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3 May 2017 The adaptive significance of variation in avian incubation periods
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Abstract

In spite of strong selection by time-dependent mortality on the length of the embryo development (incubation) period, time to hatching varies substantially among species, independently of body size. One view, strongly supported by the work of Thomas Martin and his colleagues, maintains that this variation reflects parental strategies to minimize their own mortality risk at the nest—strategies that influence egg temperature and embryo growth rate. A second, not incompatible, view maintains that variation in the incubation period reflects a trade-off between the growth rate of the embryo and its subsequent quality as a free-living individual. We evaluate several lines of evidence relating nest attendance by adults and the quality of the immune system to the length of the incubation period. Particularly important is the role of sibling competition in selecting for rapid embryo growth and early hatching, and the fact that many species with prolonged incubation periods are raised either as single chicks or in broods with staggered hatching, which predetermines the outcome of sibling competition.

INTRODUCTION

Among species of birds that lay eggs of similar size, the time required for embryo development and hatching varies by a factor of >2 (Rahn and Ar 1974). Part of this variation in the incubation period is related to the degree of development (precocity) of the hatchling, with the self-sufficient (precocial) neonates of such birds as ducks and chickens requiring more time to develop than the dependent (altricial) neonates of songbirds and others (Starck 1993, Starck and Ricklefs 1998). This variation partly reflects the general inverse relationship between rate of growth and functional maturity documented in birds (Ricklefs 1979, Ricklefs et al. 1994). However, even among altricial species that have similar functional capacity at hatching, the log-transformed length of the incubation period for eggs of the same size has a standard deviation of 0.093 log10 units, corresponding to a factor of 1.24; the range between 2 standard deviations on either side of the mean incubation period for a given egg size, which includes ∼95% of the species, represents a factor of 1.53, or a 53% increase of the longer period over the shorter period (Ricklefs 1993). Considering the high mortality rates of eggs caused by predation, weather, and other factors, why some species of birds with similar neonates take longer to hatch their eggs than others requires explanation.

Avian biologists have proposed a range of hypotheses to account for this variation in incubation periods. Certainly, time-dependent mortality—caused by weather and predators—favors more rapid development, all else being equal (Ricklefs 1969, 1984, Remeš and Martin 2002). Møller (2005) suggested that parasites in the nest might have a similar effect. To ensure rapid development, avian embryos must be maintained by the incubating parent within a narrow range of elevated temperatures. This creates a conflict for the parent between incubation of the eggs and self-maintenance. The primary consideration regarding variation in the duration of incubation is the degree to which adults control embryo development time by their incubation behavior; additional variation in development time might also reflect intrinsic growth programs of embryos. Thomas Martin and his colleagues have argued that variation in the incubation period reflects the proportion of time that parents incubate their eggs (Martin 1996, 2002, Martin et al. 2007, 2011, 2013, 2015). Accordingly, low nest attentiveness would represent primarily a strategy to reduce parental exposure to causes of adult mortality at the nest, simply by the parents not being there, what Cresswell (2008) and Lima (1998) have referred to as the nonlethal effects of predation. The time required for embryo development is inversely related to the temperature at which the egg is maintained, which depends on the incubation behavior of the parents.

Alternatively, Ricklefs (1993) suggested that slow embryo growth reflects a developmental strategy associated with increased quality of the neonate and consequently with the individual's potential life span and lifetime reproductive rate. Both considerations—temperature and individual quality—could influence the length of the incubation period. Here, we argue that the weight of evidence favors incubation strategies that reflect a trade-off between the quality of the individual and its rate of development as an embryo. This issue is important—if the incubation period is related to aspects of individual performance that influence life span and reproductive success, understanding how embryo development affects individual quality could reveal crucial trade-offs governing the evolution of life histories.

The Basic Parameters

(1) All the nutrients required by the embryo are provided in the egg at the time it is laid (Romanoff and Romanoff 1949). However, gas exchange occurs throughout incubation, including inflow of oxygen to support metabolism, and outflow of carbon dioxide and water vapor (Rahn and Ar 1974, Rahn et al. 1979, Ar and Rahn 1980, Rahn and Ar 1980). These processes, including retention of sufficient water in the egg over the incubation period, are critical to embryo development and are adjusted by parental behavior and the quality (including porosity) of the eggshell (Rahn et al. 1977).

(2) The length of the embryo growth period determines the energy efficiency of growth (Romanoff 1960, Ricklefs 1974, 1996) and, therefore, the nutrients that must be provisioned initially to produce a chick. In general, slower growth requires more energy because the embryo's metabolism must be maintained for a longer period. Balancing this, slow growth requires a somewhat lower rate of energy consumption, and thus gas exchange—reducing the rate at which water is lost from the egg, although not necessarily the total transpiration over the incubation period (Rahn and Ar 1974).

(3) Embryo growth and development require that the parents warm their eggs. The length of the incubation period is inversely related to egg temperature, as shown by extensive experimentation with artificial incubation (Romanoff 1960, Ricklefs 1987, Deeming and Fergusen 1991, Hepp et al. 2006, Ardia et al. 2009). In some species, both parents incubate the eggs, which they maintain at a high temperature more or less continuously (Skutch 1976, Conway and Martin 2000, Chalfoun and Martin 2007). In other species, only one sex—typically the female—incubates and the eggs go through cycles of heating and cooling corresponding to on and off bouts (Hainsworth and Voss 2002, Martin et al. 2007, 2015).

(4) Species vary in the degree of functional maturity of the neonate (Nice 1962, Starck 1993, Ricklefs and Starck 1998). In general, more mature tissues grow more slowly (Ricklefs et al. 1994, Shea et al. 1995), and chicks with a higher degree of functional maturity at hatching (e.g., precocial species such as ducks and chickens) have longer incubation periods than altricial species such as doves and songbirds.

