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ANIMAL PRODUCTION • Cienc. Rural 55 (8) • 2025 • https://doi.org/10.1590/0103-8478cr20240219 linkcopy

Open-access Weaning of Colossoma macropomum larvae of different ages using different feeding strategies

Desmame de larvas de Colossoma macropomum de diferentes idades utilizando diferentes estratégias de alimentação

AuthorshipSCIMAGO INSTITUTIONS RANKINGS

    ABSTRACT:

    The present study evaluated the weaning of Colossoma macropomum. 6,720 larvae were distributed in 28 tanks (28 L) in a recirculating aquaculture system. Artemia nauplii were offered to the larvae in increasing quantities. The abrupt weaning treatments then began by directly providing extruded commercial feed on the 6th (W6), 11th (W11) and 16th (W16) day of larviculture. The co-feeding treatments (W6co, W11co and W16co) involved a period of co-feeding, whereby the amount of Artemia nauplii was reduced by 20% each day while simultaneously offering a commercial diet. Treatment W6 and W6co had lower weight after the 15th day (21.25 ± 5.35 mg and 25.96 ± 8.52 mg, respectively) and 20th day (34.94 ± 21.24 mg and 41.87 ± 22.61 mg, respectively) day of larviculture. W16 and W16co had greater weight after the 25th day (216.12 ± 43.19 mg and 220.40 ± 14.92 mg, respectively) and 30th day (380.67 ± 88.35mg and 366.96 ± 88.87 mg, respectively). W16 and W16co had greater length at the end of 30 days of larviculture in relation to weaning at younger ages, with a final average of 28.215 ± 1.580 mm and 28.179 ±1.260 mm, respectively. All treatments experienced a reduction in SGR between the 6th and 10th day of larviculture, Treatments W6co, W16 and W16co had higher values (18.80 ± 9.25% day-1, 18.48 ± 3.69% day-1 and 21.21 ± 2.29% day-1, respectively) and W11 the lowest values between the 21st and 25th day (4.17 ± 3.51% day-1). Survival after 30 days was lowest for W6 (64.02 ± 4.49%) and highest for W11co, W16 and W16co (80.89 ± 2.07%, 81.07 ± 2.42% and 85.63 ± 8.30%, respectively). We concluded that, for C. macropomum larviculture, treatments W16 and W16co are better weaning strategies for growth performance and survival.

    Key words:
    feeding; tambaqui; food management; abrupt transition; co-feeding.

    RESUMO:

    O presente estudo avaliou o desmame de Colossoma macropomum. Um total de 6.720 larvas foram distribuídas em 28 tanques (28L) em sistema de recirculação de água. Náuplios de Artemia foram oferecidos às larvas em quantidades crescentes. Os tratamentos de desmame abrupto iniciaram-se então com fornecimento direto de ração comercial extrusada no 6º (W6), 11º (W11) e 16º (W16) dia de larvicultura. Os tratamentos de co-alimentação (W6co, W11co e W16co) envolveram um período de co-alimentação, em que a quantidade de náuplios de Artemia foi reduzida em 20% a cada dia, oferecendo simultaneamente uma dieta comercial. Os tratamentos W6 e W6co apresentaram menor peso após o 15º dia (21,25 ± 5,35 mg e 25,96 ± 8,52 mg, respectivamente) e 20º dia (34,94 ± 21,24 mg e 41,87 ± 22,61 mg, respectivamente) de larvicultura. W16 e W16co apresentaram maior peso após o 25º dia (216,12 ± 43,19mg e 220,40 ± 14,92 mg, respectivamente) e 30º dia (380,67 ± 88,35 mg e 366,96 ± 88,87 mg, respectivamente). W16 e W16co tiveram maior comprimento ao final de 30 dias de larvicultura em relação ao desmame em idades mais jovens, com média final de 28,215 ± 1,580 mm e 28,179 ± 1,260mm, respectivamente. Todos os tratamentos apresentaram redução na taxa de crescimento especifico (TCE) entre o 6º e o 10º dia de larvicultura. Os tratamentos W6co, W16 e W16co apresentaram maiores valores (18,80 ± 9,25% dia-1, 18,48 ± 3,69% dia-1 e 21,21 ± 2,29% dia-1, respectivamente) e W11 os menores valores entre o 21º e o 25º dia (4,17 ± 3,51% dia-1). A sobrevivência após 30 dias foi menor para W6 (64,02 ± 4,49%) e maior para W11co, W16 e W16co (80,89 ± 2,07%, 81,07 ± 2,42% e 85,63 ± 8,30%, respectivamente). Concluímos que, para a larvicultura de C. macropomum, os tratamentos W16 e W16co são melhores estratégias para desempenho de crescimento e sobrevivência.

