Open-access The importance of Brazilian Conservation Units for the diversity of gall-inducing insects: a study on gall-inducing insect richness in the Chapada Diamantina National Park, state of Bahia, Brazil

Abstract

Conservation Units (CUs) tend to have a high richness of herbivorous insects, including gall-inducing insects. Despite this, gall surveys carried out in these environments are punctual and some units have never had their galls investigated, such as the Chapada Diamantina National Park, Bahia (Chapada Diamantina Parna). Aiming to reduce this gap and contribute to future studies in CUs, this study aimed to survey the galls of the Chapada Diamantina Parna, Lençóis, as well as to investigate trends in research on galls in CUs in Brazil. For that, collections were carried out on monthly trips for one year. Published gall surveys were compiled. A total of 107 morphotypes induced in 88 host species were recorded. Most galls are formed in leaves, globoid in shape, green in color, and induced by Cecidomyiidae. This park has a relatively high richness of galls compared to other CUs, demonstrating its importance in the conservation of gall-inducing insects. The results also revealed that the number of surveys has been increasing over the years and that the Southeast concentrates the largest number of studies, a region that also gathers the largest number of specialists, demonstrating a geographic bias in the data.

Key words Cecidomyiidae; Fabaceae; Gall-inducing insects-host plant interaction; semiarid

INTRODUCTION

Preserved environments with high biodiversity tend to have a high richness of herbivorous insects (Root 1973, Fleck & Fonseca 2007). Among the different types of herbivory observed in these environments, the endo-phytophagous habit is considered one of the most threatened by environmental changes, including gall-inducing insects, which are considered the most sophisticated on planet Earth (Shorthouse et al. 2005), as they can induce structures called galls through disordered processes of hyperplasia and/or hypertrophy and cell differentiation in different organs of host plants (Mani 1964, Oliveira & Isaias 2010, Ferreira & Isaias 2013).

The galls provide a microenvironment for the gall-inducing and protect it against abiotic and biotic factors, allowing its success in development and energetic resources for its nutrition (Price et al. 1987, Stone & Schönrogge 2003). On the other hand, plants have their growth and reproduction phase impaired, because, as the galls grow, their nutrients are withdrawn, which can lead to the loss of their branches, fruit, and, in the most severe cases, to death (Price et al. 1987).

Studies on the richness of gall-inducing insects have demonstrated the importance of this insect guild to assess the preservation of the environment (Santos et al. 2012, Santana & Isaias 2014, Brito et al. 2018). The entomofauna associated with galls respond to environmental disturbances, such as resulting losses of species, richness, and abundance that also impact their natural enemies (Oliveira 2009). Therefore, knowledge about the richness of gall-inducing insects can help in urban planning and management (Julião et al. 2005), in environmental monitoring and conservation (Santana & Isaias 2014, Melo Jr et al. 2018), and also provide broad content for scientific dissemination by involving different scientific concepts and thus being an ally in preservation activities, through the dissemination of data through social media (Santos-Silva & Araújo 2022).

Brazilian Conservation Units (CUs) are protected natural areas that aim to maintain biological diversity in the national territory, including jurisdictional waters, the protection of rare, endemic, vulnerable, or endangered species, and the preservation and restoration of the diversity of natural ecosystems (Law 9985/2000). The number of CUs and the area they protect have been growing in recent decades in Brazil (Drummond et al. 2009). This growth is fundamental and urgent to ensure the conservation of biodiversity, especially in Brazil, which is the fifth largest country in terms of territory in the world, with 8,516,000 km2, considered to house the greatest biological diversity on the planet, with at least 46,975 native species of algae, fungi, and plants, of which 19,669 are endemic to the country (BFG 2021). Despite this, only 18% area is covered by CUs, which add up to approximately 1.6 million km2, around 2,300 CUs in Brazil. The area within the CUs is still very small in relation to the size of Brazilian biomes. The Amazon, for example, has only 27.3% territory in protected areas. Other biomes are even less protected, such as the Cerrado 9% and the Caatinga only 7.1% (WWF Unidades de Conservação no Brasil 2019).

The history of the study of galls in CUs begins with Lara & Fernandes (1996) in areas of the Serra do Cipó National Park (Minas Gerais). And subsequently, important contributions were given to the South region (e.g., Flor 2020, Mendonça Jr et al. 2010, Mendonça Jr 2011), Southeast (e.g., Fernandes et al. 2001, Carneiro et al. 2009, Maia et al. 2014, Maia & Mascarenhas 2017), Central-West (e.g., Bergamini et al. 2017, Urso-Guimarães et al. 2021), North (e.g., Almada & Fernandes 2011, Julião et al. 2014), and Northeast (e.g., Santos et al. 2011a, b, Santos et al. 2012). However, due to the size and importance of CUs in the Neotropical region, there is still much to be done, aiming to increase knowledge about the ecology and biology of the organisms involved in the gall-inducing insect-host plant interaction in CUs throughout Brazil.

The Chapada Diamantina National Park (Chapada Diamantina Parna) is an example of the few conservation areas in the state of Bahia (Harley & Simmons 1986, Giulietti et al. 1997, Silva et al. 2004) and the largest legally protected area outside the Amazon (Funch et al. 2009). Despite this, it has never been considered for a study of galls, consequently, the knowledge of the interactions established between inducers of galls and their host plants is completely unknown.

Considering that the Chapada Diamantina Parna is an area of maximum priority in the Brazilian Northeast with high biodiversity and level of endemism (Harley & Simmons 1986, Giulietti et al. 1997, Silva et al. 2004) and that no attention has been given to know its galls and host plants, this study aimed to survey and characterize the galls, providing a list of morphotypes, host plants and gall-inducing insects at the Chapada Diamantina Parna, Lençóis (Bahia), as well as to investigate trends in research on gall-inducing insects in CUs in Brazil to contribute to future biological and ecological studies in Brazilian CUs.

MATERIALS AND METHODS

Study area

The Chapada Diamantina is in the Espinhaço Mountain Range, in the state of Bahia, covering different ranges, including the Serra do Sincorá (CPRM 1994), which occupies the central part of the eastern edge of Chapada, including the Chapada Diamantina Parna (12°25’–13°20’S and 41°35’41°20’W) (Funch & Harley 2007). In the phytogeographic domain of the Caatinga, the Chapada Diamantina Parna have 1,520 km2 and is formed by a mosaic of landscapes and vegetation cover. The relief is quite uneven, with large residual massifs, rocky tops, steep slopes and deep narrow valleys, and high, narrow, and elongated mountain ranges (Misi & Silva 1994). Lençóis is one of the six municipalities that comprise Chapada Diamantina Parna (Figura 1) and has all the different vegetation types found in the limits of the park, namely: cerrado stricto sensu with discontinuous areas of arboreal elements and continuous areas dominated by herbaceous vegetation and small bushes; rupestrian field with areas comprising herbs, subshrubs, shrubs, and small trees that generally grow at altitudes above 900 m in poor soils and forest formations, ranging from submontane to montane, and from semi-deciduous to deciduous or evergreen (Franca-Rocha et al. 2004, Santos et al. 2021). The climate of the region is Tropical Semi-humid (Alvares et al. 2013), with a marked rainy season (November to March) and a strong dry season (July to November) (Funch et al. 2009). The average annual rainfall is above 1,000 mm and the average annual temperatures range between 18 and 22 ºC (Funch et al. 2009).

Sampling of galls and host plants

Galls and their host plants were collected in areas of cerrado s.s., rupestrian field, secondary montane forest, and gallery forest in the period of one year, from August 2021 to July 2022, covering the dry and rainy seasons. Monthly collections were taken in different locations (Table I), namely Bodão Waterfall, Mandassaia River, Poço Harley, Primavera Waterfall, Palmital Waterfall, Ribeirão do Meio, Sossego Waterfall, and Vale do Lapão. The altitude of each collection location and its area were obtained in the field by GPS. Each collection was carried out by two people and lasted eight hours per trip, totaling 96 hours of sampling effort.

