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Iheringia. Série Zoologia

Print version ISSN 0073-4721On-line version ISSN 1678-4766

Iheringia, Sér. Zool. vol.108  Porto Alegre  2018  Epub June 11, 2018

http://dx.doi.org/10.1590/1678-4766e2018015 

Article

Gall-inducing insects of deciduous and semideciduous forests in Rio Grande do Sul State, Brazil

Insetos indutores de galhas das florestas decidual e semidecidual no Estado do Rio Grande do Sul, Brasil

1Departamento de Ecologia, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Av. Bento Gonçalves 9500, Porto Alegre, RS, 91501-970, Brazil. (anapgoetz@gmail.com; milton.mendonca@ufrgs.br)

2Institut Méditerranéen de Biodiversité et d’Ecologie (IMBE), Université d’Avignon et des Pays de Vaucluse, CNRS, IRD, Aix Marseille Université, IUT d’Avignon, Avignon cedex 9, France.

3CAPES Foundation, Ministry of Education of Brazil, Brasília, DF, 70040-020, Brazil

ABSTRACT

Galls are specific changes induced by insects on plant organs mainly through increases in plant cell number and/or size. Gall diversity is easy to recognize in the field because gallers are mostly species-specific, and thus each gall morphotype can be a proxy for a galling species. Insect galls are virtually unknown in Seasonal Deciduous and Semi-Deciduous forests of southern Brazil. Here, galls and host plants were surveyed between 2015 and 2017 in four forest fragments of Rio Grande do Sul State in these two vegetation types, in secondary-growth and areas under restoration. We recorded 89 gall morphotypes, with gallers belonging to Lepidoptera and Diptera, with the latter represented mainly by Cecidomyiidae. Galls were associated to 46 plant species in 27 families. Asteraceae, Piperaceae, Fabaceae, Myrtaceae and Lauraceae were the richest families in terms of galls, whilst Piper aduncum and Mikania glomerata were superhosts. Most galls occurred in leaves and shoots. The most common shapes were fusiform, globoid and lenticular. Forty-eight gall morphotype records are new for both Rio Grande do Sul and Brazil, an expressive number considering only two seasonal forest types sampled and few sampling points, showing how important surveys still are for these little know fauna both in taxonomic and ecological terms.

KEYWORDS Insect-plant interaction; host plant; morphotype; gall richness

RESUMO

Galhas são alterações específicas induzidas por insetos sobre órgãos das plantas principalmente através de aumento no número e/ou tamanho das células vegetais. A diversidade de galhas é reconhecível em campo porque os galhadores são na sua vasta maioria espécie-específicos e assim cada morfotipo de galha serve como proxy para uma espécie de galhador. Insetos galhadores são virtualmente desconhecidos nas florestas estacionais deciduais e semideciduais do sul do Brasil. Galhas e plantas hospedeiras foram inventariadas entre 2015 e 2017 em quarto fragmentos florestais do Estado do Rio Grande do Sul nestas duas formações vegetacionais, em áreas com sucessão secundária e sob restauração. Foram encontrados 89 morfotipos de galhas, com galhadores pertencentes a Lepidoptera e Diptera, com os últimos representados principalmente por Cecidomyiidae. As galhas estiveram associadas a 46 espécies de plantas em 27 famílias. Asteraceae, Piperaceae, Fabaceae, Myrtaceae e Lauraceae foram as famílias mais ricas em termos de galhas, sendo Piper aduncum e Mikania glomerata considerados super-hospedeiras. A maioria das galhas ocorreu em folhas e ramos. As formas mais comuns foram fusiforme, globoide e lenticular. Dos morfotipos de galhas registrados, 48 são novos para o Rio Grande do Sul e o Brasil, um número expressivo considerando que somente dois tipos de florestas foram amostradas em um número restrito de pontos amostrais, demonstrando a importância de levantamentos para esta fauna quase desconhecida tanto em termos taxonômicos quanto ecológicos.

