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The importance of a Biosphere Reserve of Atlantic Forest for the conservation of stream fauna

A importância de uma Reserva da Biosfera da Mata Atlântica para a Conservação da Fauna de Riachos

Abstracts

Preservation of terrestrial fauna and flora has been the main reason for the settlement of most protected areas in the past 30 years, but although those areas may include water bodies, this does not necessarily mean that the biodiversity of freshwater environments are also protected. In the present study, the fauna inventory of eight streams (1st, 2nd, 4th and 5th orders) of three microbasins of Japi Mountain, a Biosphere Reserve of Atlantic Forest recognised by UNESCO since 1994, located in São Paulo state, southeast of Brazil, was conducted. The hypothesis of this study is that the conservation of this area is important for the maintenance of the aquatic biodiversity of this biome, and so, this world hotspot deserves priority conservation actions. From 2005 to 2007, benthic macroinvertebrates, fishes and, eventually, anuran amphibians were sampled in these streams. The results showed that Japi Mountain contributes to the conservation of 138 taxonomic units of the aquatic biota and covers a rich and representative biodiversity of freshwater fauna of the world (0.2%), Neotropical region (0.9%), Brazil (2.4%) and São Paulo state (17.9%). The studied streams in the Environmental Protection Area help protect endangered taxa like the fishes Neoplecostomus paranensis and Pareiorhina cf rudolphi, and shelter freshwater invertebrates and fishes whose distribution is restricted to the Brazilian territory. Japi Mountain is also an important haven of species that was missing there like the frog species Vitreorana eurygnatha. Thus, this species inventory emphasises the importance of conservation actions of the freshwater environments of this Biosphere Reserve of Atlantic Forest.

amphibians; freshwater; fish; invertebrates; protected areas


A conservação da fauna e flora terrestres tem sido a principal razão para o estabelecimento da maioria das áreas protegidas nos últimos 30 anos, porém, apesar de muitas destas áreas apresentarem corpos d'água, isto não significa necessariamente que a biodiversidade dos ambientes dulcícolas também estará protegida. No presente trabalho foi realizado o levantamento da fauna de oito riachos (1a, 2a, 4a e 5a ordens) de três microbacias da Serra do Japi, localizada no estado de São Paulo e reconhecida como Reserva da Biosfera da Mata Atlântica pela UNESCO desde 1994. A hipótese do estudo é de que a conservação desta área seja de grande importância para a manutenção de sua biodiversidade aquática, comprovando assim a necessidade de ações prioritárias de conservação deste bioma. No período de 2005 a 2007 foram amostrados nestes riachos os macroinvertebrados bentônicos, peixes e, eventualmente, anfíbios anuros. Os resultados revelaram que a Serra do Japi contribui na conservação de 138 unidades taxonômicas da biota aquática e abriga rica e representativa biodiversidade da fauna de água doce do mundo (0,2%), da região neotropical (0,9%), do Brasil (2,4%) e do estado de São Paulo (17,9%). Os riachos das áreas de proteção ambiental estudados ajudam na proteção de táxons listados como vulneráveis a extinção no estado, como Neoplecostomus paranensis e Pareiorhina cf rudolphi, e abrigam animais dulcícolas de distribuição restrita ao território brasileiro. A Serra do Japi também constitui um importante reduto de espécies até então desaparecidas, como o anuro Vitreorana eurygnatha. Assim, este levantamento enfatizou a importância de ações de conservação dos ambientes aquáticos desta Reserva da Biosfera da Mata Atlântica.

anfíbios; água doce; peixes; invertebrados; áreas protegidas


Introduction

Preservation of terrestrial fauna and flora has been the main reason for the settlement of most protected areas in the past 30 years, and because most include water bodies, some of these protected areas also protect the biodiversity of freshwater environments. However, as emphasised by Agostinho et al. (2005)AGOSTINHO, AA., THOMAZ, S. and GOMES, LC., 2005. Conservation of the biodiversity of Brazil's Inland Waters. Conservation Biology, vol. 19, no. 3, p. 646-652. http://dx.doi.org/10.1111/j.1523-1739.2005.00701.x.
http://dx.doi.org/10.1111/j.1523-1739.20...
, these areas need the inventory studies of species to determine their effective importance to the preservation of the aquatic biota.

The lack of basic knowledge on the biodiversity of freshwater environments in Brazil is an obstacle to preservation studies (Agostinho et al., 2005AGOSTINHO, AA., THOMAZ, S. and GOMES, LC., 2005. Conservation of the biodiversity of Brazil's Inland Waters. Conservation Biology, vol. 19, no. 3, p. 646-652. http://dx.doi.org/10.1111/j.1523-1739.2005.00701.x.
http://dx.doi.org/10.1111/j.1523-1739.20...
). According to Rocha (2002)ROCHA, O., 2002. Perfil do conhecimento de biodiversidade em águas doces no Brasil. In LEWINSOHN, T. and PRADO, PI. (Ed.). Biodiversidade brasileira: síntese do estado atual do conhecimento. São Paulo: Contexto. p. 165-169., only 30% of the freshwater invertebrate diversity is presently known and some taxon as Porifera, Cnidaria, Platyhelminthes, Nemertea, Nematoda, Nematomorpha, Bryozoa, Annelida and several insect groups need specialists, collections and/or minimum updated information on identification, distribution and autoecology.