Table I
Gall collection sites and host plants occurring in the Chapada Diamantina National Park, in the municipality of Lençóis, state of Bahia, Brazil.

All architectures of plants (herbaceous, shrubs, trees, and lianas) up to 2 meters in height were inspected. Information about the external morphology of the galls was recorded in the field, such as organ of occurrence, shape, and color. Regarding the shape of the gall, the terminology proposed by Isaias et al. (2013) was adopted. All galls were photographed in the field to help characterize the morphotypes. Samples of the collected host plants were herborized for identification based on consultation with the specialized literature that provides identification keys, consultation with specialists, and comparison with the collections of the herbarium of the Universidade do Estado da Bahia (HUNEB, Caetité collection). The APG IV classification system (2016) was followed for family circumscriptions. Information on geographic distribution and the spelling of the scientific names of host plants were checked on the Flora e Funga do Brasil website (http://floradobrasil.jbrj.gov.br).

To obtain the gall-inducing insects and associated fauna, samples of each gall morphotype collected were transported in sealed plastic bags and duly identified. In the laboratory, each gall was morphologically characterized and separated into two lots, one for dissection to describe its internal structure and obtain immature insects and the other to obtain adult insects and associated fauna. Each gall was placed separately in plastic pots, sealed, and labeled, with a piece of cotton dampened in water to maintain the humidity of the environment and inspected daily. When there was more than one gall morphotype simultaneously in the same organ (which is common in the case of leaves), morphotypes were separated so that there was no mixing of the fauna associated with different galls. The other part of the samples was dissected with the aid of a stereomicroscope to remove the larvae. At this stage, we recorded the number of internal larval chambers. All insects obtained were preserved in 70% ethanol and sent to the Diptera Laboratory of the Museu Nacional, Universidade Federal do Rio de Janeiro, to be identified.

Studies of galls in Brazilian Conservation Units

Articles on gall-inducing insect surveys in Brazilian CUs were compiled from articles indexed on the platform “Portal de Periódicos Capes” (www.periódicos.capes.gov.br) and Google Scholar (https://scholar.google.com.br) in May 2022, using the keywords “insect”, “galls” and “conservation units”, the results of the articles had their titles, abstracts and, when necessary, the full text inspected to filter only studies on gall-inducing insects in CUs in Brazil. Thus, articles were included in the compilation only when there was an explicit indication that the study was wholly or partially carried out in conservation units in Brazil.

Statistical analyses

To evaluate the association of the percentage of gall morphotypes and gall inducing orders in relation to vegetation type and host plant families, we used Pearson’s chi-square tests and Fisher’s exact test. The Yates’s correction was applied whenever necessary in chi-square analyses. In case of significant results, pairwise comparisons were performed considering the significance (p-value) with Bonferroni correction. All analyses were performed in R 4.3.0 (R Core Team 2023).

RESULTS

Survey of galls

Along the eight studied trails at the Chapada Diamantina Parna, 107 gall morphotypes were recorded in 88 species, belonging to 77 genera and 38 botanical families (Table II, Figures 2-7). Of the total number of morphotypes, most were found in cerrado s.s. vegetation (n=71; 67%) followed by areas of montane forest (n=24; 22%), gallery forest (n=7; 7%), and rupestrian fields (n= 5; 4%).

Table III
Surveys of galls and their host plants in Conservation Units in Brazil.

Most galls were induced in species of the families Myrtaceae (n=10) and Fabaceae (n=8), followed by Melastomataceae (n=7) and Malpighiaceae (n=7). The genera with the highest gall richness were Eugenia L. (Myrtaceae) (n=5), Copaifera L. (Fabaceae) (n=4), and Byrsonima Rich. ex Kunth (Malpighiaceae) (n=4). All morphotypes found in the Chapada Diamantina Parna are new records for the park. Galls were also recorded for the first time in Brazil on Paralychnphora bicolor (DC.) MacLeish (Asteraceae) (Figure 2j), Handroanthus chrysotrichus (Mart. ex DC.) Mattos (Bignoniaceae) (Figure 2n), Periandra coccinea (Schard.) Benth. (Fabaceae) (Figure 4b), Senna multijuga (Rich.) H.S. Irwin & Barneby (Fabaceae) (Figure 4c), Luehea candicans Mart. (Malvaceae) (Figure 4r), and Marcetia bahiensis (Brade & Markgraf) Wurdack. (Melastomataceae) (Figure 5a). Eight are endemic to Brazil: Marcetia bahiensis, Paralychnphora bicolor, Periandra coccinea, Copaifera duckei Dwyer (Fabaceae), Copaifera luetzelburgii Harms (Fabaceae), Eugenia catharinae O. Berg (Myrtaceae), Manihot tripartite (Spreng) Müll. Arg., (Euphorbiaceae), and Qualea cryptantha (Spreng.) Warm. (Volchysiaceae).

Figure 1
Geographic Location of the Chapada Diamantina National Park, Lençóis, state of Bahia, Brazil.
Figure 2
Entomogenous galls at the Chapada Diamantina National Park, Lençóis, state of Bahia, Brazil. a-b. Astronium fraxinifolium Schott ex Spreng; c. Anacardium sp.; d. Anacardiaceae Indet. e. Duguetia flagellaris Huber; f. Annona sp.; g. Thaumatophyllum sp.; h. Baccharis minutiflora Mart. ex Baker; i. Moquiniastrum paniculatum (Less) G. Sancho; j. Paralychnophora bicolor (DC.) MacLeish; k-l. Asteraceae Indet. 1. m. Asteraceae Indet. 2. n. Handroanthus chrysotrichus (Mart. Ex DC.) Mattos; o-p. Bignoniaceae Indet. 1; q. Bignoniaceae Indet. 2; r. Bignoniaceae Indet. 3; s. Boragnaceae Indet.; t. Protium heptaphyllum (Aulb.) Marchand. Photos: Gabriela Bomfim.

The vast majority of galls were induced on leaves (n=76%), preferentially on the adaxial face (n=58%) followed by the stem (n=20%) and more rarely in buds (n=2%) (Figure 4t), flowers (n=1%) (Figure 4b) and fruit (n=1%) (Figure 2a). All morphotypes occurred in a single plant organ, with only one exception, the globoid galls induced in an unidentified species of Boraginaceae (Figure 5s), observed both on the stem and on the leaves in cerrado s.s. areas.

Galls occurred in plants with different habits: shrubs (n=51%), trees (n=29%), subshrub (n=13%), herbs (n=5%), and lianas (n=2%). They are grouped into six different shapes: globoid (n=44%), lenticular (n=19%), fusiform (n=18%), conical (n=3%), leaf fold (n=2%), and marginal Roll (n=1%). There was also a record of amorphous galls in 13% morphotypes (n=15). Most occurred in groups (n=69%) and had only one larval chamber (n=84%). Among the analyzed morphotypes, 78% did not present trichomes, that is, they were glabrous (Table I).

Concerning color, green (n=41%) (Figure 3i), brown (n=32%) (Figure 3s), white (n=8%) (Figure 4r), yellow (n=7%) (Figure 5j), or, more rarely, purple (n=5%) (Figure 5r), red (n=4%) (Figure 5q), black (n=2%) (Figure 2n), and orange (n =1%) galls were found (Figure 2a). Stem galls induced in an unidentified Fabaceae species (Figure 4d) varied in color, from yellowish at the beginning of their developmental stage to brown when senescent.

