skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Laying sequence interacts with incubation temperature to influence rate of embryonic development and hatching synchrony in a precocial bird

Abstract

Incubation starts during egg laying for many bird species and causes developmental asynchrony within clutches. Faster development of late-laid eggs can help reduce developmental differences and synchronize hatching, which is important for precocial species whose young must leave the nest soon after hatching. In this study, we examined the effect of egg laying sequence on length of the incubation period in Wood Ducks (Aix sponsa). Because incubation temperature strongly influences embryonic development rates, we tested the interactive effects of laying sequence and incubation temperature on the ability of late-laid eggs to accelerate development and synchronize hatching. We also examined the potential cost of faster development on duckling body condition. Fresh eggs were collected and incubated at three biologically relevant temperatures (Low: 34.9°C, Medium: 35.8°C, and High: 37.6°C), and egg laying sequences from 1 to 12 were used. Length of the incubation period declined linearly as laying sequence advanced, but the relationship was strongest at medium temperatures followed by low temperatures and high temperatures. There was little support for including fresh egg mass in models of incubation period. Estimated differences in length of the incubation period between eggs 1 and 12 were 2.7 d, 1.2 d, and 0.7 d at medium,more » low and high temperatures, respectively. Only at intermediate incubation temperatures did development rates of late-laid eggs increase sufficiently to completely compensate for natural levels of developmental asynchrony that have been reported in Wood Duck clutches at the start of full incubation. Body condition of ducklings was strongly affected by fresh egg mass and incubation temperature but declined only slightly as laying sequence progressed. Our findings show that laying sequence and incubation temperature play important roles in helping to shape embryo development and hatching synchrony in a precocial bird.« less

Authors:
ORCiD logo; ;
Publication Date:
Research Org.:
Univ. of Georgia, Athens, GA (United States)
Sponsoring Org.:
USDOE Office of Environmental Management (EM)
OSTI Identifier:
1418194
Alternate Identifier(s):
OSTI ID: 1506647
Grant/Contract Number:  
FC09-07SR22506
Resource Type:
Published Article
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Name: PLoS ONE Journal Volume: 13 Journal Issue: 1; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES

Citation Formats

Hepp, Gary R., Kennamer, Robert A., and Yildirim, ed., Arda. Laying sequence interacts with incubation temperature to influence rate of embryonic development and hatching synchrony in a precocial bird. United States: N. p., 2018. Web. doi:10.1371/journal.pone.0191832.
Hepp, Gary R., Kennamer, Robert A., & Yildirim, ed., Arda. Laying sequence interacts with incubation temperature to influence rate of embryonic development and hatching synchrony in a precocial bird. United States. doi:10.1371/journal.pone.0191832.
Hepp, Gary R., Kennamer, Robert A., and Yildirim, ed., Arda. Fri . "Laying sequence interacts with incubation temperature to influence rate of embryonic development and hatching synchrony in a precocial bird". United States. doi:10.1371/journal.pone.0191832.
@article{osti_1418194,
title = {Laying sequence interacts with incubation temperature to influence rate of embryonic development and hatching synchrony in a precocial bird},
author = {Hepp, Gary R. and Kennamer, Robert A. and Yildirim, ed., Arda},
abstractNote = {Incubation starts during egg laying for many bird species and causes developmental asynchrony within clutches. Faster development of late-laid eggs can help reduce developmental differences and synchronize hatching, which is important for precocial species whose young must leave the nest soon after hatching. In this study, we examined the effect of egg laying sequence on length of the incubation period in Wood Ducks (Aix sponsa). Because incubation temperature strongly influences embryonic development rates, we tested the interactive effects of laying sequence and incubation temperature on the ability of late-laid eggs to accelerate development and synchronize hatching. We also examined the potential cost of faster development on duckling body condition. Fresh eggs were collected and incubated at three biologically relevant temperatures (Low: 34.9°C, Medium: 35.8°C, and High: 37.6°C), and egg laying sequences from 1 to 12 were used. Length of the incubation period declined linearly as laying sequence advanced, but the relationship was strongest at medium temperatures followed by low temperatures and high temperatures. There was little support for including fresh egg mass in models of incubation period. Estimated differences in length of the incubation period between eggs 1 and 12 were 2.7 d, 1.2 d, and 0.7 d at medium, low and high temperatures, respectively. Only at intermediate incubation temperatures did development rates of late-laid eggs increase sufficiently to completely compensate for natural levels of developmental asynchrony that have been reported in Wood Duck clutches at the start of full incubation. Body condition of ducklings was strongly affected by fresh egg mass and incubation temperature but declined only slightly as laying sequence progressed. Our findings show that laying sequence and incubation temperature play important roles in helping to shape embryo development and hatching synchrony in a precocial bird.},
doi = {10.1371/journal.pone.0191832},
journal = {PLoS ONE},
number = 1,
volume = 13,
place = {United States},
year = {2018},
month = {1}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.1371/journal.pone.0191832

