Insect galls on Myrtaceae : richness and distribution in brazilian restingas

Inventories in Brazilian restingas have been indicating that Myrtaceae are the plant family with the greatest richness of insect galls. A compilation of published data plus new records was elaborated with the aim of stablishing the number of gall morphotypes on this family in this physiognomy of the Atlantic Forest, producing a list of galled species, pointing out the predominant gall features, evaluating the taxonomical knowledge of the gallers, listing the associated fauna, and based on host plant endemisms and monophagy proposing the endemism of some galling species. Myrtaceae harbor 111 morphotypes of insect gall (about 75% induced by Cecidomyiidae, Diptera) on 25 host plant species, 15 endemic. Eugenia L. highlights as the plant genus with the highest number of galled species and gall richness. Leaves are the most galled organ. There is a predominance of globoid and fusiform shapes, green color, glabrous surface and a single internal chamber. The taxonomical data on gallers is deficient as many records have been presented at supraspecific levels. The associated fauna is rich and includes parasitoids, inquilines and predators. Twelve species of Cecidomyiidae, a single species of Curculionidae (Coleoptera) and one species of Eriococcidae (Hemiptera) have been associated exclusively with endemic hosts and then are proposed in the present study as endemic too. The geographical distribution of many galls and respective gallers are restricted to the State of Rio de Janeiro, where most inventories have been carried out. For the first time, Eugeniamyia dispar, previously known from a rural area of Rio Grande do Sul and restinga areas of São Paulo, is recorded in the State of Rio de Janeiro.


Introduction
Restingas are one of the Atlantic Forest phytophysiognomies, which are defined as long strips of marine sandy depositions, dated of Quaternary (Araújo 1992).In the past, they occupied about 80% of the Brazilian coast (Lacerda et al. 1993), but due to human activities, especially property speculation, this physiognomy has been suffering a great loss of area.For this reason, restingas are considered one of the most threatened Atlantic Forest physiognomies.Tthe main formations are found from Bahia (Northeast region) to São Paulo (Southeast region) (Neiman 1989).
Restinga vegetation is adapted to extreme environmental conditions, such as high salinity, low water availability and strong sun radiation (Scarano et al. 2001).Nevertheless, this phytophysiognomy harbors a considerable biological diversity and a great variety of unique vegetal communities (Lacerda et al. 1982, Rizzini 1992) due to the topographic diversity of the environmental conditions (Araújo & Henriques 1984).
Myrtaceae are one of the most species-rich woody plant families in Brazilian restingas (Araújo 2000, Souza & Morin 2008, Lourenço & Barbosa 2012), the second most speciose in the Atlantic Forest biome (Stehman et al. 2009), and the fourth in Brazil (Forzza et al. 2010).In fact, this family is highly representative of a variety of biomes of the Neotropics.
The most speciose taxa of Myrtaceae in Brazilian restingas are Eugenia L. and Myrcia DC. (Giaretta & Peixoto 2015, Martins et al. 2008, Rosario et al. 2005).Both have been also pointed out as the most species-rich genera of Myrtaceae in Brazil with 350 and 260 species, respectively (Landrum & Kawasaki 1997, Sobral et al. 2018) and in the world with 1,038 and 753 species, respectively (Govaerts et al., 2014).
Several insect gall inventories have been conducted in restinga areas, all in the Southeast region of Brazil, mainly in the state of Rio de Janeiro (Angra dos Reis - Maia 2011).These inventories have been showing considerable insect gall diversity and highlighting Myrtaceae as the plant family with the greatest number of galled species and the highest gall richness (Table 1).Such richness probably is related to the hygrothermic stress caused by daily temperature contrasts, humity, wind gusts, strong sun radiation and sandy soil (Monteiro et al. 1994, Maia 2001a, Monteiro et al. 2004).
As the available information about insect galls on Myrtaceae are scattered in several publications, the current knowledge is not consolidated.The present review aims to compile all published data on them, add new records and answer the following questions: 1) How many insect galls have been recorded on Myrtaceae in restingas?, 2) How many species of Myrtaceae are galled in this physiognomy?, 3) Which are the galled species?, 4) How is geographic distribution of these plant species and what is their origin and conservational status?, 5) Which are the galled plant organs?, 6) Which are the most frequent gall features (shape, colour, presence or absence of trichomes, number of internal chamber)?, 7) Which are the galling taxa?, 8) How is the geographic distribution of the galling species?, 9) is there any endangered galler?, and 10) How is the composition of predaceous, inquilinous and parasitoids guilds?.

