Insect galls of the Tijuca National Park, Rio de Janeiro (RJ, Brazil): richness and characterizationABSTRACT
The Tijuca National Park comprises the world's largest urban forest. It has a rich flora, with around 1,550 plant species. For the first time, the insect galls of this area were investigated. We carried out 12 monthly collections from January to December/2009. Samples of host plants were pressed and identified. Galls were photographed and characterized according to their external morphology and number of chambers. Gall-inducing insects and secondary inhabitants were obtained from gall dissecation as well as from rearing in laboratory. Data on origin and geographic distribution of plant species were retrieved from Flora e Funga do Brasil website. We found 72 gall morphotypes on 43 plant species (36 genera, and 23 families). Rubiaceae, Sapindaceae, Salicaeae and Melastomataceae were the botanical families with the highest gall richness. Psychotria cf. bahiensis DC. (Rubiaceae) and Serjania sp. (Sapindaceae) highlighted as super host plant species. Five host plants are endemic to Brazil; they shelters eight gall morphotypes. Due to the high specificity of the gall-inducing insects, we considered them co-endemic, Leaf galls were the most frequent. Gall-inducers were represented mainly by Cecidomyiidae. Galls of Tijuca National Park followed the patterns already known from Brazil, but it richness is relatively low when compared to other areas of the Atlantic forest.
Keywords: Atlantic forest; Cecidomyiidae; Insect-plant interaction; Secondary fauna
Introduction
Insect galls are abnormal plant growths induced by some insect taxa. They are considered as one of the most sophisticated examples of insect-plant interaction (Shorthouse et al., 2005).
In the State of Rio de Janeiro, inventories of insect galls were carried out in Maricá (Maia, 2001), Arraial do Cabo (Monteiro et al., 1994), Cabo Frio: Ilha do Cabo Frio (Maia and Souza, 2013), Carapebus (Maia, 2001), Rio de Janeiro: Grumari (Oliveira and Maia, 2005), and Angra dos Reis: Ilha Grande (Maia and Oliveira, 2010). Some galls were also recorded from Paraty (Maia, 2020), and Cabo Frio: Parque Municipal da Boca da Barra (Rodrigues and Maia, 2020). No previous insect galls inventory is known from the Tijuca National Park (22o55’-23o00’S and 43o11'-43o19' W). Only two galls have been recorded: a bud gall induced by Zalepidota piperis Rübsaamen, 1907 on Piper arboreum Aubl. (Piperaceae) (Monteiro and Oda, 1999), and a leaf gall induced by Liodiplosis conica Gagné, 2001 on Mikania glomerata Sprengel (Asteraceae) (Gagné et al., 2001).
The Tijuca National Park is a mountainous hand-planted rainforest in the city of Rio de Janeiro, Brazil. It is the world's largest urban forest, covering 3,953 ha. It comprises hundreds of species of plants and wildlife, many threatened by extinction, found only in the Atlantic Rainforest. All the original forest had been destroyed to make way for coffee farms, being replanted in the second half of the 19th century. In 1961, it was declared a National Park. It comprises 1,550 plant species, a rich fauna and 120 archaeological sites. The vegetation is classified as Montane Dense Ombrophylous Forest (ICMBio, 2024), and the local climate is classified as Af by Köeppen (Coelho-Neto, 1992).
The main objective of this study is to provide an inventory of insect galls of the Tijuca National Park and to contribute to the knowledge of the insect galls of the Atlantic Forest.
Material and methods
We collected insect galls monthly from January to December/2009, along the seven trails: Estrada da Cascatinha, Viveiros de Pássaros, Excelsior, Bom Retiro, A Fazenda, Jardim dos Manacás, and Açude da Solidão.
We investigated plants for insect galls during seven hours per collection, in a total of 84 hours of sampling. We examined all organs, except for the subterraneous roots. We pressed samples of host plants, preferably in the fertile state, in the field. Dr. Gracialda Costa Ferreira (Universidade Federal Rural da Amazônia, Pará) identified botanical species and the voucher material was deposited in the herbarium of the UFRAM.
