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Gall-inducing insects from Campos de Altitude, Brazil

Abstracts

Gall-inducing insects are very specious in vegetations of southeastern Brazil. Our goal was describe the gall richness by characterizing their external forms and their patterns of occurrence on host plants. Samples were collected from Campos de Altitude at four regions of the Mantiqueira Range: 1) Parque Estadual da Serra do Brigadeiro, 2) Parque Nacional do Caparaó, 3) Parque Estadual do Ibitipoca, 4) Parque Nacional do Itatiaia. We found 93 gall species within 13 families, 30 genera and 50 host plant species. We recorded 38 gall species in Parque Estadual da Serra do Brigadeiro, 21 in Parque Nacional do Caparaó, 23 in Parque Estadual do Ibitipoca and 20 in Parque Nacional do Itatiaia. Asteraceae represented 33% of the species collected, followed by Melastomataceae at 17%; with each one concentrating 56% and 18% of the galling insects, respectively. 98% of galls were Cecydomiidae (Diptera). The most attacked organ was the stem (56%), followed by the leaf (23%). Only 12% of the galls described in our study had been already recorded in previous studies, thus reinforcing the need to increase the sampling effort toward a better understanding of the richness and the natural history of gall-inducing insects from Brazil.

biodiversity; biogeography; herbivory; host plant; altitude


Insetos indutores de galhas são muito ricos em espécies nas formações vegetais do sudeste do Brasil. O objetivo deste estudo foi descrever a riqueza de morfotipos de galha por meio da caracterização de suas formas externas e os padrões de ocorrência nas plantas hospedeiras. As amostragens foram realizadas em campos rupestres e altitudinais de quatro regiões da Serra da Mantiqueira: 1) campos de altitude do Parque Estadual do Brigadeiro e 2) Parque Nacional do Caparaó, 3) Parque Estadual do Ibitipoca e Parque Nacional do Itatiaia. Foram registradas 93 espécies de galhas induzidas por insetos em 13 famílias, 30 gêneros e 50 espécies de plantas hospedeiras. Sendo 38 a riqueza de insetos indutores de galhas do Parque Estadual do Brigadeiro, 21 do Parque Nacional do Caparaó, 23 do Parque Nacional do Caparaó e 20 do Parque Nacional do Itatiaia. As famílias com maior riqueza foram Asteraceae (33%) e Melastomataceae (17%). A família Cecydomiidae (Diptera) foi a mais frequente (98%). O órgão mais atacado foi o caule (56%) seguido de folha (23%). O fato de apenas 12% das galhas descritas neste estudo já terem sido registradas em trabalhos anteriores, reforça a necessidade em aumentar o esforço amostral na direção de um maior conhecimento sobre a riqueza e história natural dos insetos indutores de galhas no Brasil.

biodiversidade; biogeografia; herbivoria; planta hospedeira; altitude


Introduction

Galls are produced by an increase in the size (hypertrophy) and/or in the number of plant cells (hyperplasia), which results in the formation of symmetrical structures in one or more organs of the host plant (Mani 1964MANI, M.S. 1964. The ecology of plant galls. Junk, The Hague., Raman 2007RAMAN, A. 2007. Insect-induced plant galls of India: unresolved questions. Curr Sci. 92:748-757.). Gall-inducing insects are considered the most sophisticated and capable due to their ability to manipulate the host plants for their benefit (Abrahamson & Weis 1997ABRAHAMSON, W.G. & WEIS, A.E. 1997. Evolutionary ecology across three trophic levels: goldenrods, gallmakers and natural enemies. Princeton University Press, New Jersey, 456p., Shorthouse et al. 2005SHORTHOUSE, J.D., WOOL, D. & RAMAN, A. 2005. Gall-inducing insects - Nature's most sophisticated herbivores. Basic. Appl. Ecol. 6:407-411. http://dx.doi.org/10.1016/j.baae.2005.07.001
http://dx.doi.org/10.1016/j.baae.2005.07...
, Fernandes et al. 2010FERNANDES, G.W., COELHO, MS. & LÜTTGE, U. 2010. Photosynthetic efficiency of Clusia arrudae leaf tissue with and without Cecidomyiidae galls. Braz. J. Biol. 70:723-728. PMid:21085778. http://dx.doi.org/10.1590/S1519-69842010000400004
http://dx.doi.org/10.1590/S1519-69842010...
). Galls could be considered to be an extension of the inductor phenotype, since their morphological characteristics depend on the inductor genotype as well as on environmental factors such as heat, humidity, and soil (Weis et al. 1988WEIS, A.E., WALTON, R. & CREGO, C.L. 1988. Reactive plant tissue sites and the population biology of gall makers. Annu Rev Entomol. 33:467-486. http://dx.doi.org/10.1146/annurev.en.33.010188.002343
http://dx.doi.org/10.1146/annurev.en.33....
). Galls can be induced by bacteria, fungi, algae, nematodes, rotifers, copepods, plant (Loranthaceae), however, the most common are those induced by insects (Raman et al. 2005RAMAN, A., SCHAEFER, C.W. & WITHERS, T.M. 2005. Biology, ecology, and evolution of gall-inducing arthropods. Science, New Hampshire.). Recent estimates point to a richness of around 130,000 species of Gall-inducing insects on the face of the planet with approximations ranging from 5 to 30 million insect species (Espírito-Santo & Fernandes 2007ESPÍRITO-SANTO, M.M. & FERNANDES, G.W. 2007. How many species of gall- inducing insects are there on earth, and where are there? Ann Entomol. Soc. Am. 100:95-99.). Despite the high richness of gall morphotypes recorded in several Brazilian ecosystems, only 159 species have been described in Brazil (Maia 2005MAIA, V.C. 2005. Catálogo dos Cecidomyiidae (Diptera) do estado do Rio de Janeiro. Biota. Neotrop. 5:1-26. http://dx.doi.org/10.1590/S1676-06032005000300014
http://dx.doi.org/10.1590/S1676-06032005...
); and, considering the height diversity of these ecosystems, very few studies have been conducted which focus on the natural history and descriptions of gall morphotypes. Some of the ecosystems were only recently sampled, while others are still awaiting research (Coelho et al. 2009COELHO, M.S., ALMADA, E.D., FERNANDES, G.W., CARNEIRO, M.A.A., SANTOS, R.M., QUINTINO, A.V. & SANCHEZ-AZOFEIFA, A. 2009. Gall inducing arthropods from a seasonally dry tropical forest in Serra do Cipó, Brazil. Rev. Bras. Entomol. 53:404-414. http://dx.doi.org/10.1590/S0085-56262009000300015
http://dx.doi.org/10.1590/S0085-56262009...
). We are not aware of any studies conducted on Campos de Altitude from Serra da Mantiqueira.

