Skip to main content
SpringerLink
Log in

Effects of calcium supplementation on growth and biochemistry in two passerine species breeding in a Ca-poor and metal-polluted area

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

    We’re sorry, something doesn't seem to be working properly.

    Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Abstract

Several studies provide evidence of calcium (Ca)-limited reproduction in birds. A Ca-supplementation experiment was carried out in 2014 in a Ca-poor area associated with metal pollution in SW Finland. We aimed to evaluate the relationship between Ca availability and heavy metal exposure in free-living passerines, and to compare Ca levels in plasma and feces and the effects of Ca supplementation and metals on breeding, nestling growth, and plasma biochemistry in great tits and pied flycatchers. Although the Ca supplement was used by parents, in general the treatment had limited effects on growth and biochemistry, suggesting that parents are capable of finding sufficient Ca-rich foods to allow nestlings to grow properly. Snail shells were an abundant Ca source in the moderately polluted zone for pied flycatcher, and great tits likely combines the intake of snail shells and other anthropogenic Ca-rich items. Great tits had higher Ca concentrations in feces and plasma than pied flycatcher nestlings, suggesting that they need and sustain higher Ca levels and seem to be more opportunistic in search for Ca than pied flycatcher, since they consumed more of the supplemented Ca. Negative effects of pollution in nestling size and fledgling number were found in great tit. This species may suffer especially from the lower food quality and quantity in the polluted area. The pied flycatcher seems to be adapted to low Ca availability and they can successfully breed when metal concentrations are not too high. Our results show that great tits and pied flycatchers may employ different strategies in response to low Ca availability.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /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 excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Explore related subjects

Discover the latest articles, news and stories from top researchers in related subjects.

References

  • Alonso-Alvarez C, Ferrer M (2001) A biochemical study of fasting, subfeeding, and recovery processes in yellow-legged gulls. Physiol Biochem Zool PBZ 74:703–713. doi:10.1086/322932

    Article  CAS  Google Scholar 

  • Anthony LE, Edozien JC (1975) Experimental protein and energy deficiencies in the rat. J Nutr 105:631–648

    CAS  Google Scholar 

  • Belskii E, Grebennikov M (2014) Snail consumption and breeding performance of pied flycatchers (Ficedula hypoleuca) along a pollution gradient in the Middle Urals, Russia. Sci Total Environ 490:114–120. doi:10.1016/j.scitotenv.2014.04.116

    Article  CAS  Google Scholar 

  • Berglund ÅMM, Koivula MJ, Eeva T (2011) Species- and age-related variation in metal exposure and accumulation of two passerine bird species. Environ Pollut 159:2368–2374. doi:10.1016/j.envpol.2011.07.001

    Article  CAS  Google Scholar 

  • Berglund ÅMM, Rainio MJ, Eeva T (2012) Decreased metal accumulation in passerines as a result of reduced emissions. Environ Toxicol Chem SETAC 31:1317–1323. doi:10.1002/etc.1814

    Article  CAS  Google Scholar 

  • Berglund ÅMM, Rainio MJ, Eeva T (2015) Temporal trends in metal pollution: using bird excrement as indicator. PLOS ONE 10:e0117071. doi:10.1371/journal.pone.0117071

    Article  Google Scholar 

  • Cramp S, Perrins CM (1993) Handbook of the birds of Europe, the Middle East and North Africa. The birds of the Western Palearctic Vol 7: Flycatchers to Shrikes. Oxford University Press, London, U.K

    Google Scholar 

  • Dauwe T, Janssens E, Eens M (2006a) Effects of heavy metal exposure on the condition and health of adult great tits (Parus major). Environ Pollut 140:71–78. doi: 10.1016/j.envpol.2005.06.024

  • Dauwe T, Snoeijs T, Bervoets L, et al (2006b) Calcium availability influences lead accumulation in a passerine bird. Anim Biol 56:289–298. doi: 10.1163/157075606778441822

  • Derome J, Lindroos AJ (1998) Effects of heavy metal contamination on macronutrient availability and acidification parameters in forest soil in the vicinity of the Harjavalta Cu–Ni smelter, SW Finland. Environ Pollut 99:225–232

    Article  CAS  Google Scholar 

  • Derome J, Nieminen T (1998) Metal and macronutrient fluxes in heavy-metal polluted Scots pine ecosystems in SW Finland. Environ Pollut 103:219–228

    Article  CAS  Google Scholar 

  • Edozien JC, Switzer BR (1977) Effects of dietary protein, fat and energy on blood hemoglobin and hematocrit in the rat. J Nutr 107:1016–1021