PALAVRAS-CHAVE Interação inseto-planta; planta-hospedeira; morfotipo; riqueza de galhas

Insect-induced galls are anomalous growth on plant organs originating from increases in plant cell number (hyperplasia) and/or size (hypertrophy) (Mani, 1964). Galling insect species can even be separated and identified based on gall morphology along with host plant organ and species (Price et al., 1998). Each galling insect species is responsible for inducing a unique structure, a gall with distinct anatomy and physiology compared to other such species (Shorthouse et al., 2005). Most gallers are species-specific relative to the plant host, with the latter usually belonging to specific plant clades as well, with clear evolutionary associations (Mendonça, 2007). New surveys of these gall-based plant-herbivore trophic networks on unexplored sites and vegetation types can work as repeated tests for these ecological and phylogenetic patterns, with regional preferences either confirmed or revised by new knowledge.

Since the end of the 1980s decade, studies on galling insects increased considerably in Brazil, mainly related to natural history and distribution (Fernandes et al., 2014). Nowadays, work is being carried out in all different regions of this country: North (e.g. Almada & Fernandes, 2011), Northeast (e.g. Nogueira et al., 2016), Central-West (e.g. Araújo et al,. 2015) and Southeast (e.g. Maia & Carvalho-Fernandes, 2016). In Southern Brazil, studies on galling insect diversity are still scarce, however there are recent records for Paraná (Carvalho et al., 2015; Santos & Ribeiro, 2015) and Rio Grande do Sul States (e.g. Dalbem & Mendonça, 2006, Mendonça, 2007, 2011; Mendonça et al.; 2010, Toma & Mendonça, 2013). Mendonça et al. (2014) listed insect galls known from the two biomes occurring in Rio Grande do Sul (RS), Atlantic forest and Pampas. Surveys covered different vegetation types, mostly subtropical gallery forests and subtropical moist forests, without being able to represent Seasonal forests, a rather common vegetation type in the region.

This study aims to increase the present knowledge on galling insects and their host plants by surveying Deciduous and Semideciduous Seasonal forests in Rio Grande do Sul State and comparing with already established ecological and evolutionary patterns on gall occurrence.

MATERIAL AND METHODS

This study was carried out in forest fragments of Semideciduous Seasonal (SS) and Deciduous Seasonal (DS) forest formation types, in two localities of Rio Grande do Sul State, Brazil. SS samples took place in Canela municipality, in an area belonging to the State Electric Company (Companhia Estadual de Energia Elétrica, CEEE-RS). Samples in DS occurred in Santa Tereza municipality, in private property areas with authorisation granted for scientific research.

The SS sites face a Cfb climate (Köppen classification) with average temperatures for the hottest month at 22°C and for the coldest month from -3°C and 18°C (Moreno, 1961). This type of forest formation is characteristic of regions with temperature climatic seasonality and has a percentage of deciduous trees between 25 and 50%, evident in the winter (IBGE, 2012). The DS sites are under a Cfa climate with average temperatures for the hottest month above 22°C and for the coldest month from -3°C and 18°C (Moreno, 1961). As with the SS forests, DS occurs in seasonal environments, having however at least 50% of trees losing leaves in the cold season (Espírito-Santo et al., 2006).

Eight seasonal samples were done during 2015 and 2017 (one yearly sample for autumn and winter and three yearly samples for summer and spring) in four forest fragments (two for each vegetation type) in two distinct successional stages. For the SS forests in Canela, two fragments had advanced secondary growth (29°22’58.1”S, 50°44’08.1”W and 29°22’50.4”S, 50°44’11.9”W) and two others had 10 years since restoration actions were undertaken (29°22’50.2”S, 50°44’03.2”W and 29°22’44.1”S, 50°43’49.8”W). For the DS forests in Santa Tereza, there were also fragments being the first two at an advanced secondary succession (29°09’27.5”S, 51°41’34.6”W and 29°09’45.8”S, 51°42’33.2”W), as well as two areas with eight years since restoration took place (29°09’44.8”S, 51°42’32.8”W and 29°09’47.8”S, 51°42’40.5”W). Each fragment was explored by two persons during 60 min in search for galls in all plant species. Overall there were 64 h of sampling in each locality.

All galls were collected and took to the lab, where they were separated in morphotypes according to external morphology in combination with galled organ and host plant species. Galls were photographed, dissected under stereoscopic microscope to obtain immature galling inducers and characterize and describe galls (shape, colour and number of chambers) according to Isaias et al. (2013).

