Home Sweet Home: Yeasts Living in Substrates Related with Melipona scutellaris in the Brazilian Atlantic Forest

Renan do Nascimento Barbosa; Jadson D. P. Bezerra; Joana C. de Moura; José Ewerton F. dos Santos; Isaias Oliveira Junior; Cristina M. de Souza-Motta; Neiva T. de Oliveira

doi:10.13102/sociobiology.v71i2.10359

Authors

Renan do Nascimento Barbosa Universidade Federal de Pernambuco, Centro de Biociências, Departamento de Micologia, Recife-PE, Brazil
Jadson D. P. Bezerra Universidade Federal de Goiás, Instituto de Patologia Tropical e Saúde Pública, Departamento de Biociências e Tecnologia, Goiânia-GO, Brazil
Joana C. de Moura Universidade Federal de Pernambuco, Centro de Biociências, Departamento de Micologia, Recife-PE, Brazil
José Ewerton F. dos Santos Universidade Federal de Pernambuco, Centro de Biociências, Departamento de Micologia, Recife-PE, Brazil
Isaias Oliveira Junior Universidade Federal de Pernambuco, Centro de Biociências, Departamento de Micologia, Recife-PE, Brazil
Cristina M. de Souza-Motta Universidade Federal de Pernambuco, Centro de Biociências, Departamento de Micologia, Recife-PE, Brazil
Neiva T. de Oliveira Universidade Federal de Pernambuco, Centro de Biociências, Departamento de Micologia, Recife-PE, Brazil

DOI:

https://doi.org/10.13102/sociobiology.v71i2.10359

Keywords:

Ascomycota, Basidiomycota, native bees, insect-fungus associations, yeast symbiosis

Abstract

The interaction between stingless bees and fungi has garnered recent interest due to potential mutual benefits. In Brazil, Melipona scutellaris stands out ecologically and economically. We investigated its microbiota, focusing on yeast species in pot-honey, pot-pollen, and nest surfaces. Samples from the Atlantic Forest (Pernambuco state, Brazil) were analyzed through morphological and physiological methods and D1/D2 LSU rDNA sequence analysis. We identified 20 yeast species, comprising 15 ascomycetes and five basidiomycetes, representing 11 and five genera, respectively. All yeast species, except Blastobotrys meliponae, were reported for the first time in association with M. scutellaris. Honey exhibited the highest species richness. In this study, the species Blastobotrys meliponae, Meyerozyma caribbica, Wickerhamomyces anomalus, and Moniliella carnis were exclusively isolated from honey. The understanding of the ecological association between stingless bees and yeasts, as revealed in our research, can significantly aid in insect conservation programs. We present the first report of yeasts associated with M. scutellaris substrates living in the Brazilian Atlantic Forest.

Downloads

Download data is not yet available.

References

Alves, R.M.O., Alfredo, C., Souza, B.A. & Santos, W.S. (2012). Areas of natural occurrence of Melipona scutellaris Latreille, 1811 (Hymenoptera: Apidae) in the state of Bahia, Brazil. Anais da Academia Brasileira de Ciencias, 84: 679-688. DOI: https://doi.org/10.1590/S0001-37652012000300010

Amos, B.A., Leemon, D.L., Hayes, R.A., Cribb, B.W. & Furlong, M.J. (2018). Associations between the small hive beetle and the yeast Kodamaea ohmeri throughout the host life cycle. Journal of Economic Entomology, 111: 1501-1508. DOI: https://doi.org/10.1093/jee/toy121

Barbosa, R.N., Bezerra, J.D.P., Souza-Motta, C.M., Frisvad, J.C., Samson, R.A., Oliveira, N.T. & Houbraken, J. (2018). New Penicillium and Talaromyces species from honey, pollen and nests of stingless bees. Antonie van Leeuwenhoek, 111: 1883-1912. DOI: https://doi.org/10.1007/s10482-018-1081-1

Barbosa, R.N., Bezerra, J., Souza-Motta, C., Gomes, B.S., Costa, C. & Melo, H. (2016). Prospection on yeasts from stingless bees honey in Brazilian Tropical Dry Forest (Caatinga). Gaia Scientia, 10: 151-159. DOI: https://doi.org/10.21707/gs.v10.n04a11

