Egg Neglect Research Articles

Comparative egg attendance patterns of incubating polar petrels

BackgroundThe internal environment of eggs in most birds is regulated by transferring heat energy through contact incubation, maintaining nest microclimate, and frequent egg turning by the incubating parent on its nest. However, we lack information about egg attendance patterns in birds that breed in polar environments where variations in life history are expected to influence incubation behavior. Moreover, crevice/burrow nesting petrels in high-latitude regions are known for periodically leaving their egg unattended (hereafter ‘egg neglect’), but there is little reporting on the internal condition of unattended eggs. At Dumont d’Urville Station, Antarctica, we studied the incubation behavior of 24 snow (Pagodroma nivea) and 15 Cape (Daption capense) petrel pairs using egg loggers that recorded egg turning rates, orientation changes, and temperatures at 1 Hz for durations of 3–6 days.ResultsEgg turning frequency (1.31 ± 0.33 vs. 1.38 ± 0.39 turns h−1), angle change per turn (43.1 ± 43.2 vs. 48.6 ± 43.7° turn−1), and egg temperature (34.1 ± 2.3 vs. 34.1 ± 2.0 °C) were nearly identical for snow and Cape petrels, respectively. However, egg neglect was only observed in snow petrel nests (based on egg temperature changes) where loggers recorded mean durations of 1.34 ± 1.15 days (maximum duration of 3.63 days). During periods of neglect, eggs cooled to 5.5 ± 1.8 °C over an average of 91 min, but were rewarmed by parents in only 76 min at a rate of 0.33 °C min−1.ConclusionsEgg temperatures of both species during regular incubation were within 1–2 °C of other high-latitude petrel species, but neglected snow petrel eggs remained several degrees above freezing, which was likely attributed to crevice nesting where neglected eggs are buffered by environmental conditions. Using egg rewarming rates, thermal capacity of eggs, and published metabolic rates, we estimate egg rewarming costs in snow petrels to be 1.5 to 1.9 × BMR. Excluding egg neglect periods, turning rates for both petrel species were lower than other seabirds studied using biologging devices, which may be associated with the prolonged incubation periods that are characteristic of procellariiform seabirds.

Evidence of incubation trade‐offs in Leach's Storm‐Petrel (Oceanodroma leucorhoa): ptilochronology as a measure of reproductive investment in a long‐lived seabird

Avian incubation investment represents a trade‐off between the energetic demands of the parent and the thermal needs of the embryo. Parental energy balance and investment in somatic maintenance relative to incubation investment can be indexed by the rate of feather growth. Feather growth rates, or ptilochronology, of adult Leach's Storm‐Petrels Oceanodroma leucorhoa were used to assess parental investment to (1) determine whether individuals that invest heavily in current reproduction pay a cost for future reproduction as indicated by a cost for somatic maintenance and (2) assess whether this trade‐off is detected using ptilochronology, which may be a more direct measure of reproductive investment compared with body mass in seabirds. We found positive relationships between duration of the incubation period and both egg neglect and a mated pair's mean rate of induced feather growth, although we did not find a relationship between either egg neglect and feather growth or hatching success and feather growth. Our results suggest that during the incubation period a trade‐off exists between energy allocated to self‐maintenance and reproduction in this species, although egg neglect does not appear to be the mechanism that extends the incubation period in response to increased energetic demands of somatic maintenance. The lack of correlation between feather growth and egg neglect further suggests that some pairs may be better able to manage competing demands of self‐maintenance and incubation, possibly due to individual quality, coordination of incubation effort, burrow quality or some other factor.

Does short-term fasting lead to stressed-out parents? A study of incubation commitment and the hormonal stress responses and recoveries in snow petrels

The hormonal stress response is flexible and can be modulated by individuals according to its costs and benefits. Therefore, it is predicted that parents in poor body condition should modify their hormonal stress response, and thus, redirect energy allocation processes from parental care to self-maintenance when stressors occur. To test this prediction, most studies on free-living vertebrates have only focused on the stress response while the stress recovery – how quickly hormonal levels return to baseline values – has been neglected. Moreover, most studies have only focused on corticosterone – the primary mediator of allostasis – without paying attention to prolactin despite its major role in mediating parental behaviors. Here, we examined the effect of a short-term fasting event on the corticosterone and prolactin stress responses and recoveries, and we subsequently explored their relationships with parental decision in the snow petrel (Pagodroma nivea). By comparing the hormonal profiles of fasting and non-fasting snow petrels, we showed that parents modulate their corticosterone (but not prolactin) stress response according to their energetic status. We also described for the first time the hormonal stress recoveries in wild birds and found that they did not differ between fasting and non-fasting birds. Importantly, egg neglect was negatively correlated with circulating prolactin but not corticosterone levels in this species, demonstrating therefore a complex link between body condition, parental behavior and circulating corticosterone and prolactin levels. We suggest that both corticosterone and prolactin play a major role in the way parents adjust to stressors. This multiple signaling may allow parents to fine-tune their response to stressors, and especially, to activate specific allostasis-related mechanisms in a timely manner.

