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Dietary carotenoids and bacterial infection in wild and domestic convict cichlids (Amatitlania spp.)

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Abstract

Honest signaling of carotenoid-based ornaments may be reinforced by dietary limitation and by competing physiological demands for carotenoids. This study measured dietary carotenoids in a natural population of the convict cichlid Amatitlania siquia, a species in which females possess carotenoid-based ventral coloration. The zoonotic pathogen Edwardsiella spp. was detected in wild A. siquia, but carotenoids in the stomachs of wild fish did not vary significantly with parasite infection. We followed this with a laboratory experiment on domestic convict cichlids to test whether increased dietary carotenoid (ß-carotene) would decrease oxidative stress and facilitate clearance of experimental infections of Edwardsiella tarda. Fish maintained on a medium carotenoid diet (similar to the diets of wild fish) recovered from E. tarda infections more rapidly than fish on control diets, though fish on high carotenoid diets did not experience a similar benefit. There was an interaction between carotenoid diet and E. tarda such that uninfected fish on the medium carotenoid diet were significantly more colorful along their ventral surface compared to fish on the control and high carotenoid diets. Neither diet nor E. tarda infection affected oxidative damage, antioxidant capacity, or carotenoid content of the skin. From our field and laboratory data we conclude that carotenoid intake by wild convict cichlids occurs at a rate sufficient to affect bacterial infection and ventral coloration, but more data are needed from wild populations to verify the functional significance of these interactions.

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References

  • Amar EC, Kiron V, Satoh S, Okamoto N, Watanabe T (2000) Effects of dietary β-carotene on the immune response of rainbow trout Oncorhynchus mykiss. Fish Sci 66:1068–1075

    Article  CAS  Google Scholar 

  • Amar EC, Kiron V, Satoh S, Watanabe T (2001) Influence of various dietary synthetic carotenoids on bio-defence mechanisms in rainbow trout, Oncorhynchus mykiss (Walbaum). Aquac Res 32:162–173

    Article  CAS  Google Scholar 

  • Anderson C, Wong SC, Fuller A, Zigelski K, Earley RL (2015) Carotenoid-based coloration is associated with predation risk, competition, and breeding status in female convict cichlids (Amatitlania siquia) under field conditions. Environ Biol Fish 98:1005–1013

    Article  Google Scholar 

  • Babin A, Clotilde B, Moret Y (2010) Dietary supplementation with carotenoids improves immunity without increasing its cost in a crustacean. Am Nat 176:234–241

    Article  PubMed  Google Scholar 

  • Baeta R, Faivre B, Motreuil S, Gaillard M, Moreau J (2008) Carotenoid trade-off between parasitic resistance and sexual display: an experimental study in the blackbird (Turdus merula). Proc R Soc B 275:427–434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beeching SC, Gross SH, Bretz HS, Hariatis E (1998) Sexual dichromatism in convict cichlids: the ethological significance of female ventral coloration. Anim Behav 56:1021–1026

    Article  PubMed  Google Scholar 

  • Bertrand S, Alonso-Alvarez C, Devevey G, Faivre B, Prost J, Sorci G (2006) Carotenoids modulate the trade-off between egg production and resistance to oxidative stress in zebra finches. Oecologia 147:576–584

    Article  PubMed  Google Scholar 

  • Blount JD, Metcalfe NB, Birkhead TR, Surai PF (2003) Carotenoid modulation of immune function and sexual attractiveness in zebra finches. Science 300:125–127

    Article  CAS  PubMed  Google Scholar 

  • Blount JD, Rowland HM, Drijfhout FP, Endler JA, Inger R, Sloggett JJ, Hurst GDD, Hodgson DJ, Speed MP (2012) How the ladybird got its spots: effects of resource limitation on the honesty of aposematic signals. Funct Ecol 26:334–342

    Article  Google Scholar 

  • Brown AC, McGraw KJ, Clotfelter ED (2013) Dietary carotenoids increase yellow nonpigment coloration of female convict cichlids (Amantitlania nigrofasciata). Physiol Biochem Zool 86:312–322

