Abstract:

Insect galls host a rich and diverse fauna of secondary dwellers, which compose the associated fauna. In Brazil, many inventories of insect galls in Cerrado areas have recorded secondary dwellers. These records were scattered in several papers. This study gathered literature data to provide an overview of the arthropod fauna associated with insect galls in the Brazilian Cerrado. We searched for scientific publications in online academic databases and retrieved 16 papers with data on the secondary dwellers. We limited our search to the period from 1988 to 2020. We updated the name of plant species and verified endemism and geographic distribution in Flora do Brasil 2020FLORA DO BRASIL 2020. http://floradobrasil.jbrj.gov.br. (last access in 20/Dec/2020).
http://floradobrasil.jbrj.gov.br... . We provided plant species uses based on the Tropical Useful Plants 2014. We found 163 gall morphotypes with secondary dwellers (16.8% of the total of gall morphotypes of the Brazilian Cerrado) on 94 plant species in 37 families. Asteraceae, Fabaceae, Myrtaceae, and Malpighiaceae exhibited the greatest number of records. These are the richest families in insect galls in the Brazilian Cerrado. Most arthropod fauna were recorded in galls of Cecidomyiidae (Diptera). Most records were in leaf galls, the predominant galled organ. Parasitoids were more frequent than successors, inquilines, and predators. Eulophidae and Eurytomidae were the most frequent parasitoid families. Inquilines were represented by Coleoptera, Diplopoda, Diptera, Hemiptera, Hymenoptera, Lepidoptera, Psocoptera, and Thysanoptera; successors by Acari, Araneae, Cecidomyiidae (Diptera), Coleoptera, Collembola, and Formicidae (Hymenoptera), whereas predators by Pseudoscorpiones and Diptera. Most records were presented in suprageneric categories, showing that the taxonomic knowledge is very deficient. 29 plant species are endemic to Brazil and totaled 45 gall morphotypes with secondary dwellers; 46 plant species are useful and host secondary dwellers in 62 gall morphotypes. These data add ecological and economic importance to these arthropods.

Keywords:
Parasitoids; inquilines; predators; successors; galling-insects

Resumo:

As galhas de insetos abrigam uma fauna rica e diversificada de habitantes secundários que compõem a fauna associada. No Brasil, muitos inventários de galhas de insetos em áreas de Cerrado registram habitantes secundários. Estes registros, dispersos em vários artigos, foram reunidos para fornecer uma visão ampla da fauna de artrópodes associados às galhas de insetos no Cerrado brasileiro. Buscamos publicações científicas nas bases de dados acadêmicas virtuais e encontramos 16 artigos com informações de habitantes secundários. Limitamos nossa busca ao período de 1988 a 2020. Atualizamos o nome das espécies botânicas e verificamos sua distribuição geográfica e endemismos no site Flora do Brasil 2020FLORA DO BRASIL 2020. http://floradobrasil.jbrj.gov.br. (last access in 20/Dec/2020).
http://floradobrasil.jbrj.gov.br... . Fornecemos os usos das espécies vegetais com base no site Tropical Useful Plants 2014. Encontramos 163 morfotipos de galhas com habitantes secundários (16,8% do total de morfotipos de galhas do Cerrado brasileiro) em 94 espécies de plantas de 37 famílias. Asteraceae, Fabaceae, Myrtaceae e Malpighiaceae exibiram o maior número de registros. Estas são as famílias mais ricas em galhas de insetos no Cerrado brasileiro. A maioria da fauna de artrópodes foi assinalada em galhas de Cecidomyiidae (Diptera). A maioria dos registros foi em galhas foliares, órgão vegetal com maior riqueza de galhas. Os parasitoides foram mais frequentes que os sucessores, inquilinos e predadores. Eulophidae e Eurytomidae foram as famílias de parasitoides mais frequentes. Os inquilinos foram representados por Coleoptera, Diplopoda, Diptera, Hemiptera, Hymenoptera, Lepidoptera, Psocoptera, e Thysanoptera; os sucessores por Acari, Araneae, Cecidomyiidae (Diptera), Coleoptera, Collembola e Formicidae (Hymenoptera); enquanto os predadores por Pseudoscorpiones e Diptera. A maioria dos registros foi apresentada em categorias supragenéricas, mostrando que o conhecimento taxonômico é muito deficiente. Vinte e nove plantas são endêmicas do Brasil e totalizam 45 morfotipos de galhas com habitantes secundários; 46 espécies vegetais são úteis e hospedam habitantes secundários em 62 morfotipos de galhas. Estas informações acrescentam importância ecológica e econômica a estes artrópodes.

