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Diversity of insect galls from Mato Grosso State, Brazil: North Pantanal

Diversidade de galhas de insetos do Estado do Mato Grosso, Brasil: Pantanal Norte

Abstract:

The Pantanal Biome occupies 20% of the Brazilian territory extending its distribution over two Brazilian States, Mato Grosso and Mato Grosso do Sul. This Biome is one of Brazil's poorly known regions concerning insect gall and their interactions with host plants. In this study, we characterized for the first time the gall morphology, identified host plants and the gall makers from an area of Brazilian wetlands from Mato Grosso State, known as Pantanal Matogrossense. We sampled Pantanal Biome areas in Poconé municipality, along the Transpantaneira Road, Mato Grosso State, Brazil, in two expeditions, July 2012 and January 2013, with a total effort of 2 hours. We characterized 91 morphotypes of insect galls in 54 host plant species; 28 gall makers in 24 host plant species; the richest host plant families are Fabaceae, Myrtaceae, and Sapindaceae. Psidium guineense Sw. is the super host species. This area in Pantanal Matogrossense is the second in the richness of gall morphotypes (N=91) and average morphotypes/plant species (1.7), comparing phytophysiognomies. Additionally, 15 plant species are new record as host in galler-host plant interaction in the world. This number represents 30% of the total of host plant species sampled in Poconé. This inventory is new knowledge to the Pantanal Matogrossense and representing a unique testimony of insect-plant interactions consumed by the unprecedented fire that occurred in Pantanal Biome in the dry season of 2020.

Keywords:
Biodiversity; Brazilian wetlands; conservation; gall makers; Neotropical region; insect-plant- interaction

Resumo:

O Bioma Pantanal ocupa 20% do território brasileiro estendendo sua distribuição sobre dois Estados brasileiros, Mato Grosso e Mato Grosso do Sul. Esta é uma das regiões menos estudadas do Brasil com relação aos insetos e suas interações. Neste estudo, caracterizamos pela primeira vez a morfologia de galhas, identificamos plantas hospedeiras e galhadores em áreas do Pantanal Norte, conhecido como Pantanal Matogrossense. As amostragens foram feitas em áreas do Bioma Pantanal, no município de Poconé, ao longo da Estrada Transpantaneira, Mato Grosso, Brasil em duas expedições, julho de 2012 e janeiro de 2013. Caracterizamos 91 morfotipos de galhas entomógenas em 54 espécies de plantas hospedeiras; identificamos 28 galhadores em 24 espécies de plantas hospedeiras; as famílias de plantas hospedeiras mais ricas em galhas são Fabaceae, Myrtaceae e Sapindaceae. Psidium guineense Sw. é a espécie superhospedeira. Esta área no Pantanal Matogrossense é a segunda tanto em riqueza de morfotipos de galhas (N=91) quanto na média de morfotipos por espécie de planta hospedeira (1,7), em fitofisionomias comparáveis. Além disso, 15 espécies de plantas são novos registros como hospedeiras para galhas de insetos no mundo. Esse número representa 30% do total de plantas amostradas em Poconé. Todos os dados deste inventário são conhecimentos novos para o Pantanal Mato-grossense e para o estado do Mato Grosso, representando um testemunho único das interações inseto-planta que foram consumidas pelo fogo sem precedentes ocorrido no Bioma Pantanal em sua estação seca de 2020.

Palavras-chave:
Biodiversidade; conservação; galhadores; interação inseto-planta; Pantanal Matogrossense; região Neotropical

