Mycophagy associations in Diptera can be divided into four distinct groups based on the lifestyle of each species. Primary mycophagists feed exclusively on fungi (basidiome or mycelium). Secondary mycophagists are called saprobes and feed on decaying hosts. Detritivores may feed on much decaying biological material, in this case they may oviposit on basidiome. Predators occur in association with all fungal structures, and their larvae are mainly predatory in the last stage (Santa-Brígida et al. 2012)SANTA-BRÍGIDA, R., WARTCHOW, F., MEDEIROS, P.S., GOTTSCHALK, M.S., SITTA, N. and SUSS, L., 2012. Insects parasitizing edible ectomycorrhizal mushrooms. Berlin: Springer, pp. 335-353.. For a better understanding of mycophagous flies, the selection of habit depends of fungi occurrence (Bunyard, 2018BUNYARD, B.A., 2018. Deadly Amanita Mushrooms as Food. Fungi, vol. 10, no. 4, pp. 40-48.). In addition, basidiomata only form with humidity and temperature specific to each species (Putzke and Putzke, 2017PUTZKE, J. and PUTZKE, M.T., 2017. Cogumelos-Fungos Agaricales no Brasil. Famílias Agaricaceae, Amanitaceae, Bolbitaceae, Entolomataceae, Coprinaceae/Psathyrellaceae, Crepidotaceae e Hygrophoraceae. 1ª ed. São Gabriel: Editora JP, pp 168-269.). An important point is that the larval phase of Diptera is relatively short (Yamashita and Hijii, 2007YAMASHITA, S. and HIJII, N., 2007. The role of fungal taxa and developmental stage of mushrooms in determining the composition of the mycophagous insect community in a Japanese forest. European Journal of Entomology, vol. 2, no. 104, pp. 225-233. http://dx.doi.org/10.14411/eje.2007.035.
http://dx.doi.org/10.14411/eje.2007.035...
), which may well coincide with the period of basidiome occurrence.
Gottschalk et al. (2009)GOTTSCHALK, M.S., BIZZO, L., DOGE, J.S., PROFES, M.S., HOFMANN, P.R. and VALENTE, V.L., 2009. Drosophilidae (Diptera) associated to fungi: differential use of resources in anthropic and Atlantic Rain Forest areas. Iheringia. Série Zoologia, vol. 99, no. 4, pp. 442-448. http://dx.doi.org/10.1590/S0073-47212009000400016.
http://dx.doi.org/10.1590/S0073-47212009...
and Bunyard (2018)BUNYARD, B.A., 2018. Deadly Amanita Mushrooms as Food. Fungi, vol. 10, no. 4, pp. 40-48. infer in their studies that mycophagous flies of Drosophilidae are associated with more than 31 species of mushrooms, some toxic such as Amanita muscaria (L.) Lam (Agaricaceae), including Drosophila fallen (Fallen, 1823), Leucophenga varia (Walker, 1849), Mycodrosophila dimidiate (Loew, 1862), and Zygothrica hypandriata (Burla, 1956BURLA, H., 1956. Die Drosophiliden-Gattung Zygothrica und ihre Beziehung zur Drosophila-Untergattung Hirtodrosophila. Mitteilungen aus dem Zoologischen Museum in Berlin, vol. 32, no. 2, pp. 189-321.). In addition, Bunyard and Foote (1990)BUNYARD, B.A. and FOOTE, B.A., 1990. Acalyptrate Diptera reared from higher fungi in northeastern Ohio. Entomological News, vol. 101, no. 2, pp. 117-121. reported that the life cycle of Drosophila putrida (Sturtevant, 1916) was associated with the mushroom Oudemansiella radicata (Relhan) Singer (Physalacriaceae).
Oudemansiella cubensis (Berk. & MA Curtis) RH Petersen (2010) has a fleshy pileus and is described in Brazil, Costa Rica, Cuba, Dominican Republic, Ecuador, Colombia, and Argentina (Petersen et al., 2008PETERSEN, R.H., DESJARDIN, D.E. and KRUGER, D., 2008. Three type specimens designated in Oudemansiella. Fungal Diversity, vol. 32, no. 4, pp. 81-96.; Wartchow et al., 2010WARTCHOW, F., PEREIRA, J., DRECHSLER-SANTOS, E.R., GOMES-SILVA, A.C., TIAGO, P.V., PUTZKE, J. and CAVALCANTI, M.A.Q., 2010. Two Oudemansiella species with echinulate basidiospores from South America with O. macracantha lectotypified. Mycotaxon, vol. 113, no. 1, pp. 119-127. http://dx.doi.org/10.5248/113.119.
http://dx.doi.org/10.5248/113.119...
