Morphology and molecules on opposite sides of the diversity gradient: Four cryptic species of the Cliona celata (Porifera, Demospongiae) complex in South America revealed by mitochondrial and nuclear markers

Molecular Phylogenetics and Evolution

Volumn 62, Issue 1, 2012, Pages 529-541

  de Paula, Thiago Silva ^a   Zilberberg, Carla ^b   Hajdu, Eduardo ^b   Lôbo Hajdu, Gisele ^a  

^a STATE UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Excavating sponges; Marine sponges; Molecular markers; Morphologic variation

Indexed keywords

RIBOSOMAL SPACER DNA; RNA 28S;

ANIMAL; ARTICLE; BAYES THEOREM; BIOLOGICAL MODEL; CLASSIFICATION; DNA SEQUENCE; GENETIC MARKER; GENETIC VARIABILITY; GENETICS; HISTOLOGY; IRELAND; MITOCHONDRIAL GENE; MONTE CARLO METHOD; PHYLOGENY; PHYLOGEOGRAPHY; PROBABILITY; REGRESSION ANALYSIS; SOUTH AMERICA; SPONGE (PORIFERA); STATISTICAL MODEL;

ANIMALS; BAYES THEOREM; DNA, RIBOSOMAL SPACER; GENES, MITOCHONDRIAL; GENETIC MARKERS; GENETIC VARIATION; IRELAND; LIKELIHOOD FUNCTIONS; MARKOV CHAINS; MODELS, GENETIC; MONTE CARLO METHOD; PHYLOGENY; PHYLOGEOGRAPHY; PORIFERA; REGRESSION ANALYSIS; RNA, RIBOSOMAL, 28S; SEQUENCE ANALYSIS, DNA; SOUTH AMERICA;

CLIONA CELATA; CLIONAIDAE; DEMOSPONGIAE; PORIFERA;

EID: 83655191118     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2011.11.001     Document Type: Article

References (105)