Palavras-chave:
Parasitoides; inquilinos; predadores; sucessores; insetos galhadores

Introduction

Galls are a classic example of niche construction (Gilbert 2009GILBERT, S.F. 2009. The adequacy of model systems for evo-devo: modeling the formation of organisms/modeling the formation of society. In A. Barberousse M. Morange & T. Pradeu (eds.) Mapping the Future of Biology. Evolving Concepts and Theories, Boston Studies in the Philosophy of Science, Springer, U.S.A., p.57-68.). They represent discrete microhabitats that support relatively closed communities of specialist inhabitants (Shorthouse & Rohfritsch 1992SHORTHOUSE, J.D. & ROHFRITSCH, O. 1992. The biology of insect-induced galls. Oxford University Press, Oxford., Williams 1994WILLIAMS, M.A.J. 1994. Plant Galls: Organisms, Interactions, Populations. Oxford University Press., Crespi et al. 1997CRESPI, B.J., CARMEAN, B.A. & CHAPMAN, T.W. 1997. Ecology and evolution of galling thrips and their allies. Annu Rev Entomol 42:51-71.). Galls are abnormal plant growths induced by various parasitic organisms, mainly insects. Insect galls provide the inducers with food and shelter at the expense of the host plant (Tooker et al. 2008TOOKER, J.F., ROHR, J.R., ABRAHAMSON, W.G. & DE MORAES, C.M. 2008. Gall insects can evade and alter indirect plant defenses. New Phytol 178:657-671). Galls serve as ''incubators'' for the developing insects in which they gain nutrition and protection from both abiotic factors (e.g., sun irradiation, wind, rain and snow) and natural enemies such as pathogens, predators and parasitoids (Price et al. 1987PRICE, P.W., FERNANDES, G.W. & WARING, G.L. 1987. Adaptive nature of insect galls. Environ Entomol 16:15-24., Stone & Schonrogge 2003STONE, G.N. & SCHONROGGE, K. 2003. The adaptive significance of insect gall morphology. Trends Ecol Evol 18:512-522). Galls act as a ''nutrient sink'' into which the plant translocates concentrated soluble nutrients for the growth of those cells. These nutrients, which are especially rich in amino acids, are then used by the gall-inducer for its own growth (White 2010WHITE, T.C.R. 2010. Why do many galls have conspicuous colours? An alternative hypothesis. Arthropod Plant Inte 4:149-150.).

Gall tissues are attractive for non-galling herbivores as food sources (Sugiura & Yamazaki 2009SUGIURA, S. & YAMAZAKI, K. 2009.Gall-attackingbehaviorinphytophagousinsects, with emphasis on Coleoptera and Lepidoptera. Terr Arthrop Rev.2:41-61., Yamazaki & Sugiura 2016YAMAZAKI, K. & SUGIURA, S. 2016.Stem-galling moths provide cetoniine beetles with feeding sites via sap exudation of invasive alien plants. Entomol.Sci.19:142-146.). There is a rich and diverse fauna of secondary dwellers of galls. They compose the associated fauna and include parasitoids, predators, cecidophages, successors, inquilines, kleptoparasites and symbionts (Luz & Mendonça-Júnior 2019LUZ, F.A. & MENDONÇA-JÚNIOR, M.S. 2019. Guilds in insect galls: who is who. Fla Entomol 102: 207-210.).

In Brazil, there are several inventories of insect galls in Cerrado areas, mainly in the states of Minas Gerais and Goiás (Araújo et al. 2014ARAÚJO, W.S., SANTOS, B.B., GUILHERME, F.A.G. & SCARELI-SANTOS, C. 2014. Galling insects in the Brazilian Cerrado: ecological patterns and perspectives. In G.W. Fernandes & J. C. Santos (eds.). Neotropical Insect Galls. Springer, New York, U.S.A, p.257-272.). The Cerrado is the second largest phytogeographical domain of Brazil, occupying an area of ca. 2 million km² (23% of the national territory) (Oliveira & Ratter 2002OLIVEIRA FILHO, A.T. & RATTER, J.A. 2002. Vegetation physiognomies and woody flora of the cerrado biome. In The cerrados of Brazil (P.S. Oliveira & R.J. Marquis, eds.). Columbia University Press, New York, p.91-120.) and one of the phytogeographical domains with the highest plant diversity in the world, containing over 12,000 species (Klink & Machado 2005KLINK, C.A. & MACHADO, R.B. 2005. Conservation of the Brazilian Cerrado. Conserv Biol 19:707-713., Mendonça et al. 2008MENDONÇA, R.C., FELFILI, J.M., WALTER, B.M.T., SILVA-JÚNIOR, M.C., REZENDE, A.V., FILGUEIRAS, T.S., NOGUEIRA, P.E. & FAGG, C.W. 2008. Flora vascular do Bioma Cerrado: checklist com 12.356 espécies. In S.M. Sano, S.P. Almeida & J.F. Ribeiro (eds.). Cerrado: ecologia e flora. Embrapa, Brasília, BR, p.421-1279.). Furthermore, the Cerrado is considered one of the world`s biodiversity hotspots and a priority conservation area (Myers et al. 2000MYERS, N., MITTERMEIER, R.A., MITTERMEIER, C.G., FONSECA, G.A. & KENT, J. 2000. Biodiversity hotspots for conservation priorities. Nature 403:853.). Cintra et al. (2020)CINTRA, F.C.F., ARAÚJO, W S., MAIA, V.C, URSO-GUIMARÃES, M.V., VENÂNCIO, H., ANDRADE, J.F., CARNEIRO, M.A.A., ALMEIDA, W.R. & SANTOS, J.C. 2020. Plant-galling insect interactions: a dataset of host plants and their gall-inducing insects for the Brazilian savannah. Ecology 101. https://doi.org/10.1002/ecy.3149
https://doi.org/10.1002/ecy.3149... published a dataset of host plants and their gall-inducing insects for the Brazilian Cerrado, which represented a major effort to compile species lists of host plant communities for galling insects of the Neotropical region. However, Cintra et al. (2020)CINTRA, F.C.F., ARAÚJO, W S., MAIA, V.C, URSO-GUIMARÃES, M.V., VENÂNCIO, H., ANDRADE, J.F., CARNEIRO, M.A.A., ALMEIDA, W.R. & SANTOS, J.C. 2020. Plant-galling insect interactions: a dataset of host plants and their gall-inducing insects for the Brazilian savannah. Ecology 101. https://doi.org/10.1002/ecy.3149
https://doi.org/10.1002/ecy.3149... did not address the associated fauna.

