Evolution of passerine incubation behavior: influence of food, temperature, and nest predation

Abstract.— Incubation behavior is one component of reproductive effort and thus influences the evolution of life-history strategies. We examined the relative importance of body mass, frequency of mate feeding, food, nest predation, and ambient temperature to explain interspecific variation in incubation behavior (nest attentiveness, on- and off-bout durations, and nest trips per hour) using comparative analyses for North American passerines in which only females incubate. Body mass and frequency of mate feeding explained little variation in incubation behavior. We were also unable to detect any influence of food; diet and foraging strategy explained little interspecific variation in incubation behavior. However, the typical temperature encountered during reproduction explained significant variation in incubation behavior: Species breeding in colder environments take shorter bouts off the nest, which prevents eggs from cooling to temperatures below the physiological zero temperature. These species must compensate for shorter off-bouts by taking more of them (thus shorter on-bouts) to obtain needed energy for incubation. Nest predation also explains significant variation in incubation behavior among passerines: Species that endure high nest predation have evolved an incubation strategy (long on- and off-bouts) that minimizes activity that could attract predators. Nest substrate explained additional variation in incubation behavior (cavity-nesting birds have shorter on-bouts and make more frequent nest trips), presumably because nest predation and/or temperature varies among nest substrates. Thus, nest predation can influence reproductive effort in a way previously not demonstrated–by placing a constraint on parental activity at the nest. Incubating birds face an ecological cost associated with reproductive effort (predation of entire brood) that should be considered in future attempts to explain avian life-history evolution.     

Life-history variation within a three-spined stickleback population in the Camargue

Among individuals of female three-spined sticklebacks Gasterosteus aculeatus from a population in the Camargue, southern France, studied in 12 successive years, adult L _T ranged from 31–64 mm, clutch size ranged from 33–660 eggs, and mean egg diameter per clutch ranged from 1.15–1.67 mm. Because the population was strictly annual, inter-annual variation corresponded to variation among generations having experienced different environmental conditions. Body mass varied significantly among years, suggesting an effect of varying environmental conditions. Gonad mass and clutch size increased with body mass, but mean egg diameter was not correlated to body mass. Body mass-adjusted gonad mass, interpreted as reproductive effort per clutch, did not vary significantly among years, suggesting that this trait was not influenced by environmental conditions. Body mass-adjusted clutch size and egg size varied significantly among years. Inter-annual variation in body length at breeding, clutch size and egg size was of the same order of magnitude as inter-population variation reported by other authors for this species. During the breeding season, reproductive effort and clutch size tended to increase. Egg size tended to decrease during the breeding season but this seasonal pattern varied among years. Observed life-history variation is discussed both in terms of its evolutionary significance and methodological implications in the study of life-history variation among populations.     

Habitat-specific clutch size and cost of incubation in eiders reconsidered

The energetic incubation constraint hypothesis (EICH) for clutch size states that birds breeding in poor habitat may free up resources for future reproduction by laying a smaller clutch. The eider (Somateria mollissima) is considered a candidate for supporting this hypothesis. Clutch size is smaller in exposed nests, presumably because of faster heat loss and higher incubation cost, and, hence, smaller optimal clutch size. However, an alternative explanation is partial predation: the first egg(s) are left unattended and vulnerable to predation, which may disproportionately affect exposed nests, so clutch size may be underestimated. We experimentally investigated whether predation on first-laid eggs in eiders depends on nest cover. We then re-evaluated how nesting habitat affects clutch size and incubation costs based on long-term data, accounting for confounding effects between habitat and individual quality. We also experimentally assessed adult survival costs of nesting in sheltered nests. The risk of egg predation in experimental nests decreased with cover. Confounding between individual and habitat quality is unlikely, as clutch size was also smaller in open nests within individuals, and early and late breeders had similar nest cover characteristics. A trade-off between clutch and female safety may explain nest cover variation, as the risk of female capture by us, mimicking predation on adults, increased with nest cover. Nest habitat had no effect on female hatching weight or weight loss, while lower temperature during incubation had an unanticipated positive relationship with hatching weight. There were no indications of elevated costs of incubating larger clutches, while clutch size and colony size were positively correlated, a pattern not predicted by the ‘energetic incubation constraint’ hypothesis. Differential partial clutch predation thus offers the more parsimonious explanation for clutch size variation among habitats in eiders, highlighting the need for caution when analysing fecundity and associated life-history parameters when habitat-specific rates of clutch predation occur.     

