The energetic costs of egg heating constrain incubation attendance but do not determine daily energy expenditure in the pectoral sandpiper

Heating eggs during incubation may be relatively energeticallycostly, affecting the outcome or number of breeding attempts.We determined the effect of reduced egg heating costs on nestattendance, change in body mass, and daily energy expenditure(DEE using the doubly labeled water technique) by heating nestsof pectoral sandpipers. We also considered ground temperature,which may influence overall incubation costs, and mass reservesand stage of incubation, which may influence an individual'sability to respond to changes in overall incubation cost. Thetotal proportion of time spent in attending the eggs was significantlygreater in nests that were experimentally heated (3.6% or 52min daily), and this effect was significantly greater at lowground temperatures (14.7% or 211.7 min daily). Mass changewas independent of experimental heating when controlling forattendance, although mass loss rate was greater for birds thatattended more (for every 10% increase in daily proportion ofattendance 0.12 extra grams of body mass were lost per hour),and overall daily attendance increased by 0.5% for every extra1 g of body mass. DEE was greater for birds that had the higherrates of mass gain (for every 0.1 g of mass gained per hour,DEE increased by 20.5 kJ per day) but was independent of experimentalheating when controlling for attendance. Overall, the resultssuggest that females are constrained from attending more bytheir energy reserve levels being depleted at least partly bythe costs of egg heating, but these costs probably do not determineDEE, as costs off the nest may far exceed those incurred whilesitting. Breeding in the arctic is clearly energetically demanding:pectoral sandpipers had an average DEE of 361.1 ± 8.9kjd^–1, a mean power output of 4.1 W, equivalent to 6.1times basal metabolic rate (n = 24 birds).     

How to save the rarest Darwin's finch from extinction: the mangrove finch on Isabela Island

Habitat destruction and predation by invasive alien species has led to the disappearance of several island populations of Darwin''s finches but to date none of the 13 recognized species have gone extinct. However, driven by rapid economic growth in the Galápagos, the effects of introduced species have accelerated and severely threatened these iconic birds. The critically endangered mangrove finch (Camarhynchus heliobates) is now confined to three small mangroves on Isabela Island. During 2006–2009, we assessed its population status and monitored nesting success, both before and after rat poisoning. Population size was estimated at around only 100 birds for the two main breeding sites, with possibly 5–10 birds surviving at a third mangrove. Before rat control, 54 per cent of nests during incubation phase were predated with only 18 per cent of nests producing fledglings. Post-rat control, nest predation during the incubation phase fell to 30 per cent with 37 per cent of nests producing fledglings. During the nestling phase, infestation by larvae of the introduced parasitic fly (Philornis downsi) caused 14 per cent additional mortality. Using population viability analysis, we simulated the probability of population persistence under various scenarios of control and showed that with effective management of these invasive species, mangrove finch populations should start to recover.     

The importance of microclimate variation in determining size,growth and survival of avian offspring: experimental evidence from a cavity nesting passerine

Organisms are expected to balance energy allocation in such a way that fitness is maximized. While much research has focussed on allocation strategies of reproducing parents, in particular birds, relatively little attention has been paid to how nestlings allocate energy while in the nest. Nestling birds are faced with a trade-off between devoting energy to growth or to thermoregulation, and in altricial species it is likely that the thermal environment of the nest site influences the nature of this trade-off. Here, we experimentally investigate how altering the microclimate of nests affects the growth, size and survival, as well as cell-mediated immune (CMI) response, of nestling tree swallows (Tachycineta bicolor) in a temperate environment. We place air-activated heating pads in nests of swallows when young were between 4 days and 16 days of age, and compared performance of offspring to control nests. Our manipulation raised temperatures of heated nests by approximately 5°C compared to control nests. Offspring in heated nests had enhanced survival while in the nest, and we also found that they were heavier and had longer ninth primary feathers at 16 days of age. In addition, heating nest boxes resulted in significantly faster growth of primaries, and there was a trend for growth rates of mass to also be higher in heated nests. There were no significant differences between heated and control nests in growth rate or size of tarsus at age 16 days, and we speculate that this lack of response to elevated nest temperatures may be due to growth of skeletal structures being limited by other factors such as calcium availability. We also found no difference between heated and control nests in CMI response. Nonetheless, our results show overall that increasing temperatures of nests has significant benefits that enhance the fitness of offspring. As provisioning rates to offspring did not differ between heated and control nests, we suspect that the beneficial effects of heating were not the consequence of changes in parental behaviour. Our results provide insight into factors, other than food supply, that have important consequences in determining reproductive success of birds breeding in temperate environments.     