Barbosa, R.N., Leong, S.L., Vinnere-Pettersson, O., Chen, A.J., Souza-Motta, C.M., Frisvad, J.C., Samson, R.A., Oliveira, N.T. & Houbraken, J. (2017). Phylogenetic analysis of Monascus and new species from honey, pollen and nests of stingless bees. Studies in Mycology, 86: 29-51. DOI: https://doi.org/10.1016/j.simyco.2017.04.001

Barbosa, R.N., Santos, J.E.F., Bezerra, J.D.P., Istel, Ł., Houbraken, J., Oliveira, N.T. & Souza-Motta, C. M. (2022). Brazilian Atlantic Forest and Pampa biomes in the spotlight: an overview of Aspergillus, Penicillium, and Talaromyces (Eurotiales) species and the description of Penicillium nordestinense sp. nov. Acta Botanica Brasilica, 36: e2021 abb0390. DOI: https://doi.org/10.1590/0102-33062021abb0390

Barry, J., Metz, M., Hughey, J., Quirk, A. & Bochman, M. (2018). Two novel strains of Torulaspora delbrueckii isolated from the honey bbee microbiome and their use in hhoney Fermentation. Fermentation, 4: 22. DOI: https://doi.org/10.3390/fermentation4020022

Batra, L.R., Batra, S.W.T. & Bohart, G.E. (1973). The mycoflora of domesticated and wild bees (Apoidea). Mycopathologia et Mycologia Applicata, 49: 13-44. DOI: https://doi.org/10.1007/BF02057445

Benda, N.D., Boucias, D., Torto, B. & Teal, P. (2008). Detection and characterization of Kodamaea ohmeri associated with small hive beetle Aethina tumida infesting honey bee hives. Journal of Apicultural Research, 47: 194-201. DOI: https://doi.org/10.1080/00218839.2008.11101459

Beux, M.R., Ávila, S., Surek, M., Bordin, K., Leobet, J., Barbieri, F., Ferreira, S.M.R. & Rosa, E.A.R. (2022). Microbial biodiversity in honey and pollen pots produced by Tetragonisca angustula (Jataí). Brazilian Archives of Biology and Technology, 65: e22210440. DOI: https://doi.org/10.1590/1678-4324-2022210440

Blackwell, M. (2011). The fungi: 1, 2, 3 ... 5.1 million species? American Journal of Botany, 98: 426-438. DOI: https://doi.org/10.3732/ajb.1000298

Boekhout, T., Amend, A.S., El Baidouri, F., Gabaldón, T., Geml, J., Mittelbach, M., Robert, V., Tan, C.S., Turchetti, B., Vu, D., Wang, Q.-M. & Yurkov, A. (2021). Trends in yeast diversity discovery. Fungal Diversity, 114: 491-537. DOI: https://doi.org/10.1007/s13225-021-00494-6

Brysch-Herzberg, M. (2004). Ecology of yeasts in plant-bumblebee mutualism in Central Europe. FEMS Microbiology Ecology, 50: 87-100. DOI: https://doi.org/10.1016/j.femsec.2004.06.003

Buzzini, P., Turchetti, B. & Yurkov, A. (2018). Extremophilic yeasts: the toughest yeasts around? Yeast, 35: 487-497. DOI: https://doi.org/10.1002/yea.3314

Camargo, J.M.F., Garcia, M.M.B. & Castrillon A. (1992). Notas prévias sobre a bionomia de Ptilotrigonalurida (Hymenoptera, Apidae, Meliponinae): Associação de

leveduras em pólen estocado. Boletim do Museu Paraense Emílio Goeldi – Série Zoologia, 2: 391-395.

Cano, R.J., Borucki, M.K., Higby-Schweitzer, M., Poinar, H.N., Poinar, G.O. & Pollard, K.J. (1994). Bacillus DNA in fossil bees: an ancient symbiosis? Applied and Environmental Microbiology, 60: 2164-2167. DOI: https://doi.org/10.1128/aem.60.6.2164-2167.1994

Canto, A., Herrera, C.M. & Rodriguez, R. (2017). Nectar-living yeasts of a tropical host plant community: diversity and effects on community-wide floral nectar traits. PeerJ, 5: e3517. DOI: https://doi.org/10.7717/peerj.3517

Cappelli, A., Favia, G. & Ricci, I. (2021). Wickerhamomyces anomalus in Mosquitoes: A Promising Yeast-Based Tool for the “Symbiotic Control” of Mosquito-Borne Diseases. Frontiers in Microbiology, 11: 621605. DOI: https://doi.org/10.3389/fmicb.2020.621605