). The species is mentioned as native in South America (Putzke and Putzke, 2017PUTZKE, J. and PUTZKE, M.T., 2017. Cogumelos-Fungos Agaricales no Brasil. Famílias Agaricaceae, Amanitaceae, Bolbitaceae, Entolomataceae, Coprinaceae/Psathyrellaceae, Crepidotaceae e Hygrophoraceae. 1ª ed. São Gabriel: Editora JP, pp 168-269.). There are no known cases of mycophagous flies associated with this mushroom in the literature. There are no reports of mycophagous of feeding habits to Zygothrica candens (Burla, 1956BURLA, H., 1956. Die Drosophiliden-Gattung Zygothrica und ihre Beziehung zur Drosophila-Untergattung Hirtodrosophila. Mitteilungen aus dem Zoologischen Museum in Berlin, vol. 32, no. 2, pp. 189-321.), and this is the first report involving O. cubensis. Also, the fly is distributed only in Brazil and Ecuador, considered native to South America (Tidon et al., 2022TIDON, R., GOTTSCHALK, M.S., SCHMITZ, H.J., and MARTINS, M.B., 2022 [viewed 6 September 2022]. Drosophilidae. In: JARDIM BOTÂNICO DO RIO DE JANEIRO, ed. Catálogo taxonômico da fauna do Brasil [online]. Rio de Janeiro: JBRJ. Available from: http://fauna.jbrj.gov.br/fauna/faunadobrasil/183449
http://fauna.jbrj.gov.br/fauna/faunadobr...
). Thus, the present study aimed to describe the first record of mycophagy and the association of Z. candens with the mushroom O. cubensis in southern Brazil.
The study was conducted in September 2021 in the National Forest (FLONA) in São Francisco de Paula, Rio Grande do Sul, Brazil (-29°25'22”S and -50°23'11”W), a conservation unit of approximately 1,606.00 hectares of native Atlantic Forest, with fragments of dense ombrophilous forest and mixed ombrophilous forest. Samples were collected in the Centenarian Araucaria Trail. Four basidiomata of mushroom with signs of mycophagy growing on the substrate of Araucaria angustifolia Bertol. (Kuntze), and five adult flies in the basidiomata were collected to identification. The mushrooms and flies were collected under license SISBIO n° 78538-1.
Basidiomata were dried at 40°C and stored in paper bags for taxonomic identification using the key of Putzke and Putzke (2017)PUTZKE, J. and PUTZKE, M.T., 2017. Cogumelos-Fungos Agaricales no Brasil. Famílias Agaricaceae, Amanitaceae, Bolbitaceae, Entolomataceae, Coprinaceae/Psathyrellaceae, Crepidotaceae e Hygrophoraceae. 1ª ed. São Gabriel: Editora JP, pp 168-269.. Drosophilids were preserved in tubes containing 70% ethyl alcohol and identified based on external morphology and genitalia (male and female) according to Burla (1956)BURLA, H., 1956. Die Drosophiliden-Gattung Zygothrica und ihre Beziehung zur Drosophila-Untergattung Hirtodrosophila. Mitteilungen aus dem Zoologischen Museum in Berlin, vol. 32, no. 2, pp. 189-321. and Grimaldi (1987)GRIMALDI, D.A., 1987. Phylogenetics and taxonomy of Zygothrica (Diptera, Drosophilidae). New York: American Museum of Natural History. Bulletin of the AMNH, vol. 186, article 2.. Both samples were examined with optical microscope Olympus DP53 and Zeiss Discovery V20. Subsequently, the samples were deposited at the Laboratório de Taxonomia de Fungos in Universidade Federal do Pampa, Campus São Gabriel, Rio Grande do Sul, Brazil.
