Are gall midge species (Diptera, Cecidomyiidae) host-plant specialists?

Espécies de moscas galhadoras (Diptera, Cecidomyiidae) são especialistas em plantas hospedeiras?

SYSTEMATICS, MORPHOLOGY AND BIOGEOGRAPHY

Are gall midge species (Diptera, Cecidomyiidae) host-plant specialists?

Espécies de moscas galhadoras (Diptera, Cecidomyiidae) são especialistas em plantas hospedeiras?

Marco Antonio A. Carneiro^I; Cristina S. A. Branco^II; Carlos E. D. Braga^II; Emmanuel D. Almada^II; Marina B. M. Costa^II; Valéria C. Maia^III; Geraldo Wilson Fernandes^II

^ILaboratório Entomologia Ecológica, Universidade Federal de Ouro Preto, Campus Morro do Cruzeiro, 35400-000 Ouro Preto-MG, Brazil. [e-mail]

^IIEcologia Evolutiva & Biodiversidade, Universidade Federal de Minas Gerais; Caixa Postal 486, 30161-970 Belo Horizonte-MG, Brazil. [e-mail], [e-mail], [e-mail], [e-mail], [e-mail]

^IIIMuseu Nacional, Quinta da Boa Vista, São Cristóvão, 20940-040 Rio de Janeiro-RJ, Brazil. [e-mail]

ABSTRACT

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

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 fascinating herbivores because of their ability to control and redirect plant development (Shorthouse et al. 2005). Galling insects are a type of herbivores that, in order to complete their life cycle, obligatorily induce galls on the host plant. Plant galls are cells, tissues or organs of abnormal growth formed due to an increase in cell volume (hypertrophy) and/or cell number (hyperplasia) in response to feeding or other stimuli by foreign organisms (Rohfritsch & Shorthouse 1982; Dreger-Jauffret & Shorthouse 1992; Raman et al. 2005). A new definition of galls was coined by Raman (2007) excluding plant growth induced by bacteria and fungi, which form amorphous growths that are called tumors. Insect induced galls on the other hand, result in mostly symmetrical growth forms. From an evolutionary point of view, galls can be seen as extended phenotypes of insects or adaptations that allow inducers to feed on high quality tissues, and protect themselves from natural enemies and/or harsh environments (Price et al. 1986, 1987; Weis et al. 1988; Nyman & Julkunen-Tiitto 2000; Stone & Schönrogge 2003).

Gall-inducers are speciose in the Neotropical region, but despite their richness, little is known about their taxonomy (e.g. Fernandes & Price 1988; Fernandes et al. 1996, 2001; Gonçalves-Alvim & Fernandes 2001; Julião et al. 2004). The gall midges (Diptera, Cecidomyiidae) represent the largest taxon of gall-inducing insects in the Neotropical region (Fernandes et al. 1996; Lara & Fernandes 1996) with nearly 500 described species classified into 170 genera (Gagné 1994, 2004). However, the richness of gall midges is highly underestimated. A recent study estimated the global richness of galling insects to be approximately 120,000 species (Espírito-Santo & Fernandes 2007), making the knowledge of this guild essential for ecological studies.

It is widely accepted that most gall-inducing insects are highly specific to their host plants and organs, that is, they induce galls on a single or closely related species (Dreger-Jauffret & Shorthouse 1992; Floate et al. 1996). Therefore, several authors have used gall morphotypes as a surrogate of the insect species (Fernandes & Price 1988; Floate et al. 1996; Price et al. 1998; Hanson & Gómez-Laurito 2005) due to their high host plant and plant organ specificity (Dreger-Jauffret & Shorthouse 1992; Shorthouse et al. 2005). As a result of this high specificity, gall morphotypes have been also used as tools in plant systematics (Raman 1996; Abrahamson et al.1998). For instance, galling species were used to distinguish between two Chrysothamnus nauseosus (Pall. ex Pursh) Britton subspecies (Floate et al. 1996). Other studies have also demonstrated the same intimate relationship between galling insects and their host plants. Hybrids of Quercus L., Populus L., and Salix L. were discriminated from parental host plants by their respective gall inducers (Aguilar & Boecklen 1992; Fritz et al. 1994; Floate & Whitham 1995).

In tropical areas, where the taxonomic knowledge of gall midges is scarce, the use of gall morphotypes associated with host species as a surrogate of the inducer species is widespread in ecological studies (e.g., Fernandes & Price 1988; Fernandes et al. 1996, 2001; Araújo et al. 2003; Dalbem & Mendonça. 2006; Urso-Guimarães & Scareli-Santos 2006). These studies assumed that galls differing in morphology and host species are induced by different species. The specificity of gall-inducing insects to particular gall morphologies has not been tested in southern latitudes in the tropics, as they have been in northern latitudes. The purpose of this study was to examine whether the use of gall morphotype associated with host plant species might be a surrogate of insect species in the Brazilian fauna. If this is correct, then the described galling insect species for which we have data on the galls would be specialists on host plant species and organs, with each galling species inducing morphologically similar galls on a single organ of the given host plant. The analyses were restricted to the family Cecidomyiidae, as this family represents the most common galling insect taxon in the region and, consequently, most patterns of gall-inducing species in Brazil may be strongly dependent upon the responses of cecidomyiid species. In addition, taxonomic knowledge of non-cecidomyiid galling insects is still incipient (e.g., Maia 2006), impairing a more detailed attempt to correlate gall morphology and host species to the gall inducer in these other taxa.

MATERIAL AND METHODS

The gall midges and host plant species database was compiled from taxonomic reviews of the gall midges of the Neotropical Region (e.g., Gagné 1994, 2004; Maia 2005a, and references therein) and from subsequent published papers (Maia 2005b, 2007; Maia & Fernandes 2005ab, 2006, 2007; Oliveira & Maia 2005). The undescribed species used in the data base were separated on the basis of gall midge morphology by V.C. Maia. Galls vary enormously in shape, host organ, epidermal cover and host plant species attacked (Stone & Schönrogge 2003). We used these variables to describe and categorize them. The terms fusiform and elliptical, globulous and globular, spheroid and spherical were used as synonymous throughout the analyses, but were kept separate in the table to maintain the original description.