1. Barucca M., Azzini F., Bavestrello G., Biscotti M.A., Calcinai B., Canapa A., Cerrano C., Olmo E. The systematic position of some boring sponges (Demospongiae, Hadromerida) studied by molecular analysis. Mar. Biol. 2007, 151:529-535.
2. Bavestrello G., Calcinai B., Cerrano C., Pansini M., Sarà M. The taxonomic status of some Mediterranean clionids (Porifera: Demospongiae) according to morphological and genetic characters. Bull. Inst. Roy. Sci. Nat. Belgique, Biol. 1996, 66(Suppl.):185-195.
3. Bell J.J., Barnes D.K.A., Turner J.R. The importance of micro and macro morphological variation in the adaptation of a sublittoral demosponge to current extremes. Mar. Biol. 2002, 140:75-81.
4. Bergquist P.R. The marine fauna of New Zealand: Porifera, Demospongiae, part 1. (Tetractinomorpha and Lithistida). Inst. Mem. 1968, 37:1-105.
5. Bickford D., Lohman D.J., Sodhi N.S., Ng P.K.L., Meier R., Winker K., Ingram K.K., Das I. Cryptic species as a window on diversity and conservation. Trends Ecol. Evol. 2006, 22:148-155.
6. Blanquer A., Uriz M.-J. Cryptic speciation in marine sponges evidenced by mitochondrial and nuclear genes, A phylogenetic approach. Mol. Phylogenet. Evol. 2007, 45:392-397.
7. Bookstein F.L. Can biometrical shape be a homologous character?. Homology: The Hierarchical Basis of Comparative Biology 1994, 197-227. Academic Press. B.K. Hall (Ed.).
8. Boury-Esnault N. Résultats Scientifiques des Campagnes de la 'Calypso'. Campagne de la 'Calypso' au large des côtes atlantiques de l'Amérique du Sud (1961-1962). I. 29. Spongiaires. Ann. I. Oceanogr. Paris 1973, 49:263-295.
9. Boury-Esnault N., Hajdu E., Klautau M., Custodio M., Borojevic R. The value of cytological criteria in distinguishing sponges at the species level, the example of the genus Polymastia. Can. J. Zool. 1994, 72:795-804.
10. Boury-Esnault N., Klautau M., Bézac C., Wulff J., Solé-Cava A.M. Comparative study of putative conspecific sponge populations from both sides of the Isthmus of Panama. J. Mar. Biol. Ass. UK 1999, 79:39-50.
11. Bucklin A., Hedgecock D. Biochemical genetic evidence for a third species of Metridium (Coelenterata, Atiniaria). Mar. Biol. 1982, 66:1-7.
12. Bucklin A., Steinke D., Blanco-Bercial1 L. DNA barcoding of marine metazoa. Annu. Rev. Mar. Sci. 2011, 3:471-508.
13. Burton M. Las esponjas marinas del Museo Argentino de Ciencias Naturales. Parte I. Ann. Mus. Argent. Cienc. Nat. 1940, 40:95-121.
14. Calcinai B., Arillo A., Cerrano C., Bavestrello G. Taxonomy-related differences in the excavating micro-patterns of boring sponges. J. Mar. Biol. Ass. UK 2003, 83:37-39.
15. Calcinai B., Azzini F., Bavestrello G., Cerrano C., Pansini M., Thung D.-C. Boring sponges from Ha Long Bay, Tonkin Gulf, Vietnam. Zool. Stud. 2006, 45:201-212.
16. Calendini, F., Martin J.-F., 2005. PaupUP v1.0.3.1 A Free Graphical Frontend for Paup* Dos software.
17. Carballo J.L., Hajdu E. Micromorphology in Mycale taxonomy (Mycalidae, Poecilosclerida, Demospongiae), with the description of two new micracanthoxea-bearing species. Contr. Zool. 1998, 67:187-195.
18. Carballo J.L., Sanchez-Moyano J.E., Garcia-Gomez J.C. Taxonomic and ecological remarks on boring sponges (Clionidae) from the Straits of Gibraltar (southern Spain): tentative bioindicators?. Zool. J. Linn. Soc. 1994, 112:407-424.
19. Carballo J.L., Cruz-Barraza J.A., Gómez P. Taxonomy and description of clionaid sponges (Hadromerida, Clionaidae) from the Pacific of Mexico. Zool. J. Linn. Soc. 2004, 141:353-397.
20. Carreras-Carbonell J., Macpherson E., Pascual M. Rapid radiation and cryptic speciation in mediterranean triplewn blennies (Pisces, Tripterygiidae) combining multiple genes. Mol. Phylogenet. Evol. 2005, 37:751-761.
