Abstract:

The present study reviews the records of occurrences of fish species found in the Mamirauá Sustainable Development Reserve (MSDR). The reserve is located in a large section of the middle Solimões River basin, in its interflow with Japurá River. For the elaboration of the list of fish species occurring in Mamirauá Reserve, we used a database of different studies on fish communities carried out in the area over the last three decades, in addition to the material deposited in the ichthyological collections of three scientific institutions, the National Institute for Amazon Research - INPA, the Mamirauá Sustainable Development Institute - IDSM and the Science and Technology Museum of the Catholic University of Rio Grande do Sul - PUCRS. The ichthyofauna of the MSDR is composed of 541 species, encompassing 45 families and 15 orders. These correspond to 20% of all valid species known for the entire Amazonia so far. As observed in other studies in the Neotropical Region, the more represented orders were Siluriformes (209 species) and Characiformes (185 species), followed by the Gymnotiformes (78 species). The results presented here demonstrate a considerable increase (86%) in the knowledge about the fish diversity found in Mamirauá Reserve, in relation to its first list of fish species, published in the 90's. This increase reflects not only the growth in number of studies on fish diversity in the area, with new surveys, but also the continuous taxonomic work on the collections, and descriptions of twenty-eight new species, with one hundred and ten type series. Further surveys are expected to take place in the Northwestern, more isolated areas of the Reserve, and will allow the identification of new occurrences, and may even unveil new fish species yet to be described to Science..

Keywords:
Amazon; Checklist; Distribution; First record; Neotropical; Taxonomy

Resumo:

Este estudo apresenta uma revisão dos registros de ocorrências das espécies de peixes encontradas na Reserva de Desenvolvimento Sustentável Mamirauá (RDSM), ampla área localizada na bacia do Médio Solimões, em seu interflúvio com o Rio Japurá. Para a elaboração da lista de peixes que ocorrem na Reserva Mamirauá foram utilizados os bancos de dados de diferentes estudos sobre comunidades de peixes realizados na área ao longo das últimas décadas, além de informações referentes ao material tombado nas coleções ictiológicas de três instituições científicas, o Instituto Nacional de Pesquisas da Amazônia- INPA,o Instituto de Desenvolvimento Sustentável Mamirauá - IDSM e o Museu de Ciências e Tecnologia da Pontifícia Universidade Católica do Rio Grande do Sul - PUCRS. A ictiofauna da RDSM é composta por 541 espécies, incluindo 45 famílias e 15 ordens. Estes valores correspondem a cerca de 20% de todas espécies válidas conhecidas para toda a Amazônia até o momento. Assim como em outros estudos na região Neotropical as ordens que apresentaram as maiores riquezas foram siluriformes (209 espécies) e Characiformes (185 espécies), seguidas de Gymnotiformes (78 espécies). Os resultados apresentados neste trabalho demonstram um aumento considerável (86%) no conhecimento sobre a diversidade de peixes encontrados na Reserva Mamirauá, em relação à primeira lista de peixes da RDSM, publicada na década de 1990. Este aumento reflete não apenas o crescimento no número de estudos sobre a diversidade de peixes na área, com a ocorrência de novos levantamentos, como também a intensificação dos trabalhos taxonômicos de classificação e descrição de vinte oito novas espécies com cento e dez séries tipos. Novos levantamentos deverão ocorrer nas áreas mais isoladas da Reserva, na sua porção noroeste. Estas atividades permitirão a identificação de novas ocorrências, e podem até revelar espécies novas a serem descritas..

Palavras-chave:
Amazônia; Lista de verificação; Distribuição; Primeiro registro; Neotropical; Taxonomia

Introduction

At the end of the XX century, an attempt to inventory the fish fauna of the Mamirauá Reserve was made, and produced a first list of 291 species (Crampton 1999CRAMPTON, W. G. R. Os peixes da Reserva Mamirauá: diversidade e história natural na planície alagável da Amazônia. In: Estratégias para Manejo de Recursos Pesqueiros em Mamirauá. (QUEIROZ H.L. & CRAMPTON, W. eds.), Sociedade Civil Mamirauá/CNPq, Brasília, p. 10-36, 1999.). This first effort was limited by the lack of human and financial resources and did not encompassed a representative portion of the reserve. Seemingly, the problems that led to a limited list of fish species for the Mamirauá area are the same observed for the entire Amazon basin. The current knowledge on the Amazonian fish diversity is far from adequate, and the estimates on the number of existing fish species varies greatly (Malabarba et al., 1998MALABARBA, L. R.; REIS, R. E.; VARI, R. P.; LUCENA, Z. M.; LUCENA, C. A. (Eds). Phylogeny and Classification of Neotropical Fishes. Porto Alegre, Edipucrs, p. 603, 1998.; Carvalho et al. 2009CARVALHO, L.; ZUANON, J.; SAZIMA, I. Natural History of Amazon Fishes.In: Tropical biology and conservation management: case studies. Encyclopedia of Life Support Systems (EOLSS) (DEL CLARO, K., OLIVEIRA, P.S., RICO-GRAY, V. eds.) Publishers, Oxford, p. 113-144, 2009.; Albert et al. 2011ALBERT J.; PETRY, P.; REIS, R. Major biogeographic and phylogeographic patterns. In: Historical biogeography of Neotropical Freshwater Fishes (ALBERT, J.S., REIS, R.E. eds.). University of California Press, Berkeley, p. 21-57, 2011. https://doi.org/10.1525/california/9780520268685.003.0002
https://doi.org/10.1525/california/97805... ; van der Sleen & Albert 2017VAN DER SLEEN, P.; ALBERT, J. Field Guide to the Fishes of the Amazon, Orinoco, and Guianas. Princeton University Press, Princeton. 2017.https://doi.org/10.2307/j.ctt1qv5r0f
https://doi.org/10.2307/j.ctt1qv5r0f... ; Dagosta & De Pina, 2019DAGOSTA, F.; DE PINNA, M. The fishes of the Amazon: Distribution and biogeographical patterns, with a comprehensive list of species. Bulletin of the American Museum of Natural History, v. 431, p. 1-163, 2019. https://doi.org/10.1206/0003-0090.431.1.1
https://doi.org/10.1206/0003-0090.431.1.... ; Oberdorff et al., 2019OBERDORFF, T.; DIAS. M.; JÉZEQUEL, C.; ALBERT, J.; ARANTES, C.; BIGORNE, R.; CARVARJAL-VELLEROS, F.; DE WEVER, A.; FREDERICO, R.; HIDALGO, M.; HUGUENY, B.; LEPRIEUR, F.; MALDONADO, M.; MALDONADO-OCAMPO, J.; MARTENS, K.; ORTEGA, H.; SARMIENTO, J.; TEDESCO, P.; TORRENTE-VILARA, G.; WINEMILLER, K.; ZUANON, J. Unexpected fish diversity gradients in the Amazon basin. Science advances, v. 5, n. 9, eaav8681, 2019. https://doi.org/10.1126/sciadv.aav8681
https://doi.org/10.1126/sciadv.aav8681... ). But it is widely accepted that there are approximately 2700 already described fish species living in the Amazon basin (Dagosta & De Pina, 2019DAGOSTA, F.; DE PINNA, M. The fishes of the Amazon: Distribution and biogeographical patterns, with a comprehensive list of species. Bulletin of the American Museum of Natural History, v. 431, p. 1-163, 2019. https://doi.org/10.1206/0003-0090.431.1.1
https://doi.org/10.1206/0003-0090.431.1.... ). Nevertheless, a strikingly high number of fish species are being described for the Amazon every year (Valsecchi et al., 2017VALSECCHI, J.; MARMONTEL, M.; FRANCO, C.L.B.; CAVALCANTE, D.P.; COBRA, I.V.D.; LIMA, I.J.; LANNA, J.M.; FERREIRA, M.T.M.; NASSAR, P.M.; BOTERO-ARIAS, R.; MONTEIRO, V. Atualização e composição da lista - Novas Espécies de Vertebrados e Plantas na Amazônia 2014-2015. WWF e IDSM. Brasília, DF e Tefé, AM, p. 111, 2017.). Unfortunately, a relevant portion of the currently known fish fauna, like in other important megadiverse freshwater ecosystems of the World, is now threatened (Darwall et al, 2016DARWALL, W. R.; FREYHOF, J. Ö. R. G. Lost fishes, who is counting? The extent of the threat to freshwater fish biodiversity. Conservation of freshwater fishes, p. 1-36, 2016.; Arthington et al. 2016ARTHINGTON, A. H.; DULVY, N. K.; GLADSTONE, W.; WINFIELD, I. J. Fish conservation in freshwater and marine realms: status, threats and management. Aquatic Conservation: Marine and Freshwater Ecosystems, v. 26, p. 838-857, 2016.; IBAMA, 2018IBAMA. Livro Vermelho da Fauna Ameaçada de Extinção: V. VI- Peixes. ICMBio/MMA, Brasília, p. 1232, 2018.). Although some of the areas of the Central Amazonia and its floodplains have been intensively surveyed during the last half century (Correa et al., 2008CORREA, S. B.; CRAMPTON, W. G. R.; CHAPMAN, L. J.; ALBERT, J. S. A comparion of flooded forest and floating meadow fish assemblages in an upper Amazon floodplain. Journal of Fish Biology, v. 72, p. 629-644, 2008. doi: 10.1111/j.1095-8649.2007.01752.x.
https://doi.org/10.1111/j.1095-8649.2007... ; Freitas et al., 2014FREITAS, C. E. C.; SIQUEIRA-SOUZA, F. K.; FLORENTINO, A. C.; HURD, L. E. The importance of spacial scales to analysis of fish diversity in Amazonian floodplain lakes and implications for conservation. Ecology of Freshwater Fish, v. 23, p. 470-477, 2014.; Siqueira-Souza et al., 2016SIQUEIRA-SOUZA, F. K.; FREITAS, C. E. C.; HURD, L. E.; PETRERA Jr, M. 2016. Amazon floodplain fish diversity at different scales: do time and place really matter? Hydrobiologia, v. 776, n. 1, p. 99-110, 2016. Doi: 10.1007/s10750-016-2738-2.
https://doi.org/10.1007/s10750-016-2738-... ), some areas remain virtually unknown, or very poorly known, demonstrating the importance of inventory studies in the region. There is very few information available about the fish diversity of the middle Solimões region, a vast and biologically important part of the Western Brazilian Amazonia.