Material and Methods
A bibliographic survey was done to elaborate a list of insect galls on Myrtaceae in restingas.It was carried out by consulting the database Web of Science using "insect gall" and "restinga" as keywords Additionally, new records of insect galls are provided.They were obtained from surveys carried out in the Parque Natural Municipal Chico Mendes (Rio de Janeiro, RJ), in February, 2016.The park has 10 paths totaling five quilometers.These paths were pursued in the search of galls for two hours by two persons.The hiking method was adopted to allow the observation of a large number of specimens.Galls were photographed as voucher material.
Botanic names were updated and conservational status of all plant species as well as data on plant endemisms were verified, using the site Flora do Brasil (2020).Based on the high specificity of the gallers in relation to the host plants, galling species associated exclusively with endemic plants were proposed as endemic.Similarly, gallers associated exclusively with threatened plants were proposed as threatened too.
Unfortunately, the morphological gall characterization is not standardized in the literature.The fullest descriptions include galled plant organ, gall shape, color, presence or absence of trichomes, and number of internal chamber, but these features were not equally contemplated in the analysed inventories.Some of them offer very parsimoniosy descriptions.Part of the missing features was retrieved based on gall pictures whenever possible.Besides, different authors adopt different terms to refer to the same gall shape.They are listed in the present study.With regard to the gall morphology, published data are not standardized, resulting in not comparable descriptions as well as in information gaps.Furthermore, different terms have been used to describe the same gall shape.A total of 33 terms were retrieved from literature, but several correspond to the same shape: 1) conical = dropshaped = triangular, 2) lenticular = discoid = epidermic = parenchymal, 3) globoid = globose = globular = spherical = spheroid, 4) cylindrical = tubular, 5) fusiform = elliptical, 6) edge leaf roll = marginal leaf roll, 7) leaf roll = total leaf roll = entire leaf roll, 8) rosette = leaves rosette.In the present study, the following terms were adopted: conical, lenticular, globoid, cylindrical, fusiform, marginal leaf roll, leaf roll, and rosette.Other recorded shapes were claviform, spiraled, ovoid, bivalve, star-shaped, pineapple-shaped, biconical, and leaf blade fold.These last terms were retained in this publication.

