Phenol-rich fulvic acid as a water additive enhances growth, reduces stress, and stimulates the immune system of fish in aquaculture
1.
FAO. The State of World Fisheries and Aquaculture 2018. (Food and Agriculture Organization of the United Nations, 2018).
2.
Zuo, Z.-H., Shang, B.-J., Shao, Y.-C., Li, W.-Y. & Sun, J.-S. Screening of intestinal probiotics and the effects of feeding probiotics on the growth, immune, digestive enzyme activity and intestinal flora of Litopenaeus vannamei. Fish Shellfish Immunol. 86, 160–168. https://doi.org/10.1016/j.fsi.2018.11.003 (2019).
CAS Article PubMed Google Scholar
3.
Hoseinifar, S. H., Sun, Y., Wang, A. & Zhou, Z. Probiotics as means of diseases control in aquaculture, a review of current knowledge and future perspectives. Front. Microbiol. 9, 2429. https://doi.org/10.3389/fmicb.2018.02429 (2018).
Article PubMed PubMed Central Google Scholar
4.
Reverter, M., Bontemps, N., Lecchini, D., Banaigs, B. & Sasal, P. Use of plant extracts in fish aquaculture as an alternative to chemotherapy: Current status and future perspectives. Aquaculture 433, 50–61. https://doi.org/10.1016/j.aquaculture.2014.05.048 (2014).
Article Google Scholar
5.
Lieke, T. et al. Sustainable aquaculture requires environmental-friendly treatment strategies for fish diseases. Rev. Aquac. 12, 943–965. https://doi.org/10.1111/raq.12365 (2019).
Article Google Scholar
6.
Noga, E. J. Fish Disease: Diagnosis and Treatment. Vol. 2nd Edn 143–148 (Wiley, 2011).
7.
Haugarvoll, E., Bjerkås, I., Nowak, B. F., Hordvik, I. & Koppang, E. O. Identification and characterization of a novel intraepithelial lymphoid tissue in the gills of Atlantic salmon. J. Anat. 213, 202–209. https://doi.org/10.1111/j.1469-7580.2008.00943.x (2008).
Article PubMed PubMed Central Google Scholar
8.
Zhang, Z., Swain, T., Bøgwald, J., Dalmo, R. A. & Kumari, J. Bath immunostimulation of rainbow trout (Oncorhynchus mykiss) fry induces enhancement of inflammatory cytokine transcripts, while repeated bath induce no changes. Fish Shellfish Immunol. 26, 677–684. https://doi.org/10.1016/j.fsi.2009.02.014 (2009).
CAS Article PubMed Google Scholar
9.
Jeney, G. & Anderson, D. P. Enhanced immune response and protection in rainbow trout to Aeromonas salmonicida bacterin following prior immersion in immunostimulants. Fish Shellfish Immunol. 3, 51–58. https://doi.org/10.1006/fsim.1993.1005 (1993).
Article Google Scholar
10.
Steinberg, C. E. W. Ecology of Humic Substances in Freshwaters: Determinants from Geochemistry to Ecological Niches. Vol. 1 (Springer, 2003).
11.
Haitzer, M., Höss, S., Traunspurger, W. & Steinberg, C. E. W. Effects of dissolved organic matter (DOM) on the bioconcentration of organic chemicals in aquatic organisms—A review. Chemosphere 37, 1335–1362. https://doi.org/10.1016/S0045-6535(98)00117-9 (1998).
ADS CAS Article PubMed Google Scholar
12.
Thurman, E. M. Organic Geochemistry of Natural Waters. Vol. 1 (Nijhoff, M./Junk, W. Publishers, 1985).
13.
IHSS. What are Humic Substances? http://humic-substances.org .
14.
Meinelt, T. et al. Reduction in vegetative growth of the water mold Saprolegnia parasitica (Coker) by humic substance of different qualities. Aquat. Toxicol. 83, 93–103. https://doi.org/10.1016/j.aquatox.2007.03.013 (2007).
CAS Article PubMed Google Scholar
15.
