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Are Fabaceae the principal super-hosts of galls in Brazil?

Abstract

We surveyed 58 scientific articles published between 1987 and 2018 to evaluate the representative nature of the Fabaceae as hosts of insect galls in Brazil, and to gain a better understanding of the interactions between gall-inducing insects and plants and the evolutionary ecology of those insects and their plant hosts. A total of 438 gall morphotypes were reported as being generated by gall-inducing insects on 178 Fabaceae host species belonging to five subfamilies Caesalpinioideae (22 genera and 79 spp.), Cercidoideae (1 genus and 11 spp.), Detarioideae (6 genera and 17 spp.), Dialioideae (2 genera and 2 spp.), and Papilionoideae (26 genera and 69 spp.). The plant host genera demonstrating the greatest richness of gall-inducing insects were Inga, Bauhinia, and Copaifera; the super-host species were Copaifera langsdorffii, Bauhinia brevipes, and Copaifera sabulicola. Most of the galls were observed on leaves; they were mostly globoid, green, glabrous, isolated, and unilocular. The principal gall inducers belonged to Cecidomyiidae; the associated fauna was represented by Collembola, Coleoptera, Diptera, Formicidae, Hemiptera, Hymenoptera, Lepidoptera, Pseudoscorpionida, and Thysanoptera. Fabaceae are the principal super-hosts of galls and one of the most diverse families of angiosperms in Brazil, aggregating evidences for the hypotheses of floristic richness and taxon size.

Key words
Cecidomyiidae; cerrado; insect-plants interactions; Leguminosae; super-host

INTRODUCTION

Galls are complex structures that develop through interactions between host plants and inducing organisms. Plant cells may undergo hypertrophy due to abnormal differentiation in response to both mechanical and chemical inductors, resulting in the characteristic growths that shelter gall-inducing insects (Raman 2007RAMAN A. 2007. Insect-induced plant galls of India: unresolved questions. Curr Sci 92(6): 748-757.). Different groups of organisms can induce galls, including acarids, nematodes, and fungi, although insects are the most frequent group (Mani 1964MANI MS. 1964. Ecology of Plant Galls. Junk, The hague, 434 p.).

Insect gall-inducers generally demonstrate greater degrees of host specificity than most other phytophagous taxa (Carneiro et al. 2009CARNEIRO MAA, BORGES RAX, ARAÚJO APA & FERNANDES GW. 2009. Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, Minas Gerais, Brasil. Rev Bras Entomol 53(4): 570-592.). When a given gall-inducing insect interacts with more than one plant species, those plants are generally phylogenetically closely related species (Bourg & Hanson 2014BOURG A & HANSON P. 2014. Host specificity of gall midges (Diptera: Cecidomyiidae) on ten species of Inga (Fabaceae). In: Fernandes GW & Santos JC (Eds), Neotropical insect galls. New York: Springer, p. 151-161.).

Gall diversity is intimately linked to plant diversity (Wright & Samways 1998WRIGHT MG & SAMWAYS MJ. 1998. Insect species richness tracking plant species richness in a diverse flora: Gall-insects in the Cape Floristc Region, South Africa. Oecologia 115(3): 427-433., Cuevas-Reyes et al. 2004CUEVAS-REYES P, QUESADA M, HANSON P, DIRZO R & OYAMA K. 2004. Diversity of gall-inducing insects in a Mexican tropical dry Forest: the importance of plant species richness, life forms, host plant age and plant density. J Trop Ecol 92(4): 707-716.), and greater numbers of plant species in a given environment create more ecological niches to be exploited (Wright & Samways 1998WRIGHT MG & SAMWAYS MJ. 1998. Insect species richness tracking plant species richness in a diverse flora: Gall-insects in the Cape Floristc Region, South Africa. Oecologia 115(3): 427-433., Cuevas-Reyes et al. 2004CUEVAS-REYES P, QUESADA M, HANSON P, DIRZO R & OYAMA K. 2004. Diversity of gall-inducing insects in a Mexican tropical dry Forest: the importance of plant species richness, life forms, host plant age and plant density. J Trop Ecol 92(4): 707-716., Mendonça Júnior 2007CUEVAS-REYES P, QUESADA M, HANSON P, DIRZO R & OYAMA K. 2004. Diversity of gall-inducing insects in a Mexican tropical dry Forest: the importance of plant species richness, life forms, host plant age and plant density. J Trop Ecol 92(4): 707-716.). Additionally, plant families (or genera) with greater numbers of species will host greater richnesses of gall-inducing insects than plant taxa with smaller numbers of species (Gonçalves-Alvim & Fernandes 2001GONÇALVES-ALVIM SJ & FERNANDES GW. 2001. Comunidades de insetos galhadores (Insecta) em diferentes fitofisionomias do cerrado em Minas Gerais, Brasil. Rev Bras Zool 18(Supl 1): 289-305., Veldtman & Mcgeoch 2003VELDTMAN R & MCGEOCH MA. 2003. Gall-forming insect species richness along a non-scleromorphic vegetation rainfall gradient in South Africa: the importance of plant community composition. Austral Ecol 28(1): 1-13.). Plant taxa that host the greatest numbers of associated gall-inducing insects are known as super-hosts (Fernandes & Price 1988FERNANDES GW & PRICE PW. 1988. Biogeographical gradients in galling species richness: tests of hypotheses. Oecologia 76(2): 161-167., Veldtman & Mcgeoch 2003VELDTMAN R & MCGEOCH MA. 2003. Gall-forming insect species richness along a non-scleromorphic vegetation rainfall gradient in South Africa: the importance of plant community composition. Austral Ecol 28(1): 1-13., Espírito-Santo & Fernandes 2007ESPÍRITO-SANTO MM & FERNANDES GW. 2007. How many species of gall-inducing insects are there on earth, and where are there? Ann Entomol Soc Am 100(2): 95-99.). In spite of a general consensus concerning the existence of plant groups that are more susceptible to gall induction, the ecological mechanisms and selective pressures which influence that pattern have yet to be sufficiently explained.