Results
A total of 111 insect gall morphotypes on 25 plant species of nine genera were accounted (Table 2).This value represents 90.2% of the gall records on Myrtaceae for restinga, as 12 morphotypes were not included as they were associated with six undetermined plant species.Eugenia L. and Myrcia DC. showed the highest number of galled species (ten each) and the greatest gall richness (47 and 34 morphotypes, respectively).The other genera included a single galled species and from one to ten gall morphotypes.Eugenia and Myrcia together harbored about 73.0% of the gall richness.
All host plant species are native, being 15 endemic in Brazil.Among the last, 11 occur exclusively in the Atlantic Forest (Table 2).Concerning the conservational status, six plant species are less concerning, 18 have not been yet evaluated, and one is data deficient (Table 2).
Leaves were the most galled plant organ (about 63.0%), but galls on stems, buds, flowers (flower buds and flower peduncles) and fruits were also recorded (Table 3).The richness of bud and stem galls were similar, about 17.5% and 14.0%, respectively.Fruit and flower galls were rare (each with less than 3%).
The most frequent shapes were conical and globoid (both with 18 morphotypes), fusiform and lenticular (both with 13 morphotypes), and marginal leaf roll (10 morphotypes).The other shapes included from seven to a single morphotype.Green galls predominated (n=55, about 49.5%), but brown, yellowish, reddish, whitish and black galls were also found.Most galls exhibited a single color, whereas few varied in color.Most galls were glabrous (n=85, about 76.6%) and a single morphotype was hairy (0.90%).There is no information about the others.Seventy-four morphotypes were one-chambered (66.67%), eight were multichambered (7.21%) and a single one showed from one to three chambers (0.90%) (Table 3).
Inquilines were recorded in 17 gall morphotypes.They were represented by Diptera, Lepidoptera, Hymenoptera, Coleoptera, Hemiptera, and Thysanoptera.All morphotypes hosted a single inquilinous order, except two of them (1.bud or leaf vein gall on Myrcia splendes, and 2) marginal roll on Neomitranthes obscura).Diptera were found in five gall morphotypes, Lepidoptera and Hymenoptera in three each, Coleoptera and Hemiptera in two each, and Thysanoptera in one.Diptera were represented by Cecidomyiidae (Dasineura tavaresi Maia, 1995 in the municipality of Rio de Janeiro, and Neolasioptera eugeniae in the Parque Municipal Chico Mendes.Furthermore, the globoid gall of stems of Eugenia uniflora is reported for the first time in the State of Rio de Janeiro (it was previously known only in Espírito Santo and the galler is unknown).And finally, the records of star-shaped galls (induced by Cecidomyiidae) and leaf rolls (induced by Thysanoptera) on Myrciaria floribunda are new in the municipality of Rio de Janeiro.
The morphological characterization of galls on Myrtaceae in Brazilian restingas is compiled and presented below in alphabetical order of the host plant species.Data on galled organ, gall shape, color, indumentum, number of internal chamber, galler and other dwellers are presented whenever available.Informations about their geographical distribution in Brazilian restingas are added.

Discussion
In Brazilian restingas, Myrtaceae included from 18.18% to 11.38% of the total number of galled plant species (Table 1 Rio de Janeiro is the most investigated Brazilian State, for this reason, it harbors most records.The geographical distribution of all galled plants is wider than that of the gallers, indicating that these insects can probably have a greater area of occurrence.
Galling species that occur exclusively on endemic plants were proposed as endemic too, based on their specificity of hosts.Concerning the conservational status, the gallers could not be evaluated as data on the host plants are deficient.
The presence of parasitoids, inquilines and predators has been frequently reported in gall inventories, not only in restingas and in Myrtaceae, but also in other ecosystems and plant families (Maia 2001a Gynaikothrips uzeli (Thysanoptera) are known only on Myrtaceae at restingas.These diverse associated fauna highlights the importance of the galling species as ecosystem engineers, as they provide a new niche, the gall, which can be used by several arthropods.
Although restingas are the best studied phytophysiognomy of Brazil, new records were added, as many areas have not yet been studied.
Eugenia L. is the plant genus with the greatest richness of host species and gall morphotypes.Leaves are the most frequent galled organ.Globoid shape, green color, absence of trichomes and a single internal chamber are the predominant gall traits.Many arthropods, mainly insects, have been reported as dwellers of galls, where they play the role of parasitoids, inquilines and predators, highlighting the importance of the gallers as ecosystem engineers.The taxonomical knowledge of the galling species and other dwellers is still deficient.Great efforts are necessary to refine it, involving field trips, rearing, and taxonomist participation.

Table 1 .
Plant families with the highest number of galled species and greatest gall richness in Brazilian restingas.

