Feed Preferences of Salminus Brasiliensis (Pisces, Characidae) Larvae in Fish Ponds ⁎ Daniela Flávia Orísia Ribeiro, Alex Pires De Oliveira Nuñer

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Aquaculture 274 (2008) 65–71 www.elsevier.com/locate/aqua-online

Feed preferences of Salminus brasiliensis (Pisces, Characidae) larvae in fish ponds ⁎ Daniela Flávia Orísia Ribeiro, Alex Pires de Oliveira Nuñer

Laboratório de Biologia e Cultivo de Peixes de Água Doce, Universidade Federal de Santa Catarina, Departamento de Aqüicultura, Rodovia SC 406, 3532, Florianópolis, Santa Catarina, CEP 88066-000, Brazil

Received 8 March 2007; received in revised form 8 November 2007; accepted 8 November 2007

Abstract

Feed preferences of dorado, Salminus brasiliensis, in the early stages of life was studied in larvae, stocked 5 days after hatching in three earthen commercial ponds (810 m2, 900 m2 and 1480 m2) at a density of 30 m−2. Larvae were fed on natural food from ponds supplemented with a commercial ration (40% crude protein), and for 12 days fish samples were taken daily in the morning and in the afternoon from each pond to analyze the food items present in the diet. Zooplankton available in the environment was also analyzed. Feeding was intensive since 94% of the larvae guts examined contained food. Since the commercial diet was not found in the dorado guts, the natural diet dominated the artificial food, but the cannibalistic behavior typically found in laboratory conditions was not observed. Insect larvae and cladocerans were the main prey items found in the gut of the larvae. In fish ponds dorado larvae can be considered a generalist feeder, since small amounts of different food items were consumed, but they tend to specialize in some items, according to their developmental stage. © 2007 Elsevier B.V. All rights reserved.

Keywords: Salminus brasiliensis; Larvae; Natural food; Fish ponds; Dorado

1. Introduction tribution in the water column, predator's catching efficiency, water temperature and turbidity (Moore and Moore, 1976). In the early stages of development, natural food provides According to these authors, changes in the feeding habits of a essential nutrients ensuring fish survival and growth (Furuya fish species are a function of the interactions among several et al., 1999), as well as playing a very important role in larvae environmental factors that will influence food item selection. culture and rearing of fingerlings (Kubitza, 1998). Although fish feeding is selective, it can vary according to food Fish feeding can be analyzed by direct observation of the availability meaning that most fish species show extremely feeding behavior and/or by identifying the gut contents, which adaptable feeding habits, using items readily available in the represents food availability in a certain environment (Andrian environment (Azevedo, 1972). and Barbieri, 1996). Studying fish anatomy also provides basic Salminus brasiliensis Cuvier, 1816, is a carnivorous species information about the feeding habits of fish and a careful from its early life stages. Newly-hatched larvae are on average examination of the digestive apparatus gives a good idea of their (±standard deviation) 4.96±0.18 mm long (Zaniboni-Filho favorite diet or, at least, can guide new studies regarding their et al., 2004), and when larvae reach a length of 6.75 mm, there is feeding (Wooton, 1990). a total absorption of the vitelline sac (Nakatani et al., 2001). The main factors that determine the type of prey ingested are Santos and Godinho (2002) reported that larvae cultured at feeding preference (Shaw et al., 2003; Hagiwara et al., 2007; temperatures of 23–25 °C, absorbed the vitelline sac by the third Nunn et al., 2007), prey availability, its mobility and dis- day after hatching. In the wild, 3-day-old larvae start feeding on plankton, microcrustaceans, cladocerans, copepods and larvae ⁎ Corresponding author. Tel./fax: +55 48 3389 5216. of Odonata and Chironomidae (Morais Filho and Schubart, E-mail address: [email protected] (A.P.O. Nuñer). 1955). In captivity this species develops cannibalism, which

Fig. 1. Daily water temperature, pH, dissolved oxygen and total ammonia concentrations in ponds stocked with Salminus brasiliensis larvae. Pond 1=◊; Pond 2=Δ; Pond 3=□. Clear symbols=morning sampling; solid symbols=afternoon sampling.

