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Diversidad de especies y distribucion de cangrejos de agua dulce (Decapoda: Pseudothelphusidae) de la cuenca del Rio Grande de Terraba, vertiente Pacifica de Costa Rica.

Species diversity and distribution of freshwater crabs (Decapoda: Pseudothelphusidae) inhabiting the basin of the Rio Grande de Terraba, Pacific slope of Costa Rica

INTRODUCTION

Knowledge and literature about the taxonomic diversity of decapod crustaceans has increased considerably during the last decades (Ng et al., 2008). Most of these publications focused on decapods inhabiting marine ecosystems; however, there has been also a significant increase in studies concerning freshwater decapods, including representatives of the two families of Brachyura from the neotropical region (among others, Magalhaes, 2003a, 2003b; Rodriguez & Magalhaes, 2005; Magalhaes & Turkay, 2008a, 2008b; Yeo et al., 2008; Cumberlidge et al., 2009; Pereira et al., 2009; Villalobos & Alvarez, 2010). Currently, there are approximately 6,800 valid species of brachyuran crabs and about 1,300 (19.4%) of these have been reported from freshwater habitats (Ng et al., 2008; Yeo et al., 2008).

The taxonomic composition of the freshwater decapod fauna of Costa Rica is fairly well known and is composed by three families: Palaemonidae and Atyidae (Caridea), and Pseudothelphusidae (Brachyura). The latter includes the freshwater crabs, a very diverse group, which is currently comprised by 40 genera and roughly 255 species and subspecies in the neotropics (Rodriguez & Magalhaes, 2005). Of these, a total of 15 species of four genera can be found in Costa Rica (C. Magalhaes et al., unpublished data.). The vast majority of the studies on freshwater crabs in Costa Rica concerns taxonomic aspects (Rathbun, 1893, 1896, 1898, 1905; Smalley, 1964; Bott, 1968;

Pretzmann, 1965, 1972, 1978, 1980; Villalobos, 1974; Rodriguez, 1982, 1994, 2001; Rodriguez & Hedstrom, 2000; Hobbs III, 1991; Magalhaes et al., 2010). Apart from these, there are just two publications concerning their ecology: one study on the distribution of Potamocarcinus nicaraguensis in the basins of the rivers San Carlos and Sarapiqui, northern Costa Rica (Villalobos & Burgos, 1975), and one report on the offspring production and juvenile occurrence of Potamocarcinus magnus in the Costa Rican territory (Wehrtmann et al., 2010).

Detailed information about species diversity and ecological features of the freshwater decapods fauna is of special importance when evaluating the possible environmental impacts, which may be caused by the construction of dams for hydroelectric plants (Holmquist et al., 1998; Benstead et al., 1999; March et al., 2003; Greathouse et al., 2006). The Instituto Costarricense de Electricidad (ICE) is planning to construct, in the southern Pacific lowlands, one of the largest hydroelectric plants in Central America (ICE, 2009). Lara & Wehrtmann (2011) already analyzed the species composition of river shrimps in this area and recommended the incorporation of structures permitting the passage of the migrating shrimps to mitigate negative effects of the construction of the hydroelectric power plant. Therefore, the present study aimed to amplify the existing information about the freshwater fauna in the study area and to provide basic information on the species diversity and distribution of freshwater crabs inhabiting the area (basin of the Rio Grande de Terraba), where the ICE plans to implement one of the largest damming projects in the region.

MATERIALS AND METHODS

Study area

The study was carried out in the Rio Grande de Terraba basin, provinces of San Jose and Puntarenas, Pacific slope of Costa Rica (Fig. 1). The basin is the largest in the country and covers an area of 5,085 [km.sup.2]; its rivers have a total length of 4,997 km (TNC, 2009). The principal tributaries are the Rio General and the Rio Coto Brus, which drain into the Rio Grande de Terraba; the discharge of this river (recorded at a station located at an altitude of 60 m above sea level) varies between 100 (dry season) and 1,050 [m.sup.3] [s.sup.-1] (rainy season) (ICE, unpublished data). The drainage area is comprised by numerous other tributary streams originating in the Cordillera de Talamanca at altitudes of up to 3,820 m and is characterized by the formation of a low altitude mountainous ridge, which is oriented parallel to the Pacific coast (TNC, 2009). A description of physical and chemical parameters and the benthic diversity as indicator of the environmental quality of the Rio Grande de Terraba and some tributaries have been presented by Umana-Villalobos & Springer (2006). The area has been characterized by a constantly growing human population, accompanied by strong deforestation, especially in its lower regions (Umana-Villalobos & Springer, 2006), which is also critical for the hydropower sector of Costa Rica (Leguia et al., 2008). The hydroelectric project El Diquis contemplates the construction of a retaining dam, located 4 km upstream of the bridge over the Rio General, at the locality of El Brujo; the base of the dam will be located at 140 m above sea level, and the reservoir will have an area of 6,815 hectares with an installed capacity of 631 megawatts (MW) (ICE, 2009).

