Skip to main content

Advertisement

SpringerLink
Log in

Nest-dwelling ectoparasites reduce antioxidant defences in females and nestlings of a passerine: a field experiment

  • Physiological ecology - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Ectoparasites may imply a cost in terms of oxidative stress provoked by inflammatory responses in hosts. Ectoparasites may also result in costs for nestlings and brooding females because of the direct loss of nutrients and reduced metabolic capacity resulting from parasite feeding activities. These responses may involve the production of reactive oxygen and nitrogen species that may induce oxidative damage in host tissues. Our goal was to examine the effect of ectoparasites in terms of oxidative stress for nestlings and adult females in a population of pied flycatchers Ficedula hypoleuca. We manipulated the entire nest ectoparasite community by reducing ectoparasite loads in some nests through a heating treatment and compared them with a control group of nests with natural loads. A marker of total antioxidant capacity (TAS) in plasma and total levels of glutathione (tGSH) in red blood cells as well as a marker of oxidative damage in plasma lipids (malondialdehyde; MDA) were assessed simultaneously. Levels of tGSH were higher in heat-treated nests than in controls for both females and nestlings. Higher TAS values were observed in females from heat-treated nests. In nestlings there was a negative correlation between TAS and MDA. Our study supports the hypothesis that ectoparasites expose cavity-nesting birds to an oxidative challenge. This could be paid for in the long term, ultimately compromising individual fitness.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Agarwal R, Chase SD (2002) Rapid, fluorimetric-liquid chromatographic determination of malondialdehyde in biological samples. J Chromatogr B 775:121–126

    Article  CAS  Google Scholar 

  • Alonso-Alvarez C, Ferrer M (2001) A biochemical study of fasting, subfeeding, and recovery processes in yellow-legged gulls. Physiol Biochem Zool 74:703–713

    Article  CAS  PubMed  Google Scholar 

  • Alonso-Alvarez C, Galván I (2011) Free radical exposure creates paler carotenoid-based ornaments: a possible interaction in the expression of black and red traits. PloS One 6:e19403

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Alonso-Alvarez C, Velando A (2012) Benefits and costs of parental care. In: Royle NJ, Smiseth PT, Kolliker M (eds) The evolution of parental care. Oxford University Press, Oxford, pp 40–61

    Chapter  Google Scholar 

  • Atkinson CT, van Riper C (1991) Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus. In: Loye JE, Zuk M (eds) Bird-parasite interactions: ecology, evolution and behaviour. Oxford University Press, New York, pp 19–48

    Google Scholar 

  • Baron RW, Weintraub J (1987) Immunological responses to parasitic arthropods. Parasitol Today 3:77–82

    Article  CAS  PubMed  Google Scholar 

  • Bauchau V (1997) Do parasitic mites decrease growth of nestling pied flycatchers Ficedula hypoleuca? Ardea 85:243–247

    Google Scholar 

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

    Article  Google Scholar 

  • Blount JD, Houston DC, Surai PF, Møller AP (2004) Egg–laying capacity is limited by carotenoid pigment availability in wild gulls Larus fuscus. Proc R Soc Lond B Biol Sci 271:S79–S81

    Article  CAS  Google Scholar 

  • Brommer JE, Pitala N, Siitari H, Kluen E, Gustafsson L (2011) Body size and immune defense of nestling blue tits (Cyanistes caeruleus) in response to manipulation of ectoparasites and food supply. Auk 128:556–563

    Article  Google Scholar 

  • Calabrese EJ (2007) Threshold dose-response model-RIP: 1911 to 2006. BioEssays 29:686–688

    Article  PubMed  Google Scholar 

  • Cantarero A, López-Arrabé J, Redondo AJ, Moreno J (2013a) Behavioural responses to ectoparasites in pied flycatchers Ficedula hypoleuca: an experimental study. J Avian Biol 44:591–599

