Advertisement

Ecological Research

, Volume 32, Issue 4, pp 559–566 | Cite as

Reproduction compromises adaptive immunity in a cyprinid fish

  • Indrikis A. Krams
  • Katariina Rumvolt
  • Lauri Saks
  • Ronalds Krams
  • Didzis Elferts
  • Jolanta Vrublevska
  • Markus J. Rantala
  • Sanita Kecko
  • Dina Cīrule
  • Severi Luoto
  • Tatjana Krama
Original Article

Abstract

Vertebrates differ in their ability to mount an adaptive immune response to novel antigens. Bioenergetic resources available to an organism are finite; investment in reproduction compromises immune function and may therefore affect critical life history trade-offs. We tested whether reproduction impairs the ability to produce an antibody response against a novel antigen in roach (Rutilus rutilus). The antigen approach has rarely been used in fish studies, and the ability to produce an antibody response during reproductive season has never been tested in cyprinid fish before. The fish in an experimental group were injected with a Brucella abortus (BA) antigen, while the fish in a control group were injected with an isotonic saline solution. Blood samples were extracted from all the fish to obtain the total number and proportion of blood cells such as lymphocytes, neutrophils and antioxidant glutathione. The groups were tested during the spawning season and one week after it had ended. The roach were unable to mount an immune response during spawning but produced a robust response after it. We conclude that reproduction is costly in roach, as indicated by the increased concentration of neutrophils in fish injected with BA during spawning, as well as the negative associations between neutrophil counts and glutathione levels. This study demonstrates the potential of BA antigen as a research tool in experimental research on fish ecological immunology.

Keywords

Adaptive immunity Fish Life history Reproduction Spawning Trade-offs 

Notes

Acknowledgements

We thank Prof. Arturs Škute for support during all phases of this study. We also thank Riina, Rein and Risto Kalda and Imre Taal for their assistance. The study was funded by the Science Council of Latvia (Grant No. # 290/2012) (to I.A. Krams and T. Krama), by a project (Grant No. # 2013/0067/1DP/1.1.1.2.0/13/APIA/VIAA/060) of the European Social Fund, and a personal grant (PUT1223) from the Estonian Ministry of Education and Science (to I.A. Krams and T. Krama). The research reported here complied with the legal ethical requirements of the Republic of Estonia (ethical permit #56 issued by the Ministry of Rural Affairs).