For many centuries the floodplain areas of the Amazon, annually inundated by white sediment-rich waters, have been visited and studied. Most of the material collected in these expeditions was sent to foreign institutions, mainly in Europe (Filho, 2009FILHO, J. Grandes expedições à Amazônia brasileira 1500-1930. Metalivros, São Paulo, p. 241, 2009.). The majority of the large cities and small towns in the Amazon are located in the várzea ecosystem, and almost all the commercial fisheries in the Amazon is carried out in várzea water bodies. The Amazonian varzea is a particular type of wetland, a seasonal floodplain forest inundated by whitewater rivers, with an intricate mosaic of waterbodies and annually flooded shores (Junk et al., 2011JUNK, W. J.; PIEDADE, M. T. F.; SCHÖNGART, J.; COHN-HAFT, M.; ADENEY, J. M.; WITTMANN, F. A classification of major naturally-occurring Amazonian Lowland wetlands. Wetlands, v. 31, p. 623-640, 2011. doi:10.1007/s13157-011-0190-7
https://doi.org/10.1007/s13157-011-0190-... ; Junk et al., 2014JUNK, W. J.; PIEDADE, M. T. F.; LOURIVAL, R.; WITTMANN, F.; KANDUS, P.; LACERDA, L. D.; BOZELLI, R. L.; ESTEVES, F. A.; NUNES DA CUNHA, K.; MALTCHIK, L.; SCHÖNGART, J.; SCHAEFFER-NOVELLI, Y.; AGOSTINHO, A. A. 2014. Brazilian wetlands: their definition, delineation, and classification for research, sustainable management, and protection. Aquatic Conservation: Marine and Freshwater Ecosystems, v. 24, p.5-22, doi:10.1002/aqc.2386
https://doi.org/10.1002/aqc.2386... ). Probably this is why we have the existing information about its fish fauna (Santos et al., 1991SANTOS, G. M.; FERREIRA, E. J. G.; ZUANON, J. A. S. Ecologia de peixes da Amazônia. In: Bases científicas para estratégias de preservação e desenvolvimento da Amazônia: fatos e perspectivas (VAL, A.L.; FIGLUIOLO, R.; FELDBERG, E. Eds.). Manaus: INPA/UFAM, Imprensa Universitária, v. 1, p. 263-280, 1991.; Goulding et al. 1996GOULDING, M.; SMITH, N. J. H.; MAHAR, D. J. Floods of Fortune - Ecology and economy along the Amazon. New York: Columbia University Press, p. 193, 1996.; Saint-Paul et al., 2000SAINT-PAUL, U.; ZUANON, J.; VILLACORTA-CORREA, M.A.; GARCIA, M.; FABRÉ, N. N.; BERGER, U.; JUNK, W.J. Fish communities in central Amazonian white- and blackwater floodplains. Environmental Biology of Fishes, v. 57, p. 235-250, 2000.; Zuanon et al., 2008ZUANON, J.; PY-DANIEL, L. H. R.; FERREIRA, E. J. G.; CLARO JR., L. H.; MENDONÇA, F. P. Padrões de distribuição da ictiofauna na várzea do Sistema Solimões-Amazonas entre Tabatinga (AM) e Santana (AP). In: Conservação da várzea: identificação e caracterização de regiões biogeográficas (ALBERNAZ, A.L.K.M. Org.).). Records are, however, focused on the large-bodied species, most of commercial value, and a very few information is available about occurrence and distribution of the fish fauna in most parts of the Amazonian várzea. This information is usually originated in species lists from very restricted areas, tend to be taxonomically unreliable and not supported by voucher specimens deposited in the main scientific fish collections. Despite these limitations, it is generally recognized that the ichthyofauna found in the Solimões-Amazonas várzea is placed among the more diverse of the Amazon, especially at the Western parts of the Central Brazilian Amazon, upstream from Manaus, the capital city of Amazonas State. This várzea ecosystem holds at least 647 fish species, including areas from the borders with Peru and Colombia, and the mouth, in the Atlantic coast (Zuanon et al., 2008ZUANON, J.; PY-DANIEL, L. H. R.; FERREIRA, E. J. G.; CLARO JR., L. H.; MENDONÇA, F. P. Padrões de distribuição da ictiofauna na várzea do Sistema Solimões-Amazonas entre Tabatinga (AM) e Santana (AP). In: Conservação da várzea: identificação e caracterização de regiões biogeográficas (ALBERNAZ, A.L.K.M. Org.).).

Fish surveys and other similar studies in the Middle Solimões region were intensified in the early 1990's through an intense research program implemented to support the regulation of the management for the newly created Mamirauá Sustainable Development Reserve - RDSM. The RDSM was the first protected area of this category implemented in Brazil. One of the main characteristics of this type of protected area, is the participatory management of natural resources by the local populations, combined with the scientific research to support their activities (Queiroz 2005QUEIROZ, H. A RDSM-um modelo de área protegida de uso sustentável. Estudos Avançados. Dossiê Amazônia, v. 54, n. 2, p. 183-204, 2005. https://doi.org/10.1590/S0103-40142005000200011
https://doi.org/10.1590/S0103-4014200500... ). In this way, a large inventory was made for the Mamirauá Reserve area and its adjacent rivers, generating a first list of fish species (Crampton 1999CRAMPTON, W. G. R. Os peixes da Reserva Mamirauá: diversidade e história natural na planície alagável da Amazônia. In: Estratégias para Manejo de Recursos Pesqueiros em Mamirauá. (QUEIROZ H.L. & CRAMPTON, W. eds.), Sociedade Civil Mamirauá/CNPq, Brasília, p. 10-36, 1999.). The vast majority of the material collected at that time was deposited in large national collections such as INPA, and also the Science and Technology Museum of Pontifical Catholic University of Rio Grande do Sul (PUCRS). Part of this material collected at Mamirauá Reserve was used to build a small reference collection at Mamirauá Institute, located in the town of Tefé, Amazonas State.