Introduction

The Pantanal biome occupies 20% of the Brazilian territory (Junk et al. 2013JUNK, W.J., PIEDADE, M.T.F., LOURIVAL, R., WITTMANN, F., KANDUS, P., LACERDA, L.D., BOZELLI, R.L., ESTEVES, F.A., NUNES DA CUNHA, C., MALTCHIK, L., SCHÖNGART, J., SCHAEFFER‐NOVELLI, Y. & AGOSTINHO, A.A. 2013. Brazilian wetlands: their definition, delineation, and classification for research, sustainable management, and protection. Aquat. Conserv. 24:5-22.), extending its distribution over two Brazilian States, Mato Grosso and Mato Grosso do Sul. The Brazilian wetlands, called Pantanal popularly, are considered a hyper-seasonal savannah under contrasting stresses due to alternation between periods of drought and prolonged flooding (Eiten 1982EITEN, G. 1982. Brasilian "Savannas". In Ecology of Tropical Savannas: Ecological Studies (Huntley & Walker, eds.). Springer Verlag, Berlin, p. 25-47. , Marengo et al. 2021MARENGO, J.A., CUNHA, A.P., CUARTAS, L.A, LEAL, K.R.D., BROEDEL, E, SELUCHI, M.E., MICHELIN, C.M, BAIÃO, C.F.D.P., ÂNGULO, E.C., ALMEIDA, E.K., KAZMIERCZAK, M.L., MATEUS, N.P.A., SILVA, R.C. & BENDER, F. 2021. Extreme Drought in the Brazilian Pantanal in 2019-2020: Characterization, Causes, and Impacts. Front. water. 3:e639204. https://doi.org/10.3389/frwa.2021.639204.
https://doi.org/10.3389/frwa.2021.639204...
). Pantanal harbors deciduous or semi-deciduous forests shedding leaves during the dry season, deciduous forest and Cerrado vegetation in inselbergs and evergreen floodplain forests in the lower areas along rivers and channels (Nunes da Cunha et al. 2007NUNES DA CUNHA, C., JUNK, W.J. & LEITÃO-FILHO, H.F. 2007. Woody vegetation in the Pantanal of Mato Grosso, Brazil: a preliminary topology. Amazoniana. 19:159-184.). Its vegetation is highly influenced by Chaco Biome (Pott et al. 2011POTT, A., OLIVEIRA, A.K.M., DAMASCENO-JUNIOR, G.A., & SILVA, J.S.V. 2011. Plant diversity of the Pantanal wetland. Braz. J. Biol. 71(suppl.): 65-273.). It is considered a hotspot of biodiversity, with more than 2,000 species of vascular plants (Pott et al. 2011POTT, A., OLIVEIRA, A.K.M., DAMASCENO-JUNIOR, G.A., & SILVA, J.S.V. 2011. Plant diversity of the Pantanal wetland. Braz. J. Biol. 71(suppl.): 65-273.) and more than 2,000 species of animals, except terrestrial invertebrates (Junk et al. 2006JUNK, W.J., NUNES DA CUNHA, C., WANTZEN, K.M., PETERMANN, P., STRÜSSMANN, C., MARQUES, M.I. & ADIS, J. 2006. Biodiversity and its conservation in the Pantanal of Mato Grosso, Brazil. Aquat. Sci. 68:278-309.), with the seasonal flood-pulsing harboring habitat specialization (e.g., morphological, anatomical and physiological adaptations) (Junk et al. 2013JUNK, W.J., PIEDADE, M.T.F., LOURIVAL, R., WITTMANN, F., KANDUS, P., LACERDA, L.D., BOZELLI, R.L., ESTEVES, F.A., NUNES DA CUNHA, C., MALTCHIK, L., SCHÖNGART, J., SCHAEFFER‐NOVELLI, Y. & AGOSTINHO, A.A. 2013. Brazilian wetlands: their definition, delineation, and classification for research, sustainable management, and protection. Aquat. Conserv. 24:5-22.).