References

  1. Adamo SA, Jensen M, Younger M (2001) Changes in lifetime immunocompetence in male and female Gryllus texensis (formerly G. integer): trade-offs between immunity and reproduction. Anim Behav 62:417–425CrossRefGoogle Scholar
  2. Agranovich I, Scott DE, Terle D, Lee K, Golding B (1999) Down-regulation of Th2 responses by B. abortus, a strong Th1 stimulus, correlates with alterations in the B7.2-CD28 pathway. Infect Immun 67:4418–4426PubMedPubMedCentralGoogle Scholar
  3. Ahmad I, Hamid T, Fatima M, Chand HS, Jain SK, Athar M, Raisuddin S (2000) Induction of hepatic antioxidants in freshwater catfish (Channa punctatus Bloch) is a biomarker of paper mill effluent exposure. Biochim Biophys Acta 1519:37–48CrossRefGoogle Scholar
  4. Alonso-Alvarez C, Bertrand S, Faivre B, Chastel O, Sorci G (2007) Testosterone and oxidative stress: the oxidation handicap hypothesis. Proc R Soc B 274:819–825CrossRefPubMedGoogle Scholar
  5. Amat JA, Aguilera E, Visser GH (2007) Energetic and developmental costs of mounting an immune response in greenfinches (Carduelis chloris). Ecol Res 22:282–287CrossRefGoogle Scholar
  6. Ardia DR (2005) Individual quality mediates trade-offs between reproductive effort and immune function in tree swallows. J Anim Ecol 74:517–524CrossRefGoogle Scholar
  7. Bonneaud C, Mazuc J, Gonzalez G, Haussy C, Chastel O, Faivre B, Sorci G (2003) Assessing the cost of mounting an immune response. Am Nat 161:367–379CrossRefPubMedGoogle Scholar
  8. Boughton RK, Joop G, Armitage SAO (2011) Outdoor immunology: methodological considerations for ecologists. Funct Ecol 25:81–100CrossRefGoogle Scholar
  9. Briviba K, Watzl B, Nickel K, Kulling S, Bös K, Rechkemmer G, Achim B (2010) A half-marathon and a marathon run induce oxidative DNA damage, reduce antioxidant capacity to protect DNA against damage and modify immune function in hobby runners. Redox Rep 10:325–331CrossRefGoogle Scholar
  10. Cīrule D, Krama T, Vrublevska J, Rantala M, Krams I (2012) A rapid effect of handling on counts of white blood cells in a wintering passerine bird: a more practical measure of stress? J Ornithol 153:161–166CrossRefGoogle Scholar
  11. Cook J (1994) The effects of stress, background color and steroid hormones on the lymphocytes of rainbow trout (Oncorhynchus mykiss). PhD Thesis. University of Sheffield, SheffieldGoogle Scholar
  12. Davis AK, Maney DL, Maerz JC (2008) The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Funct Ecol 22:760–772CrossRefGoogle Scholar
  13. Deerenberg C, Arpanius V, Daan S, Bos N (1997) Reproductive effort decreases antibody responsiveness. Proc R Soc B 264:1021–1029CrossRefPubMedCentralGoogle Scholar
  14. Demas GE, Nelson RJ (eds) (2011) Eco-Immunology. Oxford University Press, New YorkGoogle Scholar
  15. Demas GE, Drazen DL, Nelson RJ (2003) Reductions in total body fat decrease humoral immunity. Proc R Soc B 270:905–911CrossRefPubMedPubMedCentralGoogle Scholar
  16. Demas GE, Zysling DA, Beechler BR, Muehlenbein MP, French SS (2011) Beyond phytohaemagglutinin: assessing vertebrate immune function across ecological contexts. J Anim Ecol 80:710–730CrossRefPubMedGoogle Scholar
  17. Eisenberg T, Hamann H-P, Kaim U, Schlez K, Seeger H, Schauerte N, Melzer F, Tomaso H, Scholz HC, Koylass MS, Whatmore AM, Zschöcka M (2012) Isolation of potentially novel Brucella spp. from frogs. Appl Environ Microbiol 78:3753–3755CrossRefPubMedPubMedCentralGoogle Scholar
  18. El-Tras WF, Tayel AA, Eltholth MM, Guitian JJ (2010) Brucella infection in fresh water fish: evidence for natural infection of Nile catfish, Clarias gariepinus, with Brucella melitensis. Vet Microbiol 141:321–325CrossRefPubMedGoogle Scholar
  19. Folstad I, Karter A (1992) Parasites, bright males, and the immunocompeence handicap. Am Nat 139:603–622CrossRefGoogle Scholar
  20. Galván I, Alonso-Alvarez C (2008) An intracellular antioxidant determines the expression of a melanin-based signal in a bird. PLoS One 3:e3335CrossRefPubMedPubMedCentralGoogle Scholar
  21. Garcia MM, Brooks BW, Stewart RB, Dion W, Trudel JR, Ouwerkerk T (1987) Evaluation of gamma radiation levels for reducing pathogenic bacteria and fungi in animal sewage and laboratory effluents. Can J Vet Res 51:285–289PubMedPubMedCentralGoogle Scholar
