Log in

Ectoparasites exposure affects early growth and mouth colour in nestlings of a cavity-nesting raptor

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Nest-dwelling ectoparasites are a major source of stress for growing nestling birds, as they can negatively impact on growth and physiology, with consequences on pre-fledging mortality. Ectoparasites are expected to also affect chromatic traits involved in parent-offspring communication, because their expression requires the same resources used by nestlings for parasites defence and/or it is linked to individual state. However, the effects of ectoparasites on growth, condition and expression of begging components are poorly known, especially in raptors. Here, we examined the effects of an experimental ectoparasites removal on growth (body mass and forearm length) and expression of begging traits (size and colour of flange, cere and gape) in lesser kestrel (Falco naumanni) nestlings. Our manipulation was very effective in removing ectoparasites and parasite load had several detrimental effects on early growth and expression of visual signals directed to parents. Deparasitized nestlings grew faster in terms of body mass and forearm length, as well as mouth width and cere length. In addition, the red chromaticity of cere decreased with age, with deparasitized nestlings showing a faster decrease concomitantly with the increase in body growth. Such negative effects disappeared in later nestling stages and ectoparasites did not affect pre-fledging survival. Our results showed that visual components of begging have the potential to reveal individual condition during early nestling stages, above and beyond ectoparasite infection. They are also consistent with previous evidence that ectoparasites weakly affect fitness in colonial and cavity-nesting avian hosts, which have evolved greater resistance due to prolonged host-parasite interactions.

Significance statement

Ectoparasites are considered a major stressor for nestling birds, as they can negatively affect their growth, survival but also traits involved in parent-offspring communication. We experimentally show that ectoparasite infection has only little and transient negative effects on the early growth of lesser kestrel nestlings. However, nestlings recover from such a slower growth without paying any cost in terms of final body size and pre-fledging survival. In addition, we reveal that mouth colour does not mirror the level of ectoparasite infestation, but it is a reliable signal of nestlings’ individual general condition. Therefore, ectoparasites only weakly affect fitness in this species, likely because of the intense host-parasite interaction, which is typical of colonial and cavity-nesting species.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

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

Similar content being viewed by others

Data availability

The datasets analysed in this study are attached as a Supplementary Material.

References

  • Aparicio JM (1997) Cost and benefits of surplus offspring in the lesser kestrel (Falco naumanni). Behav Ecol Sociobiol 41:129–137

    Article  Google Scholar 

  • Ardia DR (2005) Tree swallows trade off immune function and reproductive effort differently across their range. Ecology 86:2040–2046

    Article  Google Scholar 

  • Asghar M, Hasselquist D, Hansson B, Zehtindjiev P, Westerdahl H, Bensch S (2015) Hidden costs of infection: chronic malaria accelerates telomere degradation and senescence in wild birds. Science 347:436–438

    Article  CAS  PubMed  Google Scholar 

  • Atkinson CT, Thomas NJ, Hunter DB (2009) Parasitic diseases of wild birds. John Wiley & Sons, Hoboken

    Google Scholar 

  • Avery ML, Primus TM, Mihaich EM, Decker DG, Humphrey JS (1998) Consumption of fipronil-treated rice seed does not affect captive blackbirds. Pestic Sci 52:91–96

    Article  CAS  Google Scholar 

  • Avilés JM, Parejo D (2013) Colour also matters for nocturnal birds: owlet bill coloration advertises quality and influences parental feeding behaviour in little owls. Oecologia 173:399–408

    Article  PubMed  Google Scholar 

  • Avilés JM, Pérez-Contreras T, Navarro C, Soler JJ (2009) Male spotless starlings adjust feeding effort based on egg spots revealing ectoparasite load. Anim Behav 78:993–999

    Article  Google Scholar 

  • Bergman TJ, Beehner JC (2008) A simple method for measuring colour in wild animals: validation and use on chest patch colour in geladas (Theropithecus gelada). Biol J Linn Soc 94:231–240

    Article  Google Scholar 

  • Bize P, Piault R, Moureau B, Heeb P (2006) A UV signal of offspring condition mediates context-dependent parental favouritism. Proc R Soc Lond B 273:2063–2068

    Google Scholar 

  • Bize P, Jeanneret C, Klopfenstein A, Roulin A (2008) What makes a host profitable? Parasites balance host nutritive resources against immunity. Am Nat 171:107–118

