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Feeding ecology of Pachyurus bonariensis Steindachner, 1879 (Sciaenidae: Perciformes) in the Ibicui river, Southern Brazil: ontogenetic, seasonal and spatial variations/Ecologia trofica de Pachyurus bonariensis Steindachner, 1879 (Sciaenidae: Perciformes) no Rio Ibicui, sul do Brasil: variacoes ontogeneticas, sazonais e espaciais.

1. Introduction

Knowledge of the feeding ecology of a species is basic biological knowledge and may allow inferences regarding its population dynamics. This biological knowledge is fundamentally important for the evaluation of fish communities and the conservation of the entire freshwater ecosystem (Fugi and Hahn, 1991). It is necessary to know the trophic spectrum and the feeding activity of the species in its natural habitat, to attain success in conservation efforts. Knowledge of autoecology and of the ecological role of fish populations is mainly derived from diet studies based on analyses of stomach contents (Windell and Bowen, 1978).

The feeding ecology of Neotropical fishes varies widely. The most common differences are ontogenetic, seasonal and spatial, and are reported for a large number of species (Aranha et al., 2000; Lucena et al., 2000; Abelha et al., 2001; Mazzoni and Rezende, 2003; Araujo et al., 2005; Barreto and Aranha, 2006; Rezende and Mazzoni, 2006; Viana et al., 2006; Fugi et al., 2007; Pacheco et al., 2008). The two last sources of variations, seasonal and spatial, are primarily related to changes in food resource composition and availability, which are associated with productivity variations and physicochemical changes in aquatic ecosystems. On the other hand the ontogenetic variations are usually related to morphological changes that lead to shifts in prey selection and capture (Abelha et al., 2001; Vitule and Aranha, 2002; Araujo et al., 2005; Rezende and Mazzoni, 2006; Fugi et al., 2007).

The family Sciaenidae, with approximately 287 species and 78 genera, includes mostly marine fishes and some genera with a secondary adaptation to estuarine and freshwater environments (Casatti, 2003). Among these genera, six are restricted to freshwater and four, Pachyurus, Pachypops, Plagioscion and Petilipinnis, are endemic to South America (Casatti, 2003). The food items most often consumed by members of this family are benthic animals such as crustaceans, polychaetes, mollusks, insects and small fish, and sometimes algae (Mourao and Torres, 1984; Lunardon, 1990; Vazzoler, 1991; Hahn et al., 1997; Figueiredo and Vieira, 1998; Vendel and Chaves, 1998; Hahn et al., 1999; Soares and Vazzoler, 2001; Alvim and Peret, 2004; Branco et al., 2005; Bennemann et al., 2006; Fugi et al., 2007; Pacheco et al., 2008). The sciaenid Pachyurus bonariensis occurs naturally in the rivers of the Parana-Paraguay-Uruguay system, downstream from the Itaipu Reservoir, including Argentina, Brazil, Paraguay and Uruguay (Casatti, 2001) The P. bonariensis diet was studied once, in two lakes (locally called bays) of the Pantanal, where it had a diet composed mainly of Chironomidae and Ephemeroptera, with important ontogenetic shifts (Fugi et al., 2007). However, an older and not empirical study pointed out that the food of this species was composed of aquatic plants and organic substances from the mud (Devincenzi and Teague, 1942).

The aim of this study was to study the trophic ecology of P. bonariensis in the Ibicui River, where it is one of the dominant species (Behr, 2005). For this, the dietary composition and the feeding activity were studied, and its ontogenetic, seasonal and spatial variations. The dietary composition was analysed to investigate, in Ibicui River, its insectivorous specialised diet (Fugi et al., 2007). The ontogenetic, seasonal and spatial variations in trophic spectrum were also investigated to confirm its specialised diet at different situations and to analyse what is the mainly source of dietary variations, those principally due to food availability, seasonal and spatial, or the ontogenetic variation. Its feeding activity was analysed to investigate the influence of year seasons and spatial heterogeneity on food ingestion.