Figure 3
Entomogenous galls at the Chapada Diamantina National Park, Lençóis, state of Bahia, Brazil. a-b. Protium heptaphyllum (Aulb.) Marchand; c. Calophyllum brasiliense Cambess.; d. Calophyllum sp. e. Clusiaceae Indet.; f. Combretum Glaucocarpum Mart.; g. Terminalia sp.; h. Parinari obtusifolia Hook. f.; i. Diospyros sp.; j. Manihot tripartite (Spreng) Müll. Arg.; k-l. Croton sp.; m-n. Euphorbiaceae indet.; o. Erythroxylum suberosum A. St. – Hil.; p. Erythroxylum sp.; q. Calliandra dysantha Benth.; r. Copaifera duckei Dwyer; s-t. Copaifera langsdorffii Desf. Photos: Gabriela Bomfim.
Figure 4
Entomogenous galls at the Chapada Diamantina National Park, Lençóis, state of Bahia, Brazil. a. Copaifera luetzelburgii Harms; b. Periandra coccinea (Schard.) Benth.; c. Senna multijuga (Rich.) H.S. Irwin & Barneby; d. Fabaceae Indet.; e. Lauraceae Indet. 2.; f. Lauraceae Indet. 2; g. Lauraceae Indet. 3; h-i. Struthanthus sp.; j. Lythraceae Indet.; k-m. Byrsonima gardneriana A. Juss.; n. Byrsonima guilleminiana A. Juss.; o. Malpighiaceae Indet. 1; p. Malpighiaceae Indet. 2; q. Malpighiaceae Indet. 3; r. Luehea candicans Mart.; s. Helicteres sp.; t. Macairea radula (Bonpl.) DC. Photos: Gabriela Bomfim.
Figure 5
Entomogenous galls at the Chapada Diamantina National Park, Lençóis, state of Bahia, Brazil. a. Marcetia bahiensis (Brade & Markgraf) Wurdack.; b. Miconia albicans (SW.) Triana; c. Miconia alborufescens Naudin; d. Miconia sp. e. Leandra sp.; f. Tibouchina sp.; g. Trichilia catigua A. Juss.; h-i. Guarea sp.; j. Meliaceae Indet.; k-l. Eugenia catharinae O. Berg; m- Campomanesia sp. n-p. Eugenia sp.; q. Myrcia neoobscura E.Lucas & C.E.Wilson; r. Myrtaceae Indet. 1; s. Myrtaceae Indet. 2; t. Myrtaceae Indet. 3. Photos: Gabriela Bomfim.
Figure 6
Entomogenous galls at the Chapada Diamantina National Park, Lençóis, state of Bahia, Brazil. a. Nyctaginaceae Indet.; b. Ouratea nana (A. St. Hil.) Engl. c. Ouratea sp.; d. Passiflora sp.; e. Pogonophora schomburgkiana Miers ex Benth.; f. Phyllanthaceae Indet.; g. Piper arboretum Aubl.; h. Proteaceae Indet.; i-j. Randia armata var. pubescens (K. Schum.) Standl.; k. Psychotria sp.; l. Rubiaceae Indet. 1; m. Rubiaceae Indet. 2; n. Allophylus racemosus Sw.; o. Serjania glabrata Kunth. p-q. Sapindaceae Indet.; r. Pouteria torta (Mart.) Radlk.; s. Siparuna guianensis Aubl; t. Smilax sp. Photos: Gabriela Bomfim.

Of the 107 gall morphotypes recorded here, the gall-inducing insects of only 22 were identified (14 at the family level and only four at the species level, Lopesia linearis Maia, 2003, Lopesia similis Maia, 2004, Myrciaryiamia admirabilis Maia, 2007, and Schismatodiplosis lantanae Rübsaamen, 1916 (Diptera, Cecidomyiidae). Among the gall-inducing insects not identified at the species level are representatives of the order Diptera (Cecidomyiidae) (n=13), Hymenoptera (n=3), Coleoptera (n=1), and Lepidoptera (n=1) (Table II). Regarding the associated fauna, parasitoids Hymenoptera (n=15), inquilines, Thysanoptera (n=3), Lepidoptera (n=2), and Coleoptera (n=1), and successors, Formicidae (n=3), Psocoptera (n=1), and mites (n=1) were recorded (Table II).

The results indicated that the percentage of gall inducing orders were not associated to vegetation type (χ2 = 14.7, df = 9, p = 0.098) and host plant family (Fisher’s exact test: p = 0.367). However, the percentage of gall morphotypes were associated to vegetation (χ2 = 90.9, df = 3, p < 0.001), indicating that cerrado and montane forest harboured more gall species compared to other phytophysiognomies (p < 0.004 in all cases) (Figure 8a). Host plant species was also associated to the percentage of gall species (χ2 = 63.0, df = 37, p = 0.005), but pairwise comparisons were not significant in any case (Figure 8b).

Figure 7
Entomogenous galls at the Chapada Diamantina National Park, Lençóis, state of Bahia, Brazil. a-b. Lantana camara L; c. Qualea cryptantha (Spreng.) Warm. d. Qualea parviflora Mart.; e-f. Drimys brasiliensis Miers. Photos: Gabriela Bomfim.
Figure 8
Bar charts indicating chi-square significant results for the association between percentage of gall morphotypes and (a) vegetation type and (b) host plant family. For vegetation type, pairwise comparisons indicated that cerrado had more gall species than other phytophysiognomies, and montane forest in relation to gallery forest and rupestrian field. No significant results were found in pairwise comparisons among host plant families.
Figure 9
Number of inventories of insect galls carried out in conservation units in Brazil: (a) number of publications for Brazilian regions; and (b) number of publications for Brazilian states.
Figure 10
Geographic distribution of insect gall inventories carried out in conservation units in Brazil.

Studies of galls in Brazilian Conservation Units

A total of 46 gall surveys carried out in Brazilian CUs were published from 1996 to 2022 (Table III, Figures 9-10). The number of publications found has increased over the years, especially in the last decade. The vast majority of gall surveys were carried out in the Southeast region of Brazil (n=27 studies) (Table III). The Central-West, North, South, and Northeast regions were less studied, with four, four, six and six studies, respectively (Figures 8-9). Among the Brazilian states, Minas Gerais led in the number of papers (n=13), followed by Rio de Janeiro (n=10) and Pernambuco (n=4) (Table III).

DISCUSSION

Approximately 27 years ago, Brazilian researchers began studying galls in CUs in Brazil, the first work was carried out by Lara & Fernandes (1996) in the Serra do Cipó National Park in Minas Gerais, but the host plants were not scientifically identified. Since then, the number of gall surveys in CUs has been increasing in different regions of Brazil, with the majority carried out in the Southeast region. The present study documents an increasing trend in the scientific production on gall-inducing insects in CUs, but it reflects a geographic bias: the researchers involved are concentrated in the southeastern region of Brazil, mainly in the states of Minas Gerais and Rio de Janeiro.

Of the 26 Brazilian states, there are surveys of galls in 12 of them, with the states of Minas Gerais and Rio de Janeiro with the highest number. Only one published study was conducted in a CU in the state of Bahia, our study is the second; this can be because surveys of galls in this state are recent and still punctual (Costa et al. 2014a, b, Nogueira et al. 2016, Brito et al. 2018, Lima & Calado et al. 2018, Vieira et al. 2018, Santana et al. 2020, Campos et al. 2021, Santos-Silva et al. 2022, Melo & Santos-Silva 2023), which reinforces the need for greater collection effort, especially in neglected CUs to minimize sampling bias and provide a better knowledge base of the richness of gall-inducing insects and their host plants for the conservation of these organisms.

In the present study, the number of morphotypes found, 107 galls induced in 88 host plant species, is considered relatively high compared to other surveys carried out in CUs in Brazil (Table III). For example, in Serra Verde State Park (MG), 75 gall morphotypes were recorded in 43 plant species during twelve monthly collections in the Cerrado (Santana & Isaias et al. 2014), while in Praia do Sul State Biological Reserve (RJ), 36 morphotypes were observed in 22 host species that grow in restinga areas surveyed in two monthly collections (Maia & Oliveira 2010), and at the Serra dos Pireneus State Park (GO), 21 different types of galls were surveyed in 21 species of host plants in different Cerrado phytophysiognomies during twelve collections in quarterly trips (Araújo et al. 2007). Even considering differences in sampling effort, the richness of host plants, and other variables, our data reveal the potential of the Chapada Diamantina Parna for the conservation of gall-inducing insects and their host plants. In addition, the record of six new morphotypes in six different plant species for Brazil further reinforces the importance of this unit for the conservation of gall-inducing insects and corroborates studies that predict that the richness of gall-inducing insects is high and poorly studied in CUs in Brazil (Santana & Isaias 2014).