Geographic variation in avian incubation periods and parental influences on embryonic temperature

Theory predicts shorter embryonic periods in species with greater embryo mortality risk and smaller body size. Field studies of 80 passerine species on three continents yielded data that largely conflicted with theory; incubation (embryonic) periods were longer rather than shorter in smaller species, and egg (embryo) mortality risk explained some variation within regions, but did not explain larger differences in incubation periods among geographic regions. Incubation behavior of parents seems to explain these discrepancies. Bird embryos are effectively ectothermic and depend on warmth provided by parents sitting on the eggs to attain proper temperatures for development. Parents of smaller species, plus tropical and southern hemisphere species, commonly exhibited lower nest attentiveness (percent of time spent on the nest incubating) than larger and northern hemisphere species. Lower nest attentiveness produced cooler minimum and average embryonic temperatures that were correlated with longer incubation periods independent of nest predation risk or body size. We experimentally tested this correlation by swapping eggs of species with cool incubation temperatures with eggs of species with warm incubation temperatures and similar egg mass. Incubation periods changed (shortened or lengthened) as expected and verified the importance of egg temperature on development rate. Slower development resulting from cooler temperatures may simply be a cost imposed on embryos by parents and may not enhance offspring quality. At the same time, incubation periods of transferred eggs did not match host species and reflect intrinsic differences among species that may result from nest predation and other selection pressures. Thus, geographic variation in embryonic development may reflect more complex interactions than previously recognized.     

Nest desertion by a cowbird host: an antiparasite behavior or a response to egg loss?

Natural selection can favor songbirds that desert nests containingeggs of the parasitic brown-headed cowbird (Molothrus ater).However, the high variability in desertion of parasitized nestswithin species is perplexing in light of the typically highcosts of parasitism. Because nest desertion can also be a responseto partial clutch predation, we first asked if Bell's vireos(Vireo bellii) deserted nests in response to the presence ofcowbird eggs (antiparasite response hypothesis) or to egg removalby predators and female cowbirds (egg predation hypothesis).Second, we asked whether variation in nest desertion was dueto intrinsic differences among individuals or to variation innest contents. We monitored a large number of nests (n = 494)and performed a clutch manipulation experiment to test thesehypotheses. The number of vireo eggs that remained in a nestwas a strong predictor of desertion both within and among pairs.Neither the presence of a single cowbird egg, which leads tonest failure for this host, nor the number of cowbird eggs receivedin a vireo nest influenced nest desertion. Furthermore, vireosdid not desert experimental nests when we immediately exchangedcowbird eggs for vireo eggs but deserted if we removed vireoeggs and replaced them with cowbird eggs the following morning.Desertion of parasitized nests by Bell's vireos can be almostentirely explained as a response to partial or complete clutchloss and does not appear to have been altered by selection frombrood parasitism.     

Don'T put all your eggs in one nest: spread them and cut time at risk

Abstract In many egg-laying animals, some females spread their clutch among several nests. The fitness effects of this reproductive tactic are obscure. Using mathematical modeling and field observations, we analyze an unexplored benefit of egg spreading in brood parasitic and other breeding systems: reduced time at risk for offspring. If a clutch takes many days to lay until incubation and embryo development starts after the last egg, by spreading her eggs a parasitic female can reduce offspring time in the vulnerable nest at risk of predation or other destruction. The model suggests that she can achieve much of this benefit by spreading her eggs among a few nests, even if her total clutch is large. Field data from goldeneye ducks Bucephala clangula show that egg spreading enables a fecund female to lay a clutch that is much larger than average without increasing offspring time at risk in a nest. This advantage increases with female condition (fecundity) and can markedly raise female reproductive success. These results help explain the puzzle of nesting parasites in some precocial birds, which lay eggs in the nests of other females before laying eggs in their own nest. Risk reduction by egg spreading may also play a role in the evolution of other breeding systems and taxa-for instance, polyandry with male parental care in some birds and fishes.     