    Article  Google Scholar 

  • Cantarero A, López-Arrabé J, Rodríguez-García V, González-Braojos S, Ruiz-de-Castañeda R, Redondo AJ, Moreno J (2013b) Factors affecting the presence and abundance of generalist ectoparasites in nests of three sympatric hole-nesting bird species. Acta Ornithol 48:39–54

    Article  Google Scholar 

  • Christe P, Richner H, Oppliger A (1996) Of great tits and fleas: sleep baby sleep. Anim Behav 52:1087–1092

    Article  Google Scholar 

  • Cohen J (1992) A power primer. Psychol Bull 112:155–159

    Article  CAS  PubMed  Google Scholar 

  • Cohen A, Klasing K, Ricklefs R (2007) Measuring circulating antioxidants in wild birds. Comp Biochem Physiol B 147:110–121

    Article  PubMed  CAS  Google Scholar 

  • Collias NE, Collias EC (1984) Nest building and bird behavior. Princeton University Press, Princeton

    Book  Google Scholar 

  • Costantini D (2008) Oxidative stress in ecology and evolution: lessons from avian studies. Ecol Lett 11:1238–1251

    PubMed  Google Scholar 

  • Costantini D (2011) On the measurement of circulating antioxidant capacity and the nightmare of uric acid levels. Method Ecol Evol 2:321–325

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Costantini D, dell’Ariccia G, Lipp HP (2008) Long flights and age affect oxidative status of homing pigeons (Columba livia). J Exp Biol 211:377–381

    Article  CAS  PubMed  Google Scholar 

  • Costantini D, Monaghan P, Metcalfe NB (2010) Ecological processes in a hormetic framework. Ecol Lett 13:1435–1447

    Article  PubMed  Google Scholar 

  • de Ayala RM, Saino N, Møller AP, Anselmi C (2007) Mouth coloration of nestlings covaries with offspring quality and influences parental feeding behavior. Behav Ecol 18:526–534

    Article  Google Scholar 

  • de Coster G, de Neve L, Verhulst S, Lens L (2012) Maternal effects reduce oxidative stress in female nestlings under high parasite load. J Avian Biol 43:177–185

    Article  Google Scholar 

  • Demas GE, Chefer V, Talan MI, Nelson RJ (1997) Metabolic costs of mounting an antigen-stimulated immune response in adult and aged C57BL/6 J mice. Am J Physiol 273:R1631–R1637

    CAS  PubMed  Google Scholar 

  • Dotan Y, Lichtenberg D, Pinchuk I (2004) Lipid peroxidation cannot be used as a universal criterion of oxidative stress. Prog Lipid Res 43:200–227

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Dugas MB (2012) Cross-fostering reveals that among-brood differences in ornamental mouth coloration mostly reflect rearing conditions in nestling house sparrows. Biol J Linn Soc 106:169–179

    Article  Google Scholar 

  • Edward DA, Chapman T (2011) Mechanisms underlying reproductive trade-offs: costs of reproduction. In: Flatt T, Heyland A (eds) Mechanisms of life history evolution. Oxford University Press, Oxford, pp 137–152

    Chapter  Google Scholar 

  • Eeva T, Lehikoinen E, Nurmi J (1994) Effects of ectoparasites on breeding success of great tits (Parus major) and pied flycatchers (Ficedula hypoleuca) in an air-pollution gradient. Can J Zool 72:624–635

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Fitze PS, Clobert J, Richner H (2004a) Long-term life-history consequences of ectoparasite-modulated growth and development. Ecology 85:2018–2026

    Article  Google Scholar 

  • Fitze PS, Tschirren B, Richner H (2004b) Life history and fitness consequences of ectoparasites. J Anim Ecol 73:216–226

    Article  Google Scholar 

  • Galván I, Alonso-Alvarez C (2008) An intracellular antioxidant determines the expression of a melanin-based signal in a bird. PLoS One 3:e3335

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Galván I, Alonso-Alvarez C (2009) The expression of melanin-based plumage is separately modulated by exogenous oxidative stress and a melanocortin. Proc R Soc Lond B Biol Sci 276:3089–3097