    Article  PubMed  Google Scholar 

  • Brown AC, Leonard H, McGraw KJ, Clotfelter ED (2014) Maternal effects of carotenoid supplementation in an ornamented cichlid fish. Funct Ecol 28:612–620

    Article  Google Scholar 

  • Clotfelter ED, Ardia DR, McGraw KJ (2007) Red fish, blue fish: trade-offs between pigmentation and immunity in Betta splendens. Behav Ecol 18:1139–1145

    Article  Google Scholar 

  • Cohen AA, McGraw KJ, Wiersma P, Williams JB, Robinson WD, Robinson TR, Brawn JD, Ricklefs RE (2008) Interspecific associations between circulating antioxidant levels and life-history variation in birds. Am Nat 172:178–193

    Article  PubMed  Google Scholar 

  • Collins CH, Lyne PM (1976) Microbiological methods. Butterworths, London

    Google Scholar 

  • Cuthill IC, Bennett ATD, Partridge JC, Maier EJ (1999) Plumage reflectance and the objective assessment of avian sexual dichromatism. Am Nat 153:183–200

    Article  Google Scholar 

  • Dowling DK, Simmons LW (2009) Reactive oxygen species as universal constraints in life-history evolution. Proc R Soc B 276:1737–1745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • El-Agamey A, Lowe GM, McGarvey DJ, Mortensen A, Phillip DM, Truscott TG, Young AJ (2004) Carotenoid radical chemistry and antioxidant/pro-oxidant properties. Arch Biochem Biophys 430:37–48

    Article  CAS  PubMed  Google Scholar 

  • Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408:239–247

    Article  CAS  PubMed  Google Scholar 

  • Grether GF, Hudon FJ, Millie DF (1999) Carotenoid limitation of sexual coloration along an environmental gradient in guppies. Proc R Soc B 266:1317–1322

    Article  CAS  PubMed Central  Google Scholar 

  • Grether GF, Hudon J, Endler JA (2001) Carotenoid scarcity, synthetic pteridine pigments and the evolution of sexual coloration in guppies (Poecilia reticulata). Proc R Soc B 268:1245–1253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Halver JE (1989) Fish nutrition. Academic Press, San Diego

    Google Scholar 

  • Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387

    Article  CAS  PubMed  Google Scholar 

  • Hartleb CF, Moring JR (1995) An improved gastric lavage device for removing stomach contents from live fish. Fish Res 24:261–265

    Article  Google Scholar 

  • Haugan JA, Liaaen-Jensen S (1994) Algal Carotenoids 54. Carotenoids of brown algae (Phaeophyceae). Biochem Syst Ecol 22:31–41

    Article  CAS  Google Scholar 

  • Hill GE (2011) Condition-dependent traits as signals of the functionality of vital cellular processes. Ecol Lett 14:625–634

    Article  PubMed  Google Scholar 

  • Hill GE, Johnson JD (2012) The vitamin A-redox hypothesis: a biochemical basis for honest signaling via carotenoid pigmentation. Am Nat 180:E127–E150

    Article  PubMed  Google Scholar 

  • Hill GE, McGraw KF (2006) Bird coloration. Harvard University Press, Cambridge

    Google Scholar 

  • Hõrak PE, Sild E, Soomets U, Sepp T, Kilk K (2010) Oxidative stress and information content of black and yellow plumage coloration: an experiment with greenfinches. J Exp Biol 213:2225–2233

    Article  PubMed  Google Scholar 

  • Jackson JK (2003) Science and categories: representations of mating behaviour in convict cichlids (Archocentrus nigrofasciatum). ProQuest, UMI Dissertations Publishing

  • Jacobs PB, LeBoeuf RD, McCommas SA, Tauber JD (1982) The cleavage of carotenoid esters by cholesterol esterase. Comp Biochem Physiol B 72:157–160

    Article  Google Scholar 

  • Johnson AM, Fuller RC (2015) The meaning of melanin, carotenoid, and pterin pigments in the bluefin killifish, Lucania goodie. Behav Ecol 26:158–167