The evolution of egg rejection by cuckoo hosts in Australia and Europe

Exploitation of hosts by brood parasitic cuckoos is expectedto stimulate a coevolutionary arms race of adaptations and counteradaptations.However, some hosts have not evolved defenses against parasitism.One hypothesis to explain a lack of host defenses is that thelife-history strategies of some hosts reduce the cost of parasitismto the extent that accepting parasitic eggs in the nest is evolutionarilystable. Under this hypothesis, it pays hosts to accept cuckooeggs if (1) the energetic cost of raising the cuckoo is low,(2) there is time to renest, and (3) clutch size is small. Weparasitized the nests of host and nonhost species with nonmimeticmodel eggs to test whether the evolution of egg recognitionby cuckoo hosts could be explained by life-history variablesof the host. The most significant factor explaining rates ofrejection of model eggs was whether or not a species was a cuckoohost, with hosts rejecting model eggs at a higher rate thannonhosts. Egg-rejection rates were also explained by visibilitywithin the nest and by cuckoo mass. We found little supportfor the life-history model of egg rejection. Our results suggestthat parasitism is always sufficiently costly to select forhost defenses and that the evolution of defenses may be limitedby proximate constraints such as visibility within the nest.     

Costs of large communal clutches for male and female Greater Rheas Rhea americana

The breeding system of the Greater Rhea Rhea americana is almost unique among birds as it combines harem polygyny and sequential polyandry, with communal egg-laying and uniparental male care. In this species, large communal clutches (more than 30 eggs) are rare and have a lower hatching success than smaller clutches. Here we analyse the proximate causes of hatching failures and the costs of large communal clutches (and therefore the costs of extensive polygyny) for males and females. We evaluated if length of the nesting period, egg viability, egg losses during incubation and male parental activity at the nest were affected by clutch size. We also evaluated if chicks hatched from large clutches have a lower survival during the first 2 months after hatching. Large clutches had longer nesting period and lower hatching success, mainly as a result of bacterial contamination of the eggs and increased hatching asynchrony. In addition, large clutches tended to lose more eggs as a result of accidental breakage or predation. Male activity at the nest and chick survival were not related to clutch size. Low hatching success, nest predation risk and energetic costs associated with large clutches penalize females that join large harems and males that accept additional eggs into the nest.     

Covariation between clutch size, egg weight and egg shape: comparative evidence for chelonians

The variation in reproductive variables is documented both within and across species of chelonians. At both the generic and family levels, egg weight and clutch size show positive, significant correlations with adult carapace length. There is a negative correlation across both genera and families between clutch size and egg weight after removing the effects of body size, suggesting an evolutionary trade-off between these two life-history characteristics. However, the trade-off is not complete, since clutch size is positively correlated with clutch weight after removing the effects of body size. Terrestrial species lay fewer and larger eggs for their size than freshwater or marine species, but this association is statistically confounded by the fact that chelonian families form ecological groups. There is no significant association between habitat and clutch weight after removing the effects of body size, nor between latitude and either egg weight or clutch size, but temperate species have a heavier clutch weight after removing the effects of body size. Larger species lay eggs that are more spherical, but after controlling for body size, egg shape is not associated with clutch size. The patterns of covariation between adult weight, egg weight and clutch size contrast with those reported for birds and mammals, and some reasons for these differences are discussed.     

Maternal investment in reproduction and its consequences in leatherback turtles

Maternal investment in reproduction by oviparous non-avian reptiles is usually limited to pre-ovipositional allocations to the number and size of eggs and clutches, thus making these species good subjects for testing hypotheses of reproductive optimality models. Because leatherback turtles (Dermochelys coriacea) stand out among oviparous amniotes by having the highest clutch frequency and producing the largest mass of eggs per reproductive season, we quantified maternal investment of 146 female leatherbacks over four nesting seasons (2001–2004) and found high inter- and intra-female variation in several reproductive characteristics. Estimated clutch frequency [coefficient of variation (CV) = 31%] and clutch size (CV = 26%) varied more among females than did egg mass (CV = 9%) and hatchling mass (CV = 7%). Moreover, clutch size had an approximately threefold higher effect on clutch mass than did egg mass. These results generally support predictions of reproductive optimality models in which species that lay several, large clutches per reproductive season should exhibit low variation in egg size and instead maximize egg number (clutch frequency and/or size). The number of hatchlings emerging per nest was positively correlated with clutch size, but fraction of eggs in a clutch yielding hatchlings (emergence success) was not correlated with clutch size and varied highly among females. In addition, seasonal fecundity and seasonal hatchling production increased with the frequency and the size of clutches (in order of effect size). Our results demonstrate that female leatherbacks exhibit high phenotypic variation in reproductive traits, possibly in response to environmental variability and/or resulting from genotypic variability within the population. Furthermore, high seasonal and lifetime fecundity of leatherbacks probably reflect compensation for high and unpredictable mortality during early life history stages in this species.     