As taxonomic characters, O. cubensis has a pileus 30-120 mm in diameter, grayish white. Surface of the pileus with scales and glutinous. Fleshy context with grayish-white lamellae of 1.5 mm, adnate. Stipe white, fibrillose-squamous with a base of 30-140 × 2-20 mm (Figure 1A). White or cream spores with 10-16 μm, globose to subglobose, smooth and thick-walled, inamyloid, hyaline. Basidia with 50-120 × 18-30 μm, clavate and tetrasporic. Pleurocystidia and cheilocystidia numerous with 70-200 × 15-50 μm, versiform (Figure 1B). Pileipellis formed by piriform or subglobose elements. Context formed by broad filamentous hyphae. Cortical layer of the stipe formed by thin filamentous hyphae. Grows on wood. Distribution in Brazil in Porto Alegre city - Rio Grande do Sul state (Putzke and Pereira, 1988PUTZKE, J. and PEREIRA, A.B., 1988. O Gênero Oudemansiella Speg. no Rio Grande do Sul, Brasil. Caderno de Pesquisa. Série Biologia, vol. 1, no. 1, pp. 47-69.), and São Paulo city - São Paulo state (Singer, 1989SINGER, R., 1989. New taxa and new combinations of Agaricales (Diagnoses Novorum Agaricalium IV). Fieldiana. Botany, vol. 21, no. 2, pp. 1-133.). In São Francisco de Paula city - Rio Grande do Sul state this is the first record of the species.
Macro and microstructures of the species analyzed in this study. Oudemansiella cubensis: pileus top view 1-A, bottom view 2-A, arrows indicating adult flies found in the basidiome 3-A, spores 1-B, basidium 2-B, lamellar trama 3-B. Zygothrica candens female: lateral view 1-C, frontal view head 2-C, genitalia (oviscapt valve + spermathecal capsule) 3-C, dorsal view abdomen 4-C, dorsal view thorax 5-C. Zygothrica candens male: lateral view 1-D, frontal view head 2-D, genitalia (hypandrium in V-shaped and pregonites + phallus and phallapodeme) 3-D, dorsal view abdomen 4-D, dorsal view thorax 5-D.
During the collection of material, individuals in holometabolous development stages (embryos, larvae, pupae and adults) of Z. candens were found in the lamellar region of O. cubensis. According to Burla (1956)BURLA, H., 1956. Die Drosophiliden-Gattung Zygothrica und ihre Beziehung zur Drosophila-Untergattung Hirtodrosophila. Mitteilungen aus dem Zoologischen Museum in Berlin, vol. 32, no. 2, pp. 189-321. as taxonomic characters, Z. candens has head brown, eyes red, pedicel and scape brown, total length 18-25 mm. Orbital and bristles plates are brown. Front and face ochre with ocellar tringle occupying approximately 1/2 of the frontal length. Thorax with dark and light bands brownish-brown, scutellum brown and slighter in the margins, legs yellow. Wings hyaline, without distinct spots with veins straight. Abdomen yellow with brown bands on tergites. Terminalia in U-shaped form with frontal lobes small. Hypandrium in V-shaped form containing many growth lines. Phallapodeme short in lateral view (Figure 1C and D). Distribution in Brazil in Boracéia city - São Paulo state (Val and Kaneshiro, 1988VAL, F.C. and KANESHIRO, K.Y., 1988. Drosophilidae (Diptera) from the Estação Biologica de Boraceia, on the coastal range of the State of São Paulo, Brazil: Geographical distribution. Rio de Janeiro: Academia Brasileira de Ciências, pp. 189-203.) and Itatiaia city - Rio de Janeiro state (Burla 1956BURLA, H., 1956. Die Drosophiliden-Gattung Zygothrica und ihre Beziehung zur Drosophila-Untergattung Hirtodrosophila. Mitteilungen aus dem Zoologischen Museum in Berlin, vol. 32, no. 2, pp. 189-321.; Wheeler, 1970WHEELER, M.R., 1970. Family Drosophilidae: a catalogue of the Diptera of the Americas south of the United States. São Paulo: Museu de Zoologia, Universidade de São Paulo, pp. 79.1-79.65.). There is already a case for the São Francisco de Paula city - Rio Grande do Sul state (Gauterio et al., 2020GAUTERIO, T.B., MACHADO, S., LORETO, E.L., GOTTSCHALK, M.S. and ROBE, L.J., 2020. Phylogenetic relationships between fungus-associated Neotropical species of the genera Hirtodrosophila, Mycodrosophila and Zygothrica (Diptera, Drosophilidae), with insights into the evolution of breeding sites usage. Molecular Phylogenetics and Evolution, vol. 145, pp. 106733. http://dx.doi.org/10.1016/j.ympev.2020.106733.
http://dx.doi.org/10.1016/j.ympev.2020.1...
).
In relation to the characteristics of the interaction of mycophagy between fly and mushroom, the mushroom has shown signs of predation in the lamellar portions of the basidiome. In the analyzes of internal structures of digestive system of the fly, spores mushroom were found in the hindgut. External structures, such as wings, legs, thorax and abdomen also showed attached spores.
