Elsevier

Aquaculture

Volume 561, 15 December 2022, 738667
Aquaculture

DHA-enrichment of live and compound feeds influences the incidence of cannibalism, digestive function, and growth in the neotropical catfish Pseudoplatystoma punctifer (Castelnau, 1855) during early life stages

https://doi.org/10.1016/j.aquaculture.2022.738667Get rights and content

Highlights

  • Cannibalism in Pseudoplatystoma punctifer is affected by nutrition.

  • Dietary DHA supplied to larvae conditions the digestive physiology of juveniles.

  • Dietary DHA during the larval phase reduces cannibalism at the juvenile stage.

  • Dietary DHA during the early juvenile stage of P. punctifer promotes growth.

Abstract

Pseudoplatystoma punctifer is a highly appreciated fish species native to the Amazon basin, whose commercial farming has been hampered by low survival during early life stages due to the high incidence of cannibalism and the low acceptability of compound diets at weaning. Dietary DHA is known to promote digestive system development and maturation and growth, whereas its deficiency induces stress. The aim of this study was to evaluate the effect of dietary DHA supplementation on the incidence of cannibalism, digestive physiology, and growth performance during the early life stages of P. punctifer to improve current feeding protocols. Four dietary treatments were generated using a commercial enrichment product with high DHA content. Fish larvae were fed non-enriched or enriched Artemia from 4 to 15 days post fertilization (dpf) and fed a non-enriched or enriched compound diet from 15 to 26 dpf, coinciding with the start of the juvenile stage. Growth, survival, incidence of cannibalism, proximate and fatty acid composition, histology of the intestine and liver, and quantitative gene expression of the main digestive enzymes (amy, try, ctr, pga, pla2, and lpl) were analyzed in the different dietary groups at the end of each feeding period. Results showed that dietary DHA supplementation influenced P. punctifer in a developmental stage-dependent manner. In particular, DHA-enriched Artemia provided during the larval stage contributed to reduce the incidence of cannibalism and improved survival at the early juvenile stage, while enriching the compound diet improved growth. The expression level of genes involved in protein and carbohydrate digestion (ctr, amy) was higher in groups fed enriched Artemia despite that both enriched and non-enriched Artemia displayed similar proximate composition, suggesting that different dietary fatty acid profiles may modulate the expression of these digestive enzyme precursors. The group transitioning from enriched Artemia to non-enriched compound diet showed a higher expression of most genes at the early juvenile stage. At the histological level, the group fed non-enriched Artemia and compound diet showed a significant accumulation of lipids in the intestine relative to the liver, contrary to the rest of the groups that showed similar amounts of lipids in both tissues, indicating a more balanced lipid metabolism. The group fed both DHA-enriched Artemia and compound diet provided the best results in terms of growth, survival, incidence of cannibalism, and digestive physiology. In conclusion, this study showed that the nutritional history during the larval period affected fish nutrition and behavior during the early juvenile stage.

Introduction

The most cultivated catfish species in South America belong to the genus Pseudoplatystoma Bleeker, 1862, which are piscivorous migratory species native to the major river basins of South America and have total lengths of up to 140 cm (Buitrago–Suárez and Burr, 2007; Gisbert et al., 2022). Current aquaculture production mostly relies on interspecific (e.g., Pseudoplatystoma reticulatum x Pseudoplatystoma corruscans) and intergeneric hybrids with omnivorous pimelodid species (Leiarius marmoratus or Phractocephalus hemioliopterus), since the latter present less cannibalism during early life stages and more readily accept compound diets than the Pseudoplatystoma spp. parent species (Gisbert et al., 2022; Hashimoto et al., 2012). However, given the risks associated to the culture of hybrid species (Hashimoto et al., 2015; Hashimoto et al., 2013), research efforts are being made to develop more efficient culture practices for pure Pseudoplatystoma species, as is the case for Pseudoplatystoma punctifer (Castelnau, 1855), a species native to the Amazon basin (e.g., Castro-Ruiz et al., 2021a, Castro-Ruiz et al., 2021b; Castro-Ruiz et al., 2019; Darias et al., 2015; Gisbert et al., 2014). The commercial farming of this highly appreciated species has been hampered by low survival during early life stages due to the high incidence of cannibalism and the low acceptability of compound diets at weaning (Baras et al., 2011; Gisbert et al., 2014). However, recent studies have found a strong correlation between nutrition and the cannibalistic behavior in this species; in particular, that when using a feeding protocol adapted to digestive capacities and nutritional needs during early life stages, growth and survival are substantially improved (Castro-Ruiz et al., 2021a, Castro-Ruiz et al., 2021b; Castro-Ruiz et al., 2019; Darias et al., 2015).