Gall-inducers can influence the distribution and abundance of organisms in diverse communities by providing a physical structure that can be later used as shelter from the physical environment, protection from natural enemies as well as food resources. Therefore, they alter the local environment through habitat modification or amelioration of abiotic stress, with direct and indirect effects on other components of communities and ecosystem properties (Cuddington et al. 2007CUDDINGTON, K., BYERS. J., HASTINGS, A. & WILSON, W. 2007. Ecosystem engineers: plants to protists. Academic Press, Elsevier, New York.). This valuable role of gall-inducers as ecosystem engineers (Cornelissen et al. 2016CORNELISSEN, T., CINTRA, F.C.F. & SANTOS, J.C. 2016. Shelter-building insects and their role as ecosystem engineers. Neotrop Entomol 45:1-12. ) reinforces the importance of studying the associated fauna and knowing its composition, richness and ecological interactions.

The present study aims to compile data on arthropods associated with insect galls in the Brazilian Cerrado and answer the following questions: i) which guilds are represented? ii) which is the most frequent? iii) which is the most diverse? iv) what is the composition of each one? v) which plants host these guilds? vi) how many gall morphotypes host them? vii) do these guilds occur in endemic or useful hosts? vii) which galling insects stand out for sheltering the secondary fauna more often?

Material and Methods

We searched for papers in online academic databases: ISI Web of Knowledge, Google Scholar, Scielo, Scopus and JStor, using the terms "insect gall"/"galhas de insetos", "inventories"/"inventários, and "Brazilian Savanah"/"Cerrado. We found 32 papers, 16 of them with data on the associated fauna. We used the Flora do Brasil 2020FLORA DO BRASIL 2020. http://floradobrasil.jbrj.gov.br. (last access in 20/Dec/2020).
http://floradobrasil.jbrj.gov.br... website to verify botanical names and plant endemisms. We also looked for data on plant uses in the site Useful Tropical Plants 2014USEFUL TROPICAL PLANTS 2014. Available on: http://tropical.theferns.info. Accessed in: 20.December.2020.
http://tropical.theferns.info... .

We organized tables, according to the level of plant identification: species - Table 1, genus - Table 2, and family - Table 3. These tables include the following data: host plant, galled organ, gall-inducer, associated fauna, food habit, locality and reference. Whenever the name of host plant species was updated, we presented the original name in brackets after the reference.

We counted the number of gall morphotypes only for host plant species. We compared morphotypes in the same plant species when recorded by different authors to avoid repeated counting. We adopted this procedure only when gall illustrations were available.

Concerning the guilds of the associated fauna, we kept the term "inquiline" as used in the original publications, although we recognize problems in its use, since it includes cecidophages, kleptoparasites, and inquilines. However, original data are insufficient to allow re-categorization.

Results

We found records of the associated fauna in 163 gall morphotypes, 94 plant species and 37 plant families. Fabaceae (N=52) (31.9%), Asteraceae (N=15) (9.2%), Myrtaceae, and Malpighiaceae (N=10 each) (6.1%) had the greatest number of gall morphotypes with records of the associated fauna (Table 4).

Most records (N=105) (64.4%) were in galls of Diptera, mainly Cecidomyiidae (N=102) (62.6%), but galls of Hemiptera, Lepidoptera, Hymenoptera, Coleoptera, and Thysanoptera also hosted secondary dwellers (Table 5), Hemiptera were the second most common gall-inducers, but with very low percentage (4.3% only). Leaf galls had the most records (N=117) (71.8%), followed by stem galls (N=43) (26.4%). Galls on buds, spines and reproductive structures also hosted secondary dwellers. Some galls were induced in two plant organs or more (Table 6).

Parasitoids were the most frequent guild, being reported in 147 gall morphotypes (90.2%). They were followed by successors, inquilines, and predators, reported in 13 (8.0%), 12 (7.4%) and three (1.8%) gall morphotypes, respectively, showing that these guilds were infrequent (Table 7).

Parasitoids were represented by 12 Hymenopteran families. Among them, Eulophidae, Eurytomidae, Torymidae, and Encyrtidae were the most frequent, with records in 41gall morphotypes (29.7% of the parasitized morphotypes), 20 (13.6%), 14 (9.5%) and 12 (8.2%), respectively.

Sucessors included insects of three orders (Coleoptera, Diptera and Hymenoptera), as well as other arthropods (Acari, Araneae, and Collembola); inquilines included insects of seven orders (Coleoptera, Diptera, Hemiptera, Hymenoptera, Lepidoptera, Psocoptera, and Thysanoptera), and Diplopoda, whereas predators were the least diverse, being represented by Pseudoscorpiones and Diptera; all of these taxa were recorded in few gall morphotypes (from 5 to 1) (Table 8).