At the Chapada Diamantina Parna, the phytophysiognomy of the cerrado s.s. gathers most of the galls (n=67%), compared to the other investigated phytophysiognomies, corroborating other studies that indicate that the Cerrado biome and its phytophysiognomies have the richest fauna of gall-inducing insects in Brazil (Araújo 2018, Cintra et al. 2020, Campos et al 2021). This biome is confirmed as home to the richest savanna flora in the world (Forzza et al. 2012) and hosts a greater number of galls, with a record of approximately 968 interactions between gall-inducing insects in 505 host plants (Cintra et al. 2020).

At the Chapada Diamantina Parna, family Myrtaceae together with Fabaceae hosted the highest number of galls, which reflects the diversity of these plant families in the local flora. Santos et al. (2021) recorded 82 species and 9 genera of Myrtaceae in the limits of the Chapada Diamantina Parna and its surroundings, especially in the municipality of Lençóis. A similar result is observed for the Fabaceae family, which leads in different floristic surveys and phytophysiognomies at the Chapada Diamantina Parna as well as in the seasonal forest (Couto et al. 2011), in the cerrado (Grillo 2008), and in the gallery forest (Ribeiro-Filho et al. 2009). The main reason for the great importance these families as a super-host of galls is the relatively large number of Brazilian species. According to the plant taxon size hypothesis, species-rich families tend to host a higher richness of gall-inducing insects (Fleck & Fonseca 2007).

The genera Eugenia, Copaifera, and Byrsonima had the highest gall richness in the studied phytophysiognomies of the Chapada Diamantina Parna, here considered super-hosts, as has already been registered for cerrado and rupestrian field environments in Bahia (Costa et al. 2014a, Nogueira et al. 2016, Campos et al. 2021, Vieira et al. 2018), and the caatinga-cerrado transition in northern Minas Gerais (Luz et al. 2012). These same genera were observed to be richer in species at the Chapada Diamantina Parna, Eugenia (Santos et al. 2021), Copaifera, and Byrsonima (Couto et al. 2011), which corroborates the hypothesis of floristic diversity, taxa with greater richness are also the most abundant in the occurrence of galls (Fernandes & Price 1988, Veldtman & Mcgeoch 2003, Espírito-Santo & Fernandes 2007).

Most galls were found on shrubs (n=51%) and trees (n=29%), and were significantly rare on herbs (n=5%), and lianas (n=2%). This is a common pattern in different surveys carried out in Brazil (Cuevas-Reyes et al. 2004, Araújo et al. 2006, Espírito-Santo & Fernandes 2007, Gonçalves-Alvim & Fernandes 2001, Lara et al. 2002). This can be explained by the plant architecture hypothesis that the greater the architectural complexity of the plant, the greater the richness and abundance of associated herbivore insects (Lawton & Schröder 1977, Lawton 1983).

Almost all galls occurred in only one plant organ, with a single exception of the induced gall on an unidentified species of the Bignoniaceae family, whose galls occur on both stems and leaves, confirming the specificity of the gall-inducing insect for the host plant organ (Dreger-Jauffret & Shorthouse 1992). The highest number of induced galls on leaves (n=76%) followed by stems (n=20%), as observed in this study, is similar to the patterns recorded for Brazil (e.g., Fernandes & Negreiros 2006, Santos et al. 2011a, b, 2012, Toma & Mendonça Jr 2013, Santana & Isaias 2014, Nogueira et al. 2016, Silva et al. 2018), including its different conservation units (e.g., Gonçalves-Alvim & Fernandes 2001, Araújo et al. 2007, Bregonci et al. 2010, Santana & Isaias 2014). This is because leaves are considered more plastic host organs compared to stems (Isaias et al. 2013). Moreover, they are generally the most available and abundant plant organs, being easily observed, in contrast to the others (Santana & Isaias 2014). Leaves also have higher levels of nutritional reserves due to their photosynthetic capacity (Castro et al. 2012). Considering the occurrence of galls on available leaf surfaces, 42% registered morphotypes were induced on the abaxial face. Edward & Wratten (1998) point out that the abaxial face offers less stressful microclimatic conditions than the adaxial surface.

The induction of galls on buds, fruits, and flowers is less frequent in surveys throughout Brazil. At the Chapada Diamantina Parna, it is not different, only two globoid galls were induced in buds of Macairea radula (Bonpl.) DC. (Melastomataceae) and an unidentified species of the Euphorbiaceae family, both occurring in the cerrado s.s. Galls on buds were also recorded by Maia & Oliveira (2010) in Praia do Sul State Biological Reserve in Erythroxylum ovalifolium Peyr. (Erythroxylaceae), Dalechampia leandrii Baill. (Euphorbiaceae), Myrciaria jaboticaba (Vell.) O. Berg (Myrtaceae), and Psidium cattleianum Sabine (Myrtaceae). In the reproductive structures, a fusiform gall was found in the fruit of Astronium fraxinifolium Schott ex Spreng (Anacardiaceae). In Brazil, there is a record of galls on the fruit of Fridericia conjugata (Vell.) Mart. (Bignoniaceae) (Maia & Silva 2016) and Davilla rugosa Poir. (Dilleniaceae) (Vieira et al. 2018) in Atlantic Forest and Cerrado environments, respectively, for example. Fruits affected by gall-inducing insects may or may not present externally evident deformation, and the galls consist of sets of larval chambers surrounded by lignified tissue that may or may not be fused and/or to seeds. Due to the rigidity of the mature gall and the “cluster of chambers” aspect, it is not possible to define the exact shape or size. This can lead to the misinterpretation that they are just seeds that are all fused (Wikler 1999, 2000).

The predominance of globoid galls resembles the pattern observed in the Neotropical region (Isaias et al. 2013), where it was recorded in caatinga (Santos et al. 2011a, b, Carvalho-Fernandes et al. 2012), cerrado s.s. (Nogueira et al. al. 2016, Lima & Calado 2018, Vieira et al. 2018) environments, and in the Atlantic Forest (Carvalho-Fernandes et al. 2009, Alcântara et al. 2017). In conversation units, this same pattern is observed (Araújo et al. 2007, Bregonci et al. 2010, Santana & Isaias 2014).

Most of the recorded galls are green in color, indicating the presence of chlorophyll and the existence of photosynthetic processes, which can be an advantage for host plants, as they increase photosynthetic capacity due to hyperplasia and hypertrophy of plant cells (Magalhães 2010). Green galls can be good models for studying photosynthesis and cytological responses to galling stress, as investigated by Oliveira et al. (2011). Some studies in tropical areas have shown that photosynthesis in galls is not enough to maintain their structure and they are used as accessories to the host plant machinery (Oliveira et al. 2011, Castro et al. 2012). Change in gall color was verified in induced stem gall in an unidentified species of the family Fabaceae. Although these changes are not well understood, they are probably associated with the growth of gall-inducing insects, the development phase of the gall, or even the action of other trophic levels (Dias et al. 2013, Santana & Isaias 2014).

Many gall surveys carried out in Brazil show isolated galls and galls with a single larval chamber as predominant (e.g., Carvalho-Fernandes et al. 2012, Maia & Silva 2016, Alcântara et al. 2017, Vieira et al. 2018, Campos et al. 2021, Urso-Guimarães et al. 2021). Nevertheless, the present study observed a greater number of grouped galls. The distribution of isolated or grouped galls reflects the oviposition pattern of females of each species (Gagné 1994). According to Urso-Guimarães & Scareli-Santos (2006), the occurrence in clusters may be important for the protection of galls by diluting the effects of natural enemies, but further studies are required to prove or disprove these observations.