Among the plant families with the greatest richness of host species in the neotropical region is Fabaceae (Leguminosae) (Gagné 1994GAGNÉ RJ. 1994. The gall midges of the Neotropical Region. Ithaca: Cornell University Press, 364 p.). Fabaceae represent the third-largest angiosperm family, with 770 genera and approximately 19,500 species distributed among the subfamilies Caesalpinioideae, Cercidoideae, Detarioideae, Dialioideae, Duparquetioideae, and Papilionoideae (LPWG 2013LPWG - LEGUME PHYLOGENY WORKING GROUP. 2013. Towards a new classification system for legumes: Progress report from the 6th International Legume Conference. S Afr J Bot 89: 3-9., 2017). The Fabaceae comprise also the largest plant family in Brazil, with wide distribution and an estimated 2,834 species distributed throughout the Amazon Forest, Atlantic Forest, Caatinga, Cerrado, Pampa, and Pantanal phytogeographical domain (BFG 2015BFG – THE BRAZIL FLORA GROUP. 2015. Growing knowledge: An overview of seed plant diversity in Brazil. Rodriguésia 66(4): 1085-1113.).

The Fabaceae are among the most highly valued plants throughout the world (Queiroz 2009QUEIROZ LP. 2009. Leguminosas da Caatinga. Feira de Santana: Universidade Estadual de Feira de Santana; Associação Plantas do Nordeste, 443 p., LPWG 2017LPWG - LEGUME PHYLOGENY WORKING GROUP. 2017. A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny. Taxon 66(1): 44-77.). They are sources of human foods (e.g., Phaseolus vulgaris L.); and popular folk medicines (e.g., Glycyrrhiza glabra L.); they serve as forage plants (e.g., Medicago sativa L.); and they provide wood (e.g., Dalbergia nigra [Vell.] Alemão ex Benth.), oils (e.g., Arachis hypogaea L.), resins (e.g., Copaifera multijuga Hayne), and dyes (e.g., Glycine max [L.] Merril) (Polhill & Raven 1981POLHILL RM & RAVEN PH. 1981. Advances in Legume Systematics. Royal Botanic Garden, Kew 1: 425., Lima et al. 1994LIMA HC, CORREIA CMB & FARIAS DS. 1994. Leguminosae. In: MPM de Lima & RR Guedes-Bruni RR (Eds). Reserva Ecológica de Macaé de Cima: Nova Friburgo-RJ: Aspectos Florísticos das Espécies Vasculares. Jardim Botânico do Rio de Janeiro, 1a ed., p. 167-228.).

In spite of the floristic importance of the Fabaceae and their roles as hosts for galling inducers, information concerning the diversity and distribution of those insects and their association with their host species is scattered in the scientific literature. Only a single publication has dealt with gall diversity and associations with plant host species in the Serra Geral Mountains in Caetité, Bahia State, Brazil (Costa et al. 2014aCOSTA EC, CARVALHO-FERNANDES SP & SANTOS-SILVA J. 2014a. Galhas entomógenas associadas à Leguminosae do entorno do riacho Jatobá, Caetité, Bahia, Brasil. R Bras Bioci 12(2): 115-120.). The present study therefore seeks to evaluate the representative nature of Fabaceae as hosts to galls in Brazil, contribute to our taxonomic knowledge of the inducer species and their respective plant hosts, update data concerning the geographic distributions of those plants in Brazil, and provide subsidies for future biological and ecological studies on those themes.

MATERIALS AND METHODS

The occurrence of galls associated with Fabaceae was verified by consulting the Portal de Periódicos da Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Capes), ProQuest, SciELO, Scopus, SPELL, and Springer Science databases, as well as Google Scholar (http://scholar.google.com.br), during the period between August/2017 and July/2018, utilizing the following descriptors: Brazil, Cecidomyiidae, Galls, Fabaceae, and Leguminosae. Only papers published in the period from 1987 to 2018 were considered, because the gall studies became more frequent in Brazil in the early the 1980s (Moreira 2006MOREIRA GRP. 2006. Galhas entomógenas no Brasil: oportunidade de estudo sobre interação inseto-planta. In: Mariath JE & Santos RP (Orgs). Os avanços da botânica no inicio do século XXI do 57° Congresso Nacional de Botânica. Porto Alegre, Sociedade de Botânica do Brasil. p. 532-537.). Undergraduate theses or dissertations were not included in the searches due to the difficulty of encountering fully work.