    Article  PubMed  Google Scholar 

  • 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 161:367–379

    Article  PubMed  Google Scholar 

  • Bortolotti GR, Fernie KJ, Smits JE (2003) Carotenoid concentration and coloration of American Kestrels (Falco sparverius) disrupted by experimental exposure to PCBs. Funct Ecol 17:651–657

    Article  Google Scholar 

  • Brooks ME, Kristensen K, Van Benthem KJ, Magnusson A, Berg CW, Nielsen A, Bolker BM (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J 9:378–400

    Article  Google Scholar 

  • Brown CR, Brown MB, Rannala B (1995) Ectoparasites reduce long-term survival of their avian host. Proc R Soc Lond B 262:313–319

    Article  Google Scholar 

  • Brown CR, Hannebaum SL, O’Brien VA, Page CE, Rannala B, Roche EA, Brown MB (2021) The cost of ectoparasitism in Cliff Swallows declines over 35 years. Ecol Monogr 91:e01446

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Capelle KJ, Whitworth TL (1973) The distribution and avian hosts of Carnus hemapterus (Diptera: Milichiidae) in North America. J Med Entomol 10:525–526

    Article  CAS  PubMed  Google Scholar 

  • Casagrande S, Costantini D, Fanfani A, Tagliavini J, Dell’Omo G (2007) Patterns of serum carotenoid accumulation and skin colour variation in kestrel nestlings in relation to breeding conditions and different terms of carotenoid supplementation. J Comp Physiol B 177:237–245

    Article  CAS  PubMed  Google Scholar 

  • Casagrande S, Dell'Omo G, Costantini D, Tagliavini J, Groothuis T (2011) Variation of a carotenoid-based trait in relation to oxidative stress and endocrine status during the breeding season in the Eurasian kestrel: a multi-factorial study. Comp Biochem Physiol A 160:16–26

    Article  CAS  Google Scholar 

  • Christe P, Richner H, Oppliger A (1996) Begging, food provisioning, and nestling competition in great tit broods infested with ectoparasites. Behav Ecol 7:127–131

    Article  Google Scholar 

  • Christe P, Møller AP, de Lope F (1998) Immunocompetence and nestling survival in the house martin: the tasty chick hypothesis. Oikos 83:175–179

    Article  CAS  Google Scholar 

  • Clayton DH, Moore J (1997) Host–parasite evolution. General principles and avian models. Oxford University Press, Oxford

    Google Scholar 

  • Costantini D, Coluzza C, Fanfani A, Dell’Omo G (2007) Effects of carotenoid supplementation on colour expression, oxidative stress and body mass in rehabilitated captive adult kestrels (Falco tinnunculus). J Comp Physiol B 177:723–731

    Article  CAS  PubMed  Google Scholar 

  • Dawson RD, Bortolotti GR (1997) Ecology of parasitism of nestling American Kestrels by Carnus hemapterus (Diptera, Carnidae). Can J Zool 75:2021–2026

    Article  Google Scholar 

  • Dawson RD, Bortolotti GR (2006) Carotenoid-dependent coloration of male American kestrels predicts ability to reduce parasitic infections. Naturwissenschaften 93:597–602

    Article  CAS  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 Lope F, Møller AP, De la Cruz C (1998) Parasitism, immune response and reproductive success in the house martin Delichon urbica. Oecologia 114:188–193

    Article  PubMed  Google Scholar 

  • De Simone JG, Clotfelter ED, Black EC, Knutie SA (2018) Avoidance, tolerance, and resistance to ectoparasites in nestling and adult tree swallows. J Avian Biol 49:jav-01641

    Article  Google Scholar 

  • Descamps S, Blondel J, Lambrechts MM, Hurtrez-Boussès S, Thomas F (2002) Asynchronous hatching in a blue tit population: a test of some predictions related to ectoparasites. Can J Zool 80:1480–1484

    Article  Google Scholar 

  • Dey CJ, Valcu M, Kempenaers B, Dale J (2015) Carotenoid-based bill coloration functions as a social, not sexual, signal in songbirds (Aves: Passeriformes). J Evol Biol 28:250–258

    Article  CAS  PubMed  Google Scholar 

  • Dugas MB (2009) House sparrow, Passer domesticus, parents preferentially feed nestlings with mouth colours that appear carotenoid-rich. Anim Behav 78:767–772

    Article  Google Scholar 

  • Dugas MB, Doumas LT (2014) Ectoparasite density is associated with mouth colour and size in nestling house sparrows Passer domesticus. Ibis 156:682–686

