Open-access Insect galls of the Chapada Diamantina, Rio de Contas, Bahia, Brazil

Abstract

We surveyed insect galls and their host plants in areas of Caatinga and Cerrado in the municipality of Rio de Contas, in the extreme south of the Chapada Diamantina (Bahia state), between 703 and 1,897 m altitude, in order to contribute to the knowledge and conservation of local biodiversity. The survey was conducted in eight locations, adopting the random walking methodology for sampling, four in Caatinga and four in Cerrado, covering distinct phytophysiognomies (cerrado sensu stricto, gallery forest, shrubby caatinga, riparian forest, and rocky field). Eighty-four different insect gall morphotypes were reported, 48 (57.14%) of them on 42 host species in Cerrado and 36 (42.86%) on 24 host species in Caatinga. Most galls occurred on leaves (48.72%) and were globoid (53.76%), glabrous (52.92%), isolated (55.44%), usually one-chambered (61.32%), and brown (25.2%). The gall-inducing insects identified belonged to Lepidoptera (n = 1), Thysanoptera (n = 1), Hemiptera (n = 2), and Diptera (Cecidomyiidae) (n = 16). This was the first inventory of galls in the Chapada Diamantina, so all records are new for the region. We also recorded the first occurrences of galls on two Cerrado plant species and on two in the Caatinga. We found a significant positive correlation between gall richness and plant species richness, suggesting that radiation of gall-inducing insects may be associated with plant species richness.

Keywords: Cecidomyiidae; Fabaceae; Gall-inducing insect; Host plant; Semi-arid

INTRODUCTION

Gall inventories are essential to know the richness of gall-inducing insects and their host plants, moreover they provide reliable data on the identification of the host plants and of gall-inducing insects, plus the detailed characterization of the gall. As example, we can mention some recent inventories: Campos et al. (2021), Maia & Mascarenhas (2022), and Proença & Maia (2023). Furthermore, new species of gall-inducing insects (as Clinodiplosis cecropiae Proença & Maia, 2020 and Distinctamyia matogrossensis Proença & Maia, 2021, for example), as well as the associated fauna, can be discovered during these inventories (Campos et al., 2021; Maia & Mascarenhas, 2022; Proença & Maia, 2023), thus contributing to knowledge about the biological interactions between different guilds. In addition, these studies increase knowledge of regional biodiversity and help in the search for patterns of distribution of the gall-inducing species involved; these data can be used in the preparation of management plans and biodiversity conservation of both natural and priority areas for conservation of flora and fauna (Silva et al., 2011).

Investigations on the richness of gall-inducing insects and their host plants have been carried out in different phytophysiognomies in Brazil (Araújo et al., 2019), including cerrado s.s. (e.g.,Araújo et al., 2014; Campos et al., 2021), caatinga (e.g.,Santos et al., 2011a; Carvalho-Fernandes et al., 2012), restinga (e.g.,Maia, 2001, 2018), rocky fields (e.g.,Carneiro et al., 2009b; Coelho et al., 2013a), dry tropical forest (Coelho et al., 2009), montane fields (Coelho et al., 2013b), and moist forest (e.g.,Julião et al., 2005; Almada & Fernandes, 2011). There are still large gaps in our knowledge about the richness of gall-inducing insects of several phytophysiognomies of Northeastern Brazil, due to the large area and scattered studies concentrated in two of its nine states, Bahia and Pernambuco (Santos et al., 2011b; Carvalho-Fernandes et al., 2012; Costa et al., 2014a, b; Nogueira et al., 2016; Alcântara et al., 2017; Brito et al., 2018; Santos et al., 2018; Silva et al., 2018; Vieira et al., 2018; Santos et al., 2019; Santana et al., 2020; Campos et al., 2021; Santos-Silva et al., 2022). Recently, Cintra et al. (2021) compiled the occurrence of 100 host plant species and 156 morphospecies of gall-inducing insects for the Caatinga based on information available in the literature. The true numbers of gall-inducing insects and host plant species in the Caatinga, however, should be greater because many areas of the region have never been inventoried including the Chapada Diamantina (northern portion of the Espinhaço Range, Bahia).