2. Material and Methods

This study was carried out at three locations along the Ibicui River, one of the main tributaries of the Uruguay River. The Ibicui basin is nearly flat, and the river flows slowly over a mainly sandy bed. It is located within the Pampas biome in the State of Rio Grande do Sul, Southern Brazil. Rambo (1994) described the Ibicui as a shallow river, with broad floodplains and surrounded by swamps and gallery forests. The sampling locations were: in the beginning stretch of the river, near the confluence of the Ibicui-Mirim and Santa Maria rivers (29[degrees] 47' S and 54[degrees] 56' W); in the intermediate stretch (29[degrees] 33' S and 55[degrees] 37' W) and near the mouth of the river (29[degrees] 25' S and 56[degrees] 38' W) (Figure 1).

At each point, two different environments were sampled: the main channel (lotic--LO), and in the nearby channels or lagoons (lentic--LE) that are connected to the main channel for most of the year.

The collections were carried out every two months at each location, from December 1999 to January 2002. Ten-metre-long gill nets with 1.5, 2.0, 2.5 and 3.0 cm meshes (measured between adjacent knots) were used. For mesh sizes of 4.0, 5.0, 6.0, 8.0 and 10.0 cm and for trammel nets 4.0/20, 5.0/20 cm and 6.0/20, 20 m of net were used. The nets were set out for 24 hours in each environment, and were checked every six hours (6:00 AM; 12:00 PM; 6:00 PM and 12:00 AM). In the seasonal analyses, the sampling years were analysed together, and the months were combined according to the seasons: spring (October, November, December), summer (January, February, March), autumn (April, May, June), and winter (July, August, September).

For the diet analysis of P. bonariensis, ten individuals from each sample (each net in each hour) were randomly selected, for a total of 324 individuals analysed of the total 602 captured. Voucher specimens were deposited in the Museu de Ciencias e Tecnologia, Pontificia Universidade Catolica do Rio Grande do Sul, Porto Alegre, Brazil: MCP26675 and MCP28419. The total standard lengths of theses fishes ranged from 11.4-24.9 (17.3 [+ or -] 2.6) cm and the total weight from 8.2-199 (63.5 [+ or -] 31.7) g. For the ontogenetic analysis the individuals were separated in four length classes based on its standard lengths. Length class 1: 11.4-14.3 cm; length class 2: 14.4-17.3 cm; length class 3: 17.4-20.3 cm and length class 4: 20.4-24.9 cm.

[FIGURE 1 OMITTED]

For each individual, a stomach fullness degree (FD) was assigned to investigate the feeding activity of the species. The FD represents how full the stomach was, and these were divided into the following classes: 0 (empty), 1 (up to 30%), 2 (between 30 and 70%) and 3 (over 70%). The feeding activity was compared between seasons by the Kruskal-Wallis Test, followed by Dunn's Multiple Comparisons Test. Feeding activity was also compared between lentic and lotic environments, for this, the fullness degree for each these environmental was submitted to the Mann-Whitney Test. Kruskal-Wallis and Mann-Whitney tests were run using the GraphPad Instat program.

The stomachs analysed had their food items identified and quantified (to the level of order) by the volumetric method according to Albrecht and Pellegrini-Caramaschi (2003). The volume measurement and the frequency of occurrence were analysed using the Alimentary Index (IAi) proposed by Kawakami and Vazzoler (1980). Food items in an advanced state of digestion were classified as (organic matter-digested O.M.-digested). The items that represented less than 1 in the Alimentary Index (IAi) were combined under the term "Diverse" in the graphs and analyses. Larvae and pupae of Diptera were counted separately because they have different ecologies.

The IAi of each fish group was submitted to a similarity analysis through the Bray-Curtis coefficient, using the statistical program Past. These fish groups were set according to its length class, year seasons and environment (lotic or lentic), generating 36 possible groups. However some possible groups did have any fish captured. Just the mainly items were considered in the development of the cluster analysis. This cluster analysis has the purpose to determine the main important source of variation to P. bonariensis diet. In other words, to determine the factor, ontogenetic, seasonal or spatial one, that will most separate the groups.