    Article  Google Scholar 

  • Dugas MB, Rosenthal GG (2010) Carotenoid-rich mouth colors influence the conspicuousness of nestling birds. Behav Ecol Sociobiol 64:455–462

    Article  Google Scholar 

  • Ewen JG, Thorogood R, Brekke P, Cassey P, Karadas F, Armstrong DP (2009) Maternally invested carotenoids compensate costly ectoparasitism in the hihi. P Natl Acad Sci USA 106:12798–12802

    Article  CAS  Google Scholar 

  • Fair J, Whitaker S, Pearson B (2007) Sources of variation in haematocrit in birds. Ibis 149:535–552

    Article  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 

  • Forbes S, Thornton S, Glassey B, Forbes M, Buckley NJ (1997) Why parent birds play favourites. Nature 390:351–352

    Article  CAS  Google Scholar 

  • Ganbold O, Azua J, Munkhbayar M, Khuderchuluun O, Paek WK, Purevee E, Reading RP (2020) First records of the parasitic flies Carnus hemapterus and Ornithophila gestroi on lesser kestrels (Falco naumanni) in Mongolia. J Raptor Res 54:66–73

    Article  Google Scholar 

  • García-Heras MS, Arroyo B, Simmons RE, Camarero PR, Mateo R, García JT, Mougeot F (2017) Pollutants and diet influence carotenoid levels and integument coloration in nestlings of an endangered raptor. Sci Total Environ 603:299–307

    Article  PubMed  Google Scholar 

  • Gil D, Bulmer E, Celis P, Lopez-Rull I (2008) Adaptive developmental plasticity in growing nestlings: sibling competition induces differential gape growth. Proc R Soc Lond B 275:549–554

    Google Scholar 

  • Gray DA (1996) Carotenoids and sexual dichromatism in North American passerine birds. Am Nat 148:453–480

    Article  Google Scholar 

  • Griffiths R, Double MC, Orr K, Dawson RJ (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075

    Article  CAS  PubMed  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 

  • Hoi H, Krištofık J, Darolová A, Hoi C (2010) Are parasite intensity and related costs of the milichiid fly Carnus hemapterus related to host sociality? J Ornithol 151:907–913

    Article  Google Scholar 

  • Hoi H, Darolová A, Krištofík J, Hoi C (2018) The effect of the ectoparasite Carnus hemapterus on immune defence, condition, and health of nestling European Bee-eaters. J Ornithol 159:291–302

    Article  Google Scholar 

  • Huber SK (2008) Effects of the introduced parasite Philornis downsi on nestling growth and mortality in the medium ground finch (Geospiza fortis). Biol Conserv 141:601–609

    Article  Google Scholar 

  • Hunt S, Kilner RM, Langmore NE, Bennett AT (2003) Conspicuous, ultraviolet-rich mouth colours in begging chicks. Proc R Soc Lond B 270:S25–S28

    Article  Google Scholar 

  • Johnson LS, Albrecht DJ (1993) Effects of haematophagous ectoparasites on nestling house wrens, Troglodytes aedon: who pays the cost of parasitism? Oikos 66:255–262

    Article  Google Scholar 

  • Kilner R (1997) Mouth colour is a reliable signal of need in begging canary nestlings. Proc R Soc Lond B 264:963–968

    Article  Google Scholar 

  • Kilner R, Davies NB (1998) Nestling mouth colour: ecological correlates of a begging signal. Anim Behav 56:705–712

    Article  CAS  PubMed  Google Scholar 

  • Kužner J, Turk S, Grace S, Soni-Gupta J, Fourie JJ, Marchiondo AA, Rugg D (2013) Confirmation of the efficacy of a novel fipronil spot-on for the treatment and control of fleas, ticks and chewing lice on dogs. Vet Parasitol 193:245–251

    Article  PubMed  Google Scholar 

  • La Gioia G, Melega L, Fornasari L (2017) Piano d’Azione Nazionale per il grillaio Falco naumanni: Quaderni di Conservazione della Natura. MATTM– ISPRA, Roma, p 41

    Google Scholar 

  • Lachish S, Knowles SCL, Alves R, Wood MJ, Sheldon BC (2011) Fitness effects of endemic malaria infections in a wild bird population: the importance of ecological structure. J Anim Ecol 80:1196–1206