Unlike invertebrates, vertebrates are better known. Regarding the freshwater diversity, fish deserves attention because Brazil is the holder of the largest ictiofauna of the world (Lewinsohn and Prado, 2002LEWINSOHN, T. and PRADO, PI., 2002. Biodiversidade brasileira: síntese do estado atual do conhecimento. São Paulo: Contexto.; Agostinho et al., 2005AGOSTINHO, AA., THOMAZ, S. and GOMES, LC., 2005. Conservation of the biodiversity of Brazil's Inland Waters. Conservation Biology, vol. 19, no. 3, p. 646-652. http://dx.doi.org/10.1111/j.1523-1739.2005.00701.x.
http://dx.doi.org/10.1111/j.1523-1739.20...
). Considering the occurrence and distribution of 2,587 freshwater fish species registered in the country (Buckup et al., 2007BUCKUP, PA., MENEZES, NA. and GHAZZI, MS., 2007. Catálogo das espécies de peixes de água doce do Brasil. Rio de Janeiro: Museu Nacional.), headwater streams have an essential role to preserve this group as 70-80% of this richness is exclusively and/or preferably found in small water bodies (Buckup, 1999BUCKUP, PA., 1999. Sistemática e biogeografia de peixes de riachos. In CARAMASCHI, EP., MAZZONI, R. and PERESNETO, TR. (Ed.). Ecologia de peixes de riachos. Rio de Janeiro: Universidade Federal do Rio de Janeiro. p. 91-138. Série Oecologia Brasiliensis, vol. 6.; Castro, 1999CASTRO, RMC., 1999. Evolução da ictiofauna de riachos sul-americanos: padrões gerais e possíveis processos causais. In CARAMASCHI, EP., MAZZONI, R. and PERES-NETO, TR. (Ed.). Ecologia de peixes de riachos. Rio de Janeiro: Universidade Federal do Rio de Janeiro. p. 139-155. Série Oecologia Brasiliensis, vol. 6.; Pompeu et al., 2009POMPEU, PS., REIS, LS., GANDINI, CV., SOUZA, RCR. and FAVERO, JM, 2009. The Ichthyofauna of upper rio Capivari: defining conservation strategies based on the composition and distribution of fish species. Neotropical Ichthyology, vol. 7, no. 4, p. 659-666. http://dx.doi.org/10.1590/S1679-62252009000400015.
http://dx.doi.org/10.1590/S1679-62252009...
; Oyakawa and Menezes, 2010OYAKAWA, OT. and MENEZES, NA., 2010. Checklist dos peixes de água doce do Estado de São Paulo, Brasil. Biota Neotropica, vol. 11, no. 1a. Available from: <http://www.biotaneotropica.org.br/v11n1a/pt/abstract?inventory+bn0021101a2011>.
http://www.biotaneotropica.org.br/v11n1a...
).

The knowledge availability also reflects the number of species considered endangered, and the most studied groups present a greater number of species in the Red Book List of the Endangered Brazilian Fauna (Machado et al., 2008MACHADO, ABM., DRUMMOND, GM., PAGLIA, AP., 2008. Livro vermelho da fauna brasileira ameaçada de extinção. Brasília: MMA; Belo Horizonte: Fundação Biodiversitas. 2 vol. 1420 p.). From 627 species, 194 (31%) are from freshwater, 134 are fish, 16 are amphibians and 45 are invertebrates.

Besides the need of knowing if the Environmental Protection Areas help the conservation of non-threatened or threatened aquatic taxa, the functionality effectiveness of these areas need to be analysed regarding their contribution as a reserve of local, regional and global biodiversity (Balian et al., 2008BALIAN, EV., SEGERS, H., LÊVÊQUE, C. and MARTENS, K., 2008. The freshwater animal diversity assessment: an overview of the results. Hydrobiologia, vol. 595, no. 1, p. 627-637. http://dx.doi.org/10.1007/s10750-007-9246-3.
http://dx.doi.org/10.1007/s10750-007-924...
). Thus, in the present study, we made the fauna inventory of streams of three micro basins in Japi Mountain, located in a reserve of the Atlantic Forest. We also aimed to contribute to the knowledge of threatened species and areas that may serve as shelter for groups with restrict geographical distribution. The hypothesis of this study is that the conservation of this area is important for the maintenance of the aquatic biodiversity of this biome, and so, this world hotspot deserves priority conservation actions.

Methods

Study area

Japi Mountain is located in the countryside of São Paulo state, is part of the Environmental Protection Areas (EPAs) of Jundiaí (47.67% of the total area), Cabreúva (41.16%) and Cajamar (0.68%), and integrates the Piracicaba-Capivari-Jundiaí Water Conservation and Management Unit that gathers important effluents of the Medium Tiete River basin (Figure 1). Japi Mountain has a total extension of 19,170 ha or 350 Km2 and it is considered one of the last and biggest remaining continuous area of deciduous seasonal forest area of the state of São Paulo (Morellato, 1992MORELLATO, LPC., 1992. História natural da Serra do Japi: ecologia e preservação de uma floresta no sudeste do Brasil. Campinas: Ed. Unicamp/FAPESP.).

Figure 1.
Location of the study area (South America, southeastern Brazil, São Paulo state) with the indication of de limits of Japi Mountain (draw in the center), including the municipalities of Jundiaí, Cabreúva and Cajamar. The hydrographic maps show details of the sampled sites in each of the three studied microbasins (Er- Ermida, GX- Guaxinduva, CG- Caguaçu). The numbers (1, 2, 3, 4, 5) refer to the order of the sampled stretches; for Guaxinduva an upstream (GX5u) and a downstream stretch (GX5d) were sampled.

In 1994, Japi Mountain was classified by UNESCO as a Reserve of the Atlantic Forest Biosphere and a world hotspot deserving priority actions to preserve its biodiversity. The protection and preservation of Japi Mountain are supported by several legal mechanisms like: the Protection Law for Animals (Decree No 24645/34); Water Code (Decree No 24634/34); Mining Code (Decree No 227/67); Fauna Protection Law (Law No 5197/67); Law for the Creation of Ecological Stations and Environmental Protection Areas (Law No 6938/6902/ 81); Article No 225 of the Federal Constitution 1988 that imposes the public power the preservation and restoration of ecosystems, preservation of diversity and integrity of genetic heritage of the Country; Forestry Code (Federal Law No 4771/65); State Law No 9146/95 about financial compensation mechanisms for municipalities that have protected areas; Resolution No 11 of March 8th 1983 of the Defense Council of the Historical, Archeological, Architectural and Tourism Heritage (Condephaat) on the protection of Japi Mountain area. However, as emphasised by Jesus and Cavalheiro (2004)JESUS, N. and CAVALHEIRO, F., 2004. Aspectos antrópicos, legais e conservacionistas na Serra do Japi, SP. In SANTOS, JE., CAVALHEIRO, F., PIRES, JSR., OLIVEIRA, CH. and PIRES, AMZCR. (Ed.). Faces da polissemia da paisagem: ecologia, planejamento e percepção. São Carlos: Rima. vol. 2. p. 805-821, such legal mechanisms are not enough to guarantee the protection of the area because 90% of their lands are private properties, the fiscalisation is precarious, and the lack of knowledge about its biodiversity makes its monitoring and management difficult.

