Insect galls on Asteraceae in Brazil: richness, geographic distribution, associated fauna, endemism and economic importance

Galhas de insetos em Asteraceae no Brasil: riqueza, distribuição geográfica, fauna associada, endemismo e importância econômica

Ismael Cividini Flor Alene Ramos Rodrigues Sharlene Ascendino Silva Barbara Proença Valéria Cid Maia About the authors

Abstract:

An overview of insect galls on Asteraceae in Brazil is presented. We used the Web of Science database to find publications about insect galls from 1988 to 2020. We analyzed 88 publications and collected data from 51 of those. A total of 487 gall morphotypes were counted on 157 plant species of 42 genera. This value singled out Asteraceae as the richest plant family in number of gall morphotypes in Brazil. Most morphotypes were recorded in the Atlantic Forest (41%) and Cerrado (30.5%), the most surveyed biomes in Brazil. Baccharis L. supported the greatest gall richness (43.9%), which could be explained by the hypotheses of geographic area and taxon size. Baccharis concinna G.M. Barroso, B. dracunculifolia DC. and B. platypoda DC. were indicated as superhost species. Most galls were induced on stems (52.2%), a pattern known in Asteraceae for gall-inducing Tephritidae and Chloropidae, and extended in the present study to Cecidomyiidae. Most galls were fusiform (42.5%), which can be related to the highest number of gall on stems. Cecidomyiidae (Diptera) were the most frequent inducers, as observed worldwide. The presence of other dwellers - parasitoids, cecidophages, kleptoparasites, and successors - were reported in 8.8% of the gall morphotypes, being parasitoids the most frequent, as found in other Brazilian publications. Most host plants (58%) are endemic to Brazil, 14% are useful and few are vulnerable or endangered (six and four species, respectively). Due to the high host specificity, the gall-inducers associated with these plants can also be considered either endemic, important, vulnerable and/or endangered, respectively.

Keywords:
Gall-inducing insects; insect-plant interaction; Compositae

Resumo:

Um panorama geral das galhas de insetos em Asteraceae no Brasil é apresentado. Usamos a base de dados "Web of Science" para encontrar publicações sobre galhas de insetos de 1988 a 2020. Analisamos 88 publicações no total, porém obtivemos dados de apenas 51. Um total de 487 morfotipos de galhas foi contabilizado em 157 espécies de plantas de 42 gêneros. Este valor indica as Asteraceae como a família botânica mais rica em número de morfotipos de galhas no Brasil. A maioria dos morfotipos foi registrada na Mata Atlântica (41%) e no Cerrado (30.5%), biomas mais investigados no Brasil. Baccharis L. suportou a maior riqueza de galhas (43.9%), o que poderia ser explicado pelas hipóteses de área geográfica e tamanho do táxon. Baccharis concinna G.M. Barroso, B. dracunculifolia DC. E B. platypoda DC. foram indicadas como as espécies super hospedeiras. A maioria das galhas foi induzida em caules (52.2%), um padrão conhecido em Asteraceae para Tephritidae e Chloropidae indutores de galhas, e estendido no presente estudo para Cecidomyiidae. A maioria das galhas foi fusiforme (42.5%), o que pode estar relacionado ao maior número de galhas em caule. Os Cecidomyiidae (Diptera) foram os indutores mais frequentes, como no mundo inteiro. A presença de outros ocupantes - parasitoides, cecidófagos, cleptoparasitas e sucessores - foi assinalada em 8.8% dos morfotipos de galhas, sendo os parasitoides os mais frequentes, como em outras publicações no país. A maioria das plantas hospedeiras são endêmicas do Brasil (58%), 14 são úteis e algumas são vulneráveis ou ameaçadas (seis e quatro, respectivamente). Devido à alta especificidade de plantas hospedeiras, os indutores de galhas associados a estas plantas podem ser considerados endêmicos, de importância econômica, vulneráveis e/ou ameaçados, respectivamente.

Palavras-chave:
Insetos indutores de galhas; interação inseto-planta; Compositae

Introduction

The Asteraceae family presents the largest number of species recorded in the world, totaling 32,581 species (Willis 2017WILLIS, K.J. 2017. State of the world's plants 2017. Report. Royal Botanic Gardens, Kew. https://stateoftheworldsplants.org/ (last acess in 05/01/2021)
https://stateoftheworldsplants.org/...
). This group is found in all continents, except Antarctica, being more common in rural environments than in forests (Anderberg et al. 2007ANDERBERG, A.A., BALDWIN, B.G., BAYER, R.J., BREITWIESER, J., JEFFREY, C., DILLON, M.O., ELDENÄS, P., FUNK, V.A., GARCIA-JACAS, N., HIND, D.J.N., KARIS, P.O., LACK, H.W., NESOM, G., NORDENSTAM, B., OBERPRIELER, C., PANERO, J.L., PUTTOCK, C., ROBINSON, H., STUESSY, T.F., SUSANNA, A., URTUBEY, E., VOGT, R., WARD, J. & WATSON, L.E. 2007. Compositae. In The families and genera of vascular plants (J.W. Kadereit & C. Jeffrey, eds.). Springer, Berlin. p.61-588.). In Brazil, Asteraceae are the third family in species diversity among Angiosperms and in number of endemisms (BFG 2018BFG - The Brazil Flora Group. 2018. Brazilian Flora 2020: innovation and collaboration to meet Target 1 of the Global Strategy for Plant Conservation (GSPC). Rodriguésia 69:1513-1527.) with approximately 289 genera and 2,173 species, of which 71 genera and 1,367 species are endemic (Flora do Brasil 2020FLORA DO BRASIL 2020. Jardim Botânico do Rio de Janeiro. http://floradobrasil.jbrj.gov.br/ (last acess in 29/12/2020)
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), occurring preferentially in open environments, such as savannahs and rupestrian fields (Hind & Miranda 2008HIND, D.J.N. & MIRANDA, E.B. 2008. Lista preliminar da família Compositae na Região Nordeste do Brasil. Royal Botanic Gardens, Kew.).