The study reports the first observation of mycophagy association of Z. candens with O. cubensis in southern Brazil. The natural population of Zygothrica has already been described in Rio Grande do Sul state (Valer et al., 2016VALER, F.B., BERNARDI, E., MENDES, M.F., BLAUTH, M.L. and GOTTSCHALK, M.S., 2016. Diversity and associations between Drosophilidae (Diptera) species and Basidiomycetes in a Neotropical forest. Anais da Academia Brasileira de Ciências, vol. 88, no. 1, suppl. 1, pp. 705-718. http://dx.doi.org/10.1590/0001-3765201620150366. PMid:27142546.
http://dx.doi.org/10.1590/0001-376520162...
; Gauterio et al., 2020GAUTERIO, T.B., MACHADO, S., LORETO, E.L., GOTTSCHALK, M.S. and ROBE, L.J., 2020. Phylogenetic relationships between fungus-associated Neotropical species of the genera Hirtodrosophila, Mycodrosophila and Zygothrica (Diptera, Drosophilidae), with insights into the evolution of breeding sites usage. Molecular Phylogenetics and Evolution, vol. 145, pp. 106733. http://dx.doi.org/10.1016/j.ympev.2020.106733.
http://dx.doi.org/10.1016/j.ympev.2020.1...
). However, the occurrence of Z. candens on O. cubensis is new. This fact can be associated with fungi species whose known distribution from southern region of the country (Petersen et al., 2008PETERSEN, R.H., DESJARDIN, D.E. and KRUGER, D., 2008. Three type specimens designated in Oudemansiella. Fungal Diversity, vol. 32, no. 4, pp. 81-96.; Wartchow et al., 2010WARTCHOW, F., PEREIRA, J., DRECHSLER-SANTOS, E.R., GOMES-SILVA, A.C., TIAGO, P.V., PUTZKE, J. and CAVALCANTI, M.A.Q., 2010. Two Oudemansiella species with echinulate basidiospores from South America with O. macracantha lectotypified. Mycotaxon, vol. 113, no. 1, pp. 119-127. http://dx.doi.org/10.5248/113.119.
http://dx.doi.org/10.5248/113.119...
).
Neotropical mycophagous flies are also represented in the Drosophilidae. Bunyard (2018)BUNYARD, B.A., 2018. Deadly Amanita Mushrooms as Food. Fungi, vol. 10, no. 4, pp. 40-48. studied three mycophagous flies feeding on Amanita sp., which is considered a toxic species. Nevertheless, drosophilids are not only associated with toxic mushrooms. Other Agaricomycetes, belonging to the families Agaricaceae and Boletaceae (Bunyard, 2007BUNYARD, B.A., 2007. Legerdemain in the fungal domain: the use and abuse of insects by fungi. American Entomologist, vol. 53, no. 4, pp. 236-239. http://dx.doi.org/10.1093/ae/53.4.236.
http://dx.doi.org/10.1093/ae/53.4.236...
), as well as Oudemansiella sp. (Physalacriaceae) have already been described in the literature in mycophagy associations with drosophilids (Bunyard and Foote, 1990BUNYARD, B.A. and FOOTE, B.A., 1990. Acalyptrate Diptera reared from higher fungi in northeastern Ohio. Entomological News, vol. 101, no. 2, pp. 117-121.). The latter are classified as non-toxic mushrooms (Putzke and Putzke, 2017PUTZKE, J. and PUTZKE, M.T., 2017. Cogumelos-Fungos Agaricales no Brasil. Famílias Agaricaceae, Amanitaceae, Bolbitaceae, Entolomataceae, Coprinaceae/Psathyrellaceae, Crepidotaceae e Hygrophoraceae. 1ª ed. São Gabriel: Editora JP, pp 168-269.). In the study by Gauterio et al. (2020)GAUTERIO, T.B., MACHADO, S., LORETO, E.L., GOTTSCHALK, M.S. and ROBE, L.J., 2020. Phylogenetic relationships between fungus-associated Neotropical species of the genera Hirtodrosophila, Mycodrosophila and Zygothrica (Diptera, Drosophilidae), with insights into the evolution of breeding sites usage. Molecular Phylogenetics and Evolution, vol. 145, pp. 106733. http://dx.doi.org/10.1016/j.ympev.2020.106733.
http://dx.doi.org/10.1016/j.ympev.2020.1...
with analyzes of the phylogenetic relationships of Zygothrica and other genera of drosophilids associated with fungi, it was inferred that the neotropical group has a lineage close with neotropical fungi of Auriculariales and Agaricales. In these two cited orders, the use of the fly as a breeding site and the presence of its larvae are reported in the fungi, but the taxonomic information on the fungi was not mentioned. However, this factor could be an of the most important indicators of this association.