The Campos de Altitude were named by Barreto (1949)BARRETO, H.L. 1949. Regiões fitogeográficas de Minas Gerais. Bol. Geogr. 14:14-28. of “Campos Alpinos” and by Rizzini (1963)RIZZINI, C.T. 1963. Nota prévia sobre a divisão fitogeográfica do Brasil. Instituto Brasileiro de Geografia Estatística, Rio de Janeiro. of “Campos Altimontanos”. However, these classifications include ecosystems that, despite their physiognomic similarities, differ in lithological characteristics, geological origins, surrounding matrix, as well as in biological characteristics, such as floristic composition (Rizzini 1979RIZZINI, C.T. 1979. Tratado de fitogeografia do Brasil. Hucitec, São Paulo.). As a result of said differences, the fields located at high altitudes were subdivided into “Campos Quartizíticos” and “Campos Altimontanos” by Rizzini (1979)RIZZINI, C.T. 1979. Tratado de fitogeografia do Brasil. Hucitec, São Paulo. and later into “Campos Rupestres” and “Campos de Altitude” by Ferri (1980)FERRI, M.G. 1980. Vegetação Brasileira. Editora da Universidade de São Paulo, São Paulo..

Campos Rupestres are composed predominantly of quartzite and sandstone rocks and are mainly associated with the Cerrado, although they can be found immersed in matrices of other biomes (Caiafa & Silva 2005CAIAFA, A.N. & SILVA, A.F. 2005. Composição florística e espectro biológico de um campo de altitude no Parque Estadual da Serra do Brigadeiro, Minas Gerais- Brasil. Rodriguésia. 56:163-173.). Unlike the Campos Rupestres, the Altitudinal Fields occur predominantly on granite rocks and are immersed in a matrix of Atlantic Rainforest (Moreira & Camelier 1977MOREIRA, A.A.N. & CAMELIER, C. 1977. Relevo. In Geografia do Brasil: Região Sudeste. Fundação Instituto Brasileiro de Geografia e Estatística, Rio de Janeiro, p.1-50.). The vegetation of both physiognomies is predominantly dominated by herbs and shrubs, however, Asteraceae, Melastomataceae, Orchidaceae, Bromeliaceae are the most common families in Campos de Altitude whereas, Asteraceae, Xyridaceae, Velloziaceae, Cyperaceae, and Melastomataceae are the most common families in the Rupestrian Fields. Adding to their biological and geological importance, mountain environments from southeastern Brazil are headwaters regions. For example, the Campos de Altitude associated with “Serra do Mar” and the Mantiqueira Range are responsible for supplying the water needs of 25% of the Brazilian population which may explain, per se their conservation (Safford 1999SAFFORD, H.D. 1999. Brazilian Páramos I: An introduction to the physical environment and vegetation of the campos de altitude. J. Biogeogr. 26:693-712. http://dx.doi.org/10.1046/j.1365-2699.1999.00313.x
http://dx.doi.org/10.1046/j.1365-2699.19...
). Furthermore, Campos de Altitude from Mantiqueira Range and their disjunctions are associated with the Cerrado and Atlantic Rain Forest biomes, two biodiversity hotspots (Myers et al. 2000MYERS, N., MITTERMEIER, R.A., MITTERMEIER, C.G., FONSECA, G.A.B. & KENT, J. 2000. Biodiversity hotspots for conservation priorities. Nature 403:853-858. PMid:10706275. http://dx.doi.org/10.1038/35002501
http://dx.doi.org/10.1038/35002501...
).

This work is part of a project to describe the natural history of galling insects, their galls, and their host plants at Campos de Altitude from Serra da Mantiqueira and Espinhaço Range (Carneiro et al. 2009bCARNEIRO, M.A.A., BORGES, R.A.X., ARAÚJO, A.P.A. & FERNANDES, G.W. 2009b. Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, MG. Rev. Bras. Entomol. 53:570-592. http://dx.doi.org/10.1590/S0085-56262009000400007
http://dx.doi.org/10.1590/S0085-56262009...
). Our goal was describe the gall richness through the characterization of the shape and occurrence patterns of the gall as related to its host plants at four regions of Serra da Mantiqueira.

Material and Methods

Samples were collected in four Campos de Altitude from Mantiqueira Range: 1) Parque Estadual do Brigadeiro (PESB), 2) Parque Nacional do Caparaó (PNC), 3) Parque Estadual do Ibitipoca (PEIB) and 4) Parque Nacional do Itatiaia (PNI).

The PESB is located in the “Zona da Mata” of Minas Gerais, between the meridians 42° 20′ and 42° 40′ S and the parallels 20° 20′ and 21° 00′ (Engevix 1995ENGEVIX. 1995. Caracterização do meio físico da área autorizada para criação do Parque Estadual da Serra do Brigadeiro - Relatório técnico final dos estudos - 8296-RE-H4-003/94 “VER. 1”. Instituto Estadual da Floresta, BIRD/PRÓ- FLORESTA/SEPLAN, Belo Horizonte.). Its lithology consists largely of granite formations (Machado-Filho et al. 1983MACHADO-FILHO, L., RIBEIRO, M.W., GONZALEZ, S.R., SCHENINI, C.A., SANTOS-NETO, A., PALMEIRA, R.C.B., PIRES, J.L., TEIXEIRA, W. & CASTRO, H.E.F. 1983. Geologia. In Projeto RADAMBRASIL (Brasil). Rio de Janeiro, Vitória, p.56-66.). The climate is classified as medium mesothermal (CWb) with an annual average temperature and rainfall of 18 °C and 1,300 mm, respectively. The predominant vegetation is composed of secondary semi-deciduous forest fragments (Veloso et al. 1991VELOSO, H.P., RANGEL FILHO, A.L.R. & LIMA, J.C.A. 1991. Classificação da vegetação brasileira, adaptada a um sistema universal. Departamento de Recursos Naturais e Estudos Ambientais, Rio de Janeiro.) and altitudinal fields (Ferri 1980FERRI, M.G. 1980. Vegetação Brasileira. Editora da Universidade de São Paulo, São Paulo.). A floristic survey carried out in Altitudinal Fields from PESB Caiafa & Silva (2005)CAIAFA, A.N. & SILVA, A.F. 2005. Composição florística e espectro biológico de um campo de altitude no Parque Estadual da Serra do Brigadeiro, Minas Gerais- Brasil. Rodriguésia. 56:163-173. recorded 81 vascular plant species, with Asteraceae and Orchidaceae standing out as the most representative families.

