Open Access
1 February 2013 Parental Behavior Controls Incubation Period and Asynchrony of Hatching in Magellanic Penguins: Reply to Demongin, Poisbleau and Eens (2013)
Ginger A. Rebstock, P. Dee Boersma
Author Affiliations +

We defined incubation period as the time from the laying of an egg to its hatching (Rebstock and Boersma 2011) because this full period is ecologically important and matters to both parents' and offspring's fitness. Birds have many patterns of incubation onset and various degrees of egg neglect following onset of incubation. Onset of incubation is difficult to measure in the field and even if known, ignoring the period before onset of incubation misses many of the selective forces acting on incubation patterns and periods.

Demongin and colleagues (2013) disagreed with our definition of incubation period (Rebstock and Boersma 2011) as “the time from the laying of an egg to its hatching” (see also Welty 1962), preferring the more common definition of “the period from the onset of incubation of an egg to its hatching.” Both definitions describe periods that can be highly variable within a species (Boersma and Wheelwright 1979, Frere et al. 1992, Hipfner et al. 2001) and may vary between eggs in a clutch (Greenlaw and Miller 1983, Boonstra et al. 2010, Rebstock and Boersma 2011). The time from when the egg was laid to when it hatches is ecologically important and matters to both parents' and offspring's fitness because of risks of pre dation at the nest (Stoleson and Beissinger 2001) and other costs (Ricklefs 1993). Birds have many patterns of incubation onset (Wang and Beissinger 2011) and various degrees of egg neglect following onset of incubation (e.g., Boersma and Wheelwright 1979, Boersma 1982, Nuechterlein and Buitron 2002, Marin 2008). The onset of incubation is harder to determine than when each egg is laid, and the minimum temperature at which development begins is often unknown. We argue how the eggs are treated is important. As our study showed, parental incubation behavior, not an intrinsic difference between the eggs, controlled the incubation period and the asynchrony of hatching of eggs of the Magellanic Penguin (Spheniscus magellanicus).

Defining the incubation period as the time between the laying and hatching of the last egg in a clutch misses the ecological and physiological importance of the variation in the time the eggs spend in the nest. How long eggs remain in the nest, regardless of whether they are incubated, affects parents and eggs. Incubation is energetically costly and reduces foraging time (Dobbs and Martin 1998, Cooper et al. 2005, Carey 2011, Galván and Sanz 2011). Female Magellanic Penguins stay on (or next to) the nest fasting from egg laying until relieved by the mate, which can be up to 3 weeks (Boersma et al. 1990). Eggs are at risk of predation every day they are in the nest (Bosque and Bosque 1995, Walls et al. 2011). A long period before the onset of incubation increases the eggs' risk of predation. In many species the parents are also at risk of pre dation while incubating (Martin 2002; Cervencl et al. 2011). A prolonged egg period increases the breeding season, a disadvantage to species with long breeding seasons and short windows of appropriate weather and food availability (Hodum 2002, Creuwels et al. 2008). Eggs may lose viability prior to the beginning of effective incubation, especially if ambient temperatures are high (Beissinger et al. 2005). Longer incubation periods associated with reduced egg temperatures may result in smaller chicks and disfavor their growth and survival (Boersma and Wheelwright 1979, Olson et al. 2006, Ardia et al. 2010).

Patterns of incubation onset vary widely by species. Eggs are warmed to full incubation temperature before clutch completion in some species (Stoleson and Beissinger 2001, Ruiz-deCastañeda et al. 2012). For example, the female may incubate the eggs at night before clutch completion, but may not incubate steadily during the day until the clutch is complete (Haftorn 1988, Wang and Weathers 2009). In other species, such as the Yellow-eyed Penguin (Megadyptes antipodes) and Black-legged Kittiwake (Rissa tridactyla), partial incubation may persist long after clutch completion (Wang and Beissinger 2011). We showed that the daily mean temperature of Magellanic Penguin eggs increases steadily for about the first 18 days after laying, at least 2 weeks after clutch completion. A gradual increase in egg temperature is common among penguins (Burger and Williams 1979, St. Clair 1992, de León et al. 2001, Massaro et al. 2006).

Egg neglect or intermittent incubation is common in tubenose seabirds (Procellariiformes), and exposure to low temperatures after the egg has reached effective incubation temperatures does not prevent hatching but lengthens the incubation period (Boersma 1982, Carey 2011). In the Fork-tailed Storm-Petrel (Oceanodroma furcata) eggs must be warm for 37 days but, because of egg neglect, may take up to 68 days to hatch (Boersma and Wheelwright 1979). Egg neglect is also found in other groups of birds, such as hummingbirds (Webb 1987), alcids (Sealy 1984), and swifts (Marín 2008). Throughout incubation of Magellanic Penguin eggs, large temporary temperature drops are common, as our paper showed.