Antônio Clóvis de Britto Araújo (Museu Nacional/UFRJ) photographed the gall morphotypes in field, using a digital photographic camera. The authors characterized each morphotype based upon shape, color, presence or absence of trichomes, number of internal chambers, and galling insect based on Isaias et al. (2013).
We obtained immature insects by dissection of samples of each gall morphotype under a stereoscopic microscope. We kept samples of each gall morphotype individually in plastic pots layered at the bottom with damp cotton and covered by fine screening to obtain pupal exuviae and adults. We checked all pots daily for emergence.
We stored all insects in microvials with 70% alcohol and subsequently mounted gall midges (Diptera: Cecidomyiidae) on slides for microscope, following the methodology outlined by Gagné (1994). We identified the gall-inducing genera and species based on host plant data, gall morphology and original description of the inducers. All material was deposited in the Entomological Collection of Museu Nacional (MNRJ)/UFRJ.
We used the website Flora e Funga do Brasil (2024) to verify the correct spelling of botanical species, their synonyms, authors, distribution in Brazil and origin.
Results
We found 72 gall morphotypes in the Tijuca National Park. They are associated with 43 plant species (36 genera and 23 families) (Table 1). Rubiaceae, Sapindaceae, Melastomataceae, and Salicaeae were the plant families with the highest gall richness (10, 8, 7 and 6, respectively). The average of gall morphotypes per plant species in botanical families varied from 1.0 to 4.0. Thirteen families (62.5%) showed the lowest medium number, while Sapindaceae, Salicaceae, Nyctaginaceae, and Asteraceae presented the highest average (the first 4.0 and the other three 3.0) (Table 2). Psychotria cf. bahiensis DC. (Rubiaceae) and Serjania sp. (Sapindaceae) highlighted as super host plant species.
Characterization of insect galls from the Tijuca National Park, Rio de Janeiro (RJ), Brazil.
Insect galls of the Tijuca National Park, Rio de Janeiro, RJ, Brazil: (a) Discoid leaf gall on Hydnocarpus cf. wightiana (Achariaceae); (b) Conical leaf on Oxandra sp. (Annonaceae); (c-d) On Araceae: (c) Fusiform leaf gall on Heteropis sp.; (d) Fusiform leaf gall on Monstera sp.; (e-g) On Mikania glomerata (Asteraceae): (e) Conical leaf gall; (f) Globoid leaf gall; (g) Fusiform leaf gall; (h) Fusiform leaf gall on Paratecoma peroba (Bignoniaceae); (i) Globoid leaf gall on Cordia sp. (Boraginaceae); (j) Globoid leaf gall on Licania sp. (Chrysobalanaceae); (k-l) On Croton sp. (Euphorbiaceae): (k) Globoid leaf gall; (l) Fusiform stem gall; (m-r) On Fabaceae: (m-n) On Albizia sp.: (m) Globoid leaf gall; (n) Fusiform leaf gall; (o-r) On Inga sp.: (o) Fusiform leaf gall; (p) Lenticular leaf gall; (q) Fusiform leaf gall; (r) Conical leaf gall; (s) On Nectandra membranacea (Lauraceae), globoid leaf gall.
Insect galls of the Tijuca National Park, Rio de Janeiro, RJ, Brazil: (a-f) On Melastomatacae: (a, b) On Clidemia sp.: (a) Globoid leaf gall; (b) Fusiform stem gall; (c) On Miconia cf. ceramicarpa, globoid leaf gall; (d) On Miconia nervosa, globoid leaf gall; (e) On Miconia prasina, globoid leaf gall; (f) On Miconia pyrifolia, globoid leaf gall; (g) On Miconia sp., globoid leaf gall; (h-i) On Trichilia silvatica (Meliaceae): (h) globoid leaf gall; (i) fusiform leaf gall; (j-n) On Myrtaceae: (j-k) On Eugenia sp.: (j) conical leaf gall; (k) globoid leaf gall; (l-n) On Myrcia aethusa: (l) Marginal roll; (m) conical bud gall; (n) fusiform stem gall; (o-p) On Guapira opposita (Nyctaginaceae): (o) conical leaf gall; (p) globoid leaf gall; (q-r) On Piperaceae, globoid leaf gall: (q) On Piper arboreum, leaf gall; (r) On Piper sp., leaf gall; (s-t) On Rubiaceae: (s) On Amaioua sp., fusiform leaf gall; (t) On Faramea sp., globoid leaf gall.