Insect galls are pathological structures that originate new formations in plant tissues, as a result of mechanical and/or chemical stimulation by insects (Bronner 1992BRONNER, R. 1992. The role of nutritive cells in the nutrition of cynipids and cecidomyiids. In Biology of insect induced galls (J.D. Shorthouse & O. Rohfritsch, eds.). Oxford University Press, New York, p.118-140.). According to Mani (1964)MANI, M.S. 1964. Ecology of Plant Galls. W. Junk, The Hague., galls are induced in any part of a plant, both in vegetative and reproductive organs, providing food and shelter for the larva until its adult stage. Although the entomogenous galls occur in any part of the plants, they are most common on leaves and branches (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 (last access in 21/11/2020)
http://dx.doi.org/10.1590/1676-0611-bn-2...
).

Several plants of economic interest are vulnerable to damage by gall-inducing insects, including ornamental, edible, medicinal and pesticidal plants, as well as species used in carpentry, cosmetics, cabinet making, and agroforestry (Maia 2018MAIA, V.C. 2018. Gall-inducing insects of restinga areas (Atlantic Forest) in Brazil: economic importance. Pap. Avulsos Zool. 58: e20185850.). Most galling pests have been reported from the Old World and North America, whereas few examples are known from South America, especially in plants of the Asteraceae family.

In the last 30 years, several insect gall inventories in different Brazilian phytophysiognomies have been published (Araújo 2018ARAÚJO, W.S. 2018. 30 years of research on insect galls in Brazil: a scientometric review. Pap. Avulsos Zool. 58: e20185834.). Most of them comprise galls on Asteraceae and indicate this family as one of the most important in gall richness. Other families are also important, such as Fabaceae (Santos-Silva & Araújo 2020SANTOS-SILVA, J. & ARAÚJO, T.J. 2020. Are Fabaceae the principal super-hosts of galls in Brazil? An. Acad. Bras. Cienc. 92(2): e20181115.) and Myrtaceae (Maia 2019MAIA, V.C. 2019. Insect galls on Myrtaceae: richness and distribution in Brazilian restingas. Biota Neotrop. 19(1): e20180526. http://dx.doi.org/10.1590/1676-0611-bn-2018-0526 (last acess in 05/01/2021)
http://dx.doi.org/10.1590/1676-0611-bn-2...
). As data are scattered in the literature, the number of host plant species and gall-inducing species are unknown, as well as data on their associated fauna, distribution, endemism, and economic importance.

The main goal of this paper is to present a panoramic view of insect galls on Asteraceae in Brazil. The specific objectives are: (1) to inventory the gall morphotypes on Asteraceae species in Brazil; (2) register the distribution of the galls phytogeographic domains; (3) determine the most frequent morphotype as well as the most attacked plant organ and the presence or absence of pubescence; (4) provide information about the identification of the inducers and the guilds of associated fauna; (5) obtain information about the origin, endemism, status of conservation, and the economic importance of the host plants and their gall inducing species.

Material and Methods

Insect gall scientific articles sampling Brazilian areas published from 1988 until 2020 were analyzed in order to collect information about insect galls on Asteraceae in Web of Science between August, 2020 and October, 2020 (www.periodicos.capes.gov.br). The following descriptors were used: Brazil/Brasil, Galls/Galhas, Insect galls/Galhas de insetos, Gall-inducing insects/Insetos galhadores, Cecidomyiidae, Asteraceae, Compositae. We only considered host plants identified to species level, to avoid overestimating gall morphotypes number.

Botanical names and synonyms were verified in Flora do Brasil (2020)FLORA DO BRASIL 2020. Jardim Botânico do Rio de Janeiro. http://floradobrasil.jbrj.gov.br/ (last acess in 29/12/2020)
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, as well as data on plant origin, geographic distribution and conservation categories (EN - endangered, LC - least concern, NE - not evaluated, NT - near threatened, VU - vulnerable) (IUCN 2020IUCN 2020. The IUCN red list of threatened species. https://www.iucnredlist.org. (last acess in 14/09/2021).
https://www.iucnredlist.org...
). Plant uses were verified using the websites Useful Tropical Plants Database (2014 - http://tropical.theferns.info) and EMBRAPA (https://www.embrapa.br/). The following categories were considered: agroforestry, edible, medicinal and other uses. Phytogeographic domains were retrieved from the original papers or verified in vegetation maps of Brazil (IBGE 2004IBGE 2004. Mapas de biomas e vegetação. http://www.ibge.gov.br/. (last acess in 05/01/2021)
http://www.ibge.gov.br/...
). Host plants that occur exclusively in one single domain were considered as endemic of this domain. The plant species that presented the highest number of galls were considered galls' super-hosts.

Gall shapes were standardized based on Isaias et al. (2013)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(3):230-239., whenever possible. When published data were insufficient for standardization, we kept the terminology of the original papers. To establish the number of gall morphotypes per plant species, we compared gall morphology. Whenever we found galls with similar morphological characterization, but listed as different morphotypes in the same paper, we adopted the author(s)' concept.

In the present study, all records of Cecidomyiidae (Diptera) as gall-inducer were converted in Cecidomyiinae records, since this is the single subfamily of Cecidomyiidae which includes cecidogenous species (Gagné & Jaschhof 2021GAGNÉ, R.J. & JASCHHOF, M. 2021. A catalog of the Cecidomyiidae (Diptera) of the world. 5th EditionDigital. https://www.ars.usda.gov/ARSUserFiles/80420580/Gagne_Jaschhof_2021_World_Cat_5th_Ed.pdf (last acess in 08/01/2021)
https://www.ars.usda.gov/ARSUserFiles/80...
). Concerning the associated fauna, records of inquilines were converted in records of cecidophages and kleptoparasites, according to the criteria proposed by Luz & Mendonça-Júnior (2019)LUZ, F.A. & MENDONÇA-JÚNIOR, M.S. 2019. Guilds in insect galls: who is who. Fla. Entomol. 102(1):207-210..