Concerning the taxonomic knowledge, only four species, Anthonomus vis Clark, 1992 (Coleoptera), Meunieriella spinosa Urso-Guimarães, 2019URSO-GUIMARÃES, M.V. 2019. Two new species of the tribe Alycaulini (Diptera: Cecidomyiidae) from Brazil. Fla Entomol 101 603-610. (Diptera), Salina celebensis (Schäffer, 1898), and Seira mendoncae Bellini & Zeppelini, 2008 (Collembola); and five genera, Camptoneuromyia Felt, 1908, Clinodiplosis Kieffer, 1895, Lestodiplosis Kieffer, 1894 (Cecidomyiidae), and Fiebrigella Duda, 1921 (Chloropidae), and Polyxenus Latreille, 1802 were identified. All other records were at suprageneric levels.

We found 36 host plant genera with records of the associated fauna on undetermined species. They included 24 plant families and totaled at most 55 gall morphotypes (Table 2). Among plant families, five were represented only by undetermined species, namely: Chrysobalanaceae, Loranthaceae, Lythraceae, Meliaceae, and Metteniusaceae. Therefore, they were not included in the Table 1. Adding them, the number of host plant families with records of associated fauna rises to 42. Concerning genera data, Arrabidaea DC. (Bignoniaceae), Hirtella L. (Chrysobalanaceae), Doliocarpus Rol. (Dilleniaceae), Manihot Mill. and Sebastiania Spreng, (Euphorbiaceae), Emmotum Dsv. ex Ham. (Metteniusiaceae), Struthanthus Mart. (Loranthaceae), Diplusodon Pohl. (Lythraceae), Heteropterys Kunth. and Thryallis L. (Malpighiaceae), Tibouchina Aubl. (Melastomataceae), Guarea F. Allam ex L. and Trichilia P. Browne (Meliaceae), Camponanesia Ruiz et Pav. (Myrtaceae), and Paullinia L. (Sapindaceae) are added, increasing the number of host genera to 108. The following arthropod taxa were recorded as secondary dwellers: Hymenoptera: Braconidae, Chalcididae, Elasmidae, Encyrtidae, Eulophidae, Eurytomidae, Formicidae, Perilampidae, Pteromalidae, Tanaostigmatidae, Torymidae, and Trichogrammatidae; Diptera: Sciaridae and Brachycera; Thysanoptera; Collembola: Salina celebensis, Salina sp. and Seria mendoncae; Acari; Araneae; and Pseudoscorpiones. Among them, Elasmidae, Perilampidae, Tanaostigmatidae, Trichogrammatidae, and Brachycera are added, increasing the richness of parasitoid families from 12 to 16, and including Brachycera in the "inquilines" guild. Records at family level (Table 3) added Acanthaceae, Solanaceae, Tiliaceae and Turneraceae, increasing from 42 to 46 the number of host families with associated fauna.

Multiparasitism was recorded in 23 gall morphotypes (15.6% of the total of parasitized gall morphotypes). The number of parasitoid taxa in the same gall morphotype varied from two to five. The highest numbers were recorded in galls on Byrsonima variabilis (Malpighiaceae), five (Eulophidae, Eupelmidae, Eurytomidae, Ichneumonidae, and Platygastridae) in stem galls and four (Eulophidae, Eurytomidae, Torymidae, and Signiphoridae) in leaf galls. Four taxa of parasitoids (Elasmidae, Eurytomidae, Eulophidae, and Torymidae) were also reported in galls on Doliocarpus sp. (Dilleniacaeae).

Different inquilines - Clinodiplosis sp. (Cecidomyiidae) and Lepidoptera were found in a bud gall on Davilla brasiliana DC. (Dilleniaceae), as well as Polyxenus sp. (Diplopoda) and Psocoptera in a leaf gall on Smilax oblongifolia Pohl ex Griseb (Smilacaceae). Two successors - Seria mendoncae and Salina celebensis (Collembola) were recorded in a leaf gall on Bauhinia brevipes Vogel (Fabaceae); and two predators in a bud gall on Leandra aurea (Cham.) Cogn. (Melastomataceae). Furthermore, 17 gall morphotypes hosted more than one ecological guild: successors + inquilines (N=2), parasitoids + inquilines (N=7), parasitoids + successors (N=5), predators + parasitoids (N=2) and parasitoids + predators + inquilines (N=1).