(5) The length of the incubation period exhibits little genetic variation within populations (e.g., ∼3 hr genetic standard deviation in the European Starling [Sturnus vulgaris]; Ricklefs and Smeraski 1983). Selection on early postnatal growth rate in chickens and quail has had no effect on the length of the incubation period; nor has selection on the incubation period itself (Siegel et al. 1968, Marks 1979). Thus, although it is clear that the incubation period has undergone evolutionary diversification, this seemingly has required very long periods of divergent unidirectional selection on very conservative traits.

(6) Eggs and their contained embryos are exposed to various mortality factors, many of which, including predation and destruction by storms, are time-dependent (Ricklefs 1969), such that continued exposure increases realized mortality. Thus, any extension of the incubation period increases risk to both the eggs and the parents.

(7) Selection on the duration of incubation balances costs and benefits to both embryos and parents because offspring success is a component of adult fitness.

The Issues

(1) Incubation periods vary widely among species of birds. In small passerines, the embryo development period can be as short as 11–12 days, or >20 days. In general, more species exhibit prolonged incubation in the tropics than in temperate climates. Martin and his colleagues (Martin 2002, 2004, Martin et al. 2007, 2013, 2015) have argued that most variation in the length of the incubation period reflects parental strategies to reduce their own exposure to time-dependent mortality at the nest. This reduction in parental attendance comes with associated costs expressed in terms of longer incubation periods and reduced nest survival. Because the contribution of an adult's survival to its own evolutionary fitness (its reproductive value) is greater than the contribution of any particular clutch of eggs, parents should generally favor personal survival over clutch survival when the two come into conflict. The nest is assumed to be a dangerous place for parent birds, and they can enhance their own survival by reducing the time spent on the nest each day, with the consequences that the eggs are maintained at a lower average temperature and embryo development is prolonged. Parent birds of some species might also require more time to obtain food for their own needs, which would leave less time for incubation each day among single-sex incubators. Nest (clutch) mortality rates are higher in the tropics than in temperate regions (Ricklefs 1969, Martin 1995, Martin et al. 2007), though overlap does occur (Robinson et al. 2000). And, as mentioned above, incubation periods of many species (though not all) are, on average, longer in the tropics (Skutch 1976, Ricklefs 1993, Conway and Martin 2000).

(2) Time-dependent mortality of eggs is unavoidable, but predation of adults at the nest site is rare, particularly for open-nesting species whose nest sites afford adequate escape routes (Robinson et al. 2005). For example, among ∼600 nesting attempts of 2 antbird species (Thamnophilidae) in Panama, mortality of adults at nests was observed in only 2 cases (Rompré and Robinson 2008). Another nesting study on a tropical understory antbird also failed to show any adult mortality (Tarwater 2008). Observations on other species, mostly based on video recording at nests, similarly have reported few instances of predation on adults at the nest. For example, video monitoring of 132 nests of Blackcaps (Sylvia atricapilla) in Germany yielded 40 instances of predation by 8 species of predator, with no mention of predation on adults: “When predators approached a nest, adult Blackcaps usually stayed at the nest almost until the predators arrived, leaving at the last second” (Schaefer 2004:172). Similar observations have been reported in multiple studies, including 69 nests of 10 passerine species in grassland habitats, with no mention of adults depredated at the nest, in spite of considerable nest loss (Pietz and Granfors 2000); 142 nests of Black-capped Vireos (Vireo atricapilla), with 59 predator visits and 48 nest depredations, but no adult mortality recorded, “although one incubating female narrowly escaped capture by a snake” (Stake and Cimprich 2003:351); no mention of adult mortality at 52 video-monitored nests of Field Sparrows (Spizella pusilla) and Indigo Buntings (Passerina cyanea) (Thompson et al. 1999); 165 nests of various temperate species monitored with cameras, and with predators identified at 61 of 74 depredated nests, with no mention of adult mortality (Thompson and Burhans 2003); and video monitoring of 182 flycatcher nests and 122 bunting nests in the midwestern United States, recording 144 nest failures but no predation of adult females on the nest (Cox et al. 2014). The general impression from these and similar studies is that parent birds, particularly of open-nesting species, are exquisitely sensitive to the approach of predators to their nests and do not experience undue risk when attending their nests.

Moreover, annual survival of small birds is generally higher, overall, in tropical than in temperate regions (Karr et al. 1990, Ricklefs 1993, Sandercock et al. 2000, Ricklefs et al. 2011), in spite of greater nest mortality rates in the tropics (Ricklefs 1969, Oniki 1979, Skutch 1985), a further indication that adult safety at the nest is not a major contributor to adult survival or to variation in the incubation period. Nest predation rates—although higher, on average, in the tropics—overlap substantially between tropical and temperate locations (Ricklefs 1969, Robinson et al. 2000). Thus, while nest predation undoubtedly exerts a strong influence on avian reproduction, we argue that variation in the length of the incubation period primarily reflects selection on the quality of the neonate, which influences the average life expectancy and lifetime reproductive success of individuals. As in many endeavors, it takes more time to produce a better product.