The articles were organized according to their year of publication and journal, and subsequently classified according to topic (the area(s) of knowledge they best matched) – plant anatomy, ecology, taxonomy and inventory – based on their title and abstract to consider only articles appropriate to the scope of the present research.

To avoid over-counting of the gall morphotypes and their host plant, only gall records that reported the host species were considered; those records that reported only the family, subfamily or genus of host plant were not. The informations about morphotypes found in the compiled papers were standardized following the terminology proposed by Isaias et al. 2013ISAIAS RMS, CARNEIRO RGS, OLIVEIRA DC & SANTOS JC. 2013. Illustrated and annotated checklist of Brazilian gall morphotypes. Neotrop Entomol 42(3): 230-239..

The plant taxa were organized alphabetically based on their Fabaceae subfamilies, genera, and species, following the legume LPWG classification system (LPWG 2017LPWG - LEGUME PHYLOGENY WORKING GROUP. 2017. A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny. Taxon 66(1): 44-77.). The correct orthography and authors’ names were confirmed by consulting the International Plant Name Index (https://www.ipni.org/). The numbers of Fabaceae species per phytogeographical domain and those of the other most diverse angiosperm families in Brazil were obtained by consulting the Flora do Brasil 2020 site (http://reflora.jbrj.gov.br) and the Brazil Flora Group (BFG 2015BFG – THE BRAZIL FLORA GROUP. 2015. Growing knowledge: An overview of seed plant diversity in Brazil. Rodriguésia 66(4): 1085-1113.), respectively. Plant host and morphotype record for more than one vegetation or transition area were counted in each vegetation involved.

RESULTS

A total of 268 articles were published in the scientific literature between 1987 and 2018 concerning the occurrence of galls associated with Fabaceae, of which 58 focused on Brazil. Those articles were published in 26 different scientific periodicals, principally the Biota Neotropica (18.9%), Revista Brasileira de Entomologia (15.5%), and Brazilian Journal of Biology (6.8%); they are listed in Table I.

Table I
Articles concerning galls induced in Leguminosae in Brazil that were published in scientific journals between 1987 and 2018 and indexed on the Portal Platform of Periodicals CAPES (www.periodicos.capes.gov.br)

The first records of insect galls induced on Fabaceae hosts were published by the naturalist Joaquim da Silva Tavares between 1905 and 1925 (Table II). There were significant increases in the numbers of published records after that, especially in the years after 2,000. Current knowledge concerning gall-inducing insects associated with Fabaceae is based on a variety of approaches focusing on plant anatomy (the anatomy and histochemistry of galls), ecology (investigations of ecological factors at the population level), taxonomy (systematics and descriptions of gall-inducing species), and primarily inventories (checklists of gall inducers and their plant hosts) (Table I).

Table II
The first records of gall-inducing insects associated with Fabaceae undertaken by the naturalist J.S. Tavares between 1905 and 1925 (Gagné & Jaschhof 2017GAGNÉ RJ & JASCHHOF M. 2017. A Catalog of the Cecidomyiidae (Diptera) of the World. 4th ed., Digital, 762 p.).

A total of 438 distinct gall morphotypes hosting gall-inducing insects have been recorded in Brazil among 178 species of

Fabaceae belonging to five subfamilies: Caesalpinioideae (22 genera and 79 spp.), Cercidoideae (1 genus and 11 spp.), Detarioideae (6 genera and 17 spp.), Dialioideae (2 genera and 2 spp.), and Papilionoideae (26 genera, and 69 spp.) (Table SI- Supplementary Material, Figs 1, 2).

Figure 1
Insect galls associated on Fabaceae occurring in Brazil. 1-4, Bauhinia pulchella Benth., 5-6, Bauhinia sp., 7-8, Bauhinia acuruana Moric., 9-10, Calliandra macrocalyx Hamrs, 11-12, Copaifera langsdorffii Desf. Images: Tainar Araujo.
Figure 2
Insect galls associated on Fabaceae occurring in Brazil. 13-14, Copaifera langsdorffii Desf., 15-17, Copaifera sabulicola J.A.S. Costa & L.P. Queiroz., 18-21, Mimosa gemmulata Barneby, 22, Mimosa tenuiflora (Willd.) Poir., 23, Senegalia sp., 24, Senegalia langsdorffi (Benth.) Seigler & Ebinger. Images: Tainar Araújo (13-20; 23-24) and Juliana Santos (21-22).