    Article  CAS  Google Scholar 

  • García-Berthou E (2001) On the misuse of residuals in ecology: testing regression residuals vs. the analysis of covariance. J Anim Ecol 70:708–711

    Article  Google Scholar 

  • Golden TR, Hinerfeld DA, Melov S (2002) Oxidative stress and aging: Beyond correlation. Aging Cell 1:117–123

    Article  CAS  PubMed  Google Scholar 

  • González-Braojos S, Vela AI, Ruiz-de-Castañeda R, Briones V, Cantarero A, Moreno J (2012) Is nestling growth affected by nest reuse and skin bacteria in pied flycatchers Ficedula hypoleuca? Acta Ornithol 47:119–127

    Article  Google Scholar 

  • Goodenough AE, Stallwood B (2010) Intraspecific variation and interspecific differences in the bacterial and fungal assemblages of blue tit (Cyanistes caeruleus) and great tit (Parus major) nests. Microb Ecol 59:221–232

    Article  PubMed  Google Scholar 

  • Griffith OW (1999) Biologic and pharmacologic regulation of mammalian glutathione synthesis. Free Radical Bio Med 27:922–935

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Heeb P, Werner I, Kölliker M, Richner H (1998) Benefits of induced host responses against an ectoparasite. Proc R Soc Lond B Biol Sci 265:51–56

    Article  Google Scholar 

  • Heeb P, Kölliker M, Richner H (2000) Bird-ectoparasite interactions, nest humidity, and ectoparasite community structure. Ecology 81:958–968

    Google Scholar 

  • Helfenstein F, Losdat S, Møller AP, Blount JD, Richner H (2010) Sperm of colourful males are better protected against oxidative stress. Ecol Lett 13:213–222

    Article  PubMed  Google Scholar 

  • Hõrak P, Saks L, Karu U, Ots I, Surai PF, McGraw KJ (2004a) How coccidian parasites affect health and appearance of greenfinches. J Anim Ecol 73:935–947

    Article  Google Scholar 

  • Hõrak P, Surai PF, Ots I, Møller AP (2004b) Fat soluble antioxidants in brood-rearing great tits Parus major: relations to health and appearance. J Avian Biol 35:63–70

    Article  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  PubMed  CAS  Google Scholar 

  • Hõrak P, Saks L, Zilmer M, Karu U, Zilmer K (2007) Do dietary antioxidants alleviate the cost of immune activation? An experiment with greenfinches. Am Nat 170:625–635

    Article  PubMed  Google Scholar 

  • Isaksson C, Örnborg J, Stephensen E, Andersson S (2005) Plasma glutathione and carotenoid coloration as potential biomarkers of environmental stress in great tits. EcoHealth 2:138–146

    Article  Google Scholar 

  • Jenni-Eiermann S, Jenni L (1998) What can plasma metabolites tell us about the metabolism, physiological state and condition of individual birds? An overview. Biol Conserv Fauna 102:312–319

    Google Scholar 

  • Lambrechts MM, Adriaensen F, Ardia DR, Artemyev AV, Atiénzar F, Bánbura J, Barba E, Bouvier J-C, Camprodon J, Cooper CB, Dawson RD, Eens M, Eeva T, Faivre B, Garamszegi LZ, Goodenough AE, Gosler AG, Grégoire A, Griffith SC, Gustafsson L, Scott-Johnson L, Kania W, Keišs O, Llambias PE, Mainwaring MC, Mänd R, Massa B, Mazgajski TD, Møller AP, Moreno J, Naef-Daenzer B, Nilsson J-A, Norte AC, Orell M, Otter KA, Park CR, Perrins CM, Pinowski J, Porkert J, Potti J, Remeš V, Richner H, Rytkönen S, Shiao M-T, Silverin B, Slagsvold T, Smith HG, Sorace A, Stenning MJ, Stewart I, Thompson CF, Török J, Tryjanowski P, van Noordwijk AJ, Winkler DW, Ziane N (2010) The design of artificial nestboxes for the study of secondary hole-nesting birds: a review of methodological inconsistencies and potential biases. Acta Ornithol 45:1–26

