Insect galls of the Tijuca National Park, Rio de Janeiro (RJ, Brazil): richness and characterization

ABSTRACT

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 (22^o55’-23^o00’S and 43^o11'-43^o19' 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 19^th 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.

Table 1
Characterization of insect galls from the Tijuca National Park, Rio de Janeiro (RJ), Brazil.

Host Plant		Gall characterization (n=72)			Insects obtained	Figure
Family (n=23)	Species (n=42)	Host organ	Shape/ Color	Pubescence/Nr. internal chambers
Achariaceae	Hydnocarpus cf. wightiana Blume	Leaf	Discoid/Green	Absent/1	Not determinedG	1a
Annonaceae	Annona sp.	Leaf	Conical Brown	Absent/1	CecidomyiidaeG	-
	Malmea sp.	Leaf	Globoid Yellow	Absent/1	Not determinedG	-
	Oxandra sp.	Leaf	Globoid Yellow	Present/1	CecidomyiidaeG	1b
Araceae	Heteropis sp.	Leaf	Fusiform Green	Absent/1	Not determinedG HemipteraS	1c
	Monstera sp.	Leaf	Fusiform Yellow	Absent/1	Not determinedG	1d
Asteraceae	Mikania glomerata Spreng.	Leaf	Conical Green	Absent/1	Liodiplosis conicaG Gagné, 2001G	1e
		Leaf	Globoid Green	Absent/1	Liodiplosis spherica Gagné, 2001G	1f
		Leaf vein	Fusiform Green	Absent/1	Asphondylia glomeratae Gagné, 2001G	1g
Bignoniaceae	Paratecoma peroba (Record) Kuhlm.	Leaf vein	Fusiform Green	Absent/1	CecidomyiidaeG	1h
	Tecoma sp.	Leaf vein	Fusiform Green	Absent/1	CecidomyiidaeG	-
Boraginaceae	Cordia sp.	Leaf	Globoid Green	Present/1	CecidomyiidaeG	1i
Chrysobalanaceae	Licania sp.	Leaf	Globoid Yellow	Present/1	CecidomyiidaeG	1j
						-
Clusiaceae	Not determined	Leaf (vein)	Fusiform Green	Absent/1	Not determinedG
Euphorbiaceae	Bia alienata Didr.	Leaf	Globoid Green	Present/1	CecidomyiidaeG	-
	Croton sp.	Leaf	Globoid Yellow	Present/1	CecidomyiidaeG	1k
		Stem	Fusiform Brown	Absent/1	Not determinedG	1l
	Sebastiania brasiliensis Spreng.	Leaf	Marginal roll Green	Absent/1	CecidomyiidaeG	-
Fabaceae	Albizia sp.	Leaf	Globoid Brown	Absent/1	Not determinedG	1m
		Leaf (vein)	Fusiform Brown	Absent/1	Not determinedG	1n
	Inga sp.	Leaf (vein)	Fusiform Green	Absent/	CecidomyiidaeG	1o
		Leaf	Lenticular Green	Absent/1	Not determinedG	1p
		Leaf	Fusiform Green	Absent/1	CecidomyiidaeG	1q
		Leaf	Conical Red	Absent/1	CecidomyiidaeG	1r
Lauraceae	Nectandra membranacea (Sw,) Griseb.	Leaf	Globoid Brown	Present/1	CecidomyiidaeG	1s
Melastomataceae	Clidemia sp.	Leaf	Globoid Green	Present/1	CecidomyiidaeG SciaridaeC	2a
		Stem	Fusiform Brown	Absent/1	CecidomyiidaeG	2b
	Miconia cf. ceramicarpa (DC.) Cogn.	Leaf	Globoid Green	Present/1	CecidomyiidaeG	2c
	Miconia nervosa (Sm.) Triana	Leaf	Globoid Red	Present/1	CecidomyiidaeG HymenopteraP	2d
	Miconia prasina (Sw.) DC.	Leaf	Globoid Green	Present/1	CecidomyiidaeG	2e
	Miconia pyrifolia Naudin	Leaf	Globoid Green	Present/1	CecidomyiidaeG	2f
