Occurrence and characterization of entomogenic galls in an area of Cerrado sensu stricto and Gallery forest of the state of Bahia, Brazil

Abstract

We surveyed insect galls in an area of Cerrado sensu stricto and Gallery forest in the municipality of Caetité (BA) to contribute to current knowledge of the local flora and its associated gall-inducing insects. Monthly collections were made between February/2015 and January/2016, totaling 12 field campaigns (involving two or three people and lasting four hours) that followed an established path through the countryside. A total of 63 gall morphotypes were identified on 47 host plant species belonging to 22 families; 17 morphotypes were found in the Gallery forest and 46 in Cerrado vegetation. The plant families showing the greatest gall richness were Leguminosae (n=15), Myrtaceae (n=9), and Asteraceae (n=7). The species with the greatest number of galls was Mimosa gemmulata Barneby (Leguminosae) (n=3). Most galls were observed on leaves (66%) and stems (24%); they were mostly green (49.3%) or brown (26%), with globoid shapes (39.7%) or marginal roll (17.4%), and were unilocular (87%), glabrous (62%) and isolated (89%). Cecidomyiidae (Diptera) were the principal gall-inducing insects. The associated fauna was principally composed of Hymenoptera. Eight plant taxa were recorded for the first time as hosts of galling fauna.

Key words
Cecidomyiidae; plant-insect interactions; Leguminosae; semiarid

INTRODUCTION

Many insect species associate with plants to increase their chances of survival. Those interactions between insect and their host plants can be mutualistic, benefiting both of the associated individuals, or they may benefit only one of the organisms involved – as is the case of parasitism (Price 1991). Insect parasites generally do not kill their host plant, although they may harm them by feeding on vital organs (Begon et al. 2007).

Gall-inducing insects are excellent examples of parasites that induce morphological and anatomical alterations in plant tissues or organs through processes of hyperplasia and hypertrophy (Mani 1964). These processes are stimulated by mechanical or chemical factors originated from the insects (Hori 1992), and can interfere with the flux of the photosynthates and nutrients produced by those plants (Schoonhoven et al. 2005).

Galls, also known as cecidia, provide protection for the immature stages of the inducing insects against abiotic environmental factors such as sunlight excess and water stress as well against natural enemies (Stone and Schönrogge 2003). Galls can occur on essentially all plant organs, from the extremities of their roots to their apical buds, and both on vegetative and reproductive parts – although they are more numerous and diversified on the aerial portions of the plants, especially on leaves (Mani 1964, Maia 2013).

Studies on galls have increased expressively in recent years in Brazil. Most of them regards inventories of gall diversity in different ecosystems (e.g., Araújo et al. 2012, Costa et al. 2014a, b, Nogueira et al. 2016), while others have investigated ecological aspects of gall-inducing insects or described new species (e.g., Maia and Souza 2007, Maia et al. 2010, Maia 2014), as well as the structural and ultrastructural natures of gall tissues (e.g., Arduin and Kraus 2001, Moura et al. 2009, Oliveira and Isaias 2010, Isaias et al. 2011, Suzuki et al. 2015). Additional studies have focused on the importance of galls as bioindicators (Moreira et al. 2007, Oliveira 2009).

Gall inventories have concentrated in the southeastern region of Brazil, with the Cerrado and Atlantic Forest biomes being the most intensively studied (e.g., Fernandes et al. 1996, Gonçalves-Alvim and Fernandes 2001, Maia and Fernandes 2004, Fernandes et al. 2009). Few studies have focused on dryland Caatinga vegetation (Santos et al. 2011, Silva et al. 2011, Carvalho-Fernandes et al. 2012, Costa 2016), the Amazon Forest (Almada and Fernandes 2011, Maia 2011, Silva et al. 2011, Araújo et al. 2012, Julião et al. 2014), and Caatinga-Cerrado ecotones (Costa et al. 2014a, b, Nogueira et al. 2016).

In spite of recent progress, the knowledge on the diversity and distribution of galls in Bahia State is still relatively limited. Most sampling efforts have been concentrated in the southwestern region of the state, with studies in the Gallery forests (Costa 2016), Cerrado (Costa 2016, Nogueira et al. 2016), Caatinga (Santos et al. 2011, Carvalho-Fernandes et al. 2012, Costa 2016), and Caatinga-Cerrado transition zones (Costa et al. 2014a, b, Nogueira et al. 2016). Additionally, five new records of species of Cecidomyiidae were recently reported for that state (Maia 2014). In Caetité only three Cecidomyiidae species are known (Gagné and Jaschhof 2017), Styraxdiplosis caetitensis Tavares, 1915 and Dialeria styracis Tavares, 1918 associated with undetermined species of Styrax (Styracaceae), and Anadiplosis caetetensis Tavares, 1920 in an undetermined species of Mimosoideae (Leguminosae), now Mimosoid clade (LPWG 2017).

