Microturbellarians (Platyhelminthes and Acoelomorpha) in Brazil: invisible organisms?

Microturbelários (Platyhelminthes e Acoelomorpha) no Brasil: organismos invisíveis?

J. A. L. Braccini S. V. Amaral A. M. Leal-Zanchet About the authors

Abstract

Microturbellarians typically belong to the benthos and may occur in a wide variety of environments. They are abundant in freshwater and marine ecosystems and may occur in moist terrestrial habitats. However, turbellarians are seldom taken into account in studies of biodiversity. Most studies on Brazilian microturbellarians had taxonomical purposes and were done in the years 1940-1950. Thus, information on their occurrence and ecological aspects are dispersed throughout several papers. We intend here to summarize the biogeographical distribution and ecological aspects of microturbellarians recorded for Brazil, indicating the main gaps in their knowledge and possible actions to enhance studies on this group. There are 239 species of microturbellarians registered for Brazil, with records distributed in 12 states. However, just three states located in southern Brazil have records of 94% of microturbellarian species. Thus, knowledge on the systematics and geographical distribution of Brazilian microturbellarians clearly reflect the scientific activity over many years or decades in two states of southeastern and southern Brazil. Considering the scant information on this group in Brazil, which is also the situation of the Neotropical microturbellarians in general, some actions should be proposed. First, it would be necessary to sample in the diverse biomes, as well as in the various river and sea basins, based on standardized sampling protocols. Second, it would be necessary to encourage diverse research groups to include microturbellarians and/or turbellarians in general into biodiversity inventories and studies on community structure of invertebrates. Third, it is necessary to increase the number of research groups on microturbellarians, in order to augment the studies on their morphology, systematics, and ecology. Considering their abundance, species richness and ecological importance in aquatic environments, despite some peculiarities regarding their sampling, sorting and identification procedures, the challenge to study microturbellarians and enhance knowledge about them in Brazilian ecosystems should be faced.

Keywords:
Platyhelminthes; species diversity; Neotropical region; systematics; ecology

Resumo

Microturbelários são tipicamente bentônicos e podem ocorrer em uma ampla variedade de ambientes. São abundantes em ecossistemas marinhos e de água doce, podendo ocorrer em ambientes terrestres úmidos. Entretanto, turbelários raramente são considerados em estudos de diversidade. A maioria dos estudos sobre microturbelários brasileiros tiveram propósito taxonômico e foram realizados nos anos 1940-1950. Assim, informações sobre ocorrência e aspectos ecológicos estão dispersos em diversos artigos. O objetivo deste trabalho é sumarizar a distribuição biogeográfica e aspectos ecológicos dos microturbelários registrados para o Brasil, indicando as principais lacunas do conhecimento e possíveis ações para ampliar estudos sobre esse grupo. Há 239 espécies de microturbelários registradas no Brasil, com registros distribuídos em 12 estados. No entanto, 94% das espécies de microturbelários foram registradas em apenas três estados localizados no sul e sudeste do Brasil. Assim, o conhecimento sobre a sistemática e distribuição geográfica dos microturbelários claramente reflete as atividades científicas realizadas por muitos anos ou mesmo décadas em dois estados do sudeste e sul do Brasil. Considerando as escassas informações existentes sobre esse grupo no Brasil, assim como a situação dos microturbelários neotropicais em geral, algumas ações devem ser propostas. Primeiramente, é necessário realizar amostragens em diversos biomas, assim como nas várias bacias e regiões hidrográficas marinhas, baseadas em protocolos de amostragem padronizados. Em segundo lugar, faz-se necessário incentivar diversos grupos de pesquisa a incluir microturbelários e/ou turbelários em geral em inventários da biodiversidade e estudos de estrutura de comunidades de invertebrados. Em terceiro lugar, é necessário ampliar o número de grupos de pesquisa em microturbelários, para aumentar os estudos sobre sua morfologia, sistemática e ecologia. Considerando sua abundância, riqueza de espécies e importância ecológica em ambientes aquáticos, apesar de suas peculiaridades de amostragem, triagem e identificação, o desafio de estudar e ampliar o conhecimento sobre microturbelários em ecossistemas brasileiros deve ser enfrentado.

Palavras-chave:
Platyhelminthes; diversidade de espécies; região Neotropical; sistemática; ecologia

1 Introduction

Turbellarians are acoelomate, soft-bodied worms that have a sac-like gut and typically ciliated epidermal cells. Most turbellarians are hermaphrodites with cross fertilization following copulation, showing a complex reproductive system (Cannon, 1986Cannon, L.R.G., 1986. Turbellaria of the World: a guide to families and genera. Brisbane: Queensland Museum. 136 p.; Rieger et al., 1991Rieger, R.M., Tyler, S., SMITH, J.P.S. and RIEGER, G.E., 1991. Platyhelminthes: Turbellaria. In: F.W. HARRISON, ed. Microscopic anatomy of invertebrates. New York: Wiley-Liss, vol. 3, pp. 7-140.). Traditionally, flatworms used to belong to the phylum Platyhelminthes, which can be subdivided into three clades, viz. Acoelomorpha, Catenulida e Rhabditophora (Rieger et al., 1991Rieger, R.M., Tyler, S., SMITH, J.P.S. and RIEGER, G.E., 1991. Platyhelminthes: Turbellaria. In: F.W. HARRISON, ed. Microscopic anatomy of invertebrates. New York: Wiley-Liss, vol. 3, pp. 7-140.), since Rhabditophora also includes the parasitic forms. The Acoelomorpha, however, has been removed from the Platyhelminthes into its own phylum (Baguñà and Riutort, 2004Baguñà, J. and Riutort, M., 2004. The dawn of bilaterian animals: the case of the acoelomorph flatworms. BioEssays, vol. 26, pp. 1046-1057.; Tyler et al., 2014Tyler, S., Schilling, S., Hooge, M. and Bush, L.F., 2014 [viewed 10 October 2014]. Turbellarian taxonomic database. Version 1.7 [online]. Orono: University of Maine. Available from: http://turbellaria.umaine.edu
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; Littlewood, 2006Littlewood, D.T.J., 2006. The evolution of parasitism in flatworms. In: A.G. MAULE and N.J. MARKS, eds. Parasitic flatworms: molecular biology, biochemistry, immunology and physiology. Wallingford: CAB International, pp. 1-36.; Larsson and Jondelius, 2008Larsson, K. and Jondelius, U., 2008. Phylogeny of Catenulida and support for Platyhelminthes. Organisms, Diversity & Evolution, vol. 8, no. 5, pp. 378-387. http://dx.doi.org/10.1016/j.ode.2008.09.002.
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; Boll et al., 2013Boll, P.K., Rossi, I., Amaral, S.V., Oliveira, S.M., Müller, E.S., Lemos, V.S. and Leal-Zanchet, A.M., 2013. Platyhelminthes ou apenas semelhantes a Platyhelminthes? Relações filogenéticas dos principais grupos de turbelários. Neotropical Biology and Conservation, vol. 8, no. 1, pp. 41-52. http://dx.doi.org/10.4013/nbc.2013.81.06.
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). The term turbellarians continues to be used and will be applied here without taxonomic connotation.