Subsequently, with the consolidation of the Mamirauá Sustainable Development Institute (IDSM), several other inventories were carried out in the region, generating new lists of fish species for the RDSM, and representing a considerable increase in the knowledge about the richness of the fish fauna of that protected area. The previous reference collection was greatly improved with new deposits from this reserve and other protected areas, and also from different parts of the Western Brazilian Amazonia, which became the current IDSM ichthyological collection. However, this recently generated information on the RDSM was never compiled in a single checklist. Therefore, the goal of the present paper, is to provide an updated list of the fish fauna that occur in the Mamirauá Sustainable Development Reserve.

Material and Methods

1. Study area

The fish collections were all conducted during field expeditions to the Mamirauá Sustainable Development Reserve (RDSM), in the Brazilian Central Amazon floodplain (Figure 1). Mamirauá is a wetland site of international importance listed under the UN Ramsar Convention, and the largest protected area of flooded forests in Brazil. The whole reserve's area (1,124,000 ha) if formed exclusively by the lowland floodplains of the Solimões and Japurá rivers, a complex mosaic of flooded forests interspaced by different types of water bodies; lakes, "canos" (channels), rivers and "paranãs" (river connections), each of them with particular physical and biological features, but connected at least once a year, since the entire reserve is completely flooded for 3 to 6 months annually (Henderson, 1999HENDERSON, P. A. 1999. O Ambiente Aquático da Reserva Mamirauá. In: Estratégias Para Manejo de Recursos Pesqueiros em Mamirauá (Queiroz, H.L. & Crampton, W.G.R. eds). SCM, MCT/CNPq, Brasília, p. 208, 1999.). The mosaic of forests (Wittmann et al. 2006WITTMANN, F.; SCHONART, J.; MONTERO, J.; MOTZER, T.; JUNK, W.; PIEDAD, M.; QUEIROZ, H.; WORBES, M. Tree species composition and diversity gradients in white water forests across the Amazon Basin. Journal of Biogeography, v. 3, n. 8, p. 1334-1347, 2006. https://doi.org/10.1111/j.1365-2699.2006.01495.x
https://doi.org/10.1111/j.1365-2699.2006... ) and water bodies, lakes and channels, at Mamirauá is typical of the várzea environment (Figure 2).

Figure 1
Map showing the Mamirauá Sustainable Development Reserve, Amazonas State, Brazil, with the geographical distribution of the points of distribution of fish sampling sites (black dots), and the main water bodies in the region (rivers, lakes and channels).

Figure 2
Examples of permanent and temporary aquatic environments sampled during the fish collections carried out at the Mamirauá Reserve: a) Japurá River; b) Solimões River; c) Mamirauá lake channel; d) Taracuazinho lake; e) Taxizal flood pool; f) Igapó (flooded forest) in Mamiraua system lake.

During a complete hydrological cycle, the water level in Mamirauá varies by more than 10 m (Ramalho et al. 2009RAMALHO, E.; MACEDO, J.; VIEIRA, T.; VALSECCHI, J.; CALVIMONTES, J.; MARMONTEL, M.; QUEIROZ, H. Ciclo hidrológico nos ambientes de várzea da Reserva de Desenvolvimento Sustentável Mamirauá Médio Rio Solimões, Período de 1990 a 2008. Uakari, v. 5, n. 1, p. 61-87, 2009.), alternating wet and dry periods in a typical annual flood pulse (Junk et al., 1989JUNK, W. J.; BAYLEY, P. B.; SPARKS, R. E. The flood pulse concept in river-floodplain systems. Canadian special publication of fisheries and aquatic sciences, v. 106, n. 1, p. 110-127, 1989.). Four seasons can be identified, based on water level (Gaston & He, 2011GASTON, K.; HE, F.; MAGURAN, A.; MCGILL, B. Species occurrence and occupancy. In: Biological diversity: frontiers in measurement and assessment (MAGURRAN, A.E. & MC GILL, B.J. eds). Oxford University Press, Oxford. p. 141-151, 2011.). These are (i) high water season, from May until mid-July; (ii) falling water season, from mid-July to September; (iii) low water season, in the months of September, October and November; and (iv) rising water season, from December to April. These water bodies support a large fish fauna (Henderson & Crampton 1997HENDERSON, P.; CRAMPTON, W. G. R. A comparison of fish diversity and abundance between nutrient-rich and nutrient-poor lakes in the Upper Amazon. Journal of Tropical Ecology, v. 13 n. 2, p. 175-198, 1997. https://doi:10.1017/S0266467400010403
https://doi:10.1017/S0266467400010403... ), with diverse communities in each of the major aquatic habitats present (Henderson & Hamilton 1995HENDERSON, P.; HAMILTON, H. Standing crop and distribution of fish in drifting and attached floating meadow within an Upper Amazonian varzea lake. Journal of Fish Biology, v. 47, n. 2, p. 266-276, 1995. https://doi:10.1111/j.1095-8649.1995.tb01894.x
https://doi:10.1111/j.1095-8649.1995.tb0... ).

The floodplain area in the confluence of Japurá and Solimões Rivers, where Mamirauá is located, is characterized by high atmospheric temperatures with average annual ranging from 28°C to 30°C, with maximum monthly ranging from 33°C to 35°C and minimum monthly ranging from 20°C to 22°C. The highest precipitations are concentrated between December and May (Ramalho et al., 2009RAMALHO, E.; MACEDO, J.; VIEIRA, T.; VALSECCHI, J.; CALVIMONTES, J.; MARMONTEL, M.; QUEIROZ, H. Ciclo hidrológico nos ambientes de várzea da Reserva de Desenvolvimento Sustentável Mamirauá Médio Rio Solimões, Período de 1990 a 2008. Uakari, v. 5, n. 1, p. 61-87, 2009.) when it can reach 300 mm per month during the wettest years and the annual precipitation in the reserve is in average 3000 mm. The Japurá and Solimões Rivers consists of large white water rivers, carrying sediments from the erosion of the Andes, and forming large inundated habitats. Solimões River is one of the largest Amazonian rivers (discharge 53.3 x 10³ m³/second) and the main channel of the Amazon Basin, until it gets the discharge of blackwaters from the Negro River and creates the mighty Amazon River. Japurá River, on the other hand, although smaller (discharge 14,5 x 10³ m³/second) is the Brazilian name for the Caquetá River, from Colombia. Successive erosion and deposition processes along the geological history of this floodplain created a complex mosaic of permanent and temporary waterbodies. The annual variation of water level responds for the various degrees of connectivity between those different waterbodies and the two main rivers. There are five main aquatic environments types in the Mamirauá Reserve relevant to the present work, since they were systematically surveyed over the years: the main rivers, lakes, canos and paranãs, flooded florest and the temporary pools formed inside the forest, when the water level recedes. The paranãs are channels connecting the main rivers, while the canos are channels that transport water from the rivers and from main channels to lower order aquatic environments within the floodplain, like smaller channels or lakes. Since canos are very shallow, some of them may dry completely during the low water periods. The lakes, on the other hand, may vary in shapes and sizes, and usually retain water during the entire hydrologic cycle. Therefore, lakes may retain a loose connection to the main channel during low water phase. During the high water period, all water bodies are connected and a direct communication is established among them all (Table 1).