This situation is worrisome as the biodiversity of Bahia is increasingly threatened by deforestation for pasture formation, agriculture, civil construction, and the illegal extraction of wood products (Ministério do Meio Ambiente 2002). The conversion of natural environments into urban and agricultural areas leads to the loss and fragmentation of habitats and consequent biodiversity reductions and disruptions of plant-insect interactions (Tabarelli 1998). Previous studies have demonstrated that the richness of entomogenous galls in the interior of forest fragments responds negatively to anthropogenic disturbances, diminishing sharply as biodiversity losses and increasing plant mortality rates impoverish those fragments (Urso-Guimarães et al. 2003, Moreira et al. 2007).

Within that context, we undertook a survey of insect galls and their host plants in an area of Cerrado and Gallery forest vegetation in the municipality of Caetité, Bahia State, Brazil.

MATERIALS AND METHODS

Current study was undertaken along the Jacaraci trail (14°05’18”S, 42°29’56”W, at 1,110 meters a.s.l.) located along the urban border of the municipality of Caetité (BA). The trail is approximately 3 kilometers long and passes through areas of Cerrado sensu stricto vegetation growing on sandy soils with exposed rock outcrops, as well as a Gallery forest along the Riacho Alegre Creek.

Collections were undertaken on a monthly basis between February/2015 and January/2016, totalling 12 field campaigns along the entire extension of the trail. All plant architectures (herbs, shrubs, trees, and vines) visible up to 3 m above the ground were searched for galls involving two or three people and lasting approximately 4 hours each. When encountered, the galls were photographed and classified into morphotypes following Isaias et al. (2013).

Plant voucher specimens were collected in the field and subsequently prepared for herbarium storage at the Laboratório de Botânica of the Departamento de Ciências Humanas, Campus VI at the Universidade do Estado da Bahia. The plants were identified using analytical keys from the specialized literature, as well as by comparisons with herbarium specimens previously identified by specialists and held in the herbaria of the Universidade do Estado da Bahia (HUNEB/Caetité Collection) and Universidade Estadual de Feira de Santana (HUEFS). One voucher of each species was deposited in the HUNEB/Caetité Collection herbarium. The taxon list is organized alphabetically according to family, genus, and species, following the APG IV classification system (2016).

Some of the collected galls were held in plastic pots with moistened paper towels in the Laboratório de Botânica of the Universidade do Estado da Bahia – DCH/Campus VI to allow eclosion of the inducing insects. The remaining galls were examined under a stereomicroscope and any immature forms of the insects were removed for identification and the numbers of chambers in the galls were counted. Any immature or adult insects were stored in 70% ethanol. The identifications of immature forms (without corresponding adult insects) were made by comparisons with insect morphotypes and host plants previously identified in Cerrado vegetation and in Gallery forests. All the examined material was deposited in the Entomological Collection of the Museu Nacional (MNRJ /UFRJ).

RESULTS

We recorded 63 gall morphotypes on 47 host plant species belonging to 22 families in the vegetation along the Jacaraci trail (Table I). Of the total number of galls (63), 17 were observed in the Gallery forest (on 14 plant species of 9 families) and 46 in Cerrado vegetation (on 33 plant species of 16 families). The plant families with the greatest gall richness were Leguminosae (Fabaceae) (n=15), Myrtaceae (n=9), and Asteraceae (n=7). The Leguminosae had the largest number of host species (nine), followed by Myrtaceae and Malpighiaceae (seven and five species, respectively). Bauhinia L. (Leguminosae-Cercidoideae), Mimosa L. (Leguminosae-Caesalpinioideae), Guarea F.Allam. ex L. (Meliaceae), and Eugenia L. (Myrtaceae) were the genera that hosted the greatest number of galls (6, 3, 3, and 3, respectively). The species showing the greatest gall richness was Mimosa gemmulata Barneby, with three associated morphotypes.

TABLE I
Descriptions of the entomogenic galls encountered in areas of Cerrado sensu stric to and Gallery forest along the Jacaraci trail, Caetité, Bahia State, Brazil.v*New record

