Fishes of Paranaguá Estuarine Complex, South West Atlantic

Peixes do Complexo Estuarino de Paranaguá, Atlântico Sul Oeste

INVENTORIES

Fishes of Paranaguá Estuarine Complex, South West Atlantic

Peixes do Complexo Estuarino de Paranaguá, Atlântico Sul Oeste

Ana Carolina dos Passos^I,*; Riguel Feltrin Contente^II; Ciro Colodetti Vilar de Araujo^III; Felippe Alexandre Lisboa de Miranda Daros^IV; Henry Louis Spach^V; Vinícius Abilhôa^VI; Luis Fernando Fávaro^VII

^ILaboratório de Biologia de Peixes, Programa de Pós-graduação em Sistemas Costeiros e Oceânicos, Departamento de Ciências da Terra, Centro de Estudos do Mar, Universidade Federal do Paraná - UFPR, CP 50002, CEP 83255-000, Pontal do Paraná, PR, Brasil

^IILaboratório de Ecologia Reprodutiva, Instituto Oceanográfico, Universidade de São Paulo-USP, CEP 05508-120, São Paulo, SP, Brasil

^IIIPrograma de Pós-graduação em Ecologia e Conservação, Universidade Federal do Paraná - UFPR, CP 19031, CEP 81531-980, Curitiba, PR, Brasil

^IVLaboratório de Biologia de Peixes, Programa de Pós-graduação em Zoologia, Departamento de Ciências da Terra, Centro de Estudos do Mar, Universidade Federal do Paraná - UFPR, CP 50002, CEP 83255-000, Pontal do Paraná, PR, Brasil

^VLaboratório de Biologia de Peixes, Departamento de Ciências da Terra, Centro de Estudos do Mar, Universidade Federal do Paraná-UFPR, CP 50002, CEP 83255-000, Pontal do Paraná, PR, Brasil

^VILaboratório de Ictiologia, Museu de História Natural Capão da Imbuia, Secretaria Municipal do Meio Ambiente, Prefeitura Municipal de Curitiba, CEP 82810080, Curitiba, PR, Brasil

^VIILaboratório de Reprodução e Comunidade de Peixes, Universidade Federal do Paraná - UFPR, CP 19031, CEP 81531-980, Curitiba, PR, Brasil

ABSTRACT

The objective of this work was to present an updated checklist of the currently known fishes in the Paranaguá Estuarine Complex (PEC) and provides comments on conservation status for the treated species. We used a large dataset derived from a pool of studies which have been conducted within there along the last 30 years. Each study was based on monthly samplings and conducted in several estuarine habitat; thus, the pool covers practically all estuarine habitats and takes into account the seasonal cycle in the system. The PEC ichthyofauna represents a mixture between that fauna typical from the tropical Brazilian coast and that with affinities of temperate Argentinean and Uruguayan zones. The PEC harbors a rich fish fauna of 213 species, inserted in the families that are common along the Brazilian coast. Only a minor part (8%) of the PEC fish fauna was evaluated as regards the conservation status, mostly because of the lack of basic biological and ecological information for most species. Despite part of the among-estuaries differences are due to different and incomplete sampling efforts, the richness in the PEC is surprisingly higher than other systems in Brazil and around world, which emphasize the importance of the region for global biodiversity conservation.

Keywords: ichthyofauna, species list, Paraná, West Atlantic.