2. Data collection

To prepare this checklist, a database was built with the information from different studies carried out mainly in the Southern, Eastern and Southeastern parts of the area (see black dots in Figure 1) over the last decades (Crampton, 1999CRAMPTON, W. G. R. Os peixes da Reserva Mamirauá: diversidade e história natural na planície alagável da Amazônia. In: Estratégias para Manejo de Recursos Pesqueiros em Mamirauá. (QUEIROZ H.L. & CRAMPTON, W. eds.), Sociedade Civil Mamirauá/CNPq, Brasília, p. 10-36, 1999.; Chaves 2006CHAVES, R. Diversidade e densidade ictiofaunística em lagos de várzea da Reserva de Desenvolvimento Sustentável Mamirauá. Dissertação de mestrado, Universidade Federal do Pará, Belém, PA, 2006.; Santos 2007SANTOS, M. Estudo da comunidade de peixes do capim flutuante do paraná do Apara, Reserva de Sustentável Mamirauá. Monografia de Conclusão do Cusro de Ciências Biológicas, Universidade Federal de Lavras, Lavras, MG. 2007.; Reis 2007REIS, L. Estudo das comunidades de peixes em poças de inundação formadas na mata de várzea da Reserva de Desenvolvimento Sustentável Mamirauá, Amazonas, Brasil. Monografia de Conclusão do Cusro de Ciências Biológicas, Universidade Federal de Lavras, Lavras, MG. 2007.). Whenever necessary, the collected material was revised in the fish collection of the IDSM. Additionally, we searched for all material collected at the RDSM in other important ichthyological collections in Brazil: Museum of Science and Technology (MCP) of the Pontifical Catholic University of Rio Grande do Sul, Museum of Zoology of the University of São Paulo (MZUSP), University of Campinas (ZUEC) and National Institute for Amazonian Research (INPA), available on SpeciesLink (www.specieslink.org.br). After the list was compiled, possible names and synonyms, and their occurrence, were confronted with information available in the Eschmeyer's Catalog of Fishes (Fricke et al.2020). To avoid possible synonymies between species cataloged by the many studies in the area, we applied the precautionary principle and remove all risks of double entries.

Results

Until the present, the ichthyofauna of the Mamirauá Sustainable Development Reserve is composed of 541 species, including 45 families and 15 orders (Table 2). These figures correspond to about 20% of all species valid for the Amazon (Dagosta and De Pinna 2019DAGOSTA, F.; DE PINNA, M. The fishes of the Amazon: Distribution and biogeographical patterns, with a comprehensive list of species. Bulletin of the American Museum of Natural History, v. 431, p. 1-163, 2019. https://doi.org/10.1206/0003-0090.431.1.1
https://doi.org/10.1206/0003-0090.431.1.... ), and represent a 86% increase in relation to the first list produced for the RDSM, published in the end of the last century (Crampton, 1999CRAMPTON, W. G. R. Os peixes da Reserva Mamirauá: diversidade e história natural na planície alagável da Amazônia. In: Estratégias para Manejo de Recursos Pesqueiros em Mamirauá. (QUEIROZ H.L. & CRAMPTON, W. eds.), Sociedade Civil Mamirauá/CNPq, Brasília, p. 10-36, 1999.). As detected in other studies and fish fauna surveys in Neotropical sites, the most represented orders were Siluriformes, with 209 species, and Characiformes, with 185 species (Beltrão and Soares 2018BELTRÃO, H. & SOARES, M.Variação temporal na composição da ictiofauna do lago e igarapés da Reserva de Desenvolvimento Sustentável RDS-Tupé, Amazônia Central. Biota Amazônica, v. 8, n. 1, p. 34-42, 2018.; Beltrão et al. 2019BELTRÃO H.; ZUANON, J.; FERREIRA, E. Checklist of the ichthyofauna of the Rio Negro basin in the Brazilian Amazon. Zookeys, v. 881, p. 53-89, 2019. https://doi.org/10.3897/zookeys.881.32055.
https://doi.org/10.3897/zookeys.881.3205... ; Dagosta and De Pinna 2019DAGOSTA, F.; DE PINNA, M. The fishes of the Amazon: Distribution and biogeographical patterns, with a comprehensive list of species. Bulletin of the American Museum of Natural History, v. 431, p. 1-163, 2019. https://doi.org/10.1206/0003-0090.431.1.1
https://doi.org/10.1206/0003-0090.431.1.... ). Together they represent more than 70% of the fish species richness at Mamirauá Reserve. Next in importance comes the Gymnotiformes, with 78 species. The gymnotids are remarkably diverse at the Mamirauá Reserve, where several new species have been described during the last two decades (Albert & Crampton 2001ALBERT, J.; CRAMPTON, W. Five new species of Gymnotus (Teleostei: Gymnotiformes) from an Upper Amazonian floodplain, with descriptions of electric organ discharges and ecology. Ichthyological Exploration of Freshwaters, v. 12, p. 241-266, 2001.; Crampton et al. 2004CRAMPTON, W. G. R.; HULEN, K.; ALBERT, J. Sternopygus branco: A New Species of Neotropical Electric Fish (Gymnotiformes: Sternopygidae) from the Lowland Amazon Basin, with Descriptions of Osteology, Ecology, and Electric Organ Discharges. Copeia, v. 2, p. 245-259, 2004.https://doi.org/10.1643/CI-03-105R1
https://doi.org/10.1643/CI-03-105R1... ; Crampton et al. 2005CRAMPTON, W. G. R.; THORSEN, D.; ALBERT, J. Three New Species from a Diverse, Sympatric Assemblage of the Electric Fish Gymnotus (Gymnotiformes: Gymnotidae) in the Lowland Amazon Basin, with Notes on Ecology. Copeia, v. 1, p. 82-99, 2005. https://doi.org/10.1643/CI-03-242R2
https://doi.org/10.1643/CI-03-242R2... ) (Figure 3f). At least, three new gymnotid species were recently discovered, two Apteronotids and one Hypopomids, and are under description. In the fourth place, the Cichliformes, with 40 species, is another species-rich order present. At Mamirauá we included in the checklist Apistogrammoides pucallpaensis Meinken, 1965, which had its first record for Brazil published recently (Oliveira et al. 2019OLIVEIRA, J. C.; OLIVEIRA, J. A.; ROSSATO, D. P. C. First record of Apistogrammoides pucallpaensis Meinken, 1965 (Perciformes, Cichlidae) for Brazil, in addition to fecundity information. Acta Limnologica Brasiliensia, Rio Claro, v. 31, n. 8, 2019. https://doi.org/10.1590/s2179-975x4218
https://doi.org/10.1590/s2179-975x4218... ) (Figure 3d).

Figure 3
Representative individuals of some species collected at Mamiraua Reserve: a) Anablepsoides "mamiraua" sp.n ♂; b) Anablepsoides "mamiraua" sp.n ♀; c) Ancistrus cf. hoplogenys; d) Apistogrammoides pucallpaensis; e) Curimatopsis microlepis; f) Gymnotus mamiraua; g) Moenkhausia hemigrammoides; h) Pyrrhulina zigzag; i) Triportheus angulatus; j) Serrasalmus sp. n.

The species richness at the family level also follows the general pattern found in the Neotropics. The five richest families are Characidae, with 61 species, Loricariidae with 55 species, Cichlidae with 37 species, Apteronotidae with 33 species and Auchenipteridae with 25 species. These numbers correspond to 39% of the total species richness at Mamirauá. Remarkably, family Characidae alone holds 11% of the total richness, demonstrating the diversity of this fish family at the protected area.

The richest aquatic environment present was the floodplain lakes (369 spp.), followed by the "canos" and paranás (301 spp.), and the rivers (261 spp.). In all aquatic environments Characiformes was the dominant order, followed by Siluriformes and Cichliformes. Such richness distribution among orders is expected for the Neotropical fish fauna, being reported from several prior studies (Queiroz et al., 2013QUEIROZ, L.; TORRENTE-VILARA, G.; OHARA, W.; PIRES, T.; ZUANON, J.; DORIA, C. Peixes do rio Madeira, volumes 1, 2 e3. Santo Antônia Energia, São Paulo. 2013.; Sleen and Albert, 2018SLEEN, P., ALBERT J. S. Field Guide to the Fishes of the Amazon, Orinoco e Guianas. Princeton University Press, Princeton. 2018.; Beltrão et al., 2019BELTRÃO H.; ZUANON, J.; FERREIRA, E. Checklist of the ichthyofauna of the Rio Negro basin in the Brazilian Amazon. Zookeys, v. 881, p. 53-89, 2019. https://doi.org/10.3897/zookeys.881.32055.
https://doi.org/10.3897/zookeys.881.3205... ; Dagosta and De Pinna, 2019DAGOSTA, F.; DE PINNA, M. The fishes of the Amazon: Distribution and biogeographical patterns, with a comprehensive list of species. Bulletin of the American Museum of Natural History, v. 431, p. 1-163, 2019. https://doi.org/10.1206/0003-0090.431.1.1
https://doi.org/10.1206/0003-0090.431.1.... ) (figure 4).

