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Latin american journal of aquatic research

On-line version ISSN 0718-560X

Lat. Am. J. Aquat. Res. vol.42 no.3 Valparaíso July 2014

 

Research Article

 

Distribution and feeding habits of three sea robin species (Bellator brachychir, Prionotus nudigula and Prionotus punctatus ) in the Campos Basin, southeastern Brazil

Distribución y hábitos alimentarios de tres especies de rubio (Bellator brachychir, Prionotus nudigula y Prionotus punctatus) en la cuenca de Campos, sureste de Brasil

 

Ricardo R.B. de São Clemente1, Paulo A.S. Costa1 & Agnaldo S. Martins2

1 Universidade Federal do Estado do Rio de Janeiro, Laboratório de Dinâmica de Populações Marinhas Departamento de Ecologia e Recursos Marinhos, IBIO, Av. Pasteur, 458 - sala 410, Urca Rio de Janeiro, RJ, 22290-240, Brazil.
2 Universidade Federal do Espírito Santo, Departamento de Oceanografia e Ecologia
Vitória, 29075-910, ES, Brazil.
Corresponding author: Ricardo Raphael Bastos de São Clemente (rrbsc17@hotmail.com)


ABSTRACT. The distribution, size structure, and feeding of three sea robin species belonging to the family Triglidae (Bellator brachychir, Prionotus nudigula and Prionotus punctatus) were studied based on specimens caught with bottom trawls on the continental shelf of Campos Basin, southeastern Brazil. The two Prionotus species were more concentrated in the inner shelf (<50 m), while B. brachychir was generally more abundant on the outer shelf (50-100 m). In general, the three species showed a carcinophagous diet, but with small overlap in their main preys. While amphipods was the most important prey to B. brachychir, isopods and shrimps were the basic food item found in P. nudigula and P. punctatus diet, respectively. This reduction in interspecific competition for food was followed by some degree of spatial segregation and thermal preferences for each species.

Keywords: sea robin, Triglidae, distribution, feeding ecology, Campos Basin, southeastern Brazil.


RESUMEN. La distribución, estructura de tamaños, y la alimentación de tres especies de rubio pertenecientes a la familia Triglidae (Bellator brachychir, Prionotus nudigula y Prionotus punctatus) se estudiaron sobre la base de ejemplares capturados con redes de arrastre de fondo en la plataforma continental de la cuenca de Campos, en el sureste de Brasil. Las dos especies de Prionotus estaban más concentradas en la plataforma interior (<50 m), mientras que B. brachychir fue generalmente más abundante en la plataforma exterior (50-100 m). En general, las tres especies mostraron una dieta carcinófaga, pero con pequeño solapamiento en sus principales presas. Los anfípodos fueron la presa más importante de B. brachychir, los isópodos y camarones fueron el alimento básico encontrado en la dieta de P. nudigula y P. punctatus, respectivamente. Esta reducción de la competencia interespecífica por alimentos fue seguida por un cierto grado de segregación espacial y preferencias térmicas para cada especie.

Palabras clave: rubio, Triglidae, distribución, ecología alimentaria, cuenca de Campos, sureste de Brasil.


 

INTRODUCTION

Family Triglidae, known as sea robins, includes 105 species distributed in 10 genera (Nelson, 2006). The three species that occur in Brazil, Bellator brachychir (Regan, 1914), Prionotus nudigula (Ginsburg, 1950) and Prionotus punctatus (Bloch, 1793) are relatively common in sandy and mudflat continental shelf areas in the southeastern and southern coast (Figueiredo & Menezes, 1980; Fagundes-Netto & Gaelzer, 1991; Haimovici et al., 1994, 1996; Haimovici, 1997).

These species are frequently found in commercial trawls on the shelf, mainly as bycatch (Haimovici et al., 1996; Viana, 1998). Between 2000 and 2010, catches of P. punctatus in southern Brazil amounted 3,600 ton year-1, on the average (GEP/UNIVALI, 2007, 2008, 2009, 2010, 2011). The species showed signs of overexploitation and a 15% reduction in fishing effort have been suggested to increase the cost-benefit ratio (Magro et al., 2000).

Studies on growth, feeding, fishing and ecology of P. punctatus primarily developed in southeastern and southern Brazil, mainly due to its growing importance in the fisheries in the 1980's. According to Andrade et al. (2006), this was one of the main demersal fisheries motivated by the negative perspectives of catching species usually taken as target.