Part of the sampled galls was kept in sealed plastic bags to obtain adult galling insects. These were preserved in 70% ethanol and identified to the lower taxonomic level possible. However, some gall morphotypes were found empty, which made inducer identification impossible, although there is no doubt these galls were insect-induced. Host plant shoots, reproductive when possible, were identified with the help of taxonomic literature and/or botanical specialists. Biological material is deposited in the scientific collection of the Laboratório de Ecologia de Interações, UFRGS. Host plant taxa were organised according to Angiosperm Phylogeny Group IV classification (APG, 2016).

RESULTS

Overall 89 gall morphotypes were found, with most insect inducer species being Diptera, and Cecidomyiidae having 55% of all galling species. Lepidoptera represented only 3.3% of galling species and 38.2% of the morphotypes could not be identified, either coming from empty galls or only found occupied by parasitoids (Hymenoptera and Diptera). Among all gall morphotypes found here, 48 are considered as new records for the host plant species (Tab. I), comparing with pertinent literature - that is, no mention of a gall on a given plant, with the structure and inducer reported here, could be found.

Table I Host plants, morphological characters and inducers for galls sampled in Semideciduous Seasonal (S) and Deciduous Seasonal (D) forest formation types, in two localities of Rio Grande do Sul State, Brazil, from 2015 to 2017. Number of chambers in the gall: M, monothalamous; P, polythalamous; N.O., not observed. Gall color: B, Brown; G, green; LB, light brown; LG, light green; RE, red; RO, rosy; Y, yellow; W, white. For each forest formation type galls could have been recorded in areas of: S, secondary sucession and/or R, restoration. Yearly season gall was recorded (SP, spring; A, autumn; SU, summer; W, winter). * indicates an insect galler on a plant species never mentioned as galled by an insect of this family before. 