21. Carvalho M.S., Hajdu E. Comments on brazilian Halichondria Fleming (Halichondriidae, Halichondrida, Demospongiae), with the description of four new species from the São Sebastião Channel and its environs (Tropical Southwestern Atlantic). Rev. Brasil. Zool. 2001, 18:161-180.
22. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 2000, 17:540-552.
23. Christiansen P. Neotype of Neofelis diardi (Mammalia, Carnivora, Felidae). Zootaxa 2009, 2110:58-68.
24. Cuartas E.I. Demospongiae (Porifera) de Mar del Plata (Argentina), con la descripción de Cliona lisa sp.n. y Plicatellopsis reptans sp.n. Nerítica 1991, 6:43-63.
25. Dawson M.N., Gupta A.S., England M.H. Coupled biophysical global ocean model and molecular genetic analyses identify multiple introductions of cryptogenic species. Proc. Natl. Acad. Sci. USA 2005, 102:11968-11973.
26. de Paula, T.S., 2009. O complexo Cliona celata Grant, 1826 (Porifera, Demospongiae) na América do Sul: uma abordagem molecular e morfológica. Master Thesis. Universidade do Estado do Rio de Janeiro, Rio de Janeiro.
27. Desqueyroux R., Moyano H. Zoogeografía de demospongias chilenas. Bol. Soc. Biol. Concepción 1987, 58:39-66.
28. Desqueyroux-Faúndez R., van Soest R.W.M. Shallow waters demosponges of the Galápagos islands. Rev. Suisse Zool. 1997, 104:379-467.
29. Ferrario F., Calcinai B., Erpenbeck D., Galli P., Wörheide G. Two Pione species (Hadromerida, Clionaidae) from the Red Sea: a taxonomical challenge. Org. Divers. Evol. 2010, 10:275-285.
30. Folmer O., Black M., Hoeh W., Lutz R., Vrijenhoek R. DNA primers for amplification of mitochondrial cytochrome C oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 1994, 3:294-299.
31. Fromont J., Craig R., Rawlinson L., Alder J. Excavating sponges that are destructive to farmed pearl oysters in Western and Northern Australia. Aquacult. Res. 2005, 36:150-162.
32. Gaston K.J. Rarity 1994, Chapman and Hall, London.
33. Grant R.E. Notice of a new zoophyte (Cliona celata Gr.) from the Frith of Forth. Edinburgh N. Philos. J. 1826, 8:78-81.
34. Hartman W.D. Natural history of the marine sponges of southern New England. Bull. Peabody Mus. Nat. Hist. 1958, 12:1-155.
35. Hellberg M.E. Gene flow and isolation among populations of marine animals. Annu. Rev. Ecol. Evol. Syst. 2009, 40:291-310.
36. Hill M.S., Hill A.L. Morphological plasticity in the tropical sponge Anthosigmella varians, responses to predators and wave energy. Biol. Bull. 2002, 202:86-95.
37. Holmes K.E. Effects of eutrophication on bioeroding sponge communities with the description of new West Indian sponges, Cliona spp. (Porifera: Hadromerida: Clionidae). Invert. Biol. 2000, 119:125-138.
38. Systema Porifera, A Guide to The Classification of Sponges 2002, Kluwer, New York. J.N.A. Hooper, R.W.M. van Soest (Eds.).
39. Hooper J.N.A., Wiedenmayer F. Porifera. Zoological Catalogue of Australia 1994, vol. 12:1-624. Melbourne, CSIRO Australia.
40. Jobb, G., 2008. TREEFINDER version of October 2008. 2008. Munich, Germany. Distributed by the author at http://www.treefinder.de.
41. Klautau M., Valentine C. Revision of the genus Clathrina (Porifera, Calcarea). Zool. J. Linn. Soc. 2003, 139:1-62.
42. Klautau M., Russo C.A.M., Lazoski C., Boury-Esnault N., Thorpe J.P., Solé-Cava A.M. Does cosmopolitanism result from overconservative systematics? A case study using the marine sponge Chondrilla nucula. Evolution 1999, 53:1414-1422.
43. Klecka W.R. Discriminant Analysis (Sage University Paper Series on Quantitative Applications in the Social Sciences, No. 07-019) 1980, Beverly Hills, CA.
44. Knowlton N. Sibling species in the sea. Annu. Rev. Ecol. Syst. 1993, 24:189-216.
