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Diversity of gall-inducing insects in the high altitude wetland forests in Pernambuco, Northeastern Brazil

Diversidade de insetos indutores de galhas em brejos de altitude de Pernambuco, Nordeste do Brasil

Abstracts

We report on the richness of galling insects in the altitudinal wetland forests of Pernambuco State, Northeastern Brazil. We found 80 distinct types of insect galls on 49 species of host plants belonging to 28 families and 35 genera. Most of the galled plant species belong to Nyctaginaceae, Fabaceae, Meliaceae, Sapindaceae and Myrtaceae. The most common gall were spheroid and globoid; most galls were glabrous, predominantly green and with one chamber, and on the leaves. Most galls were induced by Cecidomyiidae (Diptera). The results of this study contribute to existing knowledge richness of galling insects and host-plant diversity in the altitudinal wetland forests of Northeastern Brazil.

insect galls; species richness; Cecidomyiidae; insect herbivory; host plants


Este artigo reporta sobre a riqueza de insetos galhadores em brejos de altitude de Pernambuco, Brasil. Foram encontrados 80 morfotipos de galhas sobre 49 espécies de plantas hospedeiras pertencentes a 28 famílias e 35 gêneros. Muitas das plantas galhadas pertencem a Nyctaginaceae, Fabaceae, Meliaceae, Myrtaceae e Sapindaceae. Os tipos morfológicos de galhas mais comuns foram esferoide e globoide, glabro, predominantemente verde e com uma câmara, e sobre as folhas. Muitas galhas foram induzidas por Cecidomyiidae (Diptera). Os resultados deste estudo contribuem para o conhecimento da riqueza de insetos galhadores e da diversidade de plantas hospedeiras em brejos de altitude do nordeste do Brasil.

galhas entomógenas; riqueza de espécies; Cecidomyiidae; insetos herbívoros; plantas hospedeiras


ECOLOGY

Diversity of gall-inducing insects in the high altitude wetland forests in Pernambuco, Northeastern Brazil

Diversidade de insetos indutores de galhas em brejos de altitude de Pernambuco, Nordeste do Brasil

Santos, JC.I, * * e-mail: jcsantos@inbio.ufu.br ; Almeida-Cortez, JS.II; Fernandes, GW.III

IInstituto de Biologia, Universidade Federal de Uberlândia - UFU, CP 593, CEP 38400-902, Uberlândia, MG, Brazil

IIDepartamento de Botânica, Centro de Ciências Biológicas, Universidade Federal de Pernambuco - UFPE, Av. Prof. Moraes Rêgo, s/n, CEP 50670-901, Recife, PE, Brazil

IIIEcologia Evolutiva & Biodiversidade, Departamento de Biologia Geral - DBG, Instituto de Ciencias Biologicas - ICB, Universidade Federal de Minas Gerais - UFMG, CEP 30161-970, Belo Horizonte, MG, Brazil

ABSTRACT

We report on the richness of galling insects in the altitudinal wetland forests of Pernambuco State, Northeastern Brazil. We found 80 distinct types of insect galls on 49 species of host plants belonging to 28 families and 35 genera. Most of the galled plant species belong to Nyctaginaceae, Fabaceae, Meliaceae, Sapindaceae and Myrtaceae. The most common gall were spheroid and globoid; most galls were glabrous, predominantly green and with one chamber, and on the leaves. Most galls were induced by Cecidomyiidae (Diptera). The results of this study contribute to existing knowledge richness of galling insects and host-plant diversity in the altitudinal wetland forests of Northeastern Brazil.

Keywords: insect galls, species richness, Cecidomyiidae, insect herbivory, host plants.