	Miconia sp.	Leaf	Globoid Yellow	Absent/1	CecidomyiidaeG	2g
Meliaceae	Trichilia silvatica C. DC.	Leaf	Globoid Brown	Absent/1	CecidomyiidaeG HymenopteraP	2h
		Leaf	Fusiform Green	Absent/1	CecidomyiidaeG	2i
Monimiaceae	Mollinedia uleana Perkins	Leaf	Marginal roll Green	Absent/1	CecidomyiidaeG	-
Myrtaceae	Eugenia sp.	Leaf	Conical Green	Absent/1	CecidomyiidaeG	2j
		Leaf	Globoid Yellow	Absent/1	CecidomyiidaeG	2k
	Myrcia aethusa (O. Berg) N. Silveira	Leaf	Leaf roll Green	Absent/1	Not determinedG	2l
		Bud	Conical Green	Present/1	CecidomyiidaeG	2m
		Stem	Fusiform Brown	Present/multtichambered	CecidomyiidaeG	2n
Nyctaginaceae	Guapira opposita (Vell.) Reitz.	Leaf	Conical Green	Absent/1	Bruggmannia acaudataG Maia, 1994	2o
		Leaf	Globoid Green	Absent/1	CecidomyiidaeG	2p
		Bud	Globoid Green	Absent/1	CecidomyiidaeG	-
Phyllanthaceae	Phyllanthus sp.	Stem	Fusiform Brown	Absent/multichambered	Not determinedG	-
Piperaceae	Piper arboreum Aubl.	Leaf	Globoid Green	Absent/1	CecidomyiidaeG	2q
	Piper sp.	Leaf	Globoid Green	Absent/1	CecidomyiidaeG	2r
Rubiaceae	Amaioua sp.	Leaf(petiole and midvein)	Fusiform Green	Absent/multichambered	CecidomyiidaeG	2s
	Faramea sp.	Leaf	Globoid Green	Absent/1	CecidomyiidaeGHemipteraS	2t
	Palicourea sp.	Leaf	Globoid Green	Absent/1	CecidomyiidaeG	-
	Psychotria cf. bahiensis DC.	Leaf	Globoid Green	Absent/1	CecidomyiidaeG	3a
		Leaf	Globoid green	Absent/1	CecidomyiidaeG	3b
		Fruit	Globoid Green	Absent/1	HymenopteraP	-
		Leaf	CylindricalGreen	Absent/1	HymenopteraP	3c
		Leaf	Globoid Black	Absent/1	CecidomyiidaeG	3d
		Stem	Fusiform Brown	Absent/multichambered	CecidomyiidaeG	-
	Psychotria sp.	Leaf	Ovoid Green	Absent/1	CecidomyiidaeG	3e
Salicaceae	Casearia sp.	Stem	Fusiform Brown	Absent	CecidomyiidaeG	3f
		Leaf	Marginal roll Green	Absent/1	Not determinedG	3g
		Leaf Midvein	Fusiform Green	Absent/1	CecidomyiidaeG	3h
		Leaf	Globoid	Absent/1	Liothrips sp. (Thysanoptera)	3i
	Homalium sp.	Leaf	Lenticular Green	Absent/1	CecidomyiidaeG	3j
		Bud	Conical Green	Absent/1	CecidomyiidaeG	3k
Sapindaceae	Cupania scrobiculata Rich.	Leaf	Globoid Green	Present/1	CecidomyiidaeG	-
						-
	Serjania sp.	Leaf	Globoid Brown	Absent/1	CecidomyiidaeG HymenopteraP
		Leaf midvein	Fusiform Green	Absent/1	Not determinedG	3l
		Leaf	Lenticular Yellowish	Absent/1	Not determinedG	3m
		Leaf	Conical Yellowish	,Absent/1	CecidomyiidaeG	3n
		Stem	Fusiform Brown	Absent/multichambered	CecidomyiidaeG	3o
		Tendril	Fusiform Brown	Absent/multichambered	CecidomyiidaeG	3p
		Leaf	Conical Green	Absent/1	CecidomyiidaeG	3q
Solanaceae	Lycianthes pauciflora (Vahl) Bitter	Leaf	Globoid Green	Absent/1	CecidomyiidaeG	-
Sapotaceae	Pouteria sp.	Leaf	Globoid Green	Absent/1	CecidomyiidaeG	-

• C: cecidophages; G: gall-inducer; P: parasitoid; S: successor.