The PNE is located between the states of Minas Gerais and Espírito Santo (20° 25′ S, 41° 48′ W) (Safford 2001SAFFORD, H.D. 2001. Brazilian Paramos. III. Patterns and Rates of Postfire Regeneration in the Campos de Altitude. Biotropica 33:282-302.). The soil is predominantly composed of metamorphic rocks (Machado-Filho et al. 1983MACHADO-FILHO, L., RIBEIRO, M.W., GONZALEZ, S.R., SCHENINI, C.A., SANTOS-NETO, A., PALMEIRA, R.C.B., PIRES, J.L., TEIXEIRA, W. & CASTRO, H.E.F. 1983. Geologia. In Projeto RADAMBRASIL (Brasil). Rio de Janeiro, Vitória, p.56-66.). The average temperature is 10.5 °C whereas the rainfall is 1800mm (Safford 2001SAFFORD, H.D. 2001. Brazilian Paramos. III. Patterns and Rates of Postfire Regeneration in the Campos de Altitude. Biotropica 33:282-302.). The vegetation is composed of secondary semi-deciduous forests fragments and Altitudinal Fields above 2250m (Safford 2001SAFFORD, H.D. 2001. Brazilian Paramos. III. Patterns and Rates of Postfire Regeneration in the Campos de Altitude. Biotropica 33:282-302.).

The PEIB is located in the southeast of Minas Gerais (21° 42′ S, 43° 54′ W). The soil is predominantly quartzitic (Fundação... 1983). The average temperature is 18.9 °C whereas the rainfall is 1395 mm (Lemos & Melo-Franco 1976LEMOS, A.B. & MELO-FRANCO, M.V. 1976. Situação atual dos Parques Florestais e Reservas Biológicas de Minas Gerais. Fund. J. Pin. 6:33-41.). The climate is classified as medium mesothermal (CWb) (Fundação... 1983) and the region hosts different vegetation types: grassy fields, Rupestrian Fields, Fields with shrubs and small trees and wet forests “Capões de Mata” (Andrade & Souza 1995ANDRADE, P.M. & SOUZA, H.C. 1995. Contribuição ao conhecimento da vegetação do Parque Estadual do Ibitipoca, Lima Duarte Minas Gerais. Rev. arvore. 19:249-261.). Previous floristic studies have demonstrated the great importance of the region for concentrate a high biodiversity and high number of endemic species (Rodela 1998).

The PNI (22° 21′ S and 44° 40′ W) is located in central Mantiqueira range with a marked seasonality of cold, dry winters and hot, wet summers. The average temperature and precipitation is 14 °C and 2400 mm, respectively (Ribeiro et al. 2007RIBEIRO, T.R., MEDINA, B.M.O. & SCARANO, F.R. 2007. Species composition and biogeographic relations of the rock outcrop flora on the high plateau of Itatiaia, SE-Brazil. Rev. Bras. Bot. 30:623-639. http://dx.doi.org/10.1590/S0100-84042007000400008
http://dx.doi.org/10.1590/S0100-84042007...
). The fields are located in heights above 2000 meters with 550 described species (Safford 1999SAFFORD, H.D. 1999. Brazilian Páramos I: An introduction to the physical environment and vegetation of the campos de altitude. J. Biogeogr. 26:693-712. http://dx.doi.org/10.1046/j.1365-2699.1999.00313.x
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), of which 11% are endemic.

Gall sampling was performed following the methodology described by Fernandes & Price (1988FERNANDES, G.W. & PRICE, P.W. 1988. Biogeographical gradients in galling species richness: tests of hypotheses. Oecologia. 76:161-167. http://dx.doi.org/10.1007/BF00379948
http://dx.doi.org/10.1007/BF00379948...
, but see also Price et al. 1998PRICE, P.W., FERNANDES, G.W., LARA, A.C.F., BRAWN, J., GERLING, D., BARRIOS, H., WRIGHT, M.G., RIBEIRO, S.P. & ROTHCLIFF, N. 1998. Global patterns in local number of insect galling species. J. Biogeogr. 25:581-591. http://dx.doi.org/10.1046/j.1365-2699.1998.2530581.x
http://dx.doi.org/10.1046/j.1365-2699.19...
). At each sampling point a plot with 100 woody plants (between 0.3 and 2 m high) was arbitrarily selected, totaling 1,000 plants in each region and 4,000 plants overall. Each plant was sampled throughout the aerial part of the individual by direct counting of gall morphotypes. Forests, areas close to trails, or any areas with visible human interference were excluded from the sampling.

According to Carneiro et al. (2009a)CARNEIRO, M.A.A., BRANCO, C.S.A., BRAGA, C.E.D., ALMADA, E.D., COSTA, M.B.M., FERNANDES, G.W. & MAIA, V.C. 2009a. Are gall midge species (Diptera: Cecidomyiidae) host plant specialists? Rev. Bras. Entomol. 53:365-378. http://dx.doi.org/10.1590/S0085-56262009000300010
http://dx.doi.org/10.1590/S0085-56262009...
gall description associated with the identification of host-plant species is a reliable richness indicator of the gall-inducing insects. About 95% of described species of Cecidomyiids from Brazil can be identified based on the external shape associated with the host plant on which it occurs, reinforcing the use of this methodology as reliable in galling studies (Price et al. 1998PRICE, P.W., FERNANDES, G.W., LARA, A.C.F., BRAWN, J., GERLING, D., BARRIOS, H., WRIGHT, M.G., RIBEIRO, S.P. & ROTHCLIFF, N. 1998. Global patterns in local number of insect galling species. J. Biogeogr. 25:581-591. http://dx.doi.org/10.1046/j.1365-2699.1998.2530581.x
http://dx.doi.org/10.1046/j.1365-2699.19...
, Blanche 2000BLANCHE, K.R. 2000. Diversity of insect-induced galls along a temperature-rainfall gradient in the tropical savannah region of the Northern Territory, Australia. Austral Ecol. 25:311-318. http://dx.doi.org/10.1046/j.1442-9993.2000.01040.x
http://dx.doi.org/10.1046/j.1442-9993.20...
, Cuevas-Reyes et al. 2003CUEVAS-REYES, P., SIEBE, C., MARTÍNEZ-RAMOS, M. & OYAMA, K. 2003. Species richness of gall-forming insects in a tropical rain forest: correlations with plant diversity and soil fertility. Biodivers. Conserv. 12:411-422.3 http://dx.doi.org/10.1023/A:1022415907109
http://dx.doi.org/10.1023/A:102241590710...
, 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. 92:707-716., Oyama et al. 2003OYAMA, K., PÉREZ-PÉREZ, M.A., CUEVAS-REYES, P. & LUNA-REYES, R. 2003. Regional and local species richness of gall-inducing insects in two tropical rain forests in Mexico. J. Trop. Ecol. 19:595-598. http://dx.doi.org/10.1017/S0266467403003651
http://dx.doi.org/10.1017/S0266467403003...
).