RESULTS AND DISCUSSION

We recorded 196 species of gall midges on 128 host plant species belonging to 89 genera and 42 botanical families in Brazil (Tables I and ^II). Asphondylia Loew 1850 and Clinodiplosis Kieffer 1894 were the dominant genera, represented by 20 and 18 species each, respectively. Amongst those 196 species, 92.4% (181 species) were monophagous, inducing galls on a single host species (Table I). Only 11 (5.6%) species were oligophagous, inducing galls on more than one congeneric host plant species (^{Table II}). There were only four (2.0%) reports of polyphagy: Asphondylia borreriae Rübsaamen, 1905, which induces flower galls on undetermined species on two plant genera, Borreria G. Mey. 1818 and Diodia L. 1753 (Rubiaceae); Asphondylia corbulae Möhn, 1960, which induces fruit (achene) galls on Chromolaena odorata (L.) R.M. King & H. Rob., 1970 and Fleischmannia microstemon (Cass.) R.M. King & H. Rob.; Perasphondylia reticulata Möhn, 1960, which induces bud galls on Chromolaena odorata, C. ivifolia (L.) R.M. King & H. Rob. and Eupatorium sp.; and Clinodiplosis eupatorii Felt, 1911, which induces leaf galls on Chromolaena odorata, C. ivifolia and Eupatorium sp. (Asteraceae) (^{Table II}). Gall shape was undetermined for 11 gall midge species. Most galls were induced on leaves (113 galls), followed by flowers (29) and stems (26 galls). All cecidomyiid species induced galls on a single host organ, except for 18 species, which induced morphologically similar galls on more than one host plant organ (Table I and ^II): (Anadiplosis procera Tavares, 1920; Anisodiplosis waltheriae Maia, 2005; Bruggmannia monteiroi Maia & Couri, 1993; Stephomyia rotundifoliorum Maia, 1995; Contodiplosis friburgensis (Tavares, 1915), Liodiplosis conica Gagné, 2001; Liodiplosis cylindrica Gagné, 2001; Liodiplosis spherica Gagné, 2001; Mikaniadiplosis annulipes Gagné, 2001; Zalepidota ituensis Tavares, 1917; Myrciamyia maricaensis Maia, 1995; Myrciariamyia bivalva Maia, 1995; Myrciariamyia fernandesi Maia, 2004; Neomitranthella robusta Maia, 1995, Rhoasphondylia friburgensis Tavares, 1917; Neolasioptera sp. 1, Neolasioptera sp. 2, Clinodiplosis sp.).

The data clearly show that gall midges are mostly restricted to a single host plant species, hence supporting the statement that cecidomyiids are highly host-specific. Therefore, the gall morphotypes can be used as a reliable surrogate of the inducing species. Galling insects have evolved a unique and fine sintony with their host plants and each galling species exhibits a unique oviposition site (Raman 2007), although some exceptions have been recorded (Gagné 1989, 1994, 2004; Abrahamson et al. 1998; Nyman et al. 2000; Stone & Schönrogge 2003). In our review only two gall midges were classified as polyphagous. Gall midges were mostly monophagous or oligophagous species inducing galls on one or a few host species in a single genus, respectively. Otherwise, recent studies by Yukawa and colleagues (Uechi et al. 2003, 2004; Tokuda et al. 2005) have reported on polymorphic galls induced by a single species of a galling cecidomyiid on one or more host species. For example, two Japanese species of Asteraceae, Artemisia montana (Nakai) Pamp. 1930 and Artemisia princeps Pamp. 1930 supported polymorphic axillary bud galls induced by Rhopalomyia longitubifex (Shinji, 1939) (Ganaha et al. 2004, 2007). Although the failure to identify polymorphic galls could lead to miss identification of the gall inducer, this phenomenon seems to be mostly rare. In Japan, less than ten galling cecidomyiids induce polymorphic galls (Uechi et al. 2003, 2004; Tokuda et al. 2005; Ganaha et al. 2004, 2007; Mishima & Yukawa 2007) from a total of 628 described species so far (Yukawa & Rohfritsch 2005), meaning that less than 1% induces polymorphic galls. In our study we found eight cecidomyiids that possibly induce polymorphic galls on the same or on different host species (see Table I, ^II). Detailed molecular studies on galling insects would shed light on this question (see discussion on the evolutionary significance of dimorphic galls bellow).

Although reports on polymorphic galls are at best rare, gall dimorphism may be vital to understand the role and origin of gall shape diversification and gall midges speciation (Mishima & Yukawa 2007). The species of gall midges that induce morphologically similar galls on host plant congeners or on new sites (organs) on the same host plant species may represent the early stages of a host shift and formation of gall midge host races (see Ganaha et al. 2004, 2007; Joy & Crespi 2007). The colonization and radiation into new species and organs may promote the spatial and temporal isolation that favor reproductive isolation for gall midges.

The identity of the host plant species is crucially important for the recognition of the inducer in the field, as morphologically similar galls induced on different host plant species do not mean that they were induced by the same galling insect species (McLeish et al. 2006). Species of Baccharis L. 1753, for instance, are each host to a distinct galling species community, which induces similar leaf gall morph types. Burckhardt et al. (2004) described three species of Baccharopelma Burckhardt 2004 (Psyllidae) restricted to particular host species: Baccharopelma dracunculifoliae Burckhardt 2004 on Baccharis dracunculifolia DC., 1836, Baccharopelma concinnae Burckhardt 2004 on Baccharis concinna Barroso, 1976, Baccharopelma brasiliensis (Burckhardt, 1987) on Baccharis ramosissima Gardner, 1848, and Baccharopelma baccharidis (Burckhardt, 1987), on Baccharis linearis (Ruiz & Pav.) Pers. 1807. Therefore, using only gall morph types as a surrogate of inducer identity could lead to misidentifications.