45. Kober K.M., Nichols S.A. On the phylogenetic relationships of hadromerid and poecilosclerid sponges. J. Mar. Biol. Assoc. UK 2007, 87:1585-1598.
46. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. ClustalW2 and ClustalX version 2. Bioinformatics 2007, 23:2947-2948.
47. Lazoski C., Solé-Cava A.M., Boury-Esnault N., Klautau M., Russo C.A.M. Cryptic speciation in a high gene flow scenario in the oviparous marine sponge Chondrosia reniformis. Mar. Biol. 2001, 139:421-429.
48. Liedloff A.C. Mantel Nonparametric Test Calculator. Version 2.0 1999, School of Natural Resource Sciences, Queensland University of Technology, Australia.
49. Little F.J. An experimental or tentative revision of the genus Cliona utilizing the principles of numerical taxonomy. Proc. Pa. Acad. Sci. 1968, 42:38-48.
50. Lôbo-Hajdu G., Guimarães A.C.R., Salgado A., Lamarão F.R.M., Vieiralves T., Mansure J.J., Albano R.M. Intragenomic, intra- and interespecific variation in the rDNA ITS of porifera revealed by PCR-single-strand conformation polymorphism (PCR-SSCP). Boll. Mus. Ist. Biol. Univ. Genova 2004, 68:413-423.
51. López-Gappa J., Landoni N.A. Biodiversity of Porifera in the Southwest Atlantic between 35°S and 56°S. Rev. Mus. Argent. Cienc. Nat. 2005, 7:191-219.
52. Lynch M., Pfrender M., Spitze K., Lehman N., Hicks J., Allen D., Latta L., Ottene M., Bogue F., Colbourne J. The quantitative and molecular genetic architecture of a subdivided species. Evolution 1999, 53:100-110.
53. Maldonado M. The ecology of the sponge larva. Can. J. Zool. 2006, 84:175-194.
54. Mathews L.M., Adams L., Anderson E., Basile M., Gottardi E., Buckholt M.A. Genetic and morphological evidence for substantial hidden biodiversity in a freshwater crayfish species complex. Mol. Phylogenet. Evol. 2008, 48:126-135.
55. Mayr E. Animal Species and Evolution 1963, Harvard University Press, Cambridge, MA.
56. Mello A.M., Vizzini A., Longato S., Rollo F., Bonfante P., Trappe J.M. Tuber borchii versus Tuber maculatum, neotype studies and DNA analyses. Mycologia 2000, 92:326-331.
57. Mishler B.D., Theriot E.C. The phylogenetic species concept (sensu Mishler and Theriot), monophyly, apomorphy, and phylogenetic species concepts. Species concepts and phylogenetic theory, A debate 2000, 44-54. Columbia Univ. Press, New York. Q. Wheeler, R. Meier (Eds.).
58. Muricy G., Hajdu E. Porifera Brasilis, guia de identificação das esponjas marinhas mais comuns do Sudeste do Brasil 2006, Museu Nacional/UFRJ, Rio de Janeiro.
59. Muricy G., Boury-Esnault N., Bézac C., Vacelet J. Cytological evidence for cryptic speciation in Mediterranean Oscarella (Porifera, Homoscleromorpha). Can. J. Zool. 1996, 74:881-896.
60. Muricy G., Solé-Cava A.M., Thorpe J.P., Boury-Esnault N. Genetic evidence for extensive cryptic speciation in the sponge Plakina trilopha (Porifera, Demospongiae, Homoscleromorpha) from the Western Mediterranean. Mar. Ecol. Prog. Ser. 1996, 138:181-187.
61. Muricy G., Santos C.P., Batista D., Lopes D.A., Pagnoncelli D., Monteiro L.C., et al. Capítulo 3. Porifera. Biodiversidade bentônica da região central da Zona Econômica Exclusiva brasileira. Série Livros 18 2006, 109-145. Museu Nacional, Rio de Janeiro. H.P. Lavrado, B.L. Ignácio (Eds.).
62. Nakano T., Spencer H.G. Simultaneous polyphenism and cryptic species in an intertidal limpet from New Zealand. Mol. Phylogenet. Evol. 2007, 45:470-479.
63. Nichols S.A., Barnes P.A.G. A molecular phylogeny and historical biogeography of the marine sponge genus Placospongia (Phylum Porifera) indicate low dispersal capabilities and widespread crypsis. J. Exp. Mar. Biol. Ecol. 2005, 323:1-15.
64. Old M.C. The taxonomy and distribution of the boring sponges (Clionidae) along the Atlantic coast of North America. Publ. Chesapeake Biol. Lab. 1941, 44:1-30.
