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Are Gall Midge Species (Diptera, Cecidomyiidae) Host-Plant Specialists? 367

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Are Gall Midge Species (Diptera, Cecidomyiidae) Host-Plant Specialists? 367 Are gallAre midge gall species midge (Diptera, species Cecidomyiidae) (Diptera, host-plant Cecidomyiidae) specialists? host-plant specialists? 365 Marco Antonio A. Carneiro1, Cristina S. A. Branco2, Carlos E. D. Braga2, Emmanuel D. Almada2, Marina B. M. Costa2, Valéria C. Maia3 & Geraldo Wilson Fernandes2 1Laboratório Entomologia Ecológica, Universidade Federal de Ouro Preto, Campus Morro do Cruzeiro, 35400-000 Ouro Preto-MG, Brazil. [email protected] 2Ecologia Evolutiva & Biodiversidade, Universidade Federal de Minas Gerais; Caixa Postal 486, 30161-970 Belo Horizonte-MG, Brazil. [email protected], [email protected], [email protected], [email protected], [email protected] 3Museu Nacional, Quinta da Boa Vista, São Cristóvão, 20940-040 Rio de Janeiro-RJ, Brazil. [email protected] ABSTRACT. Are gall midge species (Diptera, Cecidomyiidae) host plant specialists? Despite the speciose fauna of gall- inducing insects in the Neotropical region, little is known about their taxonomy. On the other hand, gall morphotypes associated with host species have been extensively used as a surrogate of the inducer species worldwide. This study reviewed the described gall midges and their galls to test the generalization on the use of gall morphotypes as surrogates of gall midge species in the Brazilian fauna. We compiled taxonomic and biological data for 196 gall midge species recorded on 128 host plant species. Ninety two percent of those species were monophagous, inducing galls on a single host plant species, whereas only 5.6% species were oligophagous, inducing galls on more than one congeneric host plant species. Only four species induced galls on more than one host plant genus. We conclude that gall morphotypes associated with information on the host plant species and attacked organs are reliable surrogates of the gall-inducing species. KEYWORDS. Biodiversity; cecidomyiids; herbivory; insect galls; species richness. RESUMO. Espécies de moscas galhadoras (Diptera, Cecidomyiidae) são especialistas em plantas hospedeiras? Apesar do elevado número de espécies da fauna de insetos indutores de galhas na região Neotropical, muito pouco espécies foram descritas. Por outro lado, o morfotipo da galha associado com a espécie da planta hospedeira é em todo o mundo amplamente utilizado como um indicador da espécie de inseto indutor. Este estudo revê as espécies de cecidommídeos descritos e suas galhas para verificar a generalização do uso da morfologia da galha como indicador da espécie de cecidomíideo na fauna brasileira. Nós compilamos dados biológicos e taxonômicos de 196 espécies de cecidomiídeos em 128 espécies de plantas no Brasil. Noventa e dois porcento destas espécies foram monófagas, induzindo galhas em uma única espécie de planta hospedeira, enquanto somente 5,6% das espécies foram oligófagas, induzindo galhas em mais de uma espécie de planta do mesmo gênero. Somente quatro espécies induzem galhas em espécies de plantas de gêneros diferentes. Nós concluímos que o morfo-tipo da galha associado com a espécie da planta hospedeira e com o órgão atacado são indicadores confiáveis da espécie de insetos indutores de galhas. PALAVRAS-CHAVE. Biodiversidade; cecidomíideos; herbivoria; insetos galhadores; riqueza em espécies. Galling insects are amongst the most specialized and 1987; Weis et al. 1988; Nyman & Julkunen-Tiitto 2000; Stone fascinating herbivores because of their ability to control and & Schönrogge 2003). redirect plant development (Shorthouse et al. 2005). Galling Gall-inducers are speciose in the Neotropical region, but insects are a type of herbivores that, in order to complete their despite their richness, little is known about their taxonomy life cycle, obligatorily induce galls on the host plant. Plant (e.g. Fernandes & Price 1988; Fernandes et al. 1996, 2001; galls are cells, tissues or organs of abnormal growth formed Gonçalves-Alvim & Fernandes 2001; Julião et al. 2004). The due to an increase in cell volume (hypertrophy) and/or cell gall midges (Diptera, Cecidomyiidae) represent the largest taxon number (hyperplasia) in response to feeding or other stimuli of gall-inducing insects in the Neotropical region (Fernandes by foreign organisms (Rohfritsch & Shorthouse 1982; Dreger- et al. 1996; Lara & Fernandes 1996) with nearly 500 described Jauffret & Shorthouse 1992; Raman et al. 2005). A new definition species classified into 170 genera (Gagné 1994, 2004). However, of galls was coined by Raman (2007) excluding plant growth the richness of gall midges is highly underestimated. A recent induced by bacteria and fungi, which form amorphous growths study estimated the global richness of galling insects to be