Temperature and life history: experimental heating leads female tree swallows to modulate egg temperature and incubation behaviour

1. Life-history decisions are strongly affected by environmental conditions. In birds, incubation is energetically expensive and affected significantly by ambient temperature. We reduced energetic constraints for female tree swallows (Tachycineta bicolor) by experimentally heating nests during incubation by an average of 6.9 degrees C to test for changes in incubation behaviour. 2. Females in heated boxes (hereafter 'heated females') increased time spent incubating and maintained higher on-bout and off-bout egg temperatures. This indicates that female energetic constraints, not maximizing developmental conditions of offspring, determine incubation investment. Furthermore, this result suggests that embryonic developmental conditions in unmanipulated nests are suboptimal. 3. We found individual variation in how females responded to experimental heating. Early-laying (i.e. higher phenotypic quality) females with heated nests increased egg temperatures and maintained incubation constancy, while later-laying (lower quality) heated females increased incubation constancy. Changes in egg temperature were due to changes in female behaviour and not due directly to increases in internal nest-box temperatures. 4. Behaviour during the incubation period affected hatching asynchrony. Decreased variation in egg temperature led to lower levels of hatching asynchrony, which was also generally lower in heated nests. 5. Our study finds strong support for the prediction that intermittent incubators set their incubation investment at levels dictated by energetic constraints. Furthermore, females incubating in heated boxes allocated conserved energy primarily to increased egg temperature and increased incubation attentiveness. These results indicate that studies investigating the role of energetics in driving reproductive investment in intermittent incubators should consider egg temperature and individual variation more explicitly.     

Egg puncture allows shiny cowbirds to assess host egg development and suitability for parasitism

Parasitic cowbirds and cuckoos generally reduce the clutch size of the hosts they parasitize by removing or destroying some of their eggs. Shiny cowbirds (Molothrus bonariensis) puncture their hosts'' eggs both when parasitizing the nests and also when they do not parasitize them. We propose that, by puncturing the host''s eggs, shiny cowbirds gain an informational benefit. They assess the degree of development of the host''s embryos and so avoid laying in nests that would not provide enough incubation time for the parasitic eggs to hatch. Two predictions follow: (i) punctures should occur in advance or immediately before parasitic events, and (ii) the occurrence of parasitism should depend on the degree of development of the host''s embryos when punctures occurred, i.e. on the stage of incubation. Both predictions are supported by our data of shiny cowbirds parasitizing yellow-winged blackbirds (Agelaius thilius). Egg punctures are not used to reset the host''s nesting attempt when shiny cowbirds do not parasitize the nests. We discuss the potential mechanisms implicated in egg development assessment and propose a critical experiment to test this hypothesis.     

A novel 'sit and wait' reproductive strategy in social wasps

I present evidence indicating that a subset of spring females in the social wasp Polistes dominulus do not initiate colonies but rather ''sit and wait'' to adopt colonies initiated and abandoned by other conspecifics. These results are, to my knowledge, the first to demonstrate conclusively this alternative reproductive strategy in social wasps. Individuals engaging in the sit-and-wait strategy behave selfishly by adopting the most mature nests available; such nests will produce workers sooner than less mature nests and, consequently, are more likely to survive. The sit-and-wait reproductive strategy may safeguard an individual from early-season, foraging-related mortality as well as reduce early-season energy expenditure.     