Corticosterone, prolactin and egg neglect behavior in relation to mercury and legacy POPs in a long-lived Antarctic bird

Seabirds often have high loads of contaminants. These contaminants have endocrine disrupting properties but their relationships with some endocrine mechanisms are still poorly investigated in free-living organisms. This is the case for the stress response which shifts energy investment away from reproduction and redirects it towards survival. In birds, this stress response is achieved through a release of corticosterone and is also accompanied by a decrease in circulating prolactin, an anterior pituitary hormone widely involved in regulating parental cares. We measured blood concentrations of some legacy persistent organic pollutants (POPs) and mercury (Hg) and examined their relationships with the corticosterone and prolactin responses of known-age (9–46years old) incubating snow petrels (Pagodroma nivea) to a standardized capture/handling stress protocol. In this Antarctic seabird, we also investigated whether high contaminant burden correlates with a higher occurrence of egg neglect, a frequently observed behavior in snow petrels. POPs and Hg were unrelated to age. Stress-induced corticosterone concentrations were positively related to POPs in both sexes, and stress-induced prolactin concentrations were negatively related to Hg in males. Egg-neglect behavior was not related to POPs burden, but males with higher Hg concentrations were more likely to neglect their egg. This suggests that in birds, relationships between age and contaminants are complex and that even low to moderate concentrations of POPs and Hg are significantly related to hormonal secretion. In this Antarctic species, exposure to legacy POPs and Hg could make individuals more susceptible to environmental stressors such as ongoing disturbances in Polar Regions.

Parental Behavior Controls Incubation Period and Asynchrony of Hatching in Magellanic Penguins: Reply to Demongin, Poisbleau and Eens (2013)

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

Incubation routine, duration of foraging trips and regulation of body mass in Short-tailed Shearwaters (Ardenna tenuirostris)

The energy demands of incubation can present important costs in avian reproduction. In species where incubation is shared, the time that individuals have for foraging may be influenced by their own foraging success and their partner's ability to fast while incubating. To investigate the costs of incubation, 60 pairs of Short-tailed Shearwaters (Ardenna tenuirostris) were studied on Great Dog Island, Tasmania, to determine ifbody mass influences incubation routines, duration of foraging trips and neglect of eggs. Body mass throughout the incubation period varied considerably, with birds losing an average of 20% of their original body mass as a result of complete fasting while on land. Initial body mass of males was positively correlated with time spent incubating, and heavier birds had the ability to extend their incubation shift if their partner was delayed or failed to return from sea. The body mass when birds left the nest to return to sea was associated with days spent foraging, and was inversely related to the mass gained at sea. Temporary egg neglect was observed in both successful and unsuccessful breeding attempts, but increased the risk of breeding failure. No specific mass threshold at which birds left the nest if not relieved by their partner could be determined. Avian reproduction represents a trade-off in use of resources between current survival and reproductive investment. The results suggest that body mass during incubation plays an important role in the reproductive behaviour of Short-tailed Shearwaters, enabling adults to regulate the trade-off between risks of adult mortality and breeding failure.

Incubation Patterns in a Central-Place Forager Affect Lifetime Reproductive Success: Scaling of Patterns from a Foraging Bout to a Lifetime

BackgroundLong-lived seabirds face a conflict between current and lifelong reproductive success. During incubation shifts, egg neglect is sometimes necessary to avoid starvation, but may compromise the current reproductive attempt. However, factors underlying this decision process are poorly understood. We focus on the ancient murrelet, Synthliboramphus antiquus, an alcid with exceptionally long incubation shift lengths, and test the impact of environmental factors on incubation shift length in relation to reproductive success.Methodology/Principal FindingsUsing an information theoretic approach, we show that incubation shift length was a strong predictor of reproductive success for ancient murrelets at Reef Island, Haida Gwaii, British Columbia, Canada during the 2007 and 2008 breeding seasons. The most important factors explaining an individual's shift length were egg size, wind speed and the length of the mate's previous shift. Wind speed and tide height were the two most important factors for determining foraging behavior, as measured by dive frequency and depth.Conclusions/SignificanceOur study demonstrates that (i) species-specific reproductive strategies interact with environmental conditions such as wind speed to form multiple incubation patterns and (ii) maintaining regular incubation shifts is an essential component of reproductive success.