usually decimates large scale production (Zaniboni-Filho, The total length (mm) of each of the larvae was measured with a caliper, and 2004). the wet weight (g) was obtained with a 0.1 mg precision analytical scale. The gut As feeding the larvae during the first days of life is one of the contents were analyzed on Petri dishes under a stereomicroscope, and the food items were identified using the keys described by Macan (1975), Merret and main constraints in the large-scale production of juvenile fish, Cummis (1984), Borror et al. (1992) and Roldán (1988). the present study aimed to describe the diet of dorado larvae For the daily analysis of the gut contents, the larvae sampled in the morning stocked in commercial fish ponds to promote better manage- and in the afternoon were pooled and analyzed together using the method ment of the species. described by Amundsen et al. (1996), which relates the frequency of occurrence of food items and their specific abundance in the equations f=Ni/N, where Fi = frequency of occurrence of food item i; N =number of larvae with food item i in 2. Materials and methods i the gut; N=total number of larvae with some food in the gut, and Sa=(∑Si/∑St ) 100 where Sa=specific abundance (%) of food item i; Si =total number of food The experiment was carried out in December/2003 with dorado larvae item i in the larvae gut and St =total number of food items in the larvae guts that obtained by induced spawning of broodstock using carp pituitary extract (CPE) contained food item i. − 1 as the hormone in a previous dosage (0.25 mg CPE kg of broodstock) Electivity of fish larvae were analyzed by the Ivlev's index, Ei =(ri −pi)/ − 1 followed by two dosages (0.5 and 5.0 mg CPE kg ) applied in an interval of (ri +pi), where Ei is the Ivlev's index of the food type i, ri is the percentage 12 h (Zaniboni-Filho and Barbosa, 1996). After hatching, larvae were kept for 5 days in laboratory conditions and fed with Prochilodus lineatus larvae, the usual method of commercial management Table 1 that assures larvae survival. Total density (103 l− 1) of copepods and cladocerans in three ponds stocked with On the fifth day after hatching (DAH), dorado larvae averaging (±standard Salminus brasiliensis larvae during the sampling period deviation) 10.73±0.26 mm in length and 10.1±1.4 mg in weight, were transferred to commercial earthen ponds at a density of 30 larvae m−2. Pond Three ponds were used: P1 (810 m2; 1.60 m mean depth), P2 (900 m2; 1.80 m Group/species 1 2 3 Total mean depth) and P3 (1480 m2; 1.40 m mean depth), filled by gravity with Copepods 2775.4 unfiltered water from a reservoir located in the hatchery. Prior to stocking, ponds − − Nauplii 384.8 572.0 539.0 1495.8 were treated with lime (60 g m 2) and fertilized with chicken manure (300 g m 2) Cyclopoida 340.8 122.5 212.0 675.3 to promote disinfection, pH equilibrium and zooplankton growth, as zooplankton Calanoida 6.8 476.5 121.0 604.3 could be used as a food source by the larvae. A daily supplement of 4.0 kg of a Cladocerans 948.2 commercial ration (40% crude protein) was offered in equal portions at 06:00, Bosmina sp. 92.3 125.0 238.0 455.3 12:00, 18:00 and 24:00 h in each pond. Diaphanosoma sp. 122.0 88.0 230.3 440.3 In order to analyze the gut contents, larvae samples (n=5 to 8) were Bosminopsis sp. 6.0 30.3 0.0 36.3 collected from each pond in the morning (08:00 h) and in the afternoon Ceriodaphnia sp. 4.0 0.5 2.5 7.0 (18:00 h). Sampling was carried out for 12 days, the period required for larvae to Disparalona dadayi 2.3 1.3 2.0 5.5 reach commercial size. A zooplankton net was used for capturing larvae during Moina sp. 0.8 1.5 1.5 3.8 the first 6 days followed by a 1.5 mm mesh net for the next 6 days. The sampled Total 959.5 1417.5 1346.3 3723.6 larvae were kept in a 4% buffered formaldehyde solution for later analysis. D.F.O. Ribeiro, A.P.O. Nuñer / Aquaculture 274 (2008) 65–71 67

The concentrations of dissolved oxygen and total ammonia, temperature and pH were analyzed with an YSI-6600 multiparameter probe. Analyses were done in all ponds in the morning and in the afternoon, and a 24-hour cycle analysis was carried out in each pond with 1-hour intervals between readings, to evaluate daily variations. The chi-square test (Zar, 1996) was used to analyze gut fullness, zooplankton density in ponds and occurrence of food items in larvae guts. The lengths and weights, for each sampled day, were analyzed using ANOVA (α=0.05) and their relation with time was expressed by regression analyses (Zar, 1996).