    Article  Google Scholar 

  • Lesgards JF, Durand P, Lassarre M, Stocker P, Lesgards G, Lanteaume A, Prost M, Lehucher-Michel MP (2002) Assessment of lifestyle effects on the overall antioxidant capacity of healthy subjects. Environ Health Persp 110:479

    Article  Google Scholar 

  • Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121

    Google Scholar 

  • Lobato E, Moreno J, Merino S, Sanz JJ, Arriero E (2005) Haematological variables are good predictors of recruitment in nestling pied flycatchers (Ficedula hypoleuca). Écoscience 12:27–34

    Article  Google Scholar 

  • Lobato E, Merino S, Moreno J, Morales J, Tomás G, Martínez-de la Puente J, Osorno JL, Kuchar A, Möstl E (2008) Corticosterone metabolites in blue tit and pied flycatcher droppings: effects of brood size, ectoparasites and temperature. Horm Behav 53:295–305

    Article  CAS  PubMed  Google Scholar 

  • Lundberg A, Alatalo RV (1992) The pied flycatcher. Poyser, London

    Google Scholar 

  • Martínez-de la Puente J, Merino S, Lobato E, Rivero-de Aguilar J, Del Cerro S, Ruiz-de-Castañeda R, Moreno J (2009) Does weather affect biting fly abundance in avian nests? J Avian Biol 40:653–657

    Article  Google Scholar 

  • Martínez-de la Puente J, Merino S, Lobato E, Rivero-de Aguilar J, del Cerro S, Ruiz-de-Castañeda R, Moreno J (2010) Nest-climatic factors affect the abundance of biting flies and their effects on nestling condition. Acta Oecol 36:543–547

    Article  Google Scholar 

  • Martínez-de la Puente J, Merino S, Tomás G, Moreno J, Morales J, Lobato E, Martínez J (2011) Nest ectoparasites increase physiological stress in breeding birds: an experiment. Naturwissenschaften 98:99–106

    Article  PubMed  CAS  Google Scholar 

  • Mateos R, Lecumberri E, Ramos S, Goya L, Bravo L (2005) Determination of malondialdehyde (MDA) by high-performance liquid chromatography in serum and liver as a biomarker for oxidative stress: Application to a rat model for hypercholesterolemia and evaluation of the effect of diets rich in phenolic antioxidants from fruits. J Chromatogr B 827:76–82

    Article  CAS  Google Scholar 

  • McCue MD (2010) Starvation physiology: reviewing the different strategies animals use to survive a common challenge. Comp Biochem Physiol A 156:1–18

    Article  CAS  Google Scholar 

  • Meister A (1991) Glutathione deficiency produced by inhibition of its synthesis, and its reversal; applications in research and therapy. Pharmacol Ther 51:155–194

    Article  CAS  PubMed  Google Scholar 

  • Merino S, Potti J (1995) Mites and blowflies decrease growth and survival in nestling pied flycatchers. Oikos 73:95–103

    Article  Google Scholar 

  • Merino S, Potti J (1996) Weather dependent effects of nest ectoparasites on their bird hosts. Ecography 19:107–113

    Article  Google Scholar 

  • Merino S, Potti J (1998) Growth, nutrition and blow fly parasitism in nestling pied flycatchers. Can J Zool 76:936–941

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Metcalfe NB, Monaghan P (2013) Does reproduction cause oxidative stress? An open question. Trends Ecol Evol 28:347–350

    Article  PubMed  Google Scholar 

  • Miller NJ, Rice-Evans C, Davies MJ, Gopinathan V, Milner A (1993) A novel method for measuring antioxidant capacity and its application to monitoring the antioxidant status in premature neonates. Clin Sci 84:407

    Article  CAS  PubMed  Google Scholar 

  • Møller AP (1997) Parasitism and the evolution of host life history. In: Clayton DH, Moore J (eds) Host-parasite evolution: general principles and avian models. Oxford University Press, Oxford, pp 105–127