65. Palermo J.A., Brasco M.F.R., Seldes A.M. Storniamides A-D, alkaloids from a Patagonian Sponge Cliona sp. Tetrahedron Lett. 1996, 52:2727-2734.
66. Palermo J.A., Brasco M.F.R., Cabezas E., Balzaretti V., Seldes A.M. Celenamide E, a Tripeptide Alkaloid from the Patagonian Sponge Cliona chilensis. J. Nat. Prod. 1998, 61:488-490.
67. Pang R.K. The systematics of some Jamaican excavating sponges (Porifera). Postilla Peabody Mus. Yale Univ. 1973, 161:1-75.
68. Pansini M., Sarà M. Taxonomical and biogeographical notes on the sponges of the Straits of Magellan. Sci. Mar. 1999, 63:203-208.
69. Pérez-Portela R., Turon X. Cryptic divergence and strong population structure in the colonial invertebrate Pycnoclavella communis (Ascidiacea) inferred from molecular data. Zoology 2008, 111:163-178.
70. Pinheiro U.S., Hajdu E., Custódio M.R. Aplysina Nardo (Porifera, Verongida, Aplysinidae) from the Brazilian coast with description of eight new species. Zootaxa 2007, 1609:1-51.
71. Piscitelli M., Corriero G., Gaino E., Uriz M-J. Reproductive cycles of the sympatric excavating sponges Cliona celata and Cliona viridis in the Mediterranean Sea. Invert. Biol. 2011, 130:1-10.
72. Prado M.P., Torres Y.R., Berlinck R.G.S., Desiderá C., Sanchez M.A., Craveiro M.V., Hajdu E., da Rocha R.M., Machado-Santelli G.M. Effects of marine organisms extracts on microtubule integrity and cell cycle in cultured cells. J. Exp. Mar. Biol. Ecol. 2004, 313:125-137.
73. Raupach M.J., Wagele J.-W. Distinguishing cryptic species in Antarctic Asellota (Crustacea, Isopoda) - a preliminary study of mitochondrial DNA in Acanthaspidia drygalskii. Antarct. Sci. 2006, 18:191-198.
74. Ronquist F., Huelsenbeck J.P. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
75. Rosell D., Uriz M.J. Excavating and endolithic sponge species (Porifera) from the Mediterranean, species descriptions and identification key. Org. Divers. Evol. 2002, 2:55-86.
76. Rützler K. Clionid sponges from the Coast of Tunisia. Bull. Inst. Ocean. Pêche 1973, 2:623-636.
77. Rützler K. The burrowing sponges of Bermuda. Smithsonian Contr. Zool. 1974, 165:1-32.
78. Rützler K. Family Clionaidae D'Orbigny, 1851. A Guide to the Classification of Sponges 2002, 173-185. Kluwer Academic/Plenum Publishers, New York. J.N. Hooper, R.W.M. van Soest (Eds.).
79. Rützler K., Stone S.M. Discovery and significance of Albany Hancock's microscope preparations of excavating sponges (Porifera: Hadromerida: Clionidae). Proc. Biol. Soc. Washington 1986, 99:658-675.
80. Santos S., Schneider H., Sampaio I. Genetic differentiation of Macrodon ancylodon (Sciaenidae, Perciformes) populations in Atlantic coastal waters of South America as revealed by mtDNA analysis. Genet. Mol. Biol. 2003, 26:151-161.
81. Sará M. Demospongie di acque superficiali della Tera del Fuoco (Spedizioni AMZ Mares - GRSTS e SAI). Boll. Mus. Ist. Biol. Univ. Genova 1978, 46:7-117.
82. Schönberg C.H.L. An improved method of tissue digestion for spicule mounts in sponge taxonomy. Mem. Queensl. Mus. 1999, 44:533-539.
83. Schönberg C.H.L. Bioeroding sponges common to the central Australian Great Barrier Reef, descriptions of three new species, two new records, and additions to two previously described species. Senckenb. Marit. 2000, 30:161-221.
84. Schonberg, C.H.L., 2000b. Sponges of the 'Cliona viridis complex' - a key for species identification. In: Moosa, M.K., Soemodihardjo, S., Soegiarto, A., Romimohtarto, K., Nontji, A., Soekarno, Suharsono (Eds.), Proc. 9th Int. Coral Reef Symp. 1, pp. 295-300.
85. Schönberg C.H.L., Grass S., Heiermann A.T. Cliona minuscula sp. nov. (Hadromerida, Clionaidae) and other bioeroding sponges that only contain tylostyles. Zootaxa 2006, 1312:1-24.