Host plant Organ Shape Gall inducer Fig. Forest type Season
Acanthaceae
Justicia brasiliana Roth Bud FusiformM,G Cecidomyiidae Fig. 1 DR/S A/SP
Asteraceae
Calea serrata Less. Stem GloboidM,G Cecidomyiidae Fig. 2 S/DR W/SP/SU
Calea serrata Less. Stem FusiformM,LB Cecidomyiidae Fig. 3 SR SU
Calea serrata Less* Leaf (petiole) FusiformM,G Fig. 4 SR SP
Calea serrata Less* Stem FusiformP,G Fig. 5 DR SU
Calea serrata Less* Leaf AmorphousM,G Fig. 6 DS SP
Dasyphyllum spinescens (Less.) Cabrera* Stem FusiformN.O.,G Fig. 7 SS SP
Mikania glomerata Spreng. Stem GloboidP,B Asphondylia moehni Skuhravá, 1989 Fig. 8 S/DR/S A/W/SP/SU
Mikania glomerata Spreng. Leaf CylindricalM,G Liodiplosis cylindrica Gagné 2001 Fig. 9 SR W
Mikania glomerata Spreng. Leaf GloboidM,G Liodiplosis spherica Gagné, 2001 Fig. 10 SR W
Mikania glomerata Spreng. Stem/Leaf ConicalM,G Liodiplosis conica Gagné, 2001 Fig. 11 SS W
Mikania glomerata Spreng. Leaf (petiole) FusiformM,G Mikaniadiplosis annulipes Gagné, 2001 Fig. 12 DS W/SU
Mikania glomerata Spreng. Leaf (vein) FusiformM,G Fig. 13 SR SU
Mikania micrantha Kunth* Stem GloboidN.O.,B Fig. 14 DR S
Mikania micrantha Kunth* Leaf (petiole) GloboidM,G Fig. 15 DR S
Mikania micrantha Kunth* Stem FusiformM,G Fig. 16 DR SP
Mikania ternata (Vell.) B.L. Rob.* Leaf FusiformM,G/RO Fig. 17 SS SP
Moquiniastrum polymorphum (Less.) Stem FusiformM,B Cecidomyiidae Fig. 18 SR SP
Trixis praestans (Vell.) Cabrera* Bud GloboidM,G Fig. 19 DS A
Bignoniaceae
Dolichandra unguis-cati (L.) L.G.Lohmann Stem GloboidP,LB Cecidomyiidae Fig. 20 S/DR/S A/SP/SU
Cordia ecalyculata Vell.* Stem FusiformP,B Cecidomyiidae Fig. 21 SR/S W/SP
Cordia americana (L.) Gottshling & J.E.Mill. Leaf GloboidM,G Diptera Fig. 22 DR/S SP/SU
Cannabaceae
Celtis iguanaea (Jacq.) Sarg. Leaf (vein) FusiformM,G Cecidomyiidae Fig. 23 SR/S A/W/SP/SU
Celtis iguanaea (Jacq.) Sarg.* Stem FusiformN.O.,LB Fig. 24 SR/S A/W
Trema micrantha (L.) Blume* Stem FusiformP,LB Cecidomyiidae Fig. 25 SR/S A/W/SP
Cardiopteridaceae
Citronella gongonha(Mart.) R.A.Howard* Stem FusiformM,G Fig. 26 SR SU
Citronella gongonha(Mart.) R.A.Howard* Stem FusiformN.O.,G/LB Cecidomyiidae Fig. 27 SR SP
Dioscoreaceae
Dioscorea scabra Humb. & Bonpl. ex Willd.* Leaf (petiole) FusiformM,G Cecidomyiidae Fig. 28 DS W/SU
Dioscorea scabra Humb. & Bonpl. ex Willd.* Stem (aculeus) FusiformM,G Cecidomyiidae Fig. 29 DR SU
Dioscorea scabra Humb. & Bonpl. ex Willd.* Stem FusiformM,G Fig. 30 DR W/SU
Dioscorea scabra Humb. & Bonpl. ex Willd.* Bud FusiformP,G Cecidomyiidae Fig. 31 DR W/SU
Elaeocarpaceae
Sloanea monospermaVell.* Stem GloboidP,B Fig. 32 SR SU
Euphorbiaceae
Sebastiania sp. Leaf GloboidM,G Fig. 33 SS SP
Fabaceae
Bauhinia forficata Benth.* Stem FusiformM,G/B Fig. 34 DR S
Inga marginata Willd. Stem GloboidP,G/LB Cecidomyiidae Fig. 35 S/DR/S A/W/SP/SU
Inga marginata Willd. Leaf (vein) FusiformM,LB Cecidomyiidae Fig. 36 S/DR/S A/W/SP/SU
Inga marginata Willd.* Leaf GloboidM,B/Y Fig. 37 SR/S W/SP
Inga marginata Willd.* Leaf GloboidM,LB Cecidomyiidae Fig. 38 SS A/SP
Inga marginata Willd.* Stem FusiformN.O., /LB Fig. 39 SR SP
Machaerium paraguarienseHassl.* Leaf Leaf FoldM,LG Cecidomyiidae Fig. 40 DR A
Lauraceae
Ocotea puberula (Rich.) Nees* Stem/Leaf GloboidM,LG Cecidomyiidae Fig. 41 S/DR/S W/SP
Nectandra megapotamica (Spreng.) Mez Stem FusiformP,B Cecidomyiidae Fig. 42 S/DR/S A/W/SP/SU
Nectandra megapotamica (Spreng.) Mez* Leaf GloboidM,G/RO Cecidomyiidae Fig. 43 S/DR/S A/W/SP
Nectandra megapotamica (Spreng.) Mez * Leaf FusiformM,G Cecidomyiidae Fig. 44 DR/S A/SU
Nectandra megapotamica (Spreng.) Mez * Leaf LenticularM,Y/LG Fig. 45 DS SP