Figure 1
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.

Figure 2
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.

Figure 3
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.

Table 2
Richness of insect gall morphotypes by plant families, genera and species in the Tijuca National Park, Rio de Janeiro, RJ, Brazil.

Host plant family	Nr. genera	Nr. species	Nr. gall morphotypes	Average of morphotypes/species
Achariaceae	1	1	1	1.0
Annonaceae	3	3	3	1.0
Araceae	2	2	2	1.0
Asteraceae	1	1	3	3.0
Bignoniaceae	2	2	2	1.0
Boraginaceae	1	1	1	1.0
Chrysobalanaceae	1	1	1	1.0
Clusiaceae	1	1	1	1.0
Euphorbiaceae	3	3	4	1.3
Fabaceae	2	2	6	3
Lauraceae	1	1	1	1.0
Melastomataceae	2	6	7	1.7
Meliaceae	1	1	2	2.0
Monimiaceae	1	1	1	1.0
Myrtaceae	2	2	5	2.5
Nyctaginaceae	1	1	3	3.0
Phyllanthaceae	1	1	1	1.0
Piperaceae	2	2	2	1.0
Rubiaceae	4	5	10	2.0
Salicaceae	2	2	6	3.0
Sapindaceae	2	2	8	4.0
Solanaceae	1	1	1	1.0
Sapotaceae	1	1	1	1.0

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).

Table 3
Richness of insect gall morphotypes by plant organ in the Tijuca National Park, Rio de Janeiro, RJ, Brazil.

Plant organ	Nr. gall morphotypes (72)
Leaf	60 (83.3%)
Stem	7 (9.7%)
Bud	3 (4.2%)
Fruit	1 (1.4%)
Tendril	1 (1.4%)

Table 4
Richness of insect gall morphotypes by shape in the Tijuca National Park, Rio de Janeiro, RJ, Brazil.

Gall shape	Nr. gall morphotypes (72)
Globoid	32 (44.4%)
Fusiform	21 (29.1%)
Conical	9 (12.5%)
Marginal roll	3 (4.2%)
Lenticular	3 (4.2%)
Cylindrical	1 (1.4%)
Leaf roll	1 (1.4%)
Discoid	1 (1.4%)
Ovoid	1 (1.4%)

Table 5
Richness of insect gall morphotypes by color in the Tijuca National Park, Rio de Janeiro, RJ, Brazil.

Gall color	Nr. gall morphotypes (72)
Green	45 (62.5%)
Brown	13 (18.1%)
Yellow	9 (12.5%)
Red	2 (2.8%)
Black	1 (1.4%)

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).

Table 6
Richness of secondary dwellers of insect galls in the Tijuca National Park, Rio de Janeiro, RJ, Brazil.

Guild	Taxa	Nr. gall morphotypes
Parasitoids	Hymenoptera	5
Sucessors	Hemiptera	2
Cecidophages	Sciaridae	1

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).

Table 7
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.

Localities	Nr. gall morphotypes	Host plant		References
		Nr. families	Nr. spp.
Serra dos Órgãos National Park1	290	43	184	Maia and Mascarenhas (2023)
União Biological Reserve2	153	37	55	Maia and Siqueira (2020)
Guaxindiba State Ecological Station3	143	31	82	Maia and Carvalho-Fernandes (2016)
Tijuca National Park4	72	23	43	present study
Cicuta Forest3	43	15	24	Flor et al. (2018)

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.