Yamin, G. et al. The protective effect of humic substances and water and sludge from a recirculating aquaculture system on Aeromonas salmonicida infection in common carp (Cyprinus carpio). J. Fish Dis. 40, 1783–1790. https://doi.org/10.1111/jfd.12645 (2017).
CAS Article PubMed Google Scholar
16.
Kodama, H., Denso & Nakagawa, T. Protection against atypical Aeromonas salmonicida infection in carp (Cyprinus carpio L.) by oral administration of humus extract. J. Vet. Med. Sci. 69, 405–408, https://doi.org/10.1292/jvms.69.405 (2007).
17.
Fierro-Coronado, J. A. et al. Dietary fulvic acid effects on survival and expression of immune-related genes in Litopenaeus vannamei challenged with Vibrio parahaemolyticus. Aquac. Res. 49, 3218–3227. https://doi.org/10.1111/are.13789 (2018).
CAS Article Google Scholar
18.
Gao, Y. et al. Effects of fulvic acid on growth performance and intestinal health of juvenile loach Paramisgurnus dabryanus (Sauvage). Fish Shellfish Immunol. 62, 47–56. https://doi.org/10.1016/j.fsi.2017.01.008 (2017).
CAS Article PubMed Google Scholar
19.
Saebelfeld, M., Minguez, L., Griebel, J., Gessner, M. O. & Wolinska, J. Humic dissolved organic carbon drives oxidative stress and severe fitness impairments in Daphnia. Aquat. Toxicol. 182, 31–38. https://doi.org/10.1016/j.aquatox.2016.11.006 (2017).
CAS Article PubMed Google Scholar
20.
Steinberg, C. E. W. et al. Stress by poor food quality and exposure to humic substances: Daphnia magna responds with oxidative stress, lifespan extension, but reduced offspring numbers. Hydrobiologia 652, 223–236 (2010).
CAS Article Google Scholar
21.
Hseu, Y.-C. et al. Humic acid induced genotoxicity in human peripheral blood lymphocytes using comet and sister chromatid exchange assay. J. Hazard. Mater. 153, 784–791. https://doi.org/10.1016/j.jhazmat.2007.09.024 (2008).
CAS Article PubMed Google Scholar
22.
Savy, D. et al. Quantitative structure-activity relationship of humic-like biostimulants derived from agro-industrial by products and energy crops. Front. Plant Sci. 11, 581. https://doi.org/10.3389/fpls.2020.00581 (2020).
Article PubMed PubMed Central Google Scholar
23.
Pörs, Y. & Steinberg, C. E. Humic substances delay aging of the photosynthetic apparatus of Chara hispida. J. Phycol. 48, 1522–1529. https://doi.org/10.1111/jpy.12012 (2012).
CAS Article PubMed Google Scholar
24.
Muscolo, A., Sidari, M., Francioso, O., Tugnoli, V. & Nardi, S. The auxin-like activity of humic substances is related to membrane interactions in carrot cell cultures. J. Chem. Ecol. 33, 115–129. https://doi.org/10.1007/s10886-006-9206-9 (2007).
CAS Article PubMed Google Scholar
25.
Gilbert, M., Bährs, H., Steinberg, C. E. W. & Wilhelm, C. The artificial humic substance HS1500 does not inhibit photosynthesis of the green alga Desmodesmus armatus in vivo but interacts with the photosynthetic apparatus of isolated spinach thylakoids in vitro. Photosynth. Res. https://doi.org/10.1007/s11120-018-0513-0 (2018).
Article PubMed Google Scholar
26.
Perdue, E. M. in Encyclopedia of Inland Waters (ed Gene E. Likens) 806–819 (Academic Press, 2009).
27.
Chen, J., Gu, B., LeBoeuf, E. J., Pan, H. & Dai, S. Spectroscopic characterization of the structural and functional properties of natural organic matter fractions. Chemosphere 48, 59–68. https://doi.org/10.1016/S0045-6535(02)00041-3 (2002).