Carreiro, S.C., Pagnocca, F.C., Bacci, M., Lachance, M.-A., Bueno, O.C., Hebling, M.J.A., Ruivo, C.C.C. & Rosa, C.A. (2004). Sympodiomyces attinorum sp. nov., a yeast species associated with nests of the leaf-cutting ant Atta sexdens. International Journal of Systematic and Evolutionary Microbiology, 54: 1891-1894. DOI: https://doi.org/10.1099/ijs.0.63200-0

Cornman, R.S., Tarpy, D.R., Chen, Y., Jeffreys, L., Lopez, D., Pettis, J.S., van Engelsdorp, D. & Evans, J.D. (2012). Pathogen webs in collapsing honey bee colonies. PLoS ONE, 7: e43562. DOI: https://doi.org/10.1371/journal.pone.0043562

Costa Neto, D.J. & Morais, P.B. (2020). The vectoring of Starmerella species and other yeasts by stingless bees in a Neotropical savanna. Fungal Ecology, 47: 100973. DOI: https://doi.org/10.1016/j.funeco.2020.100973

Crous, P.W., Wingfield, M.J., Richardson, D.M., Leroux, J.J., Strasberg, D., Edwards, J., Roets, F., Hubka, V., Taylor, P.W.J., Heykoop, M., Martín, M.P., Moreno, G., Sutton, D.A., Wiederhold, N.P., Barnes, C.W., Carlavilla, J.R., Gené, J., Giraldo, A., Guarnaccia, V. & Guarro, J. (2016). Fungal Planet description sheets: 400-468. Persoonia – Molecular Phylogeny and Evolution of Fungi, 36: 316-458. DOI: https://doi.org/10.3767/003158516X692185

de Hoog, G.S. & Smith, M.T. (1998). Moniliella Stolk & Dakin. In: C.P. Kurtzman, J.W. Fell & T. Boekhout (Eds), The Yeasts Taxonomic Study 4th edn (pp. 785-788). Amsterdam: Elsevier. DOI: https://doi.org/10.1016/B978-044481312-1/50106-4

de Paula, G.T., Menezes, C., Pupo, M.T. & Rosa, C.A. (2021). Stingless bees and microbial interactions. Current Opinion in Insect Science, 44: 41-47. DOI: https://doi.org/10.1016/j.cois.2020.11.006

de Paula G.T., Melo, W.G.P., Castro, I., Menezes, C., Paludo, C.R., Rosa, C.A. & Pupo, M.T. (2023). Further evidences of an emerging stingless bee-yeast symbiosis. Frontiers Microbiology, 14: 1221724 DOI: https://doi.org/10.3389/fmicb.2023.1221724

Detry, R., Simon-Delso, N., Bruneau, E. & Daniel, H.-M. (2020). Specialisation of Yeast Genera in Different Phases of Bee Bread Maturation. Microorganisms, 8: 1789. DOI: https://doi.org/10.3390/microorganisms8111789

Dooms, L., Hennebert, G L. & Verachtert, H. (1971). Polyol synthesis and taxonomic characters in the genus Moniliella. Antonie van Leeuwenhoek International Journal of General and Molecular Microbiology, 37: 107-118. DOI: https://doi.org/10.1007/BF02218471

Douglas, A.E. & Smith, D.C. (1989). Are endosymbioses mutualistic? Trends in Ecology and Evolution, 4: 350-352. DOI: https://doi.org/10.1016/0169-5347(89)90090-6

Echeverrigaray, S., Scariot, F.J., Foresti, L., Schwarz, L.V., Rocha, R.K.M., da Silva, G.P., Moreira, J.P. & Delamare, A.P.L. (2021). Yeast biodiversity in honey produced by stingless bees raised in the highlands of southern Brazil. International Journal of Food Microbiology, 347: 109200. DOI: https://doi.org/10.1016/j.ijfoodmicro.2021.109200

Engel, P. & Moran, N.A. (2013). The gut microbiota of insects – diversity in structure and function. FEMS Microbiology Reviews, 37: 699-735. DOI: https://doi.org/10.1111/1574-6976.12025

Fleet, G.H. (2011). Yeast spoilage of foods and beverages. In: C.P. Kurtzman, J.W. Fell & T. Boekhout (Eds), The Yeasts (Fifth Edition) (pp.53-63). Cambrigde: Cambridge University Press. DOI: https://doi.org/10.1016/B978-0-444-52149-1.00005-7