Glabrous galls, that is, without trichomes, are commonly observed in several surveys carried out in Brazil (Araújo et al. 2007, Costa et al. 2014b, Santana & Isaias 2014, Santana et al. 2020) being frequent in the Brazilian semi-arid region (Nogueira et al. 2016, Vieira et al. 2018, Campos et al. 2021). Trichomes, when present on galls, can provide an adequate microclimate for insect development (Westphal 1992, Boczek & Griffiths 1994), protecting it against high temperatures and water stress.

Gall-inducing insects belong to the orders Coleoptera, Diptera, Hemiptera, Hymenoptera, Lepidoptera, and Thysanoptera (Maia 2013). Four orders of gall-inducing insects were identified in the phytophysiognomies investigated here, Coleoptera, Diptera, Hymenoptera, and Lepidoptera. Cecidomyiidae (Diptera) were the main inducers of galls, as expected. This family stands out as the group with the highest number of gall-inducing insects in the entire Neotropical region (e.g., Carneiro et al. 2009, Santos et al. 2011a, 2012, Maia 2013, Costa et al. 2014b, Nogueira et al. 2016, Gagné & Jaschhof 2017, Silva et al. 2018, Santana et al. 2020, Santos-Silva & Araújo 2020, Campos et al. 2021) and also in conservation units (Maia & Oliveira 2010, Santana & Isaias 2014, Bregonci et al. 2010).

Of the 107 gall morphotypes registered in the present study, inducing insects were identified in only 19, no galls were induced by Hemiptera and Thysanoptera were registered, even though these have been registered in other CUs, such as the Serra Verde State Park (Santana & Isaias 2014) and in the Praia do Sul State Biological Reserve (Maia & Oliveira 2010). This may be related to the difficulty in obtaining specimens of gall-inducing insects (including immatures and adults of both sexes, necessary for species determination), the prevalence of galls that have already been abandoned by their inducer, the lack of knowledge of the biology of inducers; and the lack of taxonomists for known gall-inducing insect groups (Espírito-Santo & Fernandes 2007, Carneiro et al. 2009, Melo Jr 2018). Thus, gall-inducing insects are taxonomically little known, especially in the Neotropics, where most species are new to science (Santana & Isaias 2014). Despite efforts to survey galls in several Brazilian ecosystems, the lack of determination of gall-inducing species is the main gap to be filled, since many studies describe the gall without identifying the gall-inducing agent (Melo Jr et al. 2018).

As indicated in the studies by Maia (2001), other organisms besides the inducers can be found inside the galls, acting as tenants, predators, successors, and parasitoids, these are part of the associated fauna. The gall-associated arthropod fauna at the Chapada Diamantina Parna included Hymenoptera (parasitoids), Coleoptera, Lepidoptera, Thysanoptera, Diptera (cecidophages), Psocoptera, mites and Formicidae (successors). Hymenoptera were identified as the most frequent natural enemies of gall-inducing insects, commonly acting as parasitoids, their habits were verified in the present study, corroborating other surveys throughout Brazil (Maia 2001, Maia & Fernandes 2004). The community of parasitoids (Hymenoptera) associated with host plants in conservation units have been widely reported in other surveys (Bregonci et al. 2010, Maia & Oliveira 2010, Santana & Isaias 2014). Predatory ants (Hymenoptera: Formicidae) were also found at the Chapada Diamantina Parna associated with three morphotypes of galls. Representatives of Formicidae were also recorded in Serra Geral in Caetité (BA) (Nogueira et al. 2016) and at the Paulo Cesar Vinha State Park (ES) (Bregonci et al. 2010).

As for the successors, mites and Psocoptera, they were less frequent occurring in only one gall morphotype induced in Byrsonima gardneriana A. Juss. (Malpighiaceae) and Copaifera langsdorffii Desf. (Fabaceae), respectively. In the literature, there are records of representatives of these organisms as successors of galls at the Paulo Cesar Vinha State Park (Bregonci et al. 2010), in species of Guapira pernambucensis (Casar.) Lundell (Nyctaginaceae) and Chaetocarpus myrsinites Baill. (Peraceae), for example.

The present study documents the increase in gall-inducing insect surveys in Brazilian CUs, with most surveys carried out in the Southeast region, which concentrates the largest number of specialists, demonstrating a geographic bias in the data. This spatial bias associated with the significant number of galls and host plants in the CUs reinforces that there is still much to be done in relation to the study of galls and their host plants in Brazilian CUs. At the Chapada Diamantina Parna, there is a high richness of galls compared to other surveys carried out, with some morphotypes and host species recorded for the first time for Brazil, which evidences the importance of this CU in the conservation of galling insects. Our results also corroborate studies that indicate leaves as the main host organs, the predominance of globoid galls, and the Cecidomyiidae as the main gall inducers.

ACKNOWLEDGMENTS

We thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq (Process Number 406111/2016-2) and Fundação de Amparo à Pesquisa do Estado da Bahia - FAPESB (Process Number 9648/2015) for financial support to this project; to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - CAPES for the scholarship awarded to the first author; to UNEB for financial and institutional support; to Henrique Venâncio for collaborating with statistical analysis; to Ítalo Sá, guide of the Chapada Diamantina Parna, for helping with collections; Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) and CNPq for the JSS research grant (Process Number E-26/202.501/2019, Process Number 160015/2019-7, respectively).

SUPPLEMENTARY MATERIAL

Table SI.