RESUMO

Este artigo reporta sobre a riqueza de insetos galhadores em brejos de altitude de Pernambuco, Brasil. Foram encontrados 80 morfotipos de galhas sobre 49 espécies de plantas hospedeiras pertencentes a 28 famílias e 35 gêneros. Muitas das plantas galhadas pertencem a Nyctaginaceae, Fabaceae, Meliaceae, Myrtaceae e Sapindaceae. Os tipos morfológicos de galhas mais comuns foram esferoide e globoide, glabro, predominantemente verde e com uma câmara, e sobre as folhas. Muitas galhas foram induzidas por Cecidomyiidae (Diptera). Os resultados deste estudo contribuem para o conhecimento da riqueza de insetos galhadores e da diversidade de plantas hospedeiras em brejos de altitude do nordeste do Brasil.

Palavras-chave: galhas entomógenas, riqueza de espécies, Cecidomyiidae, insetos herbívoros, plantas hospedeiras.

1. Introduction

The tropical altitudinal wet forests of Northeastern Brazil, locally known as "brejos de altitude", are enclaves of the Atlantic forest in altitudes above 500 m, forming "islands" of wet forest surrounded by semi-arid vegetation (caatinga) (Tabarelli and Santos, 2004). These forest islands are important for the maintenance of biological diversity for two main reasons: 1) many species are endemic, and they represent an important endemism centre; and 2) the altitudinal wet forests share several species with both the Atlantic rain forest and the Amazon rain forest; making this ecosystem singular (see Pôrto et al., 2004a).

Despite its great biological importance, there are exceedingly few ecological studies on insects in the altitudinal wet forests. In the latest review on altitudinal wet forests (see Pôrto et al., 2004a), only some termites (Isoptera) (Bandeira and Vasconcellos, 2004), bees (Hymenoptera) (Locatelli et al., 2004) and butterflies (Lepidoptera) (Gusmão-Creão and Duarte, 2004) were studied. Contrarily, the studies of some insect guilds are increasing in the Atlantic rain forests, as in galling insects. For instance, Fernandes et al. (2001) reported the galling insect richness and their host plants in the Rio Doce Valley, Minas Gerais, while Dalbem and Mendonça (2006) and Mendonça (2007) the diversity of galling arthropods and host plants in a subtropical forest of Southern Brazil; Fernandes and Negreiros (2006) and Moreira et al. (2007) provided information on galling insect community in a disturbed area; and Maia (2005) reported the diversity of the cecidomyiids (95 species) in the state of Rio de Janeiro. To our knowledge there is no study on galling insects in the altitudinal wet forests. Hence, for the first time, we report on the richness of galling insects in the altitudinal wet forests of Pernambuco in an attempt to broaden our knowledge of galling species diversity in the Atlantic forest and northeastern Brazil.

2. Material and Methods

2.1. Study area

This study was conducted in seven altitudinal wet forests of Pernambuco State, Brazil: Reserva Municipal de Bonito - Brejo de Bonito (Bonito municipality), Brejo de Bituri Grande - Brejo da Madre de Deus (Brejo Madre de Deus municipality), Reserva Biológica de Serra Negra - Brejo de Serra Negra (Bezerros municipality), Brejo de Taquaritinga do Norte (Taquaritinga do Norte municipality), Brejo de Triunfo (Trunfo municipality), Parque Municipal João Vasconcelos Sobrinho - Brejo dos Cavalos e Brejo da Serra Água Doce (Caruaru municipality). These areas were chosen arbitrarily to cover the maximum of forest variability in the State of Pernambuco and to avoid pseudo-replication between the areas (Figure 1).


