Skip to main content

Surviving at high elevations: an inter- and intra-specific analysis in a mountain bird community

Oecologia volume 184, pages 293–303 (2017)Cite this article

Abstract

Elevation represents an important selection agent on self-maintenance traits and correlated life histories in birds, but no study has analysed whether life-history variation along this environmental cline is consistent among and within species. In a sympatric community of passerines, we analysed how the average adult survival of 25 open-habitat species varied with their elevational distribution and how adult survival varied with elevation at the intra-specific level. For such purpose, we estimated intra-specific variation in adult survival in two mountainous species, the Water pipit (Anthus spinoletta) and the Northern wheatear (Oenanthe oenanthe) in NW Spain, by means of capture–recapture analyses. At the inter-specific level, high-elevation species showed higher survival values than low elevation ones, likely because a greater allocation to self-maintenance permits species to persist in alpine environments. At the intra-specific level, the magnitude of survival variation was lower by far. Nevertheless, Water pipit survival slightly decreased at high elevations, while the proportion of transient birds increased. In contrast, no such relationships were found in the Northern wheatear. Intra-specific analyses suggest that living at high elevation may be costly, such as for the Water pipit in our case study. Therefore, it seems that a species can persist with viable populations in uplands, where extrinsic mortality is high, by increasing the investment in self-maintenance and prospecting behaviours.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2

References

  • Anderson DR (2007) Model based inference in the life sciences: a primer on evidence. Springer, New York

    Google Scholar 

  • Badyaev AV (1997a) Altitudinal variation in sexual dimorphism: a new pattern and alternative hypotheses. Behav Ecol 8:675–690. doi:10.1093/beheco/8.6.675

    Article  Google Scholar 

  • Badyaev AV (1997b) Covariation between life history and sexually selected traits: an example with cardueline finches. Oikos 80:128–138. doi:10.2307/3546524

    Article  Google Scholar 

  • Badyaev AV, Ghalambor CK (2001) Evolution of life histories along elevational gradients: trade-off between parental care and fecundity. Ecology 82:2948–2960. doi:10.1890/0012-9658(2001)082[2948:EOLHAE]2.0.CO;2

    Article  Google Scholar 

  • Bastianelli G, Seoane J, Álvarez-Blanco P, Laiolo P (2015) The intensity of male-male interactions declines in highland songbird populations. Behav Ecol Sociobiol 69:1493–1500. doi:10.1007/s00265-015-1961-6

    Article  Google Scholar 

  • Bears H, Martin K, White GC (2009) Breeding in high-elevation habitat results in shift to slower life-history strategy within a single species. J Anim Ecol 78:365–375. doi:10.1111/j.1365-2656.2008.01491.x

    CAS  Article  PubMed  Google Scholar 

  • Bielby J, Mace GM, Bininda-Emonds ORP, Cardillo M, Gittleman JL, Jones KE, Purvis A (2007) The fast-slow continuum in mammalian life history: an empirical re-evaluation. Am Nat 169:748–757

    CAS  PubMed  Google Scholar 

  • Boyle AW, Sandercock BK, Martin K (2016) Patterns and drivers of intraspecific variation in avian life history along elevational gradients: a meta-analysis. Biol Rev 91:469–482. doi:10.1111/brv.12180

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and inference. A practical information-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  • Choquet R, Lebreton J-D, Gimenez O et al (2009) U-CARE: utilities for performing goodness of fit tests and manipulating CApture–REcapture data. Ecography (Cop) 32:1071–1074. doi:10.1111/j.1600-0587.2009.05968.x

    Article  Google Scholar 

  • Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, USA

    Google Scholar 

  • COA. Coordinadora Ornitolóxica D’Asturies, Indurot (2014) Atlas de las aves nidificantes de Asturies 1990-2010, Coordinadora Ornitolóxica D’Asturies

  • Coulson T, Ezard THG, Pelletier F et al (2008) Estimating the functional form for the density dependence from life history data. Ecology 89:1661–1674. doi:10.1890/07-1099.1

    CAS  Article  PubMed  Google Scholar 

  • Cramp S (1998) The complete birds of the western palearctic on CD-ROM. Oxford University Press, Oxford