The occupation and degradation of Japi Mountain is marked by the construction of Santos-Jundiaí Railroad in 1867 which led to logging of the area so that wood could be used as fuel by locomotives. Later, due to the need of human settlement expansion in the region, there was the substitution of natural areas for cultivation areas (coffee, sugarcane, rice, wheat, beans, potato, Pinus) and cattle farming. Recently, the construction of two important highways (Rodovia Anhangüera and Rodovia Marechal Rondon) has brought part of the development of the city of São Paulo to the cities of Jundiaí, Campinas and Itu, increasing the urbanisation process in natural areas close to these great urban centers (Jesus and Cavalheiro, 2004JESUS, N. and CAVALHEIRO, F., 2004. Aspectos antrópicos, legais e conservacionistas na Serra do Japi, SP. In SANTOS, JE., CAVALHEIRO, F., PIRES, JSR., OLIVEIRA, CH. and PIRES, AMZCR. (Ed.). Faces da polissemia da paisagem: ecologia, planejamento e percepção. São Carlos: Rima. vol. 2. p. 805-821). Presently, the environmental problems of Japi Mountain are associated with real estate speculation, fires caused by agricultural activity, cattle raising, balloons, vegetation suppression and land movement by private individuals, hunting, mining and vandalism (Yoshida and Gonçalves, 2004YOSHIDA, CE. and GONÇALVES, L., 2004. Identificação de problemas e ameaças da APA Jundiaí-Cabreúva (Serra do Japi) através da análise dos talões de atendimento da guarda municipal de Jundiaí/SP. Bioikos, vol. 18, p. 5-10.).

The conservation state of Japi Mountain streams is related to the environmental zoning that defines the areas of the Biological Reserve and areas of the Preservation Zone (State Decree No 43.284/98 of São Paulo and Municipal Law No 417/04 of Jundiaí). Only three out of eight studied stretches of Ribeirão Ermida microbasin are located inside the Biological Reserve and are more preserved than the stretches of Guaxinduva and Caguaçu microbasins that are located inside the Preservation Zone, where there is the presence of anthropic activity as agro-forestry-pastoral activities and small residential farms (Table 1, Figure 1).

Table 1.
Location, stream morphometry and physical and chemical characteristics of the water (mean values) determined in the eight studied sites, monthly or seasonally (July and August – dry season, January and February – wet season). Microbasin Stream = ER- Ribeirão Ermida, CG- Ribeirão Caguaíu, GX- Ribeirão Guaxinduva. Order/Stretch = 1st, 2nd, 4th, 5th orders; u- upstream, d- downstream. Zone = CZ- conservation zone, BR- biological reserve.

Because the studied streams present water flow throughout the year, they fit the classification of perennial water courses and are part of a dendritic drainage net (Figure 1), typical of regions with prevalence of rocks that offer resistance to the erosive process (Christofoletti, 1980CHRISTOFOLETTI, A., 1980. Geomorfologia. 2nd ed. São Paulo: Edgard Blücher.). Santoro and Machado (1992)SANTORO, E. and MACHADO, DL., 1992. Elementos geológicos da Serra do Japi. In MORELLATO, LPC. (Ed.). História natural da Serra do Japi: ecologia e preservação de uma floresta no Sudeste do Brasil. São Paulo: Ed Unicamp/FAPESP. p. 24-29. reported that in the case of Japi Mountain this resistance is offered by predominant quartzite rocks in the region.

The relief of the terrain where the streams are located presents very weak to medium declivity (from < 6% to 15%) (Florenzano, 2008FLORENZANO, TG., 2008. Geomorfologia: conceitos e tecnologias atuais. São Paulo: Oficina de Textos. 318 p.). Except for three 5th order stretches, the other sampled stretches are small, narrow and shallow, with fast current, high content of dissolved oxygen, low values of temperature and electric conductivity (Table 1). These characteristics for headwater streams have also been emphasised by other authors (Buckup 1999BUCKUP, PA., 1999. Sistemática e biogeografia de peixes de riachos. In CARAMASCHI, EP., MAZZONI, R. and PERESNETO, TR. (Ed.). Ecologia de peixes de riachos. Rio de Janeiro: Universidade Federal do Rio de Janeiro. p. 91-138. Série Oecologia Brasiliensis, vol. 6.; Valente and Gomes, 2005VALENTE, OF. and GOMES, MA., 2005. Conservação de nascentes: hidrologia e manejo de bacias hidrográficas de cabeceiras. Viçosa: Aprenda Fácil.).

Collection of environmental data

The morphological characteristics of the microbasins were based on the topographical map of Japi Mountain in a 1:25000 scale, obtained from the Department of Planning of Jundiaí City. Rainfall and air temperature data of the region of Jundiaí were obtained from the site of the Integrated Centre of Meteorological Information – CIIAGRO (www.ciiagro.sp.gov.br accessed in July, 2008). The measurements of the stream canal and the limnological characteristics were carried out at all collection times of biotic data and at three distinct points of the longitudinal axis of each studied stretch. The streams were characterised according to their length, depth and luminosity (Minipa digital lightmeter, MLM1010 model) and the following physical and chemical water parameters: current (floating method), temperature (°C, measured by an Incoterm thermometer for maximum and minimum temperatures), dissolved oxygen (mg/L, determined by an Instrutherm oxymeter, model MO880), pH (measured by a digital pocket pHmeter, model pH1700), electrical conductivity (mS.cm–1, measured with a pocket digital conductometer, model CD840).

Collection of fauna data

The macrofauna was collected at eight stream stretches of Japi Mountain at two periods: (1) monthly from February 2005 to January 2006, and (2) seasonally, twice in the dry season of 2006 (July and August) and twice in the rainy season of 2007 (January and February). Three microbasins were sampled: Ermida (ER), Guaxinduva (GX) and Caguaçu (CG), including stretches of 1st, 2nd, 4th 5th orders (sensu Strahler classification (Stanford, 1996STANFORD, JA., 1996. Landscapes and catchments basins. In HAUER, FR., and LAMBERT, GA. (Ed.). Methods in stream ecology. San Diego: Academic Press. p. 3-22.)), with the orders indicated by numbers near the acronyms' microbasin (Table 1).