    CAS  Google Scholar 

  • Eeva T (1996) Direct and indirect effects of air pollution on two hole-nesting bird species. PhD Thesis, University of Turku, Finland

  • Eeva T, Lehikoinen E (1995) Egg shell quality, clutch size and hatching success of the great tit (Parus major) and the pied flycatcher (Ficedula hypoleuca) in an air pollution gradient. Oecologia 102:312–323. doi:10.1007/BF00329798

    Article  Google Scholar 

  • Eeva T, Lehikoinen E (1996) Growth and mortality of nestling great tits (Parus major) and pied flycatchers (Ficedula hypoleuca) in a heavy metal pollution gradient. Oecologia 108:631–639

    Article  Google Scholar 

  • Eeva T, Lehikoinen E (2000) Pollution: recovery of breeding success in wild birds. Nature 403:851–852. doi:10.1038/35002672

    Article  CAS  Google Scholar 

  • Eeva T, Lehikoinen E (2004) Rich calcium availability diminishes heavy metal toxicity in pied flycatcher. Funct Ecol 18:548–553

    Article  Google Scholar 

  • Eeva T, Ryömä M, Riihimäki J (2005) Pollution-related changes in diets of two insectivorous passerines. Oecologia 145:629–639. doi:10.1007/s00442-005-0145-x

    Article  CAS  Google Scholar 

  • Eeva T, Sillanpää S, Salminen J-P (2009) The effects of diet quality and quantity on plumage colour and growth of great tit Parus major nestlings: a food manipulation experiment along a pollution gradient. J Avian Biol 40:491–499. doi:10.1111/j.1600-048X.2008.04535.x

    Article  Google Scholar 

  • Eeva T, Rainio K, Suominen O (2010) Effects of pollution on land snail abundance, size and diversity as resources for pied flycatcher, Ficedula hypoleuca. Sci Total Environ 408:4165–4169. doi:10.1016/j.scitotenv.2010.05.028

    Article  CAS  Google Scholar 

  • Eeva T, Rainio M, Berglund Å et al (2014) Experimental manipulation of dietary lead levels in great tit nestlings: limited effects on growth, physiology and survival. Ecotoxicol Lond Engl 23:914–928. doi:10.1007/s10646-014-1235-5

    Article  CAS  Google Scholar 

  • Ferrer M (1994) Nutritional condition of Spanish Imperial Eagle nestlings Aquila adalberti. Bird Study 41:120–123. doi:10.1080/00063659409477207

    Article  Google Scholar 

  • Fullmer CS, Edelstein S, Wasserman RH (1985) Lead-binding properties of intestinal calcium-binding proteins. J Biol Chem 260:6816–6819

    CAS  Google Scholar 

  • Graveland J (1995) The quest for calcium. Calcium limitation in the reproduction of forest passerines in relation to snail abundance and soil acidification. PhD thesis, University of Groningen, Groningen, The Netherlands

  • Graveland J (1996) Avian eggshell formation in calcium-rich and calcium-poor habitats: importance of snail shells and anthropogenic calcium sources. Can J Zool 74:1035–1044. doi:10.1139/z96-115

    Article  Google Scholar 

  • Graveland J, Berends JE (1997) Timing of the calcium uptake and effect of calcium deficiency on behaviour and egg-laying in captive Great Tits, Parus major. Physiol Zool 70:74–84

    Article  CAS  Google Scholar 

  • Graveland J, Drent RH (1997) Calcium availability limits breeding success of passerines on poor soils. J Anim Ecol 66:279–288. doi:10.2307/6028

    Article  Google Scholar 

  • Graveland J, van der Wal R (1996) Decline in snail abundance due to soil acidification causes eggshell defects in forest passerines. Oecologia 105:351–360. doi:10.1007/BF00328738

    Article  Google Scholar 

  • Graveland J, van Gijzen T (1994) Arthropods and seeds are not sufficient as calcium sources for shell formation and skeletal growth in passerines. Ardea 82:299–314

    Google Scholar 

  • Graveland J, van der Wal R, van Balen JH, van Noordwijk AJ (1994) Poor reproduction in forest passerines from decline of snail abundance on acidified soils. Nature 368:446–448. doi:10.1038/368446a0

    Article  Google Scholar 

  • Hochleithner M (1994) Chapter 11 Biochemistries. Avian medicine: principles and application, Ritchie, B.W., Harrison, G.J., Harrision, L.R. Wingers publishing, Florida.