The interaction between plants and insects is still unexplored in North Pantanal, South-western of the State of Mato Grosso, in the Midwest region of Brazil. About 15% of the insect galls inventories made in Brazil were carried out in the Midwest region (Araújo et al. 2019ARAÚJO, W.S., FERNANDES, G.W. & SANTOS, J.C. 2019. An overview of inventories of gall-inducing insects in Brazil: looking for patterns and identifying knowledge gaps. An. Acad. Bras. Ciênc. 91(1):e20180162. http://dx.doi.org/10.1590/0001-3765201920180162 (last access on 20/12/2020).
http://dx.doi.org/10.1590/0001-376520192...
). Despite that, only two have been carried out in the Pantanal biome (Julião et al. 2002JULIÃO, G.R., AMARAL, M.E. & FERNANDES, G.W. 2002. Galhas de insetos e suas plantas hospedeiras no Pantanal Sul Mato Grossense. Naturalia. 27:47-74. , Urso-Guimarães et al. 2017URSO-GUIMARÃES, M.V., CASTELO, A.C.D., KATAOKA, E. & KOCH, I. 2017. Characterization of entomogen galls from Mato Grosso do Sul, Brazil. Rev. Bras. Entomol. 61:25-42.). Both in the State of Mato Grosso do Sul, which is strongly influenced by the Cerrado biome. Julião et al. (2002)JULIÃO, G.R., AMARAL, M.E. & FERNANDES, G.W. 2002. Galhas de insetos e suas plantas hospedeiras no Pantanal Sul Mato Grossense. Naturalia. 27:47-74. and Urso-Guimarães et al. (2017)URSO-GUIMARÃES, M.V., CASTELO, A.C.D., KATAOKA, E. & KOCH, I. 2017. Characterization of entomogen galls from Mato Grosso do Sul, Brazil. Rev. Bras. Entomol. 61:25-42. found 182 morphotypes of galls in 104 host plants, of which only nine plant species and three morphotypes were common. The richest plant family in Abobral was Bignoniaceae, and the super host species was Hippocratea volubilis L. (Julião et al. 2002JULIÃO, G.R., AMARAL, M.E. & FERNANDES, G.W. 2002. Galhas de insetos e suas plantas hospedeiras no Pantanal Sul Mato Grossense. Naturalia. 27:47-74. ). In Corumbá/Porto Murtinho, Fabaceae was the richest plant family and Serjania sp. the super host species (Urso-Guimarães et al. 2017URSO-GUIMARÃES, M.V., CASTELO, A.C.D., KATAOKA, E. & KOCH, I. 2017. Characterization of entomogen galls from Mato Grosso do Sul, Brazil. Rev. Bras. Entomol. 61:25-42.).

In this study, we present the first survey of gall-inducing insects for the North Pantanal, including the characterization of gall morphology and the identification of host plants. Our study represents the first step to understanding the richness of the history of host plants' interaction and gall-inducing insects in this biodiverse and unique biome.

In the last three months of 2020, the region of Pantanal Sul Matogrossense and Matogrossense (including Poconé) was devastated by an unprecedented fire. These months correspond to the Pantanal winter, in which the waters of the Paraguay River Basin should overflow the river channels and flood the plains around them. In this period, leaves fall, fruits, and branches accumulated in the litter, generating a formidable amount of food, all consumed by the primary consumers that occupy the food chain base and sustain the unique Pantanal biodiversity. But, in the winter of 2020, the flooding did not occur. All available dry matter functioned as fuel and burned large extensions of the Pantanal, destroying much this biome's rich fauna and flora due to deforestation, cleaning, and reforming pastures using improper management practice without control techniques endanger the conservation (Marengo et al. 2021MARENGO, J.A., CUNHA, A.P., CUARTAS, L.A, LEAL, K.R.D., BROEDEL, E, SELUCHI, M.E., MICHELIN, C.M, BAIÃO, C.F.D.P., ÂNGULO, E.C., ALMEIDA, E.K., KAZMIERCZAK, M.L., MATEUS, N.P.A., SILVA, R.C. & BENDER, F. 2021. Extreme Drought in the Brazilian Pantanal in 2019-2020: Characterization, Causes, and Impacts. Front. water. 3:e639204. https://doi.org/10.3389/frwa.2021.639204.
https://doi.org/10.3389/frwa.2021.639204...
). In this terrible scenario, our inventory represents a unique testimony of insect-plant interactions consumed by the fire.