Results

1. Inventory of galls

We found 88 articles reporting insect galls sampled from Brazilian areas: 64 with gall morphotypes on Asteraceae, 51 with identified host plant species and 24 of them without Asteraceae as hosts. Asteraceae species appear as hosts of insect galls in 34 (31%) of these studies, and this family is indicated as one of the super hosts in 21 inventories. They covered five (83%) Brazilian phytogeographic domains, with the Atlantic Forest and Cerrado the most studied, with 33 and 29 inventories, respectively. The surveys totaled 487 insect gall morphotypes in association with 157 species of 42 genera (Figure 1). Baccharis L. and Mikania Willd. showed the highest number of galled species, 42 (26.7%) and 29 (18.5%), and the greatest richness of galls, 218 (43.9%) and 76 (15.6%) morphotypes, respectively. The super-host plant species were: Baccharis concinna G.M.Barroso (n=18 morphotypes; 3.7%), B. dracunculifolia DC. (n=17; 3.5%), B. platypoda DC. (n=17; 3.5%), B. reticularia DC. (n=17; 3.5%), B. retusa DC. (n=16; 3.3%), B. minutiflora Mart. ex Baker. (n=14; 2.9%), Eremanthus erythropappus (DC.) MacLeish (n=12; 2.5%) and Mikania glomerata Spreng. (n=10; 2.1%) (Supplementary Material).

Figure 1
Galls on Asteraceae in Brazil. a) fusiform gall on leaf of Mikania argyreiae DC.; b) fusiform gall on stem of Vernonia beyrichii Less.; c) globoid gall on leaf of Baccharis conyzoides (Less.) DC.; d) cylindrical gall on leaf of Mikania glomerata Spreng.; e) conical gall on stem of Mikania micrantha Kunth; f) lenticular gall on leaf of Baccharis conyzoides (Less.) DC.; g) rosette gall on lateral bud of Grazielia gaudichaudiana (DC.) R.M.King & H.Rob.; h) globoid gall on apical bud of Baccharis dracunculifolia DC.; and i) fusiform gall with pupal exuvia on Flower-head of Porophyllum ruderale (Jacq.) Cass.

2. Gall richness by phytogeographic domains

The Atlantic Forest was the domain with the highest number of gall morphotypes, 200 (41%), followed by Cerrado with 150 (30.5%), Pampa with five, Pantanal with three and Amazon rainforest with two. Caatinga (dry forest) presented the lowest number of galls, with only one morphotype. Eighty-seven (55%) host plant species were recorded only in the Atlantic Forest, sixty-seven only in the Cerrado (42%), eighty in the Atlantic Forest + Cerrado, one in the Caatinga + Cerrado, and two in the Amazon Forest. Thirty-eight host plant species (24.2%) were more widespread than their galls, 28 were as widespread as their galls and 19 host plant species were reported in phytogeographic domains outside their distribution area according to Flora do Brasil (2020)FLORA DO BRASIL 2020. Jardim Botânico do Rio de Janeiro. http://floradobrasil.jbrj.gov.br/ (last acess in 29/12/2020)
http://floradobrasil.jbrj.gov.br/...
(Table 1), showing that there is still no data on galls for Brazil.

Table 1.
Number of gall morphotypes by genera and species of Asteraceae, and the average number of gall per host plant species in each phytogeographic domain in Brazil.

3. Gall morphotypes

Thirteen distinct gall shapes were found, the most frequent were fusiform (42.5%) and globoid (35.1%) (Figures 1 and 2). The shape of two gall morphotypes was not informed. The most attacked organs were stems (n=254; 52.2%), leaves (n=165; 33.9%), bud galls (n=92; 14.2%) and flower (n=14; 2.8%) (Table 2). Galls on flowers (1.3%) were found only in Atlantic Forest and Cerrado. The majority of the galls were glabrous (58.4%), except in Pantanal where among the three galls found, two presented trichomes. Data on pubescence in 28.2% of the morphotypes (n=102) were not informed by the authors as well as the phytogeographic domains of 132 gall morphotypes. In addition, some of the galls occurred simultaneously in more than one plant organ so that the results shown in table 3 have totals higher than the overall number.

Figure 2
Number of gall morphotypes recorded on Asteraceae species in Brazil. Other morphotypes: rosette, marginal roll, amorphous, discoid*, claviform, ovoid*, spherical*, swelling* and not informed (* morphotypes with terminology not updated).

Table 2.
Number of gall morphotypes per plant organ of Asteraceae species in each phytogeographic domain in Brazil.
Table 3.
Richness of gall morphotypes per order and family of inducing insects.

4. Gall-inducing insects and associated fauna

The inducers belong to four orders: Diptera (64.7%), Lepidoptera (6%), Hemiptera (3.3%) and Coleoptera (2%). Furthermore, inducers of 117 gall morphotypes (24%) were not determined (Table 3). Two families represented Diptera: Cecidomyiidae (61.8%) and Tephritidae (2.9%). Fifteen genera of gall midges have been recorded, most of them (n=12) are represented by a single identified species, except Asphondylia (n=4 species), Liodiplosis (n=3), and Clinodiplosis (n=2). Furthermore, nine genera include undetermined species, highlighting Asphondylia due to its highest richness. Tephritidae were registered in 14 gall morphotypes, with only one inducer identified in species, Tomoplagia rudolphi (Lutz & Lima, 1918) on Vernonanthura polyanthes (Sprengel) Vega & Dematteis.

Associated fauna were found in 43 gall morphotypes (8.8%) on 30 plant species of 15 genera (Table 4). Mikania and Baccharis comprised the highest number of morphotypes with associated fauna (14 and 9, respectively). Four guilds were represented: cecidophages, kleptoparasites, parasitoids, and successors. Among them, parasitoids were the most frequent, found in 29 gall morphotypes on 24 plant species, followed by cecidophages, found in 12 gall morphotypes on 11 plant species, and kleptoparasites in eight morphotypes on three plant species. Successors were the least frequent, being found in six gall morphotypes on six plant species.

Table 4.
Associated fauna of galls on Asteraceae species and their phytogeographic domains of occurrence. (1) Cecidophages, (2) Parasitoids, (3) Kleptoparasites, (4) Successors, (5) not determined guild.