The subfamilies Caesalpinioideae (n=174), Papilionoideae (n=121), and Detarioideae (n=76) hosted the largest numbers of gall types. Inga Mill. (Caesalpinioideae), Machaerium Pers. (Papilionioideae), and Bauhinia L. (Cercidoideae) were the genera demonstrating the greatest host species richness (25, 13, and 11 species, respectively). The plant genera with the greatest richness of galls were Inga, Bauhinia, Copaifera L. (72, 62, 51 morphotypes, respectively) (Table SI). The super-host plant species were: Copaifera langsdorffii Desf. (n=28, Figure 2), Bauhinia brevipes Vogel (n=17), and Copaifera sabulicola J. A. S. Costa & L. P. Queiroz (n=12, Figure 2).

Of the 178 gall-hosting Fabaceae species in this study, 53 are endemic to Brazil, where they occur in all of the country’s phytogeographical domains (Table SI). The greatest richness of galls and host species taxa were observed in the Cerrado phytogeographical domain (n=196 morphotypes/n= 59 spp.), followed by the Atlantic forest (n=89/n=47) and Amazon forest (n= 73/n= 44) (Table III).

Table III
Numbers of Fabaceae taxa hosting galls in different Brazilian phytogeographical domain.

The plant organ having the most galls was the leaf (n=306; with galls appearing on both the adaxial and abaxial faces), followed by the stem (n=102). Most of the gall morphotypes were globoid (32%) (Table IV), green (45%), glabrous (81%), isolated (78%), and contained only a single larval chamber (80%) (Table SI).

Table IV
Gall morphotypes reported in Fabaceae in Brazil.

The gall-inducing insects identified belonged to the orders Diptera (n= 252), Hymenoptera (n=16), Coleoptera (n=11), Lepidoptera (n=7), Hemiptera (n=5), Acari (n=1), and Thysanoptera (n=1), with Cecidomyiidae (Diptera) being responsible for inducing the most varied gall morphotypes (n= 252) (Table SI). The insect fauna associated with the galls included representatives of the Hymenoptera (n=74), Coleoptera (n=3), Hemiptera (n=3), Collembola (n=2), Lepidoptera (n=2), Thysanoptera (n=2), Diptera (n=1), Formicidae (n=1), and Pseudoscorpionida (n=1) (Table SI).

DISCUSSION

A large number of published (58) papers about galls associated with Fabaceae in Brazil have been published on different journals, and it continues to grow. Three Brazilian journals, Biota Neotropica, Revista Brasileira de Entomologia, and Brazilian Journal of Biology, were the most relevant in terms of number of publications. These were the same scientific journals that published the most papers about Brazilian insect galls during the last 30 years (Araújo 2018ARAÚJO WS. 2018. 30 years of research on insect galls in Brazil: a scientometric review. Pap Avulsos de Zool 58: e20185834.). Different aspects of insect gall induced on Fabaceae have been studied in Brazil, approximately 86% of the publications described the insect gall diversity and their plant hosts at different sites. Other studies that recorded observations of galls on Brazilian Fabaceae had as their focused included papers on plant anatomy, ecology, and taxonomy; these papers represented 13.7% of the papers surveyed (Table I).

The Fabaceae host a wide variety of gall morphotypes in different Brazilian phytogeographical domains, including the Caatinga (Carvalho-Fernandes et al. 2012, Alcântara et al. 2017ALCÂNTARA JA, SOUZA EB & BRAGA PET. 2017. Ocorrência e caracterização de galhas em duas áreas do noroeste do Ceará, Brasil. Natureza on line 15(1): 33-40., Brito et al. 2018BRITO GP, COSTA EC, CARVALHO-FERNANDES SP & SANTOS-SILVA J. 2018. Riqueza de galhas de insetos em áreas de caatinga com diferentes graus de antropização do estado da Bahia, Brasil. Iheringia. Sér Zool 108: e2018003.), Atlantic forest (Fernandes & Negreiros 2006FERNANDES GW & NEGREIROS D. 2006. A comunidade de insetos galhadores da RPPN Fazenda Bulcão, Aimorés, Minas Gerais, Brasil. Lundiana 7(2): 111-120., Maia & Oliveira 2010MAIA VC & OLIVEIRA JC. 2010. Galhas de insetos da Reserva Biológica Estadual da Praia do Sul (Ilha Grande, Angra dos Reis, RJ). Biota Neotrop 10(4): 228-237., Maia & Silva 2016MAIA VC & SILVA LO. 2016. Insect galls of Restinga de Marambaia (Barra de Guaratiba, Rio de Janeiro, RJ). Braz J Biol 76(3): 787-795.), Pantanal (Julião et al. 2002JULIÃO GR, AMARAL MEC & FERNANDES GW. 2002. Galhas de insetos e suas plantas Hospedeiras no Pantanal Sul-Mato-Grossense. Naturalia 27: 47-74.), and Amazon forest (Maia 2011MAIA VC. 2011. Characterization of insect galls, gall makers, and associated fauna of Platô Bacaba (Porto de Trombetas, Pará, Brazil). Biota Neotrop 11(4): 37-53., Almada & Fernandes 2011ALMADA ED & FERNANDES GWA. 2011. Insetos indutores de galhas em florestas de terra firme e reflorestamentos com espécies nativas na Amazônia Oriental, Pará, Brasil. Bol Mus Para Emílio Goeldi Cienc Nat 6(2): 163-196.), with the highest number of plant host species (n=59) and distinct gall morphotypes (n=196) being found in Cerrado (Table IV). That gall richness reflects the high number of Fabaceae species encountered in the Cerrado phytogeographical domain (ca. 1,263) (BFG 2015BFG – THE BRAZIL FLORA GROUP. 2015. Growing knowledge: An overview of seed plant diversity in Brazil. Rodriguésia 66(4): 1085-1113.). However, these numbers for relative diversity of gall morphotypes and host plant species could be an artifact of sampling due to the known diversity of galls in Brazil is largely based on studies undertaken in Cerrado phytogeographical domain.