Save / Share:

Works referenced in this record:

Reproductive Implications of Egg-Size Variation in the Black Brant
journal, October 1992

  • Flint, Paul L.; Sedinger, James S.
  • The Auk, Vol. 109, Issue 4
  • DOI: 10.2307/4088164

The Shelf life of bird Eggs: Testing egg Viability Using a Tropical Climate Gradient
journal, August 2005

  • Beissinger, Steven R.; Cook, Mark I.; Arendt, Wayne J.
  • Ecology, Vol. 86, Issue 8
  • DOI: 10.1890/04-1624

Geographic Variation in Nests of Yellow Warblers Breeding in Churchill, Manitoba, and Elgin, Ontario
journal, August 2010


Periodic Cooling of Bird Eggs Reduces Embryonic Growth Efficiency
journal, September 2006

  • Olson, Christopher R.; Vleck, Carol M.; Vleck, David
  • Physiological and Biochemical Zoology, Vol. 79, Issue 5
  • DOI: 10.1086/506003

Variation in the onset of incubation and its influence on avian hatching success and asynchrony
journal, September 2009


Social facilitation of hatching in the bobwhite quail
journal, October 1964


Thermal Tolerance of Avian Embryos: A Review
journal, November 1987


Egg viability as a constraint on hatching synchrony at high ambient temperatures
journal, September 1999


Long-term consequences of high incubation temperature in a wild bird population
journal, April 2016


Nest box orientation affects internal temperature and nest site selection by Tree Swallows
journal, June 2006


Embryo development and ageing in birds and mammals
journal, April 2006

  • Ricklefs, Robert E.
  • Proceedings of the Royal Society B: Biological Sciences, Vol. 273, Issue 1597
  • DOI: 10.1098/rspb.2006.3544

Regulation of development time and hatch synchronization in Black Brant (Branta bernicla nigricans)
journal, June 2004


Selection for Rapid Embryo Development Correlates with Embryo Exposure to Maternal Androgens among Passerine Birds
journal, August 2007

  • Schwabl, Hubert; Palacios, Maria G.; Martin, Thomas E.
  • The American Naturalist, Vol. 170, Issue 2
  • DOI: 10.1086/519397

Uninformative Parameters and Model Selection Using Akaike's Information Criterion
journal, August 2010


Local variation in weather conditions influences incubation behavior and temperature in a passerine bird
journal, March 2015

  • Coe, Brittney H.; Beck, Michelle L.; Chin, Stephanie Y.
  • Journal of Avian Biology, Vol. 46, Issue 4
  • DOI: 10.1111/jav.00581

High atmospheric temperatures and ‘ambient incubation’ drive embryonic development and lead to earlier hatching in a passerine bird
journal, February 2016

  • Griffith, Simon C.; Mainwaring, Mark C.; Sorato, Enrico
  • Royal Society Open Science, Vol. 3, Issue 2
  • DOI: 10.1098/rsos.150371

Conclusions beyond support: overconfident estimates in mixed models
journal, November 2008


Pre-fledgling oxidative damage predicts recruitment in a long-lived bird
journal, August 2011

  • Noguera, José Carlos; Kim, Sin-Yeon; Velando, Alberto
  • Biology Letters, Vol. 8, Issue 1
  • DOI: 10.1098/rsbl.2011.0756

Embryonic Developmental Patterns and Energy Expenditure Are Affected by Incubation Temperature in Wood Ducks ( Aix sponsa )
journal, September 2011

  • DuRant, S. E.; Hopkins, W. A.; Hepp, G. R.
  • Physiological and Biochemical Zoology, Vol. 84, Issue 5
  • DOI: 10.1086/661749

Correlated evolution of maternally derived yolk testosterone and early developmental traits in passerine birds
journal, July 2005


Composition of Wood Duck Eggs in Relation to Egg Size, Laying Sequence, and Skipped Days of Laying
journal, July 1997

  • Kennamer, Robert A.; Colwell, Sheila V.
  • The Auk, Vol. 114, Issue 3
  • DOI: 10.2307/4089248

Early Onset of Incubation by wood Ducks
journal, January 2004

  • Hepp, Gary R.
  • The Condor, Vol. 106, Issue 1
  • DOI: 10.1650/7318

Hatching Asynchrony, Brood Reduction, and food Limitation in a Neotropical Parrot
journal, May 1997


Maternal androgens in black-headed gull ( Larus ridibundus ) eggs: consequences for chick development
journal, April 2001

  • Eising, C. M.; Eikenaar, C.; Schwabl, H.
  • Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 268, Issue 1469
  • DOI: 10.1098/rspb.2001.1594