The Chapada Diamantina, located between the Caatinga and Cerrado biomes, has different phytophysiognomies that change over short distances, including rocky fields, cerrado s.s., caatinga and forest (Neves et al., 2016). This mosaic of vegetation hosts a great wealth of species of fauna and flora important for the biodiversity of mountains in Brazil (Neves & Conceição, 2010) and for the study of how plants and gall-inducing insects interact. Despite this, the Chapada Diamantina was considered an extremely unknown region by the Ministério do Meio Ambiente (MMA, 2002) and therefore a priority for scientific research.

Given this context, the present study aimed to inventory for the first time the gall-inducing insects and their host plants in phytophysiognomies of the Cerrado and Caatinga biomes in the municipality of Rio de Contas, extreme south of the Chapada Diamantina, Bahia. Considering that gall-inducing insects are highly specialized on their host plants and dependent on the occurrence, abundance and distribution of plants (Cuevas-Reyes et al., 2003; Carneiro et al., 2009a, 2014), we evaluated if plant species richness is an important factor determining the species richness and composition of gall-inducing insects in adjacent habitats that differed in humidity, vegetation, and leaf phenology.

MATERIAL AND METHODS

The present study was carried out in the municipality of Rio de Contas (13°34′44″S, 41°48′41″W), which comprises 1,071 km² and is located in the extreme south of the Chapada Diamantina, in the state of Bahia (Fig. 1). This municipality has a mild mesothermal climate, Cwb type, characterized as semi-humid tropical, with rainy summers and dry winters. The rains occur more frequently in summer (November, December, and January), with a secondary peak from March to April; and the rains decrease from August to November (Harley, 1995; Nascimento et al., 2010). The vegetation is formed by shrubby caatinga, rocky fields, cerrado sensu stricto, and gallery and riparian forests, which grow on quartzite and sandstone soils, at altitudes from 700 m (SEI, 2016) to 1,970 m altitude (Pico das Almas - the third highest mountain in the Northeast region of Brazil).

Figure 1
Geographical overview of the Chapada Diamantina, showing the location of the study areas.

In order to sample a large geographic area like the municipality of Rio de Contas, the sampling effort was distributed over as many phytophysiognomies as possible. The study areas are inserted in the Cerrado and Caatinga biomes, four in each biome, covering all the phytophysiognomies of the municipality, cerrado sensu stricto, gallery forest, shrubby caatinga, riparian forest, and rocky fields (Andrade-Lima, 1981; Ribeiro & Walter, 2008; Moro et al., 2016; Table 1, Fig. 2). Ten collections were made along the trails at eight different locations during the period from July to October 2021 (Fig. 1). A team of three individuals spent four hours at each collection point, totaling a sampling effort of 40 hours. All plant habits (subshrubs, trees and creepers) up to 2 meters high were surveyed. When found, the galls were photographed, collected, stored, and labeled in plastic bags. All morphological information about the galls was recorded, including coloration, host organ, pilosity, and shape, using the terminology proposed by Isaias et al. (2013).

Table 1
Collection sites of the galls and their host plants occurring in the municipality of Rio de Contas, extreme south of the Chapada Diamantina, Bahia, Brazil.

Figure 2
Sampled area of the Chapada Diamantina, Rio de contas, Bahia, Brasil. (A-C) Rupestrian field; (D-E) Riparian forest; (F) Cerrado s.s.; (G) Shrubby caatinga; (H) Gallery forest; (I-J) Shrubby caatinga. Photos: Tainar Araújo.

Some of the galls were stored in plastic containers in the laboratory together with moistened paper towels to maintain humidity. This allows the emergence of the gall-inducing insects and any associated fauna, which was classified according to Luz & Mendonça-Júnior (2017). Other samples were dissected under a stereomicroscope to determine the number of chambers in each gall and to extract the larvae. Both the larvae and the emerging winged insects were preserved in 70% ethanol. In the empty galls, the identifications of the insect species were undertaken by comparisons with the morphotypes of known gall-inducing insects in host plants species previously identified in Cerrado and Caatinga environments in Brazil (e.g.,Santos et al., 2011a, b; Carvalho-Fernandes et al., 2012; Costa et al., 2014a; Nogueira et al., 2016; Brito et al., 2018; Vieira et al., 2018).