Indeterminate laying and flexible clutch size in a capital breeder, the common eider

Clutch size control in capital breeders such as large waterfowl has been much debated. Some studies have concluded that clutch size in ducks is determined before the start of laying and does not change in response to egg additions or removals. The response, however, may depend on the timing of tests, and experiments may have been too late for females to alter the number of eggs. We here study clutch size responses to predation of first and second eggs in the common eider, using protein fingerprinting of egg albumen to verify that the same female continues laying in the nest after predation. Sixty of 79 females with early egg predation (one or both of the two first eggs) deserted the nest. Among the 19 females that stayed and continued laying, the mean number of eggs produced was 4.4, significantly higher than the 3.7 in non-predated nests. The staying females had similar egg size and clutch initiation date as females that deserted, and their body mass and clutch initiation date was similar to that of females whose clutches were not predated. Even capital-breeding common eiders may therefore be indeterminate layers, as many females in which early eggs are removed lay more eggs than others. A previous study has shown that they can reduce their laying if eggs are added. Our results add to increasing evidence that ducks have more flexible egg production than previously thought.     

A theoretical investigation of the effect of latitude on avian life histories

Tropical birds lay smaller clutches than birds breeding in temperate regions and care for their young for longer. We develop a model in which birds choose when and how often to breed and their clutch size, depending on their foraging ability and the food availability. The food supply is density dependent. Seasonal environments necessarily have a high food peak in summer; in winter, food levels drop below those characteristic of constant environments. A bird that cannot balance its energy needs during a week dies of starvation. If adult predation is negligible, birds in low seasonal environments are constrained by low food during breeding seasons, whereas birds in high seasonal environments die during the winter. Low food seasonality selects for small clutch sizes, long parental care times, greater age at first breeding, and high juvenile survival. The inclusion of adult predation has no major effect on any life-history variables. However, increased nest predation reduces clutch size. The same trends with seasonality are also found in a version of the model that includes a condition variable. Our results show that seasonal changes in food supply are sufficient to explain the observed trends in clutch size, care times, and age at first breeding.     

Causes of reduced clutch size in a tidal marsh endemic

We tested three hypotheses of clutch size variation in two subspecies of the swamp sparrow (Melospiza georgiana georgiana and M. g. nigrescens). Swamp sparrows follow the pattern of other estuarine endemics, where clutch size is smaller among tidal salt marsh populations (M. g. nigrescens) than their closest inland relatives (M. g. georgiana). Our results support predation risk and temperature, but not adult survival, as explanations of this pattern in swamp sparrows. Coastal nests were twice as likely to fail as inland nests, and parental activity around the nest site was positively related to clutch size at both sites. When brood size was controlled for, coastal adults visited nests less often and females vocalized less frequently during visits than inland birds, which may decrease nest detectability to predators. Coastal parents waited longer than inland birds to feed offspring in the presence of a model nest predator, but there was no difference in their response to models of predators of adults, as would be expected if coastal birds possessed increased longevity. Additionally, coastal females laid more eggs than inland females over a single season, following a within-season bet-hedging strategy rather than reducing within-season investment. Coastal territories experienced ambient air temperatures above the physiological zero of egg development more often, and higher temperatures during laying correlated with smaller clutches and increased egg inviability among coastal birds. Similar effects were not seen among inland nests, where laying temperatures were generally below physiological zero. Both subspecies showed an increase in hatching asynchrony and a decrease in apparent incubation length under high temperatures. Coastal individuals, however, showed less hatching asynchrony overall despite higher temperatures. Both air temperatures during laying and predation risk could potentially explain reduced clutch size in not only coastal plain swamp sparrows, but also other tidal marsh endemics.     