Insect galls represent an extended phenotype of the gall inducing organism as their larvae have the ability to control gall development and morphology (Weis et al. 1988). The galling insect control of gall morphological is suggested by the fact that many galls with very different galler-specific morphologies may grow on the same plant host at the same time (Stone & Schönrogge 2003). In the rupestrian fields for example, 13 gall morphotypes were found on Baccharis concinna Barroso 1976 (Asteraceae) and a single individual plant supported 11 species simultaneously (Carneiro et al. 2005). Many other studies reported the same observation (e.g., Waring & Price 1989; Stone et al. 2002). In salt marsh vegetation, Eugenia umbelliflora O. Berg 1857 (Myrtaceae) and Guapira opposita (Vell.) Reitz 1970 (Nyctaginaceae) each support six galling species at the same time (Maia 2001b; Monteiro et al. 2004; Oliveira & Maia 2005).

Indeed, many studies have now shown that gall morphology is dependent on the stimuli provided by the galler (see Raman et al. 2005). In the temperate region, gall midges of the Asphondylia auripila group include 15 sympatric species which induce morphologically different galls on several organs of creosote bush, Larrea tridentata (Sessé & Moc. ex DC.) Coville, 1983 (Waring & Price 1989; Gagné & Waring 1990). Asphondylia species diversification on a host plant follows ecological shifts (= ability to induce a gall on a particular organ) and changes with timing adult emergence (Joy & Crespi 2007). Sympatric shifts on host plant organs or plant species may be responses to a combination of mistakes in oviposition site and in the developmental schedules of different tissue in plants parts (Joy & Crespi 2007). Therefore, the high species- and organ- specificity of galling insects provides further evidence of the identity of the gall inducing species.

The high specificity of host plant species shown by the cecidomyiids is also expected for all Neotropical gall forming insects. Additional support for high specificity with respect to host plants and organs is provided by recent phylogenetic studies in other taxa. Related galling insect species usually induce morphologically similar galls on phylogenetically related host plants (Nyman et al. 2000). Phylogenetic evidence also suggests that gall morphology of aphids (Stern 1995; Inbar et al. 2004), thrips (Crespi & Worobey 1998; Morris et al. 2002; McLeish et al. 2006), sawflies (Nyman et al. 2000) and gall wasps (Stone & Cook 1998; Stone et al. 2002; Cook et al. 2002) is controlled by the gall inducing organism.

Moreover, recent studies have now shown that insect taxa previously described as polyphagous may be groups of cryptic species. Nematine sawflies (Hymenoptera, Tenthredinidae) have been divided into three genera based on gall morphology: Phyllocolpa Benson, 1960 species induce leaf folds or rolls, Pontania L. 1758 species induce various leaf galls, and Euura L. 1758 species induce midrib, petiole, bud, and stem galls (Smith 1970; Price 2003, 2005). Most nematine gallers are highly host specific, except E. mucronata Hartig 1837 which induces galls on over 30 willow species in the Holarctic region (Price 2003). However, recent studies have shown that 'E. mucronata' is not a single polyphagous species, but a complex consisting of several monophagous and oligophagous sibling species or host races (Nyman 2002).

Our review strengthens the view that gall midges are highly host-plant specific and that morphologically similar galls on several host plant species are induced by different cecidomyiid species. This is consistent with observations in north temperate latitudes, even though conventional wisdom seems to expect that species differ in responses in temperate and tropical regions. However, the evidence of this study shows that herbivores in tropical and temperate regions area very similar in patterns of specificity. Within the same host plant species gall morphology and the attacked host organ are reliable indicators of distinct cecidomyiid species. Due to an insufficient number of taxonomists working on galling insects, and large numbers of gall-inducing species in the Neotropical region (see Espírito Santo & Fernandes 2007), the use of host-plant records associated with gall morphology represents a reliable tool that will allow the development of field-based ecological studies, until taxonomic work is developed (e.g. Fernandes & Price 1988; Dalbem & Mendonça 2006; Urso-Guimarães & Scareli-Santos 2006; Espírito-Santo et al. 2007). Hence, the use of gall morphology as a surrogate of the gall-inducing species should not discourage the training of students in galling species systematics. By using this approach, Neotropical ecologists may incur a little (7.7%) error, but this error is small enough that it may not lead to inaccurate conclusions. We hope that this study serves to stimulate studies in other biogeographical regions and expand it to other galling taxa.

Acknowledgments. We thank T. G. Cornelissen, P. E. Hanson, P. W. Price, F. A. O. Silveira and two anonymous reviewers for suggestions on earlier versions of the manuscript. This study was supported by CNPq (309633/2007-9), and FAPERJ (Proc. E-16/171.290/2006). We gratefully acknowledge a scholarship of the CAPES/PICDT to M. A. A. Carneiro. This study was in partial fulfillment of the requirements for PhD degree to M. A. A. Carneiro at the Universidade Federal de Minas Gerais.

REFERENCES

Abrahamson, W. G.; G. Melika; R. Scravord & G. Csóka. 1998. Gall-inducing insects provide insights into plant systematic relationships. American Journal of Botany 85: 1159-1165.

Aguilar, J. M. & W. J. Boecklen. 1992. Patterns of herbivory in the Quercus grisea x Quercus gambelii species complex. Oikos 64: 498-504.

Almeida, F. V. M.; J. C. Santos; F. A. O. Silveira & G. W. Fernandes. 2006. Distribution and frequency of Galls Induced by Anisodiplosis waltheriae Maia (Diptera: Cecidomyiidae) on the Invasive Plant Waltheria indica L. (Sterculiaceae). Neotropical Entomology 35: 435-439.

Angelo, A. & V. C. Maia. 1999. Dasineura gigantea n. sp. (Diptera, Cecidomyiidae) associada com Psidium cattleyanum (Myrtaceae) no Brasil. Revista Brasileira de Zoologia 16: 191-195.

Araújo, A. P. A.; M. A. A. Carneiro & G. W. Fernandes. 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). Revista Brasileira de Entomologia 47: 483-490.

