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
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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