REFERENCES

  • ALCÂNTARA JA, SOUZA EB & BRAGA PET. 2017. Ocorrência e caracterização de galhas em duas áreas do noroeste do Ceará, Brasil. Natureza online 15: 33-40.
  • ALMADA ED & FERNANDES GW. 2011. Insetos indutores de galhas em florestas de terra-firme em reflorestamentos com espécies nativas na Amazônia Oriental. Bol Mus Para Emilio Goeldi Ser Cienc Nat 6: 1-10.
  • ALVARES CA, STAPE JL, SENTELHAS PC, GONÇALVES JL & SPAROVEK G. 2013. Köppen’s climate classification map for Brazil. Meteorol Zeitschrift 22: 711-728.
  • APG IV. 2016. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot J Linn Soc 181: 1-20.
  • ARAÚJO APA, PAULA JD, CARNEIRO MAA & SCHOEREDER JH. 2006. Effects of host plant architecture on colonization by galling insects. Austral Ecol 31: 343-348.
  • ARAÚJO WS. 2018. 30 years of research on insect galls in Brazil: a scientometric review. Pap Avulsos Zool 58: e20185834.
  • ARAÚJO WS, GOMES-KLEIN VL & SANTOS BB. 2007. Galhas Entomógenas Associadas à Vegetação do Parque Estadual da Serra dos Pireneus, Pirenópolis, Goiás, Brasil. Rev Bras Biocienc 5(Supl. 1): 45-47.
  • ARAÚJO WS, PORFÍRIO JR ED, JORGE VA & ESPÍRITO-SANTO FILHO K. 2012. Plantas hospedeiras e galhas entomógenas em sub-bosques de florestas tropicais do Pará, Brasil. Insula 41: 59-72.
  • ARAÚJO WS, SANTOS BB & GOMES-KLEIN VL. 2011. Insect galls from Serra dos Pireneus, GO, Brazil. Biota Neotrop 11(2): 357-365.
  • ARAÚJO WS, SOBRAL FL & MARACAHIPES L. 2014. Insect galls of the Parque Nacional das Emas (Mineiros, GO, Brazil). Check List 10: 1445-1451.
  • ARRIOLA IA & MELO JR JCF. 2016. Richness of insect galls on shrub-tree restinga of a coastal plain of southern Brazil. Acta Biol Catarin 3: 121-37.
  • ARRIOLA IA, MELO JR JCF & ISAIAS RM. 2015. Questioning the environmental stress hypothesis for gall diversity of restinga vegetation on dunes. Rev Biol Trop 63: 959-970.
  • BERGAMINI BAR, BERGAMINI LL, SANTOS BB & ARAÚJO WS. 2017. Occurrence and characterization of insect galls in the Floresta Nacional de Silvânia, Brazil. Pap Avul Zool 57: 413-431.
  • BFG - THE BRAZIL FLORA GROUP. 2021. Brazilian Flora 2020: Leveraging the power of a collaborative scientific network. Taxon 71: 178-198.
  • BOCZEK JD & GRIFFITHS D. 1994. Structure and systematics of eriophyid mites (Acari: Eriophyoidea) and their relationship to host plants. In: WILLIAMS MAJ (Ed) Plant galls: organisms, interactions, populations. New York: Clarendon Press, p. 119-129.
  • BREGONCI JDM, POLYCARPO PV & MAIA VC. 2010. Galhas de insetos do Parque Estadual Paulo César Vinha (Guarapari, ES, Brasil). Biota Neotrop 10: 265-274.
  • BRITO GP, COSTA EC, CARVALHO-FERNANDES SP & SANTOS-SILVA J. 2018. Riqueza de galhas de insetos em sítios de Caatinga com diferentes graus de impacto antropogênico, Bahia, Brasil. Iheringia Ser Zool 108: 1-9.
  • CAMPOS GBD, COSTA EC, SANTOS DLS, CARVALHO-FERNANDES SP & SANTOS-SILVA J. 2021. Insect galls and associated fauna in two areas of Cerrado sensu stricto in the State of Bahia, Brazil. An Acad Bras Cienc 93: e20201442.
  • CARNEIRO MAA, BORGES RAX, ARAÚJO APA & FERNANDES GW. 2009. Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, Minas Gerais, Brasil. Rev Bras Entomol 53: 570-592.
  • CARVALHO-FERNANDES SP, ALMEIDA-CORTEZ JS & FERREIRA ALN. 2012. Riqueza de galhas entomógenas em áreas antropizadas e preservadas de Caatinga. Rev Árvore 32: 269-277.
  • CARVALHO-FERNANDES SP, ASCENDINO S, MAIA VC & COURI MS. 2016. Diversity of insect galls associated with coastal shrub vegetation in Rio de Janeiro, Brazil. An Acad Bras Cienc 88: 1407-1418.
  • CARVALHO-FERNANDES SP, CASTELO-BRANCO BP, ALBUQUERQUE FA, FERREIRA A LN, BRITO-RAMOS AB, BRAGA DVV & ALMEIDACORTEZ JS. 2009. Galhas entomógenas em um fragmento urbano de Mata Atlântica no centro de endemismo de Pernambuco. Rev Bras Biocienc 7: 240-244.
  • CASTRO AC, OLIVEIRA DC, MOREIRA ASFP, LEMOS-FILHO JP & ISAIAS RMS. 2012. Source-sink relationship and photosynthesis in the horn-shaped gall and its host plant Copaifera lagsdorffii Desf. (Fabaceae). S Afr J Bot 83: 121-126.
  • CINTRA FC, ARAÚJO WS, MAIA VC, URSO-GUIMARÃES MV, VENÂNCIO H, ANDRADE JF & SANTOS JC. 2020. Plant-galling insect interactions: a data set of host plants and their gall-inducing insects for the Cerrado. Ecology 101: e03149.
  • COELHO MS, ALMADA ED, FERNANDES GW, CARNEIRO MAA, SANTOS RM, QUINTINO AV & SANCHEZ-AZOFEIFA A. 2009. Gall inducing arthropods from a seasonally dry tropical Forest in Serra do Cipó, Brazil. Rev Bras Entomol 53: 404-414.
  • COELHO MS, CARNEIRO MAA, BRANCO C, BORGES RAX & FERNANDES GW. 2013. Gall-inducing insects from Campos de Altitude, Brazil, Biota Neotrop 13: 139-151.
  • COSTA EC, CARVALHO-FERNANDES SP & SANTO-SILVA J. 2014a. Galhas entomógenas associadas à Leguminosae do entorno do riacho Jatobá, Caetité, Bahia, Brasil. Rev Bras Biocienc 12: 115-120.
  • COSTA EC, CARVALHO-FERNANDES SP & SANTOS-SILVA J. 2014b. Galhas de insetos em uma área de transição caatinga-Cerrado no nordeste do Brasil. Sitientibus Sér Ciên Biol 14: 1-9.
  • COUTO APLD, FUNCH LS & CONCEIÇÃO AA. 2011. Composição florística e fisionomia de floresta estacional semidecídua submontana na Chapada Diamantina, Bahia, Brasil. Rodriguésia 62: 391-405.
  • CPRM - COMPANHIA DE PESQUISA DE RECURSOS MINERAIS. 1994. Parque Nacional da Chapada Diamantina - BA. Informações básicas para a gestão territorial: diagnóstico do meio físico e da vegetação. CPRM; IBAMA, Salvador.
  • CUEVAS-REYES P, QUESADA M, HANSON P, DIRZO R & OYAMA K. 2004. Diversity of gall-inducing insects in a Mexican tropical dry forest: the importance of plant species richness, life-forms, host plant age and plant density. J Ecol 92: 707-716.
  • DIAS GG, MOREIRA GRP, FERREIRA BG & ISAIAS RMS. 2013. Why do the galls induced by Calophya duvauae Scott on Schinus polygamus (Cav.) Cabrera (Anacardiaceae) change colors? Biochem Syst Ecol 48: 111-122.
  • DREGER-JAUFFRET F & SHORTHOUSE JDP. 1992. Diversity of gall-inducing insects and their galls. In: Shorthouse JD & Rohfritsch O (Eds), Biology of Insect-Induced Galls. Oxford University Press, Oxford, 8-33.
  • DRUMMOND JA, FRANCO JLA & OLIVEIRA D. 2009. O mapa das UCs será o mapa da inclusão social? Nat Conserv 7: 8-16.
  • EDWARD PJ & WRATTEN SD. 1998. Ecology of insect-plant interactions. Southampton, The Camelot Press, 60 p.
  • ESPÍRITO-SANTO MM & FERNANDES GW. 2007. How many species of gall-inducing insects are there on earth, and where are there? Ann Entomol Soc Am 100(2): 95-99.
  • FERNANDES GW, JULIÃO GR, ARAÚJO, RC, ARAÚJO SC, LOMBARDI JA, NEGREIROS D & CARNEIRO MAA. 2001. Distribution and morphology of insect galls of the Rio Doce Valley, Brazil. Naturalia 26: 211-244.
