Skip to main content
Log in

Ecoimmunology in degus: interplay among diet, immune response, and oxidative stress

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

The relationships between immunity, oxidative stress, and diet have not often been studied together. Despite this, it has been shown that dietary proteins can have effects on the functioning of the immune system and the oxidative status of animals. Here we evaluated the effects of dietary proteins on the response to an antigen and oxidative status of Octodon degus (Rodentia). We acclimated adult individuals to high-protein and low-protein diets and evaluated several aspects of the acute phase response and variables associated with oxidative status. After the immune challenge, animals acclimated to the high-protein diet had more inflammatory proteins and body mass losses than the group acclimated to a low-protein diet. Overall, the immune challenge increased the production of inflammatory proteins, total antioxidant capacity, lipid peroxidation, and duration of rest periods. In contrast, we did not find an interaction between diet and the challenge with the antigen. Overall, our results do not reveal an enhanced response to an antigen nor effects on the oxidative status of degus individuals subjected to a high-protein diet.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alonso-Alvarez C, Bertrand S, Devevey G, Gaillard M, Prost J, Faivre B, Sorci G (2004) An experimental test of dose-dependent effect of carotenoids and immune activation on sexual signals and antioxidant activity. Am Nat 164:651–659

    Article  Google Scholar 

  • Aubert A (1999) Sickness and behavior in animals: a motivational perspective. Neurosci Biobehav Rev 23:1029–1036

    Article  CAS  PubMed  Google Scholar 

  • Babior BM (1999) NADPH oxidase: an update. Blood 93:1464–1476

    CAS  PubMed  Google Scholar 

  • Barnes RH, Levitsky DA, Pond WG, Ulric M (1976) Effect of postnatal dietary protein and energy restriction on exploratory behavior in young pigs. Dev Psycol 9:425–435

    Article  CAS  Google Scholar 

  • Bertrand S, Criscuolo F, Faivre B, Sorci G (2006) Immune activation increases the susceptibility to oxidative tissue damage in zebra finches. Funct Ecol 20:1022–1027

    Article  Google Scholar 

  • Bounous G, Letourneau L, Kongshavn PAI (1983) Influence of dietary protein type on the immune system of mice. J Nutr 113:1415–1421

    Article  CAS  PubMed  Google Scholar 

  • Bozinovic F, Muñoz-Pedreros A (1995) Nutritional ecology and digestive responses of an omnivorous-insectivorous rodent (Abrothrix longipilis) feeding on fungus. Physiol Zool 68:474–489

    Article  Google Scholar 

  • Catalán TP, Barceló M, Niemeyer HM, Kalergis AM, Bozinovic F (2011) Pathogen- and diet-dependent foraging, nutritional and immune ecology in mealworms. Evol Ecol Res 13:711–723

    Google Scholar 

  • Cohen AA, McGraw KJ, Robinson WD (2009) Serum antioxidants levels in wild birds vary in relation to diet, season, life history strategy, and species. Oecologia 161:673–683

    Article  PubMed  Google Scholar 

  • Costantini D, Dell’Omo G (2006) Effects of T-cell-mediated immune response on avian oxidative stress. Comp Biochem Physiol A Mol Int Physiol 145:137–142

    Article  CAS  Google Scholar 

  • Costantini D, Møller AP (2009) Does immune response cause oxidative stress in birds? A meta-analysis. Comp Biochem Physiol A Mol Int Physiol 153:339–344

    Article  CAS  Google Scholar 

  • Costantini D, Verhulst S (2009) Does high antioxidant capacity indicate low oxidative stress? Funct Ecol 23:506–509

    Article  Google Scholar 

  • Cram DL, Blount JD, York JE, Young AJ (2015) Immune response in a wild bird is predicted by oxidative status, but does not cause oxidative stress. PLoS One 10:e0122421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cruz-Neto AP, Bozinovic F (2004) The relationship between diet quality and basal metabolic rate in endotherms: insights from intraspecific analysis. Physiol Biochem Zool 77:877–889

    Article  PubMed  Google Scholar 

  • Dasgupta A, Klein K (2016) Antioxidants in food, vitamins, and supplements: prevention and treatment of disease. Elsevier Science Publishing Co. Inc Amsterdam

    Google Scholar 

  • Davis RL, Lochmiller RL, Warde WD (1995) Splenocyte subpopulations of weanling cotton rats (Sigmodon hispidus) are influenced by moderate protein intake. J Mammal 76:912–914

    Article  Google Scholar 

  • Delers F, Strecker G, Engler R (1988) Glycosylation of chicken haptoglobin: isolation and characterization of three molecular variants and studies of their distribution in hen plasma before and after turpentine-induced inflammation. Biochem Cell Biol 66:208–217