RESUMO

O objetivo deste trabalho é apresentar uma lista de espécies atualizada a partir do conhecimento atual dos peixes no Complexo Estuarino de Paranaguá (CEP), com comentários sobre o status de conservação das espécies. Nós utilizamos um grande conjunto de dados derivados de diversos estudos conduzidos na região ao longo dos últimos 30 anos. Cada estudo foi baseado em amostragens mensais realizadas em diferentes habitats estuarinos. Dessa forma, os dados abrangem praticamente todos os habitats estuarinos e leva em conta o ciclo sazonal no sistema. A ictiofauna do CEP representa uma mistura entre a fauna típica da costa tropical brasileira e da fauna com afinidade com as zonas temperadas argentinas e uruguaias. O CEP abriga 213 espécies, inseridas em famílias que são comuns ao longo da costa brasileira. Apenas uma pequena parte (8%) das espécies foi avaliada quanto ao status de conservação, principalmente por causa da falta de informações biológicas e ecológicas básicas para a maioria das espécies. Apesar de parte das diferenças entre estuários ser devido a diferentes e incompletos esforços amostrais, a riqueza do CEP é surpreendentemente elevada em comparação com outros sistemas do Brasil e ao redor do mundo, o que enfatiza a importância da região para a conservação da biodiversidade global.

Palavras-chave: ictiofauna, lista de espécies, Paraná, Atlântico Oeste.

Introduction

The Paranaguá Estuarine Complex (PEC), situated on the coast of Paraná state (Brazil) (25º 16' and 25º 34' S and 48º 17' and 48º 42' W), represents the southern sector of one of the last and least impacted, large Brazilian coastal ecosystems, the subtropical Iguape-Cananéia-Paranaguá estuarine system. This system harbors an important biodiversity, as it is inserted in a global biodiversity hotspot, the southern sector of Brazil's Atlantic Forest Biosphere Reserve (Diegues 1995), and an abundance of socio-economically important fishery stocks (Lana et al. 2001). Several surveys and ecological studies on the fish fauna, most of which based on a monthly sampling design including a diversity of estuarine habitats, have been conducted in the PEC along the last 30 years (e.g. Corrêa et al. 1986, Spach et al. 2003, Félix et al. 2007, Queiroz et al.2007, Schwarz Junior. et al.2007, Barletta et al.2008, Contente et al. 2011). Sampling several areas within several temporal scales increases the species detectability and, thus, our ability to estimate the species richness of a given system (Magurran 2003); thus, such robust spatio-temporal information included in the data derived from the pool of these studies provide a unique opportunity to produce a full list of fish species for this system. A compilation of this nature has twofold: (I) helping to improve our understanding on the geographical distribution and macro-ecological traits of the SW Atlantic estuarine fishes (Barletta & Blaber 2007); and (II) supporting conservation efforts (Barletta et al. 2010). Particular concern must be placed to the region's fish biodiversity that is faced to serious treats, notably due to overfishing, introduction of non-native species, and habitat loss (Lana et al. 2001, Vitule et al. 2006, Caires et al. 2007), and a full check-list of species may be an important tool in impact assessments. For instance, dredgings and buildings of ports result in large impact and an ecosystem scale check-list may serve as a parameter against which the potentially affected pattern of the fish fauna may be compared, thus helping to assess the strength of impact (Sheaves 2006, Barletta et al. 2010). The objective of the present work is, therefore, to present an updated checklist of the currently known fishes in the PEC. Additionally, we provided comments on conservation status for the treated species.

Materials and Methods

1. Study area

The PEC (Figure 1) has an area of 612 km² (see map in Lana et al. 2001) characterized by distinct areas and densities of drainage, tidal flats and mean depths (Noernberg et al. 2004). The system has a diversity of habitats, like tidal flats, channels, mangroves (mainly composed by Rhizophora mangle, Avicennia schaueriana, Laguncularia racemosa, and Conocarpus erectus; Lana et al. 2001) fringed by Spartina alterniflora bank salt-marshes, tidal creeks, estuarine beaches, rivers, and rock shores near the mouth of the estuary. The PEC, a partially mixed estuary with semidiurnal tides and diurnal inequality (Knoppers et al. 1987), is connected to the Cananéia Estuarine Complex, in the north, by the Ararapira Channel and to the Atlantic Ocean, in the east, by Sueste Channel and Galheta Channel. The climate of the region is tropical (transition), with a mean annual rainfall of 2500 mm (maximum 3500 mm). The rainy season typically starts at the end of spring and lasts until nearly the end of summer. The dry season lasts from the end of autumn to the end of winter, but is interrupted by a short low-intensity rainy period that occurs at the beginning of winter (Lana et al. 2001). To further details on the system, see Lana et al. (2001) and Marone et al. (2005).

