Abstract
The present study investigated the effects of enriched Artemia franciscana with β-carotene of Dunaliella salina on color, skin carotenoid, and mucosal immune responses of platyfish, Xiphophorus maculatus. To this end, one hundred and eighty platyfish with an initial weight of 0.9 ± 0.03 g were randomly assigned into four groups in triple and were daily fed on three times. The first and second groups were fed with commercial food (control) and unenriched A. franciscana (Un-EA), respectively. In addition, the third and fourth groups were fed with enriched A. franciscana with castor oil (oil-EA) and enriched A. franciscana with β-carotene (β-carotene EA) for 8 weeks, respectively. Based on results, the highest amount of carotenoids (112.4 ± 22.79 μg g−1) was significantly observed in the group fed with β-carotene EA while the lowest amount (24.31 ± 2.36 μg g−1) was found in the group fed Un-EA. As regards lysozyme, total immunoglobulin, and alkaline phosphatase activity of the mucus, the highest amounts were detected in fish with β-carotene EA as 84.5 ± 19.09 mg dL−1, 6.4 ± 0.41 mg dL−1, and 477 ± 39.59 U L−1, respectively. Based on skin colorization results, the group fed with β-carotene EA had no significant difference regarding the transparency, yellow color, and opacity, while a* index significantly increased in this group in comparison with the control group. However, the Hue index significantly decreased in the β-carotene EA group compared with the control group. In conclusion, A. franciscana enriched with β-carotene of D. salina enhanced the mucosal immune responses and improved the skin carotenoids as well as a* index in platyfish X. maculatus.
Similar content being viewed by others
References
Alishahi M, Karamifar M, Mesbah M (2015) Effects of astaxanthin and Dunaliella salina on skin carotenoids, growth performance and immune response of Astronotus ocellatus. Aquac Int 23(5):1239–1248
Alishahi M, Ranjbar M, Ghorbanpour M, Peyghan R, Mesbah M (2010) Effects of dietary aloe vera on specific and nonspecific immunity in the common carp (Cyprinus carpio). Int J Vet Res 4(3):85–91
Ángeles Esteban M (2012) An overview of the immunological defenses in fish skin. ISRN Immunology 2012:1–29
Aranishi F, Mano N, Hirose H (1998) Fluorescence localization of epidermal cathepsins L and B in the Japanese eel. Fish Physiol Biochem 19(3):205–209
Austin B, McIntosh D (1988) Natural antibacterial compounds on the surface of rainbow trout, Salmo gairdneri Richardson. J Fish Dis 11(3):275–277
Azimirad M, Meshkini S, Ahmadifard N, Hoseinifar SH (2016) The effects of feeding with synbiotic (Pediococcus acidilactici and fructooligosaccharide) enriched adult Artemia on skin mucus immune responses, stress resistance, intestinal microbiota and performance of angelfish (Pterophyllum scalare). Fish Shellfish Immunol 54:516–522
Bendich A (1989) Carotenoids and the immune response. J Nutr 119(1):112–115
Bendich A, Shapiro SS (1986) Effect of β-carotene and canthaxanthin on the immune responses of the rat. J Nutr 116(11):2254–2262
Bogacz-Radomska L, Harasym J (2018) β-Carotene—properties and production methods. Food Qual Saf 2(2):69–74
Bon JA, Leathers TD, Jayaswal RK (1997) Isolation of astaxanthin-overproducing mutants of Phaffia rhodozyma. Biotechnol Lett 19(2):109–112
Boonyaratpalin M, Thongrod S, Supamattaya K, Britton G, Schlipalius L (2001) Effects of β-carotene source, Dunaliella salina, and astaxanthin on pigmentation, growth, survival, and health of Penaeus monodon. Aquac Res 32:182–190
Caruso G, Denaro MG, Caruso R, Mancari F, Genovese L, Maricchiolo G (2011) Response to short term starvation of growth, hematological, biochemical and non-specific immune parameters in European sea bass (Dicentrarchus labrax) and blackspot sea bream (Pagellus bogaraveo). Mar Environ Res 72(1–2):46–52