Monthly collections were conducted at four stream stretches (GX5u, GX5d, ER2, ER4) (Figure 1). In each stretch, six samples of the macroinvertebrate community were collected in a 30 m extension with a Surber sampler (30 × 30 cm and 500 mm mesh). The collected material was stored, transported in ice and later transferred to a refrigerator at 7 °C until screening (no later than three days after the collection). Macroinvertebrate screening was done visually by spreading the material in a white tray with incident light. The ictiofauna and, eventually, young forms of amphibians were collected along the bank vegetation with a 5 mm mesh sieve, fixed in formaldehyde 10% and preserved in alcohol 70% for posterior identification.

Seasonal collections were carried out in six stream stretches (ER1, ER2, ER4, CG1, CG2, CG5) (Figure 1). In each stretch, five areas of riffles of 5 m long each were selected in a 100 m extension for the aquatic fauna collections. In each area, four samples of macroinvertebrates (two from the banks and two from the middle of the stream) were collected with a Surber sampler (15 × 15 cm and 500 mm mesh), and the visually predominant substrate type in the sampler (sand, litter, gravel, rocks) was recorded. Next, the whole 5 m area was scanned with a trawl and a dip net (4 mm mesh) to capture fish and, eventually, young and adult anuran amphibians. The macroinvertebrates were fixed and preserved in alcohol 70% and the fishes were fixed in formaldehyde 10% and preserved in alcohol 70% for posterior identification. Macroinvertebrate screening was done with the use of a stereomicroscope.

The collected macroinvertebrates were deposited in the collection of the NGO Associação Mata Ciliar and the Laboratory of Stream Ecology of the Department of Zoology (UNESP – Botucatu). The fish species were deposited in the collection of the Museum of Zoology of USP and the Ichthyology Laboratory of UNESP - São José do Rio Preto.

The identification level of collected organisms was conducted mainly according to the adopted taxonomic levels in programs of macroinvertebrate and fish monitoring, and to the availability of identification keys and of specialists that could verify the identification of collected organisms. The study by Melo (2003)MELO, GA., 2003. Manual de identificação dos Crustacea Decapoda de água doce do Brasil. São Paulo: Loyola. was used to identify Crustacea Decapoda; the studies of Lopretto and Tell (1995)LOPRETTO, EC. and TELL, G., 1995. Ecosistemas de águas continentales: metodologia para su estudio. Argentina: Ediciones SUR., Merritt and Cummins (1996)MERRITT, RW. and CUMMINS, KW., 1996. An introduction to the aquatic insects of North America. Dubuque: Kemdall/Hunt., Nieser and Melo (1997)NIESER, N. and MELO, AL., 1997. Os heterópteros aquáticos de Minas Gerais: guia introdutório com chave de identificação para as espécies de Nepomorpha e Gerromorpha. Belo Horizonte: Ed. UFMG., McCafferty (1998)MCCAFFERTY, WP., 1998. Aquatic entomology: the fishermen's and ecologists' illustrated guide to insects and their relatives. Toronto: Jones and Bartlett Publishers., Fernández and Dominguez (2001)FERNÁNDEZ, HR. and DOMINGUEZ, E., 2001. Guía para la determinación de los artrópodos bentónicos sudamericanos. Tucumán: Universidad Nacional de Tucumán/Facultad de Ciencias Naturales/Instituto M. Lillo., Da-Silva et al. (2002)DA-SILVA, ER., SALLES, FF. and BAPTISTA, MS., 2002. As brânquias dos gêneros de Leptophlebiidae (Insecta: Ephemeroptera) ocorrentes no Estado do Rio de Janeiro. Biota Neotropica, vol. 2, no. 2. Available from: <http://www.biotaneotropica.org.br/v2n2/pt/abstract?short-communication+BN00902022002>.
http://www.biotaneotropica.org.br/v2n2/p...
, Costa et al. (2004)COSTA, JM., SOUZA, LO. and OLDRINI, BB., 2004. Chave para identificação das famílias e gêneros das larvas conhecidas de odonatas do Brasil: comentários e registros bibliográficos (Insecta, Odonata). Publicações Avulsas do Museu Nacional, vol. 99, p. 1-44., Olifiers et al. (2004)OLIFIERS, MH., DORVILLÉ, LFM., NESSIMIAN, JL. and HAMADA, N., 2004. A key to Brazilian genera of Plecoptera (Insecta) based on nymphs. Zootaxa, vol. 651, p. 1-15., Paprocki et al. (2004)PAPROCKI, H., HOLZENTHAL, RW. and BLAHNIK, RJ., 2004. Checklist of the Trichoptera (Insecta) of Brazil. Biota Neotropica, vol. 4, no. 1. Available from: <http://www.biotaneotropica.org.br/v4n1/pt/abstract?inventory+BN01204012004>.
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, Rio Grande do Sul (2006), Passos et al. (2007)PASSOS, MIS., NESSIMIAN, JL. and FERREIRA JUNIOR, N., 2007. Chaves para identificação dos gêneros de Elmidae (Coleoptera) ocorrentes no Estado do Rio de Janeiro, Brasil. Revista Brasileira de Entomologia, vol. 51, no. 1, p. 42-53. http://dx.doi.org/10.1590/S0085-56262007000100008.
http://dx.doi.org/10.1590/S0085-56262007...
, Calor (2007)CALOR, AR., 2007. Trichoptera. In FROEHLICH, CG. (Org.). Guia on-line: identificação de larvas de insetos aquáticos do estado de São Paulo. Available from: <http://sites.ffclrp.usp.br/aguadoce/index_trico>.
http://sites.ffclrp.usp.br/aguadoce/inde...
and Manzo and Archangelsky (2008)MANZO, V. and ARCHANGELSKY, M., 2008. A key to known larvae of South American Elmidae (Coleoptera: Byrrhoidea), with a description of the mature larva of Macrelmis saltensis Manzo. International Journal of Limnology, vol. 44, no. 1, p. 63-74. http://dx.doi.org/10.1051/limn:2008023.
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were used for Insecta identification. The researchers Dr. Gustavo Melo, from the Museum of Zoology of USP, Dr. Sérgio L. S. Bueno, from the Institute of Biosciences of USP, and Dr. Célio Magalhães, from the National Institute of Amazon Research, were consulted for the crustacean identification. The specialists, Dr Melissa O. Segura, Dr. Mateus Pepineli and Dr. Irineu de S. Onofre, from the Department of Limnology of UFSCar, verify the identification of Coleoptera-Elmidae, Diptera-Simuliidae and Odonata, respectively. Dr. Francisco de A. G. de Melo confirmed the identification of Insecta-Orthoptera.