(3) The rate of embryo growth and development varies little within a species; eggs incubated at the same temperature normally hatch within a few hours (e.g., Ricklefs and Smeraski 1983). In experiments with poultry, the incubation period varies inversely with incubation temperature, up to the maximum temperature tolerance of the embryo. Indeed, temperature is the most significant variable to influence the hatching time of a particular egg (Romanoff 1960, Deeming and Fergusen 1991, Deeming 2002). If this growth rate–egg temperature relationship were to apply to all species of birds, incubating adults would have to reach a compromise between maintaining their eggs at high temperatures (thereby reducing development time) and exposing themselves to the risk of predation at the nest site. Presumably, when adults adjust this trade-off by spending less time on the nest to reduce their own exposure to risk, average egg temperature is reduced, the embryonic development rate slows, the incubation period lengthens, and the exposure of eggs to time-dependent nest mortality increases.

Considering that daily mortality rates are so much lower for adults than for eggs, reducing adult exposure at the cost of increasing egg exposure most likely produces no overall fitness advantage. In Martin et al.'s (2015) analysis, daily nest mortality rate for open-nesting species at his Venezuela site varied between 0.030 and 0.069 (3–7%) per day. Among these species, annual adult mortality rates varied from 0.1 to 0.4, which corresponds to a range of average daily mortality rates between 0.00029 and 0.0014 (i.e. 2 orders of magnitude lower than egg mortality rates), with little evidence of increased adult mortality on the nest. Even considering that eggs can be replaced, parents seemingly would increase their lifetime reproductive success by reducing the embryo development period of their offspring, as long as neonate quality was unaffected. The assumption that embryo fitness is unaffected by lower adult attendance—and, thus, by lower incubation temperatures—is questionable, at least in species in which selection has not favored egg neglect. Recent studies indicate that lower incubation temperatures result in slower nestling growth (Nilsson et al. 2008, DuRant et al. 2013), lower hatchability (Ben-Ezra and Burness 2017), higher nestling metabolism (Ben-Ezra and Burness 2017), lower thermoregulatory performance (DuRant et al. 2013), lower immunocompetence (DuRant et al. 2012), and lower long-term survival (Berntsen and Bech 2016). We argue, instead, that balancing the effects of extrinsic mortality, and independently of temperature effects, embryos are selected to reduce development rate in order to increase neonate quality and extend individual productive life spans as adults.

The Evidence

1. Egg temperature and the length of the incubation period. Resolving the controversy over embryo development rate depends, in part, on the relationship between egg temperature and the length of the incubation period. Experimental work with poultry shows a clear inverse relationship between egg temperature and the duration of incubation (Romanoff 1960, Hepp et al. 2006). The first data available for wild birds were comparative (among species) and nonexperimental. Using published data compiled by J. B. Williams (1996) on egg temperatures of north temperate birds, Martin (2002) reported a significant negative relationship between temperature and incubation period among North American species (r = −0.49, P = 0.018, n = 23; also see Martin et al. 2007). However, in a study on egg temperature and incubation period in New World tropical birds, Tieleman et al. (2004) reanalyzed these data and observed that the full dataset, including European species (and with several typographical errors corrected from the original table), failed to show such a relationship (r [species data] = 0.06, P = 0.73, n = 38). In addition, many of these data were from old sources using different technologies that have produced biased, generally low, egg temperatures. For example, among the measurements in Martin's analysis, those made by Huggins (1941) included an egg temperature for the American Tree Sparrow (Spizelloides arborea) of 30.8°C, whereas that for the closely related Field Sparrow (Spizella pusilla) was 38.1°C; both species have 11-day incubation periods. Furthermore, among the tropical species included in the field study by Tieleman et al. (2004), egg temperature and incubation period were not significantly related, although the sign of the correlation was consistent with the hypothesis that development rate is inversely related to temperature (r [species data] = −0.35, P = 0.22, n = 14; r [phylogenetic independent contrasts] = −0.24, P = 0.42, n = 13).

More recently, Martin et al. (2015) analyzed data from 4 study sites (Arizona, Venezuela, South Africa, and Borneo). The data exhibit a strong negative relationship between average egg temperature and the length of the embryo development period (their figure 3). Over the whole sample, the common logarithm of the incubation period (days) decreased by 0.057 log10 units (SE 0.003), a decrease of −12% per degree Celsius in average egg temperature between 32.5°C and 36.5°C, and a factor of 1.7 over the 4°C range (R2 = 0.82, n = 63 species). Moreover, egg temperature was positively related to both adult and nest mortality rates, which suggests that higher time-dependent mortality selects higher nest attendance and incubation temperature to reduce the incubation period and exposure to agents of nest mortality (their figure 2).

In the context of the present analysis, our data from Panama provide a useful comparison. Martin et al.'s (2015) Venezuelan data are from a research site at 1,400–2,000 m elevation, where ambient air temperatures are as much as 7–10°C cooler than at our site in Panama at 100 m elevation. Previous studies have shown little influence of elevation below 3,000 m on incubation periods in birds (Skutch 1967, Carey et al. 1982, Carey et al. 1990, León-Velarde et al. 1997, León-Velarde and Monge-C. 2004). In Venezuela, the average 24 hr egg temperature measured in 18 passerine species was 34.6°C (SD 0.95) and the average incubation period was 16.0 days (SD 2.3; range: 12.8–19.9 days). In lowland Panama, the average 24 hr egg temperature measured in 13 passerine species—albeit using somewhat different methods—was 36.9°C (SD 0.83) and the average incubation period was 14.9 days (SD 2.2; range: 12.5–19.0 days; Tieleman et al. 2004). Based on Martin et al.'s (2015) within-site regression, the 2.3°C difference in egg temperature between the Venezuela site and our site in Panama would imply a 1.35-fold difference in the incubation periods of birds in the 2 areas, whereas a 1.07-fold difference is observed. Part of the discrepancy might have to do with measurement protocols and the choice of species. Because Martin has not worked at lowland sites in the Neotropics, no direct comparisons are available. However, at our lowland site in Panama, one of the longest incubation periods (18 days) was that of the Spotted Antbird (Hylophylax naevioides), which has biparental incubation, an 88% average 24 hr nest attentiveness, and an average 24 hr egg temperature of 36.2°C. By all accounts, the incubation period of this species should be much shorter.