    Article  CAS  PubMed  Google Scholar 

  • Demas GE, Drazen DL, Nelson RJ (2003) Reductions in total body fat decrease humoral immunity. Proc R Soc Lond B Biol Sci 270:905–911

    Article  Google Scholar 

  • Eikenaar C, Isaksson C, Hegemann A (2018) A hidden cost of migration? Innate immune function versus antioxidant defense. Ecol Evol 8:2721–2728

    Article  PubMed  PubMed Central  Google Scholar 

  • Fulk GW (1976) Notes on the activity, reproduction, and social behavior of Octodon degus. J Mammal 57:495–505

    Article  Google Scholar 

  • Good RA, West A, Yunnis EJ, Cooper WC, Jose DC, Kramer TR, Hansen MA (1976) Nutritional deficiency, immunologic function, and disease. Am J Pathol 84:599–614

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guadagni M, Biolo G (2009) Effects of inflammation and/or inactivity on the need for dietary protein. Curr Opin Clin Nutr Metab Care 12:617–622

    Article  CAS  PubMed  Google Scholar 

  • Halliwell B, Gutteridge J (2007) Free radicals in biology and medicine. Oxford University Press, Oxford

    Google Scholar 

  • Hampton MB, Kettle AJ, Winterboum CC (1998) Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing. Blood 92:3007–3017

    CAS  Google Scholar 

  • Han ES, Muller FL, Pérez VI et al (2008) The in vivo gene expression signature of oxidative stress. Physiol Genom 34:112–126

    Article  CAS  Google Scholar 

  • Hart BL (1988) Biological basis of the behavior of sick animals. Neurosci Biobehav Rev 12:123–137

    Article  CAS  Google Scholar 

  • Hasselquist D, Nilsson J-Å (2012) Physiological mechanisms mediating costs of immune responses: what can we learn from studies of birds? Anim Behav 83:1303–1312

    Article  Google Scholar 

  • Hegemann A, Matson KD, Versteegh MA, Tieleman BI (2012) Wild skylarks seasonally modulate energy budgets but maintain energetically costly inflammatory immune responses throughout the annual cycle. PLoS One 7:e36358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hõrak P (2007) Do dietary antioxidants alleviate the cost of immune activation? An experiment in greenfinches. Am Nat 170:625–635

    Article  PubMed  Google Scholar 

  • Hõrak P, Zilmer M, Saks L, Ots I, Karu U, Zilmer K (2006) Antioxidant protection, carotenoids and the costs of immune challenge in greenfinches. J Exp Biol 209:4329–4338

    Article  CAS  PubMed  Google Scholar 

  • Iriarte JA, Contreras LF, Jaksic FM (1989) A long-term study of a small-mammal assemblage in the central Chilean Matorral. J Mammal 70:79–87

    Article  Google Scholar 

  • Jayle MF, Bussier G, Tonnelat J (1956) Isolation of the haptoglobin-hemoglobin complex in human blood in homogenous state. II Bull Soc Chim Biol 38:343–349

    CAS  PubMed  Google Scholar 

  • Jennings G, Bourgeois C, Elia M (1992) The magnitude of the acute phase protein response is attenuated by protein deficiency in rats. J Nutr 122:1325–1331

    Article  CAS  PubMed  Google Scholar 

  • Kenagy GL, Nespolo RF, Vasquez RA, Bozinovic F (2002) Daily and seasonal limits of time and temperature to activity of degus. Rev Chil Hist Nat 75:567–581

    Google Scholar 

  • Klasing KC (1998) Nutritional modulation of resistance to infectious diseases. Poult Sci 77:1119–1125

    Article  CAS  PubMed  Google Scholar 

  • Klasing KC (2007) Nutrition and the immune. Br Poult Sci 48:525–537

    Article  CAS  PubMed  Google Scholar 

  • Klasing KC, Roura E (1991) Interactions between nutrition and immunity in chickens. In: Proc Cornell Nutr Conf pp 94

  • Lagos VO, Bozinovic F, Contreras LC (1995) Microhabitat use by a small diurnal rodent (Octodon degus) in a semiarid environment: thermoregulatory constraints or predation risk? J Mammal 76:900–905

    Article  Google Scholar 

  • Latshaw JD (1991) Nutrition—mechanisms of immuno-suppression. Vet Immunol Immunopathol 30:111–120

    Article  CAS  PubMed  Google Scholar 

  • Lee KP, Cory JS, Wilson K, Raubenheimer D, Simpson SJ (2006) Flexible diet choice offsets protein costs of pathogen resistance in a caterpillar. Proc R Soc B 273:823–829