2.2. Sampling galling insects richness

The altitudinal wet forests were investigated for galls over a period of seven months from January to September of 2008. In each site, galling insect richness was sampled by two people following the adapted methodology of random walking (see Julião et al., 2002; Fernandes and Negreiros, 2006), where instead of an hour-long survey, we spent three hours in each area. To maximise the sampling of richness, a distance of at least 500 m was established among the sites sampled inside the areas (Fernandes and Price, 1988). All plant organs were investigated, and each gall and host plant (up to 3 m in height) found were collected, placed in plastic bags, and then taken to a laboratory for photographic registration and description of the gall external morphology. Host plants were classified into morphospecies in the field, and later at the species level in the Herbarium UFPE (Universidade Federal de Pernambuco). The classification of species of host plants followed the system proposed by Angiosperm Phylogeny Group II (APG II, 2003), and the authors and scientific host plant names were checked on the Missouri Botanical Garden website "http://mobot.mobot.org/W3T/Search/classicvast.html". In general, 95% species of insect induce a gall on a specific tissue of a certain plant species (Carneiro et al., 2009). The use of morphospecies to represent the galling species richness has been used in several studies in different ecosystems (e.g., Price et al., 1998; Cuevas-Reyes et al., 2004; Fernandes and Negreiros, 2006; Moreira et al., 2007). Galls were characterised as reported by Fernandes and Price (1988): host plant species, number of types of galls by host plant, type of host tissue attacked, shape of galls, colour of galls, presence or absence of pubescence, and number of chambers in the gall, occurrence on the galled organ: isolated or grouped/coalescent. We chose to present only a list with the probable inducers of gall makers because many galls were naturally damaged, or without the presence of the inducer or with parasited larvae.

3. Results

We found 80 morphologically distinct types of insect galls in the altitudinal wet forests of Pernambuco. These galls were found on 49 species of host plants belonging to 28 families and 35 genera (Table 1, Figure 2). The richness of galling insects was greater in the Brejo dos Cavalos (32 species) followed by Brejo de Bonito (27 species), Brejo da Madre de Deus (15 morphotypes), Brejo de Serra Negra (eight species), Brejo de Taquaritinga do Norte (five species), Brejo de Triunfo (three species), and Brejo da Serra Água Doce with two species. The majority of insect galls were induced by species of the family Cecidomyiidae (81.25%) followed by Heteroptera (5%), Lepidoptera (1.25%), while we could not identify the remaining 12.50% (undetermined). The host plant families that supported the greater number of species of galls were: Nyctaginaceae (18.99%), Fabaceae (12.66%), Meliaceae (10.13%), and Sapindaceae and Myrtaceae with 8.86% each. The genera with the greatest number of species of galls were: Guapira (Nyctaginaceae) (15 species), Guarea (Meliaceae) (eight species), Myrcia (Myrtaceae) (six species), and Paullinia (Sapindaceae) with five species. Most galls were induced on the leaves (72.5%), followed by stems (10.0%), simultaneously on leaves and stems (6.25%), and on apical buds (5.0%). The most frequent shape of galls was spheroid (27.50%), followed by globoid (21.25%). Eighty-one percent of galls were glabrous; 53.75% were predominantly green, while 81.25% did not form clusters.


4. Discussion

Some studies on insect gall richness conducted in the Atlantic forest are concentrated in the South and Southeast of Brazil and our study represents the first contribution to the understanding on this herbivore guild distribution and diversity in the upland tropical wet forest ecosystems. A comparison with the data from other Brazilian Atlantic rain forests indicates that the richness of the insect galls in the upland forest of Pernambuco (80 species) is comparatively smaller. For instance, Fernandes et al. (2001) reported on 273 galling species in the Atlantic rain forests of the Rio Doce Valley. However, it is important to emphasize that these comparisons between studies should be viewed with caution by differences in methodology, sampling size and time. Many sampled areas of altitudinal wet forests have suffered a strong degradation in their ecosystems; e.g., loss of habitat, hunting, wood extraction, agriculture and fragmentation (see Tabarelli and Santos, 2004). Moreover, these ecosystems are true mountain top islands within the semi-arid vegetation (caatinga), and therefore, they had a smaller spatial area compared to areas of continuous Atlantic rain forests of the coast. All these factors may contribute to a reduction in the richness of insect galls in this ecosystem.

