Enhanced biodiversity of gut flora and feed efficiency in pond cultured tilapia under reduced frequency feeding strategies

RESEARCH ARTICLE Enhanced biodiversity of gut flora and feed efficiency in pond cultured tilapia under reduced frequency feeding strategies Scott A. SalgerID1, Jimi Reza2, Courtney A. Deck1, Md. Abdul Wahab2,3, David A. Baltzegar1,4, Alexander T. MurrID1, Russell J. Borski1* 1 Department of Biological Sciences, North Carolina State University, Raleigh, North Carolina, United States of America, 2 Department of Fisheries Management, Bangladesh Agricultural University, Mymensingh, Bangladesh, 3 WorldFish, Dhaka, Bangladesh, 4 Genomic Sciences Laboratory, North Carolina State University, Raleigh, North Carolina, United States of America * russell_borski@ncsu.edu Abstract Feed constitutes 50–70% of total production costs of tilapia, one of the most widely cultured finfishes in the world. We evaluated reduced-feeding strategies for improving production efficiency of Nile tilapia (Oreochromis niloticus). In a 12-week pond trial, fish were fed daily, every other day, every third day, or not at all. Ponds were fertilized to enhance natural foods. In a fifth group fish were fed daily without pond fertilization. Fish fed daily with or without pond fertilization and fish fed every other day had higher specific growth rates, survivability, and net production than the other two treatments. Fish feed efficiency and benefit to cost ratio was highest for treatments fed in a pulsatile manner (i.e. fed every other day or every third day) with fish fed on alternate days providing the best net return among all groups. Fish

fed on alternate days had more moderate gene expression levels of intestinal nutrient trans- porters which may allow for a more balanced and efficient nutrient uptake. Fecal microbe analyses identified 145 families of prokaryotic and 132 genera of eukaryotic organisms in tilapia. The highest diversity of prokaryotes was found in fish fed either every other day or daily in fertilized ponds and the highest diversity of eukaryotes was found in fish fed every other day. These studies indicate feeding Nile tilapia on alternate days along with weekly pond fertilization has no deleterious effects on growth, survivability, or production versus daily feeding regimes, but enhances feed efficiency by 76% and provides the greatest net return on investments. Our studies also suggest for the first time that combining alternate- day feeding with pond fertilization produces the greatest microbial biodiversity in the intes- tine that could contribute to enhanced feed efficiency and overall health of tilapia. Introduction Aquaculture production is one of the fastest expanding agriculture industries in the world with growth rates in excess of 40% [1]. Tilapia and other freshwater species, namely carps, will make up 60% of the fish cultured worldwide by 2025. Global production of farmed Nile tilapia (Oreo- chromis niloticus) has increased exponentially since 1985, with over 3.7 million metric tons PLOS ONE PLOS ONE | https://doi.org/10.1371/journal.pone.0236100 July 23, 2020 1 / 23 a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS

Citation: Salger SA, Reza J, Deck CA, Wahab M.A, Baltzegar DA, Murr AT, et al. (2020) Enhanced biodiversity of gut flora and feed efficiency in pond cultured tilapia under reduced frequency feeding strategies. PLoS ONE 15(7): e0236100. https://doi. org/10.1371/journal.pone.0236100 Editor: Michael H. Kogut, USDA-Agricultural Research Service, UNITED STATES Received: December 30, 2019 Accepted: June 30, 2020 Published: July 23, 2020 Peer Review History: PLOS recognizes the benefits of transparency in the peer review process; therefore, we enable the publication of all of the content of peer review and author responses alongside final, published articles. The editorial history of this article is available here: https://doi.org/10.1371/journal.pone.0236100 Copyright: © 2020 Salger et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All Prokaryotic and Eukaryotic microbiome Fastq files can be accessed in the National Center for Biotechnology information (NCBI) under GenBank BioProject