The great majority of host plants were identified to species (n=178); this is a reflection of the relatively large number of taxonomists studying legumes in Brazil, and many of the voucher specimens are of good quality.

Among the six subfamilies currently recognized for the Fabaceae, five host gall-inducing insects in Brazil – Caesalpinioideae, Cercidoideae, Detarioideae, Dialioideae, and Papilionoideae. Duparquetioideae, the only subfamily not recorded hosting galls in that country, is monospecific, and its single species (Duparquetia orchidacea Baill.) is native to tropical Africa (Lewis et al. 2005LEWIS G, SCHRIRE B, MACKINDER B & LOCK M. 2005. Legumes of the world. Royal Botanical Gardens, Kew, 577 p.).

The genus showing the greatest gall richness was Inga. That taxon comprises a large number of species (ca. 300) widely distributed in the neotropical region, with representatives present from one end of the humid tropical zone to the other (from Mexico to Uruguay), as well as in the Greater and Lesser Antilles (Pennington 1997PENNINGTON TD. 1997. The genus Inga botany. Royal Botanic Gardens, Kew, 844 p.). Brazil is estimated to have 132 species of Inga, of which 51 are endemic (BFG 2015BFG – THE BRAZIL FLORA GROUP. 2015. Growing knowledge: An overview of seed plant diversity in Brazil. Rodriguésia 66(4): 1085-1113.). A significant number of species of that genus are widely distributed – favoring their association with gall-inducing insects.

Copaifera langsdorffii stands out among super-host Fabaceae species in Brazil, especially in Cerrado vegetation (Fernandes et al. 1998, Costa et al. 2010COSTA FV, FAGUNDES MF & NEVES FS. 2010. Arquitetura da planta e diversidade de galhas associadas à Copaifera langsdorffii (Fabaceae). Austral Ecol 20(1): 9-17., Luz et al. 2012LUZ GR, FERNANDES GW, SILVA JO, NEVES FS & FAGUNDES M. 2012. Galhas de insetos em habitats xérico e mésico em região de transição Cerrado Caatinga no norte de Minas Gerais, Brasil. Neotrop Biol Conserv 7(3): 171-187.). Twenty eight gall morphotypes have been recorded on that species (e.g., Gonçalves-Alvim & Fernandes 2001GONÇALVES-ALVIM SJ & FERNANDES GW. 2001. Comunidades de insetos galhadores (Insecta) em diferentes fitofisionomias do cerrado em Minas Gerais, Brasil. Rev Bras Zool 18(Supl 1): 289-305., Maia & Fernandes 2004MAIA VC & FERNANDES GW. 2004. Insect galls from Serra de São José (Tiradentes, MG, Brazil). Braz J Biol 64(3a): 423-445., Costa et al. 2010COSTA FV, FAGUNDES MF & NEVES FS. 2010. Arquitetura da planta e diversidade de galhas associadas à Copaifera langsdorffii (Fabaceae). Austral Ecol 20(1): 9-17., Luz et al. 2012LUZ GR, FERNANDES GW, SILVA JO, NEVES FS & FAGUNDES M. 2012. Galhas de insetos em habitats xérico e mésico em região de transição Cerrado Caatinga no norte de Minas Gerais, Brasil. Neotrop Biol Conserv 7(3): 171-187., Santos et al. 2012SANTOS BB, RIBEIRO BA, SILVA TM & ARAUJO WS. 2012. Galhas de insetos em uma área de cerrado sentido restrito na região semi-urbana de Caldas Novas (Goiás, Brasil). Rev Bras Bioc 10(4): 439-445.), and it is considered one of the principal super-hosts of galls throughout the neotropical region (Oliveira & Isaias 2009OLIVEIRA DC & ISAIAS RMS. 2009. Influence of leaflet age in anatomy and possible adaptive values of the gall of Copaifera langsdorffii (Fabaceae: Caesalpinioideae). Rev Biol Tropical 57(1-2): 293-302.).