Chew BP, Park JS (2004) Carotenoid action on the immune response. J Nutr 134(1):257S–261S
Cho JH, Park IY, Kim MS, Kim SC (2002) Matrix metalloproteinase 2 is involved in the regulation of the antimicrobial peptide parasin I production in catfish skin mucosa. FEBS Lett 531(3):459–463
Choubert G, Cravedi J-P, Laurentie M (2009) Effect of alternate distribution of astaxanthin on rainbow trout (Oncorhynchus mykiss) muscle pigmentation. Aquaculture 286(1–2):100–104
Choubert G, Mendes-Pinto MM, Morais R (2006) Pigmenting efficacy of astaxanthin fed to rainbow trout Oncorhynchus mykiss: effect of dietary astaxanthin and lipid sources. Aquaculture 257(1–4):429–436
Cohen AE, Dugan LE, Hendrickson DA, Martin FD, Huynh J, Labay BJ, Casarez MJ (2014) Population of variable platyfish (Xiphophorus variatus) established in Waller Creek, Travis County. Texas Southwest Nat 59:413–419
de la Mora GI, Arredondo-Figueroa J, Ponce-Palafox J, Vernon-Carter J (2006) Comparison of red chilli (Capsicum annuum) oleoresin and astaxanthin on rainbow trout (Oncorhynchus mykiss) fillet pigmentation. Aquaculture 258(1–4):487–495
Dickerson H, Clark T (1998) Ichthyophthirius multifiliis: a model of cutaneous infection and immunity in fishes. Immunol Rev 166:377–384
Emeish S (2012) Production of natural β-carotene from Dunaliella living in the Dead Sea. Jordan J Earth Environ Sci 4(2):23–27
Fouz B, Devesa S, Gravningen K, Barja J, Toranzo A (1990) Antibacterial action of the mucus of turbot. Bull Eur Assoc Fish Pathol 10:5
Gomez-Gil B, Herrera-Vega MA, Abreu-Grobois FA, Roque A (1998) Bioencapsulation of two different Vibrio species in nauplii of the brine shrimp (Artemia franciscana). Appl Environ Microbiol 64(6):2318–2322
Gouveia L, Rema P, Pereira O, Empis J (2003) Colouring ornamental fish (Cyprinus carpio and Carassius auratus) with microalgal biomass. Aquac Nutr 9(2):123–129
Hadi Jamali, Nasrollah Ahmadifard, Farzaneh Noori, Enric Gisbert, Alicia Estevez, Naser Agh (2019) Lecithin-enriched Artemia combined with inert diet and its effects on reproduction and digestive enzymes of Aequidens rivulatus. Aquaculture 511:734253
Harpaz S, Padowicz D (2007) Color enhancement in the ornamental dwarf cichlid Microgeophagus ramirezi by addition of plant carotenoids to the fish diet. Bamidgeh 59(4):95–200
Hoseinifar SH, Hosseini M, Paknejad H, Safari R, Jafar A, Yousefi M, Van Doan H, Mozanzadeh MT (2019) Enhanced mucosal immune responses, immune related genes and growth performance in common carp (Cyprinus carpio) juveniles fed dietary Pediococcus acidilactici MA18/5M and raffinose. Dev Comp Immunol 94:59–65
Jamali H, Ahmadifard N, Noori F, Agh N, Gisbert E (2018) Improving coofeeding strategies for Neotropical green terror cichlid (Aequidens rivulatus) larvae with lecithin-enriched Artemia franciscana nauplii: effects on survival, growth performance and body composition. Aquac Res 49(12):3909–3918
Javed M, Durrani F-R, Hafeez A, Khan RU, Ahmad I (2009) Effect of aqueous extract of plant mixture on carcass quality of broiler chicks. ARPN J Agric Biol Sci 4(1):37–40
Kalinowski C, Izquierdo M, Schuchardt D, Robaina L (2007) Dietary supplementation time with shrimp shell meal on red porgy (Pagrus pagrus) skin colour and carotenoid concentration. Aquaculture 272(1–4):451–457
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
Magnadóttir B (2006) Innate immunity of fish (overview). Fish Shellfish Immunol 20(2):137–151
Montoya-Martínez C, Vega-Villasante F, Nolasco-Soria H, Espinosa-Chaurand L, Carrillo-Farnés O, Olvera-Uribe G (2014) Effects of dietary antioxidant of tomato extract and lycopene on Carassius auratus and Xiphophorus maculatus. Rev MVZ Córdoba 19(2):4059–4071
Nagashima Y, Sendo A, Shimakura K, Shiomi K, Kobayashi T, Kimura B, Fujii T (2001) Antibacterial factors in skin mucus of rabbitfishes. J Fish Biol 58(6):1761–1765