    Article  CAS  Google Scholar 

  • Li P, Yin YL, Li D, Kim SW, Wu G (2007) Amino acids and immune function. Br J Nutr 98:237–252

    Article  CAS  Google Scholar 

  • Martel SI, Riquelme SA, Kalergis AM, Bozinovic F (2014) Dietary effect on immunological energetics in mice. J Comp Physiol B 184:937–944

    Article  CAS  PubMed  Google Scholar 

  • Martínez del Rio C, Stevens BR (1989) Physiological constraint on feeding behavior: intestinal membrane disaccharidases of the starling. Science 43:794–796

    Article  Google Scholar 

  • Matson KD (2006) Are there differences in immune function between continental and insular birds? Proc R Soc B 273:2267–2274

    Article  CAS  PubMed  Google Scholar 

  • Matson KD, Cohen AA, Klasing KC, Ricklefs RE, Scheuerlein A (2006) No simple answers for ecological immunology: relationships among immune indices at the individual level break down at the species level in waterfowl. Proc R Soc B 273:815–822

    Article  PubMed  Google Scholar 

  • McNab BK (1988) Food habits and the basal rate of metabolism in birds. Oecologia 77:343–349

    Article  PubMed  Google Scholar 

  • Mendes L, Piersma T, Hasselquist D, Matson KD, Ricklefs RE (2006) Variation in the innate and acquired arms of the immune system among five shorebird species. J Exp Biol 209:284–291

    Article  PubMed  Google Scholar 

  • Monaghan P, Metcalfe NB, Torres R (2009) Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements, and interpretation. Ecol Lett 12:75–92

    Article  PubMed  Google Scholar 

  • Nemzek JA, Morrison L, Peterson JE, Bolgos G, Rush H (2003) Quantification of TNFα and IL6 bioactivity in response to lipopolysaccharide in the degu (Octodon degus). Contemp Top Lab Anim Sci 42:39–42

    CAS  PubMed  Google Scholar 

  • Nemzek JA, Hugunin KM, Opp MR (2008) Modeling sepsis in the laboratory: merging sound science with animal well-being. Comp Med 58:120–128

    CAS  PubMed  PubMed Central  Google Scholar 

  • O’Reilly EL, Eckersall PD (2014) Acute phase proteins: a review of their function, behavior, and measurement in chickens. Worlds Poult Sci J 70:27–44

    Article  Google Scholar 

  • Parasuraman S, Raveendran R, Kesavan R (2010) Blood sample collection in small laboratory animals. J Pharmacol Pharmacother 1:87–93

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pérez-Rodríguez L, Mougeot F, Alonso-Alvarez C, Blas J, Vinuela J, Bortolotti GR (2008) Cell-mediated immune activation rapidly decreases plasma carotenoids but does not affect oxidative stress in red-legged partridges (Alectoria rufa). J Exp Biol 211:2155–2161

    Article  CAS  PubMed  Google Scholar 

  • Råberg L, Grahn M, Hasselquist D, Svensson E (1998) On the adaptive significance of stress-induced immunosuppression. Proc R Soc B 265:1637–1641

    Article  PubMed  Google Scholar 

  • Ramirez-Otarola N, Narvaez C, Sabat P (2011) Membrane-bound intestinal enzymes of passerine birds: dietary and phylogenetic correlates. J Comp Physiol B 181:817–827

    Article  CAS  PubMed  Google Scholar 

  • Ramirez-Otarola N, Espinoza J, Kalergis AM, Sabat P (2018) Is there an effect of environmental temperature on the response to an antigen and the metabolic rate in pups of the rodent Octodon degus? J Therm Biol 71:17–23

    Article  CAS  PubMed  Google Scholar 

  • Sabat P, Ramírez-Otarola N, Barceló G, Salinas J, Bozinovic F (2010) Comparative basal metabolic rate among passerines and the food habit hypothesis. Comp Biochem Physiol A 157:35–40

    Article  CAS  Google Scholar 

  • Sabat P, Narváez C, Peña-Villalobos I, Contreras C, Maldonado K, Sanchez-Hernandez JC, Newsome SD, Nespolo R, Bozinovic F (2017) Coping with salt water habitats: metabolic and oxidative responses to salt intake in the rufous-collared sparrow. Front Physiol 8:654

    Article  PubMed  PubMed Central  Google Scholar 

  • Schmid-Hempel P (2011) Evolutionary parasitology: the integrated study of infections, immunology, ecology, and genetics. Oxford University Press Inc., New York