3. Results

The overall median of fullness degree was 2 (lower quartile = 1; upper quartile = 3). There were significant differences in feeding activity among seasons (kW = 14.41; p < 0.01) (Table 1) but not among lentic and lotic environments (U = 11983.50; p = 0.19) (Table 2). Dunn's Multiple Comparisons Test indicated significant differences (p < 0.05) in feeding activity between winter and all the other seasons (see Table 1).

Pachyurus bonariensis showed a relatively wide trophic spectrum, composed mainly of insects. Juvenile forms of Ephemeroptera, Diptera-larvae, Odonata and Trichoptera were the predominant items (Figure 2). Crustaceans, mollusks, annelids, coleopterans, Diptera-pupae and plant matter were also consumed, but less than the other groups.

The first separation in the cluster analysis (Figure 3), branches A, B and C, occurred due to length classes. The branches A and B corresponded to individuals from length classes 3 and 4, while individuals of branch C were from length classes 1 and 2. The year seasons did not make any specific separation, all the seasons were dispersed in all the branches. Concerning the spatial variations, there was separation between lentic and lotic environments just inside branch C. This separation placed all groups from lentic environment in branches 3 and 4 and almost all groups from lotic environment in branches 5 and 6. The food items responsible for the branches separations can be observed in Table 3. The great consumption of Odonata formed branch A1. Branch B1 was formed due to the consumption of Ephemeroptera. For groups in branch C3 Diptera was the main item. The group from branch C4 consumed Diptera and Ephemeroptera. The groups that formed branch C5 consumed Diptera and Trichoptera. The groups from the last branch, C6, consumed mainly Trichoptera.

[FIGURE 3 OMITTED]

4. Discussion

Pachyurus bonariensis showed high feeding activity, especially compared to piscivorous fishes: their stomachs were almost always full, in all situations. It is common for invertivorous fishes to show higher feeding activity than piscivorous ones (Lucena et al., 2000; Soares and Vazzoler, 2001; Vitule and Aranha, 2002; Braga, 2005; Fagundes et al., 2007). The variations in feeding activity among the seasons of the year are closely related to the lowest fullness degree obtained in the winter, with this season differing significantly from the others. Previous studies also reported lower degrees of stomach fullness in the cold seasons (Hahn et al., 1997; Bennemann et al., 2000; Braga, 2005; Branco et al., 2005; Barreto and Aranha, 2006; Viana et al., 2006). This situation may be related to lower food availability--decrease of prey populations, less reproductive activity (Dufech and Fialho, 2006) or decreased metabolic activity of the predators (Viana et al., 2006).

Previously, the diet of P. bonariesis had been approached just in descriptive works of the Uruguay River, without empiric observations. However, these works did not arrive at the same conclusion about its diet. Lopez and Castello (1968) opted for an insectivorous diet, while Devincenzi and Teague (1942) considered that aquatic plants and organic substances from the mud were the main items consumed by this fish. Recently, the diet of P. bonariensis has been studied with more attention by Fugi et al. (2007). These authors point to an insectivorous specialised diet, where Chironomidae and Ephemeroptera larvae were the main items consumed. In this study, aquatic insects were the mainly item found, corroborating Lopez and Castello (1968) and Fugi et al. (2007). The main items found by Fugi et al. (2007) were also the most important ones here, however two others insect orders were also important: Odonata and Trichoptera. Pacheco et al. (2008) also found an insectivorous diet for P schomburgkii Gunther, 1860 and P. paucirastrus Aguilera, 1983. The predominance of aquatic insects in the food of fish is common in freshwater communities (Sabino and Castro, 1990; Aranha et al., 2000; Abes et al., 2001; Andrade and Braga, 2005; Pouilly et al., 2004; Braga, 2005; Fugi et al., 2007; Pacheco et al., 2008), making the insect larvae a very important food category for fish (Zavala-Camin, 1996). Certain benthic insects, such as Diptera larvae and Ephemeroptera, are abundant in rivers with sandy bottoms (Braga, 2005) such as the Ibicui River.