References

• Almada, E. D., Fernandes, G. W. A., 2011. Insetos indutores de galhas em florestas de terra firme e em reflorestamentos com espécies nativas na Amazônia Oriental, Pará, Brasil. Bol. Mus. Para. Emílio Goeldi, sér. Cienc. Naturais 6, 163-196.
• Ansaloni, L. S., Salmazo, J. R., Guimarães, M. V. U., 2018. Entomogen galls in a Seasonal Semideciduous Forest area in Sorocaba, Southeast of São Paulo State, Brazil. Biota Neotrop. 18 (4), e20180523. https://doi.org/10.1590/1676-0611-bn-2018-0523
  » https://doi.org/10.1590/1676-0611-bn-2018-0523
• Araújo, W. S., Porfírio-Júnior, E. D., Jorge, V. A., Espírito-Santo Filho, K., 2012. Plantas hospedeiras e galhas entomógenas em sub-bosques de florestas tropicais do Pará, Brasil. Insula (Madrid) 41, 59-72. https://doi.org/10.5007/2178-4574.2012n41p59
  » https://doi.org/10.5007/2178-4574.2012n41p59
• Araújo, W. S., Porfírio-Junior, E. D., Ribeiro, B. A., Silva, T. M., Silva, E. C., Guilherme, F. A. G., Scareli-Santos, C., Santos, B. B., 2015. Checklist of host plants of insect galls in the state of Goiás in the Midwest region of Brazil. Biodivers. Data J. 3, e6835. https://doi.org/10.3897/BDJ.3.e6835
  » https://doi.org/10.3897/BDJ.3.e6835
• Bergamini, B. A. R., Bergamini, L. L., Santos, B. B., Araújo, W. S., 2017. Occurrence and characterization of insect galls in the Floresta Nacional de Silvania, Brazil. Pap. Avulsos Zool. 7 (32), 413-431. https://doi.org/10.11606/0031-1049.2017.57.32
  » https://doi.org/10.11606/0031-1049.2017.57.32
• Coelho, M. S., Almada, E. D., Fernandes, G. W., Carneiro, M. A. A., Santos, R. M., Quintino, A. V., Sanchez-Azofeifa, A., 2009. Gall inducing arthropods from a seasonally dry tropical Forest in Serra do Cipó, Brazil. Rev. Bras. Entomol. 53 (3), 404-414. https://doi.org/10.1590/S0085-56262009000300015
  » https://doi.org/10.1590/S0085-56262009000300015
• Coelho-Neto, A. L., 1992. O Geoecossistema da Floresta da Tijuca. In: Abreu, M.A. (Ed.), Natureza e Sociedade no Rio de Janeiro. Biblioteca Carioca. Secretaria Municipal de Cultura, Turismo e Esporte, Rio de Janeiro, pp. 104–142.
• Costa, K. C. S., Araújo, W. S., 2019. Gall-inducing arthropods of Parque da Sapucaia. Pap. Avulsos Zool. 59, e20195931. https://doi.org/10.11606/1807-0205/2019.59.31
  » https://doi.org/10.11606/1807-0205/2019.59.31
• Flor, I. C., Flor, J. C., Furtado, P. S. N., 2018. Insect galls of the Floresta da Cicuta (Volta Redonda, RJ, Brazil). Pap. Avulsos Zool. 58, e20185824. https://doi.org/10.11606/1807-0205/2018.58.24
  » https://doi.org/10.11606/1807-0205/2018.58.24
• Flor, I. C., Maia, V. C., 2020. Dois novos registros de galhas de insetos em Guapira opposita (Vell.) Reitz. (Nyctaginaceae) e Casearia sylvestris Sw. (Salicaceae) no Parque Nacional do Itatiaia (PNI), Sudeste, Brasil. Biota Amazôn. 9 (4), 53-54. https://doi.org/10.18561/2179-5746/biotaamazonia.v9n4p53-54
  » https://doi.org/10.18561/2179-5746/biotaamazonia.v9n4p53-54
• Flora e Funga do Brasil, 2024. Available in: https://floradobrasil.jbrj.gov.br/ (accessed 09 April 2024).
  » https://floradobrasil.jbrj.gov.br