Nelis HJ, De Leenheer A (1991) Microbial sources of carotenoid pigments used in foods and feeds. J Appl Bacteriol 70(3):181–191
Nhan HT, Minh TX, Liew HJ, Hien TTT, Jha R (2019) Effects of natural dietary carotenoids on skin coloration of false clownfish (Amphiprion ocellaris Cuvier, 1830). Aquac Nutr 25:1–7. https://doi.org/10.1111/anu.12887
Nigam AK, Kumari U, Mittal S, Mittal AK (2017) Evaluation of antibacterial activity and innate immune components in skin mucus of Indian major carp, Cirrhinus mrigala. Aquac Res 48(2):407–418
Ponce-Palafox JT, Arredondo-Figueroa JL, Vernon-Carter EJ (2006) Carotenoids from plants used in diets for the culture of the Pacific white shrimp (Litopenaeus vannamei). Revista Mexicana de Ingeniería Química 5:2
Ramamoorthy K, Bhuvaneswari S, Sankar G, Sakkaravarthi K (2010) Proximate composition and carotenoid content of natural carotenoid sources and its colour enhancement on marine ornamental fish Amphiprion ocellaris (Cuveir, 1880). World J Fish Mar Sci 2(6):545–550
Robertson AR (1977) The CIE 1976 color-difference formulae. Color Res Appl 2(1):7–11
Shephard KL (1993) Mucus on the epidermis of fish and its influence on drug delivery. Adv Drug Deliv Rev 11(3):403–417
Shlomai P, Ben-Amotz A, Margalith P (1991) Production of carotene stereoisomers by Phycomyces blakesleeanus. Appl Microbiol Biotechnol 34(4):458–462
Sicuro B (2018) Nutrition in ornamental aquaculture: the raise of anthropocentrism in aquaculture? Rev Aquac 10(4):791–799
Sorgeloos P, Dhert P, Candreva P (2001) Use of the brine shrimp, Artemia spp., in marine fish larviculture. Aquaculture 200(1–2):147–159
Subramanian S, MacKinnon SL, Ross NW (2007) A comparative study on innate immune parameters in the epidermal mucus of various fish species. Comp Biochem Physiol B: Biochem Mol Biol 148(3):256–263
Sun X, Chang Y, Ye Y, Ma Z, Liang Y, Li T, Jiang N, Xing W, Luo L (2012) The effect of dietary pigments on the coloration of Japanese ornamental carp (koi, Cyprinus carpio L.). Aquaculture 342:62–68
Supamattaya K, Kiriratnikom S, Boonyaratpalin M, Borowitzka L (2005) Effect of a Dunaliella extract on growth performance, health condition, immune response and disease resistance in black tiger shrimp (Penaeus monodon). Aquaculture 248(1–4):207–216
Thompson I, Choubert G, Houlihan D, Secombes C (1995) The effect of dietary vitamin A and astaxanthin on the immunocompetence of rainbow trout. Aquaculture 133(2):91–102
Torrissen, O.J. and Naevdal, G (1984) Pigmentation of salmonids-genetical variation in carotenoid deposition in rainbow trout. Aquaculture 38(1):59–l66
Uribe C, Folch H, Enriquez R, Moran G (2011) Innate and adaptive immunity in teleost fish: a review. Vet Med (Praha) 56(10):486–503
Wang H, Tang W, Zhang R, Ding S (2019) Analysis of enzyme activity, antibacterial activity, antiparasitic activity and physico-chemical stability of skin mucus derived from Amphiprion clarkii. Fish Shellfish Immunol 86:653–661
Yasir I, Qin JG (2010) Effect of dietary carotenoids on skin color and pigments of false clownfish, Amphiprion ocellaris, Cuvier. J World Aquacult Soc 41(3):308–318
Yokoyama A, Miki W (1995) Composition and presumed biosynthetic pathway of carotenoids in the astaxanthin-producing bacterium Agrobacterium aurantiacum. FEMS Microbiol Lett 128(2):139–144
Acknowledgments
The authors wish to thank all of the people who helped with the research in Artemia and Aquaculture Research Institute and Faculty of Natural Resources, Urmia University (Urmia-Iran).
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Abdollahi, Y., Ahmadifard, N., Agh, N. et al. β-Carotene-enriched Artemia as a natural carotenoid improved skin pigmentation and enhanced the mucus immune responses of platyfish Xiphophorus maculatus. Aquacult Int 27, 1847–1858 (2019). https://doi.org/10.1007/s10499-019-00437-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10499-019-00437-8