Almost all recorded plant species are native to Brazil, except Leonotis nepetifolia (L.) R.Br which is naturalized. Among the native species, 29 are endemic to Brazil (30.8%) (Table 1). The endemic plants host secondary dwellers in 50 gall morphotypes. Nine hosts are restricted to the Cerrado: Bauhinia holophylla (Bong.) Steud., Copaifera depilis Dwyer, C. luetzelburgii Harms, C. sabulicola J. Costa & L.P. Queiroz (Fabaceae), Byrsonima starnardii W. R. Anderson, Peixotoa goiana C. E. Anderson (Malpighiaceae), Pleroma candolleanum (Mart. ex DC.) Triana (Melastomataceae), Psidium salutare var. pohlianum (O. Berg.) Laundrum (Myrtaceae) and Ouratea floribunda (A. St-Hil.) Engl. (Ochnaceae), whereas Calliandra macrocalyx Harms (Fabaceae) is restricted to the Caatinga. Nevertheless, this plant species is cited in the present paper, because it was recorded in a transition area between the Cerrado and the Caatinga. The endemic plants host four different ecological guilds: 1) parasitoids of seven Hymenopteran families (Braconidae, Encyrtidae, Eulophidae, Eupelmidae, Eurytomidae, Ichneunomidae, and Platygastridae), 2) successors (Formicidae, Acari, and Coleoptera), 3) predators (Pseudoscorpiones), and 4) inquilines (Lygaeidae: Hemiptera, and Camptoneuromyia sp.: Cecidomyiidae).

Forty-six host plant species are useful and host secondary dwellers in 62 gall morphotypes. Several species have multiple uses, but most (33) (71.7%) are used in carpentry and/or cabinet making, 27 (58.7%) are medicinal and 15 (32.6%) are edible (Table 9). The useful plants host parasitoids of eight families (Braconidae, Encyrtidae, Eulophidae, Eurytomidae, Platygastridae, Pteromalidae, Signiphoridae, and Torymidae), inquilinous Lepidoptera, Hemiptera, and Camptoneuromyia sp. (Cecidomyiidae); and successors (Acari and Collembola).

Data on the associated fauna are distributed in 12 localities of four Brazilian states: Minas Gerais - Tiradentes (Serra de São José - 21⁰04'S and 44⁰08'W) with records in 33 gall morphotypes, Belo Horizonte (Campus Pampulha - 19⁰48'S and 43⁰57'W) with 26, Delfinópolis - 20⁰15'S and 46⁰45'W with seven, and Serra do Cipó - 19⁰12-34'S and 43⁰27-38'W) with one; Goiás - Silvânia (16⁰38'S and 48⁰39'W) with 18, Serra dos Pireneus (15⁰48'S and 48⁰52'W) with 14, Goiânia (16⁰36'S and 49⁰16'W) with 13, Hidrolândia (17⁰00'S and 49⁰12'W) with 13, and Caldas Novas (17⁰42'S and 48⁰38'W) with 4; Bahia - Barreiras (11⁰37'S and 44⁰34'W) with 19 and Caetité (14⁰05'S and 42⁰29'W) with 19; and São Paulo (Altinópolis - 21⁰00'S and 47⁰23'W) with 16.

Discussion

Cintra et al. (2020)CINTRA, F.C.F., ARAÚJO, W S., MAIA, V.C, URSO-GUIMARÃES, M.V., VENÂNCIO, H., ANDRADE, J.F., CARNEIRO, M.A.A., ALMEIDA, W.R. & SANTOS, J.C. 2020. Plant-galling insect interactions: a dataset of host plants and their gall-inducing insects for the Brazilian savannah. Ecology 101. https://doi.org/10.1002/ecy.3149
https://doi.org/10.1002/ecy.3149... recorded a total 968 gall morphotypes in the Brazilian Cerrado. In the present paper, we reported the associated fauna in 163 gall morphotypes, which corresponds to only 16.8% of the total. This low value appears to suggest that the presence of secondary dwellers are not frequent, but we have to consider that from 32 papers, only 50% addressed the associated fauna. The plant families with the greatest richness of secondary dwellers were the same ones pointed out by Cintra et al. (2020)CINTRA, F.C.F., ARAÚJO, W S., MAIA, V.C, URSO-GUIMARÃES, M.V., VENÂNCIO, H., ANDRADE, J.F., CARNEIRO, M.A.A., ALMEIDA, W.R. & SANTOS, J.C. 2020. Plant-galling insect interactions: a dataset of host plants and their gall-inducing insects for the Brazilian savannah. Ecology 101. https://doi.org/10.1002/ecy.3149
https://doi.org/10.1002/ecy.3149... as those with the highest gall richness.

The associated fauna was reported in all known orders of gall-inducing insects: Diptera Hemiptera, Lepidoptera, Hymenoptera, Coleoptera, and Thysanoptera. The majority was found in galls of Cecidomyiidae, the most frequent inducers in the Brazilian Cerrado. Leaf and stem galls supported most records as they are the most galled plant organs. Some galls hosted more than one ecological guild, which emphasizes the importance of gall-inducers as ecosystem engineers.