Galls can be induced on the leaves, stems, buds, branches, flower buds, flowers, and fruits of host plants (Figure 2). Most galls have been observed on leaves (n=306), corroborating the global pattern described by Mani (1964)MANI MS. 1964. Ecology of Plant Galls. Junk, The hague, 434 p.. According to that author, leaves have greater abundances of nutrients and mineral resources than other plant organs, favoring the greater incidence of galls. The second most prevalent plant organ where galls occur is the stem (n=102). Galls were likewise encountered on leaf buds, branches, shoots, inflorescences, flower buds and fruits, although at lower frequencies. A predominance of galls on leaves and stems has also been observed in other plant families, such as Asteraceae, Melastomataceae, and Myrtaceae (Malves & Frieiro-Costa 2012MALVES K & FRIEIRO-COSTA FA. 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., Maia 2013MAIA VC. 2013. Insect galls of São Tomé das Letras (MG, Brazil). Biota Neotrop 13(4): 164-189., 2014, Maia & Carvalho-Fernandes 2016MAIA VC & CARVALHO-FERNANDES SP. 2016. Insect galls of a protected remnant of the Atlantic Forest tableland from Rio de Janeiro State (Brazil). Rev Bras Entomol 60(1): 40-56.).

Most gall morphotypes occur on a single plant organ, but there are records of galls forming on both the leaves and buds of Machaerium nyctitans (Vell.) Benth. (Papilionoideae) and Mimosa melanocarpa Benth. (Caesalpinioideae) (Maia & Mascarenhas 2017MAIA VC & MASCARENHAS B. 2017. Insect Galls of the Parque Nacional do Itatiaia (Southeast Region, Brazil). An Acad Bras Cienc 89: 505-575.).

The galls induced on Fabaceae demonstrate a wide variety of shapes, varying from simple intumescences to complex structures resembling fruits. Nine distinct gall shapes were recorded, with globoid shape being most common (32% of the morphotypes reported) (Table IV). Globoid galls have been the predominant morphotype in all of the inventories undertaken in the neotropical region (Isaias et al. 2013ISAIAS RMS, CARNEIRO RGS, OLIVEIRA DC & SANTOS JC. 2013. Illustrated and annotated checklist of Brazilian gall morphotypes. Neotrop Entomol 42(3): 230-239.).

The insect inducers of gall morphotypes were examined in Brazil; 145 of the 293 were identified to order or family. Representatives of the orders Coleoptera, Diptera, Hymenoptera, Hemiptera, Lepidoptera, and Thysanoptera have been identified as gall-inducing insects, with Cecidomyiidae (Diptera) inducing the most gall morphotypes (n= 252) – similar to the general pattern recorded for the neotropics. Six insect orders have gall-inducing representatives in the neotropics: Diptera, Lepidoptera, Hymenoptera, Coleoptera, Hemiptera, and Thysanoptera. Diptera predominate among them, with more than 1,000 gall morphotypes reported, induced principally by Cecidomyiidae (Maia et al. 2008MAIA VC, MAGENTA MAG & MARTINS SE. 2008. Ocorrência e caracterização de galhas de insetos em áreas de Restinga de Bertioga (São Paulo, Brasil). Biota Neotrop 8(1): 167-197.).

Cecidomyiidae stands out as the principal insect family inducing galls in many Fabaceae species, for example on Andira paniculata Benth. (=Andira vermifuga [Mart.] Benth.) (Santos et al. 2012SANTOS BB, RIBEIRO BA, SILVA TM & ARAUJO WS. 2012. Galhas de insetos em uma área de cerrado sentido restrito na região semi-urbana de Caldas Novas (Goiás, Brasil). Rev Bras Bioc 10(4): 439-445.), Bauhinia brevipes, Calliandra dysantha Benth., Copaifera langsdorffii, Hymenaea courbaril L., Platymiscium floribundum Vogel (Luz et al. 2012LUZ GR, FERNANDES GW, SILVA JO, NEVES FS & FAGUNDES M. 2012. Galhas de insetos em habitats xérico e mésico em região de transição Cerrado Caatinga no norte de Minas Gerais, Brasil. Neotrop Biol Conserv 7(3): 171-187.), Bauhinia acuruana Moric. (Nogueira et al. 2016NOGUEIRA RM, COSTA ECC, CARVALHO-FERNANDES SP & SANTOS-SILVA J. 2016. Insect galls from Serra geral, Caetité, BA, Brazil. Biota Neotrop 16(1): e20150035.), Mimosa tenuiflora (Brito et al. 2018BRITO GP, COSTA EC, CARVALHO-FERNANDES SP & SANTOS-SILVA J. 2018. Riqueza de galhas de insetos em áreas de caatinga com diferentes graus de antropização do estado da Bahia, Brasil. Iheringia. Sér Zool 108: e2018003.), and Mimosa gemmulata Barneby (Vieira et al. 2018VIEIRA LG, NOGUEIRA RM, COSTA EC, CARVALHO-FERNANDES SP & SANTOS-SILVA J. 2018. Insect galls in Rupestrian field and Cerrado stricto sensu vegetation in Caetité, Bahia, Brasil. Biota Neotrop 18(2): e20170402.). Some new species of Cecidomyiidae are responsible for inducing galls in Fabaceae were recently described from Brazil, for example, Lopesia grandis Maia, 2001 on Dalbergia ecastaphyllum (L.) Taub.; Lopesia aldinae Fernandes & Maia, 2010 on Aldina heterophylla Spruce ex Benth.; Lopesia mimosae Maia, 2010 and Lopesia pernambucensis Maia, 2010 on Mimosa hostilis Benth. (=Mimosa tenuiflora); Lopesia chapadensis Garcia & Urso-Guimarães, 2018 on Andira vermifuga (Mart.) Benth. (Maia 2001MAIA VC. 2001. New genera and species of gall midges (Diptera, Cecidomyiidae) from three restingas of Rio de Janeiro State, Brazil. Rev Bras Zool 18(Supl 1): 1-32., Fernandes et al. 2010FERNANDES SPC, MAIA VC & RAFAEL, JA. 2010. Gall midges (Diptera, Cecidomyiidae) associated with Aldina heterophylla Spr. ex Benth. (Fabaceae) from Brazil. Biota Neotrop 10(1): 161-166., Maia et al. 2010MAIA VC, MAGALHÃES H & SANTOS JC. 2010. Two new species of Lopesia Rubsaamen (Diptera, Cecidomyiidae) associated with Mimosa hostilis (Mimosaceae) in Brazil. Rev Bras Entomol 54(4): 578-583., Garcia & Urso-Guimarães 2018GARCIA CA & URSO-GUIMARÃES MV. 2018. Three New Species of Lopesia Rübsaamen (Diptera: Cecidomyiidae) from Brazil. Fla Entomol 101(2): 203-211.).