2. Experimental manipulation of incubation temperatures. In an experiment designed to test the effect of natural variation in parental incubation behavior on rate of embryo development, Martin et al. (2007) switched eggs between nests of species with long and short incubation periods. The results showed that incubation periods were shifted, generally by 1–2 days, in the direction of the foster nest, which suggests a role for the incubation behavior of the parent. However, the shifts were considerably smaller than the difference between the natural incubation periods of the donor and foster species.

In a “common-garden” experiment, Robinson et al. (2008) artificially incubated 50 eggs of the House Wren (Troglodytes aedon), from 2 populations with differing natural incubation periods (12–13 days [temperate, n = 27] vs. 14 days [tropical, n = 23]). When placed under identical conditions, eggs from the 2 populations hatched in relation to their natural incubation periods (13.6 vs. 14.9 days, P < 0.0001), which suggests that the difference in embryo growth rate between the populations was intrinsic. In a more comprehensive experiment, Robinson et al. (2014) incubated the eggs of a variety of Panamanian birds, with natural incubation periods varying between 12 and 19 days, at a constant temperature of 36.5°C and observed no decrease in the hatching times of the species with the longer incubation periods, and 1- to 2-day increases in those species with the shorter incubation periods.

3. Summed brooding time of parents on nests with long and short incubation periods. If absences from nests and resulting low egg temperatures were responsible for the long incubation periods of some birds, one would expect that the adults would benefit from less exposure on the nest over the period required to hatch the eggs. Ricklefs and Brawn (2013) showed that this was not the case for a number of species in Panama, based on automatic recording of the intervals during which parents incubated eggs. In 6 species of lowland, inner-forest flycatchers (Tyrannidae) and antbirds (Thamnophilidae), with natural incubation periods between 17.9 and 23.3 days, the total time that the parents together incubated the eggs varied between 14.2 and 19.5 days. Thus, in tropical species with long incubation periods, parents spent more total time at the nest between laying and hatching the eggs than the overall duration of the incubation periods of many species in the area, which may be as short as 12–14 days (e.g., Clay-colored Thrush [Turdus grayi], Red-throated Ant-Tanager [Habia fuscicauda], and Yellow-green Vireo [Vireo flavoviridis]). Reducing the percentage of time on the nest, to reduce predation risk or increase foraging time, actually increases the total nest attendance time required to hatch the clutch.

Of course, certain times of day or night might be more dangerous at the nest than others, and being away from the nest during such periods might increase adult safety. In one study of forest understory birds in Panama, which used thermistors in the nest to identify the time of clutch predation events, two-thirds of 21 events occurred between 1100 and 1800 hours, and none took place at night (Libsch et al. 2008). Adults of these species incubate continuously through the night, whereas the afternoon period is the low point of adult nest attendance in the daily cycle (Ricklefs and Brawn 2013), but also the warmest part of the day. Nights near the equator are longer than those at higher latitudes during their respective breeding seasons. Because most birds sleep on the nest following the onset of full incubation, one could consider the hours of nighttime darkness as one long on-bout. When this period is considered to offset longer daytime off-bouts in the tropics, the 24 hr constancy of incubating birds exhibits almost no variation with respect to latitude (Álvarez and Barba 2014).

4. Evidence concerning the quality of the hatched chick. Tropical birds typically live longer than temperate birds (Karr et al. 1990, Brawn et al. 1995, Ricklefs 1997, Sandercock et al. 2000, Ricklefs and Shea 2007, Ricklefs et al. 2011, Martin et al. 2015), and this applies especially to tropical species with long incubation periods (Ricklefs 1993). Thus, prolonged embryo development might be associated with lower adult mortality rates in some way, including by delaying the aging process. Possibly relevant to this postulate, among 4 species of birds whose incubation periods ranged from 17 days (Japanese Quail [Coturnix japonica]) to 42 days (Leach's Storm-Petrel [Oceanodroma leucorhoa]), lipid peroxidation and DNA breakage near the end of embryo growth were inversely related to the length of the embryo development period (Tsunekage 2013, Tsunekage and Ricklefs 2015). Thus, more slowly growing embryos either resisted damage better or repaired damage more readily than more rapidly growing embryos.

Ricklefs and Scheuerlein (2001) characterized the rate of aging in several populations of birds in captivity in relation to body and brain mass, incubation period, postnatal growth rate, and genome size, and found that the logarithm of the Weibull rate of aging (ω; Ricklefs 1998) decreased with increasing log-transformed brain mass (b = −0.285 ± 0.059, r2 = 0.43) independently of variation in body size and incubation period. Thus, in that analysis, intrinsic longevity appeared to be unrelated to the rate of embryo growth, although many long-lived birds, such as parrots and albatrosses, also have very long embryo development periods.

In an analysis of data from the literature reporting results of microscopic examination of blood smears, Ricklefs (1992) found that the prevalence of hemosporidian (malarial) parasites is inversely related to the length of the incubation period ([species data] r2 = −0.75). Ricklefs suggested that longer development periods enabled increased resistance to parasites by providing extended time for diversification of the immunoglobulin molecules that are responsible for specific immunity. This hypothesis has not been tested experimentally, or by surveys of the diversity of the immune system response. However, Lee et al. (2008) found a strong positive correlation ([phylogenetic generalized least squares analysis] P < 0.001, r2 = 0.23) between the length of the incubation period and constitutive (“natural”) antibodies in 70 species of Neotropical birds; other life-history variables were not significantly associated with variation in natural antibodies.