Parasitoids were represented by Hymenoptera of six families, the most frequent being Eulophidae (n=9) and Eurytomidae (n=4). Multiparasitism was reported in six gall morphotypes. Cecidophages were represented by Diptera, Hemiptera, Coleoptera, Lepidoptera, and Thysanoptera. Diptera were the most frequent being found in seven gall morphotypes followed by Coleoptera (n=4), Lepidoptera (n=3), Hemiptera (n=2), and Thysanoptera (n=2). Kleptoparasites were represented by Cecidomyiidae (Diptera), while successors by Formicidae (Hymenoptera) and Collembola. Spiders were recorded in a single gall morphotype, but the authors did not include these organisms in any guild (Silva et al. 2018SILVA, A.R.F., NOGUEIRA, R.M., COSTA, E.C., CARVALHO-FERNANDES, S.P. & SANTOS-SILVA, J. 2018. 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.).

The four guilds were reported only in Atlantic Forest, while only kleptoparasites were not recorded in the Cerrado. In the Caatinga-Cerrado transition and Amazon Forest only one guild was reported, successors and kleptoparasites, respectively. Thirty gall morphotypes hosted associated fauna in the Atlantic Forest, 11 in the Cerrado, one in Amazon Forest, and one in the Caatinga-Cerrado transition.

5. Origin, endemism and economical importance

Regarding the origin of the host plant species, 96.8% (n=152) are native to Brazil, among them 58% (n=91) are endemic to Brazil, 25.3% (n=23) being endemic to the Atlantic Forest, 30.8% to Cerrado and 1.1% to Caatinga (Table 5). Chromolaena ivifolia (L.) R.M.King & Lamp; H.Rob. and Mikania lindleyana DC. were recorded in the Amazon rainforest and Aspilia latissima Malme and Vernonanthura brasiliana (L.) H.Rob. in the Pantanal, species that are native but not endemic. There was no occurrence of Asteraceae in the Caatinga, but one species was recorded in a transition area between Caatinga to Cerrado.

Table 5.
Origin of Asteraceae host species and number of gall morphotypes in Brazil.

Concerning IUNC (2020)IUCN 2020. The IUCN red list of threatened species. https://www.iucnredlist.org. (last acess in 14/09/2021).
https://www.iucnredlist.org...
conservation categories, plant species were classified into: NE: 79.6% (n=125 plants; 392 morphotypes), LC: 7.6% (n=12; 43), NT: 4.5% (n=7; 13), VU: 3.8% (n=6; 30) and EN: 2.5% (n=4; 6). The Cerrado presented the largest number of threatened species (EN, NT and VU), 13, followed by the Atlantic Forest biomes with four (VU).

Among the 157 host plants, only 22 (14%) are economically useful, most being medicinal (59%), 36.3% have agroforestry use and only 18.8% are edible. Furthermore, 54.5% have other uses (Table 6). These plants host 98 gall inducing insects, most of them are Cecidomyiinae (65.3%), followed by Tephritidae (7.1%), Hemiptera (5.1%), Lepidoptera (4%) and Coleoptera (2%). In 16.3% the galling insects were not determined. Eighteen inducers were identified at species level and six at genera level.

Table 6.
The Asteraceae species hosting insect galls in Brazil, their economic importance, and the number of gall inducer morphospecies by host plant.

Discussion

In this study we compiled 487 gall morphotypes on Asteraceae, a higher number than compiled on Fabaceae (n=437) by Santos-Silva & Araújo (2020)SANTOS-SILVA, J. & ARAÚJO, T.J. 2020. Are Fabaceae the principal super-hosts of galls in Brazil? An. Acad. Bras. Cienc. 92(2): e20181115., showing that Asteraceae are the main insect gall hosts in Brazil. Nevertheless, the number of galled species is higher in Fabaceae (n=178) than in Asteraceae (n=157). Although the Cerrado has the largest number of Asteraceae species (n=1,238) (Flora do Brasil 2020FLORA DO BRASIL 2020. Jardim Botânico do Rio de Janeiro. http://floradobrasil.jbrj.gov.br/ (last acess in 29/12/2020)
http://floradobrasil.jbrj.gov.br/...
), the Atlantic Forest presents the highest number of galled plant species, gall morphotypes and articles reporting galls. In a similar study with Fabaceae, Santos-Silva & Araújo (2020)SANTOS-SILVA, J. & ARAÚJO, T.J. 2020. Are Fabaceae the principal super-hosts of galls in Brazil? An. Acad. Bras. Cienc. 92(2): e20181115. reported the greatest gall richness in the Cerrado, while the Atlantic Forest occupied the second place. The highest gall richness of Atlantic Forest and Cerrado can be explained by the fact that these biomes have been more intensely surveyed and additionally they housed the first research centers focusing on gall-inducing insects in Brazil (Universidade Federal de Minas Gerais and Universidade Federal do Rio de Janeiro, respectively) (Araújo et al. 2019ARAÚJO, W.S., FERNANDES, G.W. & SANTOS, J.C. 2019. An overview of inventories of gall inducing insects in Brazil: looking for patterns and identifying knowledge gaps. An. Acad. Bras. Cienc. 91(1): e20180162.).