Ganter, P.F. (2006). Yeast and invertebrate associations. In: G. Péter, C. Rosa (Eds), Biodiversity and ecophysiology of yeasts (pp. 303-370). Berlin, Heidelberg: Springer Berlin Heidelberg. DOI: https://doi.org/10.1007/3-540-30985-3_14

Gibson, C.M. & Hunter, M.S. (2010). Extraordinarily widespread and fantastically complex: comparative biology of endosymbiotic bacterial and fungal mutualists of insects. Ecology Letters, 13: 223-234. DOI: https://doi.org/10.1111/j.1461-0248.2009.01416.x

Gilliam, M., Roubik, D.W. & Lorenz, B.J. (1990). Microorganisms associated with pollen, honey, and brood provisions in the nest of a stingless bee, Melipona fasciata. Apidologie, 21: 89-97. DOI: https://doi.org/10.1051/apido:19900201

Gilliam, M. (1997). Identification and roles of non-pathogenic microflora associated with honey bees1. FEMS Microbiology Letters, 155: 1-10. DOI: https://doi.org/10.1016/S0378-1097(97)00337-6

Gois, G.C., Carneiro, G.G., Rodrigues, A.E., Silva, E.O. & Campos, F.S. (2010). Qualidade microbiológica do mel de abelhas Melipona scutellaris. Pubvet, 4. http://ojs.pubvet.com.br/index.php/revista/article/view/2637

Golonka, A.M. & Vilgalys, R. (2013). Nectar Inhabiting Yeasts in Virginian Populations of Silene latifolia (Caryophyllaceae) and Coflowering Species. The American Midland Naturalist, 169: 235-258. DOI: https://doi.org/10.1674/0003-0031-169.2.235

Gonçalves, P., Gonçalves, C., Brito, P.H. & Sampaio, J.P. (2020). The Wickerhamiella/Starmerella clade – A treasure trove for the study of the evolution of yeast metabolism. Yeast, 37: 313-320. DOI: https://doi.org/10.1002/yea.3463

Good, A.P., Gauthier, M.-P. L., Vannette, R. L. & Fukami, T. (2014). Honey Bees Avoid Nectar Colonized by Three Bacterial Species, But Not by a Yeast Species, Isolated from the Bee Gut. PLoS ONE, 9: e86494. DOI: https://doi.org/10.1371/journal.pone.0086494

Graves, S., Piepho, H-P., Selzer, L. & Dorai-Raj, S. (2023). Package “multcompView” Title Visualizations of Paired Comparisons. https://cran.r-project.org/web/packages/multcompView/multcompView.pdf (accessed date: 20 October 2023)

Heberle, H., Meirelles, G.V., da Silva, F.R., Telles, G.P. & Minghim, R. (2015). InteractiVenn: a web-based tool for the analysis of sets through Venn diagrams. BMC Bioinformatics, 16. DOI: https://doi.org/10.1186/s12859-015-0611-3

Hommel, R.K., Weber, L., Weiss, A., Himmelreich, U., Rilke, O. & Kleber, H.P. (1994). Production of sophorose lipid by Candida (Torulopsis) apicola grown on glucose. Journal of Biotechnology, 33: 147-155. DOI: https://doi.org/10.1016/0168-1656(94)90107-4

Hyde, K.D., Tennakoon, D.S., Jeewon, R., Bhat, D.J., Maharachchikumbura, S.S.N., Rossi, W., Leonardi, M., Lee, H.B., Mun, H.Y., Houbraken, J., Nguyen, T.T.T., Jeon, S.J., Frisvad, J.C., Wanasinghe, D.N., Lücking, R., Aptroot, A., Cáceres, M.E.S., Karunarathna, S.C., Hongsanan, S. & Phookamsak, R. (2019). Fungal diversity notes 1036–1150: taxonomic and phylogenetic contributions on genera and species of fungal taxa. Fungal Diversity, 96: 1-242.

Kaewwichian, R., Yongmanitchai, W., Kawasaki, H. & Limtong, S. (2012). Metschnikowia saccharicola sp. nov. and Metschnikowia lopburiensis sp. nov., two novel yeast species isolated from phylloplane in Thailand. Antonie van Leeuwenhoek, 102: 743-751. DOI: https://doi.org/10.1007/s10482-012-9774-3

Kurtzman, C.P., Fell, J.W. & T Boekhout. (2011a). The Yeasts (Fifth Edition). Amsterdam: Elsevier, p 2354.