Malvaceae
Luehea divaricata Mart. & Zucc. Leaf ConicalM,G/W Cecidomyiidae Fig. 46 S/D SP/SU
Luehea divaricata Mart. & Zucc. Leaf FusiformM,LB Fig. 47 DR/S SP/SU
Luehea divaricata Mart. & Zucc. Leaf GloboidM,G Fig. 48 DS SU
Melastomataceae
Leandra regnellii (Triana) Cogn.* Leaf GloboidM,RO Cecidomyiidae Fig. 49 S/DR/S A/W/SP/SU
Leandra regnellii (Triana) Cogn.* Stem FusiformP,LB Cecidomyiidae Fig. 50 SR/S A/W/SP/SU
Meliaceae
Trichilia claussenii C.DC.* Stem/Bud RossetteM,G Fig. 51 SR/S SU
Monimiaceae
Mollinedia elegans Tul.* Stem FusiformM,LB Cecidomyiidae Fig. 52 SR/S A/W/SP/SU
Mollinedia schottiana (Spreng.) Perkins* Bud ConicalM,LB Fig. 53 SR SP
Moraceae
Sorocea bonplandii(Baill.) W.C. Burger, Lanjouw & Boer* Stem FusiformM,LB Fig. 54 SR SU
Myrtaceae
Campomanesia xanthocarpa O. Berg Leaf LenticularM,LG Cecidomyiidae Fig. 55 DR SP/SU
Eugenia uniflora L. Leaf FusiformM,RE/G Clinodiplosis profusa Maia, 2001 Fig. 56 DR/S A
Eugenia uniflora L.* Leaf LenticularM,LG Fig. 57 DR A
Myrcianthes pungens (O.Berg) D. Legrand* Bud FusiformM,LG Cecidomyiidae Fig. 58 DR SP
Myrcianthes pungens (O.Berg) D. Legrand* Leaf Marginal rollM,G Fig. 59 DR SU
Psidium cattleyanum Sabine* Stem FusiformM,LG Fig. 60 DR SP
Nyctaginaceae
Guapira opposita (Vell.) Reitz Leaf GloboidM,G Cecidomyiidae Fig. 61 SR/S A/SP
Guapira opposita (Vell.) Reitz Leaf GloboidM,RO Bruggmannia robusta Maia & Couri, 1993 Fig. 62 SR/S SP
Guapira opposita (Vell.) Reitz Leaf LenticularM,G Bruggmannia elongata Maia & Couri, 1 993 Fig. 63 SR/S A/SP/SU
Guapira opposita (Vell.) Reitz Stem FusiformM,G Cecidomyiidae Fig. 64 SR SU
Phytolaccaceae
Seguieria aculeataJacq. * Leaf LenticularM,G/LB Fig. 65 SS SU
Piperaceae
Piper aduncum L. Stem FusiformP,G Cecidomyiidae Fig. 66 S/DR/S A/W/SP/SU
Piper aduncum L. Stem FusiformM,G Cecidomyiidae Fig. 67 S/DR/S A/W/SP/SU
Piper aduncum L. Leaf (vein) GloboidM,G Cecidomyiidae Fig. 68 S/DR/S A/W/SP/SU
Piper aduncum L. Leaf (petiole) FusiformM,G Cecidomyiidae Fig. 69 S/DR/S A/W/SP/SU
Piper aduncum L.* Leaf (vein) FusiformM,G Cecidomyiidae Fig. 70 S/DR/S A/W/SP/SU
Piper aduncum L.* Leaf GloboidM,G/W Cecidomyiidae Fig. 71 S/DR/S A/W/SP/SU
Piper aduncum L. Stem/Leaf AmorphousP,G Cecidomyiidae Fig. 72 S/DR/S A/W/SP/SU
Piper aduncum L.* Fruit AmorphousP,G Cecidomyiidae Fig. 73 DR/S SP
Piper mikanianum (Kunth) Steudel Stem FusiformP,B Cecidomyiidae Fig. 74 S/DR/S A/W/SP/SU
Piper mikanianum (Kunth) Steudel* Leaf LenticularM,G Fig. 75 S/DR/S W/SP/SU
Piper mikanianum (Kunth) Steudel* Fruit GloboidM,B Cecidomyiidae Fig. 76 S/DR/S SP/SU
Primulaceae
Myrsine coriacea (Sw.) R.Br. Stem FusiformM,LB Lepidoptera Fig. 77 DR A
Myrsine umbellata Mart. Bud FusiformM,G Lepidoptera Fig. 78 SR/S A/W/SU
Rubiaceae
Psychotria carthagenensis Jacq.* Leaf (vein) FusiformM,G Cecidomyiidae Fig. 79 S/DR/S SU
Psychotria carthagenensis Jacq. Leaf LenticularM,G Cecidomyiidae Fig. 80 S/DR/S A/W/SP/SU
Rudgea parquioides (Cham.) Müll.Arg.* Stem FusiformP,B Fig. 81 DR W
Rudgea parquioides (Cham.) Müll.Arg. Leaf LenticularM,G Cecidomyiidae Fig. 82 SS SP
Salicaceae
Xylosma pseudosalzmanii Sleumer* Bud GloboidM,B Fig. 83 SR W
Sapindaceae
Allophylus edulis (A.St.-Hil., Cambess. & A. Juss.) Radlk. Stem FusiformM,B Lepidoptera Fig. 84 DR/S SP/SU
Allophylus edulis (A.St.-Hil., Cambess. & A. Juss.) Radlk. Leaf (vein) LenticularM,Y/LG Diptera Fig. 85 DR/S SP/SU
Serjania sp. Stem FusiformM, LB/G Fig. 86 DR SU
Smilacaceae
Smilax sp. Stem FusiformN.O.,G Fig. 87 SS SP
Solanaceae
Cestrum strigillatum Ruiz & Pav. Bud GloboidM,LG Fig. 88 DR S
Vitaceae
Cissus striata Ruiz & Pav.* Stem FusiformP,RO/Y Cecidomyiidae Fig. 89 SR W/SP