that are called tumors. Insect induced galls on the other hand, approximately 120,000 species (Espírito-Santo & Fernandes result in mostly symmetrical growth forms. From an 2007), making the knowledge of this guild essential for evolutionary point of view, galls can be seen as extended ecological studies. phenotypes of insects or adaptations that allow inducers to It is widely accepted that most gall-inducing insects are feed on high quality tissues, and protect themselves from highly specific to their host plants and organs, that is, they natural enemies and/or harsh environments (Price et al. 1986, induce galls on a single or closely related species (Dreger- Revista Brasileira de Entomologia 53(3): 365–378, setembro 2009 366 Carneiro et al. Jauffret & Shorthouse 1992; Floate et al. 1996). Therefore, categorize them. The terms fusiform and elliptical, globulous several authors have used gall morphotypes as a surrogate of and globular, spheroid and spherical were used as the insect species (Fernandes & Price 1988; Floate et al. 1996; synonymous throughout the analyses, but were kept separate Price et al. 1998; Hanson & Gómez-Laurito 2005) due to their in the table to maintain the original description. high host plant and plant organ specificity (Dreger-Jauffret & Shorthouse 1992; Shorthouse et al. 2005). As a result of this RESULTS AND DISCUSSION high specificity, gall morphotypes have been also used as tools in plant systematics (Raman 1996; Abrahamson et We recorded 196 species of gall midges on 128 host plant al.1998). For instance, galling species were used to distinguish species belonging to 89 genera and 42 botanical families in between two Chrysothamnus nauseosus (Pall. ex Pursh) Britton Brazil (Tables I and II). Asphondylia Loew 1850 and subspecies (Floate et al. 1996). Other studies have also Clinodiplosis Kieffer 1894 were the dominant genera, demonstrated the same intimate relationship between galling represented by 20 and 18 species each, respectively. Amongst insects and their host plants. Hybrids of Quercus L., Populus those 196 species, 92.4% (181 species) were monophagous, L., and Salix L. were discriminated from parental host plants inducing galls on a single host species (Table I). Only 11 (5.6%) by their respective gall inducers (Aguilar & Boecklen 1992; species were oligophagous, inducing galls on more than one Fritz et al. 1994; Floate & Whitham 1995). congeneric host plant species (Table II). There were only four In tropical areas, where the taxonomic knowledge of gall (2.0%) reports of polyphagy: Asphondylia borreriae midges is scarce, the use of gall morphotypes associated with Rübsaamen, 1905, which induces flower galls on undetermined host species as a surrogate of the inducer species is widespread species on two plant genera, Borreria G. Mey. 1818 and Diodia in ecological studies (e.g., Fernandes & Price 1988; Fernandes L. 1753 (Rubiaceae); Asphondylia corbulae Möhn, 1960, which et al. 1996, 2001; Araújo et al. 2003; Dalbem & Mendonça. induces fruit (achene) galls on Chromolaena odorata (L.) R.M. 2006; Urso-Guimarães & Scareli-Santos 2006). These studies King & H. Rob., 1970 and Fleischmannia microstemon (Cass.) assumed that galls differing in morphology and host species R.M. King & H. Rob.; Perasphondylia reticulata Möhn, 1960, are induced by different species. The specificity of gall- which induces bud galls on Chromolaena odorata, C. ivifolia inducing insects to particular gall morphologies has not been (L.) R.M. King & H. Rob. and Eupatorium sp.; and tested in southern latitudes in the tropics, as they have been Clinodiplosis eupatorii Felt, 1911, which induces leaf galls in northern latitudes. The purpose of this study was to on Chromolaena odorata, C. ivifolia and Eupatorium sp. examine whether the use of gall morphotype associated with (Asteraceae) (Table II). Gall shape was undetermined for 11 host plant species might be a surrogate of insect species in gall midge species. Most galls were induced on leaves (113 the Brazilian fauna. If this is correct, then the described galling galls), followed by flowers (29) and stems (26 galls). All insect species for which we have data on the galls would be cecidomyiid species induced galls on a single host organ, specialists on host plant species and organs, with each galling except for 18 species, which induced morphologically similar species inducing morphologically similar galls on a single galls on more than one host plant organ (Table I and II): organ of the given host plant. The analyses were restricted to (Anadiplosis procera Tavares, 1920; Anisodiplosis waltheriae the family Cecidomyiidae, as this family represents the most Maia, 2005; Bruggmannia monteiroi Maia & Couri, 1993; common galling insect taxon in the region and, consequently, Stephomyia rotundifoliorum Maia, 1995; Contodiplosis most patterns of gall-inducing
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