Corresponding author: Fábio R. Lameiro ( oceanolameiro@yahoo.com.br ) Academic editor: Cassiano Monteiro Neto
© 2018 Fábio R. Lameiro, Mario V. Condini, Cintia P. Brito, João P. Vieira.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Lameiro FR, Condini MV, Brito CP, Vieira JP (2018) The feeding habits of the endemic Remo flounder, Oncopterus darwinii (Actinopterygii: Pleuronectidae), in an exposed sandy beach’s surf zone in southern Brazil. Zoologia 35: 1-8. https://doi.org/10.3897/zoologia.35.e15038
|
The Remo flounder, Oncopterus darwinii Steindachner, 1874 is a small Pleuronectidae (~ 250 mm TL) distributed in the warm-temperate zone from Santa Catarina (28°S – Brazil) to the Gulf of San Matías (42°S – Argentina). We studied the occurrence and diet of juveniles of this flatfish (85% < 100 mm TL) for one year (August 2009 to July 2010) in a southern Brazilian sandy beach. Individuals were much more common in spring and early summer than in the other seasons. Of the 758 individuals analyzed, only 69 (9.1%) were found with empty stomachs. The Remo flounder fed predominantly on small crustaceans (gammarid amphipods, mysids and the hipiidae Emerita brasiliensis Schmitt, 1935) and no seasonal differences were found in the composition of the diet of this flatfish. However, variations in the Index of Relative Importance (IRI) were found among seasons, which most likely can be explained by a decrease in the availability of favored food items throughout the year. The pattern of distribution of O. darwinii indicates that southern Brazilian sandy beaches are used as nursery ground for this species.
Feeding strategy, flatfish, marine fish, southwestern Atlantic Ocean
Several juvenile fish species use coastal areas (mainly sandy beaches and estuaries) as nurseries because these areas generally have higher productivity, offer lots of food and shelter from predators, and have favourable temperatures, all of which decrease the risk of mortality in the early life stages (
Flatfish species have a broad global distribution and great commercial and ecological importance (
The Remo flounder is a non-commercial fish that reaches up to 35 cm in total length. It is often caught as by-catch of artisanal and commercial fisheries in coastal waters, less than 40 m deep, throughout its distribution range (
Fish were caught from two exposed sandy beaches along the coast of Rio Grande do Sul in southern Brazil, Cassino and Mar Grosso beaches (Fig.
The fish were collected monthly from August 2009 to July 2010 using two types of beach seine nets: Beach Seine 9 m (BS-9 m) is a multifilament net 9 m in length and 1.5 m in height, 13 mm stretch mesh in the wings and a 5 mm stretch mesh in the centre 3 m section; and the Beach Seine 30 m (BS-30 m) is a net 30 m in length, 1.8 m in height and 12 mm monofilament nylon stretch mesh with a 30 cm inferior bar and 12 mm multifilament stretch mesh. Five hauls using each of the different fishing gear configurations were made in each sampling site. Fish collecting was authorized by the license issued by the “Sistema de Autorização e Informação em Biodiversidade (SISBio/ICMBio/MMA)” of the Brazilian government, under number 24417-1 (authentication code 49915343).
All individuals caught were transported on ice to the laboratory. Each individual was measured (Total Length, mm TL), weighed (g) and dissected to extract the stomach, which was preserved in 10% formaldehyde and stored in 70% alcohol a week later for analysis. Briefly, each stomach was weighed before and after removing all the food items. The food items recovered from each stomach were counted and their volume (0.1 mm3 precision) was measured. Volume was estimated based on the area occupied by each item and its height (area × height) (e.g.
A total of 758 Remo flounder flatfish were examined for stomach content analyses. The quantitative analysis of the diet consists of calculating the Coefficient of Vacuity (Cv), which is the percentage of empty stomachs with respect to the total number of stomachs examined (
To allow a clearer view of the seasonal feeding behaviour of the flatfish throughout the study period, the months were grouped into austral seasons (winter = July to September; spring = October to December; summer = January to March; and autumn = May to June). There were no individuals captured during the austral autumn and early winter (from March to July). To assess the differences in diet associated with the size of the predator (TL mm), individuals of O. darwinii were pooled into three size classes: <60 mm; 60–100 mm and >100 mm. These three size classes were chosen arbitrarily and were based on the sizes of the individuals captured by the different fishing gears. The %IRI for each food item was computed for each site and size class.
