Abstract
Oxidative stress—an imbalance between reactive pro- and neutralising antioxidants—damages cell structures and impairs fitness-relevant traits such as longevity and reproduction. Theory predicts that feeding on diets with high antioxidant content such as fruits should reduce oxidative stress; however, there is no support of this idea in free-ranging mammals. Bats cover a large variety of ecological niches, and therefore, we asked if measures of oxidative stress are lower in species with fruit diets. We measured reactive oxygen metabolites (ROM) representing total pro-oxidants produced and antioxidants in the plasma of 33 Neotropical bat species. Species with a fruit diet showed the lowest level of ROM and the highest concentration of antioxidants, followed by omnivorous and animalivorous species. Potentially, frugivorous species ingest more antioxidants with food and thus are able to neutralise more pro-oxidants than species not feeding on fruits, resulting in an overall lower level of oxidative stress. We therefore showed for the first time that measures of oxidative stress vary according to diets in free-ranging mammals.
Similar content being viewed by others
References
Alhazza IM, Haffor ASA (2007) Effects of lead toxicity on free radical production in rats. J Med Sci 7:901–904
Balaban RS, Nemoto S, Finkel T (2005) Mitochondria, oxidants, and aging. Cell 120:483–495
Buffenstein R, Edrey YH, Yang T, Mele J (2008) The oxidative stress theory of aging: embattled or invincible? Insights from non-traditional model organisms. Age 30:99–109
Carocho M, Ferreira ICFR (2013) A review on antioxidants, prooxidants and related controversy: natural and synthetic compounds, screening and analysis methodologies and future perspectives. Food Chem Toxicol 51:15–25
Celi P, Sullivan M, Evans D (2010) The stability of the reactive oxygen metabolites (d-ROMs) and biological antioxidant potential (BAP) tests on stored horse blood. Vet J 183:217–218
Celi P, Merlo M, Barbato O, Gabai G (2012) Relationship between oxidative stress and the success of artificial insemination in dairy cows in a pasture-based system. Vet J 193:498–502
Chance B, Sies H, Boveris A (1979) Hydroperoxide metabolism in mammalian organs. Physiol Rev 59:527–605
Costantini D (2008) Oxidative stress in ecology and evolution: lessons from avian studies. Ecol Lett 11:1238–1251
Costantini D, Dell'Omo G (2006a) Effects of T-cell-mediated immune response on avian oxidative stress. Comp Biochem Physiol A 145:137–142
Costantini D, Dell'Omo G (2006b) Environmental and genetic components of oxidative stress in wild kestrel nestlings (Falco tinnunculus). J Comp Physiol B 176:575–579
Costantini D, Møller AP (2008) Carotenoids are minor antioxidants for birds. Funct Ecol 22:367–370
Costantini D, Casagrande S, De Filippis S, Brambilla G, Fanfani A, Tagliavini J, Dell'Omo G (2006) Correlates of oxidative stress in wild kestrel nestlings (Falco tinnunculus). J Comp Physiol B 176:329–337
Costantini D, Cardinale M, Carere C (2007a) Oxidative damage and anti-oxidant capacity in two migratory bird species at a stop-over site. Comp Biochem Physiol C 144:363–371
Costantini D, Fanfani A, Dell'Omo G (2007b) Carotenoid availability does not limit the capability of nestling kestrels (Falco tinnunculus) to cope with oxidative stress. J Exp Biol 210:1238–1244
Costantini D, Fanfani A, Dell'Omo G (2008) Effects of corticosteroids on oxidative damage and circulating carotenoids in captive adult kestrels (Falco tinnunculus). J Comp Physiol B 178:829–835
Costantini D, Rowe M, Butler MW, McGraw KJ (2010) From molecules to living systems: historical and contemporary issues in oxidative stress and antioxidant ecology. Funct Ecol 24:950–959
Cruz-Neto AP, Garland T, Abe AS (2001) Diet, phylogeny, and basal metabolic rate in phyllostomid bats. Zoology 104:49–58
Droege W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82:47–95
Garratt M, Brooks RC (2012) Oxidative stress and condition-dependent sexual signals: more than just seeing red. Proc R Soc B 279:3121–3130
Goyns MH (2002) Genes, telomeres and mammalian ageing. Mech Ageing Dev 123:791–799
Grafen A (1989) The phylogenetic regression. Phil Trans R Soc B 326:119–157
Harman D (1955) Aging: A theory based on free radical and radiation chemistry. University of California Radiation Laboratory
Hermes-Lima M, Zenteno-Savin T (2002) Animal response to drastic changes in oxygen availability and physiological oxidative stress. Comp Biochem Physiol C Toxicol Pharmacol 133:537–556
Hoffmann FG, Baker RJ (2003) Comparative phylogeography of short-tailed bats (Carollia: Phyllostomidae). Mol Ecol 12:3403–3414