Burckhardt, D.; M. M. Espírito-Santo; G. W. Fernandes & I. Malenoviský. 2004. Gall-inducing jumping plant-lice of the Neotropical genus Baccharopelma (Hemiptera: Psylloidea) associated with Baccharis (Asteraceae). Journal Natural History 38: 2051-2071.

Carneiro, M. A. A.; G. W. Fernandes & O. F. F. DeSouza. 2005. Convergence in the variation of local and regional galling species richness. Neotropical Entomology 34: 547-553.

Cook, J. M.; A. Rokas; M. Pagel & G. N. Stone. 2002. Evolutionary shifts between host oak sections and host plant organs in Andricus gallwasps. Evolution 56: 1821-1830.

Crespi, B. J. & M. Worobey. 1998. Comparative analysis of gall morphology in Australian gall thrips: the evolution of extended phenotypes. Evolution 52: 1686-1696.

Couri, M. S. & V. C. Maia. 1992. Considerações sobre Pisphondylia Möhn, 1960 (Diptera, Cecidomyiinae, Asphondyliidi), com descrição de uma espécie nova do Brasil. Revista Brasileira de Entomologia 36: 729-730.

Dalbem, R. V. & M. S. Mendonça. 2006. Diversity of galling arthropods and host plants in a subtropical forest of Porto Alegre, Southern Brazil. Neotropical Entomology 35: 616-624.

Dreger-Jauffret, F. & J. D. Shorthouse. 1992. Diversity of gall-inducing insects and their galls, p. 8-33. In: J. D. Shorthouse & O. Rohfritsch (Eds.). Biology of insect-induced galls. Oxford, Oxford University Press, xi+285 p.

Espírito-Santo, M. M. & G. W. Fernandes. 2007. How many species of gall-inducing insects are there on earth, and where are there? Annals of the Entomological Society of America 100: 95-99.

Espírito-Santo, M. M.; F. S. Neves; F. R. Andrade-Neto & G. W. Fernandes. 2007. Plant architecture and meristem dynamics as the mechanisms determining the diversity of gall-inducing insects. Oecologia 153: 353-364.

Felt, E. P. 1908. Appendix D. New York State Museum Buletin 124: 286-422.

Felt, E. P. 1911. Two new gall midges (Dip.). Entomological News 22: 109-111.

Felt, E. P. 1912. New Itonididae (Dip.). Journal of the New York Entomological Society 20: 102-107.

Felt, E. P. 1915. New genera and species of gall midges. Proceedings of the United States Museum 48: 195-211.

Felt, E. P. 1921. Three new sub-tropical gall midges (Itonididae, Dipt.). Entomological News 32: 141-143.

Fernandes, G. W.; M. A. A. Carneiro; A. C. F. Lara; L. R. Allain; G. R. Julião; G. I. Andrade; T. R. Reis & I. M. Silva. 1996. Galling insects on Neotropical species of Baccharis (Asteraceae). Tropical Zoology 9: 315-332.

Fernandes, G. W.; G. R. Julião; R. C. Araújo; S. C. Araújo; J. A. Lombardi; D. Negreiros & M. A. A Carneiro. 2001. Distribution and morphology of insect galls of the Rio Doce Valley, Brazil. Naturalia 26: 211-244.

Fernandes, G. W. & P. W. Price. 1988. Biogeographical gradients in galling species richness: tests of hypotheses. Oecologia 76: 161-167.

Floate, K. D.; G. W. Fernandes & J. A. Nilsson. 1996. Distinguishing intrapopulacional categories of plants by their insect faunas: galls on rabbitbrush. Oecologia 105: 221-229.

Floate, K. D. & T. G. Whitham. 1995. Insects as traits in plant systematics: their use in discriminating between hybrid cottonwoods. Canadian Journal of Botany 73: 1-13.

Fritz, R. S.; C. M. Nichols-Orians & S. J. Brunsfeld. 1994. Interspecific hybridization of plants and resistance to herbivores: hypotheses, genetics, and variable responses in a diverse herbivore community. Oecologia 97: 106-117.

Gagné, R. J. 1977. The Cecidomyiidae (Diptera) associated with Chromolaena odorata (L.)K. and R. (Compositae) in the Neotropical Region. Brenesia 12/13: 113-131.

Gagné, R. J. 1984. Five new species of Neotropical Cecidomyiidae (Diptera) associated with cacao flowers, killing the buds of Clusiaceae, or preying on mites. Brenesia 22: 123-138.

Gagné, R. J. 1989. The plant-feeding midges of North America. Ithaca, Comstock, xi+368 p.

Gagné, R. J. 1994. The gall midges of the region neotropical. Ithaca, Comstock, xiv+352 p.

Gagné, R. J. 2004. A catalog of the Cecidomyiidae (Diptera) of the world. Memoirs of the Entomological Society of Washington 25: 1-408.

Gagné, R. J.; F. F. F. Ferraz & R. F. Monteiro. 1998. A new species of Neolasioptera Felt (Diptera: Cecidomyiidae) on Cuphea carthagenensis (Jacq.) Macbride (Lythraceae) in Brazil, with notes on its biology. Proceedings of Entomological Society of Washington, Washington 100: 521-525.

Gagné, R. J.; R. A. Oda & R. F. Monteiro. 2001. The gall midges (Diptera: Cecidomyiidae) of Mikania glomerata (Asteraceae) in southeastern Brazil. Proceedings of the Entomological Society Washington 103: 110-134.

Gagné, R. J. & G. L. Waring. 1990. The Asphondylia (Cecidomyiidae: Diptera) of creosote bush (Larrea tridentata) in North America. Proceedings Entomological Society Washington 92: 649-671.

Ganaha, T.; M. Nohara; S. Sato; N. Uechi; K. Yamagishi; S. Yamauchi & J. Yukawa. 2007. Polymorphism of axillary bud galls induced by Rhopalomyia longitubifex (Diptera: Cecidomyiidae) on Artemisia princes and A. Montana (Asteraceae) in Japan and Korea, with designation on new synonyms. Entomological Science 10: 157-169.