    Google Scholar 

  • Crowl TA, Covich AP (1990) Predator-induced life-history shifts in a freshwater snail. Science 247:949–951

    CAS  Article  PubMed  Google Scholar 

  • Doak DF, Morris WF (2010) Demographic compensation and tipping points in climate-induced range shifts. Nature 467:959–962

    CAS  Article  PubMed  Google Scholar 

  • Doherty PF, Grubb TC (2002) Survivorship of permanent-resident birds in a fragmented forested landscape. Ecology 83:844–857. doi:10.1890/0012-9658(2002)083[0844:SOPRBI]2.0.CO;2

    Article  Google Scholar 

  • Drummond AJ, Ho SY, Rawlence N, Rambaut A (2007) A rough guide to BEAST 1.4. Available at: http://beast.bio.ed.ac.uk/Main_Page. Accessed 17 Mar 2017

  • Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15

    Article  Google Scholar 

  • Fernández-Chacón A, Genovart M, Álvarez D et al (2015) Neighbouring populations, opposite dynamics: influence of body size and environmental variation on the demography of stream-resident brown trout (Salmo trutta). Oecologia 178:379–389. doi:10.1007/s00442-015-3222-9

    Article  PubMed  Google Scholar 

  • Foerster K, Delhey K, Johnsen A et al (2003) Females increase offspring heterozygosity and fitness through extra-pair matings. Nature 425:714–717

    CAS  Article  PubMed  Google Scholar 

  • Forslund P, Pärt T (1995) Age and reproduction in birds—hypotheses and tests. Trends Ecol Evol 10:374–378

    CAS  Article  PubMed  Google Scholar 

  • Freckleton RP, Harvey PH, Pagel M (2002) Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 160:712–726

    CAS  Article  PubMed  Google Scholar 

  • Ghalambor CK, Martin TE (2001) Fecundity-survival trade-offs and parental risk-taking in birds. Science 292:494–497

    CAS  Article  PubMed  Google Scholar 

  • Gosselink TE, Van Deelen TR, Warner RE, Mankin PC (2007) Survival and cause-specific mortality of red foxes in agricultural and urban areas of Illinois. J Wildlife Manage 71:1862–1873

    Article  Google Scholar 

  • Grant BW, Dunham AE (1990) Elevational covariation in environmental constraints and life histories of the desert lizard Sceloporus merriami. Ecology 71:1765–1776. doi:10.2307/1937584

    Article  Google Scholar 

  • Hackett SJ, Kimball RT, Reddy S et al (2008) A phylogenomic study of birds reveals their evolutionary history. Science 320:1763–1768

    CAS  Article  PubMed  Google Scholar 

  • Hille SM, Cooper CB (2015) Elevational trends in life histories: revising the pace-of-life framework. Biol Rev 90:204–213. doi:10.1111/brv.12106

    Article  PubMed  Google Scholar 

  • Hodkinson ID (2005) Terrestrial insects along elevation gradients: species and community responses to altitude. Biol Rev 80:489. doi:10.1017/S1464793105006767

    Article  PubMed  Google Scholar 

  • Jetz W, Sekercioglu CH, Böhning-Gaese K (2008) The worldwide variation in avian clutch size across species and space. PLoS Biol 6:e303

    Article  PubMed Central  Google Scholar 

  • Jetz W, Thomas GH, Joy JB et al (2012) The global diversity of birds in space and time. Nature 491:444–448

    CAS  Article  PubMed  Google Scholar 

  • Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241. doi:10.1111/j.1461-0248.2004.00684.x

    Article  Google Scholar 

  • Lack D (1948) The significance of clutch-size. Part III.—Some interspecific comparisons. Ibis 90:25–45. doi:10.1111/j.1474-919X.1948.tb01399.x

    Article  Google Scholar 

  • Laiolo P, Obeso JR (2015) Plastic responses to temperature versus local adaptation at the cold extreme of the climate gradient. Evol Biol 42:473–482. doi:10.1007/s11692-015-9341-8

