Insect galls of the Brazilian Cerrado: associated fauna

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 2020. 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..


Introduction
Galls are a classic example of niche construction (Gilbert 2009). They represent discrete microhabitats that support relatively closed communities of specialist inhabitants (Shorthouse & Rohfritsch 1992, Williams 1994, Crespi et al. 1997. 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. 2008). 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. 1987, Stone & Schonrogge 2003. 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 2010).
In Brazil, there are several inventories of insect galls in Cerrado areas, mainly in the states of Minas Gerais and Goiás (Araújo et al. 2014). The Cerrado is the second largest phytogeographical domain of Brazil, occupying an area of ca. 2 million km 2 (23% of the national territory) (Oliveira & Ratter 2002) and one of the phytogeographical domains with the highest plant diversity in the world, containing over 12,000 species (Klink & Machado 2005, Mendonça et al. 2008. Furthermore, the Cerrado is considered one of the world`s biodiversity hotspots and a priority conservation area (Myers et al. 2000). Cintra et al. (2020) 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) 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. 2007). This valuable role of gall-inducers as ecosystem engineers (Cornelissen et al. 2016) 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 2020 website to verify botanical names and plant endemisms. We also looked for data on plant uses in the site Useful Tropical Plants 2014.
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 recategorization.
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).
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), Table 2. Data on arthropods associated with insect galls in the Brazilian Cerrado: host plant (identification at genus level), gall-inducer, host organ, secondary dweller, ecological guild, locality, and reference. Ecological guild: (Inq) inquiline, (Par) parasitoid, (Suc) successor.    were recorded in a leaf gall on Bauhinia brevipes Vogel (Fabaceae); and two predators in a bud gall on Leandra aurea (Cham.) Cogn.

Host plant Gall-inducer
(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) Cintra et al. (2020) 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) as those with the highest gall richness.

Discussion
The associated fauna was reported in all known orders of gallinducing 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.
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, 1999. 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 2008), 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.