  22. Garnier R, Graham AL (2014) Insights from parasite-specific serological tools in eco-immunology. Integ Comp Biol 54:363–376CrossRefGoogle Scholar
  23. Ghasemi A, Jeddi-Tehrani M, Mautner J, Salari MH, Zarnani A-H (2015) Simultaneous immunization of mice with Omp31 and TF provides protection against Brucella melitensis infection. Vaccine 33:5532–5538CrossRefPubMedGoogle Scholar
  24. Godfroid J, Nielsen K, Saegerman C (2010) Diagnosis of Brucellosis in livestock and wildlife. Croat Med J 51:296–305CrossRefPubMedPubMedCentralGoogle Scholar
  25. Gowaty PA, Anderson WW, Bluhm CK, Drickamer LC, Kim YK, Moore AJ (2007) The hypothesis of reproductive compensation and its assumptions about mate preferences and offspring viability. Proc Nat Acad Sci USA 104:15023–15027CrossRefPubMedPubMedCentralGoogle Scholar
  26. Graham AL, Allen JE, Read AF (2005) Evolutionary causes and consequences of immunopathology. Annu Rev Ecol Evol Syst 36:373–397CrossRefGoogle Scholar
  27. Graham AL, Hayward AD, Watt KA, Pilkington JG, Pemberton JM, Nussey DH (2010) Fitness correlates of heritable variation in antibody responsiveness in a wild mammal. Science 330:662–665CrossRefPubMedGoogle Scholar
  28. Graham AL, Shuker DM, Pollitt LC, Auld SKJR, Wilson AJ, Little TJ (2011) Fitness consequences of immune responses: strenghtening the empirical framework for ecoimmunology. Funct Ecol 25:5–17CrossRefGoogle Scholar
  29. Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw 33:1–22CrossRefGoogle Scholar
  30. Hawkey CM, Dennett TB (1989) Color atlas of comparative veterinary hematology. Iowa State University Press, AmesGoogle Scholar
  31. Hawley DM, Altizer SM (2011) Disease ecology meets ecological immunology: understanding the links between organismal immunity and infection dynamics in natural populations. Funct Ecol 25:48–60CrossRefGoogle Scholar
  32. Hõrak P, 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 213:2225–2233CrossRefPubMedGoogle Scholar
  33. Hou Y, Suzuki Y, Aida Y (1999) Effects of steroids on the antibody producing activity of lymphocytes in rainbow trout. Fish Sci 65:850–855CrossRefGoogle Scholar
  34. Houwen B (2002) Blood film preparation and staining procedures. Lab Hematol 22:1–7Google Scholar
  35. Iida T, Takanishi K, Wakabayashi H (1989) Decrease in the bacterial activity of normal serum during the spawning period of rainbow trout. Bull Jpn Soc Sci Fish 55:463–465CrossRefGoogle Scholar
  36. Isaksson C, Sheldon BC, Uller T (2011) The challenges of integrating oxidative stress into life-history biology. Bioscience 61:194–202CrossRefGoogle Scholar
  37. Janeway C, Travers P, Walport M, Shlomchik M (2004) Immunobiology. Garland Publishing, New YorkGoogle Scholar
  38. Johnson KA, Flynn JK, Amend DF (1982) Onset of immunity in salmonid fry vaccinated by direct immersion in Vibrio anguillarum and Yersinia ruckeri bacterins. J Fish Dis 5:197–205CrossRefGoogle Scholar
  39. Knowles SCL, Nakagawa S, Sheldon BC (2009) Elevated reproductive effort increases blood parasitaemia and decreases immune function in birds: a metaregression approach. Funct Ecol 23:405–415CrossRefGoogle Scholar
  40. Kortet R, Taskinen J (2004) Parasitism, condition and number of front head breeding tubercles in roach (Rutilus rutilus L.). Ecol Freshw Fish 13:119–124CrossRefGoogle Scholar
  41. Kortet R, Taskinen J, Vainikka A (2002) Epizootic cutaneous papillomatosis in roach Rutilus rutilus: sex and size dependence, seasonal occurrence and between population differences. Dis Aquat Organ 52:185–190CrossRefPubMedGoogle Scholar
  42. Kortet R, Taskinen J, Sinisalo T, Jokinen I (2003a) Breeding-related seasonal changes in immunocompetence, health state and condition of the cyprinid fish, Rutilus rutilus, L. Biol J Linn Soc 78:117–127CrossRefGoogle Scholar
  43. Kortet R, Vainikka A, Rantala MJ, Jokinen I, Taskinen J (2003b) Sexual ornamentation, androgens and papillomatosis in male roach (Rutilus rutilus). Evol Ecol Res 5:411–419Google Scholar
  44. Kortet R, Vainikka A, Rantala MJ, Taskinen J (2004a) Sperm quality, secondary sexual characters and parasitism in roach (Rutilus rutilus). Biol J Linn Soc 81:111–117CrossRefGoogle Scholar