A one-way ANOVA was used to evaluate the differences in the average number of prey items and prey volume among the austral season (and predefined size classes), and post-hoc differences were evaluated using the Newman-Keuls test (α = 0.05). The normality and homogeneity of variance were assessed using Kolmogorov-Smirnov and Cochran tests (
The graphical analysis proposed by
Oncopterus darwinii occurs in the southwestern Atlantic Ocean from mid-winter (August) to mid-summer (February) and is more frequent between October and January (Fig.
The non-empty stomachs revealed 17 food items plus remains of organic material (Table
Frequency of occurrence (%F), numerical abundance(%N), volume (%V) and Index of Relative Importance (%IRI) for each prey item, in the gut of juveniles flatfish Oncopterus darwinii caught in surf zone of sandy beaches in southern Brazil.
Prey items | Cassino Beach (n = 325) | Mar Grosso Beach (n = 364) | ||||||
%F | %N | %V | %IRI | %F | %N | %V | %IRI | |
Insecta unidentified | 0.27 | 0.01 | 0.01 | <0.01 | – | – | – | – |
Bivalvia | ||||||||
Amarilladesma mactroides | 1.61 | 0.06 | 0.10 | <0.01 | 3.00 | 0.05 | 0.14 | 0.01 |
Gastropoda unidentified | 0.94 | 0.02 | 0.02 | <0.01 | – | – | – | – |
Amphipoda | ||||||||
Hyperiidae unidentified | 7.04 | 0.50 | 1.20 | 0.15 | 1.28 | 0.07 | 0.10 | <0.01 |
Bathyporeiapus bisetosus | 87.88 | 73.13 | 48.86 | 73.28 | 92.21 | 93.00 | 52.47 | 86.76 |
Phoxocephalopsidae unidentified | 12.50 | 0.85 | 2.47 | 0.57 | 8.89 | 0.93 | 0.80 | 0.17 |
Decapoda | ||||||||
Shrimp unidentified | 0.72 | 0.02 | 0.10 | <0.01 | – | – | – | – |
Crustacea unidentified | 6.13 | 0.23 | 0.82 | 0.06 | 3.53 | 0.09 | 0.10 | 0.01 |
Pinnotheridae | ||||||||
Austinixa patagoniensis | 1.48 | 0.04 | 0.25 | <0.01 | – | – | – | – |
Penaeidae | ||||||||
Farfantepenaeus paulensis | – | – | – | – | 0.19 | <0.01 | <0.01 | <0.01 |
Hippidae | ||||||||
Emerita brasiliensis | 27.87 | 2.13 | 14.05 | 3.95 | 18.70 | 2.68 | 20.99 | 6.49 |
Portunidae unidentified | 1.18 | 0.05 | 0.12 | <0.01 | 0.19 | <0.01 | <0.01 | <0.01 |
Callinectes sapidus | 4.05 | 0.13 | 1.51 | 0.10 | – | – | – | – |
Isopoda | ||||||||
Excirolana armata | 8.81 | 0.41 | 1.03 | 0.09 | 3.58 | 0.34 | 0.35 | 0.02 |
Chiriscus giambiagiae | 5.29 | 0.30 | 0.76 | 0.09 | 0.38 | 0.01 | 0.01 | <0.01 |
Mysida | ||||||||
Mysida unidentified | 56.74 | 21.93 | 28.26 | 21.69 | 19.01 | 2.76 | 24.98 | 6.53 |
Actinopterygii | ||||||||
Menticirrhus spp. | 0.27 | 0.01 | 0.09 | <0.01 | – | – | – | – |
Organic material remains | 1.99 | 0.11 | 0.35 | 0.01 | 1.47 | 0.07 | 0.05 | <0.01 |
The coefficient of vacuity was higher during the spring at both beaches (Table
Average values (± SD) of prey number and volume in the stomach contents of Oncopterus darwinii at Cassino (3–4) and Mar Grosso (5–6), respectively. The data are summarized for three seasons (winter, spring and summer) and shared letters above each box indicate non-significant differences among the seasons.
Variations in Index of Relative Importance of the main items ingested by the juvenile flatfish of the Cassino and Mar Grosso beaches, during a year. Non-empty stomachs (N), Coefficient of Vacuity (Cv), mean number and area (mm3) of preys (Nm/Am). Do not have any individual collected in Autumn.