What limits clutch size? A test of the incubation‐capacity hypothesis in a high‐elevation population of Mountain Bluebirds

Most studies of factors that limit the number of eggs that birds lay have focused on the disadvantages of having too many young to feed. Less attention has been paid to the consequences of having a large number of eggs to incubate. The incubation‐capacity hypothesis proposes that females lay as many eggs as they can effectively incubate. We tested this hypothesis in 2018 in a montane population of Mountain Bluebirds (Sialia currucoides). Most females in this population lay five or six eggs; clutches of seven occur, but are rare. We added eggs to some nests, forcing females to incubate seven eggs, while leaving other nests as controls. Among females completing incubation, those with enlarged clutches hatched as many eggs as did control females, and did so in the same amount of time. This was despite an extended period of unusually cold and often wet weather that occurred when many females were incubating. Our results firmly reject the suggestion that females typically lay no more than six eggs because they cannot effectively heat seven eggs. One or more other factors must limit clutch size. One possible factor is suggested by the fact that during the period of inclement weather, more females with enlarged clutches than control females appeared to abandon nests before completing incubation. Because larger clutches require more energy to incubate, females with seven eggs during energetically stressful conditions could more quickly reach the point where they lack sufficient energy for both incubation and self‐maintenance. Such conditions may occur frequently enough in the montane environment that, on average, laying seven eggs results in reduced lifetime reproductive success.     

Stage-dependent foraging in breeding black-legged kittiwakes Rissa tridactyla: distinguishing behavioural responses to intrinsic and extrinsic factors

Different phases of the annual cycle in birds and mammals are often associated with characteristic and recurrent foraging behaviours. The extent to which stage‐dependent changes in foraging behaviour are caused by intrinsic or extrinsic factors is unclear. We controlled for the effects of extrinsic factors by synchronising groups of incubating and chick‐rearing black‐legged kittiwakes Rissa tridactyla. Synchrony amongst incubators and rearers was achieved experimentally by switching eggs between nests. Behavioural responses to the treatment varied between the sexes. Male kittiwakes with prolonged‐incubation made fewer foraging trips but of greater duration compared to those rearing chicks resulting in no change in the time spent on trips between the two groups. Females with prolonged‐incubation carried out fewer trips than those rearing chicks but trip duration did not differ between the two stages which resulted in prolonged‐incubating birds spending a lower percentage time on trips. In contrast, foraging ranges did not differ between prolonged‐incubation and chick‐rearing birds for either sex. This suggests that extrinsic factors, such as food availability and distribution determine kittiwake foraging locations and ranges, whereas intrinsic factors, reflected in parental duties, constrain nest attendance. Female prolonged‐incubators invested lower levels of parental effort, in terms of daily energy expenditure, compared to chick‐rearers whereas males did not show stage‐related differences in energy expenditure. This provides evidence that incubation could be an energetically cheaper stage although under normal conditions this difference may be masked by temporal variation in environmental factors. We conclude that while conditions differ between the incubation and chick rearing stages for kittiwakes at this colony, they are not the main factors prompting changes in stage‐related foraging patterns. Intrinsic factors such as sex differences, or behaviours required for each stage of the annual cycle, rather than extrinsic factors related to seasonal environments, are likely to be the main proximate cause of recurring changes in behaviour between breeding stages.     

Plasticity of brood patch development and its influence on incubation periods in the yellow-eyed penguin Megadyptes antipodes: an experimental approach

In many bird species, eggs laid late in the laying period hatch after a shorter incubation period than early-laid eggs. However, the mechanisms that explain these seasonal declines in incubation periods among clutches remain poorly understood. In this study we investigated the plasticity of brood patch development during incubation in yellow-eyed penguins Megadyptes antipodes and established whether differences exist in brood patch formation among early, mean and late-breeding penguins. We also examined whether brood patch development was influenced by sex and age of birds. We then placed an artificial egg in nests a few days prior to egg laying to investigate whether the presence of an egg influences brood patch development and whether an advanced brood patch development at the time of egg laying causes declines in incubation periods. Initial brood patch width on the day the first egg was laid was dependent on sex and age, while the development of brood patch width after first egg laying was slower in early-laying birds than in mean- and late-laying birds. Initial brood patch temperature as well as temperature throughout incubation was largely dependent upon sex, whereby males had higher brood patch surface temperatures than females. Placement of an artificial egg in nests stimulated successfully brood patch development in manipulated birds, so that by the time they laid their own first egg, their brood patches were wider and had higher temperatures than those of control birds. Moreover, incubation periods of first eggs from manipulated nests were significantly shorter (43.5 days) than were those from control nests (47.3 days). Thus, variation in brood patch development and related differences in incubation temperature during early incubation could contribute to seasonal declines in incubation periods.     