In studies conducted in the Brazilian Amazon involving arthropods associated with edible mushrooms, Amaringo-Cortegano et al. (2013)AMARINGO-CORTEGANO, C.A., VARGAS-ISLA, R., MORAIS, J.M. and ISHIKAWA, N.K., 2013. Artrópodos asociados a seis especies de hongos comestibles de ocurrencia natural en Manaus, Amazonas, Brasil. Biota Amazônia, vol. 3, no. 3, pp. 54-63. http://dx.doi.org/10.18561/2179-5746/biotaamazonia.v3n3p54-63.
http://dx.doi.org/10.18561/2179-5746/bio...
found a relationship among O. cubensis and individuals of Poduromorpha and Siphonophorida. The latter order was identified in 87% of the collected samples containing mycophagous individuals. However, the authors did not report individuals of drosophilids. Doge et al. (2015)DOGE, J.S., DE OLIVEIRA, H.V. and TIDON, R., 2015. Rapid response to abiotic and biotic factors controls population growth of two invasive drosophilids (Diptera) in the Brazilian Savanna. Biological Invasions, vol. 17, no. 8, pp. 2461-2474. http://dx.doi.org/10.1007/s10530-015-0889-0.
http://dx.doi.org/10.1007/s10530-015-088...
reported that resource variability is the main factor for the Drosophilidae population size. In addition, fleshy basidiomata such as O. cubensis are reported to be preferred by the mycophagous flies (Santa-Brígida et al. 2012SANTA-BRÍGIDA, R., WARTCHOW, F., MEDEIROS, P.S., GOTTSCHALK, M.S., SITTA, N. and SUSS, L., 2012. Insects parasitizing edible ectomycorrhizal mushrooms. Berlin: Springer, pp. 335-353.). According to Gauterio et al. (2020)GAUTERIO, T.B., MACHADO, S., LORETO, E.L., GOTTSCHALK, M.S. and ROBE, L.J., 2020. Phylogenetic relationships between fungus-associated Neotropical species of the genera Hirtodrosophila, Mycodrosophila and Zygothrica (Diptera, Drosophilidae), with insights into the evolution of breeding sites usage. Molecular Phylogenetics and Evolution, vol. 145, pp. 106733. http://dx.doi.org/10.1016/j.ympev.2020.106733.
http://dx.doi.org/10.1016/j.ympev.2020.1...
, mycophagous flies and fungi coevolved. Moreover, most flies already analyzed are polyphagous and complete their life cycle in basidiomata (Bunyard, 2018BUNYARD, B.A., 2018. Deadly Amanita Mushrooms as Food. Fungi, vol. 10, no. 4, pp. 40-48.). Another important factor is the presence of soft tissues in Agaricales, macro and micronutrients, and the tolerance of mycophagous flies to fungal toxins, as concluded by Yamashita and Hijii (2007)YAMASHITA, S. and HIJII, N., 2007. The role of fungal taxa and developmental stage of mushrooms in determining the composition of the mycophagous insect community in a Japanese forest. European Journal of Entomology, vol. 2, no. 104, pp. 225-233. http://dx.doi.org/10.14411/eje.2007.035.
http://dx.doi.org/10.14411/eje.2007.035...
. Thus, even if Z. candens have occurrence in this region, it is more feasible to infer that the fly uses the mushroom as a temporal resource. In this sense, the mushroom is not the main responsible for the maintenance of its guild richness. As a benefit, the fly disperses the spores of this mushroom to distances reachable by its flight.