    Palavras-chave:
    alimentação; tambaqui; manejo alimentar; transição abrupta; coalimentação

    INTRODUCTION

    The initial feeding of fish larvae in the laboratory still depends mainly on the use of live prey (AYA et al., 2021). In addition to being well accepted, the use of rotifers and, especially, Artemia nauplii, provide adequate nutrition for growth and survival in freshwater fish larviculture (LUZ & ZANIBONI FILHO, 2001; LUZ & PORTELLA, 2005; SANTOS et al., 2022). However, the high cost and limited availability of these live organisms are significant obstacles to their use in the laboratory (PEOPLE-LE RUVET et al., 1993; AYA et al., 2021; SANTOS et al., 2022). Thus, weaning has become extremely important (HIEN et al., 2017; LJUBOBRATOVIC et al., 2020) to reduce dependence on the use of these living organisms (CELIK, 2020; LJUBOBRATOVIC et al., 2020) and; consequently, costs at this stage of production (ALVES et al., 2006; LJUBOBRATOVIC et al., 2020).

    Successful weaning of different species has been shown to be more efficient with older larvae (KESTEMONT et al., 2007; PALINSKA-ZARSKA et al., 2014; LACZYNSKA et al., 2016), which may be related to the activities of digestive enzymes (SUZER et al., 2013). Most enzymes for digesting food particles are already available in larvae and become more available as growth progresses (CAHU & ZAMBONINO-INFANTE, 1994). Thus, inappropriately performed weaning, either due to age or feeding strategy, results in lower growth and survival (PEOPLE-LE RUYET et al., 1993).

    Weaning protocols can vary among different fish species (CAHU & ZAMBONINO-INFANTE, 2001). It can be done abruptly or through co-feeding (HAMZA et al., 2007; COLBURN et al., 2012; LJUBOBRATOVIC et al., 2015; LIPSCOMB et al., 2020), with the use of a combination of live prey and commercially mashed food during a certain period (co-feeding), a strategy used to improve larval performance (CANAVATE & FERNANDEZ-DÍAZ, 1999; NHU et al., 2010; CHEPKIRUI-BOIT et al., 2011), as it improves acceptance of commercial diets (STEJSKAL et al., 2018). Conversely, sudden weaning or abrupt transition, which includes the substitution of live food for inert food, has had limited success (HERATH & ATAPATHTHU, 2013).

    Tambaqui (Colossoma macropomum) is a native species of the Amazon River basin that is widely cultivated in different regions of Brazil (CHUNG et al., 2021; PEIXE BR, 2024), being the second most produced fish in the country (PEIXEBR, 2024). The species presents fast growth, good feed conversion and rusticity in controlled systems (ASSIS et al., 2020; SANTOS et al., 2021b; BOAVENTURA et al., 2021; SILVA et al., 2021; ANANIAS et al., 2023). Its larviculture has been carried out using abrupt weaning after the use of live food (SANTOS et al., 2021a; SANTOS et al., 2022; SANTOS et al., 2024); however, other ages and feeding strategies need to be evaluated in order to further optimize its larviculture.

    Therefore, the present study evaluated the weaning of C. macropomum under larviculture using different strategies at different ages.