Building a home from foam—túngara frog foam nest architecture and three-phase construction process

Frogs that build foam nests floating on water face the problems of over-dispersion of the secretions used and eggs being dangerously exposed at the foam : air interface. Nest construction behaviour of túngara frogs, Engystomops pustulosus, has features that may circumvent these problems. Pairs build nests in periodic bursts of foam production and egg deposition, three discrete phases being discernible. The first is characterized by a bubble raft without egg deposition and an approximately linear increase in duration of mixing events with time. This phase may reduce initial over-dispersion of foam precursor materials until a critical concentration is achieved. The main building phase is marked by mixing events and start-to-start intervals being nearly constant in duration. During the final phase, mixing events do not change in duration but intervals between them increase in an exponential-like fashion. Pairs joining a colonial nesting abbreviate their initial phase, presumably by exploiting a pioneer pair''s bubble raft, thereby reducing energy and material expenditure, and time exposed to predators. Finally, eggs are deposited only in the centre of nests with a continuously produced, approximately 1 cm deep egg-free cortex that protectively encloses hatched larvae in stranded nests.     

Dynamic risk assessment: does a nearby breeding nest predator affect nest defence of its potential victim?

There is growing evidence that birds are able to discriminate different types of nest intruders and adjust their nest defence behaviour according to intruder dangerousness and distance from the nest (the dynamic risk assessment hypothesis). Here, we tested whether birds’ decisions about nest defence may additionally be affected by an increasing familiarity with a particular nest predator. We tested nest defence responses of great reed warblers Acrocephalus arundinaceus to a nest predator, the little bittern Ixobrychus minutus. Great reed warbler nests located close (≤7 m) to synchronously breeding little bitterns were “neighbour”, other nests were “solitary”. Great reed warbler specific aggression towards a little bittern dummy was much lower (~5-times) at neighbour than solitary nests. In contrast, generalised responses to a control innocuous intruder (the turtle dove, Streptopelia turtur) were statistically identical at neighbour and solitary nests. These patterns are in line with dynamic risk assessment hypothesis. We hypothesise that decreased great reed warbler aggression at neighbour nests also represents a specific behavioural adaptation to nesting in association with the little bittern. Little bitterns breeding closer to great reed warblers showed decreased risks of failure due to predation. However, further research is needed to experimentally test the causal links behind these patterns.     

The effect of human observers on the intensity of nest predation

Disused nests containing eggs from aviary birds were used to determine the effect of human observers on the intensity of nest predation. Nest predation was significantly higher for nests visited daily than for nests visited only at the end of a typical incubation period. Care should be taken by nest observers to minimise the number of visits to nests of ground-nesting birds. The average distance of nests from the edge of the supporting plant was greater for unsuccessful than successful nests, implying that the position of nests is an important factor affecting their survival. Predation rates on active nests of White-fronted Chats Ephthianura albifrons visited daily over the same period were similar to those of experimental nests, suggesting that 'artificial' nests may be a useful tool for studying nest predation.     

桂西南褐翅鸦鹃的孵卵行为与节律

2016年3~6月,在广西西南部龙州县弄岗村(22°26′35.20′′~22°30′46.90′′N,106°57′46.35′′~107°03′32.99′′E),通过野外观察和自动温度记录仪相结合的方法对褐翅鸦鹃(Centropus sinensis)的孵卵行为与节律进行了研究。结果表明,1)褐翅鸦鹃边筑巢边产卵,每2 d产1枚卵,卵长径和短径分别为(36.11±0.42)mm和(28.46±0.38)mm,卵重(16.35±0.51)g(n=44枚)。窝卵数3~5枚,孵卵期为(16.75±1.65)d(n=4巢),孵化率为45.45%(n=44枚)。孵卵期与窝卵数之间无显著相关性(r=0.865,P0.05);2)白天双亲共同参与孵卵,夜晚则由其中1只负责。夜间亲鸟的在巢时间从19时左右持续至翌日晨6时左右;3)亲鸟采取离巢次数少和离巢时间长的孵卵策略。亲鸟日活动时间在700 min以上(n=45 d),日离巢次数为(8.82±0.34)次(n=45 d),平均每次离巢持续时间为(52.91±2.35)min(n=397次),每次离巢持续时间与环境温度呈显著负相关关系(r=﹣0.113,P0.05);4)巢内平均孵卵温度为(31.7±0.3)℃(n=4巢),随孵卵天数增加而增加,并与环境温度(最高温r=0.566,最低温r=0.537,平均温r=0.706,P0.01)和日活动时间正相关(r=0.506,P0.01);5)有延迟孵卵行为。延迟孵卵期间夜晚巢内最低温是22.1℃。在桂西南北热带气候环境中,高的环境温度是保障褐翅鸦鹃孵卵成功的主要因素之一。     