,
Eugeniamyia Maia, Mendonça & Romanovski, 1997, Jorgenseniella Maia, 2005, Myrciamyia Maia, 1995, Myrciariamyia Maia, 1994, Neomitranthella Maia, 1996, and Stephomyia Rondani, 1840.Dasineura and Stephomyia were the most speciose genera associated with Myrtaceae in Brazilian restingas.Pacholenus pelliceus Boheman, 1836 (Coleoptera) and Tectococcus ovatus Hempel, 1900 (Hemiptera) were the other identified galling species.Concerning the geographic distribution, 12 galling species have been recorded, until this moment, only in restingas of Rio de Janeiro State (Table 4).The other species have a less restricted distribution.Eugeniamyia dispar, previously known from a rural area of Rio Grande do Sul and restinga areas of São Paulo, is recorded for the first time in the State of Rio de Janeiro.The distribution of Neolasioptera eugeniae Maia, 1993 includes restinga areas of RJ and an ombrophilous Forest area of Minas Gerais.Dasineura gigantea Angelo & Maia, 1999 was described from Forest areas of Paraná and Santa Catarina, and later this species was reported in restinga areas of São Paulo.Dasineura myrciariae Maia, 1993 occurs in the states of Rio de Janeiro and Espírito Santo.Jorgenseniella eugeniae Maia, 2005 and Pacholenus

Table 2 .
Galled species of Myrtaceae, their synonyms, common names, origin, distribution in Brazilian phytogeographic domains, conservational status and number of gall morphotypes in restingas.DD -deficient data, LC -less concerning, NE -not evaluated, VU -vulnerable.

Table 3 .
Gall features on Myrtaceae in Brazilian restingas (shape, color, presence or absence of trichomes, number of internal chamber, galled plant organ, galling order and gallers' taxonomical categories).The total number of gall morphotypes varies due to the available information in the literature.The number of the gall morphotypes by host organ is higher than 111, because some galls were recorded in two different plant organs. http://www.scielo.br/bnhttp://dx.doi.org/10.1590/1676-0611-BN-2018-0526

,
Resseliella sp. and Trotteria sp.) and Sciaridae.Lepidoptera included Stenoma annosa (Butler, 1877) (Depressidae) found in two gall morphotypes on Neomitranthes obscura.Stenoma annosa is a free-living species, whose caterpillar feeds on leaves of several Myrtaceae.Eventually, it feeds on galls, causing their complete destruction, which results in the death of the galling species.Besides, other record, but in order category, is known on Psidium cattleianum.Hymenoptera included Eulophidae (Aprostocetus sp. and Tetrastichinae sp.), Formicidae (Leptothorax sp.) and a record n order category.Coleoptera were represented only by Curculionidae, Hemiptera included Coccidae and Membracidae, and Thysanoptera Gynaikothrips uzeli Zimmermann, 1900.Predators were recorded in five gall morphotypes and they included Lestodiplosis sp.(Cecidomyiidae) found in four gall morphotypes, and Novohorus sp.(Olpiidae), a pseudoscorpion found in a single morphotype.Additionally, Bregonci et al. (2010) reported Thysanoptera and Formicidae (Hymenoptera) in galls of Cecidomyiidae on Myrciaria floribunda, but their habits were not informed.Three gall morphotypes are described for the first time on Myrciaria floribunda: lenticular, globoid and rosette galls, all found in the Parque Municipal Chico Mendes (Rio de Janeiro, RJ).New occurrences of gall midges species are provided herein: Eugeniamyia dispar in the State of Rio de Janeiro, Dasineura myrciariae and Myrciariamyia bivalva