Figure 4
Ranking of richness by Orders and habitat of fish species found in the Mamirauá Sustainable Development Reserve (MSDR), N = Number of species.

From the names included in the first fish species list published for Mamirauá Reserve (Crampton, 1999CRAMPTON, W. G. R. Os peixes da Reserva Mamirauá: diversidade e história natural na planície alagável da Amazônia. In: Estratégias para Manejo de Recursos Pesqueiros em Mamirauá. (QUEIROZ H.L. & CRAMPTON, W. eds.), Sociedade Civil Mamirauá/CNPq, Brasília, p. 10-36, 1999.), we removed those identified only at the genus level, since they are not present in the material deposited in any known biological collection. They are Saccoderma sp.1, Pimelodus sp.1, Pseudostegophilus sp.1, Hoplosternum sp.1, Plagioscion sp.1 and "Petalodoras sp.1". We also removed Knodus sp.1 and Tetragonopterus sp.1, both included in a scientific report (M. Catarino, unpublished), informed as collected and identified only at the genus level. We found no correspondence with any material deposited in the collections consulted. Additionally, in the present version of the fish species list, we removed three names identified at the species level, mentioned in inventories and studies carried out at Mamirauá Reserve, but not deposited in any biological collection. They are Microglanis carlae Vera Alcaraz, da Graça & Shibatta, 2008, Nannostomus harrisoni (Eigenmann, 1909), Crenicichla cametana Steindachner, 1911 and Lycengraulis grossidens (Spix & Agassiz 1829). The decision to remove these four entries from the list was based on the consideration that Microglanis carlae has its distribution restricted to the Paraguay River basin; Nannostomus harrisoni has its distribution restricted to the Demerara river basin in Guyana, and that Crenicichla cametana, occurs only in the Xingu and Tocantins-Araguaia river basins (Dagosta and De Pinna 2019DAGOSTA, F.; DE PINNA, M. The fishes of the Amazon: Distribution and biogeographical patterns, with a comprehensive list of species. Bulletin of the American Museum of Natural History, v. 431, p. 1-163, 2019. https://doi.org/10.1206/0003-0090.431.1.1
https://doi.org/10.1206/0003-0090.431.1.... ). Lycengraulis grossidens is a marine/estuarine species, with not confirmed records for freshwater habitats, and freshwater specimens identified. Consequently, it is more likely that these were misidentifications made by those responsible for the reports of the inventories consulted.

The miniature Crenuchidae Elachocharax pulcher Myers, 1927 (sensu Weitzman and Vari 1988WEITZMAN, S.; VARI, R. Miniaturization in South American freshwater fishes; an overview and discussion. Proceedings of the Biological Society of Washington, v.101, n. 2, p. 444-465, 1988.; Toledo-Piza et al. 2014TOLEDO-PIZA, M.; MATTOX, G.; BRITZ, R. Priocharax nanus, a new miniature characid from the rio Negro, Amazon basin (Ostariophysi: Characiformes), with an updated list of miniature Neotropical freshwater fishes. Neotropical Ichthyology, v. 12, n. 2, p. 229-246, 2014. https://doi.org/10.1590/1982-0224-20130171
https://doi.org/10.1590/1982-0224-201301... ), and the hemiodontid Hemiodus atranalis (Fowler, 1940) were added to this list because they were recently captured at the Mamirauá Reserve, and we also included in our list three more species that just had their first records for the Solimões river basin, Curimatopsis microlepis, Moenkhausia hemigrammoides Géry, 1965 and Pyrrhulina zigzag Zarske & Géry, 1997 (Figures 3e; 3g; 3h).

Serrasalmus cf. spilopleura and Mesonauta insignis have their geographic distribution falling far from the Mamirauá Reserve area, and their occurrence can be questioned (Dagosta and De Pinna 2019DAGOSTA, F.; DE PINNA, M. The fishes of the Amazon: Distribution and biogeographical patterns, with a comprehensive list of species. Bulletin of the American Museum of Natural History, v. 431, p. 1-163, 2019. https://doi.org/10.1206/0003-0090.431.1.1
https://doi.org/10.1206/0003-0090.431.1.... ; Kullander and Silfvergrip, 1991KULLANDER, S., SILFVERGRIP, A. 1991. Review of the South American cichlid genus Mesonauta Günther (Teleostei, Cichlidae) with descriptions of two new species. Revue Suisse de Zoologie, v. 98, p. 407-448, 1991.). A careful review of the identification of these species should be conducted in the near future.

Fifty-seven taxa in the list were not identified at the species level, and thus have an uncertain identification at this level. They were included in the list because there are deposited material in scientific collections to voucher for their names. Forty of them were identified only at the genus level, such as Potamotrygon sp.1, Microcharacidium sp.1, Microschemobrycon sp.1 and Ancistrus sp.1"mancha dorsal". Sixteen species were pre-determined with "cf.", such as Metynnis cf. maculatus, Jupiaba cf. zonata and Ancistrus cf. hoplogenys (Figure 3f). Eight species are new and are now under the process of description, listed here as Characidium sp. n., Serrasalmus sp. n., Paravandellia sp. n., Plectrochilus sp. n., Brachyhypopomus sp. n., Adontosternarchus sp. n., Sternarchella sp. n. and Anablepsoides"mamiraua" sp. n. (Figures 3a; 3b; 3c).

Discussion

The fish fauna found at the Mamirauá Reserve is typical of the Amazonian várzea ecosystem. Like other parts of the várzea (Zuanon et al. 2008ZUANON, J.; PY-DANIEL, L. H. R.; FERREIRA, E. J. G.; CLARO JR., L. H.; MENDONÇA, F. P. Padrões de distribuição da ictiofauna na várzea do Sistema Solimões-Amazonas entre Tabatinga (AM) e Santana (AP). In: Conservação da várzea: identificação e caracterização de regiões biogeográficas (ALBERNAZ, A.L.K.M. Org.).), the more represented or richest families detected at RDSM fish fauna were Characidae, Loricariidae and Cichlidae. Species found at várzea lakes at the vicinity of the Solimões river (Saint-Paul et al., 2000SAINT-PAUL, U.; ZUANON, J.; VILLACORTA-CORREA, M.A.; GARCIA, M.; FABRÉ, N. N.; BERGER, U.; JUNK, W.J. Fish communities in central Amazonian white- and blackwater floodplains. Environmental Biology of Fishes, v. 57, p. 235-250, 2000.; Freitas et al., 2014FREITAS, C. E. C.; SIQUEIRA-SOUZA, F. K.; FLORENTINO, A. C.; HURD, L. E. The importance of spacial scales to analysis of fish diversity in Amazonian floodplain lakes and implications for conservation. Ecology of Freshwater Fish, v. 23, p. 470-477, 2014.; Siqueira-Souza et al., 2016SIQUEIRA-SOUZA, F. K.; FREITAS, C. E. C.; HURD, L. E.; PETRERA Jr, M. 2016. Amazon floodplain fish diversity at different scales: do time and place really matter? Hydrobiologia, v. 776, n. 1, p. 99-110, 2016. Doi: 10.1007/s10750-016-2738-2.
https://doi.org/10.1007/s10750-016-2738-... ) are very similar to those found at lakes in Mamirauá. Similarly, the species found in floating meadows mattresses at the Eastern Peruvian Amazon (Correa et al., 2008CORREA, S. B.; CRAMPTON, W. G. R.; CHAPMAN, L. J.; ALBERT, J. S. A comparion of flooded forest and floating meadow fish assemblages in an upper Amazon floodplain. Journal of Fish Biology, v. 72, p. 629-644, 2008. doi: 10.1111/j.1095-8649.2007.01752.x.
https://doi.org/10.1111/j.1095-8649.2007... ) are also similar to those found in the floating meadows at Mamirauá. However, in all those previous accounts, species richness was not as high as the one found at Mamirauá Reserve and its aquatic environments. The study area is located in a part of the várzea considered exceptionally species-rich, and holding a set of important endemic species (Zuanon et al., 2008ZUANON, J.; PY-DANIEL, L. H. R.; FERREIRA, E. J. G.; CLARO JR., L. H.; MENDONÇA, F. P. Padrões de distribuição da ictiofauna na várzea do Sistema Solimões-Amazonas entre Tabatinga (AM) e Santana (AP). In: Conservação da várzea: identificação e caracterização de regiões biogeográficas (ALBERNAZ, A.L.K.M. Org.).).