    Article  Google Scholar 

  • Laiolo P, Dondero F, Ciliento E, Rolando A (2004) Consequences of pastoral abandonment for the structure and diversity of the alpine avifauna. J Appl Ecol 41:294–304. doi:10.1111/j.0021-8901.2004.00893.x

    Article  Google Scholar 

  • Laiolo P, Seoane J, Illera JC et al (2015a) The evolutionary convergence of avian lifestyles and their constrained coevolution with species’ ecological niche. Proc R Soc B Biol Sci 282:20151808. doi:10.1098/rspb.2015.1808

    Article  Google Scholar 

  • Laiolo P, Illera JC, Meléndez L et al (2015b) Abiotic, biotic, and evolutionary control of the distribution of C and N isotopes in food webs. Am Nat 185:169–182. doi:10.1086/679348

    Article  PubMed  Google Scholar 

  • Lescroël A, Dugger KM, Ballard G, Ainley DG (2009) Effects of individual quality, reproductive success and environmental variability on survival of a long-lived seabird. J Anim Ecol 78:798–806. doi:10.1111/j.1365-2656.2009.01542.x

    Article  PubMed  Google Scholar 

  • Low M, Arlt D, Eggers S, Pärt T (2010) Habitat-specific differences in adult survival rates and its links to parental workload and on-nest predation. J Anim Ecol 79:214–224. doi:10.1111/j.1365-2656.2009.01595.x

    Article  PubMed  Google Scholar 

  • Martin TE (1995) avian life history evolution in relation to nest sites, nest predation, and food. Ecol Monogr 65:101–127. doi:10.2307/2937160

    Article  Google Scholar 

  • Martin TE (2004) Avian life-history evolution has an eminent past: does it have a bright future? Auk 121:289–301. doi:10.1642/0004-8038(2004)121[0289:ALEHAE]2.0.CO;2

    Article  Google Scholar 

  • Martin TE, Møller AP, Merino S, Clobert J (2001) Does clutch size evolve in response to parasites and immunocompetence? Proc Natl Acad Sci 98:2071–2076. doi:10.1073/pnas.98.4.2071

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Meléndez L, Laiolo P (2014) The role of climate in constraining the elevational range of the Water pipit Anthus spinoletta in an alpine environment. Ibis 156:276–287. doi:10.1111/ibi.12127

    Article  Google Scholar 

  • Meléndez L, Laiolo P, Mironov S et al (2014) Climate-driven variation in the intensity of a host-symbiont animal interaction along a broad elevation gradient. PLoS One 9:e101942

    Article  PubMed  PubMed Central  Google Scholar 

  • Metz J, Liancourt P, Kigel J et al (2010) Plant survival in relation to seed size along environmental gradients: a long-term study from semi-arid and Mediterranean annual plant communities. J Ecol 98:697–704. doi:10.1111/j.1365-2745.2010.01652.x

    Article  Google Scholar 

  • Morgan BJT (2000) Applied stochastic modelling. Arnold, London

    Google Scholar 

  • Morrison C, Hero J-M, Browning J (2004) Altitudinal variation in the age at maturity, longevity, and reproductive lifespan of anurans in subtropical queensland. Herpetologica 60:34–44. doi:10.1655/02-68

    Article  Google Scholar 

  • Muñoz MM, Wegener JE, Algar AC (2014) Untangling intra- and interspecific effects on body size clines reveals divergent processes structuring convergent patterns in Anolis lizards. Am Nat 184:636–646

    Article  PubMed  Google Scholar 

  • Ninyerola M, Pons X, Roure JM (2005) Altas Climático Digital de la Península Ibérica. Metodología y aplicaciones en bioclimatología y geobotánica (ed) Bellaterra. Universidad Autónoma de Barcelona

  • Öberg M, Arlt D, Pärt T et al (2015) Rainfall during parental care reduces reproductive and survival components of fitness in a passerine bird. Ecol Evol 5:345–356. doi:10.1002/ece3.1345

    Article  PubMed  Google Scholar 

  • Oro D, Pradel R, Lebreton J-D (1999) Food availability and nest predation influence life history traits in Audouin’s gull, Larus audouinii. Oecologia 118:438–445. doi:10.1007/s004420050746