    Google Scholar 

  • Møller AP, de Lope F, Moreno J, González G, Pérez JJ (1994) Ectoparasites and host energetics: house martin bugs and house martin nestlings. Oecologia 98:263–268

    Article  Google Scholar 

  • Møller AP, Christe P, Garamszegi LZ (2005) Coevolutionary arms races: increased host immune defense promotes specialization by avian fleas. J Evol Biol 18:46–59

    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 

  • Moreno J, Merino S, Potti J, de León A, Rodríguez R (1999) Maternal energy expenditure does not change with flight costs or food availability in the pied flycatcher (Ficedula hypoleuca): costs and benefits for nestlings. Behav Ecol Sociobiol 46:244–251

    Article  Google Scholar 

  • Moreno J, Lobato E, Morales J, Merino S, Martínez-de La Puente J, Tomás G (2008) Pre-laying nutrition mediates maternal effects on offspring immune capacity and growth in the pied flycatcher. Oecologia 156:727–735

    Article  PubMed  Google Scholar 

  • Moreno J, Merino S, Lobato E, Ruiz-de-Castañeda R, Martínez-de La Puente J, del Cerro S, Rivero-de Aguilar J (2009) Nest-dwelling ectoparasites of two sympatric hole-nesting passerines in relation to nest composition: An experimental study. Écoscience 16:418–427

    Article  Google Scholar 

  • Moreno-Rueda G, Redondo T, Trenzado CE, Sanz A, Zúñiga JM (2012) Oxidative stress mediates physiological costs of begging in magpie (Pica pica) nestlings. PLoS One 7:e40367

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mougeot F, Martínez-Padilla J, Webster LM, Blount JD, Pérez-Rodríguez L, Piertney SB (2009) Honest sexual signalling mediated by parasite and testosterone effects on oxidative balance. Proc R Soc Lond B Biol Sci 276:1093–1100

    Article  Google Scholar 

  • Noguera JC, Kim SY, Velando A (2011) Pre-fledgling oxidative damage predicts recruitment in a long-lived bird. Biol Lett 8:61–63

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Norte AC, Ramos JA, Araujo PM, Sousa JP, Sheldon BC (2008) Health-state variables and enzymatic biomarkers as survival predictors in nestling great tits (Parus major): effects of environmental conditions. Auk 125:943–952

    Article  Google Scholar 

  • Oppliger A, Richner H, Christe P (1994) Effect of an ectoparasite on lay date, nest-site choice, desertion, and hatching success in the great tit (Parus major). Behav Ecol 5:130–134

    Article  Google Scholar 

  • Owen JP, Delany ME, Cardona CJ, Bickford AA, Mullens BA (2009) Host inflammatory response governs fitness in an avian ectoparasite, the northern fowl mite (Ornithonyssus sylviarum). Int J Parasitol 39:789–799

    Article  PubMed  Google Scholar 

  • Owen JP, Nelson AC, Clayton DH (2010) Ecological immunology of bird-ectoparasite systems. Trends Parasitol 26:530–539

    Article  PubMed  Google Scholar 

  • Pap PL, Vágási CI, Czirják GÁ, Titilincu A, Pintea A, Osváth G, Fülöp A, Barta Z (2011) The effect of coccidians on the condition and immune profile of molting house sparrows (Passer domesticus). Auk 128:330–339

    Article  Google Scholar 

  • Pérez-Rodríguez L, Romero-Haro AA, Sternalski A, Muriel J, Mougeot F, Gil D, Alonso-Alvarez C (2015) Measuring oxidative stress: the confounding effect of lipid concentration in measures of lipid peroxidation. Physiol Biochem Zool. doi:10.1086/680688

    PubMed  Google Scholar 

  • Pérez-Rodríguez L (2009) Carotenoids in evolutionary ecology: re-evaluating the antioxidant role. BioEssays 31:1116–1126

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Potti J (2007) Variation in the hematocrit of a passerine bird across life stages is mainly of environmental origin. J Avian Biol 38:726–730