    Article  PubMed  Google Scholar 

  • López-Arrabé J, Cantarero A, Pérez-Rodríguez L, Palma A, Alonso-Alvarez C, González-Braojos S, Moreno J (2015) Nest-dwelling ectoparasites reduce antioxidant defences in females and nestlings of a passerine: a field experiment. Oecologia 179:29–41

    Article  PubMed  Google Scholar 

  • Lüdecke D, Makowski D, Waggoner P, Patil I (2020) Performance: assessment of regression models performance. CRAN. https://doi.org/10.5281/zenodo.3952174

  • Magrath RD (1989) Hatching asynchrony and reproductive success in the blackbird. Nature 339:536–538

    Article  Google Scholar 

  • Magrath RD (1990) Hatching asynchrony in altricial birds. Biol Rev 65:587–622

    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  Google Scholar 

  • Merino S (2010) Immunocompetence and parasitism in nestlings from wild populations. Open Ornithol J 3:27–32

    Article  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 

  • Minias P (2015) The use of haemoglobin concentrations to assess physiological condition in birds: A review. Conserv Physiol 3:1–15

    Article  Google Scholar 

  • Mock DW, Dugas MB, Strickler SA (2011) Honest begging: expanding from signal of need. Behav Ecol 22:909–917

    Article  Google Scholar 

  • Møller AP (1990) Effects of a haematophagous mite on the barn swallow (Hirundo rustica): a test of the Hamilton and Zuk hypothesis. Evolution 44:771–784

    PubMed  Google Scholar 

  • Møller AP, Erritzøe J (1996) Parasite virulence and host immune defense: host immune response is related to nest reuse in birds. Evolution 50:2066–2072

    Article  PubMed  Google Scholar 

  • Møller AP, Nielsen JT (2007) Malaria and risk of predation: a comparative study of birds. Ecology 88:871–881

    Article  PubMed  Google Scholar 

  • Møller AP, Christe P, Lux E (1999) Parasitism, host immune function, and sexual selection. Q Rev Biol 74:3–20

    Article  PubMed  Google Scholar 

  • Møller AP, Arriero E, Lobato E, Merino S (2009) A meta-analysis of parasite virulence in nestling birds. Biol Rev 84:567–588

    Article  PubMed  Google Scholar 

  • Moreno-Rueda G, Redondo T, Ochoa D, Camacho C, Canal D, Potti J (2016) Nest-dwelling ectoparasites reduce begging effort in pied flycatcher Ficedula hypoleuca nestlings. Ibis 158:881–886

    Article  Google Scholar 

  • Morinay J, De Pascalis F, Dominoni DM, Morganti M, Pezzo F, Pirrello S, Visceglia M, De Capua E, Cecere JG, Rubolini D (2021) Combining social information use and comfort seeking for nest site selection in a cavity-nesting raptor. Anim Behav 180:167–178

    Article  Google Scholar 

  • Morrison BL, Johnson LS (2002) Feeding of house wren nestlings afflicted by hematophagous ectoparasites: a test of the parental compensation hypothesis. Condor 104:183–187

    Article  Google Scholar 

  • Mougeot F, Pérez-Rodríguez L, Martinez-Padilla J, Leckie F, Redpath SM (2007) Parasites, testosterone and honest carotenoid-based signalling of health. Funct Ecol 21:886–898

    Article  Google Scholar 

  • Mougeot F, Pérez-Rodríguez L, Sumozas N, Terraube J (2009) Parasites, condition, immune responsiveness and carotenoid-based ornamentation in male red-legged partridge Alectoris rufa. J Avian Biol 40:67–74

    Article  Google Scholar 

  • Negro JJ, Hiraldo F (1993) Nest-site selection and breeding success in the lesser kestrel Falco naumanni. Bird Stud 40:115–119

    Article  Google Scholar 

  • O’Connor JA, Sulloway FJ, Robertson J, Kleindorfer S (2010) Philornis downsi parasitism is the primary cause of nestling mortality in the critically endangered Darwin’s medium tree finch (Camarhynchus pauper). Biodivers Conserv 19:853–866

    Article  Google Scholar 

  • O'Connor JA, Robertson J, Kleindorfer S (2014) Darwin's finch begging intensity does not honestly signal need in parasitised nests. Ethology 120:228–237

    Article  Google Scholar 

  • Ortego J, Aparicio JM, Calabuig G, Cordero PJ (2007) Risk of ectoparasitism and genetic diversity in a wild lesser kestrel population. Mol Ecol 16:3712–3720