3. Results

The water temperature and the dissolved oxygen concentration were higher in the afternoons and similar among ponds. In contrast, the total ammonia concentration was higher in the mornings (Fig. 1). The dissolved oxygen concentration remained high from the sixth day of sampling, coinciding with a reduction in the total ammonia concentration, which remained well below lethal levels for dorado juveniles (Gazzola, 2003). There was a small change in pH due to the initial liming that buffered the pond water. Therefore, the observed variations in water quality parameters in the ponds remained within acceptable limits for freshwater fish culture (Boyd, 1990). Since rotifers were not consumed by dorado larvae during the experiment they were not included in the analysis. Without the rotifers, copepods were the zooplanktonic group with the largest density in all ponds, a condition derived by the high number of nauplii present (Table 1). If nauplii were ignored the densities of copepods and cladocerans were similar. Among cladocerans Bosmina sp. and Diaphanosoma sp. were the species with higher densities. A total of 591 larvae guts were examined, of which 556 (94%) contained food. Five kinds of food items were found in fish guts: P. lineatus larvae, from now on named fish larvae (fL), insect larvae (iL), cladocerans (C), copepods (Co) and adult insects (Ai). Cladocerans and insects partially digested were named cladoceran paste (Cp) and insect paste (ip) respectively, and were analyzed separately from the iL and C to allow visual observation of the beginning of digestion by dorado larvae. The daily analyses showed that larvae from different ponds ingested food items in different quantities (Pb0.05), possibly due to the different b Fig. 2. Mean daily density of the main groups of zooplankton in Salminus (P 0.05) daily density of the zooplankton groups in ponds (Fig. 2). brasiliensis larvae ponds during the sampling period in ponds 1, 2 and 3. On the first day of sampling fish larvae, insect larvae, cladocerans and copepods were found in the guts of 5-day-old dorado larvae (Fig. 3a). Insect larvae became predominant in most 6-DAH dorado guts, and a greater reduction in the occurrence of fish larvae was also noticed of food type i in larval gut and pi is the percentage of the food type i in the (Fig. 3b). From age 7-DAH, fish larvae were not found in the analyzed environment (Ivlev, 1961). This index varies from −1.0 to +1.0, with positive guts. values indicating preferred items, negative electivities indicating avoided items, and zero values indicating items that are not particularly selected. Cladoceran paste was recorded for the first time, although low in Ivlev's index was applied only for cladocerans and copepods, for which all frequency and abundance, in 8-DAH larvae in P2. The frequency and data were available, and for larvae that did not consume fish larvae prey (6 to abundance of insect larvae stayed high whereas cladocerans were 16-DAH). present and abundant. Copepods and adult insects were found in the Gut fullness was used to assess the larvae feeding activity, adopting the larvae from P1 and P3, but in low frequency (Fig. 3c). following scale: empty (gut less than 25% filled), partially empty (25–50%), Cladocerans were preyed more intensely by 10-DAH dorado larvae. partially full (50–75%) and full (over 75%). The insect larvae remained frequent, but in low abundance in most At the same time and place of larvae sampling, 20 l of pond water was larvae, while few copepods and adult insects were selected (Fig. 3d). filtered in a 50 µm mesh net to determine the zooplankton available in the However, in 11-DAH dorado larvae cladocerans tended to be less environment. This volume was concentrated to 180 ml and kept in a 4% buffered frequently eaten and an increase in the frequency of insect larvae was formaldehyde solution. Quantitative and qualitative analyses of the zooplankton community were performed under a light microscope from the organisms observed, although in low abundance. Copepods and adult insects were present in 2 ml sub-samples of the concentrated samples, and the results rare, while cladocerans paste was present again in P2, but low in were expressed as organisms l−1. Identification keys by Koste (1978), Reid frequency and abundance (Fig. 3e). In 13-DAH larvae guts the number (1985), Paggi (1995) and Elmoor-Loureiro (1997) were used to identify the of cladocerans decreased while numbers of insect larvae increased, zooplankton. following an increase in cladocerans and insects pastes. Overall, the 68 D.F.O. Ribeiro, A.P.O. Nuñer / Aquaculture 274 (2008) 65–71

Fig. 3. Specific abundance (Sa %) and frequency of occurrence (f) of food items in the guts of Salminus brasiliensis larvae at different days after hatching (DAH) in ponds 1, 2 and 3. (a) 5 DAH. m=data from morning samples; all other data from afternoon samples; (b) 6 DAH; (c) 8 DAH; (d) 10 DAH; (e) 11 DAH; (f) 13 DAH; (g) 14 DAH; (h) 16 DAH. Subscript denotes pond number. fL = fish larvae (P. lineatus larvae); iL = Insect larvae; C = Cladocerans; Co = Copepods; Ai = Adult Insects; Cp = cladoceran paste and ip = insect paste.