Sixty-three gall morphotypes observed on Brazilian Fabaceae were found to be inhabited by representatives of the orders Coleoptera, Collembola, Diptera, Formicidae, Hemiptera, Hymenoptera, Lepidoptera, Pseudoscorpionida, and Thysanoptera – composing an associated fauna (Table SI). Those inhabitants can be classified according to their lifestyles as inquilines, predators, or parasitoids that inhabit galls still occupied by the inducer insect, or as successors in galls abandoned by their inducers (and generally decomposing) (Maia et al. 2008MAIA VC, MAGENTA MAG & MARTINS SE. 2008. Ocorrência e caracterização de galhas de insetos em áreas de Restinga de Bertioga (São Paulo, Brasil). Biota Neotrop 8(1): 167-197.).

Parasitoids belonging to the order Hymenoptera in Fabaceae galls are relatively common and diverse, observed to be associated with 74 gall morphotypes. Micro-hymenoptera are the principal parasites of gall-inducing insects, and can be responsible for their mortality (Maia et al. 2008MAIA VC, MAGENTA MAG & MARTINS SE. 2008. Ocorrência e caracterização de galhas de insetos em áreas de Restinga de Bertioga (São Paulo, Brasil). Biota Neotrop 8(1): 167-197.). According to Stone et al. (2002)STONE GN, SCHONROGGE K, ATIKINSON RJ, BELLIDO D & PUJADE-VILLAR J. 2002. The population biology of oak gall waps (Hymenoptera: Cynipidae). Ann Rev Entomol 47: 633-668., approximately 115,000 species of Hymenoptera are found throughout the world, and they have been recorded in the galls of various species of Fabaceae (e.g., Andira paniculata Benth., Copaifera sabulicola, Copaifera luetzelburgii Harms, Copaifera depilis Dwyer) (Santos et al. 2018SANTOS IM, LIMA VP, SOARES MP & CALADO DC. 2018. Insect galls in three species of Copaifera L. (Leguminosae, Caesalpinioideae) occurring sympatrically in a Cerrado area (Bahia, Brazil). Biota Neotrop 18(1): e20170356.).

The Fabaceae are the principal super-hosts of galls in Brazil; they also comprise one of the most highly diverse families of angiosperms in that country, together with Orchidaceae, Asteraceae, Rubiaceae, Melastomataceae, Bromeliaceae, Poaceae, Myrtaceae, Euphorbiaceae, Malvaceae, and Malpighiaceae (Table V). Our results confirm that galling species will increase as the number of recorded host plant species increases and with plant families or genera size, aggregating evidences for the hypotheses of plant species richness (Fernandes & Price 1988FERNANDES GW & PRICE PW. 1988. Biogeographical gradients in galling species richness: tests of hypotheses. Oecologia 76(2): 161-167., Wright & Samways 1998WRIGHT MG & SAMWAYS MJ. 1998. Insect species richness tracking plant species richness in a diverse flora: Gall-insects in the Cape Floristc Region, South Africa. Oecologia 115(3): 427-433., Cuevas-Reyes et al. 2004CUEVAS-REYES P, QUESADA M, HANSON P, DIRZO R & OYAMA K. 2004. Diversity of gall-inducing insects in a Mexican tropical dry Forest: the importance of plant species richness, life forms, host plant age and plant density. J Trop Ecol 92(4): 707-716., Mendonça Júnior 2007) and of taxon size (Cornell 1985CORNELL HV. 1985. Local and regional richness of Cynipine gall wasps on California oaks. Ecology 66(4): 1247-1260., Gonçalves-Alvim & Fernandes 2001GONÇALVES-ALVIM SJ & FERNANDES GW. 2001. Comunidades de insetos galhadores (Insecta) em diferentes fitofisionomias do cerrado em Minas Gerais, Brasil. Rev Bras Zool 18(Supl 1): 289-305., Veldtman & Mcgeoch 2003VELDTMAN R & MCGEOCH MA. 2003. Gall-forming insect species richness along a non-scleromorphic vegetation rainfall gradient in South Africa: the importance of plant community composition. Austral Ecol 28(1): 1-13., Mendonça Júnior 2007). In spite of the already large number of insect inductors of galls known to be associated with the Fabaceae, that total could easily increase with more intensive studies.