The fish identification was based on the studies by Britski (1972)BRITSKI, HA., 1972. Peixes de água doce do estado de São Paulo: sistemática. In Comissão Interestadual da Bacia Paraná-Paraguai. Faculdade de Saúde Pública. Universidade de São Paulo (Ed.). Poluição e piscicultura: notas sobre poluição, ictiologia e piscicultura. São Paulo: Cibpu. p. 79-108, Menezes et al. (2007)MENEZES, NA., WEITZMAN, SH., OYAKAWA, OT., LIMA, FCT., CASTRO, RM. and WEITZMAN, MJ., 2007. Peixes de água doce da Mata Atlântica: lista preliminar das espécies e comentários sobre conservação de peixes de água doce Neotropicais. São Paulo: MZUSP., Buckup (1992)BUCKUP, PA., 1992. Redescription of Characidium fasciatum, type species of the Characidiinae (Teleostei, Characiformes). Copeia, vol. 1992, sup. supplement 4, p. 1066-1073. http://dx.doi.org/10.2307/1446639.
http://dx.doi.org/10.2307/1446639...
, Garutti and Britski (2000)GARUTTI, V. and BRITSKI, HA., 2000. Descrição de uma espécie nova de Astyanax (Teleostei: Characidae) da Bacia do Alto Rio Paraná e considerações sobre as demais espécies do gênero na Bacia. Comunicações do Museu de Ciências e Tecnologia PUCRS, Série Zoologia, vol. 13, p. 65-88., Chamon et al. (2005)CHAMON, CC., ARANDA, AT. and BUCKUP, PA., 2005. Pareiorhina brachyrhyncha (Loricariidae: Siluriformes): a new species of fish from the Paraíba do Sul slope of Serra da Mantiqueira, southeastern Brazil. Copeia, vol. 2005, sup. supplement 3, p. 550-558. http://dx.doi.org/10.1643/CI-04-276R.
http://dx.doi.org/10.1643/CI-04-276R...
and confirmed by the specialists Dr. Osvaldo T. Oyakawa, from the Museum of Zoology of USP, and Dr. Francisco Langeani Neto, from the Department of Zoology and Botany (UNESP - São José do Rio Preto).

The amphibians were identified by Daniel Contieri Rolim, from the Herpetology Laboratory of the Department of Zoology UNESP - Botucatu, who utilised the taxonomic key published by Ribeiro et al. (2005)RIBEIRO, RS., EGITO, GTBT. and HADDAD, CRB., 2005. Chave de identificação: anfíbios anuros da vertente de Jundiaí da Serra do Japi, Estado de São Paulo. Biota Neotropica, vol. 5, no. 2. Available from: <http://www.biotaneotropica.org.br/v5n2/pt/abstract?identification-key+bn03005022005>.
http://www.biotaneotropica.org.br/v5n2/p...
and the descriptions done by Bokermann (1963)BOKERMANN, WCA., 1963. Girinos de anfíbios brasileiros – 2 (Amphibia, Salentia). Revista Brasileira de Biologia = Brazilian Journal of Biology, vol. 23, p. 349-353. and Rada et al. (2007)RADA, M., RUEDA-ALMONACID, JV., VELÁSQUEZ-ÁLVAREZ, AA. and SÁNCHEZ-PACHECO, SJ., 2007. Descripción de las larvas de dos Centrolénidos (Anura: Centrolenidae) del noroccidente de la Cordillera Oriental, Colombia. Papéis Avulsos de Zoologia, vol. 47, p. 259-272.; Dr. Célio Fernando Baptista Haddad, from the Department of Zoology of UNESP-Rio Claro, confirmed their identification.

Results

The 26,219 specimens, representing 138 taxonomic units and mainly consisting of organisms from the aquatic macrofauna (Tables 2 and 3), were collected in the eight studied streams of Japi Mountain from 2005 to 2007. If each identified taxonomic unit is considered as an equivalent to a species, then Japi Mountain collaborates with almost 20% of the freshwater biodiversity of São Paulo state (Table 4).

Table 2.
List of the invertebrates sampled in eight streams located in Japi Mountain in the period of 2005-2007. Taxonomic levels and sequence based on Ruppert et al. (2005)RUPPERT, EE., FOX, RS. and BARNES, RD., 2005. Zoologia dos invertebrados. São Paulo: Roca..

Table 3.
Taxonomic list of vertebrates sampled in eight streams located at the Japi Mountain, in the period of 2005-2007. The worldwide area of occurrence of the families is indicated as: SAm- South America, CAm- Central America, NAm- Norte America, NT- Neotropic, AF-Africa, OR-Orient. Taxonomic levels of fish groups based on Reis et al. (2003)REIS, RE., KULANDER, SO. and FERRARIS, CJ., 2003. Check list of the freshwater fishes of South and Central America. Porto Alegre: EDIPUCRS.; occurrence data for fish based on Lucinda (2008)LUCINDA, PHI., 2008. Systematics and biogeography of the genus Phalloceros Eigenmann, 1907 (Cyprinodontiformes: Poeciliidae: Poeciliinae), with the description of twenty-one new species. Neotropical Ichthyology, vol. 6, no. 2, p. 113-158. http://dx.doi.org/10.1590/S1679-62252008000200001.
http://dx.doi.org/10.1590/S1679-62252008...
and Menezes et al. (2007)MENEZES, NA., WEITZMAN, SH., OYAKAWA, OT., LIMA, FCT., CASTRO, RM. and WEITZMAN, MJ., 2007. Peixes de água doce da Mata Atlântica: lista preliminar das espécies e comentários sobre conservação de peixes de água doce Neotropicais. São Paulo: MZUSP. and for amphibians based on Duellman (1999)DUELLMAN, WE., 1999. Patterns of distribution of amphibians: a global perspective. Baltimore: Johns Hopkins University Press..