Insect galls of the Tijuca National Park, Rio de Janeiro, RJ, Brazil: (a-e) On Rubiaceae: (a-d) On Psychotria cf. bahiensis: (a) globoid leaf gall; (b) globoid leaf gall; (c) cylindrical leaf gall; (d) globoid leaf gall; (e) On Psychotria sp., ovoid leaf gall; (f-k) On Salicaceae: (f-i) On Casearia sp.: (f) fusiform stem gall; (g) marginal roll; (h) fusiform leaf gall; (i) globoid leaf gall; (j-k) On Homalium sp.: (j) lenticular leaf gall; (k) conical bud gall; (l-q) On Serjania sp. (Sapindaceae): (l) fusiform leaf gall; (m) lenticular leaf gall; (n) conical leaf gall; (o) fusiform stem gall; (p) fusiform tendril gall; (q) conical leaf gall.
Richness of insect gall morphotypes by plant families, genera and species in the Tijuca National Park, Rio de Janeiro, RJ, Brazil.
All galled plant species and genera reported here are native of Brazil. Among them five species are endemic: Mollinedia uleana Perkins (Monimiaceae) (Lírio et al., 2024), Paratecoma peroba (Record) Kuhlm. (Bignoniaceae) (Lohmann, 2024), Myrcia aethusae (O. Berg.) N. Silveira (Myrtaceae) (Santos et al., 2024), Sebastiania brasiliensis Spreng. (Euphorbiaceae) (Melo, 2024), and Trichilia silvatica C. DC. (Meliaceae) (Flores, 2024), the first three are known only from the Atlantic forest, while the last two from the Atlantic forest and Cerrado.
We found galls on leaves, stems, buds, fruits and tendril, being more frequent on leaves (83.3% of the total). Galls on flowers and aerial roots were not found (Table 3). We recorded marginal rolls, leaf rolls, globoid, fusiform, discoid, lenticular, conical, cylindrical, and ovoid galls, with the majority being globoid (Table 4). Galls exhibited green, brown, yellow, red, and black colors, being predominant the first one, with 63.9% (Table 5). Most morphotypes were glabrous (79.2%), while only 20.8% showed trichomes. Concerning the number of internal chamber, 93.0% had a single chamber, whereas 7.0% had two or more (Table 1).
Richness of insect gall morphotypes by plant organ in the Tijuca National Park, Rio de Janeiro, RJ, Brazil.
Richness of insect gall morphotypes by shape in the Tijuca National Park, Rio de Janeiro, RJ, Brazil.
Richness of insect gall morphotypes by color in the Tijuca National Park, Rio de Janeiro, RJ, Brazil.
We determined most gall-inducers (83.3%). However, 12 (16.7%) were not determined since gall samples were collected after the inducer emergence or with parasitoids. Inducers were represented mainly by gall midges (Cecidomyiidae, Diptera), responsible for 59 gall morphotypes, but also by thrips (Thysanoptera), responsible for a single gall morphotype. We did not find Lepidoptera, Coleoptera, Hemiptera and Hymenoptera-induced galls. Four gall midges were identified at species level: Asphondylia glomeratae Gagné, 2001, Bruggmannia acaudata Maia, 1994, Liodiplosis conica Gagné, 2001, and L. spherica Gagné, 2001; and the gall-inducing thrips was identified at genus level: Liothrips sp. (Phlaeothripidae).