Kurtzman, C.P., Fell, J.W. & Boekhout T. (2011b.) Gene sequence analyses and other DNA-based methods for yeast species recognition. In: C.P. Kurtzman, J.W. Fell & T. Boekhout (Eds), The Yeasts (Fifth Edition) (pp. 137-144). Amsterdam: Elsevier. DOI: https://doi.org/10.1016/B978-0-444-52149-1.00010-0

Lacaz-Ruiz, R. (2000). Manual Prático de Microbiologia básica. São Paulo: EDUSP.

Lachance, M.A., Bowles, J.M. & Starmer, W. T. (2003). Metschnikowia santaceciliae, Candida hawaiiana, and Candida kipukae, three new yeast species associated with insects of tropical morning glory. FEMS Yeast Research, 3: 97-103. DOI: https://doi.org/10.1111/j.1567-1364.2003.tb00144.x

Lachance, M.A. (2011). Starmerella Rosa & Lachance (1998). In: C.P. Kurtzman, J.W. Fell & T. Boekhout (Eds), The Yeasts (Fifth Edition) (pp. 811-815). Amsterdam: Elsevier. DOI: https://doi.org/10.1016/B978-0-444-52149-1.00071-9

Lenth, R. V. (2016). Least-Squares Means: The R Package lsmeans. Journal of Statistical Software, 69. DOI: https://doi.org/10.18637/jss.v069.i01

Lorenzon, M.C. & Morgado, L. (2008). Mel com biodiversidade. Ciência Hoje. 42: 65- 67.

Marques, M.C., Trindade, W., Bohn, A. & Grelle, C.E. (2021). The Atlantic Forest: an introduction to the megadiverse forest of South America. In: M.C.M. Marques, C.E.V. Grelle (Eds). The Atlantic Forest. Switzerland (pp. 3-23). Berlim: Springer Cham. DOI: https://doi.org/10.1007/978-3-030-55322-7_1

Meireles, S.F., Santos, S.F., Rafael, M.S., Mota, A.J. & Silva, C.G.N. (2022). Yeasts from the nests of two Amazonian stingless bees: screening and PCR-RFLP molecular analysis. Symbiosis, 87: 153-163. DOI: https://doi.org/10.1007/s13199-022-00865-w

Mendiburu, F. de. (2021). Agricolae: Statistical Procedures for Agricultural Research. R-Packages. https://cran.r-project.org/package=agricolae (accessed date: 10 October 2023).

Menezes, C., Vollet-Neto, A., Marsaioli, A.J., Zampieri, D., Fontoura, I.C., Luchessi, A.D. & Imperatriz-Fonseca, V.L. (2015). A Brazilian Social Bee Must Cultivate Fungus to Survive. Current Biology, 25: 2851-2855. DOI: https://doi.org/10.1016/j.cub.2015.09.028

Myers, N., Mittermeier, R.A., Mittermeier, C.G., da Fonseca, G.A.B. & Kent, J. (2000). Biodiversity hotspots for conservation priorities. Nature, 403: 853-858. DOI: https://doi.org/10.1038/35002501

Nakase, T., Jindamorakot, S., Am-In, S., Lee, C.F., Imanishi, Y. & Limtong S (2011). Three novel species of the anamorphic yeast genus Candida in the Candida intermedia clade found in Japan, Thailand and Taiwan. Journal of General and Applied Microbiology, 57: 73-81. DOI: https://doi.org/10.2323/jgam.57.73

Nguyen, N. H., Suh, S.O. & Blackwell, M. (2007). Five novel Candida species in insect-associated yeast clades isolated from Neuroptera and other insects. Mycologia, 99: 842-858. DOI: https://doi.org/10.3852/mycologia.99.6.842

Nguyen, N.H., Suh, S.O., Erbil, C.K. & Blackwell, M. (2006). Metschnikowia noctiluminum sp. nov., Metschnikowia corniflorae sp. nov., and Candida chrysomelidarum sp. nov., isolated from green lacewings and beetles. Mycological Research, 110: 346-356. DOI: https://doi.org/10.1016/j.mycres.2005.11.010

Nicoletti, R. & Becchimanzi, A. (2022). Ecological and Molecular Interactions between Insects and Fungi. Microorganisms, 10: 96. DOI: https://doi.org/10.3390/microorganisms10010096

O’Donnell, K. (1993). Fusarium and its near relatives. In: D.R. Reynolds, J.W. Taylor (Eds), The fungal holomorph: mitotic, meiotic and pleomorphic speciation in fungal systematics (pp. 225-233). Wallingford: CAB International.