The host plant samples and their galls were mounted and deposited in the herbariums OUPR and BHCB (acronyms according to Holmgren et al. 1990HOLMGREN, P.K., HOLMGREN, N.H. & BARNETT, L.C. 1990. Index Herbariorum. Part I: The Herbaria of The World. New York Botanical Garden, New York.). The collected plants were separated into families and were then identified by specialists to the lowest taxonomic level possible. The classification of plant species followed the system proposed by Angiosperm Phylogeny Group II (2003). The galls were photographed and categorized according to color, shape, presence or absence of hairs and in accordance to the organ where they occurred (see Carneiro et al. 2009bCARNEIRO, M.A.A., BORGES, R.A.X., ARAÚJO, A.P.A. & FERNANDES, G.W. 2009b. Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, MG. Rev. Bras. Entomol. 53:570-592. http://dx.doi.org/10.1590/S0085-56262009000400007
http://dx.doi.org/10.1590/S0085-56262009...
). Galling insects were always identified when possible.

Results

In a universe of 51 families, 118 genera and 222 plant species, 93 gallind species in 13 families, 30 genera and 50 host plant species were recorded (Table 1 and 2, Figure 1-5). There were 38 gall species in PESB, 23 in PNC, 21 in PEIB and 20 in PNI. The families that concentrated the highest gall richness were those with the largest number of records. Asteraceae represented 33% of plant species collected followed by Melastomataceae, with 17%, and each concentrated 56% and 18%, of gall species, respectively.

Figure 1.
Host plants and their galls at Campos de Altitude from four regions located at Serra da Mantiqueira, Minas Gerais. PEB = Parque Estadual do Brigadeiro, PNC = Parque Nacional do Caparaó, PIB = Parque Estadual do Ibitipoca, PNI=Parque Nacional do Itatiaia. Asteraceae (Aspilia foliosa (a-b), Baccharis aratatubensis (c), Baccharis brevifolia (d), Baccharis dubia (e), Baccharis itatiaiae (f-i), Baccharis myriocephala (j), Baccharis platypoda (k-r), Baccharis pseudomyriocephala (s-t)).

Figure 2.
Host plants and their galls at Campos de Altitude from four regions located at Serra da Mantiqueira, Minas Gerais. PEB = Parque Estadual do Brigadeiro, PNC = Parque Nacional do Caparaó, PIB = Parque Estadual do Ibitipoca, PNI=Parque Nacional do Itatiaia. Asteraceae (Baccharis pseudomyriocephala (a-d), Baccharis reticularia (e-h), Baccharis salzmanii (i-n), Baccharis stylosa (o-p), Baccharis trimera (q), Baccharis uncinella (r-s), Cyrtocymura scorpioides (t).

Figure 3.
Host plants and their galls at Campos de Altitude from four regions located at Serra da Mantiqueira, Minas Gerais. PEB = Parque Estadual do Brigadeiro, PNC = Parque Nacional do Caparaó, PIB = Parque Estadual do Ibitipoca, PNI=Parque Nacional do Itatiaia. Asteraceae (Cyrtocymura scorpioides (a-b), Grazielia gaudichaudeana (c), Hololepis pedunculata (d), Mikania reticulata (e), Pseudobrickellia angustissima (f), Symphyopappus brasiliensis (g-i), Symphyopappus itatiayensis (j), Erementhus erythropappa (k-l)), Ericaceae (Gaylussacia decipiens (m)), Euphorbiaceae (Croton buxifolius (n-o), Croton dichrous (p), Croton migrans (q), Croton splendidus (r)), Fabaceae (Dalbergia sp. (s)), Lamiaceae (Hyptis monticola (t)).

Figure 4.
Host plants and their galls at Campos de Altitude from four regions located at Serra da Mantiqueira, Minas Gerais. PEB = Parque Estadual do Brigadeiro, PNC = Parque Nacional do Caparaó, PIB = Parque Estadual do Ibitipoca, PNI=Parque Nacional do Itatiaia. Lamiaceae (Hyptis racemulosa (a), sp1 (b)), Lauraceae (Ocotea tristis (c), Diplusodon buxifolius (d), Malpighiaceae (Byrsonima variabilis (e)), Melastomataceae (Camponanesia rufa (f), Lavoisiera compta (g), Leandra aurea (h), Marcetia taxifolia (i), Microlicia sp. (j-k), Tibouchina faveolata (l-o), Tibouchina collina (p), Tibouchina hospita (q), Tibouchina martiusiana (r), Tibouchina multiflora (s-t).

Figure 5.
Host plants and their galls at Campos de Altitude from four regions located at Serra da Mantiqueira, Minas Gerais. PEB = Parque Estadual do Brigadeiro, PNC = Parque Nacional do Caparaó, PIB = Parque Estadual do Ibitipoca, PNI=Parque Nacional do Itatiaia. Melastomataceae (Tibouchina multiflora (a), Tibouchina sp. (b) Myrsinaceae (Myrsine coriacea (c-d)), Orchidaceae (Epidendrum secundum (e-f)), Pentaphylacaceae (Ternstroemia brasiliensis (g-h), Poaceae (Chusquea pinifolia (i)), Verbenaceae (Lantana sp1 (j-k), sp1 (l), sp2 (m)).

Table 1.
Host plants, description of gall-inducing insects at Campos de Altitude from four regions located at Serra da Mantiqueira (PEB = Parque Estadual do Brigadeiro, PNC = Parque Nacional do Caparaó, PIB = Parque Estadual do Ibitipoca, PNI=Parque Nacional do Itatiaia).