    MATERIALS AND METHODS

    Animals and accommodations

    The experiment was carried out in the Laboratório de Aquacultura (LAQUA) of the Universidade Federal de Minas Gerais (UFMG, Brazil). Initially, C. macropomum larvae were acquired from the Biofish Aquicultura fish farm located in the city of Porto Velho - RO, Brazil. Four-days post-hatching larvae were packed in plastic bags, each containing 5 L of water, and transported by plane. The time between the closing and opening of the transport bags was 24 hours.

    At LAQUA, the larvae were acclimatized and stored in 28-L circular tanks in a recirculating aquaculture system (RAS), where they were fed with Artemia nauplii ad libitum to recover from the stress of the trip. The water of the RAS was maintained at a temperature of 28.02 ± 0.34 ºC with dissolved oxygen of 5.67 ± 0.30 mg L-1 (measured with a YSI 6920VZ2 multiparameter probe), pH of 7.83 ± 0.33 (measured with a Hanna HI98130 portable multiparameter probe) and total ammonia of 0.25 ± 0.00 mg L-1 (measured by Labcon Test colorimetric method).

    The experiment used 6,720 larvae aged five days post-hatching with initial total length and body weight of 4.23 ± 0.01 mm and 0.0011 ± 0.03 g, respectively, distributed in 24 tanks (28 L) mounted in the RAS with a larval density of 10 larvae L-1. Four RASs (mechanical filter, biological filter, return reservoir and UV filter) and four tanks were used. The tanks were adapted with a water outlet located in the center and an air diffuser coupled to a central blower. The water was directed to a gravity filtration system. The mechanical filter was composed of a glass wool blanket fixed to a support (35x25x15 cm), while the biological filter, of the same dimensions, was filled with 8 L gravel (1 cm in average diameter) to fix nitrifying bacteria. The return tank (80x60x45 cm), with a useful volume of 120 L, was equipped with a submersible pump (Bomba Submersa Sb 2000; Sarlo Better Equipamentos Ltda) with a flow rate of 1950 L h-1, and a heating system (power of 300 W) with temperature controller (GONÇALVES JUNIOR et al., 2020). Water flow in the tanks was 1.85 ± 0.2 L min-1 with four total tank changes every hour. Larviculture was carried out in slightly salinized water at 2.11 ± 0.52 g of salt L-1 (Sal garça LTFA Refinery, Mossoró, Rio Grande do Norte, Brazil. Ingredients: Sodium Chloride and Sodium Ferrocyanide; SANTOS et al., 2021a; SANTOS et al., 2022), measured (with a Hanna HI98130 portable multiparameter probe) during the 30 days of larviculture (JOMORI et al., 2013; SANTOS et al., 2021a; SANTOS et al., 2022). The photoperiod was 12 hours with luminosity of 150 lux on the water surface (Digital Lux Meter, model: ITLD 260).

    All procedures described herein were approved by the Committee for Ethics in Animals Use (CEUA / UFMG - nº 8/2021).

    Feeding and weaning

    Six forms of weaning were tested (Figure 1A), three with abrupt transition (direct replacement of live food with commercial diet) and three with a co-feeding period (five days of mixed feeding before the exclusive offer of commercial diet) applied to larvae of different ages (6, 11 and 16 days of larviculture or 11, 16 and 21 days post-hatching). Thus, a completely randomized experimental design was used with four replications for each treatment. Artemia nauplii were fed to the larvae in increasing amounts, offering 500 Artemia nauplii larva-1 daily until the 5th day of larviculture, 750 nauplii larva-1 from the 6th to 10th day of larviculture and 1,000 nauplii larva-1 from the 11th to the 15th day of larviculture, divided into three feedings a day (8:00, 12:00 and 16:00 h). Treatments with abrupt transition (W6, W11 and W16) started receiving commercial extruded diet on the 6th, 11th and 16th day of larviculture, respectively, at a rate of 10% of the biomass of each tank (SANTOS et al., 2021a; SANTOS et al., 2022), divided into three feedings a day (8:00, 12:00 and 16:00 h). For the co-feeding treatments (W6co, W11co and W16co), the amount of live food provided during the mixed feeding period was reduced by 20% each day while at the same time an extruded commercial diet was offered at the rate of 10% of the biomass of each tank (SANTOS et al., 2021a; SANTOS et al., 2022) (Figure 1B). The diet used in the experiment was Qualis Acqua fingerlings 1.5 mm, containing 460 g Kg-1 of crude protein, 80 g kg-1 of ether extract and 1030 mg kg-1 of vitamin C. However, due to the small size of the fish, this starter feed was ground in a pin mill to a particle size of < 200 μm.