By any account, the Amazon basin has a superlative number of fish species. Available estimates vary greatly, but most of them suggest a number that may reach 3,500 species (Malabarba et al., 1998MALABARBA, L. R.; REIS, R. E.; VARI, R. P.; LUCENA, Z. M.; LUCENA, C. A. (Eds). Phylogeny and Classification of Neotropical Fishes. Porto Alegre, Edipucrs, p. 603, 1998.; Junk et al. 2007JUNK, W. J.; SOARES, M. G. M.; BAYLEY, P. B. Freshwater fishes of the Amazon River basin: their biodiversity, fisheries, and habitats. Aquatic Ecosystem Health & Management, v. 10, n. 2, p. 153-173, 2007.; Carvalho et al. 2009CARVALHO, L.; ZUANON, J.; SAZIMA, I. Natural History of Amazon Fishes.In: Tropical biology and conservation management: case studies. Encyclopedia of Life Support Systems (EOLSS) (DEL CLARO, K., OLIVEIRA, P.S., RICO-GRAY, V. eds.) Publishers, Oxford, p. 113-144, 2009.; Albert et al. 2011ALBERT J.; PETRY, P.; REIS, R. Major biogeographic and phylogeographic patterns. In: Historical biogeography of Neotropical Freshwater Fishes (ALBERT, J.S., REIS, R.E. eds.). University of California Press, Berkeley, p. 21-57, 2011. https://doi.org/10.1525/california/9780520268685.003.0002
https://doi.org/10.1525/california/97805... ; van der Sleen & Albert 2017VAN DER SLEEN, P.; ALBERT, J. Field Guide to the Fishes of the Amazon, Orinoco, and Guianas. Princeton University Press, Princeton. 2017.https://doi.org/10.2307/j.ctt1qv5r0f
https://doi.org/10.2307/j.ctt1qv5r0f... ; Dagosta & De Pina, 2019DAGOSTA, F.; DE PINNA, M. The fishes of the Amazon: Distribution and biogeographical patterns, with a comprehensive list of species. Bulletin of the American Museum of Natural History, v. 431, p. 1-163, 2019. https://doi.org/10.1206/0003-0090.431.1.1
https://doi.org/10.1206/0003-0090.431.1.... ). However, some other authors suggest a significant upward trend, and that this number may reach up to 5,000 species in the next 70 years, if we maintain the current rate of description of new species (Ota et al. 2015OTA, R.; MESSAGE, H.; GRAÇA, W.; PAVANELLI, C. Neotropical Siluriformes as a Model for Insights on Determining Biodiversity of Animal Groups. PloS One, v. 10, n. 7, 2015. https://doi.org/10.1371/journal.pone.0132913.
https://doi.org/10.1371/journal.pone.013... ). These values suggest that the Amazon fish fauna may represent about 15% of all freshwater fish species described in the world at the present (Oberdorff et al. 2019OBERDORFF, T.; DIAS. M.; JÉZEQUEL, C.; ALBERT, J.; ARANTES, C.; BIGORNE, R.; CARVARJAL-VELLEROS, F.; DE WEVER, A.; FREDERICO, R.; HIDALGO, M.; HUGUENY, B.; LEPRIEUR, F.; MALDONADO, M.; MALDONADO-OCAMPO, J.; MARTENS, K.; ORTEGA, H.; SARMIENTO, J.; TEDESCO, P.; TORRENTE-VILARA, G.; WINEMILLER, K.; ZUANON, J. Unexpected fish diversity gradients in the Amazon basin. Science advances, v. 5, n. 9, eaav8681, 2019. https://doi.org/10.1126/sciadv.aav8681
https://doi.org/10.1126/sciadv.aav8681... ). The Congo River basin, in Africa, is considered the second most diverse river basin in the world, with less than half the number of fish species registered for the Amazon River basin (Snoeks et al. 2011SNOEKS, J., HARRISON, I., STIASSNY, M. The status and distribution of freshwater fishes. In: The diversity of life in African freshwaters: underwater, under threat. An analysis of the status and distribution of freshwater species throughout mainland Africa. (DARWALL, W., SMITH, K., ALLEN, D., HOLLAND, R., HARRINSON, I., BROOKS, E. eds.). IUCN, Gland, Switzerland, p. 42-91, 2011.).

Species richness in a particular area is the result of several processes operating at multiple spatial and temporal scales (Peláez & Pavanelli 2018PELÁEZ, O.; PAVANELLI, C. Environmental heterogeneity and dispersal limitation explain different aspects of β-diversity in Neotropical fish assemblages. Freshwater Biology, v. 64, n. 3, p. 497-505, 2018. https://doi.org/10.1111/fwb.13237
https://doi.org/10.1111/fwb.13237... ), comprising numerous evolutionary lineages, resulting from the interaction of geological factors associated with vicariant and dispersion agents (Lundberg, 1998LUNDBERG, J. G. The temporal context for diversification of Neotropical fishes. In: Phylogeny and classification of Neotropical fishes (MALABARBA, L, REIS, R., VARI, R., LUCENA, C., LUCENA. eds.). EDIPUCRS, Porto Alegre, p. 67-91, 1998.; Dagosta and de Pinna 2017DAGOSTA F.; DE PINNA M. Biogeography of Amazonian fishes: deconstructing river basins as biogeographic units. Neotropical Ichthyology, v. 15, n. 3, p. 1-24, 2017. https://doi.org/10.1590/1982-0224-20170034
https://doi.org/10.1590/1982-0224-201700... ). The distribution of fish species in the Amazonian sub-basins and adjacent drainage systems is complex, and amounts to numerous distribution overlaps and superlative degrees of biogeographic congruence (Dagosta and De Pinna 2017DAGOSTA F.; DE PINNA M. Biogeography of Amazonian fishes: deconstructing river basins as biogeographic units. Neotropical Ichthyology, v. 15, n. 3, p. 1-24, 2017. https://doi.org/10.1590/1982-0224-20170034
https://doi.org/10.1590/1982-0224-201700... ). The diversity patterns of this mega-fauna and the processes that generate these patterns are still only partially known (Dagosta and De Pinna 2019DAGOSTA, F.; DE PINNA, M. The fishes of the Amazon: Distribution and biogeographical patterns, with a comprehensive list of species. Bulletin of the American Museum of Natural History, v. 431, p. 1-163, 2019. https://doi.org/10.1206/0003-0090.431.1.1
https://doi.org/10.1206/0003-0090.431.1.... ). However, recent studies suggest that the richness pattern of the Amazonian ichthyofauna is supported mainly by three factors: area, climate and energy availability (Oberdorff et al. 2019OBERDORFF, T.; DIAS. M.; JÉZEQUEL, C.; ALBERT, J.; ARANTES, C.; BIGORNE, R.; CARVARJAL-VELLEROS, F.; DE WEVER, A.; FREDERICO, R.; HIDALGO, M.; HUGUENY, B.; LEPRIEUR, F.; MALDONADO, M.; MALDONADO-OCAMPO, J.; MARTENS, K.; ORTEGA, H.; SARMIENTO, J.; TEDESCO, P.; TORRENTE-VILARA, G.; WINEMILLER, K.; ZUANON, J. Unexpected fish diversity gradients in the Amazon basin. Science advances, v. 5, n. 9, eaav8681, 2019. https://doi.org/10.1126/sciadv.aav8681
https://doi.org/10.1126/sciadv.aav8681... ). The pattern shown here for Mamirauá fish species diversity is consistent with the recent predictions, but the pattern of fish endemism at Mamirauá is much higher than expected (Oberdorff et al., 2019OBERDORFF, T.; DIAS. M.; JÉZEQUEL, C.; ALBERT, J.; ARANTES, C.; BIGORNE, R.; CARVARJAL-VELLEROS, F.; DE WEVER, A.; FREDERICO, R.; HIDALGO, M.; HUGUENY, B.; LEPRIEUR, F.; MALDONADO, M.; MALDONADO-OCAMPO, J.; MARTENS, K.; ORTEGA, H.; SARMIENTO, J.; TEDESCO, P.; TORRENTE-VILARA, G.; WINEMILLER, K.; ZUANON, J. Unexpected fish diversity gradients in the Amazon basin. Science advances, v. 5, n. 9, eaav8681, 2019. https://doi.org/10.1126/sciadv.aav8681
https://doi.org/10.1126/sciadv.aav8681... ).