Several studies have investigated the relationship between the cell-mediated immune response (CMI), as assessed by the phytohemagglutinin (PHA) assay, and both embryo and chick development rate. Tella et al. (2002) found that CMI was positively related to both adult size and the length of the development period across a wide variety of birds. Among small altricial species in their sample, including song birds, body size remained a strong predictor of the PHA response, but the incubation period and postnatal development rate did not. Palacios and Martin (2006) conducted a similar analysis of CMI in small, temperate-zone land birds and found that species with higher blood-parasite prevalence had stronger PHA responses, but that CMI was unrelated, or perhaps weakly inversely related, to the length of the incubation period. Regardless, the CMI data do not address hypotheses based on specific B-cell-related immunity. In a more recent study, Martin et al. (2011) found positive relationships between CMI and a hemagglutination response test for circulating antibodies (Matson et al. 2005), and between CMI and the length of the incubation period adjusted for incubation temperature, representing the “intrinsic” temperature-corrected rate of embryo growth. Clearly, additional analyses of the relationship between immune function and embryo development are needed.

5. Adult control over hatching synchrony and selection for rapid embryo growth. Embryo growth rate is potentially influenced by a number of conflicting selective pressures. If slower embryo development leads to higher chick quality and potentially longer adult life span and reproductive success, selection should favor longer incubation periods. Time-dependent mortality, primarily nest predation, favors shorter incubation periods. However, a potentially stronger selective agent for rapid development is sibling competition for resources. Nestling birds compete for food brought by the parents, and generally the larger (hence older) chick wins the contest (Ricklefs 1965, Lack 1968). Thus, early hatching, as a result of rapid embryonic development, would be strongly selected under these conditions (Werschkul and Jackson 1979, Ricklefs 1993).

(i) Some of the slowest embryo development rates occur in species with single-egg clutches, which therefore do not experience sibling competition. As mentioned above, in species with multi-chick broods, sibling competition is strong and often determines survival in the nest (Lack 1968); the outcome of sibling competition is largely determined by the relative hatching time of the chicks. However, because there is so little genetic variation in hatching time, this becomes important only when (1) chicks tend to hatch synchronously and (2) small heritable differences in development rate influence relative hatching position in the brood (Ricklefs 1992).

(ii) Accordingly, parents can reduce the selective impact of sibling competition by staggering the hatching times of their chicks, which they do simply by initiating incubation early in the laying sequence or varying maternal hormonal deposition in eggs (Gil 2008). Species with multi-egg clutches and long incubation periods tend to have asynchronous hatching or to lack evidence of sibling competition among the nestlings (i.e. all the chicks survive; Ricklefs 1993). However, prolonging the embryo growth period must incur costs for both the parents and the embryos in terms of energy and time-dependent egg mortality. Accordingly, the benefits of slow embryo growth must be substantial.

Conclusions

The time required to incubate the eggs varies among species of birds, but the adaptive significance of this variation is poorly understood. Among single-sex incubators, time away from the nest is needed for individuals to procure food and engage in other maintenance activities. This results in reduced egg temperatures and presumably increases the duration of the incubation period. There is little evidence that nests are dangerous sites for adults or that adult survival is increased by being away from the nest. Indeed, the longer incubation periods of many tropical birds, compared to temperate species, are associated with an increase in the total time parents spend at the nest. In the absence of advantage conveyed to the parent by a long incubation period, we suggest that the advantage belongs to the hatched chick. Species of tropical songbirds with longer incubation periods exhibit higher natural antibody levels and lower prevalence of hemosporidian blood parasites, pointing to potential fitness advantages of slow embryo growth. Parental strategies (e.g., early onset of incubation during the egg-laying sequence) that reduce the fitness advantage of rapid embryo growth and early hatching in response to intrabrood competition also suggest that slower development increases individual quality, or at least individual fitness. The relationship between embryo growth rate and lifetime reproductive success clearly warrants additional investigation.

ACKNOWLEDGMENTS

We are grateful to the U.S. National Science Foundation and the National Geographic Society for support of our research on avian life histories. R.E.R. also acknowledges the generous support of the Curators of the University of Missouri. The manuscript was greatly improved by the thoughtful suggestions of the anonymous reviewers.

LITERATURE CITED

1.

Álvarez, E., and E. Barba (2014). Within and between population variations of incubation rhythm of Great Tits Parus major. Behaviour 151:1827–1845. Google Scholar

2.

Ar, A., and H. Rahn (1980). Water in the avian egg: Overall budget of incubation. American Zoologist 20:373–384. Google Scholar

3.

Ardia, D. R., J. H. Pérez, E. K. Chad, M. A. Voss, and E. D. Clotfelter (2009). Temperature and life history: Experimental heating leads female Tree Swallows to modulate egg temperature and incubation behaviour. Journal of Animal Ecology 78:4–13. Google Scholar

4.

Ben-Ezra, N., and G. Burness (2017). Constant and cycling incubation temperatures have long-term effects on the morphology and metabolic rate of Japanese Quail. Physiological and Biochemical Zoology 90:96–105. Google Scholar

5.

Berntsen, H. H., and C. Bech (2016). Incubation temperature influences survival in a small passerine bird. Journal of Avian Biology 47:141–145. Google Scholar

6.

Brawn, J. D., J. R. Karr, and J. D. Nichols (1995). Demography of birds in a Neotropical forest: Effects of allometry, taxonomy, and ecology. Ecology 76:41–51. Google Scholar

7.