Onset of incubation is nearly impossible to determine in the field for four reasons. (1) Embryonic growth and development is difficult to measure in the field. (2) The temperature required for development is usually unknown. There is not a single “physiological zero” temperature at which no development occurs for all species or even all ages of embryos within a species (Webb 1987, Decuypere and Michels 1992). Embryogenesis starts at fertilization, and the developmental stage of the embryo at egg laying varies (Decuypere and Michels 1992). The assumption is often made that 24–27 °C is the minimum temperature required for development (Beissinger et al. 2005), and lower temperatures are seldom tested. In eggs of the Adélie Penguin (Pygoscelis adeliae), Weinrich and Baker (1978) found that some development occurred at 26° C, the lowest temperature they tested. (3) During active incubation, an egg's temperature decreases from top (brood patch) to bottom (nest), making it difficult to determine the temperature experienced by the embryo (Boersma 1982). (4) Patterns of incubation onset vary by species (Wang and Beissinger 2011).

Our point is that parental behavior controlled the dates and asynchrony of hatching of Magellanic Penguin eggs, as it does in many species (Martin et al. 2007). First eggs spent more time in the nest than second eggs, which matters. Parental behavior, not intrinsic differences between the eggs, causes this discrepancy. The appropriate definition depends on the question being asked. Arguing over definitions detracts from the point and obscures the ecological importance and fitness consequences of the time the egg spends in the nest.



D. R. Ardia , J. H. Pérez , and E. D. Clotfelter . 2010. Experimental cooling during incubation leads to reduced innate immunity and body condition in nestling Tree Swallows. Proceedings of the Royal Society B 277:1881–1888. Google Scholar


S. R. Beissinger , M. I. Cook , and W. J. Arendt . 2005. The shelf life of bird eggs: testing egg viability using a tropical climate gradient. Ecology 86:2164–2175. Google Scholar


P. D. Boersma , and N. T. Wheelwright . 1979. Egg neglect in the Procellariiformes: reproductive adaptations in the Fork-tailed Storm Petrel. Condor 81:157–165. Google Scholar


P. D. Boersma 1982. Why some birds take so long to hatch. American Naturalist 120:733–750. Google Scholar


P. D. Boersma , D. L. Stokes , and P. M. Yorio . 1990. Reproductive variability and historical change of Magellanic Penguins (Spheniscus magellanicus) at Punta Tombo, Argentina, p. 15–43. In L. Davis and J. Darby [eds.] , Penguin biology. Academic Press, San Diego. Google Scholar


T. A. Boonstra , M. E. Clark , and W. L. Reed . 2010. Position in the sequence of laying, embryonic metabolic rate, and consequences for hatching synchrony and offspring survival in Canada Geese. Condor 112:304–313. Google Scholar


C. Bosque , and M. T. Bosque . 1995. Nest predation as a selective factor in the evolution of development rates in altricial birds. The American Naturalist 145:234–260. Google Scholar


A. E. Burger , and A. J. Williams . 1979. Egg temperatures of the Rockhopper Penguin and some other penguins. Auk 96:100–105. Google Scholar


M. J. Carey 2011. Incubation routine, duration of foraging trips and regulation of body mass in Short-tailed Shearwaters (Ardenna tenuirostris). Emu 111:166–171. Google Scholar


A. Cervencl , W. Esser , M. Maier , N. Oberdiek , S. Thyen , A. Wellbrock , and K.-M. Exo . 2011. Can differences in incubation patterns of Common Redshanks Tringa totanus be explained by variations in predation risk? Journal of Ornithology 152:1033–1043. Google Scholar


C. B. Cooper , W. M. Hochachka , G. Butcher , and A. A. Dhondt . 2005. Seasonal and latitudinal trends in clutch size: thermal constraints during laying and incubation. Ecology 86:2018–2031. Google Scholar


J. C. S. Creuwels , J. A. Van Franeker , S. J. Doust , A. Beinssen , B. Harding , and O. Hentschel . 2008. Breeding strategies of Antarctic Petrels Thalassoica antarctica and Southern Fulmars Fulmarus glacialoides in the high Antarctic and implications for reproductive success. Ibis 150:160–171. Google Scholar


A. De León , G. Soave , V. Ferretti , and J. Moreno . 2001. Factors that affect hatching asynchrony in the Chinstrap Penguin (Pygoscelis antarctica). Polar Biology 24:338–342. Google Scholar


E. Decuypere , and H. Michels . 1992. Incubation temperature as a management tool: a review. World's Poultry Science Journal 48:28–38. Google Scholar


L. Demongin , M. Poisbleau , and M. Eens . 2013. Parental behavior controls asynchronous hatching, but not incubation period, in the Magellanic Penguin: a commentary on Rebstock and Boersma (2011). Condor 115:1–4. Google Scholar


R. C. Dobbs , and T. E. Martin . 1998. Variation in foraging behavior among nesting stages of female Red-faced Warblers. Condor 100:741–745. Google Scholar


E. Frere , P. Gandini , and P. D. Boersma . 1992. Effects of nest type and location on reproductive success of the Magellanic Penguin Spheniscus magellanicus. Marine Ornithology 20:1–6. Google Scholar