Ganaha, T.; J. Yukawa; N. Uechi; M. Nohara & J. Paik. 2004. Identifications of some species of the genus Rhopalomyia (Diptera: Cecidomyiidae) inducing galls on Artemisia (Asteraceae) in South Korea. Esakia 44: 45-55.

Gonçalves-Alvim, S. J. & G. W. Fernandes. 2001. Biodiversity of galling insects: historical, community and habitat effects in four Neotropical savannas. Biodiversity and Conservation 10: 79-98.

Hanson, P. E. & J. Gómez-Laurito. 2005. Diversity of gall-inducing Arthropods of Costa Rica, p. 673-692. In: A. Raman, C. W. Schaefer & T. M. Withers (Eds.). Biology, ecology, and evolution of gall-inducing arthropods, Vol. 2. New Hampshire, Science Publishers Inc., xxi+817 p.

Houard, C. 1933. Les Zoocécidies des Plantes de l´Amérique du Sud e de l´Amérique Central. Paris, Hermann et Cie, 519 p.

Inbar, M.; M. Wink & D. Wool. 2004. The evolution of host plant manipulation by insects: molecular and ecological evidence from gall-forming aphids on Pistacia. Molecular Phylogenetics and Evolution 32: 504-511.

Joy, J. B. & B. J. Crespi. 2007. Adaptive radiation of gall-inducing insects within a single host-plant species. Evolution 61: 784-795

Julião, G. R.; M. E. C. Amaral; G. W. Fernandes & E. G. Oliveira. 2004. Edge effect and species-area relationships in the gall-forming insect fauna of natural forest patches in the Brazilian Pantanal. Biodiversity and Conservation 13: 2055-2066.

Kieffer, J. J. 1913. Diptera. Fam. Cecidomyiidae. Genera Isectorum 152: 1-346.

Lara, A. C. F. & G. W. Fernandes. 1996. The highest diversity of galling insects: Serra do Cipó, Brazil. Biodiversity Letters 3: 111-114.

Madeira, J. A.; V. C. Maia & R. F. Monteiro. 2002. Gall makers (Diptera, Cecidomyiidae) on Calophyllum brasiliense Camb. (Clusiaceae): descriptions and biology. Arquivos do Museu Nacional 61: 31-48.

Maia, V. C. 1993a. Considerações sobre Proasphondylia Felt (Diptera, Cecidomyiidae) com descrição de duas espécies novas associadas com Guapira opposta (Velloso) Reitz (Nyctaginaceae). Revista Brasileira de Zoologia 10: 215-218.

Maia, V. C. 1993b. Considerações sobre Stephomyia Tavares (Diptera, Cecidomyiidae, Asphondyliidi), com descrição de quatro espécies novas associadas com Eugenia L. e Neomithranthes obscura (DC.) Legr. (Myrtaceae). Revista Brasileira de Zoologia 10: 521-530.

Maia, V. C. 1993c. Uma nova espécie de Clinodiplosis Kieffer (Diptera, Cecidomyiidae) associada com Melissa officinalis Linnaeus (Labiatae) no Brasil. Revista Brasileira de Zoologia 10: 695-697.

Maia, V. C. 1993d. Descrição de duas espécies novas de Cecidomyiidae (Diptera) associadas com Eugenia spp. (Myrtaceae). Revista Brasileira de Entomologia 37: 717-721.

Maia, V. C. 1994. Myrciariamyia bivalva, gen.n. e sp.n. (Diptera, Cecidomyiidae, Oligotrophini) associado com Myrciaria floribunda (Camb.) Legr. (Myrtaceae) no Brasil. Revista Brasileira de Zoologia 11: 635-639.

Maia, V. C. 1995a. Chaves para classificação de galhas de Cecidomyiidae (Diptera) em Myrtaceae na restinga da Barra de Maricá, Rio de Janeiro. Revista Brasileira de Zoologia 12: 1009-1013.

Maia, V. C. 1995b. Dois gêneros novos de Cecidomyiidae (Diptera) associados à Myrtaceae, na restinga de Barra do Maricá, Rio de Janeiro, Brasil. Revista Brasileira de Zoologia 12: 567-574.

Maia, V. C. 1995c. Três espécies novas de Dasineura rondani (Diptera, Cecidomyiidae) associadas a Myrtaceae na restinga da Barra de Marica, Rio de Janeiro. Revista Brasileira de Zoologia 12: 1001-1008.

Maia, V. C. 1996a. Cordiamyia globosa gen.n. e sp.n. (Diptera, Cecidomyiidae, Cecidomyiidi) associado com Cordia verbenacea DC. (Boraginaceae) no Brasil. Revista Brasileira de Zoologia 13: 579-583.

Maia, V. C. 1996b. Clusiamyia nitida gen.n. e sp.n. (Diptera, Cecidomyiidae, Cecidomyiidi) associada com Clusia lanceolata Camb. (Clusiaceae) no Brasil. Revista Brasileira de Zoologia 13: 829-832.

Maia, V. C. 1999. Description of male, pupa and larva of Neolasioptera cerei Rübsaamen (Diptera, Cecidomyiidae). Revista Brasileira de Zoologia 16: 119-122.

Maia, V. C. 2001a. New genera and species of gall midges (Diptera, Cecidomyiidae) from three restingas of Rio de Janeiro State, Brazil. Revista Brasileira de Zoologia 18: 1-32.

Maia, V. C. 2001b. The gall midges (Diptera, Cecidomyiidae) from three restingas of Rio de Janeiro State, Brazil. Revista Brasileira de Zoologia 8: 583-630.

Maia, V. C. 2001c. Two new species of gall midges (Diptera, Cecidomyiidae) assocciated with Pouteria caimito var. laurifolia (Sapotaceae) in Brazil. Studia Dipterologica 8: 103-110.

Maia, V. C. 2004. Description of a new species of Bruggmannia Tavares (Diptera, Cecidomyiidae) associated with Guapira opposita (Vell.) Reitz (Nyctaginaceae) from Brazil. Revista Brasileira de Zoologia 21: 761-764.