Prey items | Cassino Beach | Mar Grosso Beach | ||||
---|---|---|---|---|---|---|
Winter | Spring | Summer | Winter | Spring | Summer | |
Bathyporeiapus unidentified | 79.84 | 58.83 | 72.27 | 54.04 | 93.02 | 36.12 |
Mysida unidentified | 17.90 | 38.58 | 0.10 | 45.95 | 6.92 | <0.01 |
Emerita brasiliensis | 0.71 | 1.48 | 26.05 | <0.01 | 0.03 | 55.02 |
Others | 1.54 | 1.11 | 1.58 | 0.01 | 0.04 | 8.86 |
N | 10 | 252 | 63 | 17 | 323 | 24 |
Cv | 0.79 | 2.51 | 0.53 | <0.01 | 5.15 | 0.13 |
Nm/Am | 14.4/ 9.83 | 11.1/ 13.4 | 8.2/ 13.98 | 13.3/ 7.57 | 33.5/ 28.8 | 6.6/ 34.39 |
The percentage of digestive vacuity was greater in the major size classes in both beaches (Table
Average values (± SD) of prey number and volume in the stomach contents of Oncopterus darwinii at Cassino (7–8) and Mar Grosso (9–10), respectively. The data are summarized for three size classes (<60 mm TL, 60–100 mm TL, and >100 mm TL), and shared letters above each box indicate non-significant differences among the size classes.
Variations in Index of Relative Importance of the main items ingested by the juvenile flatfish of the Cassino and Mar Grosso beaches, along the ontogeny. Non-empty stomachs (N), Coefficient of Vacuity (Cv), mean number and area (mm3) of preys (Nm/Am). Do not have any individual collected in Autumn.
Prey items | Cassino Beach | Mar Grosso Beach | ||||
<60 | 60–100 | >100 | <60 | 60–100 | >100 | |
Bathyporeiapus unidentified | 77.06 | 70.33 | 76.01 | 99.04 | 85.30 | 95.24 |
Mysida unidentified | 20.41 | 21.71 | 22.82 | 0.95 | 13.64 | 3.87 |
Emerita brasiliensis | 2.04 | 6.68 | 0.70 | <0.01 | 1.00 | 0.67 |
Others | 0.49 | 1.28 | 0.48 | 0.01 | 0.06 | 0.22 |
N | 62 | 219 | 44 | 145 | 163 | 56 |
Cv | 0.66 | 0.66 | 2.51 | 1.06 | 0.13 | 4.09 |
Nm/Am | 10.6/ 9.21 | 9.6/ 12.75 | 16.2/ 22.1 | 17.7/ 6.36 | 27.4/ 38.5 | 63.3/ 41.3 |
According to the Amundsen diagram, the flatfish had a specialist feeding strategy characterized by a single or few prey items, which reflects a predatory population with a narrow niche width (Fig.
The Remo flounder O. darwinii is highly abundant in the surf zone of the southern Brazilian sandy beaches in the spring and early summer, and becomes infrequent or scarce during the remainder of the year (
The low frequency of empty stomachs in our data (9.1%) is consistent with the results of other studies (
A low diversity of items was found in the digestive tract of O. darwinii (16 at Cassino and 11 at Mar Grosso) in our data. The amphipod Bathyporeiapus sp. was the most consumed food item at both sites (%IRI = 80), whereas the other two food items (Mysida group and E. brasiliensis) were responsible for almost 18% of the IRI. These results reveal that the population of O. darwinii had a specialist feeding behaviour, which is characterized by a high consumption of a few items, mainly Bathyporeiapus sp. However, some individuals in the population displayed an opportunistic behaviour towards the consumption of certain prey (Mysida group and E. brasiliensis).
No seasonal differences in the diet composition of Remo flounder juveniles were found in the present study (Bathyporeiapus sp., E. brasiliensis and the Mysida group were the main food items). However, there are variations in the IRI among seasons; this can probably be explained by a decrease in the abundance of the preferred food items throughout the year. Studies made in this region showed a peak occurrence of Bathyporeiapus sp. during the spring and a predominance of E. brasiliensis during the summer (
Our results were similar for both sites. There were no differences in the diet composition of juveniles of O. darwinii throughout its ontogeny, and the same pattern of IRI was maintained. However, a huge variation in prey number and volume found in the stomachs was observed in smaller Remo flounders, with less prey in number and volume than larger flounders. This pattern is common in different species in studies addressing diet composition and variations in ontogeny (
We are thankful to the Laboratório de Ictiologia (FURG) staff for their assistance in the field collections and sample processing and the anonymous reviewers of this manuscript. This study was funded by the Conselho Nacional de Desenvolvimento Científico e Tecnológico through the ‘PELD-Site 8’ program (CNPq process 403805/2012-0) and by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior through the ‘PVE’ program (CAPES process A101/2013). CPB is a postgraduate student and FRL is a postdoc of “Programa de Pós-Graduação em Oceanografia Biológica” at FURG.