It costs to be clean and fit: energetics of comfort behavior in breeding-fasting penguins

Background

Birds may allocate a significant part of time to comfort behavior (e.g., preening, stretching, shaking, etc.) in order to eliminate parasites, maintain plumage integrity, and possibly reduce muscular ankylosis. Understanding the adaptive value of comfort behavior would benefit from knowledge on the energy costs animals are willing to pay to maintain it, particularly under situations of energy constraints, e.g., during fasting. We determined time and energy devoted to comfort activities in freely breeding king penguins (Aptenodytes patagonicus), seabirds known to fast for up to one month during incubation shifts ashore.

Methodology/Principal Findings

A time budget was estimated from focal and scan sampling field observations and the energy cost of comfort activities was calculated from the associated increase in heart rate (HR) during comfort episodes, using previously determined equations relating HR to energy expenditure. We show that incubating birds spent 22% of their daily time budget in comfort behavior (with no differences between day and night) mainly devoted to preening (73%) and head/body shaking (16%). During comfort behavior, energy expenditure averaged 1.24 times resting metabolic rate (RMR) and the corresponding energy cost (i.e., energy expended in excess to RMR) was 58 kJ/hr. Energy expenditure varied greatly among various types of comfort behavior, ranging from 1.03 (yawning) to 1.78 (stretching) times RMR. Comfort behavior contributed 8.8–9.3% to total daily energy expenditure and 69.4–73.5% to energy expended daily for activity. About half of this energy was expended caring for plumage.

Conclusion/Significance

This study is the first to estimate the contribution of comfort behavior to overall energy budget in a free-living animal. It shows that although breeding on a tight energy budget, king penguins devote a substantial amount of time and energy to comfort behavior. Such findings underline the importance of comfort behavior for the fitness of colonial seabirds.     

Embryonic developmental patterns and energy expenditure are affected by incubation temperature in wood ducks (Aix sponsa)

Recent research in birds has demonstrated that incubation temperature influences a suite of traits important for hatchling development and survival. We explored a possible mechanism for the effects on hatchling quality by determining whether incubation temperature influences embryonic energy expenditure of wood ducks (Aix sponsa). Because avian embryos are ectothermic, we hypothesized that eggs incubated at higher temperatures would have greater energy expenditure at any given day of incubation. However, because eggs incubated at lower temperatures take longer to hatch than embryos incubated at higher temperatures, we hypothesized that the former would expend more energy during incubation. We incubated eggs at three temperatures (35.0°, 35.9°, and 37.0°C) that fall within the range of temperatures of naturally incubated wood duck nests. We then measured the respiration of embryos every 3 d during incubation, immediately after ducks externally pipped, and immediately after hatching. As predicted, embryos incubated at the highest temperature had the highest metabolic rates on most days of incubation, and they exhibited faster rates of development. Yet, because of greater energy expended during the hatching process, embryos incubated at the lowest temperature expended 20%-37% more energy during incubation than did embryos incubated at the higher temperatures. Slower developmental rates and greater embryonic energy expenditure of embryos incubated at the lowest temperature could contribute to their poor physiological performance as ducklings compared with ducklings that hatch from eggs incubated at higher temperatures.     

Variable energetic responses to clutch size manipulations in white-throated dippers Cinclus cinclus