  45. Kortet R, Vainikka A, Rantala MJ, Myntti J, Taskinen J (2004b) In vitro embryo survival and early viability of larvae in relation to male sexual ornaments and parasite resistance in roach, Rutilus rutilus L. J Evol Biol 17:1337–1344CrossRefPubMedGoogle Scholar
  46. Koskivaara M, Valtonen ET, Prost M (1991) Seasonal occurrence of gyrodactylid monogeneans on the roach (Rutilus rutilus) and variations between four lakes of differing water quality in Finland. Aqua Fenn 21:47–55Google Scholar
  47. Krama T, Suraka V, Hukkanen M, Rytkönen S, Orell M, Cīrule D, Rantala MJ, Krams I (2013) Physiological condition and blood parasites of breeding great tits: a comparison of core and northernmost populations. J Ornithol 154:1019–1028CrossRefGoogle Scholar
  48. Krams I, Vrublevska J, Cirule D, Kivleniece I, Krama T, Rantala MJ, Sild E, Hõrak P (2012) Heterophil/lymphocyte ratios predict the magnitude of humoral immune response to a novel antigen in great tits (Parus major). Comp Biochem Physiol A Mol Integr Physiol 161:422–428CrossRefPubMedGoogle Scholar
  49. Leshchinsky TV, Klasing KC (2001) Relationship between the level of dietary vitamin E and the immune response of broiler chickens. Poultry Sci 80:1590–1599CrossRefGoogle Scholar
  50. Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87–98CrossRefGoogle Scholar
  51. Lynch M (2007) The origins of genome architecture. Sinauer, Sunderland MAGoogle Scholar
  52. Mandiki SNM, Henrotte E, Milla S, Douxfils J, Wang N, Rougeot C, Vandecan M, Mélard C, Kestemont P (2011) How physiological status and immune defense are affected by photo-thermal regimes and domestication process in captive Eurasian perch? Indian J Sci Technol 4:298–299Google Scholar
  53. Martin LB, Hasselquist D, Wikelski M (2006) Investment in immune defense is linked to pace of life in house sparrows. Oecologia 147:565–575CrossRefPubMedGoogle Scholar
  54. Maule AG, Schrock R, Slater C, Fitzpatrick MS, Schreck CB (1996) Immune and endocrine responses of adult chinook salmon during freshwater immigration and sexual maturation. Fish Shellfish Immunol 6:221–223CrossRefGoogle Scholar
  55. McNamara KB, van Lieshout E, Jones TM, Simmons LW (2013) Age-dependent trade-offs between immunity and male, but not female, reproduction. J Anim Ecol 82:235–244CrossRefPubMedGoogle Scholar
  56. Meitern R, Sild E, Lind M-A, Männiste M, Sepp T, Karu U, Hõrak P (2013) Effects of endotoxin and psychological stress on redox physiology, immunity and feather corticosterone in greenfinches. PLoS One 8(6):e67545CrossRefPubMedPubMedCentralGoogle Scholar
  57. Morales A, Colell A, García-Ruiz C, Fernández-Checa JC (2009) Mitochondrial glutathione, a key survival antioxidant. Antioxid Redox Signal 11:2685–2700CrossRefPubMedPubMedCentralGoogle Scholar
  58. Muehlenbein MP, Bribiescas RG (2005) Testosterone-mediated immune functions and male life histories. Am J Hum Biol 17:527–558CrossRefPubMedGoogle Scholar
  59. Pasnik DJ, Vemulapalli R, Smith SA, Schurig GG (2003) A recombinant vaccine expressing a mammalian Mycobacterium sp. antigen is immunostimulatory but not protective in striped bass. Vet Immunol Immunopathol 95:43–52CrossRefPubMedGoogle Scholar
  60. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
  61. Pickering AD, Christie P (1980) Sexual differences in the incidence and severity of ectoparasitic infestation of the brown trout, Salmo trutta L. J Fish Biol 16:669–683CrossRefGoogle Scholar
  62. Rahman I, Kode A, Biswas SK (2007) Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nat Protoc 1:3159–3165CrossRefGoogle Scholar
  63. Raitaniemi J, Nyberg K, Torvi I (2000) Kalojen iän ja kasvun määritys. Riistan-ja kalatalouden tutkimuslaitos, HelsinkiGoogle Scholar
  64. Rajasekaran P, Surendran N, Saleem MN, Sriranganathan N, Schuring GG, Boyle SM (2011) Over-expression of homologous antigens in a leucine auxotroph of Brucella abortus strain RB51 protects mice against a virulent B. suis challenge. Vaccine 29:3106–3110CrossRefPubMedGoogle Scholar
  65. Richner H, Christe P, Oppliger A (1995) Paternal investment affects prevalence of malaria. Proc Natl Acad Sci USA 92:1192–1194CrossRefPubMedPubMedCentralGoogle Scholar