Family/species	Organ	Face	Shape	Color	Pilosity	Occurrence	Chambers	Inductor insect	Associated fauna	Figure	Vegetation
ACANTHACEAE
Ruellia sp.	Leaf	Adaxial	Globoid	Green	Yes	Isolated	1	Undetermined	Undetermined	1	Cerrado
ANACARDIACEAE
Anacardiaceae Indet.	Leaf	Adaxial	Lenticular	Green	No	Isolated	1	Undetermined	Undetermined	2	Gallery forest
ANNONACEAE
Annona leptopetala (R.E. Fr.) H. Rainer	Leaf	Adaxial	Globoid	Green	No	Isolated	1	Undetermined	Undetermined	3	Cerrado
ASTERACEAE
Asteraceae Indet. 1	Stem	---	Fusiform	Brown	No	Isolated	1	Undetermined	Hymenoptera	4	Cerrado
	Bud	---	Globoid	Green	Yes	Isolated	Various	Undetermined	Undetermined	5	Cerrado
Asteraceae Indet. 2	Leaf	Adaxial	Lenticular	Green	Yes	Isolated	1	Undetermined	Undetermined	6	Gallery forest
Dasyphyllum sp.	Leaf	Adaxial	Marginal roll	Green	Yes	Isolated	1	Undetermined	Undetermined	7	Cerrado
Moquiniastrum sp.	Leaf	Adaxial	Globoid	White	Yes	Grouped	1	Undetermined	Undetermined	8	Cerrado
	Leaf	Adaxial	Marginal roll	Green	Yes	Isolated	1	Cecidomyiidae	Hymenoptera	9	Cerrado
Verbesina macrophylla (Cass.) S.F.Blake	Bud	---	Globoid	Brown	No	Isolated	Various	Cecidomyiidae	Araneae and Lepidoptera	10	Gallery forest
CANNABACEAE
Celtis iguanaea (Jacq.) Sarg.	Leaf	Adaxial	Marginal roll	Green	No	Isolated	1	Undetermined	Undetermined	11	Gallery forest
	Stem	---	Globoid	Brown	No	Isolated	1	Undetermined	Undetermined	12	Gallery forest
CHLOROPHYCEAE
*Kielmeyera tomentosa Cambess.	Leaf	Adaxial	Lenticular	Brown	No	Isolated	1	Undetermined	Undetermined	13	Cerrado
	Leaf	Adaxial	Conical	Green	Yes	Isolated	1	Undetermined	Undetermined	14	Cerrado
COMBRETACEAE
Combretaceae Indet.	Stem	---	Fusiform	Brown	No	Isolated	1	Cecidomyiidae	Undetermined	15	Cerrado
Combretum leprosum Mart.	Leaf	Abaxial	Globoid	Green	No	Isolated	1	Cecidomyiidae	Hymetoptera	16	Cerrado
EUPHORBIACEAE
Euphorbiaceae Indet.	Leaf	Adaxial	Globoid	Green	No	Isolated	1	Undetermined	Undetermined	17	Cerrado
ERYTHROXYLACEAE
Erythroxylaceae Indet.	Leaf	Adaxial	Rosette	Green	Yes	Grouped	Various	Undetermined	Araneae and Hemiptera	18	Cerrado
LEGUMINOSAE – CERCIDOIDEAE
Bauhinia acuruana Moric.	Leaf	Adaxial	Globoid	Green	Yes	Isolated	1	Undetermined	Undetermined	-	Cerrado
	Stem	---	Fusiform	Brown	Yes	Isolated	1	Undetermined	Undetermined	19	Cerrado
Bauhinia pulchella Benth.	Leaf	Adaxial	Leaf fold	Green	No	Isolated	1	Lepidoptera	Undetermined	20	Cerrado
Bauhinia sp.	Leaf	Adaxial	Globoid	Red	Yes	Grouped	1	Lepidoptera	Undetermined	21	Cerrado
	Leaf	Adaxial	Leaf fold	Green	No	Isolated	1	Undetermined	Undetermined	22	Cerrado
	Stem	---	Fusiform	Brown	Yes	Isolated	1	Lepidoptera	Araneae	23	Cerrado
LEGUMINOSAE – CAESALPINIOIDEAE
*Calliandra macrocalyx Harms	Bud	---	Globoid	Green	Yes	Grouped	1	Undetermined	Hemynoptera	24	Cerrado
	Stem	---	Fusiform	Brown	No	Isolated	1	Undetermined	Undetermined	25	Cerrado
Inga bahiensis Benth.	Leaf	Adaxial	Globoid	Red	Yes	Grouped	1	Undetermined	Coleoptera	26	Gallery forest
Mimosa gemmulata Barneby	Leaf	Adaxial	Globoid	Red	Yes	Isolated	1	Cecidomyiidae	Hymetoptera	27	Cerrado
	Stem	---	Fusiform	Brown	No	Isolated	1	Undetermined	Undetermined	28	Cerrado
	Leaf	Adaxial	Globoid	Green	Yes	Isolated	1	Cecidomyiidae	Undetermined	29	Cerrado
Senegalia langsdorffii (Benth.) Seigler & Ebinger	Stem	---	Globoid	Brown	No	Isolated	Various	Undetermined	Undetermined	30	Cerrado
LEGUMINOSAE – DETARIOIDEAE