Galls were associated to 27 host plant families, including 40 genera and 46 nominated species (e.g. Tab. I - Figs 1-89). The most representative families were Asteraceae, with 18 gall morphotypes (20.2%), Piperaceae with 11 (12.3%), Fabaceae with seven (7.8%), Myrtaceae with six (6.7%) and Lauraceae with five (5.6%). These families comprised 52.6% of all recorded gall morphotypes. Asteraceae also had the highest number of galled plant species (n = 7), while other families had four or five species. The most representative genera in gall morphotype numbers were Piper L., with 11 (12.3%) and Mikania Willd., with 10 (11.2%). Among species, those with most galls were Piper aduncum L. (n = 8) and Mikania glomerata Spreng. (n = 6).

Figures 1-20  Insects galls of deciduous and semideciduous forests in Rio Grande do Sul State, Brazil: 1, Justicia brasiliana; 2-6, Calea serrata; 7, Dasyphyllum spinescens; 8-13, Mikania glomerata; 14-17, Mikania micrantha; 18, Moquiniastrum polymorphum; 19, Trixis praestans; 20, Dolichandra unguis-cati. Scale bar: 1 cm. 

Figures 21-40  Insects galls of deciduous and semideciduous forests in Rio Grande do Sul State, Brazil: 21, Cordia ecalyculata; 22, Cordia americana; 23-24, Celtis iguanaea; 25, Trema micrantha; 26-27, Citronella gongonha: 28-31, Dioscorea scabra; 32, Sloanea monosperma; 33, Sebastiania sp.; 34, Bauhinia forficata; 35-39, Inga marginata; 40, Machaerium paraguariense. Scale bar: 1 cm. 

Figures 41-60  Insects galls of deciduous and semideciduous forests in Rio Grande do Sul State, Brazil: 41, Ocotea puberula; 42-45, Nectandra megapotamica; 46-48, Luehea divaricata; 49-50, Leandra regnellii; 51, Trichilia claussenii; 52, Mollinedia elegans; 53, Mollinedia schottiana; 54, Sorocea bonplandii; 55, Campomanesia xanthocarpa; 56-57, Eugenia uniflora; 58-59, Myrcianthes pungens; 60, Psidium cattleyanum. Scale bar: 1 cm. 

Figures 61-80  Insects galls of deciduous and semideciduous forests in Rio Grande do Sul State, Brazil: 61-64, Guapira opposita; 65, Seguieria aculeata; 66-73, Piper aduncum; 74-76, Piper mikanianum; 77-78, Myrsine coriacea; 79-80, Psychotria carthagenensis. Scale bar: 1 cm. 

Figures 81-89  Insects galls of deciduous and semideciduous forests in Rio Grande do Sul State, Brazil: 81-82, Rudgea parquioides; 83, Xylosma pseudosalzmanii; 84-85, Allophylus edulis; 86, Serjania sp.; 87, Smilax sp.; 88, Cestrum strigillatum; 89, Cissus striata. Scale bar: 1 cm. 