2. Data collection and treatment of the data

This work is based on the compilation of data from unpublished PhD thesis and master dissertations (i.e. Abilhôa 1998, Pinheiro 1999, Fávaro 2004, Nakayama 2004, Stefanoni 2007, Pichler 2009) and from the literature dealing with the PEC fish community (e.g. Corrêa et al. 1986, Godefroid et al. 1997, 1999, Santos et al. 2002, Vendel et al. 2002, Spach et al. 2003, Vendel et al. 2003, Spach et al. 2004a, b, 2006, Félix et al. 2007, Queiroz et al.2007, Schwarz Junior et al.2007, Barletta et al. 2008, Oliveira Neto et al. 2008, Pichler et al.2008, Cortellete et al.2009, Hackradt et al.2009, Ignácio & Spach 2009, Contente et al. 2011). It is important to highlight that this study is representative of most habitats (e.g. tidal flats, channels, vegetated wetlands, tidal creeks, estuarine beaches, rivers) and the extension of the system, i.e., from the representative, upper tidal freshwater reaches (like upper Antonina Bay Estuary and upper Guaragaçu River Estuary) to the mouths of the estuary (like Pontal do Sul and Ilha das Peças beaches). Practically all studies were took place with monthly samplings along the seasonal cycle. The species in this study were reviewed as regards the taxonomic classification and the nomenclature based on Marceniuk (2005), Craig & Hastings (2007), Smith & Craig (2007), Eschmeyer (2010), Carvalho-Filho et al. (2010), Figueiredo et al. (2010), and Menezes et al. (2010). Mugil sp. was used for the species usually identified under the invalid name Mugil gaimardianus (Menezes et al. 2003). The orders and families were listed in phylogenetic order according to Eschmeyer (2010) and the species were organized within each family in alphabetical order. To analyze zoogeographic affinities, the distribution of each species was verified from the literature and then inserted into the adapted categories based on Floeter et al. (2008) and Luiz Junior et al. (2008) as follows: CT = Circumtropical, TA = Trans-Atlantic (western and eastern Atlantic Ocean), WA = Western Atlantic (northern and southern Atlantic Ocean), SWA = Southern West Atlantic (from northern Brazil to Argentina), SSWA = Southern South West Atlantic (species with temperate affinities occurring from Argentina and Uruguay to the south and southeast of Brazil), Ca = Caribbean (from Florida state to Venezuela), Br = Brazilian Province (area between the Orinoco Delta in Venezuela and Santa Catarina in Brazil), EA = Eastern Atlantic and EP = Eastern Pacific. The status of species conservation was based both on the International Union for Conservation of Nature list (International... 2012) and the Ministry of the Environment list for endangered fauna (Brasil 2004, 2008).