We used the doubly-labelled water technique to measure daily energy expenditure (DEE) of a free-living uniparental incubator, the white-throated dipper Cinclus cinclus , in Scotland. DEE was 205±8 (s.e.m.) kJ d⁻¹ for 17 females incubating their natural clutch sizes, equivalent to 3.2±0.1×basal metabolic rate (BMR). To investigate the influence of clutch size on the energy budget, we measured the DEE of 14 females with clutches increased or reduced by a single egg. Birds with reduced clutch sizes had an energy expenditure with a mean and variance that did not differ from those of birds with unmanipulated clutches. Enlarging the clutch led to an increase in energy expenditure to over 4×BMR for some individuals but not for others, resulting in greater variance in energy expenditure for birds with enlarged clutches. Individual variation in energy expenditure could not be fully explained by environmental conditions, by patterns of behaviour or clutch size. Incubating females received a maximum of only 4 kJ d⁻¹ (2% of DEE) from provisioning by the male, and mobilised up to 6 kJ d⁻¹ (3% of DEE) from reserves. Females spent 2.9±0.2 h (n=20) away from the nest each day, so a foraging rate of 95 kJ h⁻¹ was required during incubation recesses to balance DEE. This 'required foraging rate' is double previous estimates of the maximum rates of energy acquisition for birds of this size. We suggest that the greater likelihood of a raised energy expenditure associated with larger clutches, combined with the difficulties in maintaining energy supplies, may constitute a constraint on avian clutch size.     

Incubation energetics of the Laysan Albatross

Summary The energy expenditure of incubating and foraging Laysan Albatross (Diomedea immutabilis, mean body weight 3.07 kg) was estimated by means of the doubly-labelled water technique. During incubation, the energy expenditure was similar to that of resting birds that were not incubating an egg. The energy expenditure of foraging albatross (2072 kJ/day) was 2.6 times that of resting birds. It was concluded that the energy expenditure of the tropical Laysan Albatross was not less than that of species foraging over cold, high-latitude oceans. An energy budget compiled for an incubating pair of albatross revealed that the energy expenditure of the female was greater than that of the male bird, during the incubation period.     

Brent goose <Emphasis Type="Italic">Branta bernicla bernicla</Emphasis> feeding behaviour during incubation,Taïmyr Peninsula,Russia

Incubating birds must balance the time and the energy invested in incubation with the energy acquisition for their survival. Many factors such as weather and predation influence this trade-off. In Arctic geese, only females incubate, and they leave the nest regularly to feed while males invest in keeping their nests and mates safe. This study conducted on Big Bird Island (Taïmyr Peninsula) during the summer of 2004 examined the incubation behavior of dark-bellied brent geese Branta bernicla bernicla to assess the effect of date, period of day and weather conditions on the incubation and feeding behaviors of females and males. Females were at their nests only for 65% of the total time observed. This very low value, compared to other goose species, could be the result of the combined effects of good weather conditions, low predation pressure and opportunities to feed close to the nest. We found differential adjustments of male and female behaviors. Females appeared to focus on the trade-off between feeding and incubating, in relation to weather conditions, and on their own energy balance. Males appeared to respond primarily by the absence of the female from their nest.     

Protective nesting association between the Barred Warbler Sylvia nisoria and the Red-backed Shrike Lanius collurio: an experiment using artificial and natural nests

The pressure of predators may significantly affects the distribution pattern of nesting birds. Some individuals may reduce the risk of predation by nesting near other species with an aggressive nest defence. In the present study I tested the predator protection hypothesis using experimental (artificial nests) and observational (real nests) approaches on two ecologically similar passerine birds–the Barred Warbler Sylvia nisoria and the Red-backed Shrike Lanius collurio. Studies have been conducted in eastern Poland in two types of habitat: river valley and farmland. The main predators of natural and artificial nests were birds, and to a lesser extent, also mammals. I found wide variation level of predation of both types of nests in different years. Nest survival rate of artificial nests was significantly lower in the farmland than in the river valley and in natural nests I observed reverse pattern. According to the predictions of the predator protection hypothesis the survival rates of the natural and artificial nests were significantly higher in territories of individuals breeding in the protective nesting association. This type of interspecific positive interaction between two associate species can be classified as facultative mutualism.     

Diving behaviour differs between incubating and brooding Brünnich's guillemots, Uria lomvia

Bird-borne data loggers were used to investigate the foraging strategies of Brünnich's guillemots breeding in a colony in the North Water Polynya: the flight performance and diving activity of incubating birds were compared to those of chick-rearing individuals. No significant differences were recorded between the bird groups in the potential foraging range. Conversely, clear differences were revealed between incubating and chick-rearing birds in diving behaviour. Chick-rearing birds were generally foraging at a significantly greater depth, and spent significantly higher proportions of the time submerged, than brooding individuals. Despite these differences, the estimated average daily energy expenditure of chick-rearing Brünnich's guillemots was only about 6% higher than that during incubation.