Prionotus punctatus uses bays and estuaries during part of its life cycle as feeding and breeding areas (Milagre et al., 2002). Soares et al. (1994, 1998) studying feeding of P. punctatus in southeastern Brazil (23oS), found its diet based on crustaceans, especially Callinectes spp. and Portunus spp. Similar results were found by Braga & Braga (1987), with shrimps and crabs as the items most found in the stomachs of P. punctatus. Tubino (1999) performed an analysis of the distribution and feeding ecology of the three sea robin species off Cabo Frio (23oS). B. brachychir differed from the other species because it was possible to verify its greater abundance in colder and deeper waters of the studied area.

In southern Brazil (32oS), Teixeira & Haimovici (1989) found P. nudigula from 30 to 380 m and from 14° to 18°C. The diet consisted mainly of crustaceans and fish, and reproduction occurs during the spring and early fall.

Campos Basin lies in southeastern Brazil, off the states of Rio de Janeiro and Espírito Santo. According to the Brazilian Petroleum Agency, approximately 71% of national production (~1,600,000 boe day-1) is pumped into this area, mostly by the Brazilian oil and gas company Petrobras (ANP, 2013). For this reason, there is a continuous demand for environmental data to support engineering projects and evaluate the subsequent environmental risk to the coastal ecosystems. In this study we analyze the distribution and feeding of the three sea robin species on the Campos Basin continental shelf, with the objective of discerning the abundance, analyze the trophic level or, in other words, behold the ecological interaction of these species, to better understand in the future the trophic chain of southeastern Brazil.

MATERIALS AND METHODS

The data was obtained during a single 25-day scientific survey aboard the R/V Gyre, in April, 2008. The specimens were collected using a 15 m otter trawl with a 3.1 cm stretch mesh. The net was towed and opened hydro dynamically by spreading the two 7'x 14' wooden doors, with a single warp cable. The net was made of a 10.87 m head rope, a 12.60 m ground rope, and 2.08 m of maximum height, resulting in an estimated effective opening of 6.30 m, or 50% of the length of the groundrope, as described in Pauly (1980). All samplings were carried out during the day (06:00 h AM to 06:00 h PM).

After each trawling, the fish were separated from invertebrates and grouped according to species or type, and the number of specimens and the total weight of each taxon were recorded. The samples were packed in plastic drums and fixed in 10% formalin. Subsequently, the samples were transferred to 70% ethanol for preservation.

The number and weight of captured fish were considered by trawling time and converted to relative yields (n h-1 and kg h-1), which were used as abundance indicators. These data were used to map the spatial distribution of sea robin's populations in the Campos Basin shelf. In this context, sea robin species occurred in 17 trawling stations made during the survey, at depths ranging from 10 to 100 m (Fig. 1).

 
Figure 1. Trawl stations in the area of Campos Basin, southeastern Brazil, used to analyze the distribution and feeding of sea robins species.

In laboratory, the fish were measured and weighted, reproductive data were collected, and analysis of stomach contents was performed. Each individual had its total length (mm) recorded in an ichthyometer and weighted with the aid of a digital balance accurate to 0.01 g. The gonads were analyzed for sexual differentiations, maturation and stomachs were presserved in 70% alcohol for trophic studies. The food items were determined quantitatively to the lowest possible taxonomic level.

The mean trophic level was compared statistically among the considered species, according to Pauly et al. (2000) proposal, which allowed items standardization for purposes of comparisons among the analyzed species and even compared to other studies, since this classification is adopted by FishBase. The classification consists of a table with three levels of aggregation encompassing the most common prey types found in dietary studies compiled worldwide. Afterwards these values were attached to the trophic level equation proposed by Cortés (1999) and Ebert & Bizzarro (2007) to calculate the species mean trophic level:

Tropic level = 1+ [ Σ (P * TP)]

where P is the frequency of prey category in the diet and TP is the trophic position of prey category.

The frequency of occurrence, numerical importance, and weight of the preys were used to quantify their relative importance in the species' diet, according to Hyslop (1980). Subsequently, the Index of Relative Importance (IRI) was calculated as developed by Pinkas et al. (1971) according to the equation:

IRI = FO% * (N% + W%),

where FO%, N%, and W% are the frequency percentage of occurrence, numerical and weight importance of each prey, respectively.