Oksanen, J., Blanchet, F.G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Peter, R., Minchin, P.R., O’Hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H.H., Szoecs, W. & Wagner, H. (2020). Vegan: Community Ecology Package (R package Version 2.5-5). https://CRAN.R-project.org/package¼vegan (accessed date: 01 October 2023).

Olaitan, P.B., Adeleke, O.E. & Ola, I.O. (2007). Honey: a reservoir for microorganisms and an inhibitory agent for microbes. African Health Sciences, 7: 159-165.

Pagnocca, F.C., Rodrigues, A., Nagamoto, N.S. & Bacci, M. (2008). Yeasts and filamentous fungi carried by the gynes of leaf-cutting ants. Antonie van Leeuwenhoek, 94: 517-526. DOI: https://doi.org/10.1007/s10482-008-9268-5

Pimentel, M.R., Antonini, Y., Martins, R.P., Lachance, M.A. & Rosa, C.A. (2005). Candida riodocensis and Candida cellae, two new yeast species from the Starmerella clade associated with solitary bees in the Atlantic rain forest of Brazil. FEMS Yeast Research, 5: 875-879. DOI: https://doi.org/10.1016/j.femsyr.2005.03.006

R Core Team. (2021). R: The R Project for Statistical Computing. R-Project.org. https://www.r-project.org (accessed date: 20 August 2023).

Rao, V.G. & Hoog, G.S. (1975). Some notes on Torula. Persoonia, 8: 199-206.

Rosa, C.A., Lachance, M.A., Silva, J.O., Teixeira, A.C.P., Marini, M.M., Antonini, Y. & Martins, R.P. (2003). Yeast communities associated with stingless bees. FEMS Yeast Research, 4: 271-275. DOI: https://doi.org/10.1016/S1567-1356(03)00173-9

Rosa, C.A. & Lachance, M.A. (1998). The yeast genus Starmerella gen. nov. and Starmerella bombicola sp. nov., the teleomorph of Candida bombicola (Spencer, Gorin & Tullock) Meyer & Yarrow. International Journal of Systematic Bacteriology, 48: 1413-1417. DOI: https://doi.org/10.1099/00207713-48-4-1413

Santos, A.C.C., Borges, L.D.F., Rocha, N.D.C., Azevedo, V.A.C., Bonetti, A.M., Santos, A. R., Fernandes, G.R., Dantas, R.C.C. & Ueira-Vieira, C. (2023). Bacteria, yeasts, and fungi associated with larval food of Brazilian native stingless bees. Scientific Reports, 13: 5147. DOI: https://doi.org/10.1038/s41598-023-32298-w

Santos, A.R.O., Lee, D.K., Ferreira A.G., Carmo M., Rondelli, V.M., Barros, K.O., Hsiang, T., Rosa, C. A. & Lachance, M. (2020). The yeast community of Conotelus sp. (Coleoptera: Nitidulidae) in Brazilian passionfruit flowers (Passiflora edulis) and description of Metschnikowia amazonensis sp. nov., a large-spored clade yeast. Yeast, 37: 253-260. DOI: https://doi.org/10.1002/yea.3453

Santos, A.R.O., Leon, M.P., Barros, K.O., Freitas, L.F.D., Hughes, A.F.S., Morais, P.B., Lachance, M.A. & Rosa, C.A. (2018). Starmerella camargoi f.a., sp. nov., Starmerella ilheusensis f.a., sp. nov., Starmerella litoralis f.a., sp. nov., Starmerella opuntiae f.a., sp. nov., Starmerella roubikii f.a., sp. nov. and Starmerella vitae f.a., sp. nov., isolated from flowers and bees, and transfer of related Candida species to the genus Starmerella as new combinations. International Journal of Systematic and Evolutionary Microbiology, 68: 1333-1343. DOI: https://doi.org/10.1099/ijsem.0.002675

SEMAS-Secretaria de Meio Ambiente e Sustentabilidade de Pernambuco. Plano de Manejo – Parque Estadual de Dois Irmãos (2014). www.cprh.pe.gov.br. Retrieved from: http://www.cprh.pe.gov.br/ARQUIVOS_ANEXO/1%20PLANO%20DE%20MANEJO%20com%20lei%2011%20622.pdf

Shannon, C.E. & Weaver, W. (1971). The mathematical theory of communication. 14th ed. Chicago: University of Illinois Press, 140 p.