Maia, V. C. 2005a. Catálogo dos Cecidomyiidae (Diptera) do Estado do Rio de Janeiro. Biota Neotropica 5: 1-15.

Maia, V. C. 2005b. Clinodiplosis costai, a new galler species (Diptera, Cecidomyiidae) associated with Paullinia weinmanniaefolia Mart (Sapindaceae). Revista Brasileira de Zoologia 22: 676-679.

Maia, V. C. 2006. Galls of Hemiptera, Lepidoptera and Thysanoptera from central and South America. Publicações avulsas do Museu Nacional 110: 1-22.

Maia, V. C. 2007. New genera and species of gall midges (Diptera, Cecidomyiidae) associated with Guarea macrophylla (Meliaceae). Revista Brasileira de Zoologia 24: 449-456.

Maia, V. C. & W. S. de Araújo. 2009. Uma nova espécie de Schizomyia (Diptera, Cecidomyiidae), indutora de galhas nos botões florais de Jacquemontia holosericea (Convolvulaceae). Revista Brasileira de Entomologia 53: 356-360.

Maia, V. C. & M. S. Couri. 1993. Descrição de três espécies novas de Bruggmannia Tavares, 1906 (Diptera, Cecidomyiidae, Asphondyliidi) do Brasil associadas com Guapira opposita (Nyctaginaceae). Revista Brasileira de Biologia 53: 209-215.

Maia, V. C. & G. W. Fernandes. 2004. Insect galls from Serra de São José (Tiradentes, Minas Gerais, Brazil). Brazilian Journal Biology 64: 423-445.

Maia, V. C. & G. W. Fernandes. 2005a. A new genus and species of midges (Diptera: Cecidomyiidae) associated with Waltheria indica L. (Sterculiaceae). Zootaxa 1060: 27-36.

Maia, V. C. & G. W. Fernandes. 2005b. Two new species of Asphondylinii (Diptera: Cecidomyiidae) associated with Bahuinia brevipes (Fabaceae) in Brazil. Zootaxa 1091: 27-40.

Maia, V. C. & G. W. Fernandes. 2006. A new genus and species of midges (Diptera: Cecidomyiidae) associated with Parkia pendula (Fabaceae, Mimosoidae). Revista Brasileira de Entomologia 50: 1-5.

Maia, V. C. & G. W. Fernandes. 2007. Myrciariamyia admirabilis, a new species of gall midge (Diptera, Cecidomyiidae) associated with Erythroxylum suberosum (Erythroxylaceae). Zootaxa 1554: 41-48.

Maia, V. C.; M. S. Couri & R. F. Monteiro. 1992. Sobre seis espécies de Asphondylia Loew, 1850 do Brasil (Diptera, Cecidomyiidae). Revista Brasileira de Entomologia 36: 653-661.

Maia, V. C.; P. de A. L. Constantino & R. F. Monteiro. 2005. New gall midges (Diptera, Cecidomyiidae) associated with two species of Eugenia (Myrtaceae). Revista Brasileira de Entomologia 49: 347-352.

Maia, V. C.; M. S. Mendonça & H. P. Romanowski. 1996. Eugeniamyia dispar gen.n. and sp.n. (Diptera, Cecidomyiidae, Lasiopteridi) associated with Eugenia uniflora L. (Myrtaceae) in Brazil. Revista Brasileira de Zoologia 13: 1087-1090.

Maia, V. C.; R. F. Monteiro & K. L. Narahara. 2002. Two new species of gall midges (Diptera, Cecidomyiidae) associated with Protium icicariba (Burseraceae) in Brazil. Studia Dipterologica 9: 171-178.

Maia, V. C. & U. P. Oliveira. 2007. Uma nova espécie de Cecidomyiidae (Diptera) associada com Sebastiania glandulosa (Euphorbiaceae). Iheringia, Série Zoológica 97: 97-101.

Maia, V. C.; M. Zart & M. Botton. 2009a. Neolasioptera ramicola, a new species of Cecidomyiidae (Diptera) associated with Physalis angulata (Solanaceae). Revista Brasileira de Entomologia 53: 163-165.

Maia, V. C.; J. C. Santos & G. W. Fernandes. 2009b. Asphondylia fructicola, a new species of Cecidomyiidae (Diptera) associated with Solanum sp. (Solanaceae) from Brazil. Revista Brasileira de Entomologia 53: 166-170.

Mcleish, M. J.; T. W. Chapman & L. A. Mound. 2006. Gall morpho-type corresponds to separate speciers of gall-inducing thrips (Thysanoptera: Phlaeothripidae). Biological Journal of the Linnean Society 88: 555-563.

Mishima, M. & J. Yukawa. 2007. Dimorphism of leaf galls induced by Pseudasphondylia neolitseae (Diptera: Cecidomyiidae) on Neolitsea sericea (Lauraceae) and their distributional patterns in Kyushu, Japan. Bulletin of the Kyushu University Museum 5: 57-64.

Monteiro, R. F.; R. A. Oda; P. A. L. Constantino & K. L. Narahara. 2004. Galhas: diversidade, especificidade e distribuição, p. 127-141. In: C. F. D. Rocha, F. A. Esteves & F. R. Scarano (eds.). Pesquisas de longa Duração na Restinga de Jurubatiba: Ecologia, História Natural e Conservação, Vol. 1. São Carlos, RiMa Editora, vii+376 p.

Möhn, E. 1959. Gallmücken (Diptera, Cecidomyiidae) aus El Salvador. 1. Teil. Senckenbergiana Biologica 40: 297-368.

Mohn, E. 1960. Gallmücken (Diptera, Cecidomyiidae) aus El Salvador. 2. Teil. Senckenbergiana Biologica 41: 197-240.

Möhn, E. 1961. Neue Asphondyliidi-Gattungen (Diptera, Itonididae). Stuttgarter Beiträge zur Naturkunde 49: 1-14.