The host plants were collected, field-pressed, dried, and mounted according to the methodology of Peixoto & Maia (2013). The identification of the plants was done with the help of analytical keys found in specialized literature, and by comparing with the existing material in the herbarium of the Universidade do Estado da Bahia (HUNEB - Caetité Collection). Plant nomenclature was verified in the Flora e Funga do Brasil (https://floradobrasil.jbrj.gov.br), and the names are presented in alphabetical order by family, following APG IV (2016). The circumscription of the Fabaceae family was based on classification proposed by LPWG (2017). The preliminary conservation status of the plant species was verified in the Flora e Funga do Brasil, and it was defined according to the categories proposed by IUCN (2022) (EN = endangered, LC = least concern, NE = not evaluated, NT = near threatened, VU = vulnerable).

The total number of plant species sampled was used as the explanatory variable of gall-inducing species richness (Carneiro et al., 2014). To analyze the relationships between plant species richness and the gall-inducing species richness (y-axis) was adjusted using a zero-truncated model (Hilbe, 2014). The likelihood ratio test was used to compare goodness of fit of the models. The analyses were performed using the R software package (R Core Team, 2023).

RESULTS

We recorded 84 gall morphotypes on 42 species belonging to 37 genera, and 26 plant families along the eight trails of the Rio de Contas (Table 2, Figs. 3-8). Galls were recorded for the first time for Brazil on individuals of Combretum glaucocarpum Mart. (Combretaceae) (Table 2, Fig. 4H-I) and Mimosa hypoglauca Mart. (Fabaceae) (Table 2, Fig. 6O), both growing in caatinga vegetation, and on Lippia alnifolia Mart. & Schauer (Verbenaceae) (Table 2, Fig. 8H), and Drimys brasiliensis Miers (Winteraceae) (Table 2, Fig. 8K) both found in rocky fields. Most of the host species are native to Brazil, of which 12 are endemic (Table 3). In addition, a stem gall was recorded in the exotic species Mangifera indica L. (Anacardiaceae) (Table 2, Fig. 3B) in riparian forest. Concerning IUCN (2022) conservation categories, plant species were classified into NE (n = 35), LC (n = 5), VU (n = 1), and DD (n = 1) (Table 3).

Table 2
Insect gall of the da Chapada Diamantina, Rio de Contas, Bahia, Brazil. PA = Pico das Almas. CBJ = Capela do Bom Jesus. SC = Sitio das Cachoeirinhas. CF = Cachoeira do Fraga. CR = Cachoeira do Raposo. CVN = Cachoeira Véu da Noiva. ER = Estrada Real.

Figure 3
Insect gall of the da Chapada Diamantina, Rio de Contas, Bahia, Brazil. (A) Astronium fraxinifolium Schott ex Spreng.; (B) Mangifera indica L.; (C) Duguetia furfuracea (A. St.-Hil.) Saff.; (D) Annonaceae Indet.; (E-F) Annonaceae sp.; (G-J) Aspidosperma tomentosum Mart.; (K) Baccharis minutiflora Mart. ex Baker.; (L) Mikania sp.; (M) Eremanthus erythropappus (DC.) MacLeish; (N) Moquiniastrum polymorphum (Less.) G. Sancho; (O) Bignoniaceae indet.; (P) Protium heptaphyllum (Aubl.) Marchand. Photos: Tainar Araújo.

Figure 4
Insect gall of the da Chapada Diamantina, Rio de Contas, Bahia, Brazil. (A-F) Calophyllum brasiliense Cambess.; (G) Parinari obtusifolia Hook. f.; (H-I) Combretum glaucocarpum Mart.; (J) Diospyros sericea A.DC.; (K-L) Erythroxylum suberosum A. St.-Hil.; (M) Croton adamantinus Müll. Arg.; (N) Bauhinia sp.; (O-P) Bauhinia catingae Harms. Photos: Tainar Araújo.

Figure 5
Insect gall of the da Chapada Diamantina, Rio de Contas, Bahia, Brazil. (A-D) Bauhinia pulchella Benth.; (E) Calliandra sp.; (F) Calliandra dysantha Benth.; (G-K) Copaifera depilis Dwyer.; (L-N) Copaifera langsdorffii Desf.; (O-P) Copaifera luetzelburgii Harms. Photos: Tainar Araújo.