Table 4.
Total number (or the lowest estimated value) of freshwater macrofauna species described in the world, in the Neotropical region (NT), in Brazil, in the State of São Paulo (SP) and in Japi Mountain. References: IManconi and Pronzato (2008); IIVolkner-Ribeiro (1999); IIIJankowski et al. (2008); IVSilveira and Schlenz (1999); vSchockaert et al. (2008); VIForneris (1999a); VIISundberg and Gibson (2008); VIIIForneris (1999b); IXAbebe et al. (2008); XPoinar Junior (2008); XIForneris (1999c); XIIMassard and Geimer (2008); XIIIForneris (1999e); XIVBogan (2008); XVAvelar (1999); XVIStrong et al. (2008); XVIISimone (1999); XVIIIGlasby and Timm (2008); XIXSteiner and Amaral (1999); XXMartin et al. (2008); XXIRighi (1999); XXIIBalian et al. (2008); XXIIIForneris (1999d); XXIVMugnai et al. (2010); XXVMagalhães (1999); XXVIFroehlich (1999a); XXVIIHubbard and Pescador (1999); Strixino and Strixino (1999)STRIXINO, ST. and STRIXINO, G., 1999. Insetos Dípteros quironomídeos. In ISMAEL, D., VALENTI, WC., MATSUMURA-TUNDISI, T. and ROCHA, O. (Ed.). Biodiversidade do Estado de São Paulo, Brasil: invertebrados de água doce. São Paulo: FAPESP. vol. 4. p. 141-148.; Carvalho (1999)CARVALHO, AL., 1999. Insetos odonatas. In ISMAEL, D., VALENTI, WC., MATSUMURA-TUNDISI, T. and ROCHA, O. (Ed.). Biodiversidade do Estado de São Paulo, Brasil: invertebrados de água doce. São Paulo: FAPESP. vol. 4. p. 149-155.; Froehlich (1999aFROEHLICH, CL., 1999a. Outros insetos. In ISMAEL, D., VALENTI, WC., MATSUMURA-TUNDISI, T. and ROCHA, O. (Ed.). Biodiversidade do Estado de São Paulo, Brasil: invertebrados de água doce. São Paulo: FAPESP. vol. 4. p. 161-168.,b)FROEHLICH, CL., 1999b. Insetos plecópteros. In ISMAEL, D., VALENTI, WC., MATSUMURA-TUNDISI, T. and ROCHA, O. (Ed.). Biodiversidade do Estado de São Paulo, Brasil: invertebrados de água doce. São Paulo: FAPESP. vol. 4. p. 156-160. (*without Coleoptera); XXVIIILévêque et al. (2008); XXIXBuckup (1999) e Buckup et al. (2007)BUCKUP, PA., MENEZES, NA. and GHAZZI, MS., 2007. Catálogo das espécies de peixes de água doce do Brasil. Rio de Janeiro: Museu Nacional. (stream ictiofauna); XXXMenezes et al. (2007) (ictiofauna of Atlantic forest streams); XXXIRolla et al. (2012); XXXIIVences and Köhler (2008); XXXIIISBH (2010); XXXIVAraújo et al. (2009); XXXVRibeiro et al. (2005).

For the macroinvertebrate groups whose identification was more refined (Crustacea and Insecta), the importance of Japi Mountain for the conservation of Brazilian aquatic biodiversity is more evident because the area helps maintain 50% of the families and 25% of the freshwater Decapoda and Insecta genera of Brazil (Tables 2 and 5).

Table 5.
Number of families and genera of the most abundant aquatic macroinvertebrates sampled in Japi Mountain, showing worldwide, national and local data. References: IBalian et al. (2008); IIMelo (2003); IIIDe Grave et al. (2008); IVYeo et al. (2008); VBarber-James et al. (2008); VIMariano and Froehlich (2007); VIIFochetti and Tierno de Figueroa (2008); VIIILecci and Froehlich (2007); IXDe Moor and Ivanov (2008); XPaprocki et al. (2004); XIWagner et al. (2008); XIIPinho (2008); XIIIJäch and Balke (2008); XIVBenetti et al. (2006); ? scanty or inexistent data.

Analysing the geographical distribution of nine collected fish families, except for Poeciliidae and Cichlidae, Japi Mountain streams contribute to conserve the ichthyofauna restricted to the American continent, mainly Callichthyidae and Erythrinidae exclusive to South America (Table 3).

Although anurans are not a target in the collection methodology, they were occasionally caught with the fish. Tadpoles of this Centrolenidae species were collected in stream stretches located on Santa Marta Farm (CG1) and at Dog (CG2), outside the area destined to the Biological Reserve of Japi Mountain. From the data published, it is verified that Japi Mountain contributes to the preservation of approximately 14% (31 out of 225 species) of anuran amphibians recorded in São Paulo state (Table 4).

Discussion

The average values of physical and chemical measured parameters indicate that the water in the studied streams has little deleterious anthropic influence (based on values of CONAMA Resolution 357/2005) and the studied average variations may be a reflection of the spatial differences related to the conservation state of the stretches as well as natural characteristics of streams like order, morphology and geology of the microbasin. Slightly acid pH, typical of quartzite soils (Rodriguez and Shepherd, 1992RODRIGUEZ, RR. and SHEPHERD, GJ., 1992. Análise da variação estrutural e fisionômica da vegetação e características edáficas, num gradiente altitudinal na Serra do Japi. In MORELLATO, LPC. (Ed.). História natural da Serra do Japi: ecologia e preservação de uma floresta no sudeste do Brasil. São Paulo: Ed. Unicamp/FAPESP. p. 64-81), was probably the factor that influenced the average values of water pH between 5.8 to 6.7.