Egg coloration and selection for crypsis in open-nesting blackbirds

High variation in egg coloration among birds has traditionally been explained as adaptation for camouflage. We tested this hypothesis by conducting reciprocal clutch exchanges (n=301) among Brewer's blackbirds Euphagous cyanocephalus , red-winged blackbirds Agelaius phoeniceus , and yellow-headed blackbirds Xanthocephalus xanthocephalus . We predicted that clutches placed against their natural nest backgrounds would have higher survival rates than heterospecific clutches. Intraspecific clutch exchanges were used as a control. Clutch survival was monitored for a 9-d period at all nests, during which time incubation rhythm and nest defense were quantified. Intraspecific clutch exchanges did not influence incubation or nest defense. For two of the species, intraspecific clutch exchanges did not influence clutch survival; in red-winged blackbirds, however, intraspecifically exchanged clutches had somewhat depressed survival curves relative to control clutches (P=0.08). The effect of interspecific clutch exchanges differed by host species. In Brewer's nests, eggs of the yellow-headed blackbird had lower survival than Brewer's eggs (P=0.02), but survival of red-winged blackbird eggs did not differ from Brewer's eggs (P=0.50). In nests of red-winged blackbirds, all three clutch types had approximately equal survival. In yellow-headed blackbird nests, eggs of the red-winged blackbird had lower survival than yellow-headed blackbird eggs (P=0.06), and survival of Brewer's eggs did not differ from yellow-headed blackbird eggs (P=0.31). These findings support a role for egg coloration as camouflage in two of the three species studied.     

Avian growth and development rates and age-specific mortality: the roles of nest predation and adult mortality

Previous studies have shown that avian growth and development covary with juvenile mortality. Juveniles of birds under strong nest predation pressure grow rapidly, have short incubation and nestling periods, and leave the nest at low body mass. Life-history theory predicts that parental investment increases with adult mortality rate. Thus, developmental traits that depend on the parental effort exerted (pre- and postnatal growth rate) should scale positively with adult mortality, in contrast to those that do not have a direct relationship with parental investment (timing of developmental events, e.g. nest leaving). I tested this prediction on a sample of 84 North American songbirds. Nestling growth rate scaled positively and incubation period duration negatively with annual adult mortality rates even when controlled for nest predation and other covariates, including phylogeny. On the contrary, neither the duration of the nestling period nor body mass at fledging showed any relationship. Proximate mechanisms generating the relationship of pre- and postnatal growth rates to adult mortality may include increased feeding, nest attentiveness during incubation and/or allocation of hormones, and deserve further attention.     

Life-history variation of a neotropical thrush challenges food limitation theory

Since David Lack first proposed that birds rear as many young as they can nourish, food limitation has been accepted as the primary explanation for variation in clutch size and other life-history traits in birds. The importance of food limitation in life-history variation, however, was recently questioned on theoretical grounds. Here, we show that clutch size differences between two populations of a neotropical thrush were contrary to expectations under Lack's food limitation hypothesis. Larger clutch sizes were found in a population with higher nestling starvation rate (i.e. greater food limitation). We experimentally equalized clutches between populations to verify this difference in food limitation. Our experiment confirmed greater food limitation in the population with larger mean clutch size. In addition, incubation bout length and nestling growth rate were also contrary to predictions of food limitation theory. Our results demonstrate the inability of food limitation to explain differences in several life-history traits: clutch size, incubation behaviour, parental feeding rate and nestling growth rate. These life-history traits were better explained by inter-population differences in nest predation rates. Food limitation may be less important to life history evolution in birds than suggested by traditional theory.     