Parasitoids were the most frequent secondary dwellers, being represented by 12 Hymenopteran families. Among them, Eulophidae, Eurytomidae, Torymidae, and Encyrtidae predominated. In restinga areas of the Atlantic Forest, Maia & Azevedo (2009)MAIA, V.C. & AZEVEDO, M.A.P. 2009. Micro-himenópteros associados com galhas de Cecidomyiidae (Diptera) em Restingas do Estado do Rio deJaneiro (Brasil). Biota Neotrop. 9:151-164. recorded 15 families, almost all represented in the Brazilian Cerrado, except Aphelinidae, Bethylidae, Mymaridae and Scelionidae. On the other hand, Ichneumonidae and Tetracampidae were not recorded by Maia & Azevedo (2009)MAIA, V.C. & AZEVEDO, M.A.P. 2009. Micro-himenópteros associados com galhas de Cecidomyiidae (Diptera) em Restingas do Estado do Rio deJaneiro (Brasil). Biota Neotrop. 9:151-164.. Parasitoids were also reported in other biomes, as in Pantanal (Urso-Guimarães et at. 2016URSO-GUIMARÃES, M.V., CASTELLO, A.C.D., KATAOKA, E.Y. & KOCH, I. 2016. Characterization of entomogen galls from Mato Grosso do Sul, Brazil. Rev Bras Ent 6:25-42., Ascendino & Maia 2018ASCENDINO, S. & MAIA, V. C. 2018. Insects galls of Pantanal areas in the State of Mato Grosso do Sul, Brazil: characterization and occurrence. An Acad Bras Ciênc 90):1543-1564 ), Amazon (Carvalho & Mota 2018CARVALHO, A.N. & MOTA, J.S. 2018. Ocorrência e caracterização de galhas entomógenas em um fragmento florestal em estágio de sucessão ecológica na Amazônia. EntomoBrasilis 11:118-123.), and Caatinga (Costa et al. 2014COSTA, E.C., CARVALHO-FERNANDES, S.P. & SANTOS-SILVA, J. 2014. Galhas entomógenas associadas à Leguminosae do entorno do riacho Jatobá, Caetité, Bahia, Brasil. R. bras. Bioci.12:115-120., Brito et al. 2018BRITO, G.P., COSTA, E.C., CARVALHO-FERNANDES, S.P. & SANTOS-SILVA, J. 2018. Riqueza de galhas de insetos em áreas de Caatinga com diferentes graus de antropização do estado da Bahia, Brasil. Iheringia Zool 108:‍e2018003.), however as a not so diverse guild.