Copaifera sp.	Leaf	Adaxial	Leaf fold	Green	No	Isolated	1	Cecidomyiidae	Undetermined	31	Galleryforest
Hymenaea martiana Hayne	Leaf	Adaxial	Lenticular	Green	No	Isolated	1	Undetermined	Undetermined	32	Cerrado
MALPIGHIACEAE
Malpighiaceae Indet.1	Leaf	Adaxial	Lenticular	Yellow	Yes	Isolated	1	Undetermined	Undetermined	33	Cerrado
Malpighiaceae Indet. 2	Leaf	Adaxial	Marginal roll	Yellow	No	Isolated	1	Undetermined	Undetermined	-	Cerrado
Malpighiaceae Indet.3	Leaf	Adaxial	Lenticular	Green	Yes	Isolated	1	Undetermined	Undetermined	34	Cerrado
Malpighiaceae Indet.4	Stem	---	Fusiform	Brown	No	Isolated	Various	Undetermined	Undetermined	35	Cerrado
Malpighiaceae Indet.5	Leaf	Adaxial	Rosette	Red	No	Grouped	Various	Thysanoptera	Undetermined	36	Gallery forest
MALVACEAE
Sida sp.	Leaf	Adaxial	Marginal roll	Green	Yes	Isolated	1	Undetermined	Undetermined	37	Gallery forest
MELIACEAE
Guarea sp.	Leaf	Abaxial	Globoid	Brown	No	Isolated	1	Cecidomyiidae	Thysanoptera	38	Gallery forest
	Fruit	---	Globoid	Yellow	No	Isolated	1	Undetermined	Undetermined	39	Gallery forest
	Leaf	Abaxial	Marginal roll	Green	No	Isolated	1	Undetermined	Undetermined	40	Gallery forest
MORACEAE
Moraceae Indet.	Stem	---	Fusiform	Black	No	Isolated	Various	Undetermined	Undetermined	41	Cerrado
	Leaf	Adaxial	Marginal roll	Green	No	Isolated	1	Undetermined	Araneae	42	Cerrado
MYRTACEAE
*Eugenia ligustrina (Sw.) Willd.	Leaf	Adaxial	Marginal roll	Green	No	Isolated	1	Undetermined	Undetermined	43	Cerrado
	Leaf	Adaxial	Lenticular	Black	No	Isolated	1	Undetermined	Undetermined	44	Cerrado
*Eugenia stictopetala Mart. ex DC.	Leaf	Abaxial	Marginal roll	Green	No	Isolated	1	Undetermined	Undetermined	45	Cerrado
Eugenia sp.	Leaf	Adaxial	Lenticular	White	No	Isolated	1	Thysanoptera	Undetermined	46	Cerrado
Myrcia multiflora (Lam.) DC.	Leaf	Adaxial	Conical	Green	No	Isolated	1	Undetermined	Undetermined	-	Cerrado
Myrcia guianensis (Aubl.) DC.	Stem	---	Fusiform	Brown	No	Isolated	1	Undetermined	Undetermined	47	Gallery forest
Myrtaceae Indet.	Stem	---	Globoid	Brown	No	Isolated	1	Undetermined	Undetermined	48	Gallery forest
*Psidium brownianum Mart. ex DC.	Leaf	Abaxial	Globoid	Black	No	Isolated	1	Undetermined	Pseudoescorpionae	49	Cerrado
*Plinia peruviana (Poir.) Govaerts	Bud	---	Globoid	Black	Yes	Isolated	1	Lepidoptera	Undetermined	50	Gallery forest
RUBIACEAE
Rubiaceae Indet.	Leaf	Adaxial	Marginal roll	Green	No	Isolated	1	Undetermined	Araneae and Hemiptera	51	Gallery forest
Randia armata (Sw.) DC.	Stem	---	Fusiform	Brown	No	Isolated	1	Undetermined	Undetermined	52	Gallery forest
RUTACEAE
*Metrodorea mollis Taub.	Leaf	Adaxial	Lenticular	Green	No	Isolated	1	Undetermined	Undetermined	53	Cerrado
SCHOEPFIACEAE
Schoepfiaceae Indet.	Leaf	Adaxial	Marginal roll	Green	No	Isolated	Various	Undetermined	Undetermined	54	Cerrado
SOLANACEAE
Solanaceae Indet.	Bud	---	Globoid	White	Yes	Grouped	1	Undetermined	Hymenoptera	55	Cerrado
	Stem	---	Globoid	White	Yes	Isolated	1	Undetermined	Undetermined	56	Cerrado
TURNERACEAE
Turneraceae Indet.	Stem	---	Globoid	Brown	No	Isolated	1	Undetermined	Hymenoptera	57	Cerrado
VERBENACEAE
*Bouchea agrestis Schauer	Leaf	Adaxial	Globoid	Green	Yes	Isolated	1	Undetermined	Undetermined	58	Cerrado
VOCHYSIACEAE
Qualea parviflora Mart.	Leaf	Adaxial	Amorphous	Green	No	Grouped	1	Undetermined	Undetermined	59	Cerrado
	Leaf	Adaxial	Globoid	Red	Yes	Grouped	1	Cecidomyiidae	Lepidoptera	60	Cerrado