The genera with the largest number of galled species and gall morphotypes were Baccharis and Mikania. A large number of galls induced by insects have been studied on many species of Baccharis and Mikania (Fernandes et al. 2014FERNANDES, G.W., SILVA, J.O., ESPÍRITO-SANTO, M.M., FAGUNDES, M., OKI, Y. & CARNEIRO, M.A.A. 2014. Baccharis: A Neotropical Model System to Study Insect Plant Interactions. In Neotropical Insect Galls (G.W. Fernandes & J.C. Santos, eds). Springer-Verlag, London, p.193-219.). Both these genera are widely distributed throughout Brazil and they are the richer in species within the Asteraceae family, favoring their association with gall-inducing insects. The hypothesis of geographic area (Southwood 1960SOUTHWOOD, T.R.E. 1960. The abundance of the Hawaiian trees and the number of their associated insect species. Proc. Hawaii Entomol. Soc. 17(2):299-303.) and hypothesis of taxon size (Fernandes 1992FERNANDES, G.W. 1992. Plant family size and age effects on insular gall-forming species richness. Glob. ecol. biogeogr. lett. 2:71-74) could perhaps help explain the greater insect galls richness on Baccharis and Mikania. They predict that taxa with wider geographic distribution and greater species richness have potentially a greater number of associated galling insects than taxa with more restricted distribution and lower species richness. The presence of super-hosts species is common in the Neotropical region; hence contributing to the increase of the local and regional fauna of gall-inducers in the communities (Fernandes et al. 2014FERNANDES, G.W., SILVA, J.O., ESPÍRITO-SANTO, M.M., FAGUNDES, M., OKI, Y. & CARNEIRO, M.A.A. 2014. Baccharis: A Neotropical Model System to Study Insect Plant Interactions. In Neotropical Insect Galls (G.W. Fernandes & J.C. Santos, eds). Springer-Verlag, London, p.193-219.). Baccharis dracunculifolia and B. concinna were also reported by Fernandes et al. (1996)FERNANDES, G.W., CARNEIRO, M.A.A., LARA, A.C.F., ALLAIN, L.A., ANDRADE, G.I., JULIÃO, G., REIS, T.C. & SILVA, I.M. 1996. Galling insects on neotropical species of Baccharis (Asteraceae). Trop. zool. 9(2):315-332. as super-hosts, as well as Mikania glomerata in different inventories in Brazil (Maia 2013MAIA, V.C. 2013. Galhas de insetos em restingas da região sudeste do Brasil com novos registros. Biota Neotrop. 13(1):183-209. http://www.biotaneotropica.org.br/v13n1/en/abstract?inventory+bn01613012013 (last acess in 05/01/2021)
http://www.biotaneotropica.org.br/v13n1/...
, Maia & Proença 2016MAIA, V.C. & PROENÇA, B. 2016. Insect galls on Mikania glomerata (Asteraceae) in an area of Atlantic Forest in Viçosa (Minas Gerais, Brazil). Check List. 12:1988-2026.).

The highest frequency of the fusiform galls in this study differs from the pattern observed in the Neotropical region where conical galls are the most common (Isaias et al. 2014ISAIAS, R.M.S.; OLIVEIRA, D.C.; CARNEIRO, R.G.S. & KRAUS, J.E. 2014. Developmental Anatomy of Galls in the Neotropics: Arthropods Stimuli Versus Host Plant Constraints. In Neotropical Insect Galls (G.W., Fernandes & J.C. Santos, eds.). Springer-Verlag, London, p.15-34.). Santos-Silva & Araújo (2020)SANTOS-SILVA, J. & ARAÚJO, T.J. 2020. Are Fabaceae the principal super-hosts of galls in Brazil? An. Acad. Bras. Cienc. 92(2): e20181115. reported a predominance of globoid galls in Fabaceae. The highest number of fusiform galls in our study can be related to the high number of gall on stems. When compared to leaves, stems are less plastic organs, perhaps not allowing many variations in the gall shape (Valladares et al. 2006VALLADARES, F., SANCHEZ-GOMEZ, D. & ZAVALA, M.A. 2006. Quantitative estimation of phenotypic plasticity: bridging the gap between the evolutionary concept and its ecological applications. J. Ecol. 94:1103-1116.). The predominance of stem galls differ from the pattern of all zoogeographic regions, where most galls are on leaves (Mani, 1964MANI, M.S. 1964. Ecology of Plant Galls. W. Junk, The Hague.). However, the higher number of stem galls in Asteraceae is a pattern already known for some gall-inducing taxa, as Tephritidae (Friedberg 1984FRIEDBERG, A. 1984. Gall tephritidae. In Biology of gall insects (T.N. Ananthakrishmaned, ed.). Oxford & IBH, New Delhi, p.129-167.), Chloropidae (Foote et al. 1993FOOTE, R.H., BLANC, F.L. & NORRBOM, A.L. 1993. Handbook of the fruit flies (Diptera: Tephritidae) of America north of Mexico. Comstock Publishing Associates, Ithaca.), and Lepidoptera (Maia 2006MAIA, V.C. 2006. Galls of Hemiptera, Lepidoptera and Thysanoptera from Central and South America. Publ. Avulsas Mus. Nac. 110:01-24.). In the present study, the last pattern is suggested for gall midges too.

Cecidomyiidae were the most frequent gall-inducers. In fact, they represent the most diverse gall-inducing family in the whole world. They comprise about 6,590 species, about 70% of them being gall-inducing (Gagné & Jaschhof 2021GAGNÉ, R.J. & JASCHHOF, M. 2021. A catalog of the Cecidomyiidae (Diptera) of the world. 5th EditionDigital. https://www.ars.usda.gov/ARSUserFiles/80420580/Gagne_Jaschhof_2021_World_Cat_5th_Ed.pdf (last acess in 08/01/2021)
https://www.ars.usda.gov/ARSUserFiles/80...
). The Asphondylia was the most diverse gall-inducing genus in our study. This genus is speciose, cosmopolitan and easily recognizable and these features could explain its richness (Gagné & Jaschhof 2021GAGNÉ, R.J. & JASCHHOF, M. 2021. A catalog of the Cecidomyiidae (Diptera) of the world. 5th EditionDigital. https://www.ars.usda.gov/ARSUserFiles/80420580/Gagne_Jaschhof_2021_World_Cat_5th_Ed.pdf (last acess in 08/01/2021)
https://www.ars.usda.gov/ARSUserFiles/80...
). Other Diptera families include gall-inducers, as Tephritidae, but in this family, only a small percentage of species (about 10%) exhibits this habit. Nevertheless, most Tephritidae species induce galls on Asteraceae and this is recognised as a worldwide pattern (Freidberg 1984). Most described species of Cecidomyiidae induce galls on Myrtaceae in Brazil (Maia 2019MAIA, V.C. 2019. Insect galls on Myrtaceae: richness and distribution in Brazilian restingas. Biota Neotrop. 19(1): e20180526. http://dx.doi.org/10.1590/1676-0611-bn-2018-0526 (last acess in 05/01/2021)
http://dx.doi.org/10.1590/1676-0611-bn-2...
). Galls of Lepidoptera, Coleoptera and Hemiptera are less frequent than those of Cecidomyiidae, nevertheless, these orders are frequently reported (e.g. Gonçalves-Alvim & Fernandes 2001GONÇALVES-ALVIM, S.J. & FERNANDES, G.W. 2001. Biodiversity of galling insects: historical, community and habitat effects in four neotropical savannas. Biodivers. Conserv. 10:79-98., Maia et al. 2008MAIA, V.C., MAGENTA, M.A.G. & MARTINS, E.M. 2008. Ocorrência e Caracterização de galhas de insetos em áreas de restinga de Bertioga (São Paulo, Brasil). Biota Neotrop. 8(1):167-197. http://www.biotaneotropica.org.br/v8n1/en/abstract?inventory+bn02408012008 (last acess in 05/01/2021)
http://www.biotaneotropica.org.br/v8n1/e...
, Malves & Frieiro-Costa 2012MALVES, K.M. & FRIEIRO-COSTA, F.A. 2012. List of Plants with Galls Induced by Insects from the UNILAVRAS/Boqueirão Biological Reserve, Ingaí, state of Minas Gerais, Brazil. Check List. 8(3):426-431.), but always responsible for few gall morphotypes.