occurrence of copepods and most cladocerans in the guts was low The pattern for cladocerans and copepods consumption was (Fig. 3f). registered by Ivlev's index (Fig. 4), that showed the preference for Insect paste prevailed with high frequency and abundance in the cladocerans, compared to copepods, by dorado larvae until 12-DAH. In guts from 14-DAH dorado larvae (Fig. 3g) and 16-DAH larvae older larvae cladocerans were alternately substituted by copepods in (Fig. 3h). Cladocerans and copepods were almost absent, however an ponds 1 and 2, whereas in pond 3 the substitution pattern was more important increase was observed in the cladoceran paste. stable, with copepods always being selected. D.F.O. Ribeiro, A.P.O. Nuñer / Aquaculture 274 (2008) 65–71 69

available in laboratory conditions. In the afternoon, after the larvae were transferred to outdoor ponds, most larvae fed on large amounts of insect larvae, maintaining the consumption of larger food, but cladocerans were also important in the diet. Most South-American fish larvae consume very low amounts of rotifers and protozoans, preferring larger zooplankton such as cladocerans and copepods (Atencio-Garcia et al., 2003), a condition directly related to the larger size of the mouth since opening (Dostatni et al., 1999; Rowlands et al., 2006; Nunn et al., 2007), especially for those larvae with carnivorous feeding habit that also present larger length at hatching (Sato et al., 2003). These organisms are excellent natural food items for fish, especially during the first 30 days of life, since cladocerans and copepods contain 56.5% and 52.3% crude protein, respectively (Furuya et al., 1999). In the present study, preference for cladocerans was recorded until the 11th DAH since most of the guts analyzed contained these organisms, what could be related to the adequacy of their nutritional value to dorado larvae until this stage. This preference started to shift on 11th DAH, when amounts of insects begun to be recorded in the guts, mainly between the 14th and 16th DAH, showing the importance of these organisms as food sources for freshwater fish. The selection of larger preys was intensified in the diet of 12-DAH and older dorado larvae, also accompanied by the increase of copepods consumption. Galina and Hahn (2004) emphasize the importance of insects, as well as other invertebrates, in fish feeding. Regarding the change in diet, Arcifa and Meschiatti (1993) observed that tucunaré (Cichla sp.) feed on insects when juvenile (b87 mm) and on fish when adult. Several studies showed that Leporinus friderici and Leporinus affinis feed highly on items of animal origin, mainly represented by insects and their larval phases (Braga, 1990; Ferreira et al., 1998; Balassa et al., 2004), which was also recorded in this trial. Insects provide significant amounts of protein and lipids, 59.1% and 12.2%, respectively (Mera et al., 1999), and are rich in minerals such as phosphorus and potassium (Conconi and Fig. 4. Ivlev's electivity index (Ei) for Salminus brasiliensis larvae in ponds Rodríguez, 1977), representing a valuable source of food. from 6 to 16 days after hatching (DAH). a) Pond 1. b) Pond 2. c) Pond 3. Vega-Orellana et al. (2006) studied the activity of some digestive enzymes in larvae of S. brasiliensis fed on larvae of The daily analyses of gut fullness showed a higher frequency of dorado larvae with the gut partially empty and partially full, with no difference (PN0.05) observed between morning and afternoon samples (Fig. 5) or among larvae from the different ponds. Furthermore, natural food predominated over the artificial diet, which was not observed in the gut contents. Similar condition was found to larvae of Piaractus mesopotamicus and Brycon orbignyanus to which artificial food was found in guts only at the age of 17 and 13-DAH, respectively (Senhorini and Fransozo, 1994; Senhorini et al., 2002). The total length and wet weight of larvae varied between 7.6 and 49.6 mm, and 0.0031 and 1.65 g, respectively, but daily growth and weight gain did not differ (PN0.05) among the ponds during this study (Fig. 6).

4. Discussion Fig. 5. Gut fullness of Salminus brasiliensis larvae in ponds from 5 to 16 days Fish larvae prevailed in the guts of dorado larvae with 5- after hatching (DAH). Scale: 0–25%=empty; 25–50%=partially empty; 50– DAH during the morning samples, since it was the sole food 75%=partially full and N75%=full. 70 D.F.O. Ribeiro, A.P.O. Nuñer / Aquaculture 274 (2008) 65–71

Fig. 6. Regression analyses of length and wet weight of Salminus brasiliensis larvae from 5 to 16 days after hatching. Data pooled from ponds 1, 2 and 3.

P. lineatus and observed that the initial activity of pepsin was Acknowledgments recorded at 3-DAH, with increased activity at 7-DAH. In the present study, the first observations of completely digested food The authors thank Consórcio Machadinho and Tractebel in guts, represented by cladoceran paste, occurred only in one Energia for the financial support and Drs. Norma Segatti Hahn pond, with very low frequency and abundance, in 8-DAH and Evoy Zaniboni-Filho for the important suggestions added to dorado larvae. Although the observation period was similar in the text. those studies, in the present study weight gain increased only after 11-DAH and mainly later on, when the partially digested References food became more frequent and abundant. Therefore more efficient digestion was observed after that time, suggesting that Amundsen, P.A., Gabler, H.M., Staldvik, F.J., 1996. 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