Möhn, E. 1975. Gallmücken (Diptera, Itonididae) aus El Salvador. 7. Teil, Lasiopteridi. Stuttgarter Beiträge zur Naturkunde(A) 276: 1-101.

Morris, D. C.; M. P. Schwarz; S. J. B. Cooper & L. A. Mound. 2002. Phylogenetics of Australian acacia thrips: the evolution of behaviour and ecology. Molecular Phylogenetics and Evolution 25: 278-292.

Narahara, K. L.; V. C. Maia & R. F. Monteiro. 2004. Two new species of gall midges (Diptera, Cecidomyiidae) associated with Protium heptaphyllum (Aubl.) Marchand. (Burseraceae) in Brazil. Revista Brasileira de Entomologia 48: 485-490.

Novo-Guedes, R. & V. C. Maia, 2008. Gall midges (Diptera, Cecidomyiidae) associated with Heteropteris nitida DC. (Malpighiaceae). Arquivos do Museu Nacional 66: 359-362.

Nyman, T. 2002. The willow bud galler Euura mucronata Hartig (Hymenoptera: Tenthredinidae): one polyphage or many monophages? Heredity 88: 288-295.

Nyman, T. & R. Julkunen-Tiitto. 2000. Manipulation of the phenolic chemistry of willows by gall-inducing sawflies. Proceedings of the National Academy of Sciences USA 97: 13184-13187.

Nyman, T.; A. Widmer & H. Roininen. 2000. Evolution of gall morphology and host-plant relationships in willow-feeding sawflies (Hymenoptera: Tenthredinidae). Evolution 54: 526-533.

Oliveira, J. C. de & V. C. Maia. 2005. Ocorrência e caracterização de galhas de insetos na resting de Grumari (Rio de Janeiro, RJ, Brasil). Arquivos do Museu Nacional 63: 669-675.

Oliveira, U. P. de & V. C. Maia. 2008. A new species of gall midge (Diptera, Cecidomyiidae) associated with Sebastiania glandulosa (Euphrobiaceae). Arquivos do Museu Nacional 66: 355-358.

Pamplona, D. M.; V. C. Maia; M. S. Couri; C. J. E. Lamas & C. C. C. Aires. 2000. A survey on Diptera of Paquetá Island, Rio de Janeiro, RJ (Insecta, Diptera). Entomologist's Monthly Magazine 136: 169-175.

Price, P. W. 2003. Macroevolutionary theory on macroecological patterns. Cambridge, Cambridge University Press, viii+291 p.

Price, P. W. 2005. Adaptative radiation of gall-inducing insects. Basic and Applied Ecology 6: 413-421.

Price, P. W.; G. W. Fernandes & G. L. Waring. 1987. Adaptative nature of insect galls. Environmental Entomology 16: 15-24.

Price, P. W.; G. W. Fernandes; A. C. F. Lara; J. Brawn; D. Gerling; H. Barrios; M. G. Wright; S. P. Ribeiro & N. Rothcliff. 1998. Global patterns in local number of insect galling species. Journal of Biogeogeography 25: 581-591.

Price, P. W.; G. L.Waring & G. W. Fernandes. 1986. Hypotheses on the adaptive nature of galls. Proceedings of the Entomological Society of Washington 88: 361-363.

Raman, A. 1996. Nutritional diversity in gall-inducing insects and their evolutionary relationships with flowering plants. International Journal of Ecology & Environmental Sciences 22: 133-143.

Raman, A. 2007. Insect-induced plant galls of India: unresolved questions. Current Science 92: 748-757.

Raman, A.; C. W. Schaefer & T. M. Withers. 2005. Biology, ecology, and evolution of gall-inducing arthropods, Vol. 1 and 2. New Hampshire, Science Publishers Inc., xxi+817 p.

Rohfritsch, O. & J. D. Shorthouse. 1982. Insect galls, p. 131-152. In: G. Kahl & J. S. Schell (eds.). Molecular biology of plant tumors. New York, Academic Press, xxiv+615 p.

Rübsaamen, E. H. 1905. Beiträge zur Kenntnis aussereuropäischer Zoocecidien. II. Beitrag: Gallen aus Brasilien und Peru. Marcellia 4: 65-85, 115-138.

Rübsaamen, E. H. 1907. Beiträge zur Kenntnis aussereuropäischer Zoocecidien. III. Beitrag [cont.]: Gallen aus Brasilien und Peru. Marcellia 6: 110-173.

Rübsaamen, E. H. 1908. Beiträge zur Kenntnis aussereuropäischer Zoocecidien. III. Beitrag: Gallen aus Brasilien und Peru. Marcellia 7: 15-79.

Rübsaamen, E. H. 1916. Beitrag zur Kentnis aussereuropäischer Gallmücken. Sitzungsberichte der Gesellschaft Naturforschender Freunde zu Berlin 1915: 431-481.

Shorthouse, J. D.; D. Wool & A. Raman. 2005. Gall-inducing insect - Nature´s most sophicticated herbivores. Basic and Applied Ecology 6: 407-411.

Skuhravá, M. 1989. Taxonomic changes and records in palaeartic Cecidomyiidae (Diptera). Acta Entomológica Bohemoslovaca 86: 202-233.

Smith, E. L. 1970. Biosystematics and morphology of Symphyta. II. Biology of gall-making nematine sawflies of the California region. Annals Entomological Society of the American 63: 35-51.

Sousa, L. I. de & V. C. Maia. 2007. A new species of Schizomyia (Diptera, Cecidomyiidae, Asphondyliini) associated with Tetrapterys phlomoides (Malpighiaceae). Iheringia, Série Zooogica 97: 311-313.

Stern, D. L. 1995. Phylogenetic evidence that aphids, rather then plants, determine gall morfology. Proceedings Royal Society of London serie B256: 203-209.

Stone, G. N. & J. M. Cook. 1998. The structure of cynipid oak galls: patterns in the evolution of an extended phenotypes. Proceedings of the Royal Society of London Series B 265: 979-988.