We observed secondary dwellers in eight gall morphotypes. They included parasitoid Hymenoptera, successor Hemiptera, and cecidophagous Sciaridae (Diptera), which were found in five, two, and one gall morphotypes, respectively (Table 6).
Richness of secondary dwellers of insect galls in the Tijuca National Park, Rio de Janeiro, RJ, Brazil.
Discussion
Our findings in Tijuca National Park (TNP) revealed 72 gall morphotypes on 43 plant species of 23 families. When comparing these data with other forests in the state of Rio de Janeiro, such as Serra dos Órgãos National Park (SONP - Maia and Mascarenhas, 2023), União Biological Reserve (UBR - Maia and Siqueira, 2020), Guaxindiba State Ecological Station (GSES - Maia and Carvalho-Fernandes, 2016), and Cicuta Forest (CF - Flor et al., 2018), we noticed that the TNP has one of the lowest gall richness, number of host plant families and species (Table 7). However, the TNP was investigated for 12 months while the other areas were investigated for seven (SONP), five (UBR and GSES) and two months (CF). In addition, seven trails were surveyed in TNP, while four in UBR and GSES, and three in CF. Only in SONP, the number of surveyed trails (n=24) was higher than in the TNP. Therefore the collection effort was the greatest in TNP considering the sampling period (12 months), and the second largest in relation to the number of trails (seven).
Insect gall richness in forest formations of the Atlantic forest in the state of Rio de Janeiro, Brazil. 1 – high montane dense ombrophilous forest, 2 – lowlands and submontane dense ombrophilous forest, 3 – semi-deciduous seasonal forest, 4 –dense ombrophilous forest in an advanced stage of regeneration.
Furthermore, TNP, SONP, UBR, GSES, and CF differ in terms of plant physiognomy (Table 7). SONP and UBR are covered by dense ombrophilous forest and host the highest gall richness, while GSES and CF are covered by semi-deciduous seasonal forest and host the lowest richness. Considering that in semi-deciduous seasonal forest, 20 to 50% of the vegetation loses its leaves and the majority of galls occur on leaves, it is expected that the gall richness in this plant physiognomy is lower than in ombrophilous forest. Despite TNP being covered by ombrophilous forest, it showed a low gall richness. However, it is important to highlight that TNP is a secondary forest. In the past, it was almost completely destroyed for charcoal production and coffee planting in the past, and that its current vegetation is the result of a replanting process that began in 1861 (ICMBio, 2024). Therefore, the TNP plants had to be recolonized by gall-inducing insects, which may have impacted the local gall richness.
Rubiaceae, Sapindaceae, Melastomataceae and Salicaceae were the plant families with the highest gall richness in TNP. Rubiaceae and Melastomataceae highlighted as multi host families in SONP, Sapindaceae in GSES and CF, and Salicaceae is pointed out for the first time as multi host.
The average of gall morphotypes per plant species in botanical families varied from 1.0 to 4.0. Most families showed the lowest average as they did not include multi host species. On the other hand, Sapindaceae, Salicaceae, Nyctaginaceae and Asteraceae, the families with the highest average, included multi host species. Among the latter, Psychotria cf. bahiensis DC. (Rubiaceae) and Serjania sp. (Sapindaceae) highlighted as super host plant species, as they sheltered the highest richness of insect galls. Psychotria cf. bahiensis was never mentioned in gall inventories as host plant, while several species of Serjania (determined or not) were already reported in areas of Amazonian forest (Almada and Fernandes, 2011; Araújo et al., 2012; Proença and Maia, 2023), Atlantic forest (Maia 2013a, 2013b, 2014, Maia et al., 2014; Rodrigues et al., 2014; Santos and Ribeiro, 2015; Maia and Carvalho-Fernandes, 2016; Maia and Mascarenhas, 2017; Ansaloni et al., 2018; Goetz et al., 2018; Maia and Siqueira, 2020; Maia and Mascarenhas, 2022; 2023), Cerrado (Coelho et al., 2009; Saito and Urso-Guimarães, 2012; Araújo et al., 2015; Silva et al., 2015; Bergamini et al., 2017; Silva et al., 2018a, 2018b; Vieira et al., 2018; Costa and Araújo, 2019; Ribeiro et al., 2019), and Pantanal (Urso-Guimarães et al., 2017). Only in Bergamini et al. (2017) and Silva et al. (2018a), species of Serjania stood out as super host, but in both inventories they are not determined.