It was found that the condition of data normality and homoscedasticity could not be confirmed in the statistical comparisons with Shapiro-Wilk test and Levene test (Zar, 2009), reason why the chi-square statistic and nonparametric Mann-Whitney test (Siegel, 1975) were chosen. Yields (CPUE in number and weight), average weight, and average length were compared statistically among depth strata (10-50 m and 50-100 m), temperature (<20oC and >20oC), and sedimentary cover (sand and mud).

RESULTS

Spatial distribution and abundance

The 24 trawls from shelf areas yielded 852 specimens. Bellator brachychir was the most abundant (n = 537), while P. nudigula (n = 248) and P. punctatus (n = 67) occurred in smaller numbers.

Significant values were observed when comparing numerical yields and average weight of B. brachychir with depth strata, while temperature and sedimentary cover significantly affect the abundances of P. nudigula and P. punctatus (Table 1).

 

Table 1. Mean weight, relative abundance (CPUE) and total length (TL) according to depth and temperature ranges. Significance values (P) from non-parametric Mann-Whitney test. In bold are indicated the significant values (P < 0.05).
 

Although B. brachychir (34-83 mm TL) was the most abundant sea robin species, it showed a more restricted distribution in the surveyed area (Fig. 2). Mean numerical densities were significantly higher (P = 0.004) in the range of 50-100 m (142 ± 81 n h-1), corresponding to 0.6 ± 0.3 kg h-1. Catches occurred exclusively in temperatures below 20oC. P. nudigula (54-166 mm TL) was closely associated to inner-shelf stations (10-50 m). Although 91% of the specimens have been recorded between 10 and 50 m, mean numerical densities (113 ± 103 n h-1) and weight (1.5 ± 2.6 kg h-1) were not statistically different (P = 0.200). P. punctatus (54-305 mm TL) was the most widely distributed species. Although 84% of the specimens have been recorded from 10 to 50 m, yields did not vary significantly with depth strata (P = 0.100). Yields of Prionotus punctatus were significantly higher in temperatures above 20oC (P = 0.019), while catch rates (kg h-1) of P. nudigula were significantly higher (P = 0.009) below 20oC (Table 1).

 
Figure 2. Relative abundance (CPUE kg h-1) of a) B. brachychir, b) P. nudigula, and c) P. punctatus. Histograms represent densities (n h-1) recorded by total length (TL mm).

Prionotus nudigula and P. punctatus were nearly related to sandy cover, mean numerical densities (66 ± 34 n h-1; 17 ± 13 n h-1, respectively) were significantly higher (P = 0.006; P = 0.036, respectively) on this sediment. However, B. brachychir did not show significant differences (P = 0.350) between the sandy and mudflat cover.

The two Prionotus species showed little or no spatial overlap, co-occurring in a single trawl (station 38). Only in this case, a single P. nudigula specimen occurred against four ones of P. punctatus (Fig. 3).

 
Figure 3. Inverse relative abundance (CPUE) of Prionotus species in Campos Basin, southeastern Brazil.

Sexual variability and length-weight relationship

For the three analyzed species, a greater proportion of females relative to males were observed, ranging by 1.5:1 for P. nudigula, 2:1 for P. punctatus, and 4:1 for B. brachychir. The proportions were significantly different only for B. brachychir (P < 0.0001) and P. punctatus (P = 0.0006), when compared by chi-square test. The relationship between total weight (g) and total length (mm) was obtained by regression analysis using the least-square method fitted to the potential function for both sexes (Fig. 4). No significant differences (chisquare test) were found among the total lengths and weights between sexes of the same species. The CI 95% relative to the total length ranged 0.18 for B. brachychir, 0.44 for P. nudigula and 1.22 for P. punctatus.

 
Figure 4. Length-weight relationship, with sexes combined, of the three Brazilian sea robin species.

Feeding

Stomachs of B. brachychir specimens (44-84 mm TL), P. nudigula (73-141 mm TL), and P. punctatus (62-166 mm TL) were analyzed. The frequency of stomachs with contents was 63%, 86% and 45% respectively.

In general, the three species presented a diet consisting primarily of crustaceans and other invertebrates from the benthic macrofauna, although the relative importance of the main preys changed according to the species (Table 2). The most frequent items in the diet (excluding unidentified items) of B. brachychir were amphipods (38%), while isopods (39%) and cumaceans (22%) were more frequent in P. nudigula and P. punctatus.

 

Table 2. Frequency of occurrence (FO), number (N), weight (g), and Index of Relative Importance (IRI) of food items found in stomachs contents of Brazilian sea robins (B. brachychir, P. nudigula, and P. punctatus) on Campos Basin continental shelf.
 