Considering the inventory done by Biota Project FAPESP (Steiner and Amaral, 1999STEINER, TM. and AMARAL, AC., 1999. Anelídeos poliquetos. In ISMAEL, D., VALENTI, WC., MATSUMURA-TUNDISI, T. and ROCHA, O. (Ed.). Biodiversidade do Estado de São Paulo, Brasil: invertebrados de água doce. São Paulo: FAPESP. vol. 4. p. 73-79.), it is possible to infer that Japi Mountain is an important area to conserve unique species described for the state of São Paulo, like Nemertea Prostoma eilhardi (Montgomeri, 1894) (Forneris, 1999bFORNERIS, L., 1999b. Nemertinos. In ISMAEL, D., VALENTI, WC., MATSUMURA-TUNDISI, T. and ROCHA, O. (Ed.). Biodiversidade do Estado de São Paulo, Brasil: invertebrados de água doce. São Paulo: FAPESP. vol. 4. p. 25-28.) and Nematomorpha Paragordius flavescens Linstow, 1906 (Forneris, 1999cFORNERIS, L., 1999c. Nematomorfos gordióides. In ISMAEL, D., VALENTI, WC., MATSUMURA-TUNDISI, T. and ROCHA, O. (Ed.). Biodiversidade do Estado de São Paulo, Brasil: invertebrados de água doce. São Paulo: FAPESP. vol. 4. p. 35-38), even with the low identification resolution of some less abundant taxa. Besides the validity of the record of Temnocephalida order for the state, not cited by the Biota project (Forneris, 1999aFORNERIS, L., 1999a. Platelmintos turbelários. In ISMAEL, D., VALENTI, WC., MATSUMURA-TUNDISI, T. and ROCHA, O. (Ed.). Biodiversidade do Estado de São Paulo, Brasil: invertebrados de água doce. São Paulo: FAPESP. vol. 4. p. 17-23.), when contributing to the preservation of this group, Japi streams help to maintain the ecological ectosymbiosis relation between temnocephalida and crustraceans of the Aegla (Amato et al., 2003AMATO, JFR., AMATO, SB. and DAUDT, LCC., 2003. New species of Temnocephala Blanchard (Platyhelminthes, Temnocephalida) ectosymbiont on Aegla serrana Buckup & Rossi (Crustacea, Anomura) from southern Brazil. Revista Brasileira de Zoologia, vol. 20, no. 3, p. 493-500. http://dx.doi.org/10.1590/S0101-81752003000300021.
http://dx.doi.org/10.1590/S0101-81752003...
) and Trichodactylus genera (Amato et al., 2006AMATO, JFR., AMATO, SB. and SEIXAS, AS., 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, p. 796-806. http://dx.doi.org/10.1590/S0101-81752006000300026.
http://dx.doi.org/10.1590/S0101-81752006...
). Still using the Biota Project FAPESP inventory results (Steiner and Amaral, 1999STEINER, TM. and AMARAL, AC., 1999. Anelídeos poliquetos. In ISMAEL, D., VALENTI, WC., MATSUMURA-TUNDISI, T. and ROCHA, O. (Ed.). Biodiversidade do Estado de São Paulo, Brasil: invertebrados de água doce. São Paulo: FAPESP. vol. 4. p. 73-79.), Japi Mountain also collaborates for the conservation of freshwater polychaete of the Stratiodrilus genus, and it is possible to suggest that S. arreliai Amaral & Morgado, 1997 is present in Japi, considering only the distribution information (proximity to Jaraguá peak) and hosts (Aegla sp.).

Regarding genera and species of crustacean and insects recorded only in Brazil, Japi Mountain streams stand out in the maintenance of the crustaceans Aegla paulensis (Bond-Buckup et al., 2008BOND-BUCKUP, G., JARA, CG., PÉREZ-LOSADA, M., BUCKUP, L. and CRANDALL, KA., 2008. Global diversity of crabs (Aeglidae: Anomura: Decapoda) in freshwater. Hydrobiologia, vol. 595, no. 1, p. 267-273. http://dx.doi.org/10.1007/s10750-007-9022-4.
http://dx.doi.org/10.1007/s10750-007-902...
) and Macrobrachium iheringi (Coelho and Ramos-Porto, 1984COELHO, PA. and RAMOS-PORTO, M., 1984. Camarões de água doce do Brasil: distribuição geográfica. Revista Brasileira de Zoologia, vol. 2, no. 6, p. 405-410. http://dx.doi.org/10.1590/S0101-81751984000200014.
http://dx.doi.org/10.1590/S0101-81751984...
), the Ephemeroptera Tupiara (Salles et al., 2003SALLES, FF., LUGO-ORTIZ, CR., DA-SILVA, ER. and FRANCISCHETTI, CN., 2003. Novo gênero e espécie de Baetidae (Insecta: Ephemeroptera) do Brasil. Arquivos do Museu Nacional. Museu Nacional (Brazil), vol. 61, p. 23-30.), the Plecoptera Kempnyia and Guaranyperla (Lecci & Froelich 2007) and the Trichoptera Mexitrichia (Flint et al., 1999FLINT, OS., HOLZENTHAL, RW. and HARRIS, SC., 1999. Nomenclatural and systematic changes in the Neotropical caddisflies (Insecta: Trichoptera). Insecta Mundi, vol. 13, p. 73-84.).

Out of 121 fish species of streams recorded in the Atlantic Forest area in São Paulo state (Menezes et al., 2007MENEZES, NA., WEITZMAN, SH., OYAKAWA, OT., LIMA, FCT., CASTRO, RM. and WEITZMAN, MJ., 2007. Peixes de água doce da Mata Atlântica: lista preliminar das espécies e comentários sobre conservação de peixes de água doce Neotropicais. São Paulo: MZUSP.), 31 species (25%) were recorded in Japi Mountain (Rolla et al., 2012ROLLA, APPR., ESTEVES, KE. and YOSHIDA, CE., 2012. Ecologia e conservação de peixes de riachos da Serra do Japi. In VASCONCELLOS-NETO, J., POLLI, PR. and PENTEADO-DIAS, AM. (Ed.). Novos olhares, novos saberes sobre a Serra do Japi: ecos de sua biodiversidade. Curitiba: CRV. In press.). In our study, ichthyofauna sampled in 8 streams represented a high percentage of orders (67%), families (82%), genera (50%) and species (47%) also surveyed by Rolla (2008)ROLLA, APPR., 2008. A ictiofauna da Serra do Japi (SP): bases para conservação. São Paulo: Instituto de Pesca. 177 p. Dissertação de Mestrado em Aquicultura e Pesca. at fifteen collection stations of Japi Mountain.