[FIGURE 1 OMITTED]

Sampling

The study is based upon exhaustive sampling carried in 39 locations at altitudes (expressed as m above sea level) between 20 and 1,225 m along the entire basin (Fig. 1). Samples were taken in April 2007 through July 2007, between October and November 2009, and in April 2010. In order to describe the presence of each species and its distribution in the study area, the sampling locations were categorized according to its altitude: 1) lower basin (between 20 and 310 m above sea level; n = 12 sampling sites); 2) middle-low basin (between 311 and 600 m above sea level.; n = 14); 3) medium-high basin (between 601 and 1,225 m above sea level.; n =13). In each location, sampling was carried out during daytime (typically between 08:00 and 14:00 h) and lasted between 60 and 90 min. In search of crabs, we lifted rocks directly in or closely to the water body of rivers and streams. In some cases, the stream course was temporarily bypassed to drain a small part of the river or creek, which allowed observations below the rocks in the riverbed. The manually collected individuals were brought to the nearby laboratory in Cajon de Boruca and stored in a freezer for further analysis. At each sampling location, water temperature and dissolved oxygen were measured (YSI Model 85), to obtain information about the environmental conditions where each of the crab species was captured. The catch-per-unit-effort (CPUE) represents the number of crabs divided by the sampling effort (number of visits in each sampling location). The CPUE was related to the altitude of the sampling site, and a linear correlation was applied to analyze the possible correlation between the two variables.

The collected individuals were identified at the species level using descriptions provided by Smalley (1964), Villalobos (1974), Rodriguez (1982, 1994, 2001); Rodriguez & Hedstrom (2000), and Magalhaes et al. (2010). Each crab was sexed, and recorded its wet weight (digital balance; Snowrex BBA-600; [+ or -] 0.01 g), carapace width (CW; distance across the carapace at its widest point), carapace length (CL; distance along the midline, from the frontal to the posterior margin of the carapace) utilizing a digital vernier (Stanley; [+ or -] 0.01 mm). Voucher specimens were deposited in the crustacean collections of the Museo de Zoologia, Universidad de Costa Rica, and the Instituto Nacional de Pesquisas da Amazonia, Manaus, Brazil.

RESULTS

Freshwater crabs were easier to encounter in creeks with low river discharge (<1 [m.sup.3] [seg.sup.-1]) and with a river substrate composed of numerous broken rocks of different sizes (immature alluvial deposits consisting of angular grains of short transport) in areas covered by rich vegetation, providing abundant shading from canopy cover. Several crabs were collected outside the water, mainly under damp or wet rocks and crevices. The sampling locations where crabs were found were well-oxygenated river sections with dissolved oxygen values varying between 5.8-8.7 mg [L.sup.-1] and water temperatures ranging from 19.0 to 28.9[degrees]C (Table 1).

A total of 661 freshwater crabs were collected during the study period in the basin of the Rio Grande de Terraba. Of these, 309 (47.7%) were females, 319 (48.3%) were males, and the sex of 33 (4%) specimens could not be identified. No ovigerous females were encountered; however, two specimens, collected in the Rio Reventazon (305 m above sea level; 23 May 2007), and in an unnamed tributary of the Rio Ceibo (900 m above sea level; 17 July 2007) carried juveniles under the abdomen. All specimens belonged to Pseudothelphusidae, represented by three genera and eight species (Table 1). Ptychophallus was the genus with the highest number of species encountered (5 spp.), followed by Allacanthos (2 spp.) and one species of Potamocarcinus. This is the first report of Ptychophallus colombianus and P. uncinatus from [?] Costa Rica. Taxonomic diversity increased with altitude: the lower basin harbored two crab species, the middle-low basin five species, and the medium-high basin six species.