Ives AR, Midford PE, Garland T Jr (2007) Within-species variation and measurement error in phylogenetic comparative methods. Syst Biol 56:252–270
Jones KE, Purvis A, Maclarnon ANN, Bininda-Emonds ORP, Simmons NB (2002) A phylogenetic supertree of the bats (Mammalia: Chiroptera). Biol Rev Camb Philos Soc 77:223–259
LaVal RK, Rodríguez B (2002) Murcielagos de Costa Rica. Editorial INBio
McGraw KJ, Cohen AA, Costantini D, Hõrak P (2010) The ecological significance of antioxidants and oxidative stress: a marriage between mechanistic and functional perspectives. Funct Ecol 24:947–949
Metcalfe NB, Alonso-Alvarez C (2010) Oxidative stress as a life—history constraint: the role of reactive oxygen species in shaping phenotypes from conception to death. Funct Ecol 24:984–996
Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884
Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290
Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2009) Nlme: Linear and nonlinear mixed effects models. R package version 3.1-96. R Foundation for Statistical Computing, Vienna, Austria, http://CRAN.R-project.org/package=Nlme
Price T (1997) Correlated evolution and independent contrasts. Phil Trans R Soc B 352:519–529
R Development Core Team (2010) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Reth M (2002) Hydrogen peroxide as second messenger in lymphocyte activation. Nat Immun 3:1129–1134
Rose G, Passarino G, Franceschi C, De Benedictis G (2002) The variability of the mitochondrial genome in human aging: a key for life and death? Int J Biochem Cell Biol 34:1449–1460
Salmon AB, Leonard S, Masamsetti V, Pierce A, Podlutsky AJ, Podlutskaya N, Richardson A, Austad SN, Chaudhuri AR (2009) The long lifespan of two bat species is correlated with resistance to protein oxidation and enhanced protein homeostasis. FASEB J 23:2317–2326
Schinnerl M, Aydinonat D, Schwarzenberger F, Voigt CC (2011) Hematological survey of common Neotropical bat species from Costa Rica. J Zoo Wildl Med 42:382–391
Schneeberger K, Czirják GÁ, Voigt CC (2013a) Inflammatory challenge increases measures of oxidative stress in a free-ranging, long-lived mammal. J Exp Biol 216:4514–4519
Schneeberger K, Czirják GÁ, Voigt CC (2013b) Measures of the constitutive immune system are linked to diet and roosting habits of Neotropical bats. PLoS ONE 8:e54023
Selman C, Blount JD, Nussey DH, Speakman JR (2012) Oxidative damage, ageing, and life-history evolution: where now? Trends Ecol Evol 27:570–577
Sohal RS, Brunk UT (1992) Mitochondrial production of pro-oxidants and cellular senescence. Mutat Res DNAging 275:295–304
Sohal RS, Weindruch R (1996) Oxidative stress, caloric restriction, and aging. Science 273:59–63
Sohal RS, Svensson I, Brunk UT (1990) Hydrogen peroxide production by liver mitochondria in different species. Mech Ageing Dev 53:209–215
Speakman JR, Selman C (2011) The free-radical damage theory: accumulating evidence against a simple link of oxidative stress to ageing and lifespan. Bioessays 33:255–259
Timm RM, LaVal RK (1998) A field key to the bats of Costa Rica. Occasional Publication Series, University of Kansas Center of Latin American Studies 22, 1–30
Voigt CC, Rex K, Michener RH, Speakman JR (2008) Nutrient routing in omnivorous animals tracked by stable carbon isotopes in tissue and exhaled breath. Oecologia 157:31–40
Wilkinson GS, South JM (2002) Life history, ecology and longevity in bats. Aging Cell 1:124–131
York HA, Billings SA (2009) Stable-isotope analysis of diets of short-tailed fruit bats (Chiroptera: Phyllostomidae: Carollia). J Mammal 90:1469–1477
Acknowledgments
We are grateful to Daniel Lewanzik, Oliver Lindecke and Tobias Teige for their help in the field and Alexandre Courtiol for statistical advice. We thank the Organization for Tropical Studies (OTS) for allowance to use their facilities and for providing logistic support, and the Costa Rican authorities for granting permission to conduct this research [186-2012-SINAC]. This study has been funded by the Deutsche Forschungsgemeinschaft (DFG Vo 890/25).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by: Fritz Geiser
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOC 477 kb)
Rights and permissions
About this article
Cite this article
Schneeberger, K., Czirják, G.Á. & Voigt, C.C. Frugivory is associated with low measures of plasma oxidative stress and high antioxidant concentration in free-ranging bats. Naturwissenschaften 101, 285–290 (2014). https://doi.org/10.1007/s00114-014-1155-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00114-014-1155-5