Material and Methods

1. Study site

We conducted this study in two areas: Pousada Rio Clarinho and Transpantaneira Road Km 40, in Poconé Municipality (16°36'03.5" S, 56°43'46.1" W), State of Mato Grosso, Brazil (Fig. 1). This region is localized in the North Pantanal, also called Pantanal Matogrossense (Fig. 1). Its vegetation is considered a Pantanal mosaic because it is influenced by distinct biomes, with the Amazonia to the North, the Cerrado to the East, the Meridional Forests to the South, and the Chaco to the West (Pott et al. 2011POTT, A., OLIVEIRA, A.K.M., DAMASCENO-JUNIOR, G.A., & SILVA, J.S.V. 2011. Plant diversity of the Pantanal wetland. Braz. J. Biol. 71(suppl.): 65-273.). The Cerrado vegetation occupies 36% of the study area region, corresponding to 10% in the sub-region of Poconé (South-western of the State of Mato Grosso) (Silva et al. 2000SILVA, M.P., MAURO, R., MOURÃO, G.E. & COUTINHO, M. 2000. Distribuição e quantificação de classes de vegetação do Pantanal através de levantamento aéreo. Rev. Bras. Bot. 23:143-152.). The region's climate is the Tropical Climate of Savannah (Aw), with two well-defined seasons (hot and rainy in summer and dry and cold in winter). The seasonal flooding process is divided into four phases: flooding, flood, reflux, and dry (Costa et al. 2010COSTA, C.P., CUNHA, C.N. & COSTA, S.C. 2010. Caracterização da flora e estrutura do estrato arbustivo-arbóreo de um cerrado no Pantanal de Poconé, MT. Biota Neotrop. 10(3):61-73. http://dx.doi.org/10.1590/S1676-06032010000300006 (last access on 20/12/2020).
http://dx.doi.org/10.1590/S1676-06032010...
).

Figure 1
A. Map of South America indicating the Mato Grosso State and Cerrado and Pantanal Biomes extension in Brazil. B. Map of the of Cerrado and Pantanal areas with the sampling localities of North Pantanal in Poconé. C. Map of the sampling localities of Urso-Guimarães et al. (2017)URSO-GUIMARÃES, M.V., CASTELO, A.C.D., KATAOKA, E. & KOCH, I. 2017. Characterization of entomogen galls from Mato Grosso do Sul, Brazil. Rev. Bras. Entomol. 61:25-42. (Point 1- Universidade Estadual do Mato Grosso do Sul (UEMS), Aquidauana; Point 2 - Distrito de Camisão, Aquidauana; Point 3 - Sede da Fazenda Califórnia, Bodoquena; Point 4 - Base de Estudos do Pantanal, Corumbá; Point 5- Fazenda São Bento, Corumbá; Point 6 - Trilha Fazenda Retiro Conceição, Porto Murtinho; Point 7 - Trilha da Fazenda Campo Florido, Porto Murtinho) and of Julião et al. (2002)JULIÃO, G.R., AMARAL, M.E. & FERNANDES, G.W. 2002. Galhas de insetos e suas plantas hospedeiras no Pantanal Sul Mato Grossense. Naturalia. 27:47-74. (Point 1 - Rio Vermelho; Point 2 - Base de Estudos do Pantanal; Point 3 - MS-184 Highway; Point 4 - Fazenda São Bento) in Mato Grosso do Sul, Brazil.

2. Sampling

We performed two expeditions in a North Pantanal area in Poconé, State of Mato Grosso, Brazil, one in July 2012 and the other in January 2013. We selected two points to the collection, a floodable gallery forest along the Clarinho river (16° 36' 15.6" S/ 56° 43' 18.8" W), and a dry forest (Chaco edge) near the Transpantaneira Road (16° 35' 14.7" S/ 56° 44' 04.5" W), 3 kilometers apart from each other. We sampled along the trails' edges, with a 30-minute effort was made at each sampling point on each expedition, totaling 2 hours of effort following Price et al. (1998). We measured each route's length to quantify the sampled area (Urso-Guimarães et al. 2017URSO-GUIMARÃES, M.V., CASTELO, A.C.D., KATAOKA, E. & KOCH, I. 2017. Characterization of entomogen galls from Mato Grosso do Sul, Brazil. Rev. Bras. Entomol. 61:25-42.), covering 52 meters in floodable gallery forest trail and 129 meters in the dry forest trail. All gall sighted was collected, without limitation of habitus, stem diameter, or plant height. The collection method, labeling, processing samples, identification of plants, and insects followed Urso-Guimarães et al. (2017)URSO-GUIMARÃES, M.V., CASTELO, A.C.D., KATAOKA, E. & KOCH, I. 2017. Characterization of entomogen galls from Mato Grosso do Sul, Brazil. Rev. Bras. Entomol. 61:25-42. and Araújo et al. (2021)ARAÚJO W.S., URSO-GUIMARÃES M.V., MENDONÇA M..S. & SANTOS J.C. 2021. Sampling Galls and Galling Arthropods. In Measuring Arthropod Biodiversity (J.C.Santos & G.W. Fernandes, eds). Springer, Cham, p. 403-437.. The voucher specimens were deposited in the Universidade Federal de São Carlos: plants in the Herbarium SORO, and the insect material in the Laboratório de Sistemática de Diptera.