The most frequently collected species was P. paraxanthusi followed by P. tristani (Fig. 2). In contrast, P. tumimanus was encountered exclusively in one location (creek Veraguas of the sub-basin of Rio Concepcion). There was no significant relationship between the CPUE and altitude (r = -0.16; P = 0.30). However, freshwater crabs were more frequently encountered in the middle-low region of the basin (between 311 and 600 m above sea level) and less frequently in the medium-high basin (between 601 and 1,225 m above sea level).

Only two crab species (P. paraxanthusi and P. uncinatus) were found in the lower portion of the river basin, and P. paraxanthusi was by far the most common species in this section. However, the catch frequency of these two species was higher in this river section compared to the medium-high basin, where six species were found.

The crab species with the widest distribution within the basin of the Rio Grande de Terraba was P. paraxanthusi (collected in altitudes ranging from 20 to 700 m above sea level) (Fig. 3), followed by P. tristani, which was encountered exclusively in tributaries of the Cordillera de Talamanca in altitudes between 410 and 1,105 m above sea level. Other two species, P. tumimanus and P. colombianus, were caught in one single sampling location (creek Veraguas and a nameless tributary of the river Buena Vista, respectively), at 335 and 1,225 m above sea level, respectively (Fig. 4).

Among the collected species, P. paraxanthusi achieved the largest individual size (up to 62.8 mm CW), followed by P. magnus with a maximum CW of 59.2 mm. The smallest individual encountered collected belonged to P. tristani with a CW of 4.6 mm. Detailed information about the range of CL and CW for the species encountered is compiled in Table 1.

DISCUSSION

Species diversity

The results of the present study clearly demonstrate that the freshwater crab diversity of the basin of the river Grande de Terraba is considerably high: the eight species collected by us represent 53% of the 15 pseudothelphusid crab species currently recorded from Costa Rica (C. Magalhaes et al., unpublished data). Rodriguez & Hedstrom (2000) revised a small collection of freshwater crabs from the Barbilla National Park, Atlantic slope of Costa Rica, and reported two species, P. magnus and P. barbillaensis. These results, as well as the fact that only seven out of 15 crab species reported from Costa Rica (C. Magalhaes et al., unpublished data) occur at the Atlantic side of Costa Rica, seem to indicate higher crab diversity in freshwater habitats along the Pacific slope of the country. However, so far no exhaustive sampling efforts have been carried out to document the freshwater crab diversity at the Atlantic slope of Costa Rica, which may partly explain the difference of crab species encountered in the Pacific and Atlantic slopes of the country.

When compared to Central America, our relatively small study area harbors 18% of all pseudothelphusid crab species so far reported from the region (Rodriguez & Magalhaes, 2005), which highlights the ecological importance of the Rio Grande de Terraba basin for the diversity of the freshwater decapods in Costa Rica and Central America. However, the lack of similar studies impedes any valid comparison of the freshwater crab species diversity within the Central American region.