Results and Discussion

The ichthyofauna of the PEC consists of 213 species, distributed in 21 orders and 65 families (Table 1). A total of 97% (208 spp.) are Actinopterygii and 3% (5), Elasmobranchii. Twenty species (i.e. H. robertii, O. vespertilio, A. clupeoides, A. januaria, G. ocellatus, S. brasiliensis, S. plumieri, A. brasilianus, M. bonaci, L. synagris, A. probatocephalus, C. penna, P. cromis, U. parvus, G. brasiliensis, E. pisonis, S. picudilla, A. solandri, P. patagonicus and T. microphthalmus) were recorded for the first time for the PEC. Perciformes (116) dominated in number of species, followed by Clupeiformes (20), Pleuronectiformes (17), and Syngnathiformes (8). The most speciose family was Sciaenidae (23), followed by Carangidae (17), Engraulidae (12), Gobiidae (9), Haemulidae (9), and Paralichthyidae (9). This is supported by Andrade-Tubino et al. (2008) that state such families among the most important in Brazilian coast, and by Vieira & Musick (1994), which reveal them as the most conspicuous in SW Atlantic estuarine fish assemblages. Carangidae and Sciaenidae were also the two most speciose families in the two large estuaries near the PEC, the Guaratuba Bay, located just south of the PEC, and the Babitonga Bay, located 70 Km south of the PEC (Chaves & Corrêa 1998, Chaves & Vendel 2001, Vilar et al. 2011). Anchoa and Cynoscion had six species each and were the richest genera in the PEC. The following were Mugil, with five species, and Ctenogobius, Paralichthys, Sphoeroides, Sphyraena and Trachinotus, with four species each. This pattern was not found in such nearby estuaries, as Ctenogobius, followed by Eucinostomus and Oligoplites were the richest genera in Guaratuba (Chaves & Corrêa 1998, Chaves & Vendel 2001), and Mycteroperca, Mugil, Anchoa, Cynoscion, Eucinostomus and Sphoeroides were those most rich in Babitonga (Vilar et al. 2011). Comparing the species composition of PEC with that of Babitonga and Guaratuba estuaries reveals a relatively low number shared (just 35%) and relatively a high number of exclusive species (about 40%) of the PEC. This is unexpected because the distribution for most species occurring in all such estuaries overlaps. Such taxonomic differences are most likely due to differences in number of fish survey as well as in fish sampling gear and strategies (see discussion below).

In terms of number of species, the total species richness in the PEC is higher than those reported for large estuaries in Western Atlantic [Guaratuba Bay, southern Brazil (87 spp.; Chaves & Corrêa 1998, Chaves & Vendel 2001); Río de la Plata estuary, northern Argentina (60 spp.; Jaureguizar et al. 2004); Caeté River estuary, northern Brazil (82spp.; Barletta et al. 2005), Sergipe River estuary (136 spp.; Alcântara 2006), Curuçá estuary (98 spp.; Hercos 2006, Giarrizzo & Krumme 2007, Sarpedonti et al. 2008), Babitonga Bay (152 spp.; Vilar et al. 2011), Estuary of Mataripe area (36 spp.; Dias et al. 2011) and Paraguaçu River estuary (124 spp.; Reis-Filho et al. 2010)] as well as for other large, permanently open, tropical estuaries around world (number of species ranging from 81 to 197, Blaber 2002), including those of estuaries from the species-rich Indo Pacific biogeographical zones. Moreover, the PEC has a comparable fauna to large coastal ecosystems, like Gulf of Carpentaria (237 spp.) (Blaber et al. 1990) and Embley estuary (203 spp.) (Barletta & Blaber 2007), which has a large diversity of estuarine habitats, similar to that of PEC. These differences in richness and taxonomic composition may be difficult to explain. Multiple area specific synergic factors act in determining fish fauna patterns, including diversity of estuarine habits, rainfall pattern, hydrograph, oceanographic patterns, and historic dispersion pattern of taxa and so on. These operate in different intensity and scale, producing very distinct fish fauna patterns. For example, in a continental scale, the estuarine area may be critical to determine the fish richness in accordance with the species-area theory. This theory states that, the larger a given system, the larger the number of species, because the number of habitat tend to increase with the area. In fact, the PEC is larger (612 km²) than the Guaratuba Bay (48 km²), Babitonga Bay (130 km²), Sergipe River estuary (47.1 km²) and Paraguaçu River estuary (127.9 km²) and this may explain, at least in part, the higher richness in PEC. However, a considerable part of such differences among tropical fish faunas can be attributed to the incomplete effort of surveys on all range of estuarine habitats and/or the use of different sampling gears across tropical estuaries around the world (Blaber 2002).

