Skip to main content
SpringerLink
Log in

Direct and indirect effects of the El Niño Southern Oscillation on development and survival of young of a tropical passerine

  • Ecosystem ecology – original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

The El Niño Southern Oscillation (ENSO) is a global phenomenon that influences climate variation and, in turn, the ecological processes affecting the abundance and distribution of populations across taxa. For example, the ENSO can profoundly influence the development and survival of pelagic species, but the extent to which the ENSO affects offspring of terrestrial species is less well known. We used piecewise structural equation modeling to investigate the direct and indirect relationship between the ENSO and offspring development and survival in a terrestrial tropical passerine, the lance-tailed manakin (Chiroxiphia lanceolata). The Oceanic Niño Index (ONI), a measure of the ENSO, was negatively related to individual growth rate, maximum number of lesion developed by nestlings, and hatching day-of-year; which in turn mediated indirect effects on fledging success and recruitment. Further the ONI was a better predictor of nestling development compared to local temperature and rainfall. Our study establishes a link between the ENSO and the development and survival of young of a terrestrial species and underscores the need to better understand how offspring cope with global climate variation.

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
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Akaike H (1998a) Information theory and an extension of the maximum likelihood principle. In: Parzen E, Tanabe K, Kitagawa G (eds) Selected papers of Hirotugu Akaike. Springer, New York, pp 199–213

    Chapter  Google Scholar 

  • Akaike H (1998b) Prediction and Entropy. In: Parzen E, Tanabe K, Kitagawa G (eds) Selected papers of Hirotugu Akaike. Springer, New York, pp 387–410

    Google Scholar 

  • Allan R, Lindesay J, Parker D (1996) El Niño southern oscillation & climatic variability. CSIRO Publishing, Collingwood

    Google Scholar 

  • Ancona S, Drummond H (2013) Life history plasticity of a tropical seabird in response to El Niño anomalies during early life. PLoS One 8:e72665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ancona S, Sánchez-Colón S, Rodríguez C, Drummond H (2011) El Niño in the warm tropics: local sea temperature predicts breeding parameters and growth of blue-footed boobies. J Anim Ecol 80:799–808

    Article  PubMed  Google Scholar 

  • Atkinson CT, Lease JK, Dusek RJ, Samuel MD (2005) Prevalence of pox-like lesions and malaria in forest bird communities on leeward Mauna Loa Volcano, Hawaii. Condor 107:537–546

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Bilbo SD, Schwarz JM (2012) The immune system and developmental programming of brain and behavior. Front Neuroendocrinol 33:267–286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • Clements AN (1992) The biology of mosquitoes, vol 1. Development, nutrition and reproduction. Chapman & Hall, London

    Google Scholar 

  • Clements AN (2012) The biology of mosquitoes, vol 3. Transmission of viruses and interactions with bacteria. Cabi, London

    Book  Google Scholar 

  • Cruz JB, Cruz F (1990) Effect of El Niño Southern Oscillation conditions on nestling growth-rate in the dark-rumped petrel. Condor 92:160–165

    Article  Google Scholar 

  • Drummond H, Ancona S (2015) Observational field studies reveal wild birds responding to early-life stresses with resilience, plasticity, and intergenerational effects. Auk 132:563–576

    Article  Google Scholar 

  • DuVal EH (2007) Cooperative display and lekking behavior of the lance-tailed manakin (Chiroxiphia lanceolata). Auk 124:1168–1185

    Article  Google Scholar 

  • DuVal EH, Vanderbilt CC, M’Gonigle LK (2018) The spatial dynamics of female choice in an exploded lek generate benefits of aggregation for experienced males. Anim Behav 143:215–225

    Article  Google Scholar 

  • Fernando DMG, Kaluarachchi CI, Ratnatunga CN (2013) Necrotizing fasciitis and death following an insect bite. Am J Forensic Med Pathol 34:234–236

    Article  PubMed  Google Scholar 

  • Frederiksen M, Harris MP, Daunt F, Rothery P, Wanless S (2004) Scale-dependent climate signals drive breeding phenology of three seabird species. Glob Change Biol 10:1214–1221

    Article  Google Scholar 

  • Grace JB, Johnson DJ, Lefcheck JS, Byrnes JEK (2018) Quantifying relative importance: computing standardized effects in models with binary outcomes. Ecosphere 9:e02283

    Article  Google Scholar 

  • Grant PR, Grant BR, Keller LF, Petren K (2000) Effects of El Niño events on Darwin’s finch productivity. Ecology 81:2442–2457