In this study parasitoids were the most frequent guild as in several Brazilian inventories, being represented exclusively by Hymenoptera (e.g. 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(2):118-123., Silva et al. 2018SILVA, A.R.F., NOGUEIRA, R.M., COSTA, E.C., CARVALHO-FERNANDES, S.P. & SANTOS-SILVA, J. 2018. 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., 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 (last access in 21/11/2020)
http://dx.doi.org/10.1590/1676-0611-bn-2...
). In fact, they are considered the most important natural enemies of the gall-inducing insects, not only in Brazil, but also in the world (Gagné 1994GAGNÉ, R.J. 1994. The Gall Midges of the Neotropical Region. Cornell University Press, Ithaca.). Eulophidae and Eurytomidae are families usually cited as parasitoids of gall-inducers in Brazil (e.g. Maia 2001MAIA, V.C. 2001. The gall midges (Diptera, Cecidomyiidae) from three restingas of Rio de Janeiro State, Brazil. Rev. Bras. Zoo. 18(2):583-629., Carvalho-Fernandes et al. 2016CARVALHO-FERNANDES, S.P., ASCENDINO, S., MAIA, V.C. & COURI, M.S. 2016. Diversity of insect galls associated with coastal shrub vegetation in Rio de Janeiro, Brazil. An. Acad. Bras. Ciênc. 88(3):1407-1418., Ribeiro et al. 2019RIBEIRO, 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.). Cecidophages, kleptoparasites and successors are infrequent in inventories, and the insect taxa included in these guilds have been found in Asteraceae as well as in other plant families (e.g. Maia 2001MAIA, V.C. 2001. The gall midges (Diptera, Cecidomyiidae) from three restingas of Rio de Janeiro State, Brazil. Rev. Bras. Zoo. 18(2):583-629., Carvalho-Fernandes et al. 2016CARVALHO-FERNANDES, S.P., ASCENDINO, S., MAIA, V.C. & COURI, M.S. 2016. Diversity of insect galls associated with coastal shrub vegetation in Rio de Janeiro, Brazil. An. Acad. Bras. Ciênc. 88(3):1407-1418., 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 (last access in 21/11/2020)
http://dx.doi.org/10.1590/1676-0611-bn-2...
).

Few studies refer to the origin, endemism and threat category of host plant species associated with galling insects. Among the 88 scientific publications studied, only three presented this information (Maia & Mascarenhas 2017MAIA, V.C. & MASCARENHAS, B. 2017. Insect Galls of the Parque Nacional do Itatiaia (Southeast Region, Brazil). An. Acad. Bras. Ciênc. 89(1):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 (last access in 21/11/2020)
http://dx.doi.org/10.1590/1676-0611-bn-2...
, Santos-Silva & Araújo 2020SANTOS-SILVA, J. & ARAÚJO, T.J. 2020. Are Fabaceae the principal super-hosts of galls in Brazil? An. Acad. Bras. Cienc. 92(2): e20181115.). In our study 50% are endemic and this value is higher when compared to that of Santos-Silva & Araújo (2020)SANTOS-SILVA, J. & ARAÚJO, T.J. 2020. Are Fabaceae the principal super-hosts of galls in Brazil? An. Acad. Bras. Cienc. 92(2): e20181115. for Fabaceae (29%). Furthermore, 17 botanical species are under a threatened category of conservation. Given the accepted high levels of host-inducer specificity (Carneiro et al. 2009CARNEIRO M.A.A., BRANCO C.S.A., BRAGA C.E.D., ALMADA E.D., COSTA M.B.M. & MAIA V.C. 2009. Are gall midge species (Diptera, Cecidomyiidae) host-plant specialists? Rev. Bras. Entomol. 53(3):365-378.), we suggest that gall inducers associated exclusively with endemic hosts are endemic and those associated with threatened plants are also threatened.

Despite the low percentage of useful plants observed in this study, it is important to quantify the diversity of gall inducers, because their presence can cause several damage, such as, plant growth reduction, lower photosynthesis rate and reduced fruits, resulting in economic losses (McCrea et al. 1985McCREA, K.D., ABRAHAMSON, W.G. & WEIS, A.E. 1985. Golden rod ball gall effects on Solidago altissima: 14C translocation and growth. Ecology. 66:1902-1907., Fernandes 1987FERNANDES, G.W. 1987. Gall forming insects: their economic importance and control. Rev. Bras. Entomol. 31(3):379-398., Souza et al. 1998SOUZA, A.L.T., FERNANDES, G.W., FIGUEIRA, J.E.C. & TANAKA, M.O. 1998. Natural history of a gall-inducing weevil Collabismus clitellae (Coleoptera: Curculionidae) and some effects on its host plant Solanum lycocarpum (Solanaceae) in southeastern Brazil. Ann. Entomol. Soc. Am. 91:404-409.). These losses can be increased when more than one galling species occur on the same host, as we observed in 77.2% of the useful species of Asteraceae. Once again, based on species-specificity, we suggest that all Cecidomyiidae related to useful plants can be considered at least potentially of economic importance.