• Flores, T. B., 2024. Meliaceae Available in: https://floradobrasil2020.jbrj.gov.br/FB10016 (accessed 09 April 2024).
  » https://floradobrasil2020.jbrj.gov.br/FB10016
• Gagné, R. J., 1994. The Gall Midges of the Neotropical Region. Cornell Univ. Press, Ithaca.
• Gagné, R. J., Oda, R. A. M., Monteiro, R. F., 2001. The gall midges (Diptera: Cecidomyiidae) of Mikania glomerata (Asteraceae) in Southeastern Brazil. Proc. Entomol. Soc. Wash. 103, 110-134.
• Gagné, R. J., Jaschhof, M., 2021. A Catalog of the Cecidomyiidae (Diptera) of the World, 5th ed. Department of Agriculture, Agricultural Research Service, Washington, D.C., U. S., 813 pp.
• Goetz, A. P. M., Luz, F. A., Toma, T. S. P., Mendonça-Júnior, M., 2018. Gall-inducing insects of deciduous and semideciduous forests in Rio Grande do Sul State, Brazil. Iheringia Ser. Zool. 108, e2018015. https://doi.org/10.1590/1678-4766e2018015
  » https://doi.org/10.1590/1678-4766e2018015
• ICMBio, 2024. Parque Nacional da Tijuca. Available in: https://www.icmbio.gov.br/parnatijuca (accessed 04 April 2024).
  » https://www.icmbio.gov.br/parnatijuca
• Isaias, R. M. S., Carneiro, R. G. S., Oliveira, D. C., Santos, J. C., 2013. Illustrated and Annotated Checklist of Brazilian Gall Morphotypes. Neotrop. Entomol. 42, 230-239. https://doi.org/10.1007/s13744-013-0115-7
  » https://doi.org/10.1007/s13744-013-0115-7
• Lirio, E. J., Peixoto, A. L., Zavatin, D. A., Pignal, M., 2024. Monimiaceae Available in: https://floradobrasil.jbrj.gov.br/FB10105 (accessed 08 April 2024).
  » https://floradobrasil.jbrj.gov.br/FB10105
• Lohmann, L. G. 2024. Paratecoma Available in: https://floradobrasil.jbrj.gov.br/FB114203 (accessed 08 April 2024).
  » https://floradobrasil.jbrj.gov.br/FB114203
• Maia, V. C., 2001. The gall midges (Diptera, Cecidomyiidae) from three restingas of Rio de Janeiro State, Brazil. Rev. Bras. Zool. 18 (2), 305-656. https://doi.org/10.1590/S0101-81752001000200028
  » https://doi.org/10.1590/S0101-81752001000200028
• Maia, V. C., Oliveira, J. C., 2010. Galhas de insetos da Reserva Biológica Estadual da Praia do Sul (Ilha Grande, Angra dos Reis, RJ). Biota Neotrop. 10 (4), 227-238.
• Maia, V. C., 2013a. Galhas de insetos em restingas da região sudeste do Brasil com novos registros. Biota Neotrop. 13, 183-209.
• Maia, V. C., 2013b. Insect galls of São Tomé das Letras (MG, Brazil). Biota Neotrop. 13 (4), 164-189.
• Maia, V. C., Souza, M. C., 2013. Insect galls of the xeric vegetation of Ilha do Cabo Frio (Arraial do Cabo, RJ, Brazil). Biota Neotrop. 13 (3), 278-288.
• Maia, V. C., 2014. Insect galls of Itamonte (Minas Gerais, Brazil): characterization and occurrence. Biota Neotrop. 14, 1-17.
• Maia, V. C., Cardoso, L. J. T., Braga, J. M. A., 2014. Insect galls from Atlantic Forest areas of Santa Teresa, Espírito Santo, Brazil: characterization and occurrence. Bol. Mus. Biol. Mello Leitão 33 (1), 47–129.
• Maia, V. C., Carvalho-Fernandes, S. P., 2016. Insect galls of a protected remnant of the Atlantic Forest tableland from Rio de Janeiro State (Brazil). Rev. Bras. Entomol. 60, 40-56. https://doi.org/10.1016/j.rbe.2015.09.001