The total number of species listed for the Mamirauá Reserve is considerably higher than in other studies, with the species richness at Middle Solimões basin ​​reaching figures higher than those from other Amazonian sub-basins, such as the Tapajós River basin (with 529 species), the Xingu River basin (with 502 species), even though the study area of the Middle-Solimões corresponds to a small proportion of those two sub-basins. In addition, its known species richness reaches about 63% to 85% of the total species registered for the main channel of the Amazon River, depending on the source adopted (Zuanon et al., 2008ZUANON, J.; PY-DANIEL, L. H. R.; FERREIRA, E. J. G.; CLARO JR., L. H.; MENDONÇA, F. P. Padrões de distribuição da ictiofauna na várzea do Sistema Solimões-Amazonas entre Tabatinga (AM) e Santana (AP). In: Conservação da várzea: identificação e caracterização de regiões biogeográficas (ALBERNAZ, A.L.K.M. Org.).; Dagosta and De Pinna 2019DAGOSTA, F.; DE PINNA, M. The fishes of the Amazon: Distribution and biogeographical patterns, with a comprehensive list of species. Bulletin of the American Museum of Natural History, v. 431, p. 1-163, 2019. https://doi.org/10.1206/0003-0090.431.1.1
https://doi.org/10.1206/0003-0090.431.1.... ). This high value we found is probably the result of two combined factors. The first would be the high sampling effort applied during the last decades to the study area (Figure 5). The ichthyofauna of many Amazonian regions remain under-sampled, some of them are still nearly unknown to science, with no biological collection performed so far. Consequently, the differences in species richness found may simply reflect the difference in collection efforts (Queiroz et al. 2013QUEIROZ, L.; TORRENTE-VILARA, G.; OHARA, W.; PIRES, T.; ZUANON, J.; DORIA, C. Peixes do rio Madeira, volumes 1, 2 e3. Santo Antônia Energia, São Paulo. 2013.). The two sub-basins under the greatest sampling effort are the same with the highest richness, the Negro River, with 1165 registered species (Beltrão et al. 2019BELTRÃO H.; ZUANON, J.; FERREIRA, E. Checklist of the ichthyofauna of the Rio Negro basin in the Brazilian Amazon. Zookeys, v. 881, p. 53-89, 2019. https://doi.org/10.3897/zookeys.881.32055.
https://doi.org/10.3897/zookeys.881.3205... ), and the Madeira River, with 1062 species. Besides those two we have, of course, the main river channel, the Solimões-Amazonas, with 922 species recorded (Dagosta and De Pinna 2019DAGOSTA, F.; DE PINNA, M. The fishes of the Amazon: Distribution and biogeographical patterns, with a comprehensive list of species. Bulletin of the American Museum of Natural History, v. 431, p. 1-163, 2019. https://doi.org/10.1206/0003-0090.431.1.1
https://doi.org/10.1206/0003-0090.431.1.... ).

Figure 5
Species accumulation curve per year in the list of fish species recorded for Mamirauá Sustainable Development Reserve.

The other explaining factor that may be responsible for the high species richness recorded would be the location of the Mamirauá Reserve and its environmental diversity. Located in the interflow of two great rivers, Solimões and Japurá, and in a large floodplain area, Mamirauá Reserve has a complex mosaic of bodies of water that are repeatedly connected and isolated, at least once a year. This type of ecosystem and the dynamics of its permanent or temporary aquatic environments provide several habitats and microhabitats that are distinct, and therefore can support a very high species richness (Figure 4). In this part of the Amazonian floodplains the water level rises annually around 11m (Ramalho et al., 2009RAMALHO, E.; MACEDO, J.; VIEIRA, T.; VALSECCHI, J.; CALVIMONTES, J.; MARMONTEL, M.; QUEIROZ, H. Ciclo hidrológico nos ambientes de várzea da Reserva de Desenvolvimento Sustentável Mamirauá Médio Rio Solimões, Período de 1990 a 2008. Uakari, v. 5, n. 1, p. 61-87, 2009.), invading a mosaic of equally diverse array of forest types, and connecting and isolating all the local water bodies, sometimes for many consecutive months, probably with important implications for the richness of fish species in the area (Junk, et al. 1989JUNK, W. J.; BAYLEY, P. B.; SPARKS, R. E. The flood pulse concept in river-floodplain systems. Canadian special publication of fisheries and aquatic sciences, v. 106, n. 1, p. 110-127, 1989.; Arantes et al., 2017ARANTES, C. C.; WINEMILLER, K. O.; PETRERE, M.; CASTELLO, L.; HESS, L. L. Relationship between forest cover and fish diversity in the Amazon River floodplain. Journal of Applied Ecology, v. 55, n. 1, p. 386-395, 2017. Doi: 10.1111/1365-2664.12967.
https://doi.org/10.1111/1365-2664.12967... . In each part of the hydrological cycle, the aquatic environments present at the várzea can show a striking variation in water quality parameters (see Table 2). Besides that, Mamirauá Reserve lays at the confluence of the Japurá River, and the mouths of Tefé, Jutaí and Juruá Rivers are also very close, just few kilometers away. This high proximity to many other river basins and their fish faunas, with distinct levels of dissimilarity among them, could be another source of diversity and species richness. The distribution of the fish species in the Amazon sub-basins and adjacent drainage systems is complex, and amounts to numerous distributional overlaps and superlative degrees of biogeographic congruence (Dagosta and de Pinna 2017DAGOSTA F.; DE PINNA M. Biogeography of Amazonian fishes: deconstructing river basins as biogeographic units. Neotropical Ichthyology, v. 15, n. 3, p. 1-24, 2017. https://doi.org/10.1590/1982-0224-20170034
https://doi.org/10.1590/1982-0224-201700... ). In the same way the high species richness of the Solimões River near Manaus can also be explained by its close proximity to the mouth of the Negro River (Zuanon et al., 2008ZUANON, J.; PY-DANIEL, L. H. R.; FERREIRA, E. J. G.; CLARO JR., L. H.; MENDONÇA, F. P. Padrões de distribuição da ictiofauna na várzea do Sistema Solimões-Amazonas entre Tabatinga (AM) e Santana (AP). In: Conservação da várzea: identificação e caracterização de regiões biogeográficas (ALBERNAZ, A.L.K.M. Org.).).