There exists some scattered information about the freshwater crab diversity in South America, which may serve as guideline for comparison with the results of the present study. Magalhaes (2002) assessed the decapod fauna of two rivers, which form part of the Rio Madeira basin, Bolivia. He reported the presence of four freshwater crab species, all of them belonging to the family Trichodactylidae. In another study, Magalhaes (2003b) revised collections obtained in the middle and lower Rio Xingu, southern tributary of the Amazon River, Brazil, and reported a total of five freshwater crab species from this river. Surveys of decapod fauna using the Aquatic Rapid Assessment Program (AquaRAP) protocol in some South American rivers resulted in four species of crabs (one Pseudothelphusidae and three Trichodactylidae) from the upper and middle Rio Caura, Venezuela (Magalhaes & Pereira, 2003), five species (three Pseudothelphusidae, two Trichodactylidae) from the upper Rio Essequibo, Guiana (Lasso et al., 2008), five species (two Pseudothelphusidae, three Trichodactylidae) from the upper Rio Cuyuni, Venezuela (Mora-Day et al., 2009), four species (one Pseudothelphusidae, three Trichodactylidae) from Rio Pastaza, Ecuador and Peru (Magalhaes, 2005), four species (two Pseudothelphusidae, two Trichodactylidae) from upper Rio Paragua, Venezuela (Mora-Day & Blanco-Belmonte, 2008), 12 presumptive species (eight Pseudothelphusidae, four Trichodactylidae) from river drainages of the Tumucumaque Moutains National Park, Brazil (Vieira, 2008), three species (one Pseudothelphusidae, two Trichodactylidae) from the confluence of the Rio Orinoco and Rio Ventuari, Venezuela (Pereira & Garcia, 2006), and three species (one Pseudothelphusidae, two Trichodactylidae) from the middle Coppename River, Suriname (Pereira & Berrestein, 2006). According to Magalhaes & Pereira (2007), the Guayana Shield region, including parts of Colombia, Venezuela, Brazil, Guyana, Suriname and French Guiana, harbors representatives of 33 species of freshwater crabs: 21 species of Pseudothelphusidae and 12 species of Trichodactylidae. Similarly, Pereira et al. (2009) compiled the list of the decapod species from the Rio Orinoco basin, which drains large areas of the Guayana Shield and the Venezuelan Llanos in northern South America, and reported 16 species of pseudothelphusid and five species of trichodactylid crabs for the whole region. These comparisons, especially when taking into consideration the area covered by the above-mentioned studies, reveal that the Rio Grande de Terraba region, with its eight freshwater crab species, can be considered as a relatively small, but highly diverse system. Therefore, any alteration of the basin of the Rio Grande de Terraba, and especially the possible construction of a hydroelectric power plant, needs to be carefully analyzed to mitigate the damaging effects of this project on freshwater crabs (see Lara & Wehrtmann, 2011).

[FIGURE 3 OMITTED]

[FIGURE 4 OMITTED]

New geographical distribution

The results of the present study expand the known geographical distribution of Ptychophallus uncinatus and P. colombianus. The first species was recorded from Rio San Pedro, Bocas del Toro, Panama (Campos & Lemaitre, 1999) and from the Veragua Rainforest Research and Adventure Park, province of Limon, Costa Rica (C. Magalhaes et al., unpublished data); both records are from the Caribbean slope of Costa Rica and Panama, and our results extend its distribution to the Pacific slope of Costa Rica. The presence of this species on both sides of Costa Rica may indicate the ability of P. uncinatus to cross the Central American cordillera; however, this species has been found only at altitudes below 500 m above sea level. Due to these circumstances, studies on the molecular genetics of both populations present on the Caribbean and Pacific slopes are in progress to verify whether we are dealing or not with the same species. In the case of P. colombianus, the species has been previously known only from Pacific Panama, and our results indicate its presence also in Pacific Costa Rica. This range extension is not surprising, considering that Chiriqui (Panama) and our study area belongs to the same cordillera (Talamanca). Moreover, the species has been encountered in a wide range of altitudes (from 1,220 up to 3,000 m above sea level; Rodriguez, 1994), which may facilitate its distribution along the Pacific slope of Central America.

Altitudinal distribution

Our knowledge about the altitudinal distribution of Central American freshwater crabs is generally limited to sporadic collections published in taxonomic studies (e.g., Rathbun, 1898; Smalley, 1964). As far as we know, there are no published reports focusing on the ecology, including altitudinal distribution, of these freshwater crabs.

Allocanthos pittieri seems to be a species preferring higher altitudes, because we collected this species only between 900 and 1,000 m above sea level. This species was described by Rathbun (1898) from Agua Buena, Java, Province Puntarenas, Costa Rica, without mentioning the altitude where the specimens were obtained. Allocanthos yawi is a newly -described species (Magalhaes et al., 2010) found between 505 and 1,105 m above sea level (Table 1).

Our data concerning the altitudinal distribution of P. magnus (380-900 m; Table 1) are in the range of previous reports: Smalley (1964) found the species between 580-800 m above sea level, Rathbun (1896) between 800 and 1,000 m above sea level, and Rodriguez & Hedstrom (2000) encountered the species between 100 and 300 m above sea level. These data indicate that P. magnus, a species inhabiting both slopes of Costa Rica, can be found in a wide range of altitudes.