  66. Ridgeway GJ (1962) Demonstration of blood types in rainbow trout and salmon by isoimmunization. Ann New York Acad Sci 97:111–118CrossRefGoogle Scholar
  67. Rohlenová K, Šimková A (2010) Are the immunocompetence and the presence of metazoan parasites in cyprinid fish affected by reproductive efforts of cyprinid fish? J Biomed Biotechnol. Article ID 418382Google Scholar
  68. Salem SF, Mohsen A (1997) Brucellosis in fish. Vet Med (Praha) 42:5–7Google Scholar
  69. Schmid-Hempel P (2011) Evolutionary parasitology: the integrated study of infections, immunology, ecology, and genetics. Oxford University Press, New YorkGoogle Scholar
  70. Schreck CB (2010) Stress and fish reproduction: the roles of allostasis and hormesis. Gen Comp Endocrinol 165:549–556CrossRefPubMedGoogle Scholar
  71. Schulenburg H, Kurtz J, Moret Y, Siva-Jothy MT (2009) Introduction. Ecological immunology. Phil Trans R Soc B 364:3–14CrossRefPubMedGoogle Scholar
  72. Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321CrossRefPubMedGoogle Scholar
  73. Sild E, Hõrak P (2010) Assessment of oxidative burst in avian whole blood samples: validation and application of a chemiluminescence method based on Pholasin. Behav Ecol Sociobiol 64:2065–2076CrossRefGoogle Scholar
  74. Šimková A, Jarkovský J, Koubková B, Baruš V, Prokeš M (2005) Associations between fish reproductive cycle and the dynamics of metazoan parasite infection. Parasitol Res 95:65–72CrossRefPubMedGoogle Scholar
  75. Skarstein F, Folstad I, Liljedal S (2001) Whether to reproduce or not: immune suppression and cost of parasites during reproduction in the Arctic charr. Can J Zool 79:271–278CrossRefGoogle Scholar
  76. Slater CH, Schreck CB (1993) Testosterone alters the immune response of chinook salmon, Oncorhynchus tshawytscha. Gen Comp Endocrinol 89:291–298CrossRefPubMedGoogle Scholar
  77. Sommerset I, Krossøy B, Biering E, Frost P (2005) Vaccines for fish in aquaculture. Expert Rev Vaccines 4:89–101CrossRefPubMedGoogle Scholar
  78. Soto E, Brown N, Gardenfors ZO, Yount S, Revan F, Francis S, Kearney MT, Camus A (2014) Effect of size and temperature at vaccination on immunization and protection conferred by a live attenuated Francisella noatunensis immersion vaccine in red hybrid tilapia. Fish Shellfish Immunol 41:593–599CrossRefPubMedGoogle Scholar
  79. Stearns SC (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  80. Taskinen J, Kortet R (2002) Dead and alive parasites: sexual ornaments signal resistance in the male fish, Rutilus rutilus. Evol Ecol Res 4:919–929Google Scholar
  81. Vainikka A, Taskinen J, Löytynoja K, Jokinen I, Kortet R (2009) Measured immunocompetence relates to the proportion of dead parasites in a wild roach population. Funct Ecol 23:187–195CrossRefGoogle Scholar
  82. Vemulapalli R, He Y, Cravero S, Sriranganathan N, Boyle SM, Schurig GG (2000) Overexpression of protective antigen as a novel approach to enhance vaccine efficacy of Brucella abortus strain RB51. Infect Immun 68:3286–3289CrossRefPubMedPubMedCentralGoogle Scholar
  83. Wester PW, Vethaak AD, van Muiswinkel WB (1994) Fish biomarkers in immunotoxicology. Toxicology 86:213–232CrossRefPubMedGoogle Scholar
  84. Whatmore AM, Dale E-J, Stubberfield E, Muchowski J, Koylass M, Dawson C, Gopaul KK, Perrett LL, Jones M, Lawrie A (2015) Isolation of Brucella from a White’s tree frog (Litoria caerulea). JMM Case Reports. doi: 10.1099/jmmcr.0.000017 Google Scholar
  85. Xu Y-C, Yang D-B, Wang D-H (2012) No evidence for a trade-off between reproductive investment and immunity in a rodent. PLoS One 7(5):e37182CrossRefPubMedPubMedCentralGoogle Scholar
  86. Yamaguchi T, Watanuki H, Sakai M (2001) Effects of estradiol, progesterone and testosterone on the function of carp, Cyprinus carpio, phagocytes in vitro. Comp Biochem Physiol C Toxicol Pharmacol 129:49–55CrossRefPubMedGoogle Scholar
  87. Zaitseva MB, Golding H, Betts M, Yamauchi A, Bloom ET, Butler LE, Stevan L, Golding B (1995) Human peripheral blood CD4þ and CD8þ T-cells express Th1-like cytokine mRNA and proteins following in vitro stimulation with heat- inactivated B. abortus. Infect Immun 63:2720–2728PubMedPubMedCentralGoogle Scholar