  • Järup L, Alfvén T (2004) Low level cadmium exposure, renal and bone effects—the OSCAR study. Biometals Int J Role Met Ions Biol Biochem Med 17:505–509

    Article  Google Scholar 

  • Jasmin G, Solymoss B, Eu HY (1975) Effect of thyroparathyroidectomy and of a low calcium diet on the cardiomyopathy of the Syrian hamster. Recent Adv Stud Cardiac Struct Metab 10:717–729

    CAS  Google Scholar 

  • Jussila I (1997) A bioindicator study on the effects of air pollution on forest ecosystem at the Pori-Harjavalta district and northern Satakunta in SW-Finland. SYKEsarja B 12:1–78

    Google Scholar 

  • Koivula MJ, Eeva T (2010) Metal-related oxidative stress in birds. Environ Pollut 158:2359–2370. doi:10.1016/j.envpol.2010.03.013

    Article  CAS  Google Scholar 

  • Koivula MJ, Kanerva M, Salminen J-P et al (2011) Metal pollution indirectly increases oxidative stress in great tit (Parus major) nestlings. Environ Res 111:362–370. doi:10.1016/j.envres.2011.01.005

    Article  CAS  Google Scholar 

  • Mänd R, Tilgar V (2003) Does supplementary calcium reduce the cost of reproduction in the Pied Flycatcher Ficedula hypoleuca? Ibis 145:67–77. doi:10.1046/j.1474-919X.2003.00123.x

    Article  Google Scholar 

  • Mänd R, Tilgar V, Leivits A (2000) Reproductive response of great tits, Parus major, in a naturally base-poor forest habitat to calcium supplementation. Can J Zool 78:689–695. doi:10.1139/z99-255

    Article  Google Scholar 

  • McComb RB, Bowers GN, Posen S (1979) Alkaline phosphatase. Plenum Press, New York

    Book  Google Scholar 

  • Mitchell MA, Sandercock DA (1995) Creatine kinase isoenzyme profiles in the plasma of the domestic fowl (Gallus domesticus): effects of acute heat stress. Res Vet Sci 59:30–34

    Article  CAS  Google Scholar 

  • Poulin RG, Brigham RM (2001) Effects of supplemental calcium on the growth rate of an insectivorous bird, the purple martin (Progne subis). Écoscience 8:151–156

    Google Scholar 

  • Pounds JG (1984) Effect of lead intoxication on calcium homeostasis and calcium-mediated cell function: a review. Neurotoxicology 5:295–331

    CAS  Google Scholar 

  • Reynolds SJ (2001) The effects of low dietary calcium during egg-laying on eggshell formation and skeletal calcium reserves in the Zebra Finch Taeniopygia guttata. Ibis 143:205–215. doi:10.1111/j.1474-919X.2001.tb04476.x

    Article  Google Scholar 

  • Reynolds SJ, Perrins CM (2010) Dietary calcium availability and reproduction in birds. In: Thompson CF (ed) Current Ornithology Volume 17. Springer New York, pp 31–74

  • Reynolds SJ, Mänd R, Tilgar V (2004) Calcium supplementation of breeding birds: directions for future research. Ibis 146:601–614

    Article  Google Scholar 

  • Romagnoli E, Minisola G, Carnevale V et al (1998) Assessment of serum total and bone alkaline phosphatase measurement in clinical practice. Clin Chem Lab Med CCLM FESCC 36:163–168. doi:10.1515/CCLM.1998.030

    CAS  Google Scholar 

  • Sánchez-Virosta P, Espín S, García-Fernández AJ, Eeva T (2015) A review on exposure and effects of arsenic in passerine birds. Sci Total Environ 512–513:506–525. doi:10.1016/j.scitotenv.2015.01.069

    Article  Google Scholar 

  • Scheuhammer AM (1996) Influence of reduced dietary calcium on the accumulation and effects of lead, cadmium, and aluminum in birds. Environ Pollut 94:337–343. doi:10.1016/S0269-7491(96)00084-X

    Article  CAS  Google Scholar 

  • Staessen JA, Amery A, Lauwerys RR et al (1994) Renal function and historical environmental cadmium pollution from zinc smelters. The Lancet 343:1523–1527. doi:10.1016/S0140-6736(94)92936-X

    Article  CAS  Google Scholar 

  • Staessen JA, Roels HA, Emelianov D et al (1999) Environmental exposure to cadmium, forearm bone density, and risk of fractures: prospective population study. Public Health and Environmental Exposure to Cadmium (PheeCad) Study Group. Lancet Lond Engl 353:1140–1144