Table 1 .
http://www.scielo.br/bnhttp://dx.doi.org/10.1590/1676-0611-BN-2018-0526 (Maia & Fernandes 2004es of the Atlantic Forest, the rates were lower, 0.00% in Semidecidual Seasonal Forest (Flor etal.2018) and Altitude Fields(Coelho et al. 2013), from 3.86% to11.11%inOmbrophilousForest(Maia2014,Maiaetal. 2014 and Maia & Mascarenhas 2017), 8.16% in High Altitude Wetland Forest (Santos et al. 2011), and 9.75% in Tableland Forest (Maia & Carvalho-Fernandes 2015).Furthermore, Myrtaceae were not the plant family with the greatest number of galled species in these physiognomies.This position is occupied by Sapindaceae (in Semidecidual Seasonal Forest -Flor et al. 2018), Asteraceae (in Altitude Fields -Coelho et al. 2013 and Ombrophilous Forest -Maia et al. 2014 and Maia & Mascarenhas 2017), Melastomataceae (Ombrophilous Forest -Maia 2014), Nyctaginaceae (High Altitude Wetland Forest -Santos et al. 2011), and Fabaceae (in Tableland Forest -Maia & Carvalho-Fernandes 2015).The rates of gall morphotypes on Myrtaceae varied from 34.72% to 13.13% of the total number of gall morphotypes in Brazilian restingas (Table 1).In other physiognomies of the Atlantic Forest, these rates were lower, 0.00% in Semidecidual Seasonal Forest (Flor et al. 2018) and Altitude Fields (Coelho et al. 2013), from 6.40% to 10.89% in Ombrophilous Forest (Maia 2014, Maia et al. 2014 and Maia & Mascarenhas 2017), 8.86% in High Altitude Wetland Forest (Santos et al. 2011), and 9.09% in Tableland Forest (Maia & Carvalho-Fernandes 2015).These data revealed that Myrtaceae are an important host plant family mainly in restingas, while in other physiognomies of the Atlantic Forest this family can contribute to the gall richness as in the Ombrophilous Forest, High Altitude Wetland Forest and Tableland Forest or not as in Semidecidual Seasonal Forest and Altitude Fields.Eugenia and Myrcia highlighted as the Myrtaceae genera with the greatest number of galled species and gall morphotypes.Both are important components of the restinga flora, being the best represented genera of Myrtaceae in this physiognomy (Lourenço & Barbosa 2012, Souza & Morim 2008).The hypothesis of taxon size (Fernandes 1992) could explain the greater insect galls richness on Myrtaceae, Eugenia and Myrcia.It predicts that richer taxa have potentially more hosts and, consequently, a greater number of associated galling insects.Leaves have been reported as the most galled plant organ in all regions of the world.This pattern was observed for the first time by Felt 1940 and has been confirmed in several studies (Maia & Fernandes 2004, Santos et al. 2011, Maia & Carvalho-Fernandes 2016, Maia & Mascarenhas 2017), probably because leaves represent an abundant, frequent and predictable resource.Green galls predominated, probably because this is the color of the most frequent galled organ, leaf.Most galls were glabrous and onechambered.These features have been observed as the most frequent in several Brazilian inventories, not only in restingas, but also in other physiognomies of the Atlantic Forest, as well as in other domains phytogeographic(Maia & Fernandes 2004, Santos et al. 2011, Maia & Carvalho-Fernandes 2016, Maia & Mascarenhas 2017).Only 19% of the galling species have been identified in species.These results show how the taxonomical knowledge of the gallers is still incipient.Cecidomyiidae induced most galls as in all other inventories in the world.Among the gall midges genera, Clinodiplosis Kieffer, 1894 and Dasineura Rondani, 1840 have a wide world distribution, while NeolasiopteraFelt, 1908occurs in the Nearctic and Neotropical regions, and the others, Bruggmannia Tavares, 1906, Eugeniamyia Maia, Mendonça & Romanovski, 1997, Jorgenseniella Maia, 2005, Myrciamyia Maia, 1995, Myrciariamyia Maia, 1994, Neomitranthella Maia, 1996, and Stephomyia Rondani, 1840 are exclusively Neotropical.Among them, five have been recorded only in Brazil: Eugeniamyia, Myrciariamyia, Jorgenseniella, Myrciamyia, and Neomitranthella, being the last three restricted to restingas.Clinodiplosis, Dasineura, and Neolasioptera are speciose genera, with 476, 103 and 134 described species, respectively.Bruggmannia, Eugeniamyia, Myrciariamyia, and Stephomyia include 19, 2, 3 and 7 species, respectively.The others are monotypic (Gagné & Jaschhof 2017).Clinodiplosis, Dasineura, and Neolasioptera induce galls on several plant families, whereas most Bruggmannia species occurs on Nyctaginaceae, the other genera are exclusively associated with Myrtaceae (Gagné & Jaschhof 2017).