Although the purpose of this study is not to compare the richness of galling insects among sample areas, it is important to emphasize the great richness of insect galls species in the Brejo dos Cavalos (32 species) and Brejo de Bonito (27 species). This result can be interpreted because these areas have high biological diversity of important groups, such as bryophytes (Pôrto et al., 2004b) and host plants (e.g., Rodal et al., 2005) to both areas, bromeliads to Caruaru (Siqueira Filho, 2004), which indicates a high degree of preservation and conservation of these areas, and therefore a greater diversity of galling insects.

This is the first descriptive study on galling insect richness done in the altitudinal wet forests. However, many other areas of altitudinal wet forests inside the caatinga matrix are to be studied before they are totally degraded, and in order to reach a better understanding of the distribution of galling insects and their host plants along the tropical forests.

Acknowledgements - We thank two anonymous reviewers, Mr. Gilcean for field work, A. Aguiar (Patriota) for figure design, and the financial support was provided by DCR-FACEPE/CNPq (DCR-0087-2.05/06, APQ-0008-2.05/07), CNPq (309633/2007-9) and FAPEMIG (PRI-00121/10).

Received 18 June, 2009

Accepted 17 August, 2009

Distributed February 28, 2011

  • APGII - ANGIOSPERM PHYLOGENY GROUP, 2003. An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APGII. Botanical Journal of the Linnean Society, vol. 141, p. 399-436.
  • BANDEIRA, AG. and VASCONCELLOS, A., 2004. Efeitos de distúrbios florestais sobre as populações de cupins (isoptera) do brejo dos cavalos, Pernambuco. In PORTO, KC., CABRAL, JJP. and TABARELLI, M. (Orgs.). Brejos de Altitude em Pernambuco e Paraíba: História Natural, Ecologia e Conservação. Brasília, DF: Ministério do Meio Ambiente, p. 145-152. Série Biodiversidade, 9.
  • CARNEIRO, MAA., BORGES, RAX., ARAÚJO, APA. and FERNANDES, GW., 2009. Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, MG. Revista Brasileira de Entomologia, vol. 54, no. 4, p. 570-592.
  • CUEVAS-REYES, P., QUESADA, M., HANSON, P., DIRZO, R. and 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. Journal of Ecology, vol. 92, no. 4, p. 707-716.
  • DALBEM, RV. and MENDONÇA Jr., MS., 2006. Diversity of galling arthropods and host plants in a subtropical forest of Porto Alegre, Southern Brazil. Neotropical Entomology, vol. 35, no. 5, p. 616-624.
  • FERNANDES, GW. and NEGREIROS, D., 2006. A comunidade de insetos galhadores da RPPN Fazenda Bulcão, Aimorés, Minas Gerais, Brasil. Lundiana, vol. 7, no. 2, p. 111-120.
  • FERNANDES, GW. and PRICE, PW., 1988. Biogeographical gradients in galling species richness: tests of hypotheses. Oecologia,vol. 76, no. 22, p. 161-167.
  • FERNANDES, GW., JULIÃO, GR., ARAÚJO, RC., ARAÚJO, SC., LOMBARDI, JA., NEGREIROS, D. and CARNEIRO, MAA., 2001. Distribution and morphology of insect galls of the Rio Doce Valley, Brazil. Naturalia, vol. 22, p. 211-244.
  • FERREIRA, SA., FERNANDES, GW. and CARVALHO, LG., 1990. Biologia e história natural de Euphaleurus ostreoides (Homoptera: Psyllidae) cecidógeno de Lonchocarpus guilleminianus (Leguminosae). Revista Brasileira de Biologia = Brazilian Journal of Biology, vol. 50, no. 2, p. 417-423.