I. Galván , and J. J. Sanz . 2011. Mate-feeding has evolved as a compensatory energetic strategy that affects breeding success in birds. Behavioral Ecology 22:1088–1095. Google Scholar


J. S. Greenlaw , and R. F. Miller . 1983. Calculating incubation periods of species that sometimes neglect their last eggs: the case of the Sora. Wilson Bulletin 95:459–461. Google Scholar


S. Haftorn 1988. Incubating female passerines do not let the egg temperature fall below the ‘physiological zero temperature’ during their absences from the nest. Ornis Scandinavica 19:97–110. Google Scholar


J. M. Hipfner , A. J. Gaston , D. L. Martin , and I. L. Jones . 2001. Seasonal declines in incubation periods of Brünnich's Guillemots Uria lomvia: testing proximate causes. Ibis 143:92–98. Google Scholar


P. J. Hodum 2002. Breeding biology of high-latitude antarctic fulmarine petrels (Procellariidae). Journal of Zoology 256:139–149. Google Scholar


M. Marín 2008. Intermittent incubation in two neotropical swifts: an adaptation to life in the aerial environment? Ornitología Neotropical 19:391–402. Google Scholar


T. E. Martin 2002. A new view of avian life-history evolution tested on an incubation paradox. Proceedings of the Royal Society of London B 269:309–316. Google Scholar


T. E. Martin , S. K. Auer , R. D. Bassar , A. M. Niklison , and P. Lloyd . 2007. Geographic variation in avian incubation periods and parental influences on embryonic temperature. Evolution 61:2558–2569. Google Scholar


M. Massaro , L. S. Davis , and R. S. Davidson . 2006. Plasticity of brood patch development and its influence on incubation periods in the Yellow-eyed Penguin Megadyptes antipodes: an experimental approach. Journal of Avian Biology 37:497–506. Google Scholar


G. L. Nuechterlein , and D. Buitron . 2002. Nocturnal egg neglect and prolonged incubation in the Red-necked Grebe. Waterbirds 25:485–491. Google Scholar


C. R. Olson , C. M. Vleck , and D. Vleck . 2006. Periodic cooling of bird eggs reduces embryonic growth efficiency. Physiological and Biochemical Zoology 79:927–936. Google Scholar


G. A. Rebstock , and P. D. Boersma . 2011. Parental behavior controls incubation period and asynchrony of hatching in Magellanic Penguins. Condor 113:316–325. Google Scholar


R. E. Ricklefs 1993. Sibling competition, hatching asynchrony, incubation period, and lifespan in altricial birds, p. 199–276. In D. M. Power [ed.], Current Ornithology. Plenum Press, New York. Google Scholar


R. Ruiz-De-Castaneda , A. I. Vela , E. Lobato , V. Briones , and J. Moreno . 2012. Early onset of incubation and eggshell bacterial loads in a temperate-zone cavity-nesting passerine. Condor 114:203–211. Google Scholar


S. G. Sealy 1984. Interruptions extend incubation by Ancient Murrelets, Crested Auklets, and Least Auklets. Murrelet 65:53–56. Google Scholar


C. C. St. Clair 1992. Incubation behaviour, brood patch formation and obligate brood reduction in Fiordland crested penguins. Behavioral Ecology and Sociobiology 31:409–416. Google Scholar


S. H. Stoleson , and S. R. Beissinger . 2001. Does risk of nest failure or adult predation influence hatching patterns of the Greenrumped Parrotlet? Condor 103:85–97. Google Scholar


J. G. Walls , G. R. Hepp , and L. G. Eckhardt . 2011. Effects of incubation delay on viability and microbial growth of Wood Duck (Aix sponsa) eggs. Auk 128:663–670. Google Scholar


J. M. Wang , and W. W. Weathers . 2009. Egg laying, egg temperature, attentiveness, and incubation in the Western Bluebird. Wilson Journal of Ornithology 121:512–520. Google Scholar


J. M. Wang , and S. R. Beissinger . 2011. Partial incubation in birds: its occurrence, function, and quantification. Auk 128:454–466. Google Scholar


D. R. Webb 1987. Thermal tolerance of avian embryos: a review. Condor 89:874–898. Google Scholar


J. A. Weinrich , and J. R. Baker . 1978. Adélie Penguin (Pygoscelis adeliae) embryonic development at different temperatures. Auk 95:569–576. Google Scholar


J. C. Welty 1962. The life of birds. Saunders, Philadelphia. Google Scholar
© 2013 by The Cooper Ornithological Society. All rights reserved. Please direct all requests for permission to photocopy or reproduce article content through the University of California Press's Rights and Permissions website,
Ginger A. Rebstock and P. Dee Boersma "Parental Behavior Controls Incubation Period and Asynchrony of Hatching in Magellanic Penguins: Reply to Demongin, Poisbleau and Eens (2013)," The Condor 115(1), 5-7, (1 February 2013).
Received: 9 July 2012; Accepted: 1 July 2012; Published: 1 February 2013
incubation costs
incubation period
onset of incubation
parental behavior.
Back to Top