The frequency of successors was similar to that of inquilines, differing from some inventories in Atlantic Forest areas, where inquilines were more frequent than successors (e.g. Maia et al. 2008MAIA, V.C, MAGENTA, M.A.G. & MARTINS, S.E. 2008. Ocorrência e caracterização de galhas de insetos em áreas de restinga de Bertioga (São Paulo, Brasil). Biota Neotrop 8:167-197. http://dx.doi.org/10.1590/S1676-06032008000100020
http://dx.doi.org/10.1590/S1676-06032008... , Maia & Mascarenhas 2017MAIA, V.C. & MASCARENHAS, B. 2017. Insect Galls of the Parque Nacional do Itatiaia (Southeast Region, Brazil). An Acad Bras Ciênc 89:505-575., Maia & Siqueira 2020MAIA, V.C. & SIQUEIRA, E.S. 2020. Insect galls of the Reserva Biológica União, Rio de Janeiro, Brazil. Biota Neotrop. 20(1):e20190758. http://dx.doi.org/10.1590/1676-0611-BN-2019-0758.
http://dx.doi.org/10.1590/1676-0611-BN-2... ). However, other inventories showed similar frequencies between both guilds as in Maia & Carvalho-Fernandes 2016MAIA, 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., Flor et al. 2018. The taxa of inquilinesinquilinous were the same as that reported in the Atlantic Forest (Maia et al. 2008MAIA, V.C, MAGENTA, M.A.G. & MARTINS, S.E. 2008. Ocorrência e caracterização de galhas de insetos em áreas de restinga de Bertioga (São Paulo, Brasil). Biota Neotrop 8:167-197. http://dx.doi.org/10.1590/S1676-06032008000100020
http://dx.doi.org/10.1590/S1676-06032008... , Maia & Mascarenhas 2017MAIA, V.C. & MASCARENHAS, B. 2017. Insect Galls of the Parque Nacional do Itatiaia (Southeast Region, Brazil). An Acad Bras Ciênc 89:505-575., Maia & Siqueira 2020MAIA, V.C. & SIQUEIRA, E.S. 2020. Insect galls of the Reserva Biológica União, Rio de Janeiro, Brazil. Biota Neotrop. 20(1):e20190758. http://dx.doi.org/10.1590/1676-0611-BN-2019-0758.
http://dx.doi.org/10.1590/1676-0611-BN-2... ), except Diplopoda, observed until this moment only in galls from Cerrado areas. Coleoptera, Diptera, and Thysanoptera have been recorded in galls from the Amazon Forest (Maia 2011MAIA, V.C. 2011. Characterization of insect galls, gall makers, and associated fauna of Platô Bacaba (Porto de Trombetas, Pará, Brazil). Biota Neotrop. 11(4):37-53. http://www.biotaneotropica.org.br/v11n4/en/abstract?article+bn00511042011
http://www.biotaneotropica.org.br/v11n4/... ), whereas Trotteria and Camptoneuromyia (Cecidomyiidae), Phoridae, Lepidoptera, Coleoptera, Hemiptera, and Hymenoptera in galls from Pantanal (Urso-Guimarães et al. 2016URSO-GUIMARÃES, M.V., CASTELLO, A.C.D., KATAOKA, E.Y. & KOCH, I. 2016. Characterization of entomogen galls from Mato Grosso do Sul, Brazil. Rev Bras Ent 6:25-42., Ascendino & Maia 2018ASCENDINO, S. & MAIA, V. C. 2018. Insects galls of Pantanal areas in the State of Mato Grosso do Sul, Brazil: characterization and occurrence. An Acad Bras Ciênc 90):1543-1564 ). Nevertheless, we emphasize that inquilines guild has been misunderstood as it includes cecidophages, kleptoparasites and true inquilines (Luz & Mendonça-Júnior 2019LUZ, F.A. & MENDONÇA-JÚNIOR, M.S. 2019. Guilds in insect galls: who is who. Fla Entomol 102: 207-210.). Biological data are needed to relocate them in the correct guild. Successors have been reported in galls from other biomes, as Psocoptera in galls from Amazon Forest (Maia 2011MAIA, V.C. 2011. Characterization of insect galls, gall makers, and associated fauna of Platô Bacaba (Porto de Trombetas, Pará, Brazil). Biota Neotrop. 11(4):37-53. http://www.biotaneotropica.org.br/v11n4/en/abstract?article+bn00511042011
http://www.biotaneotropica.org.br/v11n4/... ) and Caatinga (Brito et al. 2018BRITO, G.P., COSTA, E.C., CARVALHO-FERNANDES, S.P. & SANTOS-SILVA, J. 2018. Riqueza de galhas de insetos em áreas de Caatinga com diferentes graus de antropização do estado da Bahia, Brasil. Iheringia Zool 108:‍e2018003.) and Araneae from the Caatinga (Brito et al. 2018BRITO, G.P., COSTA, E.C., CARVALHO-FERNANDES, S.P. & SANTOS-SILVA, J. 2018. Riqueza de galhas de insetos em áreas de Caatinga com diferentes graus de antropização do estado da Bahia, Brasil. Iheringia Zool 108:‍e2018003.). Predators showed the lowest frequency as in other inventories in Brazil (Maia 2001MAIA, V.C. 2001. The gall midges (Diptera, Cecidomyiidae) from three restingas of Rio de Janeiro State, Brazil. Revta bras. Zooi. 18(2):583-629., Maia et al. 2008MAIA, V.C, MAGENTA, M.A.G. & MARTINS, S.E. 2008. Ocorrência e caracterização de galhas de insetos em áreas de restinga de Bertioga (São Paulo, Brasil). Biota Neotrop 8:167-197. http://dx.doi.org/10.1590/S1676-06032008000100020
http://dx.doi.org/10.1590/S1676-06032008... , Bregonci et al. 2010BREGONCI, J.M, POLYCARPO, P.V. & MAIA, V.C. 2010. Galhas de insetos do Parque Estadual Paulo César Vinha (Guarapari, ES, Brasil). Insect galls of the Parque Estadual Paulo César Vinha (Guarapari, ES, Brazil). Biota Neotrop. 10(1):265-274. http://www.biotaneotropica.org.br/v10n1/en/abstract?inventory+bn01410012010.
http://www.biotaneotropica.org.br/v10n1/... , Maia 2013MAIA, V.C. 2013. Insect galls of São Tomé das Letras (MG, Brazil). Biota Neotrop. 13(4):164-189. http://www.biotaneotropica.org.br/v13n4/pt/abstract?article+bn03213042013
http://www.biotaneotropica.org.br/v13n4/... , Maia & Souza 2013MAIA, V.C. & SOUZA, M.S. 2013. Insect galls of the xeric vegetation of Ilha do Cabo Frio (Arraial do Cabo, RJ, Brazil). Biota Neotrop. 13(3):278-288. http://www.biotaneotropica.org.br/v13n3/en/abstract?inventory+bn02213032013
http://www.biotaneotropica.org.br/v13n3/... , Rodrigues et al. 2014RODRIGUES, A.R., MAIA, V.C. & COURI, M.S. 2014. Insect galls of restinga areas of Ilha da Marambaia, Rio de Janeiro, Brazil. Rev Bras Ent. 58(2):173-197., Maia & Carvalho-Fernandes 2016MAIA, 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.). Pseudoscorpiones and Diptera (Cecidomyiidae and Chloropidae) were the recorded taxa. In the Atlantic Forest, Pseudoscorpiones and Cecidomyiidae have been reported, as well as Formicidae (Maia 2001MAIA, V.C. 2001. The gall midges (Diptera, Cecidomyiidae) from three restingas of Rio de Janeiro State, Brazil. Revta bras. Zooi. 18(2):583-629., Maia et al. 2008MAIA, V.C, MAGENTA, M.A.G. & MARTINS, S.E. 2008. Ocorrência e caracterização de galhas de insetos em áreas de restinga de Bertioga (São Paulo, Brasil). Biota Neotrop 8:167-197. http://dx.doi.org/10.1590/S1676-06032008000100020
http://dx.doi.org/10.1590/S1676-06032008... , Bregonci et al. 2010BREGONCI, J.M, POLYCARPO, P.V. & MAIA, V.C. 2010. Galhas de insetos do Parque Estadual Paulo César Vinha (Guarapari, ES, Brasil). Insect galls of the Parque Estadual Paulo César Vinha (Guarapari, ES, Brazil). Biota Neotrop. 10(1):265-274. http://www.biotaneotropica.org.br/v10n1/en/abstract?inventory+bn01410012010.
http://www.biotaneotropica.org.br/v10n1/... ). The record of Chloropidae is known only in the Cerrado until this moment. Cecidomyiidae have been recorded in galls from the Amazon Forest (Maia 2011MAIA, V.C. 2011. Characterization of insect galls, gall makers, and associated fauna of Platô Bacaba (Porto de Trombetas, Pará, Brazil). Biota Neotrop. 11(4):37-53. http://www.biotaneotropica.org.br/v11n4/en/abstract?article+bn00511042011
http://www.biotaneotropica.org.br/v11n4/... ) and Pantanal (Ascendino & Maia 2018ASCENDINO, S. & MAIA, V. C. 2018. Insects galls of Pantanal areas in the State of Mato Grosso do Sul, Brazil: characterization and occurrence. An Acad Bras Ciênc 90):1543-1564 ) too, Formicidae and Pseudoscorpiones from Pantanal (Ascendino & Maia 2018ASCENDINO, S. & MAIA, V. C. 2018. Insects galls of Pantanal areas in the State of Mato Grosso do Sul, Brazil: characterization and occurrence. An Acad Bras Ciênc 90):1543-1564 ).