Stone, G. N. & K. Schönrogge. 2003. The adaptive significance of insect gall morphology. Trends Ecology and Evolution 18: 512-522.

Stone, G. N.; K. Schönrogge; R. J. Atkinson; D. Bellido & J. Pujade-Villar. 2002. The population biology of oak gall wasps (Hymenoptera: Cynipidae). Annual Review of Entomology 47: 633-668.

Tavares, J. S. 1906. Descrição de uma Cecidomyia nova do Brazil, pertencente a um genero novo. Brotéria 5: 81-84.

Tavares, J. S. 1909. Contributio prima ad cognitionem cecidologiae braziliae. Brotéria: Série Zoológica 8: 5-28.

Tavares, J. S. 1915. As cecidias das plantas do gênero Styrax no Brazil. Broteria: Série Zoológica 13: 145-160.

Tavares, J. S. 1916a. Alguns muscídeos cecidogénicos do Brazil. Brotéria: Série Zoológica 15: 155-170.

Tavares, J. S. 1916b. Cecidomyias novas do Brazil. Broteria: Série Zoológica 14: 36-57.

Tavares, J. S. 1917a. As cecidias do Brazil que se criam nas plantas da família das Melastomataceae. Broteria: Série Zoológica 15: 18-49.

Tavares, J. S. 1917b. Cecidias brazileiras que se criam em plantas das Compositae, Rubiaceae, Tiliaceae, Lythraceae e Artocarpaceae. Broteria: Série Zoológica 15: 113-181.

Tavares, J. S. 1918a. Cecidologia brazileira. Cecidias que se criam em plantas das famílias das Verbenaceae, Euphorbiaceae, Malvaceae, Anacardiaceae, Labiatae, Rosaceae, Anonaceae, Ampelidaceae, Bignoniaceae, Aristolochiaceae e Solanaceae. Broteria: Série Zoológica 16: 21-68.

Tavares, J. S. 1918b. Cecidomyias novas do Brazil. Brotéria: Série Zoológica 16: 69-84.

Tavares, J. S. 1920a. Cecidologia brazileira. Cecidias que se criam em plantas das famílias das Leguminosae, Sapotaceae, Lauraceae, Myrtaceae, Punicaceae, Aurantiaceae, Malpighiaceae, Sapindaceae, Umbelliferae, Loranthaceae, Apocynaceae, Urticaceae, Salicaceae e Graminae. Broteria: Série Zoológica 18: 82-125.

Tavares, J. S. 1920b. O gênero Bruggmannniella Tav. com descripção de uma espécie nova e a clave dichotômica dos gêneros das Asphondyliariae. Broteria: Série Zoológica 18: 33-42.

Tavares, J. S. 1921. Cecidologia brazileira. Cecidias que se criam em plantas das famílias das Leguminosae, Sapotaceae, Lauraceae, Punicaceae, Aurantiaceae, Malpighiaceae, Sapindaceae, Umbelliferae, Loranthaceae, Apocynaceae, Urticaceae, Salicaceae e Graminae. Bróteria: Série Zoológica 19: 76-112.

Tavares, J. S. 1922. Cecidologia brazileira. As restantes famílias. Broteria: Série Zoológica 20: 5-48.

Tavares, J. S. 1925. Nova contribuição para o conhecimento da Cecidologia Brazileira. Brotéria: Série Zoológica 22: 5-55.

Tokuda, M.; K. M. Harris & J. Yukawa. 2005. Morphological features and molecular phylogeny of Placochela Rübsaamen (Diptera: Cecidomyiidae) with implications for taxonomy and host specificity. Entomological Science 8: 419-427.

Uechi, N.; M. Tokuda; J. Yukawa; F. Kawamura; K. K. Teramoto & K. M. Harris. 2003. Confirmation by DNA analysis that Contarinia maculipennis (Diptera: Cecidomyiidae) is a polyphagous pest of orchids and other unrelated cultivated plants. Bulletin of Entomological Research 93: 545-551.

Uechi, N.; J. Yukawa & D. Yamaguchi. 2004. Host alternation by gall midges of the genus Asphondylia (Diptera: Cecidomyiidae). In: N. L. Evenhuis, K. Y. Kaneshiro (eds.) Contributions to the systematics and evolution of Diptera. D. Elmo Hardy Memorial Volume of Bishop Museum Bulletin in Entomology, vol. 12, 53-66.

Urso-Guimarães, M. V. & D. S. Amorim. 2002. New Brazilian species of Asphondyliini (Diptera, Cecidomyiidae). Revista Brasileira de Entomologia 46: 561-570.

Urso-Guimarães, M. V. & C. Scarelli- Santos. 2006. Galls and gall makers in plants from the Pe-Gigante Cerrado Reserve, Santa Rita do Passa Quatro, SP, Brazil. Brazilian Journal of Biology 66: 357-369.

Viceconte, K. S. de M. & V. C. Maia. prelo. Novo gênero e nova espécie de Diptera, Cecidomyiidae associada com Psittacanthus dichrous (Loranthaceae). Arquivos do Museu Nacional 3/4.

Yukawa, J. & O. Rohfritsch. 2005. Biology and Ecology of Gall-inducing Cecidomyiidae (Diptera), p. 273-304. In: A. Raman, C. W. Schaefer & T. M. Withers (eds.). Biology, ecology, and evolution of gall-inducing arthropods, Vol. 1. New Hampshire, Science Publishers Inc., xxi+429 p.

Waring, G. L. & P. W. Price. 1989. Parasitoid pressure and the radiation of a gall-forming group (Cecidomyiidae: Asphondylia spp.) on creosote bush (Larrea tridentata). Oecologia 79: 293-299.

Weis, A. E.; R. Walton & C. L. Crego. 1988. Reactive plant tissue sites and the population biology of gall makers. Annual Review of Entomology 33: 467-486.

Received 21/12/2007; accepted 24/06/2009

Publication Dates

• Publication in this collection
  19 Oct 2009
• Date of issue
  2009

History

• Accepted
  24 June 2009
• Received
  21 Dec 2007