ADS CAS Article PubMed Google Scholar
28.
Lieke, T., Zhang, X., Steinberg, C. E. & Pan, B. Overlooked risks of biochars: Persistent free radicals trigger neurotoxicity in Caenorhabditis elegans. Environ. Sci. Technol. 52, 7981–7987. https://doi.org/10.1021/acs.est.8b01338 (2018).
ADS CAS Article PubMed Google Scholar
29.
Liao, S., Pan, B., Li, H., Zhang, D. & Xing, B. Detecting free radicals in biochars and determining their ability to inhibit the germination and growth of corn, wheat and rice seedlings. Environ. Sci. Technol. 48, 8581–8587. https://doi.org/10.1021/es404250a (2014).
ADS CAS Article PubMed Google Scholar
30.
Yuan, Y. et al. Electron transfer capacity as a rapid and simple maturity index for compost. Biores. Technol. 116, 428–434. https://doi.org/10.1016/j.biortech.2012.03.114 (2012).
CAS Article Google Scholar
31.
Scott, D. T., McKnight, D. M., Blunt-Harris, E. L., Kolesar, S. E. & Lovley, D. R. Quinone moieties act as electron acceptors in the reduction of humic substances by humics-reducing microorganisms. Environ. Sci. Technol. 32, 2984–2989. https://doi.org/10.1021/es980272q (1998).
ADS CAS Article Google Scholar
32.
Abdel-Tawwab, M., Abdel-Rahman, A. M. & Ismael, N. E. M. Evaluation of commercial live bakers’ yeast, Saccharomyces cerevisiae as a growth and immunity promoter for Fry Nile tilapia, Oreochromis niloticus (L.) challenged in situ with Aeromonas hydrophila. Aquaculture 280, 185–189, https://doi.org/10.1016/j.aquaculture.2008.03.055 (2008).
33.
Sanmanee, N. & Areekijseree, M. The effects of fulvic acid on copper bioavailability to porcine oviductal epithelial cells. Biol. Trace Elem. Res. 135, 162–173. https://doi.org/10.1007/s12011-009-8508-5 (2010).
CAS Article PubMed Google Scholar
34.
Hasan, M. & Soto, D. Improving Feed Conversion Ratio and Its Impact on Reducing Greenhouse Gas Emissions in Aquaculture. (FAO, 2017).
35.
Besson, M. et al. Environmental impacts of genetic improvement of growth rate and feed conversion ratio in fish farming under rearing density and nitrogen output limitations. J. Clean. Prod. 116, 100–109 (2016).
Article Google Scholar
36.
Tort, L. Stress and immune modulation in fish. Dev. Comp. Immunol. 35, 1366–1375. https://doi.org/10.1016/j.dci.2011.07.002 (2011).
CAS Article PubMed Google Scholar
37.
Mommsen, T. P., Vijayan, M. M. & Moon, T. W. Cortisol in teleosts: Dynamics, mechanisms of action, and metabolic regulation. Rev. Fish Biol. Fisheries 9, 211–268. https://doi.org/10.1023/A:1008924418720 (1999).
Article Google Scholar
38.
Meinelt, T. et al. Humic substances affect physiological condition and sex ratio of swordtail (Xiphophorus helleri Heckel). Aquat. Sci. 66, 239–245. https://doi.org/10.1007/s00027-004-0706-9 (2004).
Article Google Scholar
39.
Bly, J. E., Quiniou, S. M. & Clem, L. W. Environmental effects on fish immune mechanisms. Dev. Biol. Stand. 90, 33–43 (1997).
CAS PubMed Google Scholar
40.
Conde-Sieira, M., Chivite, M., Míguez, J. M. & Soengas, J. L. Stress effects on the mechanisms regulating appetite in teleost fish. Front. Endocrinol. 9, https://doi.org/10.3389/fendo.2018.00631 (2018).
41.
Kalamarz-Kubiak, H. in Corticosteroids (ed Ali Gamal Al-Kaf) Chap. 7, 183–155 (InTechOpen, 2018).