There are about 6,500 species of turbellarians worldwide (Schockaert et al., 2008Schockaert, E.R., Hooge, M., Sluys, R., Schilling, S., Tyler, S. and Artois, T., 2008. Global diversity of free living flatworms (Platyhelminthes, “Turbellaria”) in freshwater. Hydrobiologia, vol. 595, no. 1, pp. 41-48. http://dx.doi.org/10.1007/s10750-007-9002-8.
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). They are distributed into the following taxa: Acoela, Nemertodermatida, Catenulida, Macrostomida, Polycladida, Prolecithophora, Lecithoepitheliata, Revertospermata, Proseriata, Tricladida, Dalytyphloplanida and Kalyptorhynchia (Schockaert et al., 2008Schockaert, E.R., Hooge, M., Sluys, R., Schilling, S., Tyler, S. and Artois, T., 2008. Global diversity of free living flatworms (Platyhelminthes, “Turbellaria”) in freshwater. Hydrobiologia, vol. 595, no. 1, pp. 41-48. http://dx.doi.org/10.1007/s10750-007-9002-8.
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; Van Steenkiste et al., 2013Van Steenkiste, N., Tessens, B., Willems, W., Backeljau, T., Jondelius, U. and Artois, T., 2013. A comprehensive molecular phylogeny of Dalytyphloplanida (Platyhelminthes: Rhabdocoela) reveals multiple escapes from the marine environment and origins of symbiotic relationships. PLoS One, vol. 8, no. 3, pp. e59917. http://dx.doi.org/10.1371/journal.pone.0059917. PMid:23536894.
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). The later two constitute the rhabdocoels. Turbellarians can be divided into two major groups, with no taxonomical association: the macroturbellarians or large worms, which include triclads and polyclads, and the microturbellarians including the other turbellarian groups, the members of which are smaller.

Turbellarians may occur in a wide variety of environments. They are abundant in freshwater and marine ecosystems and may occur in moist terrestrial habitats. They are, however, mainly marine animals, with only 1/5 of the known species occurring in freshwater (Hyman, 1951Hyman, L.H., 1951. The invertebrates: Platyhelminthes and Rhynchocoela. New York: McGraw-Hill. The Acoelomate Bilateria.; Schockaert et al., 2008Schockaert, E.R., Hooge, M., Sluys, R., Schilling, S., Tyler, S. and Artois, T., 2008. Global diversity of free living flatworms (Platyhelminthes, “Turbellaria”) in freshwater. Hydrobiologia, vol. 595, no. 1, pp. 41-48. http://dx.doi.org/10.1007/s10750-007-9002-8.
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). Turbellarians typically belong to the benthos. Triclads and polyclads occur generally on hard bottom, under stones, or associated with macrophytes, algae or gravel (Hyman, 1951Hyman, L.H., 1951. The invertebrates: Platyhelminthes and Rhynchocoela. New York: McGraw-Hill. The Acoelomate Bilateria.; Du-Bois Reymond Marcus and Marcus, 1968Du Bois-Reymond Marcus, E. and Marcus, E., 1968. Polycladida from Curação and faunistically related regions. Hague: M. Nijhoff. 106 p. Studies on the Fauna of Curaçao and other Caribbean Islands, no. 26.). Microturbellarians usually occur on sandy or muddy bottom. Most marine turbellarians are limited to the littoral zone of the ocean (Hyman, 1951Hyman, L.H., 1951. The invertebrates: Platyhelminthes and Rhynchocoela. New York: McGraw-Hill. The Acoelomate Bilateria.). Freshwater forms may occur in temporary or permanent wetlands, such as lakes, natural or artificial ponds, pools, ditches, streams and rivers (Kolasa, 1991Kolasa, J., 1991. Flatworms: Turbellaria. In: J.M. THORP and A.P. COVICH, eds. Ecology and classification of North American freshwater invertebrates. New York: Academic Press, vol. 2, pp. 145-171.; Noreña-Janssen, 1995Noreña-Janssen, C., 1995. Studies on the taxonomy and ecology of the turbellarian (Plathelminthes) in the floodplain of the Paraná river (Argentina). II. Taxonomy and ecology of the Turbellaria .Archiv für Hydrobiologie, Stuttgart, vol. 107, suppl., pp. 11-262.; Young, 2001Young, J.O., 2001. Keys to the freshwater microturbellarians of Britain and Ireland with notes on their ecology. Ambleside: The Freshwater Biological Association. 142 p. Freshwater Biological Association Scientific Publication, no. 59.), as well as in agroecosystems (Bambaradeniya et al., 2004Bambaradeniya, C.N.B., Edirisinghe, J.P., De Silva, D.N., Gunatilleke, C.V.S., Ranawana, K.B. and Wijekoon, S., 2004. Biodiversity associated with an irrigated rice agroecosystem in Sri Lanka. Biodiversity and Conservation, vol. 13, no. 9, pp. 1715-1753. http://dx.doi.org/10.1023/B:BIOC.0000029331.92656.de.
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; Vara and Leal-Zanchet, 2013Vara, D.C. and Leal-Zanchet, A.M., 2013. Turbelários límnicos (Platyhelminthes) em ecossistemas de arroz irrigado da Planície Costeira do sul do Brasil. Biota Neotropica, vol. 13, no. 4, pp. 1-11. http://dx.doi.org/10.1590/S1676-06032013000400021.
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). Some marine flatworms, such as acoels and polyclads, and freshwater rhabdocoels are planctonic (Hyman, 1951Hyman, L.H., 1951. The invertebrates: Platyhelminthes and Rhynchocoela. New York: McGraw-Hill. The Acoelomate Bilateria.; Rocha et al., 1990Rocha, O., Matsumura-Tundisi, T., Tundisi, J.G. and Fonseca, C.P., 1990. Predation on and by pelagic Turbellaria in some lakes in Brazil. Hydrobiologia, vol. 198, no. 1, pp. 91-101. http://dx.doi.org/10.1007/BF00048625.
http://dx.doi.org/10.1007/BF00048625...
; Dumont et al., 2014Dumont, H.J., Rietzler, A.C. and Han, B.P., 2014. A review of typhloplanid flatworm ecology, with emphasis on pelagic species. Inland Waters, vol. 4, no. 3, pp. 257-270. http://dx.doi.org/10.5268/IW-4.3.558.
http://dx.doi.org/10.5268/IW-4.3.558...
). Some microturbellarians may occur in humid terrestrial environments (Hyman, 1951Hyman, L.H., 1951. The invertebrates: Platyhelminthes and Rhynchocoela. New York: McGraw-Hill. The Acoelomate Bilateria.; Tessens et al., 2014Tessens, B., Janssen, T. and Artois, T., 2014. Molecular phylogeny of Kalyptorhynchia (Rhabdocoela, Platyhelminthes) inferred from ribosomal sequence data. Zoologica Scripta, vol. 43, no. 5, pp. 519-530. http://dx.doi.org/10.1111/zsc.12066.
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); land triclads may be a species-rich group in tropical and subtropical ecosystems (Carbayo et al., 2009Carbayo, F., Froehlich, E.M., Leal-Zanchet, A.M. and Amato, S.B., 2009. Turbelários (Platyhelminthes). In: R. ROCHA and W. BOEGER, eds. Estado da arte e perspectivas para a zoologia no Brasil. Curitiba: UFPR, pp. 49-64.). The temnocephalids, a group of the taxon Dalytyphloplanida, and some members of other taxonomic groups of microturbellarians live in association with other invertebrates or with turtles, usually as ectosymbionts (Hyman, 1951Hyman, L.H., 1951. The invertebrates: Platyhelminthes and Rhynchocoela. New York: McGraw-Hill. The Acoelomate Bilateria.; Jennings, 1997Jennings, J.B., 1997. Nutritional and respiratory pathways to parasitism exemplified in the Turbellaria. International Journal for Parasitology, vol. 27, no. 6, pp. 679-691. http://dx.doi.org/10.1016/S0020-7519(97)00010-6. PMid:9229251.
http://dx.doi.org/10.1016/S0020-7519(97)...
). In addition, some acoels and rhabdocoels are parasites of molluscs, echinoderms and other invertebrates (Hyman, 1951Hyman, L.H., 1951. The invertebrates: Platyhelminthes and Rhynchocoela. New York: McGraw-Hill. The Acoelomate Bilateria.; Bush, 1981Bush, L.F., 1981. Marine flora and fauna of the northeastern United States. Turbellaria: Acoela and Nemertodermatida. Seattle: U.S. Dept. of Commerce, National Oceanic and Atmospheric Administration, National Marine Fisheries Service. 71 p. NOAA Technical Report National Marine Fisheries Service Circular, no. 440.).