The altitudes where we collected P. tristani (410-1,105 m above sea level; Table 1) are similar to those reported in the literature: Smalley (1964) found the species between 580-1,200 m above sea level, Rathbun (1896) at 1,130 m above sea level, and Monge et al. (1985) at 700 m above sea level. It is concluded that P. tristani is a species preferring medium altitudes.

Previous records for P. tumimanus indicate its presence in relatively high altitudes (Rathbun, 1898: up to 1,500 m above sea level; Smalley, 1964: 1,200-1,300 m above sea level). In contrast, we collected the species only in one location at a considerably lower altitude (335 m above sea level; Table 1), which seems to indicate that P. tumimanus inhabits a wide range of altitudes.

Habitat

Detailed information about the habitat of freshwater crabs in Latin America is scarce and typically limited to general descriptions of the study area. In our study, crabs were encountered under angular rock fragments of short distance transport; these rocks may be located in the riverbed or in the shore close to the terrestrial zone, but always in humid ground. Water bodies with slow stream flow turned out to be good areas to collect freshwater crabs (see Smalley, 1964, for other Ptychophallus spp.). Freshwater crabs were also collected in shallow pools below logs, and in accumulations of leaves.

In the case of P. colombianus, we found the specimens in rapid streams descending from nearby mountains (e.g., Rio Buena Vista), which is in agreement with habitat descriptions provided by Rodriguez (1994) for individuals collected in Panama. Smalley (1964) obtained P. tristani under rocks or tree trunks at the edge of streams, sometimes even in some distance from the stream edge. Crab burrows of this species might be located under rocks or logs and are filled with water (Smalley, 1964). These descriptions coincide with the habitat where we collected P. tristani.

Final remarks

The knowledge of freshwater communities contributes to resolve questions related to the evolution, speciation, and distribution of living organisms (Mossolin & Mantelatto, 2008). In particular, freshwater crabs may serve as research objects to understand the interesting evolutionary patterns along their distribution. However, much of the necessary biological information about these decapods is far from complete, and we need to improve our knowledge about freshwater crabs from Costa Rica and the Central American region to reach a first reasonable overview on the ecological role of these decapods in freshwater systems.

DOI: 103856/vol41-issue4-fulltext-5

ACKNOWLEDGMENTS

The study was financially supported by The Hydroelectric Project El Diquis-ICE (PHED), as well as Prime Catch Seafood GmbH, Germany, and the German Investment and Development Company (Deutsche Investitions und Entwicklungsgesellschaft, DEG) within the Public-Private-Partnership project E 2118. We thank the Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPq--Brazil, Procs. 491490/2004-6, 490353/2007-0 and 490314/ 2011-2) and CONICIT-Costa Rica (CII-001-08), during the development of the International Cooperative Project, which provided financial support to FLM, CM and ISW during the Brazil-Costa Rica visiting program, making possible the analysis of material and discussions. Two of us (CM and FLM) also thank CNPq for an ongoing research grant (Proc. no. PQ-304468/2009-6, 303837/2012-8 and 302748/ 2010-5, respectively). We are grateful to Jorge Picado (ICE) for the technical support during the fieldwork. Luis Salazar, Leonel Delgado, Yonder Guzman, Edgar Chinchilla, Carlos Canales and Diego Valerin helped us during the fieldwork, and Raquel Romero-Chaves (UNIP-CIMAR, UCR) prepared the distribution maps, which is greatly appreciated.

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Received: 19 June 2012; Accepted: 5 September 2012

Luis Rolier Lara (1,2), Ingo S. Wehrtmann (3,4), Celio Magalhaes (5) & Fernando L. Mantelatto (6)

(1) Instituto Costarricense de Electricidad, Proyecto Hidroelectrico El Diquis, Puntarenas, Costa Rica

(2) Present address: Compania Nacional de Fuerza y Luz, S.A., San Jose, Costa Rica

(3) Museo de Zoologia, Escuela de Biologia, Universidad de Costa Rica, 2060 San Jose, Costa Rica

(4) Unidad de Investigacion Pesquera y Acuicultura (UNIP), Centro de Investigacion en Ciencias del Mar y Limnologia (CIMAR), Universidad de Costa Rica, 2060 San Jose, Costa Rica

(5) Instituto Nacional de Pesquisas da Amazonia, Caixa Postal 478, 69011-970 Manaus, AM, Brazil