  » https://doi.org/10.1016/j.rbe.2015.09.001
• Maia, V. C., Mascarenhas, B., 2017. Insect galls of the Parque Nacional do Itatiaia (Southeast Region, Brazil). An. Acad. Bras. Cienc. 89 (1, Suppl.), 505-575. https://doi.org/10.1590/0001-3765201720160877
  » https://doi.org/10.1590/0001-3765201720160877
• Maia, V. C., 2020. Insect galls of Paraty (State of Rio de Janeiro, Southeastern Brazil). Braz. J. Anim. Environ. Res. 3 (4), 4104-4115. Available in: https://ojs.brazilianjournals.com.br/ojs/index.php/BJAER/article/view/21224 (accessed 08 April 2024).
  » https://ojs.brazilianjournals.com.br/ojs/index.php/BJAER/article/view/21224
• Maia, V. C., Siqueira, E. S., 2020. Insect galls of the Reserva Biológica União, Rio de Janeiro, Brazil. Biota Neotrop. 20 (1), e20190758. https://doi.org/10.1590/1676-0611-BN-2019-0758
  » https://doi.org/10.1590/1676-0611-BN-2019-0758
• Maia, V. C., 2022. Review of the inquilinous fauna associated with insect galls in Brazilian restingas. Braz. J. Biol. 82, e235395. https://doi.org/10.1590/1519-6984.235395
  » https://doi.org/10.1590/1519-6984.235395
• Maia, V. C., 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 (4), e2020900. https://doi.org/10.1590/0001-3765202220200900
  » https://doi.org/10.1590/0001-3765202220200900
• Maia, V. C., Mascarenhas, B., 2023. Insect galls of Parque Nacional da Serra dos Órgãos (Rio de Janeiro State, Southeastern Brazil). Pap. Avulsos Zool. 63, e202363040. https://doi.org/10.11606/1807-0205/2023.63.040
  » https://doi.org/10.11606/1807-0205/2023.63.040
• Melo, A. L. 2024. Sebastiania Available in: https://floradobrasil.jbrj.gov.br/FB17671 (accessed 08 April 2024).
  » https://floradobrasil.jbrj.gov.br/FB17671
• Monteiro, R. F., Ferraz, F. F. F., Maia, V. C., Azevedo, M. A. P., 1994. Galhas entomógenas em restingas: uma abordagem preliminar. Anais ACIESP 3 (87), 210–220.
• Monteiro, R. F., Oda, R. A. M., 1999. Dolichophaonia gallicola (Albuq.) (Diptera: Muscidae): Espécie Cecidógena ou Inquilina? An. Soc. Entomol. Brasil 28 (3), 531–534. https://doi.org/10.1590/S0301-80591999000300021
  » https://doi.org/10.1590/S0301-80591999000300021
• Oliveira, J. C., Maia, V. C., 2005. Ocorrência e caracterização de galhas de insetos na restinga de Grumari (Rio de Janeiro, RJ, Brasil). Arch. Mus. Nac. 63 (4), 669-676.
• Proença, B., Maia, V. C., 2023. Insect galls from Amazon rainforest areas in Rondônia (Brazil). An. Acad. Bras. Cienc 95 (4), e20190869. https://doi.org/10.1590/0001-3765202320190869
  » https://doi.org/10.1590/0001-3765202320190869
• Ribeiro, A. N., Balbi, M. I. P. A., Urso-Guimarães, M. V., 2019. Characterization of insect galls from a vegetation area in Altinópolis, São Paulo State, Brazil. Pap. Avulsos Zool. 59, e20195904. https://doi.org/10.11606/1807-0205/2019.59.04
  » https://doi.org/10.11606/1807-0205/2019.59.04
• Rodrigues, A. R., Maia, V. C., 2020. Galhas de insetos do Parque Municipal da Boca da Barra, Cabo Frio, RJ. Braz. J. Anim. Environ. Res. 3 (4), 4282-4286. https://doi.org/10.34188/bjaerv3n4-124
  » https://doi.org/10.34188/bjaerv3n4-124