Microturbellarians in general were studied mainly in Brazil in the years 1940-1950 (Marcus, 1943Marcus, E., 1943. O Turbelaria Focke 1836 no Brasil. Mesostoma ehrenbergiiBoletim de Indústria Animal, vol. 6, pp. 12-15., 1944Marcus, E., 1944. Sobre duas Prorhynchidae (Turbellaria), novas para o B rasil.Arquivos do Museu Paranaense, Curitiba, vol. 4, no. 1, pp. 3-46., 1945aMarcus, E., 1945a. Sobre Catenulida Brasileiros. Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo: Série Zoologia, vol. 10, pp. 3-133., bMarcus, E., 1945b. Sobre microturbellários do Brasil. Montevideo: Museo de Historia Natural. 74 p. Comunicaciones Zoologicas, vol. 1, no. 25., 1946Marcus, E., 1946. Sobre Turbellaria brasileiros. Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo: Série Zoologia, vol. 11, p. 1-254., 1948Marcus, E., 1948. Turbellaria do Brasil. Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo: Série Zoologia, vol. 13, p. 111-243., 1949Marcus, E. 1949. Turbellaria Brasileiros (7). Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo: Série Zoologia, vol. 14, pp. 7-156., 1950Marcus, E. 1950. Turbellaria Brasileiros (8). Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo: Série Zoologia, vol. 15, pp. 5-192., 1951Marcus, E., 1951. Turbellaria Brasileiros (9). Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo: Série Zoologia, vol. 16, pp. 1-217., 1952Marcus, E., 1952. Turbellaria Brasileiros (10). Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo: Série Zoologia, vol. 17, pp. 5-187., 1954Marcus, E., 1954. Turbellaria Brasileiros (11). Papéis Avulsos do Departamento de Zoologia e Secretaria de Agricultura de São Paulo, vol. 11, no. 24, pp. 419-489.; Du-Bois Reymond Marcus, 1951Du Bois-Reymond Marcus, E., 1951. Contributions to the natural history of Brazilian Turbellaria. Comunicaciones Zoologicas del Museo de Historia Natural de Montevideo, vol. 3, no. 63, pp. 1-25.; Marcus and Macnae, 1954Marcus, E. and Macnae, W., 1954. Architomie in a species of. ConvolutaNature, vol. 173, no. 4394, pp. 130. http://dx.doi.org/10.1038/173130a0. PMid:13132888.
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), based on samplings in the northern littoral of the state of São Paulo and lentic environments of São Paulo city and its neighbourhood. Later, Rocha et al. (1990)Rocha, O., Matsumura-Tundisi, T., Tundisi, J.G. and Fonseca, C.P., 1990. Predation on and by pelagic Turbellaria in some lakes in Brazil. Hydrobiologia, vol. 198, no. 1, pp. 91-101. http://dx.doi.org/10.1007/BF00048625.
http://dx.doi.org/10.1007/BF00048625...
and Hooge and Rocha (2006)Hooge, M.D. and Rocha, C.E.F., 2006. Acoela (Acoelomorpha) from the northern beaches of the state of São Paulo, Brazil, and a systematic revision of the family Otocelididae. Zootaxa, vol. 1335, pp. 1-50. studied, respectively, freshwater rhabdocoels and acoels from the state of São Paulo. In addition, a new species of marine rhabocoel was recently described (Reygel et al., 2014Reygel, P., Schockaert, E., Janssen, T. and Artois, T., 2014. Two new species of Carcharodorhynchus Meixner, 1938 (Platyhelminthes: Rhabdocoela: Schizorhynchidae) from Brazil and Lanzarote. Marine Biodiversity, vol. 4, pp. 278-285.). Freshwater turbellarians from southern Brazil were investigated by Gamo and Leal-Zanchet (2004)Gamo, J. and Leal-Zanchet, A.M., 2004. Freshwater microturbellarians (Platyhelminthes) from Rio Grande do Sul, Brazil. Revista Brasileira de Zoologia, vol. 21, no. 4, pp. 897-903. http://dx.doi.org/10.1590/S0101-81752004000400026.
http://dx.doi.org/10.1590/S0101-81752004...
, Vara and Leal-Zanchet (2013)Vara, D.C. and Leal-Zanchet, A.M., 2013. Turbelários límnicos (Platyhelminthes) em ecossistemas de arroz irrigado da Planície Costeira do sul do Brasil. Biota Neotropica, vol. 13, no. 4, pp. 1-11. http://dx.doi.org/10.1590/S1676-06032013000400021.
http://dx.doi.org/10.1590/S1676-06032013...
and Braccini and Leal-Zanchet (2013)Braccini, J.A. and Leal-Zanchet, A.M., 2013. Turbellarian assemblages in freshwater lagoons in southern Brazil. Invertebrate Biology, vol. 132, no. 4, pp. 305-314. http://dx.doi.org/10.1111/ivb.12032.
http://dx.doi.org/10.1111/ivb.12032...
in natural wetlands and agroecosystems. Temnocephalids from various Brazilian regions were studied by Monticelli (1899)Monticelli, F.S., 1899. Sulla Mont. 1889 e sulle temnocephale en generale. Temnocephala brevicornisBollettino della Società dei Naturalisti in Napoli, vol. 12, pp. 72-127., Pereira and Cuocolo (1940Pereira, C. and Cuocolo, R., 1940. Contribução para o conhecimento da morfología, bionomia e ecologia de “ Monticelli, 1889”. Temnocephala brevicornisArquivos do Instituto de Biologia do Brasil, vol. 11, pp. 367-398., 1941Pereira, C. and Cuocolo, R., 1941. Estudos sobre “Temnocephalidae Monticelli, 1899”, com estabelecimento de dois novos gêneros australianos e descrição de duas novas espécies neotrópicas. Arquivos do Instituto de Biologia do Brasil, vol. 12, pp. 101-127.), Amato et al. (2003Amato, J.F.R., Amato, S.B. and Daudt, L.C., 2003. ecies of Temnocephala Blanchard (Platyhelminthes, Temnocephal New spida) ectosymbiont on Aegla serrana Buckup and Rossi (Crustacea, Anomura) from southern Brazil.Revista Brasileira de Zoologia, vol. 20, no. 3, pp. 493-500. http://dx.doi.org/10.1590/S0101-81752003000300021.
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, 2007Amato, J.F.R., Seixas, S.A. and Amato, S.B., 2007. A new species of Temnocephala Blanchard (Platyhelminthes, Temnocephalida) ectosymbiont on creeping water bugs, Cryphocricos granulosus De Carlo (Hemiptera, Naucoridae) from southern Brazil. Revista Brasileira de Zoologia, vol. 24, no. 4, pp. 1043-1051. http://dx.doi.org/10.1590/S0101-81752007000400022.
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, cSeixas, S.A., AMATO, J.F.R. and AMATO, S.B., 2010c. Redescription of Temnocephala iheringi (Platyhelminthes: Temnocephalida) based on specimens from Pomacea canaliculata (Mollusca: Ampullariidae) of the state of Rio Grande do Sul, Brasil: the possible type host and type locality. Zoologia, vol. 27, no. 2, pp. 245-257. http://dx.doi.org/10.1590/S1984-46702010000200012.
http://dx.doi.org/10.1590/S1984-46702010...
, 2011Seixas, S.A., AMATO, J.F.R. and AMATO, S.B., 2011. A new species of Blanchard (Platyhelminthes, Temnocephalida) ectosymbiont on Dilocarcinus septemdentatus (Decapoda, Trichodactylidae) from the Brazilian Amazonia. TemnocephalaNeotropical Helminthology, vol. 5, pp. 200-211., 2014Seixas, S.A., Amato, J.F.R., Amato, S.B. and Mascarenhas, C.S., 2014. First report of Temnocephala pereirai (PLatyhelminthes, Temnocephalidae) on (Embyididae) from Southern Brazil: a complete morphological study. Trachemys dorbigniNeotropical Helminthology, vol. 8, pp. 23.).