The Tristan ThrushNesocichla eremitaas Seabird Predator

Tristan Thrushes or Starchies Nesocichla eremita are known to feed on seabird eggs. We show they are able to open the eggs of birds as large as small albatrosses. Starchies were involved in almost half of all egg losses by Great Shearwaters Puffinus gravis during the early incubation period in a small study colony at Inaccessible Island, South Atlantic Ocean. They also enter burrows to remove and kill petrel chicks up to at least 70 g. Starchies are thus potentially significant predators of seabird eggs and chicks, and may select against egg neglect and early cessation of brooding by burrowing petrels at the Tristan islands. Starchies previously were recorded killing adult White-bellied Storm Petrels Fregetta grallaria at Inaccessible Island. This behaviour now includes White-faced Storm Petrels Pelagodroma marina. It is likely that the Starchies hunt adult storm petrels directly, taking them from their burrows.

Variation in the onset of incubation and its influence on avian hatching success and asynchrony

Variation among species in the onset of incubation has been attributed to differences in life history traits, and variation within species has been related to individual and environmental factors. We quantified within- and among-species variation in the onset of incubation in five cavity-nesting passerines, using a continuous record of diurnal and nocturnal incubation from clutch initiation through completion. We documented 11 potential patterns for the onset of incubation and showed that onset patterns were significantly related to hatching success. The onset of diurnal partial incubation and nocturnal full incubation generally occurred before diurnal full incubation, which started around clutch completion. Increases in precipitation or wind speed significantly delayed most types of incubation onset, supporting predictions of the energy constraints hypothesis. Ancillary predictions of rain and wind disproportionately delaying incubation for aerial foragers, and for species with male feeding during incubation, were not upheld. Larger clutch size accelerated the timing of full incubation onset in diurnal and nocturnal full incubation, supporting predictions of the egg viability hypothesis. Predictions of both hypotheses for the effects of minimum temperature, proportion of time above 24 °C, and seasonality on incubation onset were not supported. We observed egg neglect for up to 4 days or nights; neglect was more common at night, and consecutive nights of neglect occurred during nocturnal full incubation. Egg neglect did not significantly affect hatching success or incubation period. In conclusion, the timing of incubation onset was strongly affected by environmental and individual factors, and patterns of incubation onset affected hatching success.

Egg neglect under risk of predation in Cassin’s Auklet (Ptychoramphus aleuticus)

We tested predictions concerning the significance of egg neglect for the burrow-nesting seabird Cassin’s auklet (Ptychoramphus aleuticus (Pallas, 1811)) at a colony where endemic Keen’s mice (Peromyscus keeni Merriam, 1897) depredate unattended eggs. A video-camera probe was used to monitor neglect and predation in 32 burrows, and mass loss of incubating adults was measured in 12 separate burrows. Incubating birds lost 8.1% of their body mass over obligate 24 h incubation shifts, suggesting that incubation is costly. In response, most pairs (79%) neglected their egg at least once. As predicted, rates of neglect decreased as incubation progressed, and the costs of neglect increased. Rates of neglect increased during periods of strong winds, which create poor foraging conditions at sea. Contrary to predictions, rates of neglect did not increase when burrows were colder and self-maintenance costs were higher. Neglect was risky in that rates of egg loss by predation increased with frequency of neglect. Increased neglect early in incubation and during periods of poor foraging conditions, despite high rates of predation on neglected eggs, is consistent with the existence of a fitness trade-off between costs and benefits of neglect.

Age‐specific reproductive success in a long‐lived bird: do older parents resist stress better?