During the early life stages of fish, an optimal dietary fatty acid composition, especially polyunsaturated fatty acids (PUFA), is essential to promote adequate development and growth (Lund et al., 2012; Mourente, 2003; Watanabe, 1993). Freshwater species have lower requirements for n-3 highly unsaturated fatty acids (HUFA) than marine fish larvae (Verreth et al., 1994). However, the fatty acid composition of Artemia, naturally lacking n-3 HUFAs (Sargent et al., 1999), may also affect growth in freshwater species (Bengtson et al., 1991). In the case of P. punctifer, previous studies have shown that Artemia nauplii did not satisfy the nutritional needs of this species from 12 days post-fertilization (dpf) onwards, coinciding with the beginning of the juvenile stage, leading to decreased growth and increased incidence of cannibalism (Castro-Ruiz et al., 2019; Darias et al., 2015; Gisbert et al., 2014). DHA is particularly important during the larval development due to its structural role in biomembranes, especially in neural tissues, such as the retina and the brain (Bell et al., 1996; Mourente, 2003; Wassall and Stillwell, 2008). Dietary DHA provided in adequate quantities promotes digestive system development and maturation, growth, survival, and normal morphogenesis (Cahu et al., 2003; Takeuchi, 2014; Villeneuve et al., 2005; Zambonino Infante and Cahu, 1999), whereas dietary DHA deficiencies induce physiological stress (Lund et al., 2012). Considering that stress can favor cannibalistic behavior (Naumowicz et al., 2017) and that inadequate nutrition has shown to influence the incidence of cannibalism in P. punctifer (Castro-Ruiz et al., 2021b; Darias et al., 2015), the aim of this study was to evaluate the influence of dietary DHA supplementation on the incidence of cannibalism, digestive physiology, and growth performance during the early life stages in P. punctifer. A feeding trial in which Artemia metanauplii and compound diets were either enriched or not with DHA was used to elucidate whether the dietary requirements in DHA varied throughout development. The effects of these feeding regimes on the development and function of the digestive system of early juveniles of P. punctifer were analyzed at histological and molecular levels. Regarding the latter, the study focused on the expression of the main digestive enzyme precursors α-amylase (amy), phospholipase A2 (pla2), lipoprotein lipase (lpl), trypsinogen (try), chymotrypsinogen (ctr), and pepsinogen (pga). The outcomes of this study will contribute to improve the understanding of the nutritional needs of this species during early development and to ameliorate the deficiencies in the nutritional composition of feeds, as well as to optimize the feeding protocols used, in order to promote adequate growth and health in this Amazonian species.

Section snippets

Rearing protocol

Spawning of a sexually mature couple of P. punctifer (♀: 4.15 kg; ♂: 1.15 kg) from a broodstock maintained in captivity at the Instituto de Investigaciones de la Amazonia Peruana (IIAP, Iquitos, Peru) was hormonally induced. The female and male were injected intramuscularly with carp pituitary extract (Argent Chemical Laboratories, Inc., Redmond, WA, USA) at 5 mg kg−1 and 1 mg kg−1 of body weight, respectively. Hormone injections were administered in two doses 12 h apart: the first at 10% and

Growth performance

Growth in terms of WW and TL is shown in Fig. 2. At 14 dpf, individuals presented similar WW among dietary groups, whereas individuals from T2 and T3 groups displayed higher WW than those from C and T1 groups at 26 dpf (Fig. 2; P < 0.05). There were no differences in TL among the different dietary treatments at both sampling times (14 and 26 dpf) (P > 0.5).

Incidence and temporal occurrence of cannibalism

The incidence of cannibalism was reduced by half in all the enriched groups (T1, T2, and T3) and, as a consequence, survival increased

Discussion

Present results showed that the DHA enrichment during the Artemia feeding period (larval period) did not have any effect on growth performance. This could be related to the fact that freshwater species are able to synthesize DHA de novo from 18:3 precursors and thus often have lower n-3 HUFA requirements than marine fish larvae (Bell and Sargent, 2003). Similarly, a nutritional study performed in Clarias gariepinus showed that changes in dietary fatty acid composition did not affect larval

Conclusions

The present results showed that dietary DHA levels influenced the physiology and cannibalistic behavior of P. punctifer in a stage-dependent manner. In particular, providing DHA-enriched Artemia during the larval stage contributed to reducing the incidence of cannibalism and improved survival, whereas the DHA-enriched compound diet during the early juvenile stage improved growth. Altogether, the group fed both DHA-enriched Artemia and compound diet (T3) provided the best results in terms of

Funding

This research was supported by the International Joint Laboratory ‘Evolution and Domestication of the Amazonian Ichthyofauna’ (LMI EDIA, IRD-IIAP-UAGRM, France, Peru and Bolivia) and the IRTA.

CRediT authorship contribution statement

Diana Castro-Ruiz: Formal analysis, Investigation, Writing – original draft, Visualization. Karl B. Andree: Investigation, Resources, Writing – review & editing. Julian Magris: Investigation. Christian Fernández-Méndez: Investigation, Writing – review & editing. Carmen García-Dávila: Resources. Enric Gisbert: Formal analysis, Methodology, Investigation, Writing – review & editing, Supervision, Resources. Maria J. Darias: Conceptualization, Methodology, Investigation, Writing – original draft,

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

The authors thank Marta Sastre and Alicia Estévez (IRTA) for their contributions to proximate and fatty acids analyses. This work was done in the framework of the network LARVAplus ‘Strategies for the development and improvement of fish larvae production in Ibero-America’ (117RT0521) funded by the Ibero-American Program of Science and Technology for Development (CYTED, Spain). D.C.-R. benefited from a travel grant from the National Fund for Scientific, Technological Development and

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