Freshwater and land triclads were studied mainly in the Brazilian states of São Paulo and Rio Grande do Sul (Carbayo and Froehlich, 2008Carbayo, F. and Froehlich, E.M., 2008. Estado do conhecimento dos macroturbelários (Platyhelminthes) do Brasil. Biota Neotropica, vol. 8, no. 4, pp. 177-197. http://dx.doi.org/10.1590/S1676-06032008000400018.
http://dx.doi.org/10.1590/S1676-06032008...
; Baptista et al. 2010Baptista, V.A., Oliveira, S.M. and Leal-Zanchet, A.M., 2010. Inventário de planárias terrestres (Platyhelminthes, Tricladida) em remanescente de Floresta Estacional Decidual do sul do Brasil. Biota Neotropica, vol. 10, no. 2, pp. 247-252. http://dx.doi.org/10.1590/S1676-06032010000200027.
http://dx.doi.org/10.1590/S1676-06032010...
; Leal-Zanchet et al., 2011Leal-Zanchet, A.M., Baptista, V.A., Campos, L.M. and Raffo, J.F., 2011. Spatial and temporal patterns of land flatworm assemblages in Brazilian Araucaria forests. Invertebrate Biology, vol. 130, no. 1, pp. 25-33. http://dx.doi.org/10.1111/j.1744-7410.2010.00215.x.
http://dx.doi.org/10.1111/j.1744-7410.20...
; Amaral et al., 2014Amaral, S.V., Hack, I.R., Iturralde, G.G. and LEAL-ZANCHET, A.M., 2014. Land flatworms (Platyhelminthes: Tricladida) in remnants of deciduous forest in the northeast region of southern Brazil. Biota Neotropica, vol. 14, no. 1, pp. 1-6. http://dx.doi.org/10.1590/S1676-06020140045.
http://dx.doi.org/10.1590/S1676-06020140...
). Polyclads were mainly known from the coast of the states of São Paulo and Rio de Janeiro, as well as the northeastern coast of Brazil (Carbayo and Froehlich, 2008Carbayo, F. and Froehlich, E.M., 2008. Estado do conhecimento dos macroturbelários (Platyhelminthes) do Brasil. Biota Neotropica, vol. 8, no. 4, pp. 177-197. http://dx.doi.org/10.1590/S1676-06032008000400018.
http://dx.doi.org/10.1590/S1676-06032008...
; Bahia and Padula, 2009Bahia, J. and Padula, V., 2009. First record of Pseudoceros bicolor and (Platyhelminthes: Polycladida) from Brazil. Pericelis cataMarine Biodiversity Records, vol. 2, pp. 1-5. http://dx.doi.org/10.1017/S1755267209000918.
http://dx.doi.org/10.1017/S1755267209000...
; Bahia et al., 2012Bahia, J., Padula, V. and Delgado, M., 2012. Five new records and morphological data of five polyclad species (Platyhelminthes: Turbellaria) from Rio Grande do Norte, Northeastern Brazil. Zootaxa, vol. 3170, pp. 31-44.; Bulnes and Torres, 2014Bulnes, V.N. and Torres, Y., 2014. Pseudoceros astrorum, a new species of Polycladida (Cotylea, Pseudocerotidae) from Northeastern Brazil. Zootaxa, vol. 3881, no. 1, pp. 94-100. http://dx.doi.org/10.11646/zootaxa.3881.1.7. PMid:25543622.
http://dx.doi.org/10.11646/zootaxa.3881....
).