Carey, C., F. Leon-Velarde, and C. Monge (1990). Eggshell conductance and other physical characteristics of avian eggs laid in the Peruvian Andes. The Condor 92:790–793. Google Scholar

8.

Carey, C., E. L. Thompson, C. M. Vleck, and F. C. James (1982). Avian reproduction over an altitudinal gradient: Incubation period, hatchling mass, and embryonic oxygen consumption. The Auk 99:710–718. Google Scholar

9.

Chalfoun, A. D., and T. E. Martin (2007). Latitudinal variation in avian incubation attentiveness and a test of the food limitation hypothesis. Animal Behaviour 73:579–585. Google Scholar

10.

Conway, C. J., and T. E. Martin (2000). Evolution of passerine incubation behavior: Influence of food, temperature, and nest predation. Evolution 54:670–685. Google Scholar

11.

Cox, W. A., F. R. Thompson III, A. S. Cox, and J. Faaborg (2014). Post-fledging survival in passerine birds and the value of post-fledging studies to conservation. The Journal of Wildlife Management 78:183–193. Google Scholar

12.

Cresswell, W. (2008). Non-lethal effects of predation in birds. Ibis 150:3–17. Google Scholar

13.

Deeming, D. C. (Editor) (2002). Avian Incubation: Behaviour, Environment, and Evolution. Oxford University Press, Oxford, UK. Google Scholar

14.

Deeming, D. C., and M. W. J. Fergusen (1991). Physiological effects of incubation temperature on embryonic development in reptiles and birds. In Egg Incubation: Its Effects on Embryonic Development in Birds and Reptiles ( D. C. Deemingand M. W. J. Fergusen, Editors). Cambridge University Press, Cambridge, UK. pp. 147–172. Google Scholar

15.

DuRant, S. E., W. A. Hopkins, A. W. Carter, C. M. Stachowiak, and G. R. Hepp (2013). Incubation conditions are more important in determining early thermoregulatory ability than posthatch resource conditions in a precocial bird. Physiological and Biochemical Zoology 86:410–420. Google Scholar

16.

DuRant, S. E., W. A. Hopkins, D. M. Hawley, and G. R. Hepp (2012). Incubation temperature affects multiple measures of immunocompetence in young Wood Ducks (Aix sponsa). Biology Letters 8:108–111. Google Scholar

17.

Gil, D. (2008). Hormones in avian eggs: Physiology, ecology and behavior. Advances in the Study of Behavior 38:337–398. Google Scholar

18.

Hainsworth, F. R., and M. A. Voss (2002). Intermittent incubation: Predictions and tests for time and heat allocations. In Avian Incubation: Behaviour, Environment, and Evolution ( D. C. Deeming, Editor). Oxford University Press, London, UK. pp. 223–237. Google Scholar

19.

Hepp, G. R., R. A. Kennamer, and M. H. Johnson (2006). Maternal effects in Wood Ducks: Incubation temperature influences incubation period and neonate phenotype. Functional Ecology 20:308–314. Google Scholar

20.

Huggins, R. A. (1941). Egg temperatures of wild birds under natural conditions. Ecology 22:148–157. Google Scholar

21.

Karr, J. R., J. D. Nichols, M. K. Klimkiewicz, and J. D. Brawn (1990). Survival rates of birds of tropical and temperate forests: Will the dogma survive?The American Naturalist 136:277–291. Google Scholar

22.

Lack, D. (1968). Ecological Adaptations for Breeding in Birds. Methuen, London, UK. Google Scholar

23.

Lee, K. A., M. Wikelski, W. D. Robinson, T. R. Robinson, and K. C. Klasing (2008). Constitutive immune defences correlate with life-history variables in tropical birds. Journal of Animal Ecology 77:356–363. Google Scholar

24.

León-Velarde, F., and C. Monge. (2004). Avian embryos in hypoxic environments. Respiratory Physiology & Neurobiology 141:331–343. Google Scholar

25.

León-Velarde, F., C. Monge, and C. Carey (1997). Physiological strategies of oxygen transport in high altitude bird embryos. Comparative Biochemistry and Physiology A 118:31–37. Google Scholar

26.

Libsch, M. M., C. Batista, D. Buehler, I. Ochoa, J. Brawn, and R. E. Ricklefs (2008). Nest predation in a Neotropical forest occurs during daytime. The Condor 110:166–170. Google Scholar

27.

Lima, S. L. (1998). Nonlethal effects in the ecology of predator–prey interactions. BioScience 48:25–34. Google Scholar

28.

Marks, H. L. (1979). Changes in unselected traits accompanying long-term selection for four-week body weight in Japanese Quail. Poultry Science 58:269–274. Google Scholar

29.

Martin, T. E. (1995). Avian life history evolution in relation to nest sites, nest predation and food. Ecological Monographs 65:101–127. Google Scholar

30.

Martin, T. E. (1996). Life history evolution in tropical and south temperate birds: What do we really know?Journal of Avian Biology 27:263–272. Google Scholar

31.

Martin, T. E. (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

32.

Martin, T. E. (2004). Avian life-history evolution has an eminent past: Does it have a bright future?The Auk 121:289–301. Google Scholar

33.

Martin, T. E., E. Arriero, and A. Majewska (2011). A trade-off between embryonic development rate and immune function of avian offspring is revealed by considering embryonic temperature. Biology Letters 7:424–428. Google Scholar

34.

Martin, T. E., 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

35.

Martin, T. E., J. C. Oteyza, A. J. Boyce, P. Lloyd, and R. Ton (2015). Adult mortality probability and nest predation rates explain parental effort in warming eggs with consequences for embryonic development time. The American Naturalist 186:223–236. Google Scholar

36.