    thumbnail of Figure 1
    Figure 1
    Scheme showing the different weaning strategies used for C. macropomum larvae of different ages (A). Feeding management with Artemia nauplii during co-feeding in C. macropomum larviculture (B).

    The tanks were cleaned in the morning and afternoon with a 10% change of volume per day. Replacement was with water under the same conditions as that of the RAS.

    The water quality parameters of the RAS reservoir during the experimental period were: temperature 28.24 ± 0.24 ºC, dissolved oxygen 6.25 ± 1.15 mg L-1, water pH 7.41 ± 0.34, electrical conductivity 4.05 ± 0.35 μS cm-1 and total ammonia 0.23 ± 0.11 mg L-1.

    Growth and survival

    Animal performance was evaluated by performing biometrics at an interval of five days (n = 20 animals per treatment) and at the end of the experiment (n = 80 animals per treatment). Growth was determined by measuring weight (W) and total length (TL) of the animals using a precision digital scale (Analytical Balance Ay-220-220 g × 0.0001 g Marte - Brazil) and a digital caliper with a resolution of 0.01 mm / 0.0005 (Starrett electronic caliper measuring tool EC799A-6/150, hardened stainless steel metal, 6-inch range, 0.005” resolution, LCD digital measurement reading, Massachusetts - USA), respectively. For biometry, the larvae were anesthetized with eugenol solution (20 mg L-1) (SANTOS et al., 2021a; SANTOS et al., 2022) and subsequently returned to their original tank. Daily specific growth rate (SGR) was calculated using the weight data and the formula:

    SGR (% day-1) = 100 x (lnWf - lnWi) / interval between biometrics (days)

    Where Wi is initial weight and Wf is final weight.

    Survival rate was determined after 30 days of larviculture using the following formula:

    Survival (%) = (Number of live larvae x 100) / (Total initial number of larvae per tank)

    Statistical analysis

    Data were first submitted to the Shapiro-Wilk normality test and then analyzed by ANOVA and Tukey’s test with 5% probability. Statistical analyses were performed using the InfoStat program (DI RIENZO et al., 2015).

    RESULTS

    Weight was not influenced by the treatments during the first five days of larviculture, when all animals received the same amount of food (P > 0.05). Treatment W6 had lower weight after the 10th day of larviculture (P < 0.05). Treatments W6 and W6co had lower weight after the 15th and 20th day of larviculture (P < 0.05). Treatments W11co, W16 and W16co had greater weight after the 25th of larviculture. Treatments W16 and W16co had greater weight after the 30th day of larviculture compared to animals that were subjected to weaning at younger ages, regardless of feeding strategy (P < 0.05) (Table 1).

    Thumbnail
    Table 1
    Weight (W), length and SRG (Daily specific growth rate) (mean ± standard deviation) of C. macropomum submitted to different forms of weaning at different ages for 30 days of larviculture.

    Length was also not influenced by the treatments during the first five days of larviculture (P > 0.05). Treatments W6 and W6co had shorter length beginning after the 20th day of larviculture, similar to weight, while W16 and W16co had greater length at the end of 30 days of larviculture in relation to weaning at younger ages (P < 0.05) (Table 1).

    SGR was not influenced by the treatments for the first five days of larviculture (P > 0.05) (Table 1). All treatments experienced a reduction in SGR between the 6th and 10th day of larviculture, with W6 and W6co having the lowest value (P < 0.05). However, W6 experienced an increase in SGR during the experiment to equal that of other treatments after the 30th day of larviculture. SGR was not influenced by the treatments between the 11th and 20th day of larviculture (P > 0.05). Treatments W6co W16 and W16co had higher (19.50 ± 3.68%) and W11 lower (4.17 ± 3.51%) values for SGR between the 21st and 25th day of larviculture (P < 0.05). SGR was not influenced by the treatments between the 26th and 30th day of larviculture (8.97 ± 3.73%; P > 0.05).