Most of the gall morphotypes were encountered on a single plant organ (81%) of a single host plant; five plant species had galls on both their leaves and stems (11%) (Bauhinia sp., Bauhinia acaruana Moric., Celtis iguanaea (Jacq.) Sarg., Mimosa gemmulata, and Moraceae Indet); two species have galls on their buds and stems (6%) (Asteraceae Indet. and Solanaceae Indet.) or on a leaf and a fruit (2%) (Guarea sp.). The predominant morphotypes were globoid (39.7%), marginal roll (17.4%), fusiform (15.8%), unilocular (87%), glabrous (62%), and occurring isolated (89%). The galls varied in color: green, brown, black, white, yellow, and red. Green was the most prevalent color (49.3%), predominating on leaves (66%), but green galls were also observed on buds and stems. Brown was the second predominant color (26%), being predominately observed on plant stems (24%).

This was the first inventory of galls and their host plants in an area of Gallery forest in Caetité. As such, all records are new for the region. We also recorded the new occurrence of galls on seven Cerrado plant species: Bouchea agrestis Schauer (Fig. 58), Calliandra macrocalyx Harms(Fig. 24-25), Eugenia ligustrina (Sw.) Willd. (Fig. 43-44), Eugenia stictopetala Mart. ex DC. (Fig. 45), Metrodorea mollis Taub.(Fig. 53), Psidium brownianum Mart. ex DC. (Fig. 49), Kielmeyera tomentosa Cambess. (Fig. 13), and on a new plant species in the Gallery forest: Plinia peruviana (Poir.) Govaerts (Fig. 50).

Figure 1-20
Insect galls encountered along the Jacaraci trail in Caetité, Bahia State, Brazil and the associated morphotypes. 1, Ruellia sp., globoid. 2, Anacardiaceae Indet., lenticular. 3, Annona leptopetala (R.E. Fr.) H. Rainer, globoid. 4-5, Asteraceae Indet.1, 4, fusiform, 5, globoid. 6, Asteraceae Indet.2, lenticular. 7, Dasyphyllum sp., marginal roll. 8-9, Moquiniastrum sp., 8, globoid, 9, marginal roll. 10, Verbesina macrophylla (Cass.) S.F. Blake, globoid. 11-12, Celtis iguanaea (Jacq.) Sarg., 11, marginal roll, 12, globoid. 13-14, Kielmeyera tomentosa Cambess., 13, lenticular, 14, conical. 15, Combretaceae Indet., fusiform. 16, Combretum leprosum Mart., globoid. 17, Euphorbiaceae Indet., globoid. 18, Erythroxilaceae Indet., rosette. 19, Bauhinia acuruana Moric., fusiform. 20, Bauhinia pulchella Benth., leaf fold.

Figure 21-44
Insect galls encountered along the Jacaraci trail in Caetité, Bahia State, Brazil and the associated morphotypes. 21-23, Bauhinia sp., 21, globoid, 22, leaf fold, 23, fusiform. 24-25, Calliandra macrocalyx Harms, 24, globoid, 25, fusiform. 26, Inga bahiensis Benth., globoid. 27-29, Mimosa gemmulata Barneby, 27, globoid, 28, fusiform, 29, globoid. 30, Senegalia langsdorffii (Benth.) Seigler & Ebinger, globoid. 31, Copaifera sp., leaf fold. 32, Hymenaea martiana Hayne, lenticular. 33, Malpighiaceae Indet.1, lenticular. 34, Malpighiaceae Indet.3, lenticular. 35, Malpighiaceae Indet.4, fusiform. 36, Malpighiaceae Indet.5, rosette. 37, Sida sp., marginal roll. 38-40, Guarea sp., 38, globoid, 39, globoid, 40, marginal roll. 41-42, Moraceae Indet, 41, fusiform, 42, marginal roll. 43-44, Eugenia ligustrina (Sw.) Willd., 43, marginal roll, 44, lenticular.

Figure 45-60
Insect galls encountered along the Jacaraci trail in Caetité, Bahia State, Brazil and the associated morphotypes. 45, Eugenia stictopetala Mart. ex DC., marginal roll. 46, Eugenia sp., lenticular. 47, Myrcia guianensis (Aubl.) DC., fusiform. 48, Myrtaceae Indet, globoid. 49, Psidium brownianum Mart. ex DC., globoid. 50, Plinia peruviana (Poir.) Govaerts, globoid. 51, Rubiaceae Indet., marginal roll. 52, Randia armata (Sw.) DC., fusiform. 53, Metrodorea mollis Taub., lenticular. 54, Schoepfiaceae Indet., marginal roll. 55-56, Solanaceae Indet., 55, globoid, 56, globoid. 57, Turneraceae Indet., globoid. 58, Bouchea agrestis Schauer, globoid. 59-60, Qualea parviflora Mart., 59, amorphous, 60, globoid.

The gall-inducing insects identified belonged to the orders Diptera (n=9), Lepidoptera (n=4), and Thysanoptera (n=2). The associated fauna included Hymenoptera (n=8), Aranae (n=5), Hemiptera (n=2), Lepidoptera (n=2), Thysanoptera (n=2), Coleoptera (n=1), and Pseudoescorpionae (n=1).