Martin, T. E., R. Ton, and A. A. Niklison (2013). Intrinsic vs. extrinsic influences on life history expression: Metabolism and parentally induced temperature influences on embryo development rate. Ecology Letters 16:738–745. Google Scholar

37.

Matson, K. D., R. E. Ricklefs, and K. C. Klasing (2005). A hemolysis-hemagglutination assay for characterizing constitutive innate humoral immunity in wild and domestic birds. Developmental and Comparative Immunology 29:275–286. Google Scholar

38.

Møller, A. P. (2005). Parasites, predators and the duration of developmental periods. Oikos 111:291–301. Google Scholar

39.

Nice, M. M. (1962). Development of behavior in precocial birds. Transactions of the Linnean Society of New York 8. Google Scholar

40.

Nilsson, J. F., M. Stjernman, and J.-Å. Nilsson (2008). Experimental reduction of incubation temperature affects both nestling and adult Blue Tits Cyanistes caeruleus. Journal of Avian Biology 39:553–559. Google Scholar

41.

Oniki, Y. (1979). Is nesting success low in the tropics?Biotropica 11:60–69. Google Scholar

42.

Palacios, M. G., and T. E. Martin (2006). Incubation period and immune function: A comparative field study among coexisting birds. Oecologia 146:505–512. Google Scholar

43.

Pietz, P. J., and D. A. Granfors (2000). Identifying predators and fates of grassland passerine nests using miniature video cameras. Journal of Wildlife Management 64:71–87. Google Scholar

44.

Rahn, H., and A. Ar (1974). The avian egg: Incubation time and water loss. The Condor 76:147–152. Google Scholar

45.

Rahn, H., and A. Ar (1980). Gas exchange of the avian egg: Time, structure, and function. American Zoologist 20:477–484. Google Scholar

46.

Rahn, H., A. Ar, and C. V. Paganelli (1979). How bird eggs breathe. Scientific American 240:46–55. Google Scholar

47.

Rahn, H., C. Carey, K. Balmas, B. Bhatia, and C. V. Paganelli (1977). Reduction of pore area of the avian eggshell as an adaptation to altitude. Proceedings of the National Academy of Sciences USA 74:3095–3098. Google Scholar

48.

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

49.

Ricklefs, R. E. (1965). Brood reduction in the Curve-billed Thrasher. The Condor 67:505–510. Google Scholar

50.

Ricklefs, R. E. (1969). An analysis of nesting mortality in birds. Smithsonian Contributions to Zoology 9. Google Scholar

51.

Ricklefs, R. E. (1974). Energetics of reproduction in birds. In Avian Energetics ( R. A. Paynter, Editor). Nuttall Ornithological Club, Cambridge, MA, USA.pp. 152–292. Google Scholar

52.

Ricklefs, R. E. (1979). Adaptation, constraint, and compromise in avian postnatal development. Biological Reviews 54:269–290. Google Scholar

53.

Ricklefs, R. E. (1984). The optimization of growth rate in altricial birds. Ecology 65:1602–1616. Google Scholar

54.

Ricklefs, R. E. (1987). Comparative analysis of avian embryonic growth. Journal of Experimental Zoology 51(Supplement 1):309–323. Google Scholar

55.

Ricklefs, R. E. (1992). Embryonic development period and the prevalence of avian blood parasites. Proceedings of the National Academy of Sciences USA 89:4722–4725. Google Scholar

56.

Ricklefs, R. E. (1993). Sibling competition, hatching asynchrony, incubation period, and lifespan in altricial birds. Current Ornithology 11:199–276. Google Scholar

57.

Ricklefs, R. E. (1996). Avian energetics, ecology, and evolution. In Avian Energetics and Nutritional Ecology ( C. Carey, Editor). Chapman & Hall, New York, NY, USA. pp. 1–30. Google Scholar

58.

Ricklefs, R. E. (1997). Comparative demography of New World populations of thrushes (Turdus spp.). Ecological Monographs 67:23–43. Google Scholar

59.

Ricklefs, R. E. (1998). Evolutionary theories of aging: Confirmation of a fundamental prediction, with implications for the genetic basis and evolution of life span. The American Naturalist 152:24–44. Google Scholar

60.

Ricklefs, R. E., and J. D. Brawn (2013). Nest attentiveness in several Neotropical suboscine passerine birds with long incubation periods. Journal of Ornithology 154:145–154. Google Scholar

61.

Ricklefs, R. E., and A. Scheuerlein (2001). Comparison of aging-related mortality among birds and mammals. Experimental Gerontology 36:845–857. Google Scholar

62.

Ricklefs, R. E., and R. E. Shea (2007). Estimating annual survival in sexually dimorphic species from proportions of first-year birds. Ecology 88:1408–1419. Google Scholar

63.

Ricklefs, R. E., R. E. Shea, and I.-H. Choi (1994). Inverse relationship between functional maturity and exponential growth rate of avian skeletal muscle: A constraint on evolutionary response. Evolution 48:1080–1088. Google Scholar

64.

Ricklefs, R. E., and C. A. Smeraski (1983). Variation in incubation period within a population of the European Starling. The Auk 100:926–931. Google Scholar

65.

Ricklefs, R. E., and J. M. Starck (1998). Embryonic growth and development. In Avian Growth and Development: Evolution within the Altricial–Precocial Spectrum ( J. M. Starckand R. E. Ricklefs, Editors). Oxford University Press, New York, NY, USA. pp. 31–58. Google Scholar

66.