In many vertebrates, reproductive performance increases with advancing age but mechanisms involved in such a pattern remain poorly studied. One potential mechanism may be the hormonal stress response, which shifts energy investment away from reproduction and redirects it towards survival. In birds, this stress response is achieved through a release of corticosterone and is also accompanied by a decrease in circulating prolactin, a hormone involved widely in regulating parental cares. It has been predicted that, when the value of the current reproduction is high relative to the value of future reproduction and survival, as it is expected to be in older adults, the stress response should be attenuated to ensure that reproduction is not inhibited. We tested this hypothesis by measuring the corticosterone and prolactin responses of known-age (8-36 years old) incubating snow petrels (Pagadroma nivea) to a standardized capture/handling stress protocol. We also investigated whether an attenuation of the stress responses will correlate with a lower occurrence of egg neglect, a frequently observed behaviour in snow petrels. The probability of successfully fledging a chick increased from 6 years to 12 years before stabilizing after 12 years of age. Corticosterone response to stress was unaffected by age. Prolactin response to stress, however, was influenced clearly by age: in both sexes older breeders had higher stress-induced prolactin levels than younger ones. This was due to an increasing attenuation of the prolactin response to stress with advancing age in females, and in males this was due to a probably higher intrinsic capacity of older males to secrete prolactin. Moreover, higher stress-induced prolactin levels were correlated with a lower probability of neglecting the egg. In young breeders, the combination of a robust corticosterone increase with a lower ability to maintain prolactin secretion during acute stress is probably one of the functional causes of their lower incubation commitment. We suggest that the ability to maintain a threshold level of prolactin during a stressful situation may be an important physiological mechanism involved in the improvement of reproductive performance with advancing age in long-lived birds.

The breeding biology of the White-faced Storm Petrel (Pelagodroma marina) on Mud Islands, Port Phillip Bay, Victoria

The White-faced Storm Petrel (Pelagodroma marina) is restricted to three breeding colonies within Victoria: Mud Islands and South Channel Fort in Port Phillip Bay, and Tullaberga Island off Mallacoota. Numbers of these storm petrels breeding on Mud Islands have declined considerably since early last century. White-faced Storm Petrels were recorded on Mud Islands from early September 2002 until mid-March 2003 when the last chicks fledged. Eggs were laid from late October to early December, with chicks hatching in the later half of December. The mean incubation period was 51.7 days (± 3.2 days (s.d.), range = 38–53, n = 13), and may have been extended by periods of egg neglect. The mean nestling period was 54.8 days (±. 4.4 days (s.d.), range 50–70, n = 21). Chick growth is described. Hatching success was 54% and fledging success was 77.8%, with overall breeding success being 42%. Burrow densities were found to be influenced by plant species, vegetation height and soil moisture. The position of the burrow within the colony was shown to influence breeding success, with those nearer the edge of the storm petrel colony, closer to the marsh, and further from a colony of Australian White (Threskiornis molucca) and Straw-necked (T. spinicollis) Ibis recording higher success.

Nocturnal Egg Neglect and Prolonged Incubation in the Red-necked Grebe

Miniaturized temperature loggers placed in Red-necked Grebe (Podiceps grisegina) nests revealed that 16 of the 32 monitored pairs abandoned their nests for extended periods lasting 3-9 h during at least two of the three nights that they were monitored. When incubating pairs left their nests unattended, temperatures of the thermistored egg usually dropped precipitously to below 30°C within 15-25 min. Duration of a pair’s incubation period was positively associated with the number of minutes that the thermistored egg was below 30°C in our 3-day samples, yet nesting success remained high. Embryos appeared to be tolerant of this cooling; 26 of the 32 monitored nests hatched young, and there was no detectable increase in the failure of eggs to hatch for pairs neglecting their clutches more than 3 h per night. We suggest Red-necked Grebes preemptively leave their nests at night to avoid predation on their eggs or themselves.

Predation on Rhinoceros Auklet Eggs by a Native Population of Peromyscus

Predation by Keen's mice (Peromyscus keeni) was the single greatest cause of egg loss for Rhinoceros Auklets (Cerorhinca monocerata) at the seabird colony on Triangle Island, British Columbia in 1998. Despite studies suggesting that gape-limited ro- dents are unable to open large eggs, mouse depredation was likely responsible for the loss of more eggs than all other causes combined, with mice commonly open- ing and eating eggs of nearly twice their mass. In one study plot, mice depredated up to 34% of eggs. This high predation rate is likely related to temporary egg neglect by foraging parents. We suggest that egg dep- redation may increase in years of low marine produc- tivity, when adults increase foraging time.

Hypothermic tolerance in an embryonic American kestrel (Falco sparverius)

Embryos of several bird species tolerate acute hypothermia. However, the extent to which it can be tolerated by wild species living under natural conditions is poorly documented. At a single American kestrel (Falco sparverius) nest 15 days into incubation, we observed a 21-h bout of egg neglect by the parents during which nest (egg) temperature averaged 12.7°C. Normal incubation patterns resumed thereafter, and one of three viable eggs hatched 32 days after incubation onset, an incubation period 2.5 days longer than the mean in this study. The nestling appeared to develop and fledge normally. Although embryonic tolerance of extended hypothermia is known to occur in some seabirds, its presence in Falconiformes has not heretofore been recorded. Embryonic hypothermic tolerance may be adaptive in species with extended periods of parental absence during incubation.