    Google Scholar 

  • Hallet TB, Coulson T, Pilkington JG et al (2004) Why large-scale climate indices seem to predict ecological processes better than local weather. Nature 430:71–75

    Article  CAS  Google Scholar 

  • Harrell F (2001) Regression modeling strategies: with applications to linear models, logistic and ordinal regression, and survival analysis. Springer, New York

    Book  Google Scholar 

  • Harvell CD, Kim K, Burkholder JM et al (1999) Emerging marine diseases-climate links and anthropogenic factors. Science (80-) 285:1505–1510

    Article  CAS  Google Scholar 

  • Harvell C, Mitchell C, Ward J et al (2002) Climate warming and disease risks for terrestrial and marine biota. Science (80-) 296:2158–2163

    Article  CAS  Google Scholar 

  • Holmgren M, Scheffer M, Ezcurra E et al (2001) El Niño effects on the dynamics of terrestrial ecosystems. Trends Ecol Evol 16:89–94

    Article  CAS  PubMed  Google Scholar 

  • Hunter DB, Rohner C, Currie DC (1997) Mortality in fledgling great horned owls from black fly hematophaga and leucocytozoonosis. J Wildl Dis 33:486–491

    Article  CAS  PubMed  Google Scholar 

  • Jackson GD, Domeier ML (2003) The effects of an extraordinary El Niño/La Niña event on the size and growth of the squid Loligo opalescens off Southern California. Mar Biol 142:925–935

    Article  Google Scholar 

  • Jaksic FM (2001) Ecological effects of El Niño in terrestrial ecosystems of western South America. Ecography (Cop) 24:241–250

    Article  Google Scholar 

  • Jones BC, DuVal EH (2019) Artificial incubation does not affect the post-hatch development, health, or survival of the Lance-tailed Manakin (Chiroxiphia lanceolata), a tropical passerine. Condor Ornithol Appl 121:duy022

    Google Scholar 

  • Kiere LM, Drummond H (2016) Female infidelity is constrained by El Niño conditions in a long-lived bird. J Anim Ecol 85:960–972

    Article  PubMed  Google Scholar 

  • Klein SA, Soden BJ, Lau NC (1999) Remote sea surface temperature variations during ENSO: evidence for a tropical atmospheric bridge. J Clim 12:917–932

    Article  Google Scholar 

  • Larsen K, Petersen JH, Budtz-jørgensen E, Endahl L (2000) Interpreting parameters in the logistic regression model with random effects. Biometrics 56:909–914

    Article  CAS  PubMed  Google Scholar 

  • Lefcheck JS (2016) piecewiseSEM: piecewise structural equation modeling in R for ecolgoy, evolution, and systematics. Methods Ecol Evol 7:573–579

    Article  Google Scholar 

  • Letnic M, Tamayo B, Dickman CR (2005) The responses of mammals to La Niña (El Niño Southern Oscillation)—associated rainfall, predation, and wildfire in Central Australia. J Mammal 86:689–703

    Article  Google Scholar 

  • Lindström J (1999) Early development and fitness in birds and mammals. Trends Ecol Evol 14:343–348

    Article  PubMed  Google Scholar 

  • Madden RA, Julian PR (1972) Description of global-scale circulation cells in the tropics with a 40–50 day period. J Atmos Sci 29:1109–1123

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Martin TE (2015) Age-related mortality explains life history strategies of tropical and temperate songbirds. Science 349:966–970

    Article  CAS  PubMed  Google Scholar 

  • Martin TE, Lloyd P, Bosque C, Barton DC, Biancucci AL, Cheng YR, Ton R (2011) Growth rate variation among passerine species in tropical and temperate sites: an antagonistic interaction between parental food provisioning and nest predation risk. Evolution 65:1607–1622

    Article  PubMed  Google Scholar 

  • Masello JF, Quillfeldt P (2004) Consequences of La Niña phase of ENSO for the survival and growth of nestling burrowing parrots on the Atlantic coast of South America. Emu 104:337–346

    Article  Google Scholar 

  • Milton K (1996) Effects of bot fly (Alouattamyia baeri) parasitism on a free-ranging howler monkey (Alouatta palliata) population in Panama. J Zool 239:39–63

    Article  Google Scholar 

  • Moermond T, Denslow J (1985) Neotropical avian frugivores: patterns of behavior, morphology, and nutrition, with consequences for fruit selection. Ornithol Monogr 36:865–897

    Article  Google Scholar 

  • Monaghan P (2008) Early growth conditions, phenotypic development and environmental change. Philos Trans R Soc B Biol Sci 363:1635–1645