  • FERNANDES GW & NEGREIROS DA. 2006. comunidade de insetos galhadores da RPPN Fazenda Bulcão, Aimorés, Minas Gerais, Brasil. Lundiana 7: 111-120.
  • FERNANDES GW & PRICE PW. 1988. Biogeographical gradients in galling species richness: tests of hypotheses. Oecologia 76: 161-167.
  • FERREIRA BG & ISAIAS RMS. 2013. Developmental stem anatomy and tissue redifferentiation induced by a galling Lepidoptera on Marcetia taxifolia (Melastomataceae). Botany 91: 752-760.
  • FLECK T & FONSECA CR. 2007. Hipóteses sobre a riqueza de insetos galhadores: uma revisão considerando os níveis intra-específico, interespecífico e de comunidade. Neotropical Biol Conserv 2: 36-45.
  • FORZZA RC ET AL. 2012. New Brazilian Floristic List Highlights Conservation Challenges. BioScience 62: 39-45.
  • FLOR IC. 2020. Galhas entomógenas em três fragmentos de Mata Atlântica no extremo Sul Catarinense, Brasil. Entomol Commun 2: ec02017.
  • FRANCA-ROCHA WJSF, CHAVES JM, ROCHA CC & LOBÃO JSB. 2004. Unidades de Paisagem: delimitação e caracterização. In: JUNCÁ F, FUNCH LS & FRANCA-ROCHA WJS (Orgs). Biodiversidade e Conservação da Chapada Diamantina, PROBIO/MMA. Brasília: Ministério do Meio Ambiente, p. 31-45.
  • FUNCH RR & HARLEY RM. 2007. Reconfiguring the boundaries of the Chapada Diamantina National Park (Brazil) using ecological criteria in the context of a human-dominated landscape. Landsc Urban Plan 83(4): 355-362.
  • FUNCH RR, HARLEY RM & FUNCH LS. 2009. Mapeamento e avaliação do estado de conservação da vegetação no entorno do Parque Nacional da Chapada Diamantina, NE do Brasil. Biota Neotrop 9: 21-30.
  • GAGNÉ RJ. 1994. The gall midges of the Neotropical Region. University Press. Ithaca, 352 p.
  • GAGNÉ RJ & JASCHHOF M. 2017. A catalog of the Cecidomyiidae (Diptera) of the world. 4rd Edition. Digital.
  • GIULIETTI AM, PIRANI JR & HARLEY RM. 1997. Espinhaço Range region, Eastern Brazil. In: DAVIS SD, HEYWOOD VH, HERRERA-MACBRYDE O, VILLA-LOBOS J & HAMILTON AC (Eds) Centers of plant diversity, a guide and strategy for their conservation. Information Press, Oxford 3: 97-404.
  • GONÇALVES-ALVIM SJ & FERNANDES GW. 2001. Comunidades de insetos galhadores (Insecta) em diferentes fisionomias do cerrado em Minas Gerais, Brasil. Rev Bras Zool 18(1): 289-305.
  • GRILLO AS. 2008. Cerrado: áreas do Cercado e do Morro do Camelo. In: FUNCH LS, FUNCH, RR & QUEIROZ LP (Eds). Serra do Sincorá: Parque Nacional da Chapada Diamantina. Radami, Feira de Santana, p. 87-101.
  • HARLEY RM & SIMMONS NA. 1986. Florula of Mucugê – Chapada Diamantina – Bahia, Brazil: A Descriptive Check-list of a Campo Rupestre Area. Royal Botanic Gardens, Kew, 228 p.
  • ISAIAS RMS, CARNEIRO RGS, OLIVEIRA DC & SANTOS JC. 2013. Illustrated and Annotated Checklist of Brazilian Gall Morphotypes. Neotrop Entomol 42: 230-239.
  • JULIÃO GR, VENTICINQUE EM & FERNANDES GW. 2005. Riqueza e abundância de insetos formadores de galhas na Mamirauá Várzea, uma floresta amazônica inundada. Uakari 1: 39-42.
  • JULIÃO GR, VENTICINQUE EM, FERNANDES GW & PRICE PW. 2014. Unexpected high diversity of galling insects in the Amazonian upper canopy: the savanna out there. PLoS ONE 9: e114986.
  • LARA ACF & FERNANDES GW. 1996. The highest diversity of galling insects: Serra do Cipó, Brazil. Biodivers Lett 3: 111-114.
  • LARA ACF, FERNANDES GW & GONÇALVES-ALVIM SJ. 2002. Tests of hypotheses on patterns of gall distribution along an altitudinal gradient. Trop Zool 15: 219-232.
  • LAWTON JH. 1983. Plant architecture and the diversity of phytophagous insects. Annu Rev Entomol 28: 23-29.
  • LAWTON JH & SCHRÖDER D. 1977. Effects of plant type, size of geographical range and taxonomic isolation on number of insect species associated with British plants. Nature 265: 137-40.
  • LIMA VP & CALADO D. 2018. Morphological characterization of insect galls and new records of associated invertebrates in a Cerrado area in Bahia State, Brazil. Braz J Biol 78: 636-643.
  • LUZ GR, FERNANDES GW & SILVA JO, NEVES FS & FAGUNDES M. 2012. Galhas de insetos em habitats xérico e mésico em região de transição Cerrado Caatinga no norte de Minas Gerais, Brasil. Neotropical Biol Conserv 7: 171-187.
  • MAGALHÃES TA. 2010. Influência da fenologia no desenvolvimento e fisiologia das galhas de Eriogallococcus gen. nov. em Pseudobombax grandiflorum (Cav.) A. Robyns (Malvaceae). Dissertação de Mestrado, Universidade Federal de Minas Gerais, p. 79. (Unpublished).
  • MAIA VC. 2001. The gall midges (Diptera, Cecidomiidae) from three restingas of Rio de Janeiro State, Brazil. Rev Bras Zool 18: 583-629.
  • MAIA VC. 2013. Galhas de insetos em restingas da região sudeste do Brasil com novos registros. Biota Neotrop 13: 183-209.
  • MAIA VC, CARDOSO LJT & BRAGA JMA. 2014. Insect galls from Atlantic Forest areas of Santa Teresa, Espírito Santo, Brazil: characterization and occurrence. Boletim do MBML 33: 47-129.
  • MAIA VC & CARVALHO-FERNANDES SP. 2016. Insect galls of a protected remnant of the Atlantic Forest tableland from Rio de Janeiro State (Brazil). Rev Bras Entomol 60: 40-56.
  • MAIA VC & FERNANDES GW. 2004. Insect galls from Serra de São José (Tiradentes, MG, Brazil). Braz J Biol 64: 423-445.
  • MAIA VC & MASCARENHAS B. 2017. Insect galls of the Parque Nacional do Itatiaia (Southeast region, Brazil). An Acad Bras Cienc 89: 505-575.
  • MAIA VC & MASCARENHAS B. 2022. Insect galls from the Serra Negra do Funil Natural Heritage Private Reserve, Rio Preto, MG (Southeastern Brazil). An Acad Bras Cienc 94: e20200900.
  • MAIA VC & SILVA LO. 2016. Insect galls of Restinga de Marambaia (Barra de Guaratiba, Rio de Janeiro, RJ). Braz J Biol 76: 787-795.
  • MAIA VC & SOUZA SE. 2020. Insect galls of the Reserva Biológica União, Rio de Janeiro, Brazil. Biota Neotrop 20: e20190758.
  • MAIA VC & OLIVEIRA JC. 2010. Galhas de insetos da Reserva Biológica Estadual da Praia do Sul (Ilha Grande, Angra dos Reis, RJ). Biota Neotrop 10: 228-237.
  • MALVES K & FRIEIRO-COSTA FA. 2012. List of plants with galls induced by insects from the UNILAVRAS/Boqueirão Biological Reserve, Ingaí, State of Minas Gerais, Brazil. Checklist 8: 426-439.
  • MANI MS. 1964. Ecology of plant galls. Dr. W. Junk Publishers, The Hague, p. 434.
  • MELO GAB & SANTOS-SILVA J. 2023. Occurrence and characterization of insect galls in two areas of tropical dry forest (caatinga) in São Francisco River Natural Monument, Brazil. Entomol Beg 4: e058.
  • MELO JR JCF, ISAIAS RMS, BOEGER MRT, ARRIOLA IA & MATILDE-SILVA M. 2018. Diversidade de galhadores nas restingas do ecossistema Babitonga, Santa Catarina, Brasil. Rev Cepsul 7: eb2018003.
  • MENDONÇA JR MS. 2011. Galling arthropod diversity in the subtropical neotropics: Espinilho savannah and riparian forests compared. Rev Colomb Entomol 37: 114-119.