DISCUSSION

Leguminosae, Myrtaceae, and Asteraceae served as hosts for the largest variety of gall morphotypes along the Jacaraci trail; they are also among the principal families bearing galls in different Brazilian ecosystems, especially the Cerrado (Gonçalves-Alvim and Fernandes 2001, Urso-Guimarães and Scareli-Santos 2006, Araújo et al. 2012) (Table II).

TABLE II
Richness of gall morphotypes in host plants of Cerrado sensu stricto and Gallery forest in Brazil.

Locality	Biomes	Richest families	Richest genera	Richest species	Number of morphotypes	Mean of morphotypes
Caetité, BA (the present study)	Gallery forestCerrado	Leguminosae (15) Myrtaceae (9) Asteraceae (7)	Bauhinia L. (6) Mimosa L. (3) Guarea F.Allam. ex L. (3) Eugenia L. (3)	Mimosa gemmulata Barneby (3)	63	1.3
Goiás, GO (Bergamini et al. 2017)	Gallery forest Cerrado	Leguminosae (18) Asteraceae (17) Sapindaceae (16) Burseraceae e Myrtaceae (14) Siparunaceae (12) Celastraceae e Rubiaceae (10)	Protium Burm. f. (14) Siparuna Aubl.Sy (12) Serjania Mill. (12) Bauhinia (10)	Protium heptaphyllum (Aubl.) Marchand (14) Siparuna guianensis Aubl. (12) Serjania sp. (12)	186	3
Serra de Caetité, BA (Nogueira et al. 2016)	Cerrado	Leguminosae (22) Malpighiaceae (10)	Copaifera Desf. (10) Bauhinia (6) Mimosa (4)	Copaifera langsdorffii Desf. (9) Bauhinia acuruana Moric. (5)	49	3.5
Goiás, GO (Araújo et al. 2015)	Cerrado	Leguminosae (58) Malpighiaceae (29) Myrtaceae (28) Vochysiaceae (27)	Byrsonima Rich. ex Kunth (22) Qualea Aubl. (21) Myrcia DC. (17)	Byrsonima pachyphylla A. Juss. (8) Protium heptaphyllum (8) Qualea parviflora Mart. (8) Styrax pohlii A. DC. (8)	365	2
Goiânia, GO (Araújo et al. 2014)	Cerrado	Myrtaceae (17) Leguminosae (14)	Myrcia (10) Qualea (8) Byrsonima (6) Andira Lam. (4)	Andira cujabensis Benth. (4) Myrcia guianensis (Aubl.) DC. (4) Byrsonima coccolobifolia Kunth (3)	97	1.8
Caldas Novas- GO (Santos et al. 2012)	Cerrado	Leguminosae (14), Vochysiaceae (8) Malpighiaceae (5)	Qualea (8) Andira (6)	Andira paniculata Benth. (5) Caryocar brasiliense Cambess. (3) Qualea parviflora Mart. (3) Qualea grandiflora Mart. (3)	56	1.6
Serra dos Pireneus, GO (Araújo et al. 2011)	Gallery forest Cerrado	Leguminosae (8) Styracaceae (6) Malpighiaceae (5)	Styrax L. (6) Qualea (4)	Styrax pohlii (5) Andira paniculata (3) Qualea parviflora (3) Davilla elliptica A. St.-Hil. (2)	62	1.2
Goiânia, GO (Santos et al. 2010)	Cerrado	Leguminosae (9) Styracaceae (6) Ulmaceae (4)	Styrax (6) Celtis L. (3) Inga Mill. (3) Serjania (3) Trema Lour. (3)	Styrax pohlii (6) Inga cylindrica (Vell.) Mart. (3) Serjania obtusidentata Radlk. (3) Trema micrantha (L.) Blume (3)	34	1.9
Serra do Cipó, MG (Coelho et al. 2009)	Cerrado	Fabaceae (22) Myrtaceae (11) Asteraceae (8)	Bauhinia (10) Myrcia (6) Celtis (6) Serjania (6)	Baccharis dracunculifolia DC. (5) Bauhinia brevipes Vogel (2) Celtis brasiliensis (Gardner) Planch. (1) Terminalia argentea Mart. (1)	92	1.8
Santa Rita do Passa Quatro, SP (Urso-Guimarães and Scarelli-Santos 2006)	Cerrado	Fabaceae (7) Myrtaceae (5) Annonaceae (4)	Myrcia (4) Duguetia A. St.-Hil. (3) Bauhinia (3)	Duguetia furfuracea (A. St.-Hil.) Saff. (3) Myrcia bella Cambess. (3) Bauhinia rufa (Bong.) Steud. (3)	32	1.3
Tiradentes, MG (Maia and Fernandes 2004)	Cerrado	Leguminosae (20) Myrtaceae (18) Asteraceae (16) Melastomataceae (14)	Croton L. (4) Vernonia Schreb. (4)	Protium heptaphyllum (7) Copaifera langsdorffii (6) Croton floribundus Spreng. (5)	137	1.9
Delfinópolis, MG (Urso-Guimarães et al. 2003)	Gallery forestCerrado	Leguminosae (2) Rubiaceae (2) Vochisyaceae (2)	Bauhinia (2) Chomelia Jacq. (2) Qualea (2)	Bauhinia ungulata L. (2) Chomelia pohliana Müll. Arg. (2) Qualea parviflora (2)	22	1.2
Três Marias, MG (Gonçalves-Alvim and Fernandes 2001)	Cerrado	Leguminosae (24) Myrtaceae (10) Malpighiaceae (8) Asteraceae (7)	Byrsonima (6) Myrcia (5) Copaifera (4)	Byrsonima coccolobifolia Kunth (4) Myrcia sp. (4) Bauhinia brevipes (3) Bowdichia virgilioides Kunth (3)	92	1.5