Tabela 2.
Number of gall-inducing insects associated to plant families at Campos de Altitude from Serra da Mantiqueira, Minas Gerais. Families without galls were listed as “other families” (Amaryllidaceaem, Apocynaceae, Asclepiadaceae, Celastraceae, Cunnonaceae, Dennstaldtaliaceae, Escalloniaceae, Gesnariaceae, Lycopodiaceae, Lythraceae, Myrtaceae, Onagraceae, Orabanchaceae, Oxalacidaceae, Phyllanthaceae, Piperaceae, Proteaceae, Rubiaceae, Salicaceae, Scrophulariaceae, Solanaceae, Turneraceae, Velloziaceae).

Again, the genera and species that concentrated the greatest gall richness belong to the plant families with the highest occurrence, Asteraceae (33%) and Melastomataceae (17%). The genera that concentrated the most gall richness were Baccharis (Asteraceae) 40% followed by Tibouchina (Melastomataceae) (12%). The species with the greatest gall richness were Baccharis platypoda DC. (9%), Baccharis salzmanii DC. (6%), Baccharis pseudomyriocephala (6%), Baccharis reticularia DC. (4%), Baccharis itatiaie (4%), Tibouchina faveolata (4%). The family Cecidomyiidae (Diptera) was the most frequent (98%), followed by Tephritidae (Diptera) (1%) and the order Lepidoptera (1%).

The most common gall shapes were intumescence (26%), fusiform (25%), globose (16%) and discoid (13%). The most attacked organ was the stem (56%), followed by the leaf (32%) and the terminal branch (11%). Eighty-nine percent (89%) of galls were glabrous.

Discussion

Gall-inducing insects and their host plants have been widely studied in recent decades in different Brazilians vegetation types, e.g.: Pantanal (Julião et al. 2002JULIÃO, G.R., AMARAL, M.E.C. & FERNANDES, G.W. 2002. Galhas de insetos e suas plantas hospedeiras no Pantanal sul-mato-grossense. Naturalia. 27:47-74.), Amazon (Julião et al. 2005JULIÃO, G.R., VENTICINQUE, E.M., FERNANDES, G.W. & KRAUS, J.E. 2005. Richness and abundance of gall-forming insects in the Mamirauá Varzea, a flooded Amazoniam forest. Uakari. 1:39-42., Almada & Fernandes 2011ALMADA, E.D. & FERNANDES, G.W. 2011. Insetos indutores de galhas em florestas de terra-firme em reflorestamentos com espécies nativas na Amazônia Oriental. Bol. Mus. Para. Emilio Goeldi. Ser. Cienc. Nat. 6:1-10., Maia 2012MAIA, V.C. 2012. Characterization of insect galls, gall makers, and associated fauna of Platô Bacaba (Porto de Trombetas, Pará, Brazil). Biota. Neotrop. 11:1-17.), Restinga (Maia 2001MAIA, V.C. 2001. The gall midges (Diptera, Cecidomyiidae) from three restingas of Rio de Janeiro State, Brazil. Rev. Bras. Zool. 18:583-629. http://dx.doi.org/10.1590/S0101-81752001000200028
http://dx.doi.org/10.1590/S0101-81752001...
, 2005MAIA, V.C. 2005. Catálogo dos Cecidomyiidae (Diptera) do estado do Rio de Janeiro. Biota. Neotrop. 5:1-26. http://dx.doi.org/10.1590/S1676-06032005000300014
http://dx.doi.org/10.1590/S1676-06032005...
, Maia et al. 2002MAIA, V.C., AZEVEDO, M.A.P. & COURI, M.S. 2002. New contribution to the knowledge of the gall midges (Diptera, Cecidomyiidae) from the restinga of Barra de Maricá (Rio de Janeiro, Brazil). Stud Diptero. 9:447-452., Mendonça 2007MENDONÇA, M.S. 2007. Plant diversity and galling arthropod diversity searching for taxonomic patterns in an animal-plant interaction in the neotropics. B. Soc. Arg. Bot. 42:347-357., Oliveira & Maia 2005OLIVEIRA, J.C. & MAIA, V.C. 2005. Ocorrência e caracterização de galhas de insetos na restinga de Grumari (Rio de Janeiro, RJ, Brasil). Arq. Mus. Nac. 63:669-675.), Cerrado (Fernandes & Price 1988FERNANDES, G.W. & PRICE, P.W. 1988. Biogeographical gradients in galling species richness: tests of hypotheses. Oecologia. 76:161-167. http://dx.doi.org/10.1007/BF00379948
http://dx.doi.org/10.1007/BF00379948...
, Maia & Fernandes 2004MAIA, V.C. & FERNANDES, G.W. 2004. Insect galls from Serra de São José (Tiradentes, MG, Brazil.). Rev. Bras. Biol. 6:423-445., Gonçalves-Alvim & Fernandes 2001GONÇALVES-ALVIM, S.J. & FERNANDES, G.W. 2001. Biodiversity of galling insects: historical, community and habitat effects in four neotropical savannas. Biodivers. Conserv. 10:79-98. http://dx.doi.org/10.1023/A:1016602213305
http://dx.doi.org/10.1023/A:101660221330...
), Rupestrian Fields (Carneiro et al. 2009bCARNEIRO, M.A.A., BORGES, R.A.X., ARAÚJO, A.P.A. & FERNANDES, G.W. 2009b. Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, MG. Rev. Bras. Entomol. 53:570-592. http://dx.doi.org/10.1590/S0085-56262009000400007
http://dx.doi.org/10.1590/S0085-56262009...
), Tropical Dry Forest on Limestone Outcrops (Coelho et al. 2009COELHO, M.S., ALMADA, E.D., FERNANDES, G.W., CARNEIRO, M.A.A., SANTOS, R.M., QUINTINO, A.V. & SANCHEZ-AZOFEIFA, A. 2009. Gall inducing arthropods from a seasonally dry tropical forest in Serra do Cipó, Brazil. Rev. Bras. Entomol. 53:404-414. http://dx.doi.org/10.1590/S0085-56262009000300015
http://dx.doi.org/10.1590/S0085-56262009...
) and Caatinga (Santos et al. 2011SANTOS, J.C., ALMEIDA-CORTEZ, J.S. & FERNANDES, G.W. 2011. Righness of gall-inducing insects in the tropical dry forest (caatinga) of Pernambuco. Rev. Bras. Entomol. 55:45-54. http://dx.doi.org/10.1590/S0085-56262011000100009
http://dx.doi.org/10.1590/S0085-56262011...
). This is the first study that describes the galls and host plants of Campos de Altitude.

