The synergistic impact of Spirulina and selenium nanoparticles mitigates the adverse effects of heat stress on the physiology of rabbits bucks

PLOS ONE RESEARCH ARTICLE The synergistic impact of Spirulina and selenium nanoparticles mitigates the adverse effects of heat stress on the physiology of rabbits bucks Ibrahim T. El-Ratel1, Mawada E. Elbasuny1, Hamdy A. El-Nagar2, Abdel-Khalek E. AbdelKhalek3, Ali A. El-Raghi1, Mohammed Fouad El Basuini ID4,5*, Khaled H. El-Kholy1, Sara F. Fouda6 a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 1 Department of Animal, Poultry and Fish Production, Faculty of Agriculture, Damietta University, Damietta, Egypt, 2 Department of Biotechnology Research, Animal Production Research Institute, Agricultural Research Center, Giza, Egypt, 3 Department of Animal Production, Faculty of Agriculture, Mansoura University, Mansoura, Egypt, 4 Department of Animal Production, Faculty of Agriculture, Tanta University, Tanta, Egypt, 5 Faculty of Desert Agriculture, King Salman International University, South Sinai, Egypt, 6 Department of Poultry Production, Faculty of Agriculture, Mansoura University, Mansoura, Egypt * OPEN ACCESS Citation: El-Ratel IT, Elbasuny ME, El-Nagar HA, Abdel-Khalek A-KE, El-Raghi AA, El Basuini MF, et al. (2023) The synergistic impact of Spirulina and selenium nanoparticles mitigates the adverse effects of heat stress on the physiology of rabbits bucks. PLoS ONE 18(7): e0287644. https://doi.org/ 10.1371/journal.pone.0287644 Editor: Lamiaa Mostafa Radwan, Ain Shams University Faculty of Agriculture, EGYPT Received: January 23, 2023 Accepted: June 12, 2023 Published: July 12, 2023 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.0287644 Copyright: © 2023 El-Ratel 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 relevant data are within the paper and its Supporting Information files. Abstract Heat stress has a detrimental effect on animal fertility, particularly testicular functions, including reduced sperm output and quality, which causes an economic loss in the production of rabbits. The present trial investigated the efficacy of dietary Spirulina (SP) (Arthrospira platensis), selenium nanoparticles (SeNPs), and their combination (SP-SeNPs) on semen quality, haemato-biochemical, oxidative stress, immunity, and sperm quality of heatstressed (HS) rabbit bucks. Sixty mature bucks (APRI line) were distributed into 6 groups of ten replicates under controlled conditions. Bucks in the 1st group (control-NC) were kept under normal conditions (11–22˚C; 40–45% RH% = relative humidity), while the 2nd group (control-HS) was kept under heat stress conditions (32±0.50˚C; 60–66% RH %). The control groups were fed a commercial pelleted diet and the other four heat-stressed groups were fed a commercial pelleted diet with 1 g SP, 25 mg SeNPs, 1 g SP+25 mg SeNPs, and 1 g SP+50 mg SeNPs per kg diet, respectively. The dietary inclusion of SP, SeNPs, and their combinations significantly increased hemoglobin, platelets, total serum protein, high-density lipoproteins, glutathione, glutathione peroxidase, superoxide dismutase, and seminal plasma testosterone while decreased triglycerides, total cholesterol, urea, creatinine, and malondialdehyde compared with the control-HS. Red blood cells, packed cell volume, serum albumin, and testosterone significantly increased, while SeNPs, SP+SeNPs25, and SP+SeNPs50 significantly decreased low-density lipoproteins, aspartate, and alanine amino transferees. Total antioxidant capacity substantially increased in serum and seminal plasma, while seminal plasma malondialdehyde decreased in 25 or 50 mg of SeNPs+SP/kg groups. All supplements significantly improved libido, sperm livability, concentration, intact acrosome, membrane integrity, total output in fresh semen, and sperm quality in cryopreserved semen. SP-SeNPs50 had higher synergistic effect than SP-SeNPs25 on most PLOS ONE | https://doi.org/10.1371/journal.pone.0287644 July 12, 2023 1 / 18 PLOS ONE Funding: The author(s) received no specific funding for this work. Competing interests: The authors have declared that no competing interests exist. Spirulina and selenium nanoparticles mitigate heat stress impacts on rabbits bucks different variables studied. In conclusion, the dietary inclusion of SP plus SeNPs50 has a synergistic effect and is considered a suitable dietary supplement for improving reproductive efficiency, health, oxidative stress, and immunity of bucks in the breeding strategy under hot climates. 1. Introduction Heat stress has a detrimental effect on animal fertility and causes significant economic losses in rabbit production [1–4]. Oxidative stress performs a crucial function in semen quality, quantity, and fertility of sperm cells. Under heat stress (HS), lipid peroxidation increases, particularly when the temperature and humidity exceed the normal ranges [1, 5]. HS negatively alters testicular functions and causes DNA fragmentation [2], leading to a reduction in the output and quality of spermatozoa [3] and animal well-being [4]. HS increases sperm abnormality by impairing the mitotic division of spermatocytes during spermatogenesis [5]. These negative impacts of HS on bucks are partially associated with generating free radicals [6]. Spermatozoa of rabbits are rich in metabolic activity and poly-unsaturated fatty acids in their plasma membrane; therefore, a rise in free radicals and lipid peroxidation reduces sperm fertilizing ability [1, 7]. Additionally, the consequences of heat stress include oxidative stress, organ damage or dysfunction, endocrine disorders, immunity deficiency, impaired metabolism and energy imbalance, ultimately leading to reduced animal productivity and increased mortality [8, 9]. In order to lessen the harmful impacts of HS and to avoid buck infertility by limiting reactive oxygen species (ROS) production in rabbits, a variety of tools are available. In this way, using natural antioxidants lessens the deleterious impacts of HS on males by assisting with various physiological and metabolic processes [8–13]. Spirulina, a planktonic blue-green alga, exhibits anti-viral, anti-microbial, anti-inflammatory, hepato-protective, and antiparasitic activities and contains antioxidative pigments [14] because it contains a vibrant nutritional profile, particularly proteins, essential amino acids, fatty acids, vitamins, minerals, phytopigments, phycocyanin, polysaccharides, carotenoids, chlorophyll, and phenolic compounds [15– 18]. Nano-technology is applied in animal nutrition, and the most basic approaches in this area are nanoparticles (NPs) with 1–100 (...truncated)