Conclusions

We can conclude that Asteraceae is the main host family of insect galls in Brazil and most morphotypes were reported in the Atlantic Forest and Cerrado. The richest genera in gall morphotypes were also the most widely distributed around Brazil and one of the best represented in number of species. The most attacked plant organ and the most frequent gall morphotype on Asteraceae do not corroborate the pattern observed for the Neotropical region.

The composition of gall inducing insects and fauna associated followed what is already known for the Neotropical region. Due to Cecidomyiidae high level of specificity, they can be considered endemic, useful, vulnerable and/or threatened as well as their host plants.

Finally, this study provides important data on the presence of gall inducing insects in one of the richest families of Angiosperms in Brazil. Such studies are rare in Brazil important to consolidate the current knowledge, and to show the diversity and frequency of these insects in Brazil. They also provide subsidies to other studies such as biogeography and conservation.

Supplementary Material

The following online material is available for this article: Table - Insect galls on Asteraceae species occurring in Brazil.

References

  • ANDERBERG, A.A., BALDWIN, B.G., BAYER, R.J., BREITWIESER, J., JEFFREY, C., DILLON, M.O., ELDENÄS, P., FUNK, V.A., GARCIA-JACAS, N., HIND, D.J.N., KARIS, P.O., LACK, H.W., NESOM, G., NORDENSTAM, B., OBERPRIELER, C., PANERO, J.L., PUTTOCK, C., ROBINSON, H., STUESSY, T.F., SUSANNA, A., URTUBEY, E., VOGT, R., WARD, J. & WATSON, L.E. 2007. Compositae. In The families and genera of vascular plants (J.W. Kadereit & C. Jeffrey, eds.). Springer, Berlin. p.61-588.
  • ARAÚJO, W.S. 2018. 30 years of research on insect galls in Brazil: a scientometric review. Pap. Avulsos Zool. 58: e20185834.
  • ARAÚJO, W.S., FERNANDES, G.W. & SANTOS, J.C. 2019. An overview of inventories of gall inducing insects in Brazil: looking for patterns and identifying knowledge gaps. An. Acad. Bras. Cienc. 91(1): e20180162.
  • BFG - The Brazil Flora Group. 2018. Brazilian Flora 2020: innovation and collaboration to meet Target 1 of the Global Strategy for Plant Conservation (GSPC). Rodriguésia 69:1513-1527.
  • BRONNER, R. 1992. The role of nutritive cells in the nutrition of cynipids and cecidomyiids. In Biology of insect induced galls (J.D. Shorthouse & O. Rohfritsch, eds.). Oxford University Press, New York, p.118-140.
  • CARNEIRO M.A.A., BRANCO C.S.A., BRAGA C.E.D., ALMADA E.D., COSTA M.B.M. & MAIA V.C. 2009. Are gall midge species (Diptera, Cecidomyiidae) host-plant specialists? Rev. Bras. Entomol. 53(3):365-378.
  • CARVALHO-FERNANDES, S.P., ASCENDINO, S., MAIA, V.C. & COURI, M.S. 2016. Diversity of insect galls associated with coastal shrub vegetation in Rio de Janeiro, Brazil. An. Acad. Bras. Ciênc. 88(3):1407-1418.
  • CARVALHO, 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(2):118-123.
  • EMBRAPA (Empresa Brasileira de Pesquisa Agropecuária). 2020. Base de Dados de Pesquisa Agropecuária. https://www.bdpa.cnptia.embrapa.br/consulta/ (last access in 04/12/2020)
    » https://www.bdpa.cnptia.embrapa.br/consulta/
  • FERNANDES, G.W. 1987. Gall forming insects: their economic importance and control. Rev. Bras. Entomol. 31(3):379-398.
  • FERNANDES, G.W. 1992. Plant family size and age effects on insular gall-forming species richness. Glob. ecol. biogeogr. lett. 2:71-74
  • FERNANDES, G.W., CARNEIRO, M.A.A., LARA, A.C.F., ALLAIN, L.A., ANDRADE, G.I., JULIÃO, G., REIS, T.C. & SILVA, I.M. 1996. Galling insects on neotropical species of Baccharis (Asteraceae). Trop. zool. 9(2):315-332.
  • FERNANDES, G.W., SILVA, J.O., ESPÍRITO-SANTO, M.M., FAGUNDES, M., OKI, Y. & CARNEIRO, M.A.A. 2014. Baccharis: A Neotropical Model System to Study Insect Plant Interactions. In Neotropical Insect Galls (G.W. Fernandes & J.C. Santos, eds). Springer-Verlag, London, p.193-219.
  • FLORA DO BRASIL 2020. Jardim Botânico do Rio de Janeiro. http://floradobrasil.jbrj.gov.br/ (last acess in 29/12/2020)
    » http://floradobrasil.jbrj.gov.br/
  • FOOTE, R.H., BLANC, F.L. & NORRBOM, A.L. 1993. Handbook of the fruit flies (Diptera: Tephritidae) of America north of Mexico. Comstock Publishing Associates, Ithaca.
  • FRIEDBERG, A. 1984. Gall tephritidae. In Biology of gall insects (T.N. Ananthakrishmaned, ed.). Oxford & IBH, New Delhi, p.129-167.
  • GAGNÉ, R.J. 1994. The Gall Midges of the Neotropical Region. Cornell University Press, Ithaca.
  • GAGNÉ, R.J. & JASCHHOF, M. 2021. A catalog of the Cecidomyiidae (Diptera) of the world. 5th EditionDigital. https://www.ars.usda.gov/ARSUserFiles/80420580/Gagne_Jaschhof_2021_World_Cat_5th_Ed.pdf (last acess in 08/01/2021)
    » https://www.ars.usda.gov/ARSUserFiles/80420580/Gagne_Jaschhof_2021_World_Cat_5th_Ed.pdf
