidae (n = 27, 19 in JB, eight in MP), Lepidoptera (n = 2 in JB), Thysanoptera (n = 1 in JB), and Coleoptera (n = 1 in MP). The associated fauna was found in 17 gall morphotypes (n = 13 in JB, 10 in MP), and composed by parasitoids (Hymenoptera, n = 9, 9 in JB, four in MP), predators (Araneae, n = 3, one in JB, three in MP), inquilines (Hemiptera [n = 2, one in JB, one in MP] and Thysanoptera [n = 2, one in JB, one in MP]), and successors (Formicidae n = 1 in JB and MP).

    The Sørensen’s index values indicated high similarity in host plants between JB farm and MP archaeological site (S=0.66). These localities shared 15 host plant species (Table I). In relation to the morphotypes galls, the similarity is low (S=0.36), with only 15 gall morphotypes common to both areas, showing that these localities differed in relation to the gall composition species.

    DISCUSSION

    The gall richness in JB and MP were high in comparison to other areas with Cerrado sensu stricto vegetation (Araújo et al. 2007, Urso-Guimarães et al. 2003, Coelho et al. 2013, Nogueira et al. 2016), corroborating other studies that indicate that the Cerrado has the richest fauna of galling insects in Brazil (Araújo 2018, Cintra et al. 2020).

    The plant families with the greatest numbers of species in a given area generally correspond to those that host the greatest gall richness (Araújo et al. 2014, Santos-Silva & Araújo 2020). Leguminosae, Malpighiaceae and Myrtaceae were the main host plant families of galls in the two Cerrado s.s. areas, a result similar to reports of other inventories realized in the Bahia Cerrado (Nogueira et al. 2016, Vieira et al. 2018). Those botanical families together with Asteraceae and Melastomataceae hosting a rich diversity of gall-inducing insects in the Cerrado (n = 468 gall morphotypes), with many species bearing galls (n = 263 spp.) (Cintra et al. 2020).

    In addition to those super-host plant families, gall richness can be influenced by presence of super-host species that hosted more than double the number of gall morphotypes compared to other species (Mendonça 2007, Araújo et al. 2013), as is evidenced to Copaifera langsdorffii is this study. This species is frequent in the study area and is considered one of the principal super-hosts of galls in the Brazilian Cerrado (Costa et al. 2010, Lima & Calado 2018, Fagundes et al. 2018). According to Araújo et al. (2013), the plant species richness explains more than 49 % of the gall inducing insect species richness in the Neotropical savannas, because their important role in the attraction of natural enemies and adaptive radiation of galling species.

    Galls induced principally on leaves followed by stems is similar to the patterns seen throughout Brazil (Fernandes & Negreiros 2006, Santos et al. 2011b, 2012a, Toma & Mendonça Júnior 2013, Santana & Isaias 2014, Nogueira et al. 2016, Silva et al. 2018). Leaves are considered to be more plastic host organs as compared to stems (Isaias et al. 2013). Additionally, it has been proposed that greater incidence of leaf galls reflects higher levels of nutritional reserves available in the leaves and their photosynthetic capacities (Castro et al. 2012). Almost all galls occurred on a single plant organ, confirming the gall-inducer specificity for the host plant organ (Dreger-Jauffret & Shorthouse 1992).

    Globoid, lenticular, and fusiform galls are generally the predominate shapes in inventories in the Neotropical region (e.g., Urso-Guimarães et al. 2003, Maia 2013a, b, Costa et al. 2014b, Vieira et al. 2018, Silva et al. 2018). The association between gall morphotypes and host organs was observed, with most globoid and lenticular galls being found on leaves, while fusiform shapes were most common on host stems. Stem galls are often elongated and/or appressed to that organ, following length (Isaias et al. 2013, Ferreira & Isaias 2013, Santana & Isaias 2014). While leaf galls tend to distributed equally over the leaf blade, making maximum and efficient use of that surface as well as its total volume, which the cell expansions can occur in all directions (Isaias et al. 2013).