Figure 6
Insect gall of the da Chapada Diamantina, Rio de Contas, Bahia, Brazil. (A-B) Copaifera luetzelburgii Harms.; (C-F) Copaifera sabulicola A.S. Costa & L.P. Queiroz; (G) Dalbergia miscolobium Benth.; (H) Hymenaea courbaril L.; (I-J) Hymenaea martiana Hayne; (K-N) Mimosa gemmulata Barneby.; (O) Mimosa hypoglauca Mart.; (P) Mimosa tenuiflora (Willd.) Poir. Photos: Tainar Araújo.

Figure 7
Insect gall of the da Chapada Diamantina, Rio de Contas, Bahia, Brazil. (A) Fabaceae Indet.; (B-D) Byrsonima guilleminiana A. Juss.; (E) Malpighiaceae Indet.; (F) Sida cordifolia L.; (G) Leandra reversa DC.) Cogn.; (H) Miconia ibaguensis (Bonpl.) Triana; (I) Miconia sp.; (J) Miconia alborufescens Naudin; (K) Pleroma stenocarpum (Schrank et Mat. ex. DC.) Triana; (L) Tibouchina sp.; (M) Myrsinaceae Indet.; (N) Myrcia tomentosa (Aubl.) DC.; (O) Ouratea sp.; (P) Piper sp. Photos: Tainar Araújo.

Figure 8
Insect gall of the da Chapada Diamantina, Rio de Contas, Bahia, Brazil. (A-B) Piper sp.; (C) Roupala montana Aubl.; (D) Serjania glabrata Kunth.; (E) Serjania erecta Radlk.; (F) Trigonia nivea Cambess.; (G) Lantana camara L.; (H) Lippia alnifolia Mart. & Schauer; (I-J) Vochysia elliptica Mart.; (K) Drimys brasiliensis Miers. Photos: Tainar Araújo.

Table 3
Origin and endemism in Brazil of the host plants of galling insects occurring in Chapada Dimantina, Rio de Conta, Bahia State, Brazil. NE = Not Evaluated, DD = Data Deficient, LC = Least Concern, VU = Vulnerable.

The number of gall species increased with the number of plant species in the studied sites (equation: gall-inducing species = exp(1.01218+0.16583*plant richness), X 2 = 18. 170; p < 0.001; Fig. 9). A total of 48 gall morphotypes was found in the Cerrado biome on 36 plant species belonging to 24 genera and 18 families (Table 2, Fig. 10). Species of the families Fabaceae (n = 11), Melastomataceae (n = 4 species), Annonaceae (n = 3), and Asteraceae (n = 3) hosted the greatest gall richness with 19, four, four and three morphotypes, respectively. The genera with the greatest richness of gall morphotypes were Copaifera L. (Fabaceae) (n = 7), Bauhinia L. (Fabaceae) and Mimosa L. (Fabaceae) with four morphotypes each. The species with the highest richness of gall morphotypes was Copaifera depilis Dwyer (n = 4, Fig. 5G-K).

Figure 9
The relationship between richness of gall-inducing insects and plant richness (equation: gall-inducing species = exp(1.01218+0.16583*plant richness), X 2 = 18. 170; p < 0.001) for area of Caatinga and Cerrado in the municipality of Rio de Contas, extreme south of the Chapada Diamantina, Bahia, Brazil.

Figure 10
A Venn diagram representing the number of insect gall morphotypes exclusive and common to the cerrado sensu stricto (green), gallery forest (blue), shrubby caatinga (grey), rupestrian field (orange), and riparian forests (yellow), Chapada Diamantina, Bahia, Brazil.

For the Caatinga biome, 36 gall morphotypes were found on 24 plant species belonging to 20 genera and 14 families (Table 2, Fig. 10). The plant families that hosted the greatest richness of gall morphotypes were Fabaceae (n = 8 species, 14 morphotypes), Calophyllaceae (n = 1, 6), and Piperaceae (n = 1, 3). The plant genera with the highest richness of gall were Calophyllum L. (n = 6), Copaifera (n = 6), Bauhinia (n = 3), and Piper L. (n = 3). The superhost species was Calophyllum brasiliense Cambess (Fig. 4A-F) with six morphotypes.