    Article  CAS  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 

  • Owens IPF, Hartley IR (1998) Sexual dimorphism in birds: why are there so many different forms of dimorphism? Proc R Soc Lond B 265:397–407

    Article  Google Scholar 

  • Parejo D, Avilés JM, Rodríguez J (2010) Visual cues and parental favouritism in a nocturnal bird. Biol Lett 6:171–173

    Article  PubMed  Google Scholar 

  • Pirrello S, Pilastro A, Serra L (2015) Nest-dwelling ectoparasites influence the start and duration of the first pre-basic moult in the European starling Sturnus vulgaris. J Avian Biol 46:412–418

    Article  Google Scholar 

  • Pirrello S, Colombo E, Pilastro A, Pozzato M, Rubolini D, Saino N, Romano A (2017) Skin and flange colour, but not ectoparasites, predict condition and survival in starling nestlings. Behav Ecol Sociobiol 71:63

    Article  Google Scholar 

  • Podofillini S, Cecere JG, Griggio M, Curcio A, De Capua EL, Fulco E, Rubolini D (2018) Home, dirty home: effect of old nest material on nest-site selection and breeding performance in a cavity-nesting raptor. Curr Zool 64:693–702

    PubMed  PubMed Central  Google Scholar 

  • Podofillini S, Cecere JG, Griggio M, Corti M, De Capua EL, Parolini M, Rubolini D (2019) Benefits of extra food to reproduction depend on maternal condition. Oikos 128:943–959

    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 

  • Romano A, Rubolini D, Caprioli M, Boncoraglio G, Ambrosini R, Saino N (2011) Sex-related effects of an immune challenge on growth and begging behavior of barn swallow nestlings. PLoS One 6:e22805

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Romano A, Rubolini D, Ambrosini R, Saino N (2014) Early exposure to a bacterial endotoxin may cause breeding failure in a migratory bird. Ethol Ecol Evol 26:80–85

    Article  Google Scholar 

  • Romano A, Nodari R, Bandi C, Caprioli M, Costanzo A, Ambrosini R, Saino N (2019) Haemosporidian parasites depress breeding success and plumage coloration in female barn swallows Hirundo rustica. J Avian Biol 50:jav01889

    Article  Google Scholar 

  • Roulin A, Brinkhof MWG, Bize P, Richner H, Jungi TW, Bavoux C, Boileau N, Burneleau G (2003) Which chick is tasty to parasites?The importance of host immunology vs parasite life history. J Anim Ecol 72:75–81

    Article  Google Scholar 

  • Saino N, Calza S, Møller AP (1998) Effects of a dipteran ectoparasite on immune response and growth trade-offs in barn swallow, Hirundo rustica, nestlings. Oikos 81:217–228

    Article  Google Scholar 

  • Sara M, Bondi S, Bermejo A, Bourgeois M, Bouzin M, Bustamante J, Rubolini D (2019) Broad-front migration leads to strong migratory connectivity in the lesser kestrel (Falco naumanni). J Biogeogr 46:2663–2677

    Article  Google Scholar 

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

    Google Scholar 

  • Schuetz JG (2005) Reduced growth but not survival of chicks with altered gape patterns: implications for the evolution of nestling similarity in a parasitic finch. Anim Behav 70:839–848

    Article  Google Scholar 

  • Serra L, Pirrello S, Caprioli M, Griggio M, Andreotti A, Romano A, Rubolini D (2012) Seasonal decline of offspring quality in the European starling Sturnus vulgaris: an immune challenge experiment. Behav Ecol Sociobiol 66:697–709

    Article  Google Scholar 

  • Sheldon BC, Verhulst S (1996) Ecological immunity: costly parasite defense and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321

    Article  CAS  PubMed  Google Scholar 

  • Simon A, Thomas DW, Blondel J, Lambrechts MM, Perret P (2003) Within-brood distribution of ectoparasite attacks on nestling blue tits: a test of the tasty chick hypothesis using inulin as a tracer. Oikos 102:551–558

    Article  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 

  • Soler JJ, Neve LD, Pérez–Contreras T, Soler M, Sorci G. (2003) Trade-off between immunocompetence and growth in magpies: an experimental study. Proc R Soc Lond B 270(1512):241–248

    Article  Google Scholar 

  • Soler JJ, Aviles JM, Cuervo JJ, Perez-Contreras T (2007) Is the relation between colour and immune response mediated by nutritional condition in spotless starling nestlings? Anim Behav 74:1139–1145