In contrast to triclads and polyclads, which are collected directly, microturbellarians should be sampled with some substratum using a fine-meshed sweep-net (Young, 2001Young, J.O., 2001. Keys to the freshwater microturbellarians of Britain and Ireland with notes on their ecology. Ambleside: The Freshwater Biological Association. 142 p. Freshwater Biological Association Scientific Publication, no. 59.). Material collected by the net should be transferred to plastic vials containing water from the sampling site. The vials should be transported to the laboratory and carefully examined under a stereomicroscope (Braccini and Leal-Zanchet, 2013Braccini, J.A. and Leal-Zanchet, A.M., 2013. Turbellarian assemblages in freshwater lagoons in southern Brazil. Invertebrate Biology, vol. 132, no. 4, pp. 305-314. http://dx.doi.org/10.1111/ivb.12032.
http://dx.doi.org/10.1111/ivb.12032...
; Vara and Leal-Zanchet, 2013Vara, D.C. and Leal-Zanchet, A.M., 2013. Turbelários límnicos (Platyhelminthes) em ecossistemas de arroz irrigado da Planície Costeira do sul do Brasil. Biota Neotropica, vol. 13, no. 4, pp. 1-11. http://dx.doi.org/10.1590/S1676-06032013000400021.
http://dx.doi.org/10.1590/S1676-06032013...
). For sorting, samples may be treated by the method of reduction of oxygen (Schockaert, 1996Schockaert, E.R., 1996. Turbellarians. In: G.S. HALL, ed. Methods for the examination of organismal diversity in soils and sediments. Wallingford: CAB International, pp. 221-226.) or by examining all sampling water under the stereomicroscope (Brusa et al., 2003Brusa, F., Damborenea, C.M. and Noreña, C., 2003. A new species of (Platyhelminthes, Rhabdocoela) from Argentina and a kinship analysis of South American species of the genus. GieysztoriaZoologica Scripta, vol. 32, no. 5, pp. 449-457. http://dx.doi.org/10.1046/j.1463-6409.2003.00126.x.
http://dx.doi.org/10.1046/j.1463-6409.20...
). Live turbellarians should be transferred by a pipette to a petri dish and be examined alive for observation of general shape, size and colour pattern. After that, the internal morphology should be examined using a “squeeze preparation” technique (Gamo, 1987Gamo, J., 1987. Microturbelarios de la Península Ibérica. Miscelania Zoologica, vol. 11, pp. 41-49.; Young, 2001Young, J.O., 2001. Keys to the freshwater microturbellarians of Britain and Ireland with notes on their ecology. Ambleside: The Freshwater Biological Association. 142 p. Freshwater Biological Association Scientific Publication, no. 59.).

Considering that the macroturbellarians are the best known group among turbellarians and that their study in Brazil was summarized by Carbayo and Froehlich (2008)Carbayo, F. and Froehlich, E.M., 2008. Estado do conhecimento dos macroturbelários (Platyhelminthes) do Brasil. Biota Neotropica, vol. 8, no. 4, pp. 177-197. http://dx.doi.org/10.1590/S1676-06032008000400018.
http://dx.doi.org/10.1590/S1676-06032008...
, we will focus on Brazilian microturbellarians herein. We intend to summarize the biogeographical distribution and ecological aspects of microturbellarians recorded for Brazil, by pointing out main gaps in the knowledge about them and possible actions to enhance studies on this group.

2 Methods

Original research articles were searched in the databases Thomson Reuters (ISI) and Scielo, between August 2014 and February 2015, and in the bibliographical assets of our laboratory in the Universidade do Vale do Rio dos Sinos (UNISINOS). The following key-words were used: Platyhelminthes, Acoela, Nemertodermatida, Catenulida, Prolecithophora, Rhabdocoela, Temnocephalida, Macrostomida, Lecithoepitheliata or Revertospermata and Brazil.

We organized the data thus obtained in order to summarize the following information: species, order or other representative taxonomic group, sampling place (city and state), and type of environment where the occurrence was recorded. Regarding the environment, the following data were considered: type of substratum (sand, mud, algae etc.), type of ecosystem (marine, freshwater or brackish water) and hydric regime (lentic or lotic). In the case of temnocephalids, the associated organism was informed. The classification of marine ecoregions follows Spalding et al. (2007)Spalding, M.D., Fox, H.E., Allen, G.R., Davidson, N., Ferdaña, Z.A., Finlayson, M., Halpern, B.S., Jorge, M.A., Lombana, A.L., Lourie, S.A., Martin, K.D., Mcmanus, E., Molnar, J., Recchia, C.A. and Robertson, J., 2007. Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. Bioscience, vol. 57, no. 7, pp. 573-583. http://dx.doi.org/10.1641/B570707.
http://dx.doi.org/10.1641/B570707...
.

3 Geographical Distribution and Ecological Aspects

A total of 44 articles with records of microturbellarians in Brazil was found, 26 of which were available on the online databases Thomson Reuters (ISI) and Scielo. Eighteen other articles were found in the bibliographical assets of our laboratory (UNISINOS).

There are 239 species of microturbellarians registered for Brazil, with records distributed in 12 states. The highest number of species was recorded for the state of São Paulo, followed by Rio Grande do Sul and Paraná (Table 1). The central, northern and northeastern regions of Brazil have no or just a few records (Figure 1).

Table 1
Brazilian states with records of microturbellarians and number of species recorded per taxonomical group and state.
Figure 1
Records of microturbellarians in Brazil. Dots represent localities where microturbellarians were sampled.

Brazilian microturbellarians are distributed among 10 taxonomical groups. Dalytyphloplanida and Catenulida are the most species-rich, with about 28% and 18% of the recorded species, respectively, followed by Acoela (15%), Prolecithophora (11%), Proseriata (10%), Kalyptorhynchia (9%), and Macrostomida (7%). Lecithoepitheliata and Revertospermata are taxons with only few known species (Tables 1 and 2). The taxon Nemertodermatida has no records in Brazil.

Table 2
Species of Acoela recorded for Brazil, with localities of occurrence and type of environment and/or substratum where the microturbellarians were found.

Acoels, a group of marine flatworms, are represented by specimens sampled only in the state of São Paulo, mainly in sandy beaches, on algae or rock coasts (Tables 1 and 2). A few specimens were found on beach ponds.

Catenulids, which are mainly freshwater inhabitants, were registered in various continental environments, mainly in southeastern and southern Brazil (Table 1). They were frequently found in lentic environments, including rice fields and their canals, or in humid terrestrial environments. Six species were found in lotic environments and two species in water accumulated among leaves of Bromeliaceae (Table 3).

Table 3
Species of Catenulida recorded for Brazil, with localities of occurrence and type of environment and/or substratum where the microturbellarians were found.

Macrostomids inhabit marine and freshwater environments. They occur associated to the bottom or to the vegetation. In Brazil, 11 species were recorded in marine environments of the north coast of the state of São Paulo. Six other species were sampled in lentic continental ecosystems or in brackish water in various regions (Tables 1 and 4).

Table 4
Species of Macrostomida recorded for Brazil, with localities of occurrence and type of environment and/or substratum where the microturbellarians were found.

Rhabdocoels (Dalytyphloplanida and Kalyptorhynchia) inhabit mainly marine and freshwater environments, but some species are terrestrial. In Brazil, marine species were recorded in the north coast of the state of São Paulo, on algae, sand or mud. Freshwater species were found in lentic ecosystems, including rice fields and their canals, or lotic environments of southeastern and/or southern Brazil. Temnocephalids occur only in freshwater environments, with most species recorded in Brazil. They were found in the north, center, southeast and south of Brazil, as ectosymbiotes in turtles, decapods, insects and molluscs (Tables 1 and 5).