The ontogenetic variations were confirmed as the most important for P. bonariensis diet. The ontogenetic pattern shown by this species in the Ibicui River is widely observed in fish diets (Hahn et al., 1997; Abelha et al., 2001; Vitule and Aranha, 2002; Araujo et al., 2005; Rezende and Mazzoni, 2006; Fugi et al., 2007). The smaller individuals, length classes 1 and 2, preyed basically on Diptera-larvae and Trichoptera, the smallest items, and this pattern gradually changed as larger fish took larger food, Ephemeroptera and Odonata. Fugi et al. (2007) found similar patterns in P. bonariensis in two lakes of the Pantanal, where smaller fish preyed mostly on chironomids and larger ones preyed mostly on ephemeropterans. This pattern can be attributed to differences in energy requirements and morphological limitations (Abelha et al., 2001; Rezende and Mazzoni, 2006). Ontogenetic shifts in diet may also decrease intraspecific competition (Araujo et al., 2005).

Spatial variations also happened, but just for juveniles, length classes 1 and 2. Trichoptera was found mainly in lotic environmental and Diptera in lentic ones. Trichoptera is known to be an insect group adapted to lotic environments (Kikuchi and Uieda, 1998). The most important source of dietary variation for P. bonariensis was related to intrinsic biological characters of the species. However the food availability, heterogeneously distributed in the environment, was also important for this species, suggesting that this species can adapt its diet to environmental changes.

Regarding the Sciaenidae diet, marine species consume mainly decapod crustaceans (Lunardon, 1990; Vazzoler, 1991; Figueiredo and Vieira, 1998; Vendel and Chaves, 1998; Soares and Vazzoler, 2001; Branco et al., 2005). Freshwater sciaenids consume mainly fish and insects (Mourao and Torres, 1984; Hahn et al., 1997, 1999; Alvim and Peret, 2004; Bennemann et al., 2006; Fugi et al., 2007; Pacheco et al., 2008). It can be an adaptation of the species that invaded freshwater to the low availability of crustaceans and great availability of insects in comparison to marine habitats. The complete absence of fish in the diet of P. bonariensis, compared to other freshwater sciaenids, is likely associated with its relatively smaller body size and mouth morphology (small and sub-inferior).

Although P. bonariensis showed ontogenetic and spatial variations in the main items consumed, the main items were always insects and its diet was composed exclusively of invertebrates. These results corroborate Fugi et al. (2007), characterising P. bonariensis as a fish with a solely invertivorous feeding habit, mainly insectivorous, also in the Ibicui River.

Acknowledgements--We thank Antonio Jose Urrutia Cohendet, Cleiton Adriano Signor, Lilian Fronza, Mariana Parizotto Almeida, Musa Nabih Musa Othman and Professor Sonia Cechin for technical and logistical assistance. We are also grateful to all those who helped to identify the food items: Camila Fagundes, Carla Kotzian, Joele Baumart, Marcia Spies and Sandro Santos. Special thanks to Professors Bernardo Baldisserotto, Marilise Krugel and Mirian Albrecht for suggestions for improvements to the manuscript and/or analyses. Janet W. Reid revised the English text. Personal grants were provided by PET/SESu/MEC and CNPq.

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Lima, DO. (a) * and Behr, ER. (b) *

(a) Universidade Federal da Fronteira Sul--UFFS, Campus de Cerro Largo, Rua Joao Sebastiany, 16, CP 63, CEP 97900-000, Cerro Largo, RS, Brazil

(b) Unidade Descentralizada de Educacao Superior, Universidade Federal de Santa Maria--UFSM, Rua Francisco Guerino, 407, CEP 98300-000, Silveira Martins, RS, Brazil

* e-mail: daniela.ol.lima@gmail.com, everton_behr@hotmail.com

Received February 11, 2009--Accepted April 24, 2009--Distributed August 31, 2010 (With 3 figures)
Table 1. Fullness degree values
for Pachyurus bonariensis in each
season in the Ibicui River (N =
number of fish analyzed; FD =
median fullness degree; LQ = lower
quartile; UQ = upper quartile;
* significant difference between
winter and all other seasons).