42.
Timofeyev, M. A. et al. Natural organic matter (NOM) induces oxidative stress in freshwater amphipods Gammarus lacustris Sars and Gammarus tigrinus (Sexton). Sci. Total Environ. 366, 673–681. https://doi.org/10.1016/j.scitotenv.2006.02.003 (2006).
ADS CAS Article PubMed Google Scholar
43.
Xin, Z. et al. Species sensitivity analysis of heavy metals to freshwater organisms. Ecotoxicology 24, 1621–1631. https://doi.org/10.1007/s10646-015-1500-2 (2015).
CAS Article PubMed Google Scholar
44.
Demers, N. E. & Bayne, C. J. The immediate effects of stress on hormones and plasma lysozyme in rainbow trout. Dev. Comp. Immunol. 21, 363–373. https://doi.org/10.1016/S0145-305X(97)00009-8 (1997).
CAS Article PubMed Google Scholar
45.
Dupré-Crochet, S., Erard, M. & Nüβe, O. ROS production in phagocytes: why, when, and where?. J. Leukoc. Biol. 94, 657–670. https://doi.org/10.1189/jlb.1012544 (2013).
CAS Article PubMed Google Scholar
46.
Geng, X. et al. Effects of dietary chitosan and Bacillus subtilis on the growth performance, non-specific immunity and disease resistance of cobia, Rachycentron canadum. Fish Shellfish Immunol. 31, 400–406. https://doi.org/10.1016/j.fsi.2011.06.006 (2011).
CAS Article PubMed Google Scholar
47.
Fries, C. & Tripp, M. Depression of phagocytosis in Mercenaria following chemical stress. Dev. Comp. Immunol. 4, 233–244. https://doi.org/10.1016/S0145-305X(80)80027-9 (1980).
CAS Article PubMed Google Scholar
48.
Sesti-Costa, R., Baccan, G. C., Chedraoui-Silva, S. & Mantovani, B. Effects of acute cold stress on phagocytosis of apoptotic cells: The role of corticosterone. NeuroImmunoModulation 17, 79–87. https://doi.org/10.1159/000258690 (2010).
CAS Article PubMed Google Scholar
49.
Narnaware, Y. K., Baker, B. I. & Tomlinson, M. G. The effect of various stresses, corticosteroids and adrenergic agents on phagocytosis in the rainbow trout Oncorhynchus mykiss. Fish Physiol. Biochem. 13, 31–40. https://doi.org/10.1007/BF00004117 (1994).
CAS Article PubMed Google Scholar
50.
Dhabhar, F. S. & McEwen, B. S. Acute stress enhances while chronic stress suppresses cell-mediated immunity in vivo: A potential role for leukocyte trafficking. Brain Behav. Immun. 11, 286–306 (1997).
CAS Article Google Scholar
51.
Adel, M., Abedian Amiri, A., Zorriehzahra, J., Nematolahi, A. & Esteban, M. Á. Effects of dietary peppermint (Mentha piperita) on growth performance, chemical body composition and hematological and immune parameters of fry Caspian white fish (Rutilus frisii kutum). Fish Shellfish Immunol. 45, 841–847, https://doi.org/10.1016/j.fsi.2015.06.010 (2015).
52.
Christybapita, D., Divyagnaneswari, M. & Michael, R. D. Oral administration of Eclipta alba leaf aqueous extract enhances the non-specific immune responses and disease resistance of Oreochromis mossambicus. Fish Shellfish Immunol. 23, 840–852. https://doi.org/10.1016/j.fsi.2007.03.010 (2007).
CAS Article PubMed Google Scholar
53.
Ragland, S. A. & Criss, A. K. From bacterial killing to immune modulation: Recent insights into the functions of lysozyme. PLoS Pathog. 13, https://doi.org/10.1371/journal.ppat.1006512 (2017).
54.
Ansorg, R. & Rochus, W. Studies on the antimicrobial effect of natural and synthetic humic acids (author’s transl). Arzneimittelforschung 28, 2195–2198 (1978).