Ricklefs, R. E., T. Tsunekage, and R. E. Shea (2011). Annual adult survival in several New World passerine birds based on age ratios in museum collections. Journal of Ornithology 152:481–495. Google Scholar

67.

Robinson, W. D., S. H. Austin, T. R. Robinson, and R. E. Ricklefs (2014). Incubation temperature does not explain variation in the embryo development periods in a sample of Neotropical passerine birds. Journal of Ornithology 155:45–51. Google Scholar

68.

Robinson, W. D., T. R. Robinson, S. K. Robinson, and J. D. Brawn (2000). Nesting success of understory forest birds in central Panama. Journal of Avian Biology 31:151–164. Google Scholar

69.

Robinson, W. D., G. Rompré, and T. R. Robinson (2005). Videography of Panama bird nests shows snakes are principal predators. Ornitologia Neotropical 16:187–195. Google Scholar

70.

Robinson, W. D., J. D. Styrsky, B. J. Payne, R. G. Harper, and C. F. Thompson (2008). Why are incubation periods longer in the tropics? A common-garden experiment with House Wrens reveals it is all in the egg. The American Naturalist 171:532–535. Google Scholar

71.

Romanoff, A. L. (1960). The Avian Embryo: Structural and Functional Development. Macmillan, New York, NY, USA. Google Scholar

72.

Romanoff, A. L., and A. J. Romanoff (1949). The Avian Egg. Wiley, New York, NY, USA. Google Scholar

73.

Rompré, G., and W. D. Robinson (2008). Predation, nest attendance, and long incubation periods of two Neotropical antbirds. Ecotropica 14:81–87. Google Scholar

74.

Sandercock, B. K., S. R. Beissinger, S. H. Stoleson, R. R. Melland, and C. R. Hughes (2000). Survival rates of a Neotropical parrot: Implications for latitudinal comparisons of avian demography. Ecology 81:1351–1370. Google Scholar

75.

Schaefer, T. (2004). Video monitoring of shrub-nests reveals nest predators. Bird Study 51:170–177. Google Scholar

76.

Shea, R. E., I.-H. Choi, and R. E. Ricklefs (1995). Growth rate and function of skeletal muscles in Japanese Quail selected for four-week body mass. Physiological Zoology 68:1045–1076. Google Scholar

77.

Siegel, P. B., J. W. Coleman, H. B. Graves, and R. E. Phillips (1968). Incubation period of chickens selected bidirectionally for juvenile body weight. Poultry Science 47:105–107. Google Scholar

78.

Skutch, A. F. (1967). Life histories of Central American highland birds. Bulletin of the Nuttall Ornithological Club 7. Google Scholar

79.

Skutch, A. F. (1976). Parent Birds and Their Young. University of Texas Press, Austin, TX, USA. Google Scholar

80.

Skutch, A. F. (1985). Clutch size, nesting success, and predation on nests of Neotropical birds, reviewed. Ornithological Monographs 36:575–594. Google Scholar

81.

Stake, M. M., and D. A. Cimprich (2003). Using video to monitor predation at Black-capped Vireo nests. The Condor 105:348–357. Google Scholar

82.

Starck, J. M. (1993). Evolution of avian ontogenies. Current Ornithology 10:275–366. Google Scholar

83.

Starck, J. M., and R. E. Ricklefs (1998). Variation, constraint, and phylogeny: Comparative analysis of variation in growth. In Avian Growth and Development: Evolution within the Altricial–Precocial Spectrum ( J. M. Starckand R. E. Ricklefs, Editors). Oxford University Press, New York, NY, USA. pp. 247–265. Google Scholar

84.

Tarwater, C. E. (2008). Predators at nests of the Western Slaty Antshrike (Thamnophilus atrinucha). The Wilson Journal of Ornithology 112:620–624. Google Scholar

85.

Tella, J. L., A. Scheuerlein, and R. E. Ricklefs (2002). Is cell-mediated immunity related to the evolution of life-history strategies in birds?Proceedings of the Royal Society of London B 269:1059–1066. Google Scholar

86.

Thompson, F. R., III, and D. E. Burhans (2003). Predation of songbird nests differs by predator and between field and forest habitats. Journal of Wildlife Management 67:408–416. Google Scholar

87.

Thompson, F. R., III, W. Dijak, and D. E. Burhans (1999). Video identification of predators at songbird nests in old fields. The Auk 116:259–264. Google Scholar

88.

Tieleman, B. I., J. B. Williams, and R. E. Ricklefs (2004). Nest attentiveness and egg temperature do not explain the variation in incubation periods in tropical birds. Functional Ecology 18:571–577. Google Scholar

89.

Tsunekage, T. (2013). Oxidative stress in avian embryos. University of Missouri–St. Louis, St. Louis, MO, USA. Google Scholar

90.

Tsunekage, T., and R. E. Ricklefs (2015). Increased lipid peroxidation occurs during development in Japanese Quail (Coturnix japonica) embryos. British Poultry Science 56:262–266. Google Scholar

91.

Werschkul, D. F., and J. A. Jackson (1979). Sibling competition and avian growth rates. Ibis 121:97–102. Google Scholar

92.

Williams, J. B. (1996). Energetics of avian incubation. In Avian Energetics and Nutritional Ecology ( C. Carey, Editor). Chapman & Hall, New York, NY, USA. pp. 375–416. Google Scholar
© 2017 American Ornithological Society.
Robert E. Ricklefs, Suzanne H. Austin, and W. Douglas Robinson "The adaptive significance of variation in avian incubation periods," The Auk 134(3), 542-550, (3 May 2017). https://doi.org/10.1642/AUK-16-171.1
Received: 15 August 2016; Accepted: 1 February 2017; Published: 3 May 2017
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