    Article  CAS  Google Scholar 

  • Starck JM (1998) Structural variants and invariants in avian embryonic and postnatal development. In: Avian Growth and Development: Evolution Within the Altricial-precocial Spectrum, Starck, J.M. & Ricklefs, R.E. (eds). Oxford University Press, pp 59–88

  • Suzuki Y, Chao SH, Zysk JR, Cheung WY (1985) Stimulation of calmodulin by cadmium ion. Arch Toxicol 57:205–211

    Article  CAS  Google Scholar 

  • Svensson L (1992) Identification guide to European passerines. Södertälje, Fingraf AB

  • Tilgar V, Mänd R, Leivits A (1999) Effect of calcium availability and habitat quality on reproduction in pied flycatcher Ficedula hypoleuca and great tit Parus major. J Avian Biol 30:383–391. doi:10.2307/3677010

    Article  Google Scholar 

  • Tilgar V, Mänd R, Mägi M (2002) Calcium shortage as a constraint on reproduction in great tits Parus major: a field experiment. J Avian Biol 33:407–413. doi:10.1034/j.1600-048X.2002.02990.x

    Article  Google Scholar 

  • Tilgar V, Mänd R, Ots I, et al (2004a) Calcium availability affects bone growth in nestlings of free-living great tits (Parus major), as detected by plasma alkaline phosphatase. J Zool 263:269–274. doi: 10.1017/S0952836904005254

  • Tilgar V, Ots I, Mänd R (2004b) Bone alkaline phosphatase as a sensitive indicator of skeletal development in birds: a study of the great tit nestlings. Physiol Biochem Zool PBZ 77:530–535. doi: 10.1086/420947

  • Viñuela J, Ferrer M (1997) Regulation of growth in Red Kites and imperial eagles. Wilson Bull 109:92–101

    Google Scholar 

  • Viñuela J, Ferrer M, Recio F (1991) Age-related variations in plasma levels of alkaline phosphatase, calcium and inorganic phosphorus in chicks of two species of raptors. Comp Biochem Physiol A Physiol 99:49–54. doi:10.1016/0300-9629(91)90233-3

    Article  Google Scholar 

  • Weishaar RE, Simpson RU (1987) Vitamin D3 and cardiovascular function in rats. J Clin Invest 79(6):1706–1712

    Article  CAS  Google Scholar 

  • Wu X, Jin T, Wang Z et al (2001) Urinary calcium as a biomarker of renal dysfunction in a general population exposed to cadmium. J Occup Environ Med Am Coll Occup Environ Med 43:898–904

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Jorma Nurmi and Miia Rainio for their help with the field work and biology students of Turku University for their help in screening the nest material for snail shells.

Author information

Author notes

    Authors and Affiliations

    1. Section of Ecology, Department of Biology, University of Turku, 20014, Turku, Finland

      Silvia Espín, Sandra Ruiz, Pablo Sánchez-Virosta & Tapio Eeva

    Authors
    1. Silvia Espín
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Sandra Ruiz
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Pablo Sánchez-Virosta
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Tapio Eeva
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Silvia Espín.

    Ethics declarations

    The experiment was conducted under licenses from the Animal Experiment Committee of the State Provincial Office of Southern Finland (license number ESAVI/1650/04.10.03/2012) and the Centre for Economic Development, Transport and the Environment, ELY Centre Southwest Finland (license number VARELY/319/07.01/2014).

    Conflict of interest

    The authors declare that they have no competing interests.

    Ethical approval

    “All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.”

    Informed consent

    “Informed consent was obtained from all individual participants included in the study.”

    Funding

    This work was supported by the Academy of Finland (project 265859 to T. Eeva) and by Societas pro Fauna et Flora Fennica (to P. Sánchez-Virosta).

    Additional information

    Responsible editor: Elena Maestri

    Sandra Ruiz and Pablo Sánchez-Virosta contributed equally to this work.

    Electronic supplementary material

    Below is the link to the electronic supplementary material.

    ESM 1

    (DOC 136 kb)

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Espín, S., Ruiz, S., Sánchez-Virosta, P. et al. Effects of calcium supplementation on growth and biochemistry in two passerine species breeding in a Ca-poor and metal-polluted area. Environ Sci Pollut Res 23, 9809–9821 (2016). https://doi.org/10.1007/s11356-016-6219-y

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s11356-016-6219-y

    Keywords

    Search

    Navigation