Table 5
Species of Rhabdocoela recorded for Brazil, with localities of occurrence and type of environment and/or substratum where the microturbellarians were found.

Lecithopitheliates may occur in freshwater, terrestrial and marine environments, but they are represented in Brazil by only two freshwater species, Prorhynchus stagnalis Schultze, 1851 and Geocentrophora applanata (Kennel, 1888). Prorhynchus stagnalis, considered world-wide distributed, was recorded in various localities in southeastern and southern Brazil, whereas G. applanata was sampled in two localities of central and southeastern Brazil (Tables 1 and 6).

Table 6
Species of Prolecithophora, Lecithoepitheliata and Revertospermata recorded for Brazil, with localities of occurrence and type of environment and/or substratum where the microturbellarians were found.

Prolecithophorans inhabit freshwater and marine environments, but they have no records in Brazilian freshwater ecosystems (Vara and Leal-Zanchet, 2013Vara, D.C. and Leal-Zanchet, A.M., 2013. Turbelários límnicos (Platyhelminthes) em ecossistemas de arroz irrigado da Planície Costeira do sul do Brasil. Biota Neotropica, vol. 13, no. 4, pp. 1-11. http://dx.doi.org/10.1590/S1676-06032013000400021.
http://dx.doi.org/10.1590/S1676-06032013...
; Braccini and Leal-Zanchet, 2013Braccini, J.A. and Leal-Zanchet, A.M., 2013. Turbellarian assemblages in freshwater lagoons in southern Brazil. Invertebrate Biology, vol. 132, no. 4, pp. 305-314. http://dx.doi.org/10.1111/ivb.12032.
http://dx.doi.org/10.1111/ivb.12032...
). The members of this taxon were sampled in marine environments on coastal areas of the state of São Paulo (Table 1). They were found on algae (Padina and Ulva) or on sandy and rocky coasts (Tables 1 and 6).

Revertospermats are exclusively marine flatworms. They are represented in Brazil by a single species, Urastoma cyprinae (Graff, 1882), found on the coast of the state of São Paulo (Tables 1 and 6). It is a parasite which inhabits the gills of bivalves.

Proseriates may occur in marine and freshwater environments, but almost all Brazilian species were sampled mainly in the north coast of the state of São Paulo (Table 1). They were found mainly in small ponds with high organic matter content. Only Bothrioplana semperi Braun, 1881 was sampled in freshwater environments of southeastern and southern Brazil (Table 7).

Table 7
Species of Proseriata recorded for Brazil, with localities of occurrence and type of environment and/or substratum where the microturbellarians were found.

4 Discussion and Conclusions

Just three Brazilian states, located in southeastern and southern Brazil, concentrate 94% of the microturbellarian species recorded for the country. Two of them, São Paulo and Rio Grande do Sul, house research groups on turbellarians, clearly reflecting the scientific activity over many years or decades.

Most marine microturbellarian diversity is known only in a small portion of the Warm Temperate Southwestern Atlantic, since the marine microturbellarian groups were almost exclusively studied in a small part of the northern littoral of the state of São Paulo (Marcus, 1948Marcus, E., 1948. Turbellaria do Brasil. Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo: Série Zoologia, vol. 13, p. 111-243., 1949Marcus, E. 1949. Turbellaria Brasileiros (7). Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo: Série Zoologia, vol. 14, pp. 7-156., 1950Marcus, E. 1950. Turbellaria Brasileiros (8). Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo: Série Zoologia, vol. 15, pp. 5-192., 1952Marcus, E., 1952. Turbellaria Brasileiros (10). Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo: Série Zoologia, vol. 17, pp. 5-187.; Hooge and Rocha, 2006Hooge, M.D. and Rocha, C.E.F., 2006. Acoela (Acoelomorpha) from the northern beaches of the state of São Paulo, Brazil, and a systematic revision of the family Otocelididae. Zootaxa, vol. 1335, pp. 1-50.). Just scattered records exist for the Tropical Southwestern Atlantic and Northern Brazil Shelf.