    Treatment W6 had the lowest survival after 30 days of larviculture while W16, W11co and W16co had the highest (P < 0.05) (Figure 2).

    thumbnail of Figure 2
    Figure 2
    Survival (mean ± standard deviation) of C. macropomum submitted to different forms of weaning at different ages after 30 days of larviculture. Different letters indicate a significant difference between treatments (Tukey’s test at 5% probability).

    DISCUSSION

    For the successful weaning of C. macropomum it is important to consider the age of the larvae as well as the feeding strategy used. The ideal weaning procedure can reduce larval production costs, promote standardization of larviculture procedures and provide nutrients to fish larvae according to their nutritional needs (HAMRE et al., 2013; WANG et al., 2020). The ideal time to start weaning is specific to each species (CAHU et al., 2009; LAZO et al., 2011; PRADHAN et al., 2014) and mainly related to the development of the digestive system and larval ability to ingest, digest and absorb nutrients from imposed diets (CAHU & ZAMBONINO-INFANTE, 2001; HAMRE et al., 2013), with most enzymes becoming more available with advancing age of the animals (CAHU & ZAMBONINO-INFANTE, 1994; AYA et al., 2021). The results of the present study of different weaning strategies for C. macropomum larviculture are directly linked to this phenomenon, since weaning was more successful with older larvae.

    Weaning of animals after 6 or 11 days of larviculture led to worse performance results, regardless of the feeding strategy adopted. Early weaning strategies at 8 and 16 days post-hatching had the worst growth results for silver therapon (Leiopotherapon plumbeus) larvae, with a low ability of early-stage larvae to use artificial diet during the early stages of feeding (AYA et al., 2021). Abrupt weaning of the Chinese catfish (Leiocassis longirostris) was also not recommended for before 10 days post-hatching by LIU et al. (2012), whereas it could start at 6 days post-hatching with co-feeding. JOMORI et al. (2008) demonstrated that early weaning (3 and 6 days of feeding with live food and dry diet in the subsequent days) of pacu (Piaractus mesopotamicus) larvae had a negative effect on fish growth, with better results for animals that received live food for at least 12 days. Confirming these data, LEITÃO et al. (2011) demonstrated that pacu larvae fed with formulated diets beginning with the first feeding had worse performance indices than did larvae fed with a weaning strategy beginning on the 12th day of larviculture. Weaning age also affected larval growth of Pseudochromis fridmani (CHEN et al., 2022), with a tendency for slower larval growth with early weaning (before 32 days post-hatching) or a shorter period of Artemia feeding. Thus, as observed in the present study, there is an evident need to evaluate the ideal age for performing weaning with different species to achieve greater animal growth.

    Inadequate weaning time can make fish hungry due to poor food digestion. Without adequate intake of nutrients during the weaning period, fish will use stored energy to maintain basic metabolism and, thus, allocate less for growth, resulting in reduced growth during the weaning period, as observed for sea bass (Paralabrax maculatofasciatus; CIVERA-CERECEDO et al., 2008) and Senegalese sole (Solea senegalensis; ENGROLA et al., 2007). The present study found the best growth in weight and length to be for both abrupt weaning and co-feeding at 16 days. FREITAS et al. (2019) investigated weaning strategies for P. mesopotamicus larvae and demonstrated that late feeding transition (12 days of Artemia feeding and 6 days of cofeeding) can be performed without compromising larval growth and survival. The present study found that the use of Artemia nauplii until the 15th day of larviculture, followed by abrupt weaning and co-feeding weaning (W16co) during the 16th to 20th day of larviculture, to be the best strategies for weight and length gain of C. macropomum larvae.