    Article  Google Scholar 

  • Kim S-S, Song J-W, Kim K-W, Lee K-J (2012) Effects of dietary astaxanthin on innate immunity and disease resistance against Edwardsiella tarda in olive flounder Paralichthys olivaceus. Isr J Aquacult Bamidgeh 64:740

    Google Scholar 

  • Kolluru GR, Grether GF, South SH, Dunlop E, Cardinali A, Liu L, Carapiet A (2006) The effects of carotenoid and food availability on resistance to a naturally occurring parasite (Gyrodactylus turnbulli) in guppies (Poecilia reticulata). Biol J Linn Soc 89:301–309

    Article  Google Scholar 

  • Kolluru GR, Grether GF, Dunlop E, South SH (2009) Food availability and parasite infection influence mating tactics in guppies (Poecilia reticulata). Behav Ecol 20:131–137

    Article  Google Scholar 

  • Lee CM, Boileau AC, Boileau TWM, Williams AW, Swanson KS, Heintz KA, Erdman JW (1999) Review of animal models in carotenoid research. J Nutr 129:2271–2277

    CAS  PubMed  Google Scholar 

  • Lin SM, Nieves-Puigdoller K, Brown AC, McGraw KJ, Clotfelter EC (2010) Testing the carotenoid trade-off hypothesis in the polychromatic midas cichlid, Amphilophus citrinellus. Physiol Biochem Zool 83:333–342

    Article  CAS  PubMed  Google Scholar 

  • Lozano GA (1994) Carotenoids, parasites, and sexual selection. Oikos 70:309–311

    Article  Google Scholar 

  • Maan ME, van der Spoel M, Jimenez PQ, van Alphen JJM, Seehausen O (2006) Fitness correlates of male coloration in a Lake Victoria cichlid fish. Behav Ecol 17:691–699

    Article  Google Scholar 

  • Martinez A, Rodriguez-Girones MA, Barbosa A, Costas M (2008) Donator acceptor map for carotenoids, melatonin and vitamins. J Phys Chem A 112:9037–9042

    Article  CAS  PubMed  Google Scholar 

  • McGraw KJ, Parker RS (2006) A novel lipoprotein-mediated mechanism controlling sexual attractiveness in a colorful songbird. Physiol Behav 87:103–108

    Article  CAS  PubMed  Google Scholar 

  • McGraw KJ, Crino OL, Medina-Jerez W, Nolan PM (2006) Effect of dietary carotenoid supplementation on food intake and immune function in a songbird with no carotenoid coloration. Ethology 112:1209–1216

    Article  Google Scholar 

  • McMahan CD, Matamoros WA, Barraza E, Kutz J, Chakrabarty P (2014) Taxonomic status of the Lago Coatepeque endemic convict cichlid Amatitlania coatepeque (Teleostei: Cichlidae). Copeia 2014:633–638

    Article  Google Scholar 

  • Milinski M, Bakker TCM (1990) Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature 344:330–333

    Article  Google Scholar 

  • Mohanty BR, Sahoo PK (2007) Edwardsiellosis in fish: a brief review. J Biosci 32:1331–1344

    Article  CAS  PubMed  Google Scholar 

  • Palozza P (1998) Prooxidant actions of carotenoids in biologic systems. Nutr Rev 56:257–265

    Article  CAS  PubMed  Google Scholar 

  • Palozza PS, Serini S, Di Nicuolo F, Piccioni E, Calviello G (2003) Prooxidant effects of beta-carotene in cultured cells. Mol Asp Med 24:353–362

    Article  CAS  Google Scholar 

  • Perrot-Minnot MJ, Gaillard M, Dodet R, Cezilly F (2011) Interspecific differences in carotenoid content and sensitivity to UVB radiation in three acanthocephalan parasites exploiting a common intermediate host. Int J Parasitol 41:173–181

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna

  • Rashid MM, Nakai T, Muroga K, Miyazaki T (1997) Pathogenesis of experimental Edwardsiellosis in Japanese flounder Paralichthys olivaceus. Fish Sci 63:384–387

    CAS  Google Scholar 

  • Saleh WD (2005) Isolation and identification of Edwardsiella tarda from infected tilapia fish Oreochromis niloticus. Bull Facul Agric Cairo Univ 56:839–848