From twelve hydrographic regions, only the South Atlantic and Southern Atlantic regions have more than just occasional records of microturbellarians. Such records were mainly distributed among São Paulo, Rio Grande do Sul and Paraná (Marcus, 1943Marcus, E., 1943. O Turbelaria Focke 1836 no Brasil. Mesostoma ehrenbergiiBoletim de Indústria Animal, vol. 6, pp. 12-15., 1944Marcus, E., 1944. Sobre duas Prorhynchidae (Turbellaria), novas para o B rasil.Arquivos do Museu Paranaense, Curitiba, vol. 4, no. 1, pp. 3-46., 1945aMarcus, E., 1945a. Sobre Catenulida Brasileiros. Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo: Série Zoologia, vol. 10, pp. 3-133., 1951Marcus, E., 1951. Turbellaria Brasileiros (9). Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo: Série Zoologia, vol. 16, pp. 1-217., 1954Marcus, E., 1954. Turbellaria Brasileiros (11). Papéis Avulsos do Departamento de Zoologia e Secretaria de Agricultura de São Paulo, vol. 11, no. 24, pp. 419-489.; Gamo and Leal-Zanchet, 2004Gamo, J. and Leal-Zanchet, A.M., 2004. Freshwater microturbellarians (Platyhelminthes) from Rio Grande do Sul, Brazil. Revista Brasileira de Zoologia, vol. 21, no. 4, pp. 897-903. http://dx.doi.org/10.1590/S0101-81752004000400026.
http://dx.doi.org/10.1590/S0101-81752004...
; Vara and Leal-Zanchet, 2013Vara, D.C. and Leal-Zanchet, A.M., 2013. Turbelários límnicos (Platyhelminthes) em ecossistemas de arroz irrigado da Planície Costeira do sul do Brasil. Biota Neotropica, vol. 13, no. 4, pp. 1-11. http://dx.doi.org/10.1590/S1676-06032013000400021.
http://dx.doi.org/10.1590/S1676-06032013...
; Braccini and Leal-Zanchet, 2013Braccini, J.A. and Leal-Zanchet, A.M., 2013. Turbellarian assemblages in freshwater lagoons in southern Brazil. Invertebrate Biology, vol. 132, no. 4, pp. 305-314. http://dx.doi.org/10.1111/ivb.12032.
http://dx.doi.org/10.1111/ivb.12032...
). Considering the freshwater groups, the temnocephalids certainly constitute an exception, with species recorded for various regions in Brazil (Monticelli, 1899Monticelli, F.S., 1899. Sulla Mont. 1889 e sulle temnocephale en generale. Temnocephala brevicornisBollettino della Società dei Naturalisti in Napoli, vol. 12, pp. 72-127.; Pereira and Cuocolo, 1940Pereira, C. and Cuocolo, R., 1940. Contribução para o conhecimento da morfología, bionomia e ecologia de “ Monticelli, 1889”. Temnocephala brevicornisArquivos do Instituto de Biologia do Brasil, vol. 11, pp. 367-398., 1941Pereira, C. and Cuocolo, R., 1941. Estudos sobre “Temnocephalidae Monticelli, 1899”, com estabelecimento de dois novos gêneros australianos e descrição de duas novas espécies neotrópicas. Arquivos do Instituto de Biologia do Brasil, vol. 12, pp. 101-127.; Ferreira Yuki et al., 1993Ferreira-Yuki, V.L., Damborenea, M.C. and Osorio-Mallman, M.T., 1993. Acantochelys spixii (Duméril et Bibron,1835) (Chelidae) e Trachemys dorbigni (Duméril et Bibron, 1835) (Emydidae) (Testudines) como hospedeiros de Temnocephala brevicornis Monticelli 1889 (Temnocephalidae) (Platyhelminthes). Porto Alegre: PUCRS, pp. 75-83. Comunicações do Museu de Ciências, Série Zoológica, no. 6.; Damborenea, 1994Damborenea, M.C., 1994. Temnocefalos neotropicales: sp. n. y . Temnocephala kingsleyaeT. lutzi Monticelli, 1913 (Platyhelminthes, Temnocephalidea) comensales de crustáceos de BrasilIheringia: Série Zoologia, vol. 77, pp. 99-105.; Ernst and Lovich, 1996Ernst, C.H. and Lovich, J.E., 1996. (Maximilian’s Snacke-necked Turtle). Epizoic Comensal. Hydromedusa maximilianiHerpetological Review, vol. 27, no. 2, pp. 76-77.; Vianna and Melo, 2002Vianna, G J.C. and MELO, A.L., 2002. Aquatic Heteroptera as host of Blanchard (Platyhelminthes: Temnocephalidae) in Minas Gerais, Brazil. TemnocephalaLundiana, vol. 3, pp. 151-153.; Amato et al., 2003Amato, J.F.R., Amato, S.B. and Daudt, L.C., 2003. ecies of Temnocephala Blanchard (Platyhelminthes, Temnocephal New spida) ectosymbiont on Aegla serrana Buckup and Rossi (Crustacea, Anomura) from southern Brazil.Revista Brasileira de Zoologia, vol. 20, no. 3, pp. 493-500. http://dx.doi.org/10.1590/S0101-81752003000300021.
http://dx.doi.org/10.1590/S0101-81752003...
, 2005Amato, J.F.R., Amato, S.B. and Seixas, S.A., 2005. Temnocephala lutzi Monticelli (Platyhelminthes, Temnocephalida) ectosymbioies of Trychodactylus Latreille (Crustacea, Decapoda, Trichodactylidae) f nt on two specrom southern Brazil.Revista Brasileira de Zoologia, vol. 22, no. 4, pp. 1085-1094. http://dx.doi.org/10.1590/S0101-81752005000400038.
http://dx.doi.org/10.1590/S0101-81752005...
, 2006Amato, J.F.R., Amato, S.B. and Seixas, S.A., 2006. A new species of Temnocephala Blanchard (Platyhelminthes, Temnocephalida) ectosymbiont on Trichodactylus fluviatilis Latreille (Crustacea, Decapoda, Trichodactylidae) from southern Brazil. Revista Brasileira de Zoologia, vol. 23, no. 3, pp. 796-806. http://dx.doi.org/10.1590/S0101-81752006000300026.
http://dx.doi.org/10.1590/S0101-81752006...
, 2007Amato, J.F.R., Seixas, S.A. and Amato, S.B., 2007. A new species of Temnocephala Blanchard (Platyhelminthes, Temnocephalida) ectosymbiont on creeping water bugs, Cryphocricos granulosus De Carlo (Hemiptera, Naucoridae) from southern Brazil. Revista Brasileira de Zoologia, vol. 24, no. 4, pp. 1043-1051. http://dx.doi.org/10.1590/S0101-81752007000400022.
http://dx.doi.org/10.1590/S0101-81752007...
, 2010Amato, J.F.R., Amato, S.B., Seixas, S.A., Fonseca, M. and Ilário, R.J., 2010. Temnocephala pignalberiae Dioni, 1967 (Platyhelminthes, Temnocephalida) from two allopatric populations of Dilocarcinus pagei Stimpson, 1861 (Crustacea, Decapoda) first record for Brazil. Zootaxa, vol. 2613, pp. 15-28., 2011Amato, J.F.R., Amato, S.B., Seixas, S.A., VIDIGAL, T.H.A. and ANDRADE, C.P., 2011. Trichoptera: the newest insect order host of temnocephalans (Platyhelminthes, Temnocephalida) and the description of a new species of from Brazil. TemnocephalaZootaxa, vol. 2075, pp. 47-58.; Amato and Amato, 2005Amato, J.F.R. and AMATO, S.B., 2005. New species of Blanchard (Platyhelminthes, Temnocephalida) ectosymbiont on giant water bugs, spp. (Hemiptera, Belostomatidae) from southern Brazil. TemnocephalaBelostomaRevista Brasileira de Zoologia, vol. 22, no. 1, pp. 107-118. http://dx.doi.org/10.1590/S0101-81752005000100014.
http://dx.doi.org/10.1590/S0101-81752005...
; Seixas et al., 2010aSeixas, S.A., Amato, J.F.R. and Amato, S.B., 2010a. First report of Temnocephala rochensis (Platyhelminthes: Temnocephalida) from Pomace canaliculata (Mollusca: Ampullariidae) outside Uruguay - description updated based on specimens from the State of Rio Grande do Sul, Brazil. Zoologia, vol. 27, no. 5, pp. 820-828. http://dx.doi.org/10.1590/S1984-46702010000500019.
http://dx.doi.org/10.1590/S1984-46702010...
, bSeixas, S.A., AMATO, J.F.R. and AMATO, S.B., 2010b. Redescription of Temnocephala haswelli (Platyhelminthes: Temnocephalida) from Pomacea canaliculata (Mollusca: Ampullariidae) from Brazil: redescription update based on specimens from the state of Rio Grande do Sul, Brazil. Zoologia, vol. 27, no. 3, pp. 455-464. http://dx.doi.org/10.1590/S1984-46702010000300020.
http://dx.doi.org/10.1590/S1984-46702010...
, cSeixas, S.A., AMATO, J.F.R. and AMATO, S.B., 2010c. Redescription of Temnocephala iheringi (Platyhelminthes: Temnocephalida) based on specimens from Pomacea canaliculata (Mollusca: Ampullariidae) of the state of Rio Grande do Sul, Brasil: the possible type host and type locality. Zoologia, vol. 27, no. 2, pp. 245-257. http://dx.doi.org/10.1590/S1984-46702010000200012.
http://dx.doi.org/10.1590/S1984-46702010...
, 2011Seixas, S.A., AMATO, J.F.R. and AMATO, S.B., 2011. A new species of Blanchard (Platyhelminthes, Temnocephalida) ectosymbiont on Dilocarcinus septemdentatus (Decapoda, Trichodactylidae) from the Brazilian Amazonia. TemnocephalaNeotropical Helminthology, vol. 5, pp. 200-211., 2014Seixas, S.A., Amato, J.F.R., Amato, S.B. and Mascarenhas, C.S., 2014. First report of Temnocephala pereirai (PLatyhelminthes, Temnocephalidae) on (Embyididae) from Southern Brazil: a complete morphological study. Trachemys dorbigniNeotropical Helminthology, vol. 8, pp. 23.). Microturbellarians occurring in terrestrial environments were known only by occasional records in the state of São Paulo (Marcus, 1945bMarcus, E., 1945b. Sobre microturbellários do Brasil. Montevideo: Museo de Historia Natural. 74 p. Comunicaciones Zoologicas, vol. 1, no. 25.). Considering the six Brazilian biomes, only a small part of the Atlantic Forest, mainly the one located in Southern and Southeastern regions, have records of microturbellarians. Scattered or no records were done for the Amazonian, Caatinga, Savanna, Pampa and Pantanal biomes.