The Leguminosae hosted the greatest diversity of gall morphotypes in Cerrado areas (Gonçalves-Alvim and Fernandes 2001, Araújo et al. 2011, Luz et al. 2012). This gall richness may reflect the high number of species of Leguminosae in that vegetation type (approximately 879), but also the high numbers of their species associated with gall-inducing insects (Mendonça 2007). Asteraceae is the second largest family in terms of the number of species in that biome (Mendonça et al. 2008), with approximately 1,251 species belonging to 190 genera (Asteraceae in Lista de Espécie da Flora do Brasil 2020 em construção). These families are also representative with the greatest richness of galls in Gallery forest (Urso-Guimarães et al. 2003, Bergamini et al. 2017).

The plant genera with the greatest number of galls were: Bauhinia (n=6) (Leguminosae-Cercidoideae), Mimosa (n=3) (Leguminosae-Caesalpinioideae), Guarea (Meliaceae) (n=3), and Eugenia (Myrtaceae) (n=3). The genus Bauhinia was reported to be a super-host in the states of Minas Gerais (Coelho et al. 2009), Pernambuco (Santos et al. 2011), and Bahia (Costa et al. 2014a, Nogueira et al. 2016) in Caatinga, Cerrado and Caatinga-Cerrado transition areas. The genus Mimosa was reported in the state of Bahia (Nogueira et al. 2016), Guarea in São Paulo (Maia et al. 2008) and Eugenia in Rio de Janeiro (Maia 2001, Maia and Oliveira 2010) in Cerrado and Restinga areas. Our results differed from other inventories undertaken in Gallery forest and Cerrado vegetation, which showed the genera Qualea Aubl. (Vochysiaceae), Protium Burm. f. (Burseraceae), Baccharis L. (Asteraceae), and Byrsonima Rich. ex Kunth (Malpighiaceae) as the plant species demonstrating the greatest number of galls (Table II) (Urso-Guimarães et al. 2003, Araújo et al. 2011, Santos et al. 2012, Carneiro et al. 2009, Coelho et al. 2013, Costa 2016, Bergamini et al. 2017).

Mimosa gemmulata had the largest number of galls. Studies undertaken by Costa 2016 in the Parque Estadual Serra dos Montes Altos, Bahia, showed that same species as a super-host, with five and six distinct gall morphotypes in Cerrado and Gallery forest sites, respectively.

Galls were previously surveyed in the municipality of Caetité in areas of Cerrado and in Caatinga-Cerrado transition zones in the Serra Geral Mountains (Costa et al. 2014a, b, Nogueira et al. 2016). The current study, however, represents the first inventory undertaken in an area of Gallery forest in that municipality. The inventory undertaken by Costa (2014b) recorded 35 gall morphotypes, distributed among 17 plant families, with Leguminosae and Myrtaceae having the highest number of species hosting galls. Nogueira et al. (2016) reported 49 distinct gall morphotypes on 13 plant species belonging to 12 families. Leguminosae was the principal host plant family (with 22 morphotypes), followed by Malpighiaceae (10). Current survey undertaken in Caetité along the Jacaraci trail showed the greatest richness of gall morphotypes recorded for Bahia State (63), 46 of which occur in Cerrado vegetation and 17 in Gallery forest. These results may reflect, however, a greater sampling effort and winder duration, the fact that collections were made during both the rainy and dry seasons, and the number of collectors (2-3 individuals), and their experience for field work, as suggested by Costa 2016.

The galls recorded had been induced on leaves, stems, buds, and fruits, with leaves being the organs most affected, whether in the Cerrado or Gallery forest; no galls were observed on flowers. These results are similar to other studies undertaken in different vegetation types in Brazil, where galls have been observed predominately on leaves (Julião et al. 2005, Maia et al. 2008, Nogueira et al. 2016, Santos et al. 2010, Araújo et al. 2012), a fact that is probably related to the nutrient reserves present in these organs (Mani 1964).