    Article  Google Scholar 

  • Montgomery DC, Peck EA (1992) Introduction to linear regression analysis. Wiley, New York, NY

    Google Scholar 

  • Moran MD (2003) Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100:403–405

    Article  Google Scholar 

  • Morton E (1973) On the evolutionary advantages and disadvantages of fruit eating in tropical birds. Am Nat 107:8–22

    Article  Google Scholar 

  • Nakagawa S (2004) A farewell to Bonferroni: the problems of low statistical power and publication bias. Behav Ecol 15:1044–1045

    Article  Google Scholar 

  • Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142

    Article  Google Scholar 

  • Nakagawa S, Johnson PCD, Schielzeth H (2017) The Coefficient of determination R2 and intra-class correlation coefficient from generalized linear mixed-effects models revisited and expanded. J R Soc Interface 14:20170213

    Article  PubMed  PubMed Central  Google Scholar 

  • Namias J, Cayan DR (1981) Large-scale air–sea interactions and short-period climatic fluctuatioins. Science 214:869–876

    Article  CAS  PubMed  Google Scholar 

  • Nederhof E, Schmidt MV (2012) Mismatch or cumulative stress: toward an integrated hypothesis of programming effects. Physiol Behav 106:691–700

    Article  CAS  PubMed  Google Scholar 

  • Nevoux M, Weimerskirch H, Barbraud C (2010) Long- and short-term influence of environment on recruitment in a species with highly delayed maturity. Oecologia 162:383–392

    Article  PubMed  Google Scholar 

  • Olah G, Vigo G, Ortiz L, Rozsa L, Brightsmith DJ (2013) Philornis sp. bot fly larvae in free living scarlet macaw nestlings and a new technique for their extraction. Vet Parasitol 196:245–249

    Article  PubMed  Google Scholar 

  • Oro N, Torres R, Rodríguez C, Drummond H (2010) Climatic influence on demographic parameters of a tropical seabird varies with age and sex. Ecology 91:1205–1214

    Article  PubMed  Google Scholar 

  • Paxton KL, Cohen EB, Paxton EH et al (2014) El Niño-Southern Oscillation is linked to decreased energetic condition in long-distance migrants. PLoS One 9:e95383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2018) nlme: linear and nonlinear mixed models. R package 3.1-137. https://CRAN.R-project.org/package=nlme. Accessed 1 Aug 2018

  • Plentovich S, Hebshi A, Conant S (2009) Detrimental effects of two widespread invasive ant species on weight and survival of colonial nesting seabirds in the Hawaiian Islands. Biol Invasions 11:289–298

    Article  Google Scholar 

  • Quillfeldt P, Strange IJ, Masello JF (2007) Sea surface temperatures and behavioural buffering capacity in thin-billed prions Pachyptila belcheri: breeding success, provisioning and chick begging. J Avian Biol 38:298–308

    Article  Google Scholar 

  • R Core Team (2018) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. https://www.R-project.org/. Accessed 1 Aug 2018

  • Remeš V, Martin TE (2002) Environmental influences on the evolution of growth and developmental rates in passerines. Evolution 56:2505–2518

    Article  PubMed  Google Scholar 

  • Ricklefs RE (1968) Patterns of growth in birds. Ibis 110:419–451

    Article  Google Scholar 

  • Ropelewski CF, Halpert MS (1987) Global and regional scale precipitation patterns associated with the El Niño/Southern Oscillation. Mon Weather Rev 115:1606–1626

    Article  Google Scholar 

  • Ropelewski CF, Halpert MS, Ropelewski CF, Halpert MS (1989) Precipitation patterns associated with the high index phase of the Southern Oscillation. J Clim 2:268–284

    Article  Google Scholar 

  • Schoech SJ, Rensel M, Heiss R (2011) Short-and long-term effects of developmental corticosterone exposure on avian physiology, behavioral phenotype, cognition, and fitness: a review. Curr Zool 57:514–530

    Article  CAS  Google Scholar 

  • Schreiber EA (1994) El Niño-Southern Oscillation effects on provisioning and growth in red-tailed tropicbirds. Colon Waterbirds 17:105–119

    Article  Google Scholar 

  • Shipley B (2000) A new inferential test for path models based on directed acyclic graphs. Struct Equ Model 7:206–218

    Article  Google Scholar 

  • Shipley B (2009) Confirmatory path analysis in a generalized multilevel context. Ecology 90:363–368

    Article  PubMed  Google Scholar 

  • Shipley B (2013) The AIC model selection method applied to path analytic models compared using a d-separation test. Ecology 94:560–564