    The gall color were predominantly brown, similar to the colors reported in Cerrado and Caatinga-Cerrado transition sites in the Serra Geral at Caetité (Nogueira et al. 2016). The brown color of leaf galls often indicates their final stages of development (Carneiro et al. 2017). In addition, the gall color can also indicate the presence of parasitoids or aposematism (Inbar et al. 2010, Dias et al. 2013). As such, gall color variations represent an open field for research, and their colors may serve to alert predators to the possible presence of toxic compounds (Inbar et al. 2010).

    In spite of numerous inventories of galls in different Brazilian ecosystems, our lack of knowledge about the inducer insect species is a barrier to more comprehensive studies (Melo-Júnior et al. 2018). That situation reflects the difficulty of obtaining specimens of galling insects (including immature and adult phases of both sexes, necessary for species determinations), the prevalence of galls that have already been abandoned by their inducer, our general lack of knowledge of the life histories of the gall inducers, the limited number of taxonomists specialized in gall-inducing groups, and the high mortality rates to the host galler larvae, due the incidence of parasitoids (Espírito-Santo & Fernandes 2007, Carneiro et al. 2009b, Gagné & Jaschhof 2017, Melo-Júnior et al. 2018). Of the 98 gall morphotypes recorded in the present work, the insect inducers were identified in only 26 (24 insects to family, one to genus, and just one to species level [Myrciaryiamia admirabilis Maia, 2007, Diptera, Cecidomyiidae]). The Cecidomyiidae (Diptera) were found to be the principal gall inducers, as expected. Cecidomyiidae stands out in the literature as one of the principal gall-inducing groups in the Neotropics (e.g., Carneiro et al. 2009b, Santos et al. 2011a, 2012a, b, Maia 2013a, b, Costa et al. 2014b, Nogueira et al. 2016, Gagné & Jaschhof 2017, Silva et al. 2018, Santana et al. 2020, Santos-Silva & Araújo 2020).

    The parasitoids were more frequent than inquilines, predators, and successors - another pattern recovered in our results. Plant galls are preyed upon by a diverse group of parasitoids belong to Hymenoptera. These organisms frequently cause high mortality rates to the host gall-inducing larvae (Weis & Abrahamson 1985, Price & Clancy 1986). The parasitoid community associated with host plant from Cerrado vegetation had already been widely reported in other inventories (Maia 2001, Maia & Fernandes 2004).

    Our results add evidences to the plant diversity hypothesis, the leaves as mainly host organ, the predominance of globoid gall, and Cecidomyiidae as one of the principal gall-inducing groups in Cerrado of Caetité, Bahia. We report new species of host plants and new gall morphotypes for the Brazilian Cerrado, which contribute to the understanding of the distribution and diversity of galls in the Cerrado. The great richness of gall morphotypes and host plants found and the high incidence of galling insects of uncertain taxonomic identities indicate that many of them must represent new records for the region, which suggests for the conservation of the two study areas. Additionally, the galling insect guild and the host plant composition varied among Cerrado localities, evidencing the importance of studying and preserving different areas of the same biomes.

    ACKNOWLEDGMENTS

    The authors are grateful to Msc. Jamile Jorge Ferreira, Cleiton Couto, and Jaqueline Teixeira for their help with the field collections; to Dr. Luciano Paganucci, Dr. Flávio França, and Dr. Efigênia de Mello at the Universidade Estadual de Feira de Santana (UEFS) for their help in identifying the botanical material; and to the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq 406111/2016-2), the Fundação de Amparo à Pesquisa do Estado da Bahia (FAPESB 9648/2015) and the Universidade do Estado da Bahia (Propublic - 015/2019) for financial support. JSS is grateful to Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro - FAPERJ (E-26/202.501/2019) and CNPq (160015/2019-7) for her research grant.

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    Publication Dates

    • Publication in this collection
      24 Sept 2021
    • Date of issue
      2021

    History

    • Received
      8 Sept 2020
    • Accepted
      16 Feb 2021
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