In this study, we documented 93 gall-inducing insects, from those only 23 (23%) had been previously recorded. Previous studies have reported Baccharis platypoda DC. (Table 1, Figure 1(k, l, m, n, o) with 5 galls (Fernandes et al. 1996FERNANDES, G.W., CARNEIRO, M.A.A., LARA, A.C.F., ALLAIN, L.R., JULIÃO, G.R., ANDRADE, G.I., REIS, T.R. & SILVA, I.M. 1996. Galling insects on neotropical species of Baccharis (Asteraceae). Trop. Zool. 9:315-332. http://dx.doi.org/10.1080/03946975.1996.10539315
http://dx.doi.org/10.1080/03946975.1996....
, Carneiro et al. 2009bCARNEIRO, M.A.A., BORGES, R.A.X., ARAÚJO, A.P.A. & FERNANDES, G.W. 2009b. Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, MG. Rev. Bras. Entomol. 53:570-592. http://dx.doi.org/10.1590/S0085-56262009000400007
http://dx.doi.org/10.1590/S0085-56262009...
); Baccharis pseudomyriocephala (Table 1, Figure 1(s, t), 2(a, b, c, d) with 6 galls (Araújo et al. 2003ARAÚJO, A.P.A., CARNEIRO, M.A.A. & FERNANDES, G.W. 2003. Efeitos do sexo, do vigor e do tamanho da planta hospedeira sobre a distribuição de insetos indutores de galhas em Baccharis pseudomyriocephala Teodoro (Asteraceae). Rev. Bras. Entomol. 47:483-490. http://dx.doi.org/10.1590/S0085-56262003000400001
http://dx.doi.org/10.1590/S0085-56262003...
); Baccharis reticularia (Table 1, Figure 2(e,f,g,h) with 4 galls (Carneiro et al. 2009bCARNEIRO, M.A.A., BORGES, R.A.X., ARAÚJO, A.P.A. & FERNANDES, G.W. 2009b. Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, MG. Rev. Bras. Entomol. 53:570-592. http://dx.doi.org/10.1590/S0085-56262009000400007
http://dx.doi.org/10.1590/S0085-56262009...
); Baccharis salzmanii DC. (Table 1, Figure 2(k,m) with 2 galls (Carneiro et al. 2009bCARNEIRO, M.A.A., BORGES, R.A.X., ARAÚJO, A.P.A. & FERNANDES, G.W. 2009b. Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, MG. Rev. Bras. Entomol. 53:570-592. http://dx.doi.org/10.1590/S0085-56262009000400007
http://dx.doi.org/10.1590/S0085-56262009...
); Baccharis trimera (Table 1, Figure 2(q) with 1 gall (Carneiro et al. 2009bCARNEIRO, M.A.A., BORGES, R.A.X., ARAÚJO, A.P.A. & FERNANDES, G.W. 2009b. Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, MG. Rev. Bras. Entomol. 53:570-592. http://dx.doi.org/10.1590/S0085-56262009000400007
http://dx.doi.org/10.1590/S0085-56262009...
), Hololepis penduculata (Table 1, Figure 3(d)) with 1 gall (Carneiro et al. 2009bCARNEIRO, M.A.A., BORGES, R.A.X., ARAÚJO, A.P.A. & FERNANDES, G.W. 2009b. Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, MG. Rev. Bras. Entomol. 53:570-592. http://dx.doi.org/10.1590/S0085-56262009000400007
http://dx.doi.org/10.1590/S0085-56262009...
); Mikania meticulata (Table 1, Figure 3(e)) with 1 gall (Carneiro et al. 2009bCARNEIRO, M.A.A., BORGES, R.A.X., ARAÚJO, A.P.A. & FERNANDES, G.W. 2009b. Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, MG. Rev. Bras. Entomol. 53:570-592. http://dx.doi.org/10.1590/S0085-56262009000400007
http://dx.doi.org/10.1590/S0085-56262009...
); Symphyopappus brasiliensis (Table 1, Figure 3(g,h)) with 2 galls (Carneiro et al. 2009bCARNEIRO, M.A.A., BORGES, R.A.X., ARAÚJO, A.P.A. & FERNANDES, G.W. 2009b. Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, MG. Rev. Bras. Entomol. 53:570-592. http://dx.doi.org/10.1590/S0085-56262009000400007
http://dx.doi.org/10.1590/S0085-56262009...
). The fact that only 23% of the galls described in this study have already been recorded in previous studies reinforces the need to increase the sampling efforts of gall-inducing insects in Brazil.

The families Asteraceae and Melastomataceae are the richest and most abundant in Altitudinal and Rupestrian Fields in Brazil (Martinelli 1996MARTINELLI, G. 1996. Campos de Altitude. Editora Index, Rio de Janeiro.). In this study, the family Asteraceae was also the most frequent, representing 33% of the plants collected, followed by the Melastomataceae (17%). These results corroborate data of Safford (1999)SAFFORD, H.D. 1999. Brazilian Páramos I: An introduction to the physical environment and vegetation of the campos de altitude. J. Biogeogr. 26:693-712. http://dx.doi.org/10.1046/j.1365-2699.1999.00313.x
http://dx.doi.org/10.1046/j.1365-2699.19...
from Campos de Altitude. The author demonstrates that Asteraceae represents (20%) of all the floristic richness, whereas the genus Baccharis is responsible for 5% of it. The host plant pattern was the same. Asteraceae responded for 56% of total host plants followed by Melastomataceae (18%).