    Article  Google Scholar 

  • Potti J, Moreno J, Merino S, Frías O, Rodríguez R (1999) Environmental and genetic variation in the haematocrit of fledgling pied flycatchers Ficedula hypoleuca. Oecologia 120:1–8

    Article  Google Scholar 

  • Potti J, Dávila JA, Tella JL, Frias O, Villar S (2002) Gender and viability selection on morphology in fledgling pied flycatchers. Mol Ecol 11:1317–1326

    Article  CAS  PubMed  Google Scholar 

  • Proctor H, Owens I (2000) Mites and birds: diversity, parasitism and coevolution. Trends Ecol Evol 15:358–364

    Article  PubMed  Google Scholar 

  • Rakhshandehroo E, Razavi SM, Nazifi S, Farzaneh M, Mobarraei N (2013) Dynamics of the enzymatic antioxidants during experimental caprine coccidiosis. Parasitol Res 112:1437–1441

    Article  CAS  PubMed  Google Scholar 

  • Rendell WB, Verbeek NAM (1996) Are avian ectoparasites more numerous in nest boxes with old nest material? Can J Zool 74:1819–1825

    Article  Google Scholar 

  • Richner H, Tripet F (1999) Ectoparasitism and the trade-off between current and future reproduction. Oikos 86:535–538

    Article  Google Scholar 

  • Richner H, Oppliger A, Christe P (1993) Effect of an ectoparasite on reproduction in great tits. J Anim Ecol 62:703–710

    Article  Google Scholar 

  • Romero-Haro AA, Alonso-Alvarez C (2014) Covariation in oxidative stress markers in the blood of nestling and adult birds. Physiol Biochem Zool 87:353–362

    Article  CAS  PubMed  Google Scholar 

  • Saino N, Bertacche V, Ferrari RP, Martinelli R, Møller AP, Stradi R (2002) Carotenoid concentration in barn swallow eggs is influenced by laying order, maternal infection and paternal ornamentation. Proc R Soc Lond B Biol Sci 269:1729–1733

    Article  CAS  Google Scholar 

  • Saino N, Caprioli M, Romano M, Boncoraglio G, Rubolini D, Ambrosini R, Bonisoli-Alquati A, Romano A (2011) Antioxidant defenses predict long-term survival in a passerine bird. PLoS One 6:e19593

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sanz JJ, Moreno J (1995) Mass loss in brooding female pied flycatchers Ficedula hypoleuca: no evidence for reproductive stress. J Avian Biol 26:313–320

    Article  Google Scholar 

  • Schwilch R, Jenni L, Jenni-Eiermann S (1996) Metabolic responses of homing pigeons to flight and subsequent recovery. J Comp Physiol B 166:77–87

    Article  Google Scholar 

  • Sepp T, Karu U, Blount JD, Sild E, Männiste M, Hõrak P (2012) Coccidian infection causes oxidative damage in greenfinches. PLoS One 7:e36495

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sies H, Stahl W (1995) Vitamins E and C, beta-carotene, and other carotenoids as antioxidants. Am J Clin Nutr 62:1315S–1321S

    CAS  PubMed  Google Scholar 

  • Simon A, Thomas D, Blondel J, Perret P, Lambrechts MM (2004) Physiological ecology of Mediterranean blue tits (Parus caeruleus L.): effects of ectoparasites (Protocalliphora spp.) and food abundance on metabolic capacity of nestlings. Physiol Biochem Zool 77:492–501

    Article  PubMed  Google Scholar 

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

    Article  PubMed Central  PubMed  Google Scholar 

  • Tomás G, Merino S, Moreno J, Morales J (2007) Consequences of nest reuse for parasite burden and female health and condition in blue tits, Cyanistes caeruleus. Anim Behav 73:805–814

    Article  Google Scholar 

  • Tomás G, Merino S, Martínez-de la Puente J, Moreno J, Morales J, Lobato E (2008) Determinants of abundance and effects of blood-sucking flying insects in the nest of a hole-nesting bird. Oecologia 156:305–312