    Google Scholar 

  • Schmitter-Soto JJ (2007) A systematic revision of the genus Archocentrus (Perciformes: Cichlidae), with the description of two new genera and six new species. Zootaxa 1603:1–78

    Google Scholar 

  • Sefc KM, Brown AC, Clotfelter ED (2014) Carotenoid-based coloration in cichlid fishes. Comp Biochem Physiol A Mol Integr Physiol 173:42–51

    Article  CAS  PubMed Central  Google Scholar 

  • Shotts EB, Waltman WD (1990) A medium for the selective isolation of Edwardsiella ictaluri. J Wildl Dis 26:214–218

    Article  CAS  PubMed  Google Scholar 

  • Sies H, Stahl W, Sundquist AR (1992) Antioxidant functions of vitamins. Ann N Y Acad Sci 669:7–20

    Article  CAS  PubMed  Google Scholar 

  • Sparkes TC, Rush V, Kopp DA, Foster SA (2013) Reproductive success in a natural population of male three-spined stickleback Gasterosteus aculeatus: effects of nuptial colour, parasites and body size. J Fish Biol 82:1720–1727

    Article  CAS  PubMed  Google Scholar 

  • Tanumihardjo SA (2012) Carotenoids and human health. Springer, New York

    Google Scholar 

  • Uchida K, Kanematsu M, Sakai K, Matsuda T, Hattori N, Mizuno Y, Suzuki D, Miyata T, Noguchi N, Niki E, Osawa T (1998) Protein-bound acrolein: potential markers for oxidative stress. Proc Natl Acad Sci U S A 95:4882–4887

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vecchi M, Glinz E, Meduna V, Schiedt K (1987) HPLC separation and determination of astacene, semiastacene, astaxanthin, and other keto-carotenoids. J High Resolut Chromatogr 10:348–351

    Article  CAS  Google Scholar 

  • Wisenden BD, Keenleyside MHA (1995) Brood size and the economy of brood defence: testing Lack’s hypothesis in a biparental cichlid fish. Environ Biol Fish 43:145–151

    Article  Google Scholar 

  • Woods JA, Bilton RF, Young AJ (1999) β-carotene enhances hydrogen peroxide-induced DNA damage in human hepatocellular hepg2 cells. FEBS Lett 449:255–258

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

Special thanks to H. Gendelmen, J. Flautero and K. Smith for helping with data collection. Thank you to the Sistema Nacional de Areas de Conservacion (SINAC), specifically M. Montes and his staff, for logistical assistance in Lomas Barbudal. Thank you to L. Iwanowicz for providing Edwardsiella cultures. Thank you also to R. Hamel for helping with fish care in the laboratory, and to R. Earley, P. Brennan, and E. Jakob for helpful criticisms of this work. Funding for this work was provided by the National Science Foundation to A.C.B. (DDIG-120974), E.D.C. (IOS-1051598), and the Office of the Dean of Faculty at Amherst College, including the Faculty Research Award Program and the H. Axel Schupf ’57 Fund for Intellectual Life. All experimental and animal handling procedures were approved by the Amherst College Institutional Care and Use Committee (IACUC). Permission for the field work was obtained from Sistema Nacional de Áreas de Conservation Costa Rica under permit #02543.

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  1. Alexandria C. Brown

    Present address: Division of Biostatistics and Epidemiology, School of Public Health and Health Sciences, University of Massachusetts, Amherst, MA, 01003, USA

Authors and Affiliations

  1. Department of Biology, Amherst College, Amherst, MA, 01002, USA

    Alexandria C. Brown, Matthew D. Cahn, Sara Choi & Ethan D. Clotfelter

  2. Graduate Program in Organismic and Evolutionary Biology, University of Massachusetts, Amherst, MA, 01003, USA

    Alexandria C. Brown

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Correspondence to Ethan D. Clotfelter.

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Brown, A.C., Cahn, M.D., Choi, S. et al. Dietary carotenoids and bacterial infection in wild and domestic convict cichlids (Amatitlania spp.). Environ Biol Fish 99, 439–449 (2016). https://doi.org/10.1007/s10641-016-0485-x

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