    Article  Google Scholar 

  • Soler JJ, Ruiz-Castellano C, Figuerola J, Martín-Vivaldi M, Martínez-de la Puente J, Ruiz-Rodríguez M, Tomás G (2017) Telomere length and dynamics of spotless starling nestlings depend on nest-building materials used by parents. Anim Behav 126:89–100

    Article  Google Scholar 

  • Soravia C, Cecere JG, Rubolini D (2021) Brood sex ratio modulates the effects of extra food on parental effort and sibling competition in a sexually dimorphic raptor. Behav Ecol Sociobiol 75:62

    Article  Google Scholar 

  • Stevens M, Parraga CA, Cuthill IC, Partridge JC, Troscianko TS (2007) Using digital photography to study animal coloration. Biol J Linn Soc 90:211–237

    Article  Google Scholar 

  • Sumasgutner P, Adrion M, Gamauf A (2018) Carotenoid coloration and health status of urban Eurasian kestrels (Falco tinnunculus). PLoS One 13:e0191956

    Article  PubMed  PubMed Central  Google Scholar 

  • Svensson PA, Wong BBM (2011) Carotenoid-based signals in behavioural ecology: a review. Behaviour 148:131–189

    Article  Google Scholar 

  • Szép T, Møller AP (1999) Cost of parasitism and host immune defence in the sand martin Riparia riparia: a role for parent-offspring conflict? Oecologia 119:9–15

    Article  PubMed  Google Scholar 

  • Szép T, Møller AP (2000) Exposure to ectoparasites increases within-brood variability in size and body mass in the sand martin. Oecologia 125(2):201–207

    Article  PubMed  Google Scholar 

  • Thorogood R, Kilner RM, Karadaş F, Ewen JG (2008) Spectral mouth colour of nestlings changes with carotenoid availability. Funct Ecol 22:1044–1051

    Article  Google Scholar 

  • Tripet F, Richner H (1997) Host responses to ectoparasites: food compensation by parent blue tits. Oikos 78:557–561

    Article  Google Scholar 

  • Tschirren B, Fitze PS, Richner H (2005) Carotenoid-based nestling colouration and parental favouritism in the great tit. Oecologia 143:477–482

    Article  PubMed  Google Scholar 

  • Tschirren B, Romero-Haro AÁ, Zahn S, Criscuolo F (2021) Sex-specific effects of experimental ectoparasite infestation on telomere length in great tit nestlings. J Evol Biol 34:584–589

    Article  CAS  PubMed  Google Scholar 

  • Valera F, Hoi H, Darolova A, Kristofik J (2004) Size versus health as a cue for host choice: a test of the tasty chick hypothesis. Parasitology 129:59–68

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We wish to thank S. Podofillini, the late M. Griggio, and several students for assistance during fieldwork and lab work. We are grateful to E. De Capua (Provincia di Matera), M. Cristallo (Genio Civile Matera) and the Comune di Matera, Ufficio Scuole, for authorizing and tolerating our work and presence at the breeding colonies, as well as for constant support during field activities. We also thank Prof. Matthew Dugas and Prof. Gregorio Moreno-Rueda for the constructive comments on the early version of the manuscript.

Funding

The study was supported by institutional funding from the Università degli Studi di Milano, and the Istituto Nazionale per la Protezione e la Ricerca Ambientale (ISPRA).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Andrea Romano.

Ethics declarations

Ethics approval

Handling of wild birds was performed by the Italian Institute for Environmental Protection and Research (ISPRA) under the authorization of Law 157/1992 [Art. 4 (1) and Art. 7 (5)]. No bird was injured by the handling procedure. All applicable national and institutional guidelines for the use of animals were followed. Ethical approval from ethics committee for involving animals in this study was not required.

Conflict of interest

The authors declare no competing interests.

Additional information

Communicated by M. Leonard

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

ESM 1

(DOCX 6222 kb)

ESM 2

(XLS 4363 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Romano, A., Corti, M., Soravia, C. et al. Ectoparasites exposure affects early growth and mouth colour in nestlings of a cavity-nesting raptor. Behav Ecol Sociobiol 75, 158 (2021). https://doi.org/10.1007/s00265-021-03098-x

Download citation

  • Published:

  • DOI: https://doi.org/10.1007/s00265-021-03098-x

Keywords

Navigation