CAS PubMed Google Scholar
55.
Hertkorn, N. et al. Comparative analysis of partial structures of a peat humic and fulvic acid using one-and two-dimensional nuclear magnetic resonance spectroscopy. J. Environ. Qual. 31, 375–387. https://doi.org/10.2134/jeq2002.3750 (2002).
CAS Article PubMed Google Scholar
56.
Zheng, X. et al. Comparing electron donating/accepting capacities (EDC/EAC) between crop residue-derived dissolved black carbon and standard humic substances. Sci. Total Environ. 673, 29–35. https://doi.org/10.1016/j.scitotenv.2019.04.022 (2019).
ADS CAS Article PubMed Google Scholar
57.
Weil, J. A. & Bolton, J. R. Electron Paramagnetic Resonance: Elementary Theory and Practical Applications. Vol. 2 (Wiley, 2007).
58.
Hopkins, K. D. Reporting fish growth: A review of the basics 1. J. World Aquac. Soc. 23, 173–179. https://doi.org/10.1111/j.1749-7345.1992.tb00766.x (1992).
Article Google Scholar
59.
Fulton, T. W. The Rate of Growth of Fishes. 141–241 (Scotland, 1904).
60.
Barnham, C. A. & Baxter, A. F. Condition Factor, K, for Salmonid Fish. (Department of Primary Industries, 2003).
61.
Secombes, C. J. in Techniques in Fish Immunology Vol. 1 (eds J. S. Stolen et al.) 137–154 (SOS Publications, 1990).
62.
Chettri, J. K., Holten-Andersen, L. & Buchmann, K. Factors influencing in vitro respiratory burst assays with head kidney leucocytes from rainbow trout, Oncorhynchus mykiss (Walbaum). J. Fish Dis. 33, 593–602. https://doi.org/10.1111/j.1365-2761.2010.01160.x (2010).
CAS Article PubMed Google Scholar
63.
Crampe, M., Farley, S. R., Langston, A. & Pulsford, A. L. in Methodology in Fish Diseases Research (eds A.C. Barnes, G.A. Davidson, M. P. Hiney, & D. McIntosh) 81–91 (Fisheries Research Services, 1998).
64.
Begemann, H. & Rastetter, J. Atlas of Clinical Haematology 9–21 (Springer, Berlin, 1972).
Google Scholar
65.
Sitja-Bobadilla, A., Palenzuela, O. & Alvarez-Pellitero, P. Immune response of turbot, Psetta maxima (L.) (Pisces: Teleostei), to formalin-killed scuticociliates (Ciliophora) and adjuvanted formulations. Fish Shellfish Immunol. 24, 1–10, https://doi.org/10.1016/j.fsi.2007.06.007 (2008).
66.
Siwicki, A. in Fish Diseases Diagnosis and Preventions Methods Vol. 1 (eds A.K. Siwicki, D.P. Anderson, & J. Waluga) 105–111 (Wydawnictwo Instytutu Rybactwa Strodladowego, 1993).
67.
Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254. https://doi.org/10.1016/0003-2697(76)90527-3 (1976).
CAS Article Google Scholar
68.
Amado, L. L. et al. A method to measure total antioxidant capacity against peroxyl radicals in aquatic organisms: Application to evaluate microcystins toxicity. Sci. Total Environ. 407, 2115–2123. https://doi.org/10.1016/j.scitotenv.2008.11.038 (2009).
ADS CAS Article PubMed Google Scholar
69.
Hollander, M. & Wolfe, D. A. Nonparametric Statistical Methods. Vol. 3 115–120 (Wiley, 2015).
70.
Dunn, O. J. Multiple comparisons using rank sums. Technometrics 6, 241–252. https://doi.org/10.2307/1266041 (1964).
Article Google Scholar
71.
Siegal, S. & Castellan Jr., N. J. Nonparametric Statistics for the Behavioral Sciences. (McGraw-Hill, 1988).
72.
Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B (Methodological) 57, 289–300 (1995). More