Results

We found 91 morphotypes of insect galls in 54 host plant species from 39 genera and 19 families (Table 1 and Figs. 2-5). On average, 1.7 gall morphotypes per plant species (for comparisons with other inventories in Pantanal areas, see Table 2). Four host plants are identified only at the family level, 16 at the genus level, and five are completely unidentified. We collected 83 gall morphotypes in the gallery forest and eight in the dry forest. The richest families in morphotypes are Fabaceae (N=19, 20.9%), Myrtaceae (N=14, 15.4%), and Sapindaceae (N=11, 12%). The richest plant genera in gall morphotypes were Bauhinia (N=11, 12%), Serjania (N=8, 8.8%), Psidium (N=7, 7.7%), and Combretum (N=5, 5.5%). The plant species considered super host were Psidium guineense Sw. (N=7, 7.7%), Combretum laxum Jacq., and the Unidentified sp. 3 (N=5, 5.5% each).

Table 1
Characterization of insect galls recorded in North Pantanal in Poconé, Mato Grosso State, Brazil organized by host plant. Figures refer to the picture of the gall morphotype. All galls are uni-chambered. New records of plants species as host of galls in the world are marked with asterisk.
Table 2
Richness of gall morphotypes and plant super-hosts families and species from localities in Brazilian Pantanal areas.

Figure 2
Insect galls of North Pantanal in Poconé, Mato Grosso State, Brazil in host plants indicated. Anacardiaceae. A. Astronium graveolens, Annonaceae. B. Annona cornifolia, Bignoniaceae. C. Dolichandra quadrivalvis, D. Bignoniaceae sp.1, E. Bignoniaceae sp.3, Chrysobalanaceae. F-G. Couepia sp., H. Leptobalanus gardneri, I. Leptobalanus humilis, J. Licania sp., Combretaceae. K-P. Combretum laxum, Q. Terminalia argentea, Dilleniaceae. R. Davilla elliptica, Euphorbiaceae. S. Maprounea guianensis, Fabaceae. T. Andira vermifuga, U-Z. Bauhinia cf. pulchella.

Figure 3
Insect galls of North Pantanal in Poconé, Mato Grosso State, Brazil in host plants indicated. Fabaceae. A-B. Bauhinia mollis, C-E. B. pentandra, F-G. B. platypetala, H-J. Fabaceae sp., K-L. Galactia glaucescens, M-N. Hymenaea courbaril, O. Senegalia sp., Lamiaceae. P. Aegiphila sp. 1, Q. Aegiphila sp., 2. Malpighiaceae. R-U. Byrsonima crassifolia, V-X. B. cydoniifolia, Moraceae. Z. Ficus sp.

Figure 4
Insect galls of North Pantanal in Poconé, Mato Grosso State, Brazil in host plants indicated. Myrtaceae. A-B. Campomanesia sp. C-D. Eugenia cf. florida, E. Eugenia sp., F. Myrcia neolucida, G-L. Psidium guineense, M. Myrtaceae sp., Polygonaceae. N-O. Symmeria paniculata, P. Polygonum acuminatum, Q. Triplaris gardneriana, R-S. Coccoloba cujabensis, Rubiaceae. T. Amaioua intermedia, U. Psychotria sp., Salicaceae. V. Casearia sp., Sapindaceae. X. Magonia pubescens, Z. Matayba sp. 3.

Figure 5
Insect galls of North Pantanal in Poconé, Mato Grosso State, Brazil in host plants indicated. Sapindaceae. A. Paullinia sp., B-D. Serjania caracasana, E-H. Serjania erecta, I. Serjania sp., Smilacaceae. J-K. Smilax sp., Solanaceae. L. Cestrum sp., Symplocaceae. M. Symplocos sp., Unidentified. N. Unidentified sp. 1, O. Unidentified sp. 2, P-R. Unidentified sp. 3, S. Unidentified sp. 4, T. Unidentified sp. 5.

The galls were induced mostly in leaves (N=67, 74%) and stem (N=19, 24%); the globoid (N=32, 35%) and lenticular (N=31, 34%) gall shapes are predominant. The colors green and brown were found in equal proportion (N=43; 47% each) and the glabrous galls are dominant (N=70; 77%).