    Google Scholar 

  • Segal AW (2005) How neutrophils kill microbes. Annu Rev Immunol 23:197–223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sih A, Christensen B (2001) Optimal diet theory: when does it work, and when and why does it fail? Anim Behav 61:379–339

    Article  Google Scholar 

  • Sköld-Chiriac S, Nord A, Tobler M, Nilsson J-A, Hasselquist D (2015) Body temperature changes during simulated bacterial infection in a songbird: fever at night and hypothermia during the day. J Exp Biol 218:2961–2969

    Article  PubMed  Google Scholar 

  • Sorci G, Faivre B (2009) Inflammation and oxidative stress in vertebrate host-parasite systems. Philos Trans R Soc B 364:71–83

    Article  Google Scholar 

  • Thomason CA, Hedrick-Hopper TL, Derting TL (2013) Social and nutritional stressors: agents for altered immune function in white-footed mice (Peromyscus leucopus). Can J Zool 91:313–320

    Article  CAS  Google Scholar 

  • Torres R, Velando A (2007) Male reproductive senescence: the price of immune-induced oxidative damage on sexual attractiveness in the blue-footed booby. J Anim Ecol 76:1161–1168

    Article  PubMed  Google Scholar 

  • Tummeleht L, Mägi M, Kilgas P, Mänd R, Hõrak P (2006) Antioxidant protection and plasma carotenoids of incubating great tits in relation to health state and breeding conditions. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 144:166–172

    Article  CAS  Google Scholar 

  • Van Heugten E, Spears JW, Coffey MT (1994) The effect of dietary protein on performance and immune response in weanling pigs subjected to an inflammatory challenge. J Anim Sci 72:2661–2669

    Article  PubMed  Google Scholar 

  • van de Crommenacker J, Horrocks NPC, Versteegh MA, Komdeur J, Tieleman BI, Matson KD (2010) Effects of immune supplementation and immune challenge on oxidative status and physiology in a model bird: implications for ecologists. J Exp Biol 213:3527–3535

    Article  CAS  PubMed  Google Scholar 

  • Veloso C, Bozinovic F (2000a) Interplay between acclimation time and diet quality on basal metabolic rate in females of degus Octodon Degus (Rodentia: Octodontidae). J Zool Lond 252:531–533

    Article  Google Scholar 

  • Veloso C, Bozinovic F (2000b) Effect of food quality on the energetics of reproduction in a precocial rodent, Octodon Degus. J Mammal 81:971–978

    Article  Google Scholar 

  • Venesky MD, Wilcoxen TE, Rensel MA, Rollins-Smith L, Kerby JL, Parris MJ (2012) Dietary protein restriction impairs growth, immunity, and disease resistance in southern leopard frog tadpoles. Oecologia 169:23–31

    Article  PubMed  Google Scholar 

  • Wicher KB, Fries E (2006) Haptoglobin, a hemoglobin-binding plasma protein, is present in bony fish and mammals but not in frog and chicken. Proc Nat Acad Sci USA 103:4168–4173

    Article  CAS  PubMed  Google Scholar 

  • Wobbrock JO, Findlater L, Gergle D, Higgins JJ (2011) The aligned rank transform for nonparametric factorial analyses using only ANOVA procedures. Proc Conf Hum Factors Comput Syst 1:143–146

    Google Scholar 

  • Woorward B (1998) Protein, calories, and immune defenses. Nutr Rev 56:S84–S92

    Article  Google Scholar 

  • Yáñez J, Jaksic F (1978) Historia natural de Octodon degus (Molina) (Rodentia, Octodontidae). Museo Nacional de Historia Natural. Publicación Ocasional (Chile) 27:3–11

    Google Scholar 

  • Zuur AF, Ieno EN, Elphnick CS (2010) A protocol for data exploration to avoid common statistical problems. Met Ecol Evol 1:3–14

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful to Carolina Contreras for her help and assistance with data collection. This study was funded by FONDECYT 3160133 to NRO, FONDECYT 3140395 to DSR and FB 0002-2014 to FB. Animals were captured with permits from SAG, Chile (No. 2355/2016). All protocols were approved by the Institutional Animal Care Committee of the Pontificia Universidad Católica de Chile where the experiments were performed.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Natalia Ramirez-Otarola.

Additional information

Communicated by H. V. Carey.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLSX 21 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ramirez-Otarola, N., Sarria, M., Rivera, D.S. et al. Ecoimmunology in degus: interplay among diet, immune response, and oxidative stress. J Comp Physiol B 189, 143–152 (2019). https://doi.org/10.1007/s00360-018-1195-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-018-1195-9

Keywords

Navigation