Among the morphotypes found, four them were observed in both shrubby caatinga and cerrado s.s. (Fig. 10): the globoid leaf gall induced by Myrciaryiamia admirabilis Maia (2007) (Cecidomyiidae) on Erythroxylum suberosum A. St.-Hil. (Erythroxylaceae), the globoid leaf gall on Mimosa gemmulata Barneby (Fabaceae), the globoid leaf gall on Bauhinia pulchella Benth. (Fabaceae), and the conical leaf gall on Copaifera langsdorffii Desf. (Fabaceae).

The greatest gall richness (36 morphotypes) by life form was found in shrubs, followed by subshrubs (30 morphotypes), trees (17 morphotypes), and liana (1 morphotype), represented by 24, 24, 6 and one plant species, respectively (Table 2). The average number of gall morphotypes by plant species was 1.5 in shrubs, 1.25 in subshrubs, 2.8 in trees and 1.0 in lianas.

Galls were found on vegetative and reproductive organs: leaves (n = 58, 30 in Caatinga and 28 in Cerrado); stems (n = 23, 18 in Cerrado and 5 in Caatinga); buds (n = 2, one in Cerrado and one in Caatinga) and fruit (n = 1 in Caatinga). The most frequent shapes were globoid (n = 64, 39 in Cerrado and 25 in Caatinga); conical (n = 7, five in Caatinga and two in Cerrado), and fusiform (n = 5, three in Caatinga and two in Cerrado). Most of the galls were glabrous (n = 63, 35 in Cerrado and 28 in Caatinga), one-chambered (n = 73, 40 in Cerrado and 33 in Caatinga), and isolated (n = 66, 38 in Cerrado and 28 in Caatinga). The colors of the galls were brown, green, yellow, white, gray, black or rarely red or pink, brown being the most frequent color (n = 30, 18 in Cerrado and 12 in Caatinga). Some galls may change color during their development. The conical leaf gall on Protium heptaphyllum (Aubl.) Marchand (Burseraceae) can be black or green (Fig. 3P) and the color of the lenticular leaf gall on Copaifera sabulicola A.S. Costa & L.P. Queiroz (Fabaceae) varies from white to black (Figs. 6C-F).

The identified inducing insects belonged to the orders Diptera (Cecidomyiidae) (n = 19, eight in Caatinga and eight in Cerrado), Hemiptera (n = 2 in Cerrado), Lepidoptera (n = 1 in Cerrado), and Thysanoptera (n = 1 in Cerrado) (Table 2). The associated fauna was found in 12 morphotypes (n = 10 in Caatinga and eight in Cerrado) composed of parasitoids (Hymenoptera n = 9, five in Caatinga and four in Cerrado), inquilines (Coleoptera [n = 2, one in Cerrado and one in Caatinga], Lepidoptera [n = 3, two in Caatinga and one in Cerrado], Thysanoptera [n = 1 in Caatinga]), and successors (Formicidae n = 2 in Cerrado; Psocoptera n = 1 in Cerrado). Moreover, pseudoescorpions were observed in marginal roll galls induced on Piper sp. (Piperaceae) in Caatinga.

DISCUSSION

The Cerrado biome in the municipality of Rio de Contas showed a higher density of galls than the Caatinga of the same region, corroborating studies confirming that the Cerrado biome is the richest in terms of gall morphotypes among Brazilian biomes (Araújo, 2018; Cintra et al., 2020). To date, it is estimated that the Cerrado has approximately 968 gall morphotypes induced on 505 host plant species (Cintra et al., 2020). In contrast, Caatinga has 156 distinct morphotypes of gall and 100 host plant species (Cintra et al., 2021). The difference in the richness of gall-inducing insects between these biomes can be explained by several factors. The first factor is the difference in sampling effort, in other words, differences in sampling effort confound comparisons of species richness between local habitats or on large scales. For example, there are more than 32 inventories of galls for the Cerrado in Brazil (Cintra et al., 2020), while there are only ten one-off studies inventories for the Caatinga (Santos et al., 2011a; Carvalho-Fernandes et al., 2012; Luz et al., 2012; Costa et al., 2014a, b; Nogueira et al., 2016; Alcântara et al., 2017; Brito et al., 2018; Costa & Araújo, 2019; Santos-Silva et al., 2022). The second factor is the lower plant richness in the Caatinga; for Cintra et al. (2021), the smaller number of plant species that make up the biome may explain the lower numbers of galls. Gall-inducing insects are host-specific, and therefore one would expect a positive correlation between gall-inducing richness and plant richness (see below). The Caatinga has ca. 4,891 plant species belonging to 1,232 genera and 176 families, compared to the Cerrado, which has 12,420 plant species in 1,662 genera and 187 families. Finally, the third factor is temporal changes (seasonality). The Caatinga biome is a complex of semi-arid habitats, with low, often irregular rainfall, in which many plant species are strongly deciduous (Queiroz et al., 2017). These peculiarities of the Caatinga cause a drastic reduction in the quantity and quality of available resources for insects that induce galls preferentially on leaves (Maia et al., 2014).