In this inventory, fifteen plant species are new records as a host plant for insect galls in the world: Amaioua intermedia Mart. ex Schult. & Schult.f., Annona cornifolia A.St.-Hil., Bauhinia mollis (Bong.) D.Dietr., B. pentandra (Bong.) D.Dietr., B. platypetala Burch. ex Benth., Byrsonima cydoniifolia A.Juss., Coccoloba cujabensis Wedd, Dolichandra quadrivalvis (Jacq.) L.G.Lohmann, Galactia glaucescens Kunth, Leptobalanus gardneri (Hook.f.) Sothers & Prance, Myrcia neolucida A.R.Lourenço & E.Lucas, Polygonum acuminatum Kunth, Serjania caracasana (Jacq.) Willd., Symmeria paniculata Benth., and Triplaris gardneriana Wedd (Flora do Brasil 2020FLORA DO BRASIL 2020. Jardim Botânico do Rio de Janeiro. http://floradobrasil.jbrj.gov.br/ (last access on 10/06/2021).
http://floradobrasil.jbrj.gov.br/...
).

From the insect galls, 28 (30.8%) of the gall inducers were obtained and identified in 24 host plant species. Among the insect inducers, 60.7% belong to Diptera (N=17) and 21.4% to Hymenoptera (N=7), 7.1% to Hemiptera, and Thysanoptera (N=2 each), and 3.6% to Coleoptera (N=1). Associated fauna and other details are in Table 3. The gall inducers of 63 morphotypes are undetermined because the galls were collected empty, the specimens obtained were damaged or the morphological information in the instars obtained was insufficient to the identification. As in all surveys, the species of Cecidomyiidae were the predominant gall inducer species (Table 3).

Table 3
Gall makers and associated fauna in galls of North Pantanal in Poconé, Mato Grosso State, Brazil.

Discussion

The morphotype richness found in the gallery forests was significantly higher (N=83) when compared with the dry forest (N=8). The leaves are the organ most attacked by the gall makers in all environments (Araújo et al. 2019ARAÚJO, W.S., FERNANDES, G.W. & SANTOS, J.C. 2019. An overview of inventories of gall-inducing insects in Brazil: looking for patterns and identifying knowledge gaps. An. Acad. Bras. Ciênc. 91(1):e20180162. http://dx.doi.org/10.1590/0001-3765201920180162 (last access on 20/12/2020).
http://dx.doi.org/10.1590/0001-376520192...
), except for few studies with stems as the most affected organ always associated with dry environments (Veldtman & McGeoch 2003VELDTMAN, R. & MCGEOCH, M.A. 2003. Gall-forming insect species richness along a non-scleromorphic vegetation rainfall gradient in South Africa: the importance of plant community composition. Austral Ecol. 28:11-13., Fernandes et al. 2002FERNANDES, G.W., VARELA, O., BUCHER, E.H., CHANI, J.M., ECHEVARRÍA, A.L., ESPÍRITO SANTO, M.M., LIMA, NEGREIROS, J.D. & TOLEDO, C.S. 2002. Gall-forming insects on woody and herbaceous plant species of the semi-arid chaco forest, Argentina. Lundiana 3: 61-66., Carneiro et al. 2009CARNEIRO, M.A.A., BORGES, R.A.X., ARAÚJO, A.P.A. & FERNANDES, G.W. 2009. Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, Minas Gerais, Brasil. Rev. Bras. Entomol. 53(4):570-592., Coelho et al. 2013COELHO, M.S., CARNEIRO, M.A.A., BRANCO, C.A. & FERNANDES, G.W. 2013a. Gall-inducing insects from Serra do Cabral, Minas Gerais, Brazil. Biota Neotrop. 13(3):102-109. http://dx.doi.org/10.1590/S1676-06032013000300013 (last access on 20/12/2020).
http://dx.doi.org/10.1590/S1676-06032013...
, Toma & Mendonça 2013TOMA, T.S.P. & MENDONÇA, M.D.S. 2013. Gall inducing insects of an Araucaria Forest in Southern Brazil. Rev. Bras. Entomol. 57(2), 225-233., Kuzmanich et al. 2018KUZMANICH, N., GIORGIS, M.A., SALVO, A. 2018. Insect galls from Córdoba, Argentina: a case where stem galls predominate. Rev. Biol. Trop. 66(3): 1135-1148.). Thus, the host plant species' leaves loss during the dry season must have influenced the low number of galls found in the dry forest.