• Rodrigues, A. R., Maia, V. C., Couri, M. S., 2014. Insect galls of restinga areas of Ilha da Marambaia, Rio de Janeiro, Brazil. Rev. Bras. Entomol. 58 (2), 173-197. https://doi.org/10.1590/S0085-56262014000200010
  » https://doi.org/10.1590/S0085-56262014000200010
• Saito, V. S., Urso-Guimarães, M. V., 2012. Characterization of galls, insect galls and associated fauna of Ecological Station of Jataí (Luiz Antônio, SP). Biota Neotrop. 12 (3), 1–9.
• Santos, P. O., Ribeiro, J. E. L. S., 2015. Ocorrência e caracterização de galhas em fragmento de floresta estacional semidecidual em Telêmaco Borba, Paraná, Brasil. Semin. Cienc. Biol. Saude 36 (2), 15-24. https://doi.org/10.5433/1679-0367.2015v36n2p15
  » https://doi.org/10.5433/1679-0367.2015v36n2p15
• Santos, M. F., Amorim, B. S., Burton, G. P., Fernandes, T., Gaem, P. H., Lourenço, A. R. L., Lima, D. F., Rosa, P. O., Santos, L. L. D., Staggemeier, V. G., Vasconcelos, T. N. C., Lucas, E. J., 2024. Myrcia Available in: https://floradobrasil.jbrj.gov.br/FB37035 (accessed 24 April 2024).
  » https://floradobrasil.jbrj.gov.br/FB37035
• Shorthouse, J. D., Wool, D., Raman, A., 2005. Gall-inducing insects: nature’s most sophisticated herbivores. Basic Appl. Ecol. 6, 407-411. https://doi.org/10.1016/j.baae.2005.07.001
  » https://doi.org/10.1016/j.baae.2005.07.001
• Silva, T. M., Araújo, W. S., Santos, B. B., 2015. Ocorrência e caracterização de galhas de insetos em um fragmento de mata semicaducifólia do campus Samambaia, Goiânia, GO, Brazil. Rev. Biol. Neotrop. 12 (1), 26-38. https://doi.org/10.5216/rbn.v1i1.28343
  » https://doi.org/10.5216/rbn.v1i1.28343
• Silva, E. C., Santos, B. B., Araújo, W. S., 2018a. Insect gall occurrence in savanna and forest remnant sites of Hidrolândia, GO, Brazil Central. Pap. Avulsos Zool. 58, e20185804. https://doi.org/10.11606/1807-0205/2018.58.04
  » https://doi.org/10.11606/1807-0205/2018.58.04
• Silva, A. R. F., Nogueira, R. M., Costa, E. C., Carvalho-Fernandes, S. P., Santos-Silva, J., 2018b. Occurrence and characterization of entomogenic galls in an area of Cerrado sensu stricto and Gallery forest of the state of Bahia, Brazil. An. Acad. Bras. Cienc. 90 (3), 2903-2919. https://doi.org/10.1590/0001-3765201820170522
  » https://doi.org/10.1590/0001-3765201820170522
• Urso-Guimarães, M. V., Castello, A. C. D., Kataoka, E. Y., Koch, I., 2017. Characterization of entomogen galls from Mato Grosso do Sul, Brazil. Rev. Bras. Entomol. 61, 25-41. https://doi.org/10.1016/j.rbe.2016.08.002
  » https://doi.org/10.1016/j.rbe.2016.08.002
• Vieira, L. G., Nogueira, R. M., Costa, E. C., Carvalho-Fernandes, S. P., Santos-Silva, J., 2018. Insect galls in Rupestrian fields and Cerrado stricto sensu vegetation in Caetité, Bahia, Brazil. Biota Neotrop. 18 (2), e20170402. https://doi.org/10.1590/1676-0611-BN-2017-0402
  » https://doi.org/10.1590/1676-0611-BN-2017-0402

Edited by

Associate Editor: Marcia Couri

Publication Dates

• Publication in this collection
  07 Oct 2024
• Date of issue
  2024

History

• Received
  26 May 2022
• Accepted
  13 Aug 2024