  • GONÇALVES-ALVIM, S.J. & FERNANDES, G.W. 2001. Biodiversity of galling insects: historical, community and habitat effects in four neotropical savannas. Biodivers. Conserv. 10:79-98.
  • HIND, D.J.N. & MIRANDA, E.B. 2008. Lista preliminar da família Compositae na Região Nordeste do Brasil. Royal Botanic Gardens, Kew.
  • IBGE 2004. Mapas de biomas e vegetação. http://www.ibge.gov.br/ (last acess in 05/01/2021)
    » http://www.ibge.gov.br/
  • 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(3):230-239.
  • ISAIAS, R.M.S.; OLIVEIRA, D.C.; CARNEIRO, R.G.S. & KRAUS, J.E. 2014. Developmental Anatomy of Galls in the Neotropics: Arthropods Stimuli Versus Host Plant Constraints. In Neotropical Insect Galls (G.W., Fernandes & J.C. Santos, eds.). Springer-Verlag, London, p.15-34.
  • IUCN 2020. The IUCN red list of threatened species. https://www.iucnredlist.org (last acess in 14/09/2021).
    » https://www.iucnredlist.org
  • LUZ, F.A. & MENDONÇA-JÚNIOR, M.S. 2019. Guilds in insect galls: who is who. Fla. Entomol. 102(1):207-210.
  • MAIA, V.C. 2001. The gall midges (Diptera, Cecidomyiidae) from three restingas of Rio de Janeiro State, Brazil. Rev. Bras. Zoo. 18(2):583-629.
  • MAIA, V.C. 2006. Galls of Hemiptera, Lepidoptera and Thysanoptera from Central and South America. Publ. Avulsas Mus. Nac. 110:01-24.
  • MAIA, V.C. 2013. Galhas de insetos em restingas da região sudeste do Brasil com novos registros. Biota Neotrop. 13(1):183-209. http://www.biotaneotropica.org.br/v13n1/en/abstract?inventory+bn01613012013 (last acess in 05/01/2021)
    » http://www.biotaneotropica.org.br/v13n1/en/abstract?inventory+bn01613012013
  • MAIA, V.C. 2018. Gall-inducing insects of restinga areas (Atlantic Forest) in Brazil: economic importance. Pap. Avulsos Zool. 58: e20185850.
  • MAIA, V.C. 2019. Insect galls on Myrtaceae: richness and distribution in Brazilian restingas. Biota Neotrop. 19(1): e20180526. http://dx.doi.org/10.1590/1676-0611-bn-2018-0526 (last acess in 05/01/2021)
    » http://dx.doi.org/10.1590/1676-0611-bn-2018-0526
  • MAIA, V.C., MAGENTA, M.A.G. & MARTINS, E.M. 2008. Ocorrência e Caracterização de galhas de insetos em áreas de restinga de Bertioga (São Paulo, Brasil). Biota Neotrop. 8(1):167-197. http://www.biotaneotropica.org.br/v8n1/en/abstract?inventory+bn02408012008 (last acess in 05/01/2021)
    » http://www.biotaneotropica.org.br/v8n1/en/abstract?inventory+bn02408012008
  • MAIA, V.C. & PROENÇA, B. 2016. Insect galls on Mikania glomerata (Asteraceae) in an area of Atlantic Forest in Viçosa (Minas Gerais, Brazil). Check List. 12:1988-2026.
  • MAIA, V.C. & MASCARENHAS, B. 2017. Insect Galls of the Parque Nacional do Itatiaia (Southeast Region, Brazil). An. Acad. Bras. Ciênc. 89(1):505-575.
  • MAIA, 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 (last access in 21/11/2020)
    » http://dx.doi.org/10.1590/1676-0611-bn-2019-0758
  • MALVES, K.M. & FRIEIRO-COSTA, F.A. 2012. List of Plants with Galls Induced by Insects from the UNILAVRAS/Boqueirão Biological Reserve, Ingaí, state of Minas Gerais, Brazil. Check List. 8(3):426-431.
  • MANI, M.S. 1964. Ecology of Plant Galls. W. Junk, The Hague.
  • McCREA, K.D., ABRAHAMSON, W.G. & WEIS, A.E. 1985. Golden rod ball gall effects on Solidago altissima: 14C translocation and growth. Ecology. 66:1902-1907.
  • 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.
  • SANTOS-SILVA, J. & ARAÚJO, T.J. 2020. Are Fabaceae the principal super-hosts of galls in Brazil? An. Acad. Bras. Cienc. 92(2): e20181115.
  • SILVA, A.R.F., NOGUEIRA, R.M., COSTA, E.C., CARVALHO-FERNANDES, S.P. & SANTOS-SILVA, J. 2018. 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.
  • SOUZA, A.L.T., FERNANDES, G.W., FIGUEIRA, J.E.C. & TANAKA, M.O. 1998. Natural history of a gall-inducing weevil Collabismus clitellae (Coleoptera: Curculionidae) and some effects on its host plant Solanum lycocarpum (Solanaceae) in southeastern Brazil. Ann. Entomol. Soc. Am. 91:404-409.
  • SOUTHWOOD, T.R.E. 1960. The abundance of the Hawaiian trees and the number of their associated insect species. Proc. Hawaii Entomol. Soc. 17(2):299-303.
  • THE TROPICAL PLANTS DATABASE. 2020. http://tropical.theferns.info (last acess in 20/03/2020).
    » http://tropical.theferns.info
  • VALLADARES, F., SANCHEZ-GOMEZ, D. & ZAVALA, M.A. 2006. Quantitative estimation of phenotypic plasticity: bridging the gap between the evolutionary concept and its ecological applications. J. Ecol. 94:1103-1116.
  • WILLIS, K.J. 2017. State of the world's plants 2017. Report. Royal Botanic Gardens, Kew. https://stateoftheworldsplants.org/ (last acess in 05/01/2021)
    » https://stateoftheworldsplants.org/

Publication Dates

  • Publication in this collection
    17 Jan 2022
  • Date of issue
    2022

History

  • Received
    25 June 2021
  • Accepted
    30 Nov 2021
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