Fabaceae and Myrtaceae are two of the richest plant families in Pantanal (Pott et al. 2011POTT, A., OLIVEIRA, A.K.M., DAMASCENO-JUNIOR, G.A., & SILVA, J.S.V. 2011. Plant diversity of the Pantanal wetland. Braz. J. Biol. 71(suppl.): 65-273.). Pattern recovered in our study corroborating the hypothesis that families with the highest number of plant species also have the highest number of gall-forming species associated with them in all Brazilian biomes (Araújo et al. 2019ARAÚJO, W.S., FERNANDES, G.W. & SANTOS, J.C. 2019. An overview of inventories of gall-inducing insects in Brazil: looking for patterns and identifying knowledge gaps. An. Acad. Bras. Ciênc. 91(1):e20180162. http://dx.doi.org/10.1590/0001-3765201920180162 (last access on 20/12/2020).
http://dx.doi.org/10.1590/0001-376520192...
, Santos-Silva & Araújo 2020SANTOS-SILVA, J. & ARAÚJO, T.J. 2020. Are Fabaceae the principal super-hosts of galls in Brazil? An. Acad. Bras. Cienc. 92(2): e20181115. https://doi.org/10.1590/0001-3765202020181115.
https://doi.org/10.1590/0001-37652020201...
). Sapindaceae appears as the third richest family, because of Serjania Mill. It is a super host genus, with eight gall morphotypes in only three species, the same situation found by Urso-Guimarães et al. (2017URSO-GUIMARÃES, M.V., CASTELO, A.C.D., KATAOKA, E. & KOCH, I. 2017. Characterization of entomogen galls from Mato Grosso do Sul, Brazil. Rev. Bras. Entomol. 61:25-42.) in Corumbá. These results show the super host species' contribution to increasing the local richness of the insect-plant interactions, independently of plant species richness (Veldtman & McGeoch 2003VELDTMAN, R. & MCGEOCH, M.A. 2003. Gall-forming insect species richness along a non-scleromorphic vegetation rainfall gradient in South Africa: the importance of plant community composition. Austral Ecol. 28:11-13.).

Comparing with other studies in South Pantanal, our average (1.7) is similar to the other areas, Abobral region (1.7, Julião et al. 2002JULIÃO, G.R., AMARAL, M.E. & FERNANDES, G.W. 2002. Galhas de insetos e suas plantas hospedeiras no Pantanal Sul Mato Grossense. Naturalia. 27:47-74. ), and Corumbá/Porto Murtinho areas (1.4, Urso-Guimarães et al. 2017URSO-GUIMARÃES, M.V., CASTELO, A.C.D., KATAOKA, E. & KOCH, I. 2017. Characterization of entomogen galls from Mato Grosso do Sul, Brazil. Rev. Bras. Entomol. 61:25-42.) (Fig. 1, Table 3). From the richest plant genera in gall morphotypes, Bauhinia L. (Fabaceae) and Serjania (Sapindaceae) are species-rich genera. The plant species considered super host were Psidium guineense (N=7, 7.7%), Combretum laxum, and the Unidentified sp. 3 (N=5, 5.5% each) (Table 2). For the first time, P. guineense and C. laxum are reported as super hosts of gall morphotypes in the world.

The predominance of galls in leaves and stems with the globoid and lenticular shapes, the green and brown colors and glabrous is a pattern also found in Pantanal Sul-matogrossense (Julião et al. 2002JULIÃO, G.R., AMARAL, M.E. & FERNANDES, G.W. 2002. Galhas de insetos e suas plantas hospedeiras no Pantanal Sul Mato Grossense. Naturalia. 27:47-74. , Urso-Guimarães et al. 2017URSO-GUIMARÃES, M.V., CASTELO, A.C.D., KATAOKA, E. & KOCH, I. 2017. Characterization of entomogen galls from Mato Grosso do Sul, Brazil. Rev. Bras. Entomol. 61:25-42.) and in other biomes (Araújo et al. 2019ARAÚJO, W.S., FERNANDES, G.W. & SANTOS, J.C. 2019. An overview of inventories of gall-inducing insects in Brazil: looking for patterns and identifying knowledge gaps. An. Acad. Bras. Ciênc. 91(1):e20180162. http://dx.doi.org/10.1590/0001-3765201920180162 (last access on 20/12/2020).
http://dx.doi.org/10.1590/0001-376520192...
).