Based on the Index of Relative Importance (IRI), which integrates frequency, numbers and weight of preys, it was observed that B. brachychir fed preferentially on amphipods (IRI = 459). isopods (IRI = 1252) and tanaidaceans (IRI = 1209) were more important to P. nudigula, while shrimps (IRI = 335) and cumaceans (IRI = 280) to P. punctatus. No significant differences were registered in the composition of food items of Prionotus in relation to its sizes. Moreover, the diet of B. brachychir varied significantly (P = 0.033) with the predator size.

The three studied sea robin species showed very similar values concerning their trophic levels (Fig. 5), ranging between 3.0 and 3.4.

 
Figure 5. Mean trophic level of sea robin species according to the food items found in their stomachs. The vertical bars show the confidence interval (95%).

However, these values were considered signifycantly different (P = 0.004) according to Kruskal-Wallis test when comparing the diet of B. brachychir and P. punctatus. This can be explained by the higher consumption of fish by Prionotus Bellator(IRI = 9.7).

DISCUSSION

Although the three studied sea robin species have been recorded over the continental shelf of the Campos Basin, their distribution in the trawls suggest a possible spatial segregation that can be explained by preferences for their bathymetric and thermal distribution and also in response to the food preferences. Possibly, this mechanism is related to a reduction in interspecific competition, a frequent strategy in co-generic species, or exploitation of comparable niches in the same area.

Tubino (1999), in an extensive regional study on the sea robins in the upwelling area of Cabo Frio, suggest that Triglidae species use basically the same food resources, but in different environmental situations. He found the same sea robin species occurring throughout the year, but concentrated in specific depth ranges. These results resemble largely those found on the Campos Basin shelf, where B. brachychir was concentrated between 50-100 m depth and temperatures below 20°C, while both Prionotus species prevailed between 10-50 m, in a wider temperature range. Fagundes-Netto & Gaelzer (1991) and Teixeira & Haimovici (1989) have reported the distribution of the three sea robin species throughout the year in comparable depths and thermic ranges as reported in the present study.

A less intense deviation in the ratio among females and males was observed for the Prionotus species in the southernmost regions, with 2:1 (Andrade, 2004) and 1.2:1 (Teixeira & Haimovici, 1989), which suggest that populations change their structure in the sex proportions latitudinally.

Teixeira & Hamovici (1989), studying the feeding of the two Prionotus (P. punctatus and P. nudigula) species in southern Brazil (32oS), reported that the diet of sea robins was composed mainly by crustaceans and fish, with variations on prey's composition, according to the considered species. Similarly, Tubino (1999) found crustaceans, fish, and euphausiids as the main food sources for sea robins in the region of Cabo Frio (23oS). This suggest that the diet of sea robins showed little variation regarding latitude or depth, but vary significantly from the preferences in diet composition among the three species.

CONCLUSIONS

According to the data analyzed, it can be concluded that the two Prionotus species were spread preferentially on sandy bottoms at depths between 10 and 50 m. However, while P. nudigula occurred preferentially at lower temperatures (<20°C), P. punctatus preferred warmer waters (>20oC), whereas B. brachychir was distributed between 50 and 100 m in cooler waters (<20°C). It is noteworthy that the co-generic species belonging to the Prionotus genus showed little or no spatial superposition, co-occurring only in a single trawl.

Basically, sea robins at Campos Basin presented a carcinophagous diet, but with small overlap in their main preys. While amphipods was the most frequent prey (excluding unidentified items) to B. brachychir (38%), isopods (39%) and cumaceans (22%) were the basic food item found in P. nudigula and P. punctatus diet, respectively. This reduction in interspecific competition is followed by spatial segregation and thermal preferences for each species.

ACKNOWLEDGEMENTS

This study was coordinated by CENPES/PETROBRAS through the HABITATS Project - Campos Basin Environmental Heterogeneity. Our thanks to PETROBRAS for making it possible to collect and analyse the biological material. As well as our thanks to Faperj (Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro) for the masters scholarship (RRBSC), the PPGBIO (Programa de Pós Graduação em Ciências Biológicas-Biodiversidade Neotropical)/UNIRIO and the colleagues who participated in the collections at sea and screening the biological materials at UNIRIO (Universidade Federal do Estado do Rio de Janeiro). Two authors (PASC and ASM) were supported by grants from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

 

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Received: 25 June 2013; Accepted: 15 May 2014.

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