    Article  PubMed  Google Scholar 

  • Owens IPF, Bennett PM (1995) Ancient ecological diversification explains life-history variation among living birds. Proc R Soc London Ser B Biol Sci 261:227–232

    Article  Google Scholar 

  • Paradis E, Claude J, Strimmer K (2004) APE: analyses of Phylogenetics and Evolution in R language. Bioinforma 20:289–290. doi:10.1093/bioinformatics/btg412

    CAS  Article  Google Scholar 

  • Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. In: Statistics and Computing Series. Springer, New York

  • Pinheiro J, Bates D, DebRoy S, Sarkar D (2014) R Core Team (2014) nlme: linear and nonlinear mixed effects models. R package version 3.1-117. Available at http://CRAN.R-project.org/package=nlme. Accessed 17 Mar 2017

  • Pradel R, Hines JE, Lebreton J-D, Nichols JD (1997) Capture-recapture survival models taking account of transients. Biometrics 53:60–72. doi:10.2307/2533097

    Article  Google Scholar 

  • Price TD, Hooper DM, Buchanan CD et al (2014) Niche filling slows the diversification of Himalayan songbirds. Nature 509:222–225

    CAS  Article  PubMed  Google Scholar 

  • Promislow DEL, Harvey PH (1990) Living fast and dying young: a comparative analysis of life-history variation among mammals. J Zool 220:417–437. doi:10.1111/j.1469-7998.1990.tb04316.x

    Article  Google Scholar 

  • Ricklefs RE, Wikelski M (2002) The physiology/life-history nexus. Trends Ecol Evol 17:462–468. doi:10.1016/S0169-5347(02)02578-8

    Article  Google Scholar 

  • Sæther B-E (1989) Survival rates in relation to body weight in European birds. Ornis Scand 20:13–21. doi:10.2307/3676702

    Article  Google Scholar 

  • Sandercock BK, Jaramillo A (2002) Annual survival rates of wintering sparrows: assessing demographic consequences of migration. Auk 119:149–165. doi:10.1642/0004-8038(2002)119[0149:ASROWS]2.0.CO;2

    Article  Google Scholar 

  • Sandercock BK, Martin K, Hannon SJ (2005) Demographic consequences of age-structure in extreme environments: population models for arctic and alpine ptarmigan. Oecologia 146:13–24. doi:10.1007/s00442-005-0174-5

    Article  PubMed  Google Scholar 

  • Santoro S, Green AJ, Figuerola J (2013) Environmental instability as a motor for dispersal: a case study from a growing population of glossy ibis. PLoS One 8:e82983. doi:10.1371/journal.pone.0082983

    Article  PubMed  PubMed Central  Google Scholar 

  • Sears MW, Angilletta MJ (2003) Life-history variation in the sagebrush lizard: phenotypic plasticity or local adaptation? Ecology 84:1624–1634. doi:10.1890/0012-9658(2003)084[1624:LVITSL]2.0.CO;2

    Article  Google Scholar 

  • Sibly RM, Brown JH (2007) Effects of body size and lifestyle on evolution of mammal life histories. Proc Natl Acad Sci 104:17707–17712. doi:10.1073/pnas.0707725104

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Stearns SC (1992) The evolution of life histories, vol 249. Oxford University Press, Oxford

    Google Scholar 

  • Stearns CS (2000) Life history evolution: successes, limitations, and prospects. Naturwissenschaften 87:476–486. doi:10.1007/s001140050763

    CAS  Article  PubMed  Google Scholar 

  • Tavecchia G, Pradel R, Boy V et al (2001) Sex- and age-related variation in survival and cost of first reproduction in greater flamingos. Ecology 82:165–174. doi:10.1890/0012-9658(2001)082[0165:SAARVI]2.0.CO;2

    Article  Google Scholar 

  • Tavecchia G, Pradel R, Lebreton J-D et al (2002) Sex-biased survival and breeding dispersal probability in a patchy population of the Rock sparrow Petronia petronia. Ibis 144:E79–E87. doi:10.1046/j.1474-919X.2002.00059.x