Most of the galls were isolated and contained only a single larval chamber, a result similar to those of Costa et al. (2014a, b) and Gonçalves-Alvim and Fernandes (2001). Only 37% had some pilosity, with being the other glabrous (63%). The presence of trichomes on the galls may help defend against natural enemies, reduce water losses, and help maintain mild internal temperatures (Moura et al. 2009).

In terms of their shapes, most galls were globoid, marginal roll or lenticular in both of the environments surveyed. Globoid galls have been the predominant morphotype described in all of the inventories undertaken in the Neotropical region (Isaias et al. 2013). Similar results were found in Restinga areas in Rio de Janeiro State (Maia 2013), Caatinga-Cerrado sites in Bahia (Costa et al. 2014b) and Gallery forest in Minas Gerais (Urso-Guimarães et al. 2003).

The identification of 48 gall-inducing insects were quite difficult due to the small number of samples (with most galls showing incomplete development of the gall-inducing insects) – and they remained undetermined. The gall-inducing insects that could be identified belonged to the orders Diptera, Lepidoptera, and Thysanoptera; most were Diptera (Cecidomyiidae) (53% of the total). Cecidomyiidae constitute the largest family of that order, comprising 6,590 species belonging to 812 globally distributed genera (Gagné and Jaschhof 2017). The galls of the Lepidoptera are usually encountered on the stems and buds (Maia 2006), but we recorded their induction on the leaves of Bauhinia pulchella Benth. and Bauhinia sp. and on the buds of Plinia peruviana they were also recorded as associated fauna in cecidomyiid galls on Qualea parviflora Mart.

We recorded two gall morphotypes induced by Thysanoptera in an unidentified species of Malpighiaceae and on Eugenia sp. (Myrtaceae), both on their leaves. These results confirm the plant preferences of those organisms for inducing leaf galls (Maia 2006).

In addition to the gall-inducing insects, there is also a distinct insect fauna associated with the galls themselves. Those arthropods vary in terms of their feeding habits and can be classified as: parasitoids, predators, inquilines, and successors (Maia 2001). The microfauna associated with the galls in the present study was composed of Hymenoptera, Hemiptera, Lepidoptera, Thysanoptera, Coleoptera, Collembola, Araneae, and Pseudoscorpionida. The order Hymenoptera had the greatest number of records, occurring on galls observed on Asteraceae Indet., Moquiniastrum sp., Combretum leprosum Mart., Caliandra macrocalyx Harms, Myrtaceae Indet., Solanaceae Indet., and Turneraceae Indet. This order stands out for its parasitoids, as reported in various studies, being considered the principal taxon responsible for the deaths of gall-inducing insects. Species of Hymenoptera have been reported as parasitoids in areas of Cerrado (Maia and Fernandes 2004, Maia et al. 2008) and Gallery forest (Costa 2016), corroborating the current results.

Inquilines are organisms that simultaneously inhabit the galls and feed on the plant tissues within it – thus competing with the gall-inducing insects (Narendran et al. 2007). The inquilines encountered in the present study belonged to the Hemiptera, Lepidoptera, Thysanoptera, and Coleoptera. These same orders have also been recorded in Cerrado (Maia and Fernandes 2004) and Gallery forest sites (Costa 2016).

The fauna of successors was composed of ants, spiders, pseudoscorpions, arachnids, and Collembola – representing organisms that occupy the galls after they have been abandoned by the inducing-species. While pseudoscorpions have only infrequently been reported in galls (Maia 2001, 2011, Carvalho-Fernandes et al. 2012, Maia and Souza 2013, Costa et al. 2014a, Nogueira et al. 2016), we identified them in abandoned galls on Psidium brownianum Mart. ex DC. (Myrtaceae); other studies have recorded these organisms on two species of Myrtaceae [Myrcia tomentosa (Aubl.) DC. (Maia 2001) and Eugenia astringens Cambess.] (Costa 2014b).

Even though the study area was not extensive (a trail approximately 3 Km long), a considerable diversity of galls was observed. Of the 47 host plant taxa identified, eight were identified for the first time as gall hosts for Brazil. These results reinforce the importance of undertaking inventories of galls and their host plants in unsampled areas throughout that country, since it will contribute to the knowledge about plant species, galling insects and their interactions among different environments.

ACKNOWLEGMENTS

The authors thank Dr. Flávio França (UEFS), Dr. Efigênia de Melo (UEFS), and Dr. Marcos Sobral (UFSJ) for the identifications of the botanical material. This study composes part of the course conclusion monograph of the first author, which was supported by the Departamento de Ciências Humanas da Universidade do Estado da Bahia, Campus VI, the Programa de Pós-Graduação em Biodiversidade Vegetal (PPGBveg/UNEB), the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Proc. no 406111/2016-2), and the Fundação de Amparo à Pesquisa do Estado da Bahia (FAPESB) (Proc. no 9648/2015).

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Publication Dates

• Publication in this collection
  Jul-Sep 2018

History

• Received
  16 July 2017
• Accepted
  7 Mar 2018