The adaptation of the fly in using a spatially unpredictable temporal resource such as the basidiome may be the key that determines the success of species presence in the region. Also, the attractiveness of the mushroom resulting both from the quality of the substrate, as in the case of A. angustifolia trees, and the natural influence of the FLONA are intrinsically involved in this association. However, O. cubensis is considered an arboreal host, with wood as its main substrate (Putzke and Putzke, 2017PUTZKE, J. and PUTZKE, M.T., 2017. Cogumelos-Fungos Agaricales no Brasil. Famílias Agaricaceae, Amanitaceae, Bolbitaceae, Entolomataceae, Coprinaceae/Psathyrellaceae, Crepidotaceae e Hygrophoraceae. 1ª ed. São Gabriel: Editora JP, pp 168-269.), so the occurrence of the fungi is not restricted to the distribution of A. angustifolia. According to Bunyard (2007BUNYARD, B.A., 2007. Legerdemain in the fungal domain: the use and abuse of insects by fungi. American Entomologist, vol. 53, no. 4, pp. 236-239. http://dx.doi.org/10.1093/ae/53.4.236.
http://dx.doi.org/10.1093/ae/53.4.236...
, 2018BUNYARD, B.A., 2018. Deadly Amanita Mushrooms as Food. Fungi, vol. 10, no. 4, pp. 40-48.), it is unpredictability that drives the mechanisms of speciation in drosophilids. The occurrence of the fly and the mycophagy associated with the entire life cycle of the studied individuals, which includes oviposition, growth phases and return of the adult individual, are possibly interconnected. Therefore, further analysis should be conducted, considering that the description of this mycophagy association is unprecedented for both species and has only been described in southern Brazil.
Acknowledgements
The authors would like to thank the Laboratório de Taxonomia de Fungos from Universidade Federal do Pampa and to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001.
References
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» http://dx.doi.org/10.18561/2179-5746/biotaamazonia.v3n3p54-63 - BUNYARD, B.A., 2007. Legerdemain in the fungal domain: the use and abuse of insects by fungi. American Entomologist, vol. 53, no. 4, pp. 236-239. http://dx.doi.org/10.1093/ae/53.4.236
» http://dx.doi.org/10.1093/ae/53.4.236 - BUNYARD, B.A., 2018. Deadly Amanita Mushrooms as Food. Fungi, vol. 10, no. 4, pp. 40-48.
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- DOGE, J.S., DE OLIVEIRA, H.V. and TIDON, R., 2015. Rapid response to abiotic and biotic factors controls population growth of two invasive drosophilids (Diptera) in the Brazilian Savanna. Biological Invasions, vol. 17, no. 8, pp. 2461-2474. http://dx.doi.org/10.1007/s10530-015-0889-0
» http://dx.doi.org/10.1007/s10530-015-0889-0 - GAUTERIO, T.B., MACHADO, S., LORETO, E.L., GOTTSCHALK, M.S. and ROBE, L.J., 2020. Phylogenetic relationships between fungus-associated Neotropical species of the genera Hirtodrosophila, Mycodrosophila and Zygothrica (Diptera, Drosophilidae), with insights into the evolution of breeding sites usage. Molecular Phylogenetics and Evolution, vol. 145, pp. 106733. http://dx.doi.org/10.1016/j.ympev.2020.106733
» http://dx.doi.org/10.1016/j.ympev.2020.106733 - GOTTSCHALK, M.S., BIZZO, L., DOGE, J.S., PROFES, M.S., HOFMANN, P.R. and VALENTE, V.L., 2009. Drosophilidae (Diptera) associated to fungi: differential use of resources in anthropic and Atlantic Rain Forest areas. Iheringia. Série Zoologia, vol. 99, no. 4, pp. 442-448. http://dx.doi.org/10.1590/S0073-47212009000400016
» http://dx.doi.org/10.1590/S0073-47212009000400016 - GRIMALDI, D.A., 1987. Phylogenetics and taxonomy of Zygothrica (Diptera, Drosophilidae). New York: American Museum of Natural History. Bulletin of the AMNH, vol. 186, article 2.
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- PUTZKE, J. and PUTZKE, M.T., 2017. Cogumelos-Fungos Agaricales no Brasil. Famílias Agaricaceae, Amanitaceae, Bolbitaceae, Entolomataceae, Coprinaceae/Psathyrellaceae, Crepidotaceae e Hygrophoraceae 1ª ed. São Gabriel: Editora JP, pp 168-269.
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» http://fauna.jbrj.gov.br/fauna/faunadobrasil/183449 - VAL, F.C. and KANESHIRO, K.Y., 1988. Drosophilidae (Diptera) from the Estação Biologica de Boraceia, on the coastal range of the State of São Paulo, Brazil: Geographical distribution. Rio de Janeiro: Academia Brasileira de Ciências, pp. 189-203.
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Publication Dates
-
Publication in this collection
06 Jan 2023 -
Date of issue
2022
History
-
Received
15 Sept 2022 -
Accepted
04 Dec 2022