  • MENDONÇA JR MS, PICCARDI, HMF, JAHNKE SM & DALBEM RV. 2010. Galling arthropod diversity in adjacent swamp forests and restinga vegetation in Rio Grande do Sul, Brazil. Neotrop Entomol 39: 513-518.
  • MISI AM & SILVA G. 1994. Chapada Diamantina Oriental Bahia: geologia e depósitos. Salvador: Secretaria da Indústria, Comércio e Recursos Minerais. Serie Roteiros Geológicos, Salvador, SBG Núcleo BA-SE, p. 194.
  • MONTEIRO RF, ODA RA, NARAHARA KL & CONSTANTINO PDA. 2004. Galhas: diversidade, especificidade e distribuição. In: Rocha CDF, Esteves FA & Scarano FR (Eds). Pesquisas de longa duração na Restinga de Jurubatiba: Ecologia, história natural e conservação. São Carlos: Editora Rima 1: 127-141.
  • NOGUEIRA RM, COSTA EC, CARVVALHO-FERNANDES SP, SANTOS-SILVA J. 2016. Insect galls from Serra Geral, Caetité, BA, Brasil. Biota Neotrop 16: e20150035.
  • OLIVEIRA DC & ISAIAS RMS. 2010. Cytological and histochemical gradients induced by a sucking insect in gall of Aspidosperma australe Arg. Muell (Apocynaceae). Plant Sci 178: 350-358.
  • OLIVEIRA DC, ISAIAS RMS, MOREIRA ASFP, MAGALHÃES TA & LEMOS-FILHO JP. 2011. Is the oxidative stress caused by Aspidosperma spp. Galls capable of altering leaf photosynthesis? Plant Sci 180: 489-495.
  • OLIVEIRA JC. 2009.Viabilidade de espécies galhadoras (Diptera, Cecidomyiidae) e parasitóides (Hymenoptera) associadas à Guapira opposita (Vell.) (Nyctaginaceae) como bioindicadores da qualidade ambiental. Tese de Doutorado, Universidade Federal do Rio de Janeiro, Rio de Janeiro.
  • OLIVEIRA JC & MAIA VC. 2005. Ocorrência e caracterização de galhas de insetos na restinga de Grumari (Rio de Janeiro, RJ, Brasil). Arq Mus Nac (Rio de J) 63: 669-675.
  • PRICE PW, FERNANDES GW & WARING GL. 1987. Adaptive Nature of Insect Galls. Environ Entomol 16: 15-24.
  • R CORE TEAM. 2023. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
    » https://www.R-project.org/
  • RIBEIRO-FILHO AA, FUNCH LS & RODAL MJN. 2009. Composição florística da floresta ciliar do rio Mandassaia, Parque Nacional da Chapada Diamantina, Bahia, Brasil. Rodriguésia 60: 265-276.
  • RODRIGUES AR & MAIA VC. 2020. Galhas de insetos do parque Municipal da Boca da Barra, Cabo Frio, RJ. BJAER 3: 4282-4286.
  • ROOT RB. 1973. Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecol Monogr 34: 95-124.
  • SAITO VS & URSO-GUIMARÃES MV. 2012. Characterization of galls, insect galls and associated fauna of Ecological Station of Jataí (Luiz Antônio, SP). Biota Neotrop 12: 99-107.
  • SANTANA AP & ISAIAS RMS. 2014. Galling insects are bioindicators of environmental quality in a Conservation Unit. Acta Bot Bras 28: 594-608.
  • SANTANA CAGS, COSTA EC, CARVALHO-FERNANDES SP & SANTOS-SILVA J. 2020. Insect galls and their host plants in gallery forest in Bahia State, Brazil. Rev Bras Bot 43: 989-998.
  • SANTOS JC, ALMEIDA-CORTEZ JS & FERNANDES WG. 2011a. Richness of gall-inducing insects in the tropical dry forest (caatinga) of Pernambuco. Rev Bras Entomol 55: 45-54.
  • SANTOS JC, ALMEIDA-CORTEZ JS, FERNANDES GW. 2011b. Diversidade de insetos galhadores em florestas úmidas de altitude em Pernambuco, Nordeste do Brasil. Braz J Biol 71: 47-56.
  • SANTOS JC, ALMEDA-CORTEZ JS & FERNANDES GW. 2012. Insetos indutores de galhas da Floresta Atlântica de Pernambuco, Nordeste do Brasil. Biota Neotrop 12: 196-212.
  • SANTOS, PSND, OLIVEIRA MIUD, COUTO-SANTOS APLD & FUNCH LS. 2021. Diversity of Myrtaceae in and surroundings the Chapada Diamantina National Park, Brazil. Rodriguésia 72: e00222020.
  • SANTOS-SILVA J & ARAÚJO TJ. 2020. Are Fabaceae the principal super-hosts of galls in Brazil? An Acad Bras Cienc 92: e20181115.
  • SANTOS-SILVA J & ARAÚJO TJ. 2022. Galhas e divulgação científica: mapeamento desta temática nas redes sociais. Paubrasilia 5: e0087.
  • SANTOS-SILVA J, SANTOS GAB & SANTOS JC. 2022. Soils and seasonality influence the richness of gall-inducing insects and their host plants in a tropical dry forest. J Arid Environ 196: 1-11.
  • SHORTHOUSE JD, WOOL D & RAMAN A. 2005. Gall-inducing insects – Nature’s most sophisticated herbivores. Basic Appl Ecol 6: 407-411.
  • SILVA ARF, NOGUEIRA RM, COSTA EC, CARVALHO-FERNANDES SP & SANTOS-SILVA J. 2018. Occurrence and characterization of entomogenic galls in na área of Cerrado sensu stricto and Gallery forest of the state of Bahia, Brazil. An Acad Bras Cienc 90: 2903-2919.
  • SILVA JMC, TABARELLI M, FONSECA MT & LINS LV. 2004. Biodiversidade da Caatinga: áreas e ações prioritárias para a conservação. Universidade Federal de Pernambuco, Recife, 382 p.
  • SILVA P, ALMEIDA-SANTOS B, TABARELLI M & ALMEIDA-CORTEZ J. 2011. Occurrence of gall complexes along a topographic gradient in an undisturbed lowland forest of central Amazonia. Rev Bras Biocienc 9: 133-138.
  • STONE GN & SCHÖNROGGE N. 2003. The adaptive significance of insect gall morphology. Trends Ecol 18: 512-522.
  • TOMA TSP & MENDONÇA JR MS. 2013. Gall-inducing insects of an Araucaria Forest in Southern Brazil. Rev Bras Entomol 57: 225-233.
  • URSO-GUIMARÃES MV, KOCH I & CASTELLO ACD. 2021. Diversity of insect galls from Mato Grosso State, Brazil: Cerrado. Biota Neotrop 21(3): e20211189.
  • URSO-GUIMARÃES MV & SCARELI-SANTOS C. 2006. Galls and gallmakers in plants from Pé-de-Gigante Cerrado Reserve, Santa Rita do Passa Quatro, SP, Brazil. Rev Bras Bot 66: 357-369.
  • VELDTMAN R & MCGEOCH MA. 2003. Gall-forming insect species richness along a non-scleromorphic vegetation rainfall gradient in South Africa: the importance of plant community composition. Austral Ecol 28: 1-13.
  • VIEIRA LG, NOGUEIRA RM, COSTA EC, CARVALHO-FERNANDES SP & SANTOS-SILVA J. 2018. Insect galls in Rupestrian fields and Cerrado stricto sensu vegetation in Caetité, Bahia, Brazil. Biota Neotrop 18: e20170402.
  • WESTPHAL E. 1992. Cecidogenesis and resistance phenomena in miteinduced galls. In: Shorthouse JD & Rohfritsch O (Eds). Biology of insect-induced galls. New York, Oxford University Press, 157-170.
  • WIKLER C. 1999. Distribuição Geográfica Mundial de Psidium cattleianum Sabibe e um Cecidógeno com Possibilidades de Utilização em Controle Biológico. Tese de doutorado. Pós-Graduação em Engenharia Florestal, UFPR, Curitiba, 135.
  • WIKLER C. 2000. Gall Former as a Biological Control for Strawberry Guava – Psidium cattleianum. In: SPENCER NR (Ed) Proceedings of the X International Symposium on Biological Control of Weeds, Montana State University, Bozeman, Montana, EUA, p. 667-671.
  • WWF UNIDADES DE CONSERVAÇÃO NO BRASIL. 2019. Quanto o Brasil tem em unidades de conservação? FACTSHEET.

Publication Dates

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

History

  • Received
    1 Sept 2023
  • Accepted
    29 Dec 2023
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