We found 91 morphotypes of galls in 54 host plants, of which 87 are new registers. Only four morphotypes are common to the studies of Julião et al. (2002)JULIÃO, G.R., AMARAL, M.E. & FERNANDES, G.W. 2002. Galhas de insetos e suas plantas hospedeiras no Pantanal Sul Mato Grossense. Naturalia. 27:47-74. and Urso-Guimarães et al. (2017)URSO-GUIMARÃES, M.V., CASTELO, A.C.D., KATAOKA, E. & KOCH, I. 2017. Characterization of entomogen galls from Mato Grosso do Sul, Brazil. Rev. Bras. Entomol. 61:25-42.: the lenticular, brown, and glabrous on leaves of Bauhinia mollis, the fusiform in stems of Psidium guineense, the globoid, green, and glabrous on leaves of Magonia pubescens A.St.-Hil., and the globoid, green, and glabrous on leaves of Serjania caracasana. Thus, Brazilian Pantanal has 269 morphotypes of galls in 157 plant species, of which only two species are common of the three studies, Eugenia florida DC. and S. caracasana.The fifteen new records of host plants found in this inventory represent 30% of the total host plant species sampled in the Poconé survey (Table 2).

We also found that only three plant species, Coccoloba cujabensis, Symmeria paniculata, and Triplaris gardneriana, occur in Pantanal and Cerrado areas. These species occur exclusively in Mato Grosso and Mato Grosso do Sul States, which means the insect's interactions and these species are endemic. The low endemicity was expected because the plant species distributed in North Pantanal undergoes other biomes' influence in its composition (Pott et al. 2011POTT, A., OLIVEIRA, A.K.M., DAMASCENO-JUNIOR, G.A., & SILVA, J.S.V. 2011. Plant diversity of the Pantanal wetland. Braz. J. Biol. 71(suppl.): 65-273.).

The interactions among plants and associated entomofauna are still unknown and threatened with extinction due to deforestation. Mato Grosso State is currently one of the agricultural frontiers in Brazil. The maintenance and encouragement of taxonomic studies, such as the SISBIOTA - Diptera Brazil Program (2010-2015), are necessary to understand gall inducers' richness. Before studies funded by the SISBIOTA, only of gall inducers (Termitomastus leptoproctus Silvestri, 1901 and Schizomyia tuiuiu Urso-Guimarães & Amorim, 2002 - Diptera, Cecidomyiidae) were registered in Mato Grosso State. Three new species of cecidomyiids found in this survey are under the process of description, one species of each of the genera Bruggmanniella Tavares, Schizomyia Kieffer, and Youngomyia Felt.

This inventory became a unique testimony of insect-plant interactions in Pantanal Biome in Brazil that may have been completely devastated by fire in the dry season of 2020. We hope that with its enormous resilience, the Pantanal biome will recover the unique biodiversity lost by fire. We also expected that international organizations help Brazilian institutions to pressure the Federal Government to adopt measures for the conservation of Pantanal, a biome from South America, but is essential for humanity.

Acknowledgements

MVUG acknowledges the Conselho Nacional de Desenvolvimento Científico e Tecnológico (Proc. CNPq 563256/2010-9) and Fundação de Amparo à Pesquisa do Estado de São Paulo (Proc. Fapesp 10/52314-0) for the support to the field works under the SISBIOTA - Diptera Brazil Program. The authors also thank J. Semir - in memorian, J. Tamashiro, G.H. Shimizu, and A.V. Scatigna (IB/UNICAMP), R.B. Pinto (UFG), and M. Monge (UFU) for invaluable help in plant species identification.

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Publication Dates

  • Publication in this collection
    19 July 2021
  • Date of issue
    2021

History

  • Received
    08 Jan 2021
  • Reviewed
    10 June 2021
  • Accepted
    13 June 2021
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