In addition to taxonomical studies, freshwater microturbellarian diversity was also investigated through recent inventories and studies on community structure done in the state of Rio Grande do Sul (Gamo and Leal-Zanchet, 2004Gamo, J. and Leal-Zanchet, A.M., 2004. Freshwater microturbellarians (Platyhelminthes) from Rio Grande do Sul, Brazil. Revista Brasileira de Zoologia, vol. 21, no. 4, pp. 897-903. http://dx.doi.org/10.1590/S0101-81752004000400026.
http://dx.doi.org/10.1590/S0101-81752004...
; Braccini and Leal-Zanchet, 2013Braccini, J.A. and Leal-Zanchet, A.M., 2013. Turbellarian assemblages in freshwater lagoons in southern Brazil. Invertebrate Biology, vol. 132, no. 4, pp. 305-314. http://dx.doi.org/10.1111/ivb.12032.
http://dx.doi.org/10.1111/ivb.12032...
; Vara and Leal-Zanchet, 2013Vara, D.C. and Leal-Zanchet, A.M., 2013. Turbelários límnicos (Platyhelminthes) em ecossistemas de arroz irrigado da Planície Costeira do sul do Brasil. Biota Neotropica, vol. 13, no. 4, pp. 1-11. http://dx.doi.org/10.1590/S1676-06032013000400021.
http://dx.doi.org/10.1590/S1676-06032013...
). In these studies, many unidentified species of catenulids, lecithopitheliates, macrostomids and rhabdocoels, among others, were recorded in agroecosystems and natural lentic environments of southern Brazil (Braccini and Leal-Zanchet, 2013Braccini, J.A. and Leal-Zanchet, A.M., 2013. Turbellarian assemblages in freshwater lagoons in southern Brazil. Invertebrate Biology, vol. 132, no. 4, pp. 305-314. http://dx.doi.org/10.1111/ivb.12032.
http://dx.doi.org/10.1111/ivb.12032...
; Vara and Leal-Zanchet, 2013Vara, D.C. and Leal-Zanchet, A.M., 2013. Turbelários límnicos (Platyhelminthes) em ecossistemas de arroz irrigado da Planície Costeira do sul do Brasil. Biota Neotropica, vol. 13, no. 4, pp. 1-11. http://dx.doi.org/10.1590/S1676-06032013000400021.
http://dx.doi.org/10.1590/S1676-06032013...
). Thus, it is almost unnecessary to emphasize that the known microturbellarian diversity in Brazil represents only a very small part of the existing biodiversity.

Considering the scant information on the taxonomy and biogeography on Brazilian microturbellarians, which is also the situation of the Neotropical microturbellarians in general, some actions should be proposed. First, it would be necessary to sample in the diverse biomes, as well as in the various river and sea basins, following standardized sampling protocols, as for example, the guidelines of the Rapid Assessment Program, in order to quickly generate data about the local and regional diversity (Alonso et al., 2011Alonso, L.E., Deichmann, J.L., McKenna, S.A., Naskrecki, P. and Richards, S.J., 2011. Biodiversity exploration for conservation: the first 20 years of the Rapid Assessment Program. Arlington: Conservation International. 316 p.). Second, it would be necessary to encourage diverse research groups to include microturbellarians and/or turbellarians in general in biodiversity inventories and studies on community structure of invertebrates. Third, it is necessary to increase the number of research groups on microturbellarians, in order to augment the studies on their morphology, systematic, and ecology.

There are, however, some problems for the inclusion of microturbellarians in ample biodiversity inventories. Microturbellarians should be sorted alive under the stereomicroscope and analyzed under the microscope to study their morphology with identification purposes (Young, 2001Young, J.O., 2001. Keys to the freshwater microturbellarians of Britain and Ireland with notes on their ecology. Ambleside: The Freshwater Biological Association. 142 p. Freshwater Biological Association Scientific Publication, no. 59.; Brusa et al., 2003Brusa, F., Damborenea, C.M. and Noreña, C., 2003. A new species of (Platyhelminthes, Rhabdocoela) from Argentina and a kinship analysis of South American species of the genus. GieysztoriaZoologica Scripta, vol. 32, no. 5, pp. 449-457. http://dx.doi.org/10.1046/j.1463-6409.2003.00126.x.
http://dx.doi.org/10.1046/j.1463-6409.20...
). Thus, some adjustments in the sampling procedures used for other invertebrates are needed, such as the collection of water for sorting the live microturbellarians at the laboratory. Another problem is concerned with the identification of microturbellarians, because for the same reason mentioned above, it would be difficult to send live specimens for the identification at species level by specialists.

Besides the abundance and species richness of microturbellarians in freshwater and marine ecosystems, these organisms may feed on a wide range of benthic and planctonic invertebrates, such as oligochaetes, rotifers, cladocerans, copepods and nematodes, among other organisms including bacteria, algae and protozoans (Young, 2001Young, J.O., 2001. Keys to the freshwater microturbellarians of Britain and Ireland with notes on their ecology. Ambleside: The Freshwater Biological Association. 142 p. Freshwater Biological Association Scientific Publication, no. 59.). Thus, considering their abundance, species richness and ecological importance in aquatic environments, the challenge to study these organisms and enhance their knowledge in Brazilian ecosystems should be faced.

Acknowledgements

We thank the Brazilian Research Council (CNPq), the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul (FAPERGS) for grants and fellowships in support of this study. Juliana Espíndola is acknowlegdeged for her help in summarizing bibliographical information about marine microturbellarians. We thank MSc. Edward Benya and Paulo Firmino for the English review of the manuscript. Dr. Francisco Brusa, Universidad Nacional de La Plata, Argentina, is thanked for a critical reading of an early version of the manuscript. An anonymous reviewer is acknowledged for their helpful suggestions.

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Publication Dates

  • Publication in this collection
    08 Mar 2016
  • Date of issue
    Apr-Jun 2016

History

  • Received
    10 Oct 2014
  • Accepted
    04 Mar 2015
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