Conspecific brood parasitism and population dynamics

Conspecific brood parasitism (CBP), defined as parasitic laying of eggs in a conspecific nest without providing parental care, occurs in insects, fishes, amphibians, and many birds. Numerous factors have been proposed to influence the evolution of CBP, including nest site limitation; effects of brood size, laying order, or parasitic status on offspring survival; randomness of parasitic egg distribution; adult life-history trade-offs; and variation in parental female quality or risk of nest predation. However, few theoretical studies consider multiple possible types of parasitism or the interplay between evolution of parasitism and population dynamics. We review existing theory of CBP and develop a synthetic modeling approach to ask how best-of-a-bad job parasitism, separate-strategies parasitism (in which females either nest or parasitize), and joint-strategies parasitism (in which females can both nest and parasitize) differ in their evolutionary conditions and impacts on population dynamics using an adaptive dynamics framework including multivariate traits. CBP can either stabilize or destabilize population dynamics in different scenarios, and the role of comparable parameters on evolutionarily stable strategy parasitism rate, equilibrium population size, and population stability can differ for the different modes of parasitism.     

Egg ejection cost can limit defence strategies against brood parasitism

A cost associated with the evolution of antiparasite strategies is the failure to recognize parasitic eggs, leading the host to evict its own eggs. However, there is evidence that birds recognize their own eggs through imprinting. This leads to the question of why birds accept parasitic eggs if such eggs can be identified. Here, we tested whether egg ejection per se can be costly due to increased predation risk to the remaining clutch and whether olfactory or visual cues of egg ejection increase predation. We carried out three field experiments to answer the following questions: (a) Does ejecting an egg increase nest predation risk? (b) Does the presence of olfactory cues, such as the smell of a broken egg, increase nest predation risk? And (c) Does the presence of visual cues, such as an egg shell below the nest, increase nest predation risk? We found evidence that egg ejection increases nest predation and that olfactory cues alone also increase nest predation. The presence of visual cues did not change predation rates. These data indicate that egg ejection is costly for both host and parasitic eggs that may remain in the nest. Our results suggest why host and parasite eggs are commonly found within the same nests, despite the possibility that hosts recognize and could possibly eject the parasite’s egg.     

Clutch predation in great tinamous Tinamus major and implications for the evolution of egg color

Egg camouflage has been found to reduce predation in several ground‐nesting species. Therefore, the evolution of eggs that lack camouflage in ground nesting birds is puzzling. Even though clutch predation in the tropics is high, tinamous are the only tropical ground‐nesting birds that do not build a nest and do not lay cryptic eggs. I studied predation of great tinamou clutches in a lowland tropical forest and found that risk of predation was higher during incubation when the eggs are covered by the parent, than during laying when they are exposed, suggesting that predators primarily use cues from the incubating males to locate the clutch and not cues from the eggs. Clutch size had no effect on predation rate, even though larger clutches are more conspicuous to a human observer. Predation by visual cues is likely reduced during incubation by the camouflaged plumage and high nest attendance of males. If most predators use cues from the incubating male and not the eggs to locate clutches, then conspicuous egg color may have evolved in great tinamous as an intra‐specific signal. I evaluate hypotheses that may explain the maintenance of conspicuous egg color in tinamous.     

Variation in incubation effort during egg laying in the Mountain Bluebird and its association with hatching asynchrony

Females in many bird species reportedly begin incubation prior to clutch completion, but the nature of such incubation and the degree to which it varies among females remains undescribed for almost all species. We used continuous recording of nest‐cup temperatures to document incubation effort during egg laying at 57 Mountain Bluebird (Sialia currucoides) nests in a high‐elevation Wyoming population. We then asked whether such effort predicted the degree to which eggs hatch asynchronously. Although substantial egg heating could begin abruptly late in laying (previously reported as the norm for this species) or even after clutch completion, we found that most (>90%) females began incubation gradually, engaging in a few (usually 1–8), brief (<10 min) bouts of heating on the day they laid their first or second egg. Thereafter, females varied markedly in when they increased incubation effort and by how much. The onset of nocturnal incubation also varied, with females beginning to incubate at night after laying their prepenultimate, penultimate, or last egg and not always initially incubating through the night. As an index of the total amount of heat applied to eggs during laying, we calculated the cumulative number of degrees by which nest‐cup temperatures exceeded the threshold temperature required for embryonic development. This value varied by more than 150‐fold between nests and explained >50% of the variation in hatching asynchrony. Our results thus provide strong support for the widely held, but rarely tested, assumption that parent birds can have substantial control over the degree of hatching asynchrony by varying the amount of incubation done prior to clutch completion.