Laying-Stage nest Attendance and Onset of Incubation in Prairie Nesting Ducks
journal, January 2004


Factors affecting egg viability and incubation time in prairie dabbling ducks
journal, June 1993

  • Arnold, Todd W.
  • Canadian Journal of Zoology, Vol. 71, Issue 6
  • DOI: 10.1139/z93-156

Egg size matching by an intraspecific brood parasite
journal, January 2011


Experimental cooling during incubation leads to reduced innate immunity and body condition in nestling tree swallows
journal, February 2010

  • Ardia, Daniel R.; Pérez, Jonathan H.; Clotfelter, Ethan D.
  • Proceedings of the Royal Society B: Biological Sciences, Vol. 277, Issue 1689
  • DOI: 10.1098/rspb.2009.2138

Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation
journal, January 2009


The effects of nest size and insulation on thermal properties of tree swallow nests
journal, March 2013


Patterns of nest Attendance in Female wood Ducks
journal, January 2000


Effects of incubation delay on viability and microbial growth of Wood Duck ( Aix sponsa ) eggs
journal, October 2011

  • Walls, Johnathan G.; Hepp, Gary R.; Eckhardt, Lori G.
  • The Auk, Vol. 128, Issue 4
  • DOI: 10.1525/auk.2011.11124

Embryonic Development and Nest Attentiveness of Wood Ducks during Egg Laying
journal, August 1990

  • Kennamer, Robert A.; Iv, William F. Harvey; Hepp, Gary R.
  • The Condor, Vol. 92, Issue 3
  • DOI: 10.2307/1368677

Quantifying variable importance in a multimodel inference framework
journal, November 2015


Intrinsic vs. extrinsic influences on life history expression: metabolism and parentally induced temperature influences on embryo development rate
journal, March 2013

  • Martin, Thomas E.; Ton, Riccardo; Niklison, Alina
  • Ecology Letters, Vol. 16, Issue 6
  • DOI: 10.1111/ele.12103

Incubation Temperature Affects Growth and Energy Metabolism in Blue Tit Nestlings
journal, November 2011

  • Nord, Andreas; Nilsson, Jan-Åke
  • The American Naturalist, Vol. 178, Issue 5
  • DOI: 10.1086/662172

Yolk is a source of maternal testosterone for developing birds.
journal, December 1993


Using Artificial Nests to test Importance of Nesting Material and nest Shelter for Incubation Energetics
journal, January 2004


Warm Is Better: Incubation Temperature Influences Apparent Survival and Recruitment of Wood Ducks (Aix sponsa)
journal, October 2012


Increased susceptibility to oxidative damage as a cost of accelerated somatic growth in zebra finches
journal, October 2007


Plasticity in incubation behavior and shading by king rails Rallus elegans in response to temperature
journal, January 2017

  • Clauser, Amanda J.; McRae, Susan B.
  • Journal of Avian Biology, Vol. 48, Issue 4
  • DOI: 10.1111/jav.01056

Incubation temperature influences survival in a small passerine bird
journal, October 2015

  • Berntsen, Henrik H.; Bech, Claus
  • Journal of Avian Biology, Vol. 47, Issue 2
  • DOI: 10.1111/jav.00688

Ecological, evolutionary, and conservation implications of incubation temperature-dependent phenotypes in birds: Incubation temperature and avian offspring phenotype
journal, February 2013

  • DuRant, Sarah E.; Hopkins, William A.; Hepp, Gary R.
  • Biological Reviews, Vol. 88, Issue 2
  • DOI: 10.1111/brv.12015

Egg Viability, Nest Predation, and the Adaptive Significance of Clutch Size in Prairie Ducks
journal, November 1987

  • Arnold, Todd W.; Rohwer, Frank C.; Armstrong, Terry
  • The American Naturalist, Vol. 130, Issue 5
  • DOI: 10.1086/284736

Intraclutch hatch synchronization in the lesser snow goose
journal, June 1983

  • Davies, J. Chris; Cooke, F.
  • Canadian Journal of Zoology, Vol. 61, Issue 6
  • DOI: 10.1139/z83-187

The effects of incubation temperature on the morphology and composition of Australian Brush-turkey (Alectura lathami) chicks
journal, May 2009


Partial Incubation in Birds: Its Occurrence, Function, and Quantification
journal, July 2011


Balancing between costs and benefits of maternal hormone deposition in avian eggs
journal, March 2005

  • Groothuis, Ton G. G.; Eising, Corine M.; Dijkstra, Cor
  • Biology Letters, Vol. 1, Issue 1
  • DOI: 10.1098/rsbl.2004.0233

Elevation impacts the balance between growth and oxidative stress in coal tits
journal, May 2014


Patterns of Nest Attendance in Female Wood Ducks
journal, May 2000