Most galls were found on leaves (48.3%) and shoots (43.8%). Buds and fruits represented only 8.9% and 2.2%, respectively. There were no galls on flowers. The most common gall shape was fusiform (51.6%), followed by globoid (26.9%), lenticular (10.11%), amorphous (3.3%), conical (3.3%), cylindrical (1.1%), leaf fold (1.1%), rosette (1.1%) and marginal roll (1.1%).

DISCUSSION

The plant families with most galls in the Seasonal forests of Southern Brazil were Asteraceae, Fabaceae and Myrtaceae, all pointed out as the most common host taxa in Brazilian surveys from different regions (e.g. Maia et al., 2014; Araújo et al., 2015; Maia & Carvalho-Fernandes, 2016). Asteraceae as the family with most galled species also agrees with what was previously found for RS State, according to Mendonça (2007). These members of the daisy family were also recorded as those with the higher number of morphotypes in more recent surveys in RS (e.g. Toma & Mendonça, 2013; Mendonça et al., 2014).

Records of galls on Mikania had the highest contribution to morphotype richness in Asteraceae (10 of the 18 morphotypes in this family), with this genus already known (Mendonça et al., 2014) as a super-host (species or genera hosting many types of gall, Veldtman & McGeoch, 2003). Piper aduncum was the species attaining super-host status, followed by M. glomerata, a plant already considered as a super-host (Mendonça et al., 2014). Piperaceae, having this super-host species, ended up as the second most dominant family in this study, which is uncommon for gall surveys in Brazil. Cecidomyiidae as the most common inducer group was an expected result, since they comprise the richest family among galling arthropods (Gagné & Jaschhof, 2017), being also the most common in the Neotropical region (Gagné, 1994, Espírito-Santo & Fernandes, 2007).

Although leaves were the main galled organ, as is usual in other work (e.g. Araújo et al., 2015; Maia & Mascarenhas, 2017), leaves and shoots had similar proportions, as was found by Toma & Mendonça (2013) for a nearby survey in araucaria forest in RS. Mendonça et al. (2014), considering different localities and vegetation types, pointed out that in RS there were even more galls on shoots than on leaves. This pattern of no high prevalence of galls on leaves might be related to forest deciduousness in more temperate vegetation types in Brazil, which by losing leaves during winter could represent a less lasting resource for gallers. This hypothesis, along with the geographic question of similar results on intermediate latitudes [African savanna, Veldtman & McGeoch (2003); Neotropical rupestrian fields, Carneiro et al. (2009)], as suggested by Toma & Mendonça (2013), needs more specific tests and more regional comparisons, however.

Fusiform galls were more frequent, differently from other sites where the globoid form is more common (Maia et al., 2014; Nogueira et al., 2016), the latter being the second most common. Again, this was also found previously for the RS State by Toma & Mendonça (2013) and Mendonça et al. (2014). This pattern might be correlated with the above-mentioned relatively higher frequency of shoot galls in these more meridional environments - shoot galls are usually fusiform (Isaias et al., 2013; synonymized with elliptical).

The 48 new gall morphotype records (compared to the available literature, e.g. Almada & Fernandes, 2011; Toma & Mendonça, 2013; Mendonça et al., 2014; Maia et al., 2014; Araújo et al., 2015; Maia & Carvalho-Fernandes, 2016; Nogueira et al., 2016,), show how important survey work still is in this region, increasing our basic knowledge on galling insects. This expressive number of potentially new species of gallers reveals that especially in little explored different forest types (as seasonal Deciduous and Semi-deciduous forests), there is still much to be gained in terms of new data and new taxa.

Acknowledgments

We would like to thank CEEE-RS and Mr. Luís Brun for allowing access to the study areas; to Me. Ethiene Guerra, Prof. Mara Rejane Ritter and Dr. Milena Fermina Rosenfield for identification of host plants; and to Fundação Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for PhD scholarships (FAL and TSPT) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for undergraduate (APMG) and research scholarships (MSMJ) and for project funding.

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Received: January 25, 2018; Accepted: April 12, 2018

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