(6) Laboratory of Bioecology and Crustacean Systematics (LBSC), Department of Biology Faculty of Philosophy, Sciences and Letters of Ribeirao Preto (FFCLRP) University of Sao Paulo (USP), Postgraduate Program in Comparative Biology, Avenida Bandeirantes 3900 CEP 14040-901, Ribeirao Preto, SP, Brazil

Corresponding author: Ingo S. Wehrtmann (ingowehotmann@gmx.de)
Table 1. Species list of freshwater crabs collected during 2007 and
2010 in the Rio Grande de Terraba basin, Pacific slope of Costa Rica,
indicating wet weight, size (all individuals per species), number of
locations where the species was collected, and environmental
conditions for each of the species encountered. CL: carapace length,
CW: carapace wide.

Species                      Range of wet   Range of    Range of
                              weight (g)     CL (mm)     CW (mm)

Allacanthos pittieri           0.8-4.9      11.0-16.6   15.6-28.8
(Rathbun, 1896)
Allacanthos yawi               0.2-4.3      7.1-16.3    10.4-28.5
Magalhaes et al. (2010)
Potamocarcinus magnus          0.1-47.6     7.5-39.2    9.9-59.6
(Rathbun, 1896)
Ptychophallus uncinatus        0.1-10.3     6.6-22.3    9.4-39.2
Campos & Lemaitre, 1999
Ptychophallus colombianus      0.2-7.7      7.3-20.8    11.9-35.2
(Rathbun, 1896)
Ptychophallus paraxanthusi     0.1-42.9     3.7-37.7    5.6-62.8
(Bott, 1968)
Ptychophallus tristani         0.1-12.5     3.4-22.9    4.6-38.3
(Rathbun, 1896)
Ptychophallus tumimanus        0.3-4.6      7.3-18.0    10.8-28.2
(Rathbun, 1898)

Species                      Number of    Range of
                             collection   altitude
                               places       (m)

Allacanthos pittieri             3        900-1000
(Rathbun, 1896)
Allacanthos yawi                 2        920-1105
Magalhaes et al. (2010)
Potamocarcinus magnus            3        380-900
(Rathbun, 1896)
Ptychophallus uncinatus          3         20-500
Campos & Lemaitre, 1999
Ptychophallus colombianus        1         1200 *
(Rathbun, 1896)
Ptychophallus paraxanthusi       26        20-715
(Bott, 1968)
Ptychophallus tristani           8        410-1105
(Rathbun, 1896)
Ptychophallus tumimanus          1         335 *
(Rathbun, 1898)

Species                      Range of water      Range of
                              temperature     dissolved oxygen
                              ([degrees]C)    (mg [L.sup.-1])

Allacanthos pittieri               nd                nd
(Rathbun, 1896)
Allacanthos yawi               19.8-21.8          7.8-8.4
Magalhaes et al. (2010)
Potamocarcinus magnus          22.3-25.4          7.4-7.7
(Rathbun, 1896)
Ptychophallus uncinatus        25.9-26.2          7.2-8.1
Campos & Lemaitre, 1999
Ptychophallus colombianus          19               8.7
(Rathbun, 1896)
Ptychophallus paraxanthusi     22.6-26.9          6.9-8.7
(Bott, 1968)
Ptychophallus tristani         20.7-24.1          5.8-8.4
(Rathbun, 1896)
Ptychophallus tumimanus        23.2-28.9          7.5-8.8
(Rathbun, 1898)

* This species was collected in one single location.

Figure 2. Percentage per species regarding the total
number of collected individuals captured between April
2007 and April 2010 in the Rio Grande de Terraba basin,
Pacific slope of Costa Rica. Numbers in top of each
column indicate the number of individuals per species.

                  Percentage of collected individuals
                             (% of total)

P. paraxanthusi                   432
P. tristani                        71
P. colombianus                     61
A. yawi                            44
P. magnus                          22
P. uncinatus                       16
A. pittieri                         9
P. tumimanus                        6

Note: Table made from bar graph.
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Title Annotation:articulo en ingles
Author:Rolier Lara, Luis; Wehrtmann, Ingo S.; Magalhaes, Celio; Mantelatto, Fernando L.
Publication:Latin American Journal of Aquatic Research
Date:Sep 1, 2013
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