Souza, B.A., Marchini, L.C., Dias, C.T.S., Oda-Souza, M., Carvalho, C.A.L. & Alves, R.M.O. (2009). Avaliação microbiológica de amostras de mel de trigoníneos (Apidae: Trigonini) do Estado da Bahia. Ciência e Tecnologia de Alimentos, 29: 798-802. DOI: https://doi.org/10.1590/S0101-20612009000400015

Souza, J.R.S., Sarquis, M.I.M., Pantoja, M.C., Neto, P.Q.C., Pereira, J.O., Galvão, R.M.S. & Silva, M.I.L. (2018). Occurrence of filamentous fungi associated with stingless bees Melipona in meliponaries at the metropolitan region of Manaus, Amazonas. Revista da Biologia, 18: 1-5. DOI: https://doi.org/10.7594/revbio.18.01.01

Starmer, W.T. & Lachance, M-A. (2011). Yeast Ecology. In: C.P. Kurtzman, J.W. Fell & T. Boekhout (Eds), The Yeasts (Fifth Edition) (pp. 137-144). Amsterdam: Elsevier.

Thanh, V.N., Hien, D.D. & Thom, T.T. (2013). Moniliella byzovii sp. nov., a chlamydospore-forming black yeast isolated from flowers. International Journal of Systematic and Evolutionary Microbiology, 63: 1192-1196. DOI: https://doi.org/10.1099/ijs.0.049767-0

Torto, B., Boucias, D.G., Arbogast, R.T., Tumlinson, J.H. & Peter. (2007). Multitrophic interaction facilitates parasite-host relationship between an invasive beetle and the honey bee. Proceedings of the National Academy of Sciences, 104: 8374-8378. DOI: https://doi.org/10.1073/pnas.0702813104

van der Walt, J.P. & van der Klift, W.C. (1972). Pichia melissophila sp.n., a new osmototolerant yeast from apiarian sources. Antonie van Leeuwenhoek, 38: 361-364. DOI: https://doi.org/10.1007/BF02328106

van der Walt, J.P. (1959). Pichia robertsii nov. spec. A new haploid homothallic yeast. Antonie van Leeuwenhoek, 25: 337-343. DOI: https://doi.org/10.1007/BF02542859

Vega, C., Guzmán, B., Lachance, M., Sandy-Lynn Steenhuisen, Johnson, S.D., Herrera, C.M. (2012). Metschnikowia proteae sp. nov., a nectarivorous insect-associated yeast species from Africa. International Journal of Systematic and Evolutionary Microbiology, 62: 2538-2545. DOI: https://doi.org/10.1099/ijs.0.040790-0

Vollet-Neto, A., Maia-Silva, C., Menezes, C. & Imperatriz-Fonseca, V.L. (2016). Newly emerged workers of the stingless bee Scaptotrigona aff. depilis prefer stored pollen to fresh pollen. Apidologie, 48: 204-210. DOI: https://doi.org/10.1007/s13592-016-0464-4

Wickham, H. (2016). Data Analysis. Use R!. Springer International Publishing, 189-201. DOI: https://doi.org/10.1007/978-3-319-24277-4_9

Witzgall, P., Proffit, M., Rozpedowska, E., Becher, P.G., Andreadis, S., Coracini, M., Lindblom, T.U.T., Ream, L.J., Hagman, A., Bengtsson, M., Kurtzman, C.P., Piskur, J. & Knight, A. (2012). “This is not an Apple” – Yeast Mutualism in Codling Moth. Journal of Chemical Ecology, 38: 949-957. DOI: https://doi.org/10.1007/s10886-012-0158-y

Yun, J.-H., Jung, M.-J., Kim, P.S. & Bae, J.-W. (2018). Social status shapes the bacterial and fungal gut communities of the honey bee. Scientific Reports, 8. DOI: https://doi.org/10.1038/s41598-018-19860-7

Zacchi, L. & Vaughan-Martini, A.J.A.O.M. (2002). Yeasts associated with insects in agricultural areas of Perugia, Italy. Annals of Microbiology, 52: 237-244.