Brazilian freshwater fishes are classified in nine orders, six of which occur in the streams of the Atlantic Forest (Oyakawa et al., 2006OYAKAWA, OT., AKAMA, A., MAUTARI, KC. and NOLASCO, JC., 2006. Peixes de riachos da Mata Atlântica nas Unidades de Conservação do Vale do Ribeira de Iguape no Estado de São Paulo. São Paulo: Neotropica.; Menezes et al., 2007MENEZES, NA., WEITZMAN, SH., OYAKAWA, OT., LIMA, FCT., CASTRO, RM. and WEITZMAN, MJ., 2007. Peixes de água doce da Mata Atlântica: lista preliminar das espécies e comentários sobre conservação de peixes de água doce Neotropicais. São Paulo: MZUSP.). Characiformes, Siluriformes, Cyprinodontiformes, Synbranchiformes and Perciformes are broadly distributed worldwide and Gymnotiformes order presents distribution limited to Nearctic and Neotropical regions (Lévêque et al., 2008LÉVÊQUE, C., OBERDORFF, T., PAUGY, D., STIASSNY, MLJ. and TEDESCO, PA., 2008. Global Diversity of Fish (Pisces) in Freshwater. Hydrobiologia, vol. 595, no. 1, p. 545-567. http://dx.doi.org/10.1007/s10750-007-9034-0.
http://dx.doi.org/10.1007/s10750-007-903...
).

With identification refinement, it is noticed that Japi Mountain streams preserve broadly distributed genera and species nationwide (Callichthys callichthys, Trichomycterus, Rhamdia quelen, Astyanax, Hoplias malabaricus), species only distributed in the eastern and southeastern basins of the country (Phalloceros harpagos and Geophagus brasiliensis), and species limited to the basins of Alto Paraná, Tietê, Paraíba do Sul and Paranapanema rivers (Hypostomus ancistroides, Oligosarcus paranensis, Astyanax paranae, Characidium, Phalloceros reise) (Buckup et al., 2007BUCKUP, PA., MENEZES, NA. and GHAZZI, MS., 2007. Catálogo das espécies de peixes de água doce do Brasil. Rio de Janeiro: Museu Nacional.; Lucinda, 2008LUCINDA, PHI., 2008. Systematics and biogeography of the genus Phalloceros Eigenmann, 1907 (Cyprinodontiformes: Poeciliidae: Poeciliinae), with the description of twenty-one new species. Neotropical Ichthyology, vol. 6, no. 2, p. 113-158. http://dx.doi.org/10.1590/S1679-62252008000200001.
http://dx.doi.org/10.1590/S1679-62252008...
). It is noteworthy to point out that Japi Mountain streams also collaborated to conserve endangered species of armored catfish in São Paulo state - Neoplecostomus paranensis and Pareiorhina cf rudolphi.

Although anurans are not a target in the collection methodology, they were occasionally caught with the fish. From four identified species (Table 3), Vitreorana eurygnatha deserves attention because it was believed to be extinct in the region (Ribeiro et al., 2005RIBEIRO, RS., EGITO, GTBT. and HADDAD, CRB., 2005. Chave de identificação: anfíbios anuros da vertente de Jundiaí da Serra do Japi, Estado de São Paulo. Biota Neotropica, vol. 5, no. 2. Available from: <http://www.biotaneotropica.org.br/v5n2/pt/abstract?identification-key+bn03005022005>.
http://www.biotaneotropica.org.br/v5n2/p...
). Tadpoles of this Centrolenidae species were collected in stream stretches located on Santa Marta Farm (CG1) and at Dog (CG2), outside the area destined to the Biological Reserve of Japi Mountain. From the data published by Ribeiro et al. (2005)RIBEIRO, RS., EGITO, GTBT. and HADDAD, CRB., 2005. Chave de identificação: anfíbios anuros da vertente de Jundiaí da Serra do Japi, Estado de São Paulo. Biota Neotropica, vol. 5, no. 2. Available from: <http://www.biotaneotropica.org.br/v5n2/pt/abstract?identification-key+bn03005022005>.
http://www.biotaneotropica.org.br/v5n2/p...
and Araújo et al. (2009)ARAÚJO, OGS., TOLEDO, LF., GARCIA, PCA. and HADDAD, CFB., 2009. The amphibians of São Paulo State, Brazil amphibians of São Paulo. Biota Neotropica, vol. 9, no. 4, p. 197-209. http://dx.doi.org/10.1590/S1676-06032009000400020.
http://dx.doi.org/10.1590/S1676-06032009...
, it is verified that Japi Mountain contributes to the preservation of approximately 14% (31 out of 225 species) of anuran amphibians recorded in São Paulo state (Table 4).

Concluding remarks - The Japi Mountain (Environmental Protection Areas of Jundiaí and Cabreúva municipalities) is effective in the conservation of aquatic fauna, comprising 138 taxonomic units and showing a rich and representative biodiversity of the freshwater fauna of the world (0.2%), Neotropical region (0.9%), Brazil (2.4%) and São Paulo state (17.9%). The streams of these Environmental Protection Areas help the conservation of taxa listed as vulnerable in the state of São Paulo, such as the fish species Neoplecostomus paranensis and Pareiorhina cf rudolphi. These areas also comprise important habitats for freshwater crustaceans, aquatic insects and fish of restrict distribution in South America and in restrict basins of Brazil. The importance of Japi Mountain for the conservation of stream fauna is also emphasised when the occurrence of unknown or believed to be extinct species in the studied streams, like the coleopteran Huleechius and the anuran Vitreorana eurygnatha, are considered. Thus, this species inventory emphasises the importance of conservation actions of the freshwater environments of this Biosphere Reserve of Atlantic Forest.

Acknowledgements - We are grateful to the “Conselho Nacional de Desenvolvimento Científico e Tecnológico” (CNPq – Process Number 142300/2007-1) for the financial support, the anonymous referees for the suggestion to the manuscript and all friends and biology students from Pontifícia Universidade Católica de Campinas (PUC Campinas) who helped us in the field and laboratory procedures.

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Publication Dates

  • Publication in this collection
    May 2014

History

  • Received
    12 Dec 2012
  • Accepted
    20 Feb 2013
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