Table V
Richness of galls associated with the principal angiosperm families in Brazil.

The co-evolution of Fabaceae species and gall-inducing insects has given rise to a wide variety of associations that still require in-depth biological and ecological examination, for relatively little is currently known about their ontogeny, structure, chemistry (e.g., Isaias 1998ISAIAS RMS. 1998. Galhas entomógenas em Machaerium (Leguminosae-Papilionoidae): anatomia e histoquímica. Tese de doutorado. Universidade de São Paulo., Isaias et al. 2006ISAIAS RMS, OLIVEIRA DC, CHRISTIANO JCS & SOARES GLG. 2006. Reações de defesas químicas e estruturais de Lonchocarpus muehlbergianus Hassl. (Fabaceae) a ação do galhador Euphalerus ostreoides Crawf. (Hemiptera: Psyllidae). Rev Bras Bot 29(4): 657-667., Oliveira & Isaias 2009OLIVEIRA DC & ISAIAS RMS. 2009. Influence of leaflet age in anatomy and possible adaptive values of the gall of Copaifera langsdorffii (Fabaceae: Caesalpinioideae). Rev Biol Tropical 57(1-2): 293-302., 2010OLIVEIRA DC & ISAIAS RMS. 2010. Redifferentiation of leaflet tissues during midrib gall development in Copaifera langsdorffii (Fabaceae). S Afr J Bot 76(2): 239-248., Sá et al. 2009SÁ CEM, SILVEIRA FAO, SANTOS JC, ISAIAS RMS & FERNANDES GW. 2009. Anatomical and developmental aspects of leaf galls induced by Schizomyia macrocapillata Maia (Diptera: Cecidomyiidae) on Bauhinia brevipes Vogel (Fabaceae). Rev Bras Bot 32(2): 319-327., Suzuki et al. 2015SUZUKI AYM, BEDETTI CS & ISAIAS RMS. 2015. Detection and distribuition of cell growth regulators and celulose microfibrils during the development of Lopesia sp. galls on Lonchocarpus cultratus (Fabaceae). Botany 93(7): 435-444., Costa et al. 2018COSTA EC, CARNEIRO RGS, SANTOS-SILVA J & ISAIAS RMS. 2018. Biology and development of galls induced by Lopesia sp. (Diptera: Cecidomyiidae) on leaves of Mimosa gemmulata (Leguminosae: Caesalpinioideae). Aust J Bot 66(2): 161-172., Nogueira et al. 2018NOGUEIRA RM, COSTA EC, SANTOS-SILVA J & ISAIAS RMS. 2018. Structural and histochemical profile of Lopesia sp. Rubsaamen 1908 pinnula galls on Mimosa tenuiflora (Willd.) Poir. In a Caatinga environment. Hoehnea 45(2): 231-239.) or ecology (Almeida et al. 2006ALMEIDA CIM, LEITE GLD, ROCHA SL, MACHADO MML & MALDONADO WCH. 2006. Fenologia e artrópodes de Copaifera langsdorffii Desf. no Cerrado. Rev Bras Plantas Med 8(2): 64-70.). The synthesis provided in the current study concerning the established interactions between gall-inducing insects and the Fabaceae can provide the basis for new studies and new perspectives on their evolutionary ecology.

ACKNOWLEGMENTS

This work was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (Proc. no 406111/2016-2), by the Universidade do Estado da Bahia (Propublic/UNEB - Termo Outorga 06/2017) and by the Fundação de Amparo à Pesquisa do Estado da Bahia (Proc. no 9648/2015). JSS is grateful to Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro for her research grant (E-26/202.501/2019). The authors would like to thank anonymous reviewers for suggestions on the manuscript and Douglas Daly (NYBG) for English revision.

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SUPPLEMENTARY MATERIAL

Table SI.

Publication Dates

  • Publication in this collection
    10 Aug 2020
  • Date of issue
    2020

History

  • Received
    23 Oct 2018
  • Accepted
    11 Feb 2019
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