None of the species recorded for the study area is listed as threatened of extinction, according with the International Union for Conservation of Nature (IUCN) and IBAMA (2018)IBAMA. Livro Vermelho da Fauna Ameaçada de Extinção: V. VI- Peixes. ICMBio/MMA, Brasília, p. 1232, 2018.. Since the 2000's, several new species have been described for the area, almost all of them belonging to the Gymnotiformes, demonstrating a high species richness of this particular order at the Mamirauá Reserve, as in other várzea areas with habitats of similar diversity and structural complexity. This is probably due to the high number of taxonomic studies on this particular group of fish at Mamirauá (Albert & Crampton 2001ALBERT, J.; CRAMPTON, W. Five new species of Gymnotus (Teleostei: Gymnotiformes) from an Upper Amazonian floodplain, with descriptions of electric organ discharges and ecology. Ichthyological Exploration of Freshwaters, v. 12, p. 241-266, 2001.; Crampton et al. 2004CRAMPTON, W. G. R.; HULEN, K.; ALBERT, J. Sternopygus branco: A New Species of Neotropical Electric Fish (Gymnotiformes: Sternopygidae) from the Lowland Amazon Basin, with Descriptions of Osteology, Ecology, and Electric Organ Discharges. Copeia, v. 2, p. 245-259, 2004.https://doi.org/10.1643/CI-03-105R1
https://doi.org/10.1643/CI-03-105R1... ; Crampton et al. 2005CRAMPTON, W. G. R.; THORSEN, D.; ALBERT, J. Three New Species from a Diverse, Sympatric Assemblage of the Electric Fish Gymnotus (Gymnotiformes: Gymnotidae) in the Lowland Amazon Basin, with Notes on Ecology. Copeia, v. 1, p. 82-99, 2005. https://doi.org/10.1643/CI-03-242R2
https://doi.org/10.1643/CI-03-242R2... ; Correa et al. 2006CORREA, S. B.; CRAMPTON, W. G. R.; ALBERT, J. Three New Species of the Neotropical Electric Fish Rhabdolichops (Gymnotiformes: Sternopygidae) from the Central Amazon, with a New Diagnosis of the Genus. Copeia, v. 1, p. 27-42, 2006. https://doi.org/10.1643/0045-8511(2006)006[0027:TNSOTN]2.0.CO;2.
https://doi.org/10.1643/0045-8511(2006)0... ; Albert and Crampton 2006ALBERT, J.; CRAMPTON, W. Pariosternarchus amazonensis: a new genus and species of Neotropical electric fish (Gymnotiformes: Apteronotidae) from the Amazon River. Ichthyological Exploration of Freshwaters, v. 17, n. 3, p. 267-274, 2006.; de Santana & Crampton 2007DE SANTANA, C.; CRAMPTON, W. G. R. Revision of the Deep-channel Electric Fish Genus Sternarchogiton (Gymnotiformes: Apteronotidae). Copeia, v. 2, p. 387-402, 2007. https://doi.org/10.1643/0045-8511(2007)7[387:ROTDEF]2.0.CO;2
https://doi.org/10.1643/0045-8511(2007)7... ; de Santana & Crampton 2010DE SANTANA, C.; CRAMPTON, W. R. G. 2010.A Review of the South American Electric Fish Genus Porotergus (Gymnotiformes: Apteronotidae) with the Description of a New Species. Copeia, v. 2010, n. 1, p. 165-175, 2010. https://doi.org/10.1643/CI-05-136.
https://doi.org/10.1643/CI-05-136... ; de Santana & Vari 2010DE SANTANA, C.; VARI, R. 2010. Electric fishes of the genus Sternarchorhynchus (Teleostei, Ostariophysi, Gymnotiformes); phylogenetic and revisionary studies. Zoological Journal da Linnean Society, v. 159, p. 223-371, 2010. https://doi.org/10.1111/j.1096-3642.2009.00588.x
https://doi.org/10.1111/j.1096-3642.2009... ; Lundberg et al. 2013LUNDBERG, J.; COX-FERNANDES, C.; CAMPOS, R.; SULLIVAN, J. Sternarchella calhamazon n. sp., the amazon's most abundant species of apteronotid eletric fish, with a note on the taxonomic status of Sternarchus capanemae Steindachner, 1868 (Gymnotiformes, Apteronotidae). Proceedings of the Academy of Natural Sciences of Philadelphia, v. 162, n. 1, p. 157-173, 2013. https://doi.org/10.1635/053.162.0110.
https://doi.org/10.1635/053.162.0110... ; Sullivan et al. 2013SULLIVAN, J., ZUANON, J., COX-FERNANDES, C. Two new species and a new subgenus of toothes Brachyhypopomus eletric knifefishes (Gymnotiformes, Hypopomidae) from a the central Amazon and considerations pertaining to the evolution of a monophasic eletric organ discharge. Zookeys, v. 327, p. 1-34, 2013. https://doi.org/10.3897/zookeys.327.5427.
https://doi.org/10.3897/zookeys.327.5427... ; Carvalho & Albert 2015CARVALHO, T.; ALBERT, J. A new species of Rhamphichthys (Gymnotiformes: Rhamphichthyidae) from the amazona basin. Copeia, v. 103, n. 1, p. 34-41, 2015. https://doi:10.1643/CI-14-066.
https://doi:10.1643/CI-14-066... ; Crampton et al. 2016CRAMPTON, W. G. R.; DE SANTANA, C.; WADDELL, J.; LOVEJOY, N. A taxonomic revision of the Neotropical electric fish genus Brachyhypopomus (Ostariophysi: Gymnotiformes: Hypopomidae), with descriptions of 15 new species. Neotropical Ichthyology, v.14, n. 4, p. 639-790, 2016. https://doi.org/10.1590/1982-0224-20150146
https://doi.org/10.1590/1982-0224-201501... ; Evans et al. 2017EVANS, K.; CRAMPTON, W. G. R.; ALBERT, J. Taxonomic revision of the deep channel electric fish genus Sternarchella (Teleostei: Gymnotiformes: Apteronotidae), with descriptions of two new species. Neotropical Ichthyology, v. 15, n. 2, e160168, 2017. https://doi.org/10.1590/1982-0224-20160168
https://doi.org/10.1590/1982-0224-201601... ).

It is expected that, as new undersampled areas are explored and surveyed, especially in the Northwestern part of Mamirauá Reserve, another significant increase in the fish species list will be achieved. As can be said for the whole Amazon, improvements in the sampling effort, together with continued taxonomic revision of the collected material, will result in the increase in the number of records, of new occurrences, and even in the description of new fish species for the study area. Recent studies on the Neotropical fish fauna have led to a significant improvement on the knowledge on fish diversity in the Amazon as never before (Sleen and Albert 2018SLEEN, P., ALBERT J. S. Field Guide to the Fishes of the Amazon, Orinoco e Guianas. Princeton University Press, Princeton. 2018.; Dagosta and De Pinna 2019DAGOSTA, F.; DE PINNA, M. The fishes of the Amazon: Distribution and biogeographical patterns, with a comprehensive list of species. Bulletin of the American Museum of Natural History, v. 431, p. 1-163, 2019. https://doi.org/10.1206/0003-0090.431.1.1
https://doi.org/10.1206/0003-0090.431.1.... ; Oberdorff et al. 2019OBERDORFF, T.; DIAS. M.; JÉZEQUEL, C.; ALBERT, J.; ARANTES, C.; BIGORNE, R.; CARVARJAL-VELLEROS, F.; DE WEVER, A.; FREDERICO, R.; HIDALGO, M.; HUGUENY, B.; LEPRIEUR, F.; MALDONADO, M.; MALDONADO-OCAMPO, J.; MARTENS, K.; ORTEGA, H.; SARMIENTO, J.; TEDESCO, P.; TORRENTE-VILARA, G.; WINEMILLER, K.; ZUANON, J. Unexpected fish diversity gradients in the Amazon basin. Science advances, v. 5, n. 9, eaav8681, 2019. https://doi.org/10.1126/sciadv.aav8681
https://doi.org/10.1126/sciadv.aav8681... ), and we expect that this trend will be maintained or improved for the next decades.

Acknowledgments

The authors wish to thank Dr Henrique Lazzarotto, Dr Michel Catarino, MSc Rose Chaves, MSc Marília Santos, MSc Liana Reis and Marcela Sobanski, for carrying out fish surveys and processing the samples. Thanks to Dr Renildo Ribeiro de Oliveira for providing information on the fish lots deposited at INPA, to the Research Group on Geospatial Analysis, Environment and the Amazon Territory of the Mamirauá Institute for preparing the map, to Diego Matheus de Mello Mendes for images of fish species. We also want to thank the Mamirauá Sustainable Development Institute for support in logistics and infrastructure. Thanks to the National Council for Scientific and Technological Development - CNPq for the research grants (processes 300694/2016-4, 312542/2016-0, 300019/2017-3, 300503/2019-9,305539/2019-1 and 301024/2020-0) and for the scientific initiation scholarship of some assistants in the laboratory. Thanks to Wildlife Conservation Society and Gordon and Betty Moore Foundation for their financial support.

References

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