    Article  Google Scholar 

  • Tavecchia G, Pradel R, Genovart M, Oro D (2007) Density-dependent parameters and demographic equilibrium in open populations. Oikos 116:1481–1492. doi:10.1111/j.0030-1299.2007.15791.x

    Article  Google Scholar 

  • Vellend M, Lajoie G, Bourret A et al (2014) Drawing ecological inferences from coincident patterns of population- and community-level biodiversity. Mol Ecol 23:2890–2901. doi:10.1111/mec.12756

    Article  PubMed  Google Scholar 

  • Versteegh MA, Schwabl I, Jaquier S, Tieleman BI (2012) Do immunological, endocrine and metabolic traits fall on a single Pace-of-Life axis? Covariation and constraints among physiological systems. J Evol Biol 25:1864–1876. doi:10.1111/j.1420-9101.2012.02574.x

    CAS  Article  PubMed  Google Scholar 

  • White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46:S120–S139. doi:10.1080/00063659909477239

    Article  Google Scholar 

  • Wiersma P, Muñoz-Garcia A, Walker A, Williams JB (2007) Tropical birds have a slow pace of life. Proc Natl Acad Sci 104:9340–9345. doi:10.1073/pnas.0702212104

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Wilson S, Martin K (2011) Life-history and demographic variation in an alpine specialist at the latitudinal extremes of the range. Popul Ecol 53:459–471. doi:10.1007/s10144-011-0261-x

    Article  Google Scholar 

  • Zammuto RM, Millar JS (1985) Environmental predictability, variability, and spermophilus columbianus life history over an elevational gradient. Ecology 66:1784–1794. doi:10.2307/2937374

    Article  Google Scholar 

Download references

Acknowledgements

We are very grateful to the National Park Los Picos de Europa for providing permission to capture birds in the protected area. We are very grateful to Alvaréz P, Brunetti M., Cortés A., García J., Jiménez G., Jovani R., Juaréz N., Lomas M., Lozano M., Magaña O., and Segura A. for the great help during the field work. Thanks also to D’Amico M., Illera J.C., Santoro S., and Fernández-Chacón A. for their useful comments on the statistical analysis and Rochon E. for editing the English. We thank Olsson O. and an anonymous referee for providing insightful comments that improved this paper. Financial support was provided by the Spanish Ministry of Science and Innovation (CGL2008-02749, CGL2011-28177; FPI Grant BES-2012-053472) and Fundación Biodiversidad. JS works within the Madrid’s Government research group network REMEDINAL3-CM (S-2013/MAE-2719).

Author contribution statement

PL originally formulated the idea; LM, PL, JS, JRO, and GB performed fieldwork; GB, GT, and PL performed statistical analyses; GB wrote the manuscript; and PL, GT, JRO, and JS provided editorial advice.

Author information

Authors and Affiliations

  1. Research Unit of Biodiversity (UO, CSIC, PA), Universidad de Oviedo, 33600, Mieres, Spain

    G. Bastianelli, L. Meléndez, J. R. Obeso & P. Laiolo

  2. Institut Mediterrani d’Estudis Avançats (IMEDEA), CSIC-UIB, 07190, Esporles, Islas Baleares, Spain

    G. Tavecchia

  3. Terrestrial Ecology Group, Departamento de Ecología, Universidad Autónoma de Madrid, 28049, Madrid, Spain

    J. Seoane

Authors
  1. G. Bastianelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. G. Tavecchia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. L. Meléndez
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. Seoane
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J. R. Obeso
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. P. Laiolo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to G. Bastianelli.

Ethics declarations

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Additional information

This is the first study finding an interplay between intra- and inter-specific survival strategies that may affect species distribution along elevational gradients.

Communicated by Hannu J. Ylonen.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 2044 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Bastianelli, G., Tavecchia, G., Meléndez, L. et al. Surviving at high elevations: an inter- and intra-specific analysis in a mountain bird community. Oecologia 184, 293–303 (2017). https://doi.org/10.1007/s00442-017-3852-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-017-3852-1

Keywords

  • Adult survival
  • Elevation
  • Inter-specific variation
  • Capture–recapture analyses
  • Passerines