    Article  PubMed  Google Scholar 

  • Smith RN, Cain SL, Anderson SH et al (1998) Blackfly-induced mortality of nestling red-tailed hawks. Auk 115:368–375

    Article  Google Scholar 

  • Snyder NF, Ogden JC, Bittner JD, Grau GA (1984) Larval dermestid beetles feeding on nestling snail kites, wood storks, and great blue herons. Condor 86:170–174

    Article  Google Scholar 

  • Stenseth NC, Mysterud A, Ottersen G et al (2002) Ecological effects of climate fluctuations. Science 297:1292–1296

    Article  CAS  PubMed  Google Scholar 

  • Stenseth NC, Ottersen G, Hurrell JW et al (2003) Studying climate effects on ecology through the use of climate indices: the North Atlantic Oscillation, El Nino Southern Oscillation and beyond. Proc R Soc B Biol Sci 270:2087–2096

    Article  Google Scholar 

  • Stutchbury BE, Morton E (2001) Behavioral ecology of tropical birds. Academic Press, London

    Google Scholar 

  • Trenberth KE (1997) The definition of El Niño. Bull Am Meteorol Soc 78:2771–2777

    Article  Google Scholar 

  • Tschirren B, Rutstein AN, Postma E, Mariette M, Griffith SC (2009) Short- and long-term consequences of early developmental conditions: a case study on wild and domesticated zebra finches. J Evol Biol 22:387–395

    Article  CAS  PubMed  Google Scholar 

  • van Riper IIIC, van Riper S, Hansen W (2002) Epizootiology and effect of avian pox on Hawaiian forest birds. Auk 119:929–942

    Article  Google Scholar 

  • Velarde E, Ezcurra E, Cisneros-Mata MA, Lavín MF (2004) Seabird ecology, El Niño anomalies, and prediction of sardine fisheries in the Gulf of California. Ecol Appl 14:607–615

    Article  Google Scholar 

  • Verhulst S, Hilsson J-Å (2008) The timing of birds’ breeding seasons: a review of experiments that manipulated timing of breeding. Philos Trans R Soc B Biol Sci 363:399–410

    Article  Google Scholar 

  • Wingfield JC, Ramos-Fernandez G, Nuñez-De La Mora A, Drummond H (1999) The effects of an “El Nino” southern oscillation event on reproduction in male and female blue-footed boobies, Sula nebouxii. Gen Comp Endocrinol 114:163–172

    Article  CAS  PubMed  Google Scholar 

  • Wingfield JC, Hau M, Boersma PD et al (2018) Effects of El Niño and La Niña Southern Oscillation events on the adrenocortical responses to stress in birds of the Galapagos Islands. Gen Comp Endocrinol 259:20–33

    Article  CAS  PubMed  Google Scholar 

  • Winterfield RW, Fadly AM, Bickford A (1972) Infectivity and distribution of infectious bursal disease virus in the chicken. Persistence of the virus and lesions. Avian Dis 16:622–632

    Article  CAS  PubMed  Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Book  Google Scholar 

  • Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14

    Article  Google Scholar 

Download references

Acknowledgements

We thank the many technicians that assisted in data collection in the field. In particular, C. Vanderbilt, E. Schunke, S. Lantz, and P. Rivers contributed to multiple years of nest records and provided invaluable assistance that made this project possible. Field site access was granted by F. Koehler and the residents of Isla Boca Brava. Research permits were attained with the assistance of the staff and scientists of Autoridad Nacional del Ambiente (Ministerio de Ambiente), República de Panamá and the Museo de Vertebrados de la Universidad de Panamá. We thank Dr. Adam Smith for his advice on statistical analysis, and two anonymous reviewers for their comments and suggestions. Data relevant to this project were collected with support from National Science Foundation (NSF) Grants 0843334 and 1453408 (CAREER) awarded to E.H.D., the Florida State University, and the Max Planck Institute for Ornithology.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Florida State University, Tallahassee, FL, 32306, USA

    Blake Carlton Jones & Emily H. DuVal

Authors
  1. Blake Carlton Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Emily H. DuVal
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

BCJ planned the study. BCJ and EHD collected data, BCJ performed the statistical analysis, BCJ and EHD wrote the manuscript.

Corresponding author

Correspondence to Blake Carlton Jones.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 149 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jones, B.C., DuVal, E.H. Direct and indirect effects of the El Niño Southern Oscillation on development and survival of young of a tropical passerine. Oecologia 190, 485–496 (2019). https://doi.org/10.1007/s00442-019-04418-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-019-04418-9

Keywords

Search

Navigation