86. Solé-Cava A.M., Boury-Esnault N. Levels of inter and intraspecific differentiation in marine sponges. Mem. Queensl. Mus. 1999, 44:591-602.
87. Solé-Cava A.M., Thorpe J.P. Genetic differentiation between morphotypes of the marine sponge Suberites ficus (Demospongiae, Hadromerida). Mar. Biol. 1986, 93:247-253.
88. Solé-Cava A.M., Boury-Esnault N., Vacelet J., Thorpe J.P. Biochemical genetic divergence and systematics in sponges of the genera Corticium and Oscarella (Demospongiae, Homoscleromorpha) in the Mediterranean Sea. Mar. Biol. 1992, 113:299-304.
89. Stahls G., Savolainen E. MtDNA COI barcodes reveal cryptic diversity in the Baetis vernus group (Ephemeroptera, Baetidae). Mol. Phylogenet. Evol. 2008, 46:82-87.
90. * and other methods), version 4.0B10 2002, Sinauer Associates, Sunderland.
91. Tamura K., Dudley J., Nei M., Kumar S. MEGA4, molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24:1596-1599.
92. Thiele, J., 1905. Die Kiesel- und Hornschwämme der Sammlung Plate. Zoologische Jahrbücher 407-496 (Supplement 6, Fauna Chiliensis III, pls 27-33).
93. Thomas, P.A., 1972. Boring sponges of the reefs of Gulf of Mannar and Palk Bay. In: Mar. Proc. Symp. Corals and Coral Reefs, 1969. Biol. Assoc. India, pp. 333-362.
94. Topsent E. étude monographique des spongiaires de France. 3. Monaxonida (Hadromerina). Arch. Zool. Exp. Géneva 1900, 3:1-331.
95. Vacelet J., Perez T. Two new genera and species of sponges (Porifera, Demospongiae) without skeleton from a Mediterranean cave. Zoosystema 1998, 20:5-22.
96. van Soest, R.W.M., 1980. Marine sponges from Curaçao and other Caribbean localities. Part II. Haplosclerida. In: Hummelinck, P.W., Van der Steen, L.J. (Eds.), Uitgaven van de Natuurwetenschappelijke Studiekring voor Suriname en de Nederlandse Antillen. No. 104. Studies on the Fauna of Curaçao and other Caribbean Islands, vol. 62, pp. 1-173.
97. van Soest, R.W.M., 1984. Marine sponges from Curaçao and other Caribbean localities. Part III. Poecilosclerida. In: Hummelinck, P.W., Van der Steen, L.J. (Eds.), Uitgaven van de Natuurwetenschappelijke Studiekring voor Suriname en de Nederlandse Antillen, No. 112. Studies on the Fauna of Curaçao and other Caribbean Islands 66, pp. 1-167.
98. van Soest, R.W.M, Boury-Esnault, N., Hooper, J.N.A., Rützler, K, de Voogd, N.J., Alvarez, B., Hajdu, E., Pisera, A.B., Vacelet, J., Manconi, R., Schoenberg, C., Janussen, D., Tabachnick, K.R., Klautau, M., 2008. World Porifera database. http://www.marinespecies.org/porifera.
99. Vollmer S.V., Palumbi S.R. Testing the utility of internally transcribed spacer sequences in coral phylogenetics. Mol. Ecol. 2004, 13:2763-2772.
100. Ward R.D. Biochemical genetic variation in the genus Littorina (Prosobranchia, Mollusca). Hydrobiologia 1990, 193:53-69.
101. Species Concepts and Phylogenetic Theory: A Debate 2000, Columbia Univ. Press, New York. Q. Wheeler, R. Meier (Eds.).
102. Wiley E.O. The evolutionary species concept reconsidered. Syst. Zool. 1978, 27:17-26.
103. Willenz P., Hajdu E., Azevedo F., Klautau M., Desqueyroux-Faúndez R., Lôbo-Hajdu G., Carvalho M.S. Porifera - sponges. Marine Benthic Fauna of Chilean Patagonia 2009, 93-170. Nature in Focus, Santiago de Chile. V. Häussermann, G. Förstera (Eds.).
104. Xavier J.R., Rachello-Dolmen P.G., Parra-Velandia F., Schönberg C.H.L., Breeuwer J.A.J., van Soest R.W.M. Molecular evidence of cryptic speciation in the "cosmopolitan" excavating sponge Cliona celata (Porifera, Clionaidae). Mol. Phylogenet. Evol. 2010, 56:13-20.
105. Zilberberg, C., 2006. Reprodução clonal e sistemática molecular de esponjas (Porifera, Demospongiae). Ph.D. Thesis. Universidade Federal do Rio de Janeiro, Rio de Janeiro.