The species' classification into the geographical categories used in this study present here, which were adapted from Floeter et al. (2008) and Luiz Junior et al. (2008), fits well with the species' distribution described on the literature. This is an indicative of utility of such a classification for future studies aiming to classify SW Atlantic estuarine fishes. Most species in the PEC are widely distributed throughout the Western Atlantic (40%), followed by those that are restricted to (and occur both in) the Caribbean and Brazilian (15%), and South-West Atlantic (11%) provinces (Figure 2). Thus, the PEC fish fauna can be regarded as a mixture between the fish fauna typical from the tropical Brazilian coast and those with affinities of temperate Argentinean and Uruguayan zones.

Our results suggest an expansion of the geographical distribution for G. pygmaeus and M. auratus. G. pygmaeus, recorded in Godefroid et al. (1997, 1999), which was previously reported only for the tropical Western Atlantic, from South Carolina state to the tropical coast of Brazil, near the equator (Eschmeyer 2010), and Mullus auratus, recorded by Barletta et al. (2008), previously reported from North Carolina, USA, to the Caribbean (Floeter et al. 2008).

Only a minor part (8%) of the PEC fish fauna was evaluated as regards the conservation status: ten are on the IUCN Red List (International... 2012), 12 on the ME list (Brasil 2004, 2008), and four are on both. Of the ten species on the IUCN Red List (International... 2012), two (Epinephelus itajara and Hyporthodus nigritus) are critically endangered, one (Mycteroperca bonaci) is near threatened, one (Lutjanus analis) is vulnerable, five (Alphestes afer, Mycteroperca rubra, Acanthocybium solandri, Scomberomorus brasiliensis and S. cavalla) are least concern and one (Hippocampus reidi) is data deficient. Among the 12 species on the Ministry of the Environment List, 11 are overexploited and one is endangered (Rhinobatus horkelii). Many fishery species in PEC are found to be classified as threatened on the list for endangered fauna of the adjacent state of São Paulo (São Paulo 2010). It is supposed that many species in PEC have similar conservation status 'threatened' as face similar threats to those of São Paulo state coast, where the fishing pressure is similar to that of Paraná state. Such a setting reinforces the urgent need for critical, basic information for fish species to support their conservation effort through IUCN classification in this important estuary.

Particular concern must be place to introduction in the PEC of the species Opsanus beta, from the North Atlantic (Eschmeyer 2010), and Oreochromis niloticus from Africa. Although the impact of O. beta on the native fish fauna is still unknown (Caires et al. 2007), it is supposed to be serious, as it is a voracious, generalized predator (Gray & Winn 1961). Moreover, recent field observations have already reported O. beta as a very common by-catch in long-line inside estuary, thus affecting local fisheries. O. niloticus is classified as a pest and has been reported to adversely impact ecosystem after its introduction (Froese & Pauly 2010). Future studies assessing the degree of establishment success of such species and their impact on the local fish biodiversity are strongly recommended.

This study provides a full list of fish species of the Paranaguá Estuarine Complex based on a robust dataset, which takes into account a wide and representative spatio temporal variability, largely improving the species detectability. The ichthyofauna of the PEC contains taxa with affinities from the tropical Brazilian coast and those with affinities of temperate Argentinean and Uruguayan waters. The fish richness of the system of 213 species is surprisingly higher than other systems in Brazil and around world, which emphasize the importance of the region for global biodiversity conservation. Once we have knowledge of the species and the richness of PEC, we suggest a fauna monitoring for a regional analysis of conservation status and more details about impacts of exotic species for the creation of management and conservation proposals.

Acknowledgements

We would like to thank the CEM Geological Oceanography Laboratory for the map data base and Pâmela Emanuelly Cattani for their valuable help with the map. Funding was provided by CAPES foundation through a master grant to Ana Carolina dos Passos.

Received 21/01/2011

Revised 13/03/2012

Accepted 02/08/2012

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Publication Dates

• Publication in this collection
  08 Nov 2012
• Date of issue
  Sept 2012

History

• Received
  21 Jan 2011
• Accepted
  02 Aug 2012
• Reviewed
  13 Mar 2012