  • GUSMÃO, MAB. and CREÃO-DUARTE, AJ., 2004. Diversidade e análise faunística Sphingidae (Insecta, Lepidoptera) na mata de pau ferro, com vista ao monitoramento. In PORTO, KC., CABRAL, JJP. and TABARELLI, M. (Orgs.). Brejos de Altitude em Pernambuco e Paraíba: História Natural, Ecologia e Conservação. Brasília, DF: Ministério do Meio Ambiente, p. 179-200. Série Biodiversidade, 9.
  • JULIÃO, GR., AMARAL, ME. and FERNANDES, GW., 2002. Galhas de insetos e suas plantas hospedeiras no Pantanal Sul-Matogrossense. Naturalia, vol. 27, p. 47-74.
  • LOCATELLI, E., MACHADO, IC. and MEDEIROS, P., 2004. Riqueza de abelhas e a flora apícola em um fragmento da mata serrana (brejo de altitude) em Pernambuco, Nordeste do Brasil. In PORTO, KC., CABRAL, JJP. and TABARELLI, M. (Orgs.). Brejos de Altitude em Pernambuco e Paraíba: História Natural, Ecologia e Conservação. Brasília, DF: Ministério do Meio Ambiente, p. 163-178. Série Biodiversidade, 9.
  • MAIA, VC., 2005. Catálogo dos Cecidomyiidae (Diptera) do Estado do Rio de Janeiro. Biota Neotropica, vol. 5, no. 2, p. 189-203.
  • MENDONÇA, MS., 2007. Plant diversity and galling arthropod diversity searching for taxonomic patterns in an animal-plant interaction in the neotropics. Boletin de la Sociedad Argentina de Botanica, vol. 42, no. 3-4, p. 347-357.
  • MOREIRA, RG., FERNANDES, GW., ALMADA, ED. and SANTOS, JC., 2007. Galling insects as bioindicators of land restoration in an area of Brazilian Atlantic Forest. Lundiana, vol. 8, p. 107-112.
  • PÔRTO, KC., CABRAL, JJP. and TABARELLI, M., 2004a. Brejos de Altitude em Pernambuco e Paraíba: História Natural, Ecologia e Conservação. Brasília, DF: Ministério do Meio Ambiente, 324 p. Série Biodiversidade, 9.
  • PÔRTO, KC., GERMANO, SR. and BORGES, GM., 2004b. Avaliação dos Brejos de Altitude de Pernambuco e Paraíba, quanto à diversidade de Briófitas, para a conservação. In PORTO, KC., CABRAL, JJP. and TABARELLI, M. (Orgs.). Brejos de Altitude em Pernambuco e Paraíba: História Natural, Ecologia e Conservação. Brasília, DF: Ministério do Meio Ambiente, p. 79-97. Série Biodiversidade, 9.
  • PRICE, PW., FERNANDES, GW., LARA, ACF., BRAWN, J., GERLING, D., BARRIOS, H., WRIGHT, MG., RIBEIRO, SP. and ROTHCLIFF, N., 1998. Global patterns in local number of insect galling species. Journal of Biogeography, vol. 25, p. 581-591.
  • RODAL, MJN., SALES, MF., SILVA, MJ. and SILVA, AG., 2005. Flora de um Brejo de Altitude na escarpa oriental do planalto da Borborema, PE, Brasil. Acta Botanica Brasilica, vol. 19, no. 4, p. 843-858.
  • SIQUEIRA FILHO, JA., 2004. As bromélias nos Brejos de Altitude em Pernambuco: riqueza de espécies status de conservação. In PORTO, KC., CABRAL, JJP. and TABARELLI, M. (Orgs.). Brejos de Altitude em Pernambuco e Paraíba: História Natural, Ecologia e Conservação. Brasília, DF: Ministério do Meio Ambiente, p. 99-110. Série Biodiversidade, 9.
  • TABARELLI, M. and SANTOS, AMM, 2004. Uma breve descrição sobre a história natural dos brejos nordestinos. In PORTO, KC., CABRAL, JJP. and TABARELLI, M. (Orgs.). Brejos de Altitude em Pernambuco e Paraíba: História Natural, Ecologia e Conservação. Brasília, DF: Ministério do Meio Ambiente, p. 17-24. Série Biodiversidade, 9.
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  • Publication Dates

    • Publication in this collection
      11 Mar 2011
    • Date of issue
      Feb 2011

    History

    • Accepted
      17 Aug 2009
    • Received
      18 June 2009
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