    Article  PubMed  Google Scholar 

  • Tomás G, Merino S, Martínez-de la Puente J, Moreno J, Morales J, Lobato E, Rivero-de Aguilar J, del Cerro S (2012) Interacting effects of aromatic plants and female age on nest-dwelling ectoparasites and blood-sucking flies in avian nests. Behav Process 90:246–253

    Article  Google Scholar 

  • van de Crommenacker J, Richardson DS, Koltz AM, Hutchings K, Komdeur J (2012) Parasitic infection and oxidative status are associated and vary with breeding activity in the Seychelles warbler. Proc R Soc Lond B Biol Sci 279:1466–1476

    Article  Google Scholar 

  • von Schantz T, Bensch S, Grahn M, Hasselquist D, Wittzell H (1999) Good genes, oxidative stress and condition-dependent sexual signals. Proc R Soc Lond B Biol Sci 266:1–12

    Article  Google Scholar 

  • Wegmann M, Boegeli B, Richner H (2015) Physiological responses to increased brood size and ectoparasite infestation: Adult great tits favour self-maintenance. Physiol Behav 141:127–134

    Article  CAS  PubMed  Google Scholar 

  • Wu G, Fang YZ, Yang S, Lupton JR, Turner ND (2004) Glutathione metabolism and its implications for health. J Nutr 134:489–492

    CAS  PubMed  Google Scholar 

  • Zuk M, Stoehr AM (2002) Immune defense and host life history. Am Nat 160:S9–S22

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This study was financed by project CGL2010-19233-C03-02 to J. M. from the Spanish Ministerio de Ciencia e Innovación (MICINN). A. C. was supported by a FPU grant from the Ministerio de Educación, Ciencia y Deporte (MECD) and S. G.-B. and J. L.-A. by FPI grants from MICINN. L. P.-R. was supported by a postdoctoral contract from the Spanish Ministerio de Economía y Competitividad (MINECO), through the Severo Ochoa Programme for Centres of Excellence in R&D&I (SEV-2012-0262). Permissions for handling birds were provided by the Consejería de Medio Ambiente de Castilla y León, and J. Donés and M. Redondo of the Centro Montes de Valsaín allowed us to work in the study area. We thank E. Jiménez-Vaquero, S. Merino and E. Pérez-Badás for collaboration in the field. We are also grateful to Jonathan D. Blount for initial advice on the analysis of MDA levels. This study is a contribution to the research developed at the El Ventorrillo field station. The experiments comply with current Spanish laws, and grant holder and field researchers were officially licensed for animal manipulation following current EU regulations on animal manipulation (authorization types C and B).

Author information

Authors and Affiliations

  1. Dpto. Ecología Evolutiva, Museo Nacional de Ciencias Naturales—CSIC, C/José Gutiérrez Abascal 2, 28006, Madrid, Spain

    Jimena López-Arrabé, Alejandro Cantarero, Lorenzo Pérez-Rodríguez, Antonio Palma, Carlos Alonso-Alvarez, Sonia González-Braojos & Juan Moreno

  2. Dpto. Ecología Evolutiva, Estación Biológica de Doñana—CSIC, Avda. Américo Vespucio s/n, Isla de la Cartuja, 41092, Seville, Spain

    Lorenzo Pérez-Rodríguez

Authors
  1. Jimena López-Arrabé
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alejandro Cantarero
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lorenzo Pérez-Rodríguez
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Antonio Palma
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Carlos Alonso-Alvarez
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sonia González-Braojos
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Juan Moreno
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jimena López-Arrabé.

Additional information

Communicated by Indrikis Krams.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

López-Arrabé, J., Cantarero, A., Pérez-Rodríguez, L. et al. Nest-dwelling ectoparasites reduce antioxidant defences in females and nestlings of a passerine: a field experiment. Oecologia 179, 29–41 (2015). https://doi.org/10.1007/s00442-015-3321-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-015-3321-7

Keywords

Search

Navigation