Taxonomical knowledge of the secondary dwellers is deficient, as only four species have been identified. Besides, there are five records at the genus level, four represented by Diptera: Camptoneuromyia, Clinodiplosis, Lestodiplosis and Fiebrigella, and one by Diplopoda. Camptoneuromyia comprises only gall inquilines, Clinodiplosis includes inquilinous, predaceous as well as gall-inducing species, Lestodiplosis is exclusively predator, whereas Fiebrigella includes predaceous and parasite species (Gagné & Jaschhof 2017GAGNÉ, R.J. & JASCHHOF, M. 2017. A Catalog of the Cecidomyiidae (Diptera) of the World,4 rd ed. Digital version., Smith et al. 2008SMITH, A.R., WCISLO, W.T. & O`DONNELL, S. 2008. Body Size Shapes Caste Expression, and Cleptoparasitism Reduces Body Size in the Facultatively Eusocial Bees Megalopta (Hymenoptera: Halictidae). J Insect Behav 21:394-406.).

Records of secondary dwellers in insect galls on undetermined plants did not allow us to establish the number of gall morphotypes, since we cannot know whether these morphotypes corresponded to others already recorded in identified species. However, we considered these records as they increased the number of host plant families and genera, as well as the richness of parasitoid and inquilines.

Multiparasitism was observed in 23 gall morphotypes. The fact that two or more parasitoid species attack the same host suggests that they can act together to control the gall-inducer population. Furthermore, multiparasitism can be associated with hyperparasitism, as showed by Maia & Monteiro, 1999MAIA, V.C. & S MONTEIRO, R.F. 1999. Espécies cecidógenas (Diptera, Cecidomyiidae) e parasitoides (Hymenoptera) associados a Guapira opposita (Vell.) Reitz. (Nyctaginaceae) na restinga da Barra de Maricá, Rio de Janeiro. Revta bras Zool.16(2):483-487.. However, hyperparasitism has not yet been recorded in the Cerrado. The presence of two or more guilds in the same gall morphotype exemplifies how the associated fauna can compose complex food webs.

Endemic and useful plants host a diverse fauna of secondary dwellers. Such interactions add ecological importance to these arthropods as they can favor the host plants, acting in the control of the population of the gall-inducers (e.g. parasitoids and predators) or can damage the plants even more in the case of phytophagous dwellers.

Although the Cerrado partially or totally covers 15 states in Brazil (Ribeiro & Walter 2008RIBEIRO, J.F. & WALTER, B.M.T. 2008. As principais fitofisionomias do bioma Cerrado. In S.M. Sano, S.P. Almeida & J.F. Ribeiro (eds). Cerrado: ecologia e flora. Embrapa, Brasília, BR, p.151-212.), records of the associated fauna are restricted to four states: Minas Gerais, Goiás, Bahia, and São Paulo, showing that the current information is punctual and limited to a small fraction of the Cerrado`s territorial extension. The surveyed states correspond to those with research groups in cecidology.

Conclusion

A low percentage of the gall morphotypes from the Brazilian Cerrado hosted secondary dwellers. These galls were found on 94 plant species of 37 families. Other records on undetermined plant species increased the number of plant families to 46. The host families with the greatest number of records were the same with the highest richness of insect galls.

Most arthropod fauna were recorded in galls of Cecidomyiidae (Diptera), and on leaves, the predominant galling-insect and the most frequent galled organ. Parasitoids were the most frequent dwellers; among them, Eulophidae and Eurytomidae predominated as in other Brazilian biomes. All arthropod orders reported in the present study were also reported as part of the associated fauna in other Brazilian biomes, except Diplopoda. The taxonomic knowledge of these dwellers is very deficient as in the rest of our country.

Records of secondary dwellers of galls in endemic and useful plants add ecological and economic importance to the associated arthropods as they can favor or damage the host.

Data are restricted to MG, GO, BA and SP, the same states where there are cecidologists. This is the first overview of the fauna associated with insect galls in a Brazilian biome. Studies in other biomes are necessary to consolidate the current knowledge in our country.

Acknowledgments

To Conselho Nacional de Desenvolvimento Científico e Tecnológico by financial support (VCM - Proc. 301481/2017-2, BGS - Proc. 154199/2020-6).

References

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