    The weaning carried out in treatments W6 and W6co between the 6th and 10th day of larviculture, showed that the larvae did not adapt well to the initial feeding of commercial diet, presenting the lowest SGR values. Lower SGR values were found for larvae subjected to weaning after a shorter time in larviculture for Heterobranchus longifilis (TOKO et al., 2008), Betta splendens (FOSSE et al., 2013) and P. mesopotamicus (FREITAS et al., 2019). These findings may be directly related to enzymatic activity, which can be delayed or interrupted by early weaning or feeding with an inadequate nutritional composition (CAHU & ZAMBONINO-INFANTE, 2001). Thus, the enzymatic activity of C. macropomum must be evaluated for a better understanding of the functioning of the enzymatic system of this species during larviculture. However, the present study observed a recovery of SGR, indicating adaptation to the new diet. Digestive enzyme secretion was initiated in Heterotis niloticus larvae of 24 and 26 days post-hatching (ADITE et al., 2009), as demonstrated by higher SGR for late weaning compared to larvae weaned at 11, 13 and 15 days post-hatching. The weaning strategies of the present study did not influence SGR between the 26th and 30th day of hatching, demonstrating a similar adaptation of C. macropomum larvae to formulated diets.

    Larval survival is one of the most important parameters for determining the success of weaning (LIU et al., 2012; PRADHAN et al., 2014; KRÓL & ZIELINSKI, 2015; STEJSKAL et al., 2017). It is commonly accepted that weaning fish larvae for feeding on a commercial diet requires protocols to facilitate adaptation during a period of extensive morphological and physiological changes (STEJSKAL et al., 2017). The worst survival for C. macropomum in the present study was for W6, which reinforces the importance of age and feeding strategy in weaning. Early weaning of larvae results in low survival, as reported for Ompok bimaculatus with a range of 58.7 to 66.2% (PRADHAN et al., 2014), H. longifilis with 36.5% (TOKO et al., 2008), Channa striata with 2.3 to 15.3%, Channa micropeltes with 30.5 to 37.5% (HIEN et al., 2017) and P. mesopotamicus with 25.7% (FREITAS et al., 2019). However, survival of C. macropomum in the present study increased when weaning was performed on larvae of more advanced ages, with the highest being recorded for W11co, W16 and W16co. Weaning with larval co-feeding resulted in a higher survival rate for Nishikigoi Cyprinus carpio (FOSSE et al., 2018), after six days of exclusive feeding with Artemia, followed by 12 days of co-feeding (Artemia nauplii + dry diet), in addition to producing larvae with greater weight when compared to those fed exclusively with live food. Co-feeding is intended to improve nutrition and the condition of the larvae to more readily accept commercial diets when live feed is withdrawn (STEJSKAL et al., 2017). However, this finding was confirmed in the present study only for survival, and not for performance.

    CONCLUSION

    The present study concludes that, for C. macropomum larviculture, treatments W16 and W16co are better weaning strategies for growth performance and survival.

    ACKNOWLEDGEMENTS

    This research was funded by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq-Brasil - 402952/2021-9), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG-Brasil - APQ-01531-21), and was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Brasil - Finance code 001. R.K. Luz received research grants from CNPq (CNPq No. 310170/2023-0). F.A.C Santos received research grants from CNPq (CNPq No.150883/2024-2).

    REFERENCES

    • CR-2024-0219.R1
    • BIOETHICS AND BIOSECURITY COMMITTEE APPROVAL
      All protocols were approved by the Ethics Committee on the Use of Animals (CEUA / UFMG - nº 8/2021) of the Universidade Federal de Minas Gerais (UFMG). Thus, the authors assume full responsibility for the presented data and are available for possible questions, should they be required by the competent authorities.

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    Publication Dates

    • Publication in this collection
      26 May 2025
    • Date of issue
      2025

    History

    • Received
      15 Apr 2024
    • Accepted
      11 Nov 2024
    • Reviewed
      28 Feb 2025
    Creative Common - by 4.0
    This is an open-access article distributed under the terms of the Creative Commons Attribution License
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