Season    N    FD    LQ   UQ

Summer   135    2    1    3
Autumn   60     2    2    3
Winter   52    2 *   1    2
Spring   70     3    2    3

Table 2. Fullness degree values
for Pachyurus bonariensis in lotic
and lentic environments in the
Ibicui River (N = number of fish
analysed; FD = median fullness
degree; LQ = lower quartile; UQ =
upper quartile; LE = lentic
environment; LO = lotic environment).

Environment    N    FD   LQ   UQ

LE            151   2    1    3
LO            166   2    1    3

Table 3. Feeding indexes (IAi) of the 27 groups analysed in
the Ibicui River. The groups were set according to its length
class (1: 11.4-14.3 cm; 2: 14.4-17.3 cm; 3: 17.4-20.3 cm; 4:
20.4-24.9 cm); year seasons (SPR: spring; SUM: summer; AUT:
autumn; WIN: winter) and environment (LE: lentic; LO: lotic).
The mainly food items for each group were highlighted with
an asterisk (*). To facilitate comparisons the groups were
placed according to its position in the cluster analysis
(following this order: branches A1, B2, C3, C4, C5 and C6).

Group      Odonata   Ephemeroptera   Diptera   Trichoptera

3-SPR-LE   78.8 *     4.7            14.2       2.3
3-WIN-LO   93.6 *     1.6             2.9       1.8
4-SPR-LE   99.5 *     0.0             0.5       0.0
2-SUM-LE    0.1      82.0 *          16.0       1.9
3-SUM-LO    0.0      87.7 *           2.9       9.4
4-SPR-LO    0.0      92.4 *           6.3       1.3
4-SUM-LE    0.2      91.7 *           5.7       2.5
4-WIN-LE    8.8      85.9 *           5.4       0.0
4-SUM-LO    0.0      72.9 *           0.9      26.2
3-SUM-LE    7.8      68.3 *          19.6       4.3
3-WIN-LE   20.6      64.2 *          11.6       3.6
4-AUT-LE   27.2      65.3 *           7.5       0.0
1-SPR-LE    0.0       1.6            77.2 *    21.3
1-SPR-LO    0.0       2.6            83.3 *    14.1
2-AUT-LO    0.7      11.9            80.3 *     7.1
2-SPR-LE    1.9       7.9            78.2 *    11.9
2-AUT-LE    2.4      10.8            84.9 *     1.9
2-WIN-LE    0.0      14.7            70.6 *    14.7
1-SUM-LE   11.8       0.0            80.1 *     8.1
3-AUT-LE    0.0      49.0 *          51.0 *     0.1
1-AUT-LO    0.0      18.2            44.4 *    37.4 *
2-SPR-LO    1.8      10.8            52.1 *    35.3 *
2-SUM-LO    1.3      24.4            48.7 *    25.5 *
3-SPR-LO    9.0      24.2            38.2 *    28.6 *
1-WIN-LO    0.0       2.3            11.5      86.2 *
1-SUM-LO    0.0       6.9            35.8      57.3 *
2-WIN-LO    6.5       7.5            24.0      62.0 *

Figure 2. Feeding index(IAi)
of Pachyurus bonariensis in
the Ibicui River. The item
(organic matter-digested
O.M.-digested) refers to
invertebrates that were in
an advanced state of
decomposition. The item
"diverse" includes
unidentified insects,
Annelida, plant matter,
Decapoda, Diptera-pupae,
Coleoptera and Mollusca.

Ephemeroptera    40.7
Odonata          24.7
Diptera-larvae   13.4
Trichoptera      9.7
O.M. digested    9.7
Divers           1.6

Note: Table made from bar graph.
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Author:Lima, D.O.; Behr, E.R.
Publication:Brazilian Journal of Biology
Date:Aug 1, 2010
Words:4463
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