Digestive tract morphology and enzyme activities of juvenile diploid and triploid Atlantic salmon (Salmo salar) fed fishmeal-based diets with or without fish protein hydrolysates.

Silvia Martínez-Llorens,Derrick Kwame Odei,Velmurugu Puvanendran,Malcolm Jobling,Jorge M O Fernandes,Ørjan Hagen,Lars Olav Ulleberg,Sergio Godoy-Olmos,Stefano Peruzzi,Inger-Britt Falk-Petersen,Ana Tomás-Vidal,José L Soengas

doi:10.1371/journal.pone.0245216

Silvia Martínez-Llorens, Derrick Kwame Odei + Show 10 more

Open Access

https://doi.org/10.1371/journal.pone.0245216

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Abstract

Triploid, sterile Atlantic salmon (Salmo salar) could make a contribution to the development of the farming industry, but uncertainties about the performance and welfare of triploids have limited their adoption by farmers. In this study, we compared the ontogeny of digestive tract morphology and enzyme activities (pepsin, trypsin, chymotrypsin, alkaline phosphatase and aminopeptidase) of diploid and triploid Atlantic salmon. Fish were fed diets based on fishmeal (STD) or a mix of fishmeal and hydrolysed fish proteins (HFM) whilst being reared at low temperature from start-feeding to completion of the parr-smolt transformation. Fish weights for each ploidy and feed combination were used to calculate thermal growth coefficients (TGCs) that spanned this developmental period, and the data were used to examine possible relationships between enzyme activities and growth. At the end of the experiment, faeces were collected and analyzed to determine the apparent digestibility coefficients (ADCs) of the dietary amino acids (AAs). Digestive tract histo-morphology did not differ substantially between ploidies and generally reflected organ maturation and functionality. There were no consistent differences in proteolytic enzyme activities resulting from the inclusion of HFM in the diet, nor was there improved digestibility and AA bioavailability of the HFM feed in either diploid or triploid fish. The triploid salmon had lower ADCs than diploids for most essential and non-essential AAs in both diets (STD and HFM), but without there being any indication of lower intestinal protease activity in triploid fish. When trypsin-to-chymotrypsin activity and trypsin and alkaline phosphatase (ALP) ratios (T:C and T:ALP, respectively) were considered in combination with growth data (TGC) low T:C and T:ALP values coincided with times of reduced fish growth, and vice versa, suggesting that T:C and T:ALP may be used to predict recent growth history and possible growth potential.

Highlights

Triploid Atlantic salmon (Salmo salar) may have an important role to play in the sustainable expansion of the aquaculture industry in Norway and other salmon-producing countries
No obvious differences could be observed in the digestive tract histomorphology of newlyhatched diploid and triploid fish (S1 Fig)
Connective tissue was dominant in the folds and columnar epithelium was facing the lumen

Summary

Introduction

Triploid Atlantic salmon (Salmo salar) may have an important role to play in the sustainable expansion of the aquaculture industry in Norway and other salmon-producing countries. The salmonfarming industry in Tasmania (Australia) is an exception, where triploid salmon are farmed to circumvent early sexual maturation of fish as grilse [2]. Diploid and triploid Atlantic salmon show differences in the gross morphology of the digestive system [6] and in culturable gut microbiota [7] with potential consequences for nutrient utilization, growth and health. Little is known about the effects of feed formulations on digestive tract structure and function of triploid Atlantic salmon, but several studies carried out on diploid salmon have shown dietary effects on gut mucosal structure (e.g [9,10,11,12,13,14]). Triploid salmon require more dietary phosphorus than diploids during early development to achieve comparable bone mineralization [19]. There are indications that triploid salmon parr may have different micronutrient requirements and metabolic responses to dietary supplementation than their diploid counterparts when fed low levels of marine ingredients [20,21]

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