Gall-inducing insects are commonly found in plant families and genera richest in species (Fernandes 1992FERNANDES, G.W. 1992. Plant age and size effects on insular gall-forming species richness. GLOBAL. Ecol. Biogeogr. 2:71-74. http://dx.doi.org/10.2307/2997508
http://dx.doi.org/10.2307/2997508...
, Blanche & Westoby 1995BLANCHE, K.R. & WESTOBY, M. 1995. Gall-forming insect diversity is linked to soil fertility via host plant taxon. Ecology. 76:2334-2337. http://dx.doi.org/10.2307/1941706
http://dx.doi.org/10.2307/1941706...
). Although the families Asteraceae and Melastomataceae concentrated 74% of the gall-inducing insects, only two genera, Baccharis (Asteraceae) (42%) and Tibouchina (Melastomataceae) (12%) responded for 54% of the total. Previous studies have shown that some taxa concentrate a large number of galls (Fernandes & Price 1988FERNANDES, G.W. & PRICE, P.W. 1988. Biogeographical gradients in galling species richness: tests of hypotheses. Oecologia. 76:161-167. http://dx.doi.org/10.1007/BF00379948
http://dx.doi.org/10.1007/BF00379948...
, Fernandes et al. 1996FERNANDES, G.W., CARNEIRO, M.A.A., LARA, A.C.F., ALLAIN, L.R., JULIÃO, G.R., ANDRADE, G.I., REIS, T.R. & SILVA, I.M. 1996. Galling insects on neotropical species of Baccharis (Asteraceae). Trop. Zool. 9:315-332. http://dx.doi.org/10.1080/03946975.1996.10539315
http://dx.doi.org/10.1080/03946975.1996....
, Blanche 2000BLANCHE, K.R. 2000. Diversity of insect-induced galls along a temperature-rainfall gradient in the tropical savannah region of the Northern Territory, Australia. Austral Ecol. 25:311-318. http://dx.doi.org/10.1046/j.1442-9993.2000.01040.x
http://dx.doi.org/10.1046/j.1442-9993.20...
). Some genera have been considered super-hosts. Working with Baccharis, Fernandes et al. (1996)FERNANDES, G.W., CARNEIRO, M.A.A., LARA, A.C.F., ALLAIN, L.R., JULIÃO, G.R., ANDRADE, G.I., REIS, T.R. & SILVA, I.M. 1996. Galling insects on neotropical species of Baccharis (Asteraceae). Trop. Zool. 9:315-332. http://dx.doi.org/10.1080/03946975.1996.10539315
http://dx.doi.org/10.1080/03946975.1996....
reported 121 gall species in only 40 host plant species. In another study, Carneiro et al. (2009b)CARNEIRO, M.A.A., BORGES, R.A.X., ARAÚJO, A.P.A. & FERNANDES, G.W. 2009b. Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, MG. Rev. Bras. Entomol. 53:570-592. http://dx.doi.org/10.1590/S0085-56262009000400007
http://dx.doi.org/10.1590/S0085-56262009...
recorded that Baccharis has the highest number of gall-inducing insects in Rupestrian Fields from the Espinhaço Range. Thus, Baccharis may be the taxon that hosts the greatest number of gall-inducing insects in the Neotropics.

Investigating the correlation of the effects of soil fertility on gall-inducing insect richness in Australian National Parks, Blanche & Westoby (1995)BLANCHE, K.R. & WESTOBY, M. 1995. Gall-forming insect diversity is linked to soil fertility via host plant taxon. Ecology. 76:2334-2337. http://dx.doi.org/10.2307/1941706
http://dx.doi.org/10.2307/1941706...
found a negative correlation, however spurious. The authors argue that the genus Eucalyptus (Myrtaceae) is richer and more abundant on infertile environments and for concentrate a greater galling insect richness would be the main cause of the pattern. Other genera, such as Salix (Salicaceae) and Quercus (Fagaceae), are known to host great galling insect richness (Price 1992PRICE, P.W. 1992. Evolution and ecology of gall-inducing sawflies. In Biology of insect-induced galls. (J.D. Shorthouse, & O. Rohfritsch, eds.) Oxford University Press, New York, p.208-224.). One of the factors that contributes to the genera Eucalyptus, Quercus, Salix concentrating a greater galling richness is the fact that they recover quickly from impacts such as fire, severe droughts, as well as intense herbivory (Price 1992PRICE, P.W. 1992. Evolution and ecology of gall-inducing sawflies. In Biology of insect-induced galls. (J.D. Shorthouse, & O. Rohfritsch, eds.) Oxford University Press, New York, p.208-224., Blanche & Westoby 1995BLANCHE, K.R. & WESTOBY, M. 1995. Gall-forming insect diversity is linked to soil fertility via host plant taxon. Ecology. 76:2334-2337. http://dx.doi.org/10.2307/1941706
http://dx.doi.org/10.2307/1941706...
). The same can be said about the genera Baccharis and Eremanthus in Rupestrian Fields of the Espinhaço Range (M.A.A. Carneiro Personal Observation. But see also Carneiro et al. 2009bCARNEIRO, M.A.A., BORGES, R.A.X., ARAÚJO, A.P.A. & FERNANDES, G.W. 2009b. Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, MG. Rev. Bras. Entomol. 53:570-592. http://dx.doi.org/10.1590/S0085-56262009000400007
http://dx.doi.org/10.1590/S0085-56262009...
). However, further studies are needed in order to find factors that explain the high galling insect richness associated with these super diverse genera. In our study, 98% of galling species belong to the family Cecidomyiidae (Diptera); this reflects the great richness of this family in Brazil and in the Neotropics (Gagné 1994GAGNÉ, R.J. 1994. The gall midges of the region neotropical. Comstock, Ithaca., Fernandes et al. 2001FERNANDES, G.W., JULIÃO, G.R., ARAÚJO, R.C., ARAÚJO, S.C., LOMBARDI, J.A., NEGREIROS, D. & CARNEIRO, M.A.A. 2001. Distribution and morphology of insect galls of the Rio Doce Valley, Brazil. Naturalia. 26:211-244., 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. 92:707-716.).