Copyright information

© The Ecological Society of Japan 2017

Authors and Affiliations

  • Indrikis A. Krams
    • 1
    • 2
  • Katariina Rumvolt
    • 3
  • Lauri Saks
    • 3
  • Ronalds Krams
    • 4
  • Didzis Elferts
    • 2
    • 5
  • Jolanta Vrublevska
    • 4
  • Markus J. Rantala
    • 6
  • Sanita Kecko
    • 4
  • Dina Cīrule
    • 2
  • Severi Luoto
    • 7
    • 8
  • Tatjana Krama
    • 4
    • 9
  1. 1.Institute of Ecology and Earth SciencesThe University of TartuTartuEstonia
  2. 2.Institute of Food Safety, Animal Health and Environment BIORRīgaLatvia
  3. 3.Estonian Marine InstituteUniversity of TartuTartuEstonia
  4. 4.Department of Biotechnology, Institute of Life Sciences and TechnologyDaugavpils UniversityDaugavpilsLatvia
  5. 5.Department of Botany and EcologyUniversity of LatviaRīgaLatvia
  6. 6.Department of Biology and Turku Brain and Mind CentreUniversity of TurkuTurkuFinland
  7. 7.English, Drama and Writing StudiesUniversity of AucklandAucklandNew Zealand
  8. 8.School of PsychologyUniversity of AucklandAucklandNew Zealand
  9. 9.Department of Plant Protection, Institute of Agricultural and Environmental SciencesEstonian University of Life ScienceTartuEstonia

Personalised recommendations