The endemic plant species host a total of eight gall morphotypes. Due to the high specificity of the gall-inducing insects, we considered them co-endemic. However, these insects are not identified in species, indicating that TNP hosts endemic inducers still unknown. In SONP, UBR and CF co-endemic inducers were also reported (69, 27 and 6, respectively), representing 23.8%, 17.6% and 13.9% of the cecidogenous species. This value is the lowest in TNP (11.1%).
We found galls on leaves, stems, buds, fruits and tendril, being more frequent on leaves and stems, following the known global pattern (Isaias et al., 2013). We highlighted the highest frequency of globoid, green, glabrous, and one-chambered galls, which are the most common features in Brazilian inventories (Maia and Mascarenhas, 2017; Ansaloni et al., 2018; Goetz et al., 2018; Maia and Siqueira, 2020, and others).
The guild of inducers was composed mainly by Cecidomyiidae, the most diverse taxon of gall-inducing insects in the world (Gagné and Jaschhof, 2021). Four of them were identified at species level: Asphondylia glomeratae, Bruggmannia elongata, Liodiplosis conica, and L. spherica. The first was previously recorded in TPN (Gagné et al., 2001). On the other hand, the occurrence of the last three gall midges is new. A single gall morphotype was induced by Liothriops sp. on Casearia sp. (Salicaceae). Flor and Maia (2020) reported a similar gall in the Itatiaia National Park (Southeastern Brazil). In SONP, UBR and CF, the gall-inducing guild is more diverse than in TNP. Cecidomyiidae were reported in all of them, but in SONP, Coleoptera, Hemiptera, Hymenoptera, Lepidoptera, and Thysanoptera were also reported; in URB, Hemiptera, Hymenoptera, Lepidoptera, and Thysanoptera; and in CF Hemiptera and Lepidoptera.
We reported parasitoid, successor, and cecidophagous species in some gall morphotypes. These guilds were previously reported in several inventories (Maia, 2001;Bergamini et al., 2017; Ansaloni et al., 2018; Flor et al., 2018; Maia and Siqueira, 2020, and others). Among them, parasitoids are the most frequent, represented exclusively by Hymenoptera. Successors and cecidophages include a great diversity of arthropods (Maia, 2022). However, these guilds were represented only Hemiptera and Sciaridae, respectively, in the present study, which highlights their low diversity in TNP.
Conclusions
The richness of insect galls of the TNP is relatively low when compared to other forest areas of the Atlantic forest. Most multi host botanical taxa reported here are known from other inventories. However, Psychotria cf. bahiensis DC. (Rubiaceae) is indicated for the first time as super host. The gall-inducing guild of TNP is little diverse, including only Cecidomyiidae, responsible for almost all gall morphotypes, and Thysanoptera. Endemic host plants and co-endemic gall-inducing insects were recorded in the study area. Their presence emphasizes the importance of the TNP in the role of protecting Brazilian diversity. The predominant gall features are the same as those found in most Brazilian inventories, reinforcing the already known patterns. Gall-inducers and secondary fauna are less diverse than in other studies carried out in Brazil.
Acknowledgments
We are grateful to Dr. Gracialda Costa Ferreira (Universidade Federal Rural da Amazônia) for plant identification and Antônio Clóvis de Britto Araújo (Museu Nacional/Universidade Federal do Rio de Janeiro) for field assistance and photographies.
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Edited by
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Associate Editor: Marcia Couri
Publication Dates
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Publication in this collection
07 Oct 2024 -
Date of issue
2024
History
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Received
26 May 2022 -
Accepted
13 Aug 2024