Descriptive studies of gall-inducing insects in Brazil have a pattern that relates to the host plant organs most often attacked. Studies conducted in different biomes such as Cerrado (Maia & Fernandes 2004MAIA, V.C. & FERNANDES, G.W. 2004. Insect galls from Serra de São José (Tiradentes, MG, Brazil.). Rev. Bras. Biol. 6:423-445.), Atlantic Rain Forest (Fernandes & Negreiros 2006FERNANDES, G.W. & NEGREIROS, D. 2006. A comunidade de insetos galhadores da RPPN Fazenda Bulcão, Aimorés, Minas Gerais, Brasil. Lundiana. 7:111-120.), Pantanal (Julião et al. 2002JULIÃO, G.R., AMARAL, M.E.C. & FERNANDES, G.W. 2002. Galhas de insetos e suas plantas hospedeiras no Pantanal sul-mato-grossense. Naturalia. 27:47-74.), Tropical Dry Forests (Coelho et al. 2009COELHO, M.S., ALMADA, E.D., FERNANDES, G.W., CARNEIRO, M.A.A., SANTOS, R.M., QUINTINO, A.V. & SANCHEZ-AZOFEIFA, A. 2009. Gall inducing arthropods from a seasonally dry tropical forest in Serra do Cipó, Brazil. Rev. Bras. Entomol. 53:404-414. http://dx.doi.org/10.1590/S0085-56262009000300015
http://dx.doi.org/10.1590/S0085-56262009...
) point to higher gall richness on leaves. However, in our study, 56% of the galls concentrated on stems, while only 32% concentrated on leaves. These results differ from most studies to date. Working in Rupestrian Fields across the Espinhaço Range, Carneiro et al. (2009b)CARNEIRO, M.A.A., BORGES, R.A.X., ARAÚJO, A.P.A. & FERNANDES, G.W. 2009b. Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, MG. Rev. Bras. Entomol. 53:570-592. http://dx.doi.org/10.1590/S0085-56262009000400007
http://dx.doi.org/10.1590/S0085-56262009...
also found the same pattern of high gall richness on stems. The authors argue that insects hosted in the plant stems have a greater resistance to mechanical damage and availability of tissues of higher nutritional quality than those on leaves (see also 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. 28:1-13. http://dx.doi.org/10.1046/j.1442-9993.2003.01234.x
http://dx.doi.org/10.1046/j.1442-9993.20...
, Inbar et al. 2004INBAR, M., WINK, M. & WOOL D. 2004. The evolution of host plant manipulation by insects: molecular and ecological evidence from gall-forming aphids on Pistacia. Mol. Phylogenet. Evol. 32:504-511. PMid:15223033. http://dx.doi.org/10.1016/j.ympev.2004.01.006
http://dx.doi.org/10.1016/j.ympev.2004.0...
, Price 2005PRICE, P.W. 2005. Adaptative radiation of gall-inducing insects. Basic. Appl. Ecol. 6:413-421. http://dx.doi.org/10.1016/j.baae.2005.07.002
http://dx.doi.org/10.1016/j.baae.2005.07...
). Protection against external factors is one of the main selective pressures for the gall-inducing insects (Price et al. 1987PRICE, P.W., FERNANDES, G.W. & WARING, G.L. 1987. Adaptative nature of insect galls. Environ Entomol. 16:15-24.). However, it is unclear as to why the results from Rupestrian Fields and Campos de Altitude were the only ones to show this pattern in Brazil. Perhaps, since these sites are more exposed to abiotic factors such as wind, temperature variations and high fire frequency (Giulietti et al. 1987GIULIETTI, A.M., MENEZES, N.L., PIRANI, J.R., MEGURO, M.L. & WANDERLEY, M.G.L. 1987. Flora da Serra do Cipó: Caracterização e lista de espécies. Bol. Bot. Univ. São Paulo. 9:1-152., Giulietti & Pirani 1988GIULIETTI, A.M. & PIRANI, J.R. 1988. Patterns of Geographic distribution of some Plant Species from the Espinhaço Range, Minas Gerais, Brazil. In Proceedings of a Workshop on Neotropical Biodiversity Distribution Patterns (P.E. Vanzolini & W.R. Heyer, ed.). Academia Brasileira de Ciências, Rio de Janeiro, p.39-69., Safford 1999SAFFORD, H.D. 1999. Brazilian Páramos I: An introduction to the physical environment and vegetation of the campos de altitude. J. Biogeogr. 26:693-712. http://dx.doi.org/10.1046/j.1365-2699.1999.00313.x
http://dx.doi.org/10.1046/j.1365-2699.19...
, 2001SAFFORD, H.D. 2001. Brazilian Paramos. III. Patterns and Rates of Postfire Regeneration in the Campos de Altitude. Biotropica 33:282-302.), different from other Brazilian ecosystems, (Julião et al. 2002JULIÃO, G.R., AMARAL, M.E.C. & FERNANDES, G.W. 2002. Galhas de insetos e suas plantas hospedeiras no Pantanal sul-mato-grossense. Naturalia. 27:47-74., Fernandes & Negreiros 2006FERNANDES, G.W. & NEGREIROS, D. 2006. A comunidade de insetos galhadores da RPPN Fazenda Bulcão, Aimorés, Minas Gerais, Brasil. Lundiana. 7:111-120.) there exists a selective pressure that favors a greater number of stem galls.

Studies relating to richness patterns and to natural history of gall-inducing insects in Brazil are still incipient (Maia 2005MAIA, V.C. 2005. Catálogo dos Cecidomyiidae (Diptera) do estado do Rio de Janeiro. Biota. Neotrop. 5:1-26. http://dx.doi.org/10.1590/S1676-06032005000300014
http://dx.doi.org/10.1590/S1676-06032005...
). This is the first study that describes the galls and their host plants from Altitudinal Fields. Among the seven priorities for research and conservation of Campos de Altitude traced by Safford (1999)SAFFORD, H.D. 1999. Brazilian Páramos I: An introduction to the physical environment and vegetation of the campos de altitude. J. Biogeogr. 26:693-712. http://dx.doi.org/10.1046/j.1365-2699.1999.00313.x
http://dx.doi.org/10.1046/j.1365-2699.19...
, stands out the need for increased efforts in floristic and faunal inventories. Poor understanding of the biological resources from conservation units as well as the lack of knowledge of what is endemic or what is threatened hinders the proper management of natural resources and prevents the mapping, endemism analysis, geographical distribution as well as diversity patterns, essential for the development of conservation strategies. Therefore, further research is required in order to reach a better understanding of gall-inducing insect richness, given the importance of this guild for biodiversity conservation and its significance as a model for ecological studies.

We thank the two anonymous reviewers for the critical review and suggestions on the manuscript, Valeri Garcia for the English improvement and Dr. João Renato Stehmann for plant identifications. The Instituto Estadual de Florestas I.E.F. for logistical support. To FAPEMIG (2893/98) and CNPq (472811/2006-1; 30.9633/2007-9) for financial support. To CAPES for the scholarship awarded to M. S. Coelho and M. A. A. Carneiro. This study was in partial fulfillment for the requirements for the degree of Masters of Science in Ecology, Conservation and Management of Wildlife of M. S. Coelho, at the Universidade Federal de Minas Gerais.

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Publication Dates

  • Publication in this collection
    Dec 2013

History

  • Received
    24 Oct 2012
  • Reviewed
    24 Oct 2012
  • Accepted
    18 Nov 2013
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