Our findings indicate that there is a positive correlation between local gall-inducing insect richness and plant richness, implying that plant species can effectively predict gall-inducing species richness. Most gall-inducing insect species have a species-specific relationship with their hosts (Carneiro et al., 2009a) and, consequently, an increase in plant richness is directly related to an increase in niches available for female oviposition, and to the richness of gall-inducing insects (Strong et al., 1984; Carneiro et al., 2014). Many studies have corroborated the positive correlations of host plants richness on gall-inducing insect richness in several phytophysiognomies (Araújo, 2011; Gonçalves-Alvim & Fernandes, 2001; Oyama et al., 2003; Cuevas-Reyes et al., 2004; Carneiro et al., 2014; Coelho et al., 2017), while such a correlation was not found by others (e.g.,Fernandes & Price, 1988; Blanche, 2000; Lara et al., 2002; Araújo, 2013). The few studies that do not corroborate the positive relationships between plant species richness and gall-inducing species richness are explained by local effect of superhost taxa (see Carneiro et al., 2014).

Most of the Caatinga areas investigated are concentrated at lower altitudes ranging from 132 to 554 m, and this study is the first to be carried out in environments located above 930 m altitude (Santos et al., 2011a; Carvalho-Fernandes et al., 2012; Alcântara et al., 2017; Brito et al., 2018; Santos-Silva et al., 2022). The richness of galls in lower altitudinal strata ranged from 2 to 33 morphotypes, lower than that observed in the Caatinga areas in the present study (n = 36).

Our results do not add evidence for the altitudinal gradient hypothesis that argues that the richness of gall-inducing insects decreases with increasing altitude (Lara et al., 2002). Altitudes above 1,000 meters also do not limit the species richness of gall-inducing insects in the Cerrado biome of the Chapada Diamantina. Altitude is an important factor in the spatial distribution of insects as a whole (Freitas et al., 2007). Many of the species are widely distributed along altitudinal gradients so that their populations live at extremely low or high elevations, experiencing vastly different environmental conditions (Hodkinson, 2005). Few empirical studies have addressed how altitude impacts the species richness of gall-inducing insects on a local scale. However, prior research (Araújo & Guilherme, 2012; Coelho et al., 2017) indicates that gall-inducing insect richness was not correlated with altitude. Peaks in species richness can occur at different altitudinal points. This suggests that factors such as habitat, floristic diversity, and insect population complexity may have greater impact on gall-inducing insect richness.

In this study, the Fabaceae hosted the highest number of galls in the physiognomic forms studied in the municipality of Rio de Contas. In other regions sampled in Northeastern Brazil, this family also showed higher richness of gall-inducing insects and host plants in Caatinga habitats (Santos et al., 2011a; Carvalho-Fernandes et al., 2012), Cerrado (Silva et al., 2018; Campos et al., 2021; Santana et al., 2020). Fabaceae is among the main host families of gall inducers in Brazil together with Asteraceae (Flor et al., 2022), with a total of 438 gall morphotypes found on 178 host species, holding the largest number of host plant species (Santos-Silva & Araújo, 2020).

Among the genera of the Fabaceae, some are considered superhosts because they present a higher number of gall-inducing insects and gall morphotypes in different Brazilian biomes (Santos-Silva & Araújo, 2020); these genera includeas Copaifera, Bauhinia, and Mimosa, which hosted the highest richness of galls in the phytophysiognomies studied in Rio de Contas. These three genera combined have 25 host species in the Brazilian flora (Santos-Silva & Araújo, 2020), in which some species are reported to be superhosts of gall-inducing-insects, such as Copaifera langsdorffii Desf. (n = 28), Bauhinia brevipes Vogel (n = 17), Copaifera sabulicola J.A.S. Costa & L.P. Queiroz (n = 12) (Santos-Silva & Araújo, 2020), and Mimosa gemmulata Barneby (Costa et al., 2021).

Twelve of the host plant species studied are endemic to Brazil. The gall-inducers associated with them are proposed as co-endemic due to their high host specificity. Therefore, 22 gall-inducing species are co-endemic. Lippia alnifolia Mart. & Schauer (Verbenaceae) is endemic and vulnerable. This plant harbors a species of Cecidomyiidae, considered co-vulnerable, for the same reason. Because of poor taxonomic knowledge of gall-inducers in Brazil, none of them have been identified, which strengthens the need for conservation of the Chapada Diamantina.

Another worrisome result was the occurrence of galls on an introduced exotic plant, Mangifera indica, in riparian forest areas, which may reveal a potential conservation problem in Chapada Diamantina and a threat to the specialization of plant-gall-inducing insect networks. The presence of exotic species might reduce the interaction number for native species, which would lead to changes in the specialization of plant-gall-inducing insect networks (Araújo et al., 2017). The effects of exotic host plant species in the structure of network of gall-inducing insects associated has been poorly investigated. In the only study available on this topic, it was demonstrated that native insect herbivores were significantly more frequent on native host plant species, while exotic herbivores occurred mostly on exotic host plant species, suggesting very specific interactions even for exotic plants and insects, which results in plant-gall-inducing insect networks very specialized and similarly structured independently of exotic species presence (Araújo et al., 2017). However, this pattern should be investigated in future studies including other groups of gall-inducing arthropods and/or higher trophic levels.

Our results indicated that gall composition in Caatinga areas is clearly distinct from that in Cerrado areas, as only four gall morphotypes were shared. So, both phytogeographic domains contribute to the gall richness of the Chapada Diamantina. Although the largest number of gall morphotypes was found in shrubs and subshrubs, the highest average of gall morphotypes was reported in trees. These results favored the plant architecture hypothesis that predicts the most complex plants host the highest gall richness, since they offer the greatest number of niches for the insects (Lawton, 1983).

In this study, the galls were induced mainly on leaves, being less frequent on fruits. Only a single globoid gall was induced on the fruits of an unidentified Fabaceae species occurring in Riparian Forest (Cerrado biome). The presence of galls on reproductive structures was observed on 128 host plant species, belonging mainly to Fabaceae (78 species) (Cocoletzi et al., 2019). Galls can be induced on any vegetative structure (leaves, stems, branches and roots) or reproductive organ (flowers, fruits and seeds) (Mani, 1964). However, buds, flowers, and fruits are poorly represented as host organs, since these structures depend on the phenological stage of the plant. Gall induction on fruits should start inside the ovary where the cells are not yet differentiated, producing galls mainly without seeds, consequently the normal structure of the fruit is modified (Cocoletzi et al., 2019). Thus, the presence of galls on these organs could represent serious threats to the plants due to the impact they would have on plant performance and fitness (Fernandes, 1987).

In gall inventories for the Neotropical region, green galls are the most frequent, followed by brown. However, in the present study an inversion occurred and brown coloration was the most observed, followed by green, as was also observed in transition vegetation between caatinga and cerrado (Luz et al., 2012), caatinga (Brito et al., 2018), and cerrado s.s. (Campos et al., 2021). Galls are colorful as a result of accumulation of plant-derived pigments in their tissue and therefore can be distinguished from the surrounding host plant organs. The pigmentation is not a fixed trait and notable polymorphism can be observed (Inbar et al., 2009). Some galls may change color during their development, from lighter to darker, such as observed here and previously recorded on leaf galls induced on Lippia microphylla Cham. by Cecidomyiidae (from green to brown; Vieira et al., 2018); leaf galls on Eugenia sp. (Myrtaceae) (from yellow to reddish-yellow to black; Santana et al., 2020) and stem galls on Copaifera langsdorffii (Fabaceae; from orange to brown) (Nogueira et al., 2016). These color changes are probably associated with the developmental stages of the galls, the growth of the inducer insects and/or the action of other trophic levels (Dias et al., 2013).

The habit of inducing galls has been recorded for the orders Coleoptera, Diptera, Hemiptera, Hymenoptera, Lepidoptera and Thysanoptera (Maia, 2013). In this study, representatives of four of these orders, Diptera, Hemiptera, Lepidoptera and Thysanoptera, induced galls in the phytophysiognomies investigated. Some 49.56% of the galls waere empty and with only immature stages, which made it impossible to identify many of the inducing insects. Those that could be identified belong to the family Cecidomyiidae (Diptera). This family is responsible for inducing galls in other inventories conducted in different Brazilian ecosystems (Santos et al., 2011b; Maia & Silva, 2016; Urso-Guimarães et al., 2017; Lima & Calado, 2018; Vieira et al., 2018; Campos et al., 2021). The family Cecidomyiidae is very diverse with more than 6,500 species, most of which are gall-inducing (Gagné & Jaschhof, 2021). For Brazil, about 265 species of Cecidomyiidae are known (Maia, 2021), of which 44 species of 28 genera have been recorded in Bahia (Maia & Silva, 2020).

The gall-inducing insects are defined as guild of herbivores that to complete its life cycle necessarily develops a pathological modification in the tissue of the host plant (gall), as a result of hypertrophy and/or hyperplasia of the plant tissue, which arises from the interaction between the insect and the host plant (Weis et al., 1988). In addition to the inducing insects, other organisms can be found inside the galls that are considered as parasitoids, inquilines, cecidophages, kleptoparasites, predators, and successors. These organisms belong to the orders Coleoptera, Hymenoptera, Lepidoptera, Pseudoescorpiones, and Diptera (Maia, 2001), Hymenoptera being the most frequent parasitoids of the Brazilian flora (Maia & Azevedo, 2009). Inhabitants occurred in a single fusiform morphotype on Calophyllum brasiliense (Calophyllaceae) induced by Lepidoptera and in two globoid galls on Erythroxylum suberosum A. St.-Hil. (Erythroxylaceae) induced by Coleoptera and Lepidoptera. Hymenoptera parasitoids were also found associated with seven gall morphotypes. Successors, belonging to Psocoptera, were found in only one morphotype of gall induced on Aspidosperma tomentosum Mart. (Apocynaceae). In the literature, Psocoptera have been recorded as successors of caulinary galls on Senegalia langsdorffii (Benth.) Seigler & Ebinger and Senegalia paganuccii Seigler, Ebinger & P.G. Ribeiro in a different area of caatinga (Brito et al., 2018).

CONCLUSIONS

This study was the first to document gall and gall host richness in the Chapada Diamantina. Moreover, our results add evidences to the plant richness hypothesis, which suggests that an increase in the number plant species may be responsible for higher gall-inducing species richness at local habitats or different plant formations. The plant richness hypothesis may be the general explanation for the distribution of gall-inducing species in the Espinhaço Range, now also found in its northern portion (= Chapada Dimantina). The occurrence of endemic and/or vulnerable plants possibly supporting unique gall-inducing insects, that is, a highly correlated fauna of endemic and/or vulnerable gall-inducing insects reinforces the importance of the Chapada Diamantina for the preservation of Brazil’s biodiversity. Considering the geological, biological and ecological uniqueness of the Chapada Diamantina, as well as its extension, which reaches about 50.000 km², it is necessary to direct new efforts to document the richness of gall-inducers from other regions of the Chapada Diamantina.

ACKNOWLEDGMENTS:

We thank the Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) and CNPq for the JSS research grant (Proc. № E-26/202.501/2019, Proc. № 160015/2019-7, respectively).

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  • FUNDING INFORMATION:
    Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Proc. № 406111/2016-2) and Fundação de Amparo à Pesquisa do Estado da Bahia (FAPESB) (Proc. № 9648/2015).

Edited by

  • Edited by:
    Carlos José Einicker Lamas

Publication Dates

  • Publication in this collection
    10 June 2024
  • Date of issue
    2024

History

  • Received
    24 July 2023
  • Accepted
    19 Dec 2023
  • Published
    05 Feb 2024
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E-mail: einicker@usp.br
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