Breeding ecology of the FulmarFulmarus glacialisand the KittiwakeRissa tridactylain high‐arctic northeastern Greenland, 1993

The breeding ecology of the FulmarFulmarus glacialisand the KittiwakeRissa tridactylain the high Arctic was studied in relation to the occurrence of the northeast water polynya in northeasternmost Greenland (80d̀N). Mean laying dates were 31 May in the Fulmar and 18 June in the Kittiwake; the total nesting season for the Fulmar just matched the time window of the polynya opening period. Fulmar colony attendance fluctuated within a period of 11.6 days because of variation in nonbreeding prospectors but showed no clear diurnal variation. Fulmar incubation shifts, on average, lasted 6.1 days (range 1–13 days), which is significantly longer than elsewhere, and the average chick‐guard period of 10.9 days (range 1–17 days) was significantly shorter than in other studies. Egg neglect occurred in 18% of Fulmar nests or 0.7% of nests per day. Overall breeding success (chicks fledged per egg laid) was 0.56 in the Fulmar and 0.67 in the Kittiwake; the latter produced 1.4 young per active nest or 1.2 per completed nest. Mean Kittiwake clutch size was 2.03; larger clutches were laid early. Nest site characteristics (presumably reflecting nest predation risk) and breeding behaviour affected breeding success. in the Fulmar, hatching success was negatively correlated with laying date and the proportion of egg neglect, while overall breeding success was correlated negatively with distance to nearest neighbouring site and positively with the length of the chick‐guard period. Kittiwake breeding success was negatively correlated with laying date. Using seabirds as indicators of marine food supply, breeding success in both species suggested moderate to good food supply in the northeast water polynya in 1993, although at least in the Fulmar the high reproductive output appeared partly maintained by behavioural buffering; long incubation shifts, egg neglect and short chick‐guard periods were symptoms of foraging constraints.

Incubation routine, body mass regulation and egg neglect in the Blue Petrel Halobaena caerulea

The incubation routine and mass changes of male and female Blue Petrel Halobaena caerulea were studied at the Kerguelen Islands to investigate factors influencing the durations of incubation stints and foraging trips at sea and the factors determining nest desertion and return to the nest.The body mass at the start of an incubation shift and also when the bird was relieved varied throughout the incubation period, whereas the mass when birds deserted the nest was stable. Birds deserted the nest when their mass decreased to threshold, independent of the duration of the fast. Temporary egg neglect was observed in successful as well as in unsuccessful breeding attempts, but it increased the risk of breeding failure. The net and daily massgained at sea during the second part of the incubation period were higher than during the first part, suggesting an increase in food availability. During the first part, the mass gained at sea and time spent foraging were inversely related to the mass of the bird before it left the burrow, whereas a similar relationship did not occur thereafter.The results suggest the occurrence of a fixed mass threshold when birds decide to leave the nest if not relieved by their partner. The mass when a bird left its nest inffuenced the time spent foraging or mass gained when food was scarce. Although decision rules to leave the nest or return from the sea are related to body condition. the possibility of neglecting the eggs temporarily enables Blue Petrels to regulate the trade‐off between risks of breeding failure and risks of an increase in adult mortality. A model for behavioural decision to stop incubating or stop feeding, based on a variable set point, is proposed.

Consequences of Nest Desertion and Inattendance for Magellanic Penguin Hatching Success

Consequences of Nest Desertion and Inattendance for Magellanic Penguin Hatching Success

Embryo Metabolism and Egg Neglect in Cassin's Auklets

Incubation attendance by Cassin's Auklets (Ptychoramphus aleuticus) was determined by daily nest monitoring. The incidence of natural egg neglect was highest during the first third of the incubation period (incubation length of 38 days when parents were continuously present) and lowest between 12 and 25 days after laying. The latter corresponds to the period of most rapid embryonic growth rate. The pattern of auklet embryo metabolism is similar to that of other precocial species with prolonged incubation periods, with two differences: unpipped auklet embryos show their most rapid rise in metabolic rate relatively earlier in the incubation period. Auklet embryos have an unusually long plateau (10 days) in metabolic rate before beginning pipping. A rapid increase in metabolism is coincident with the five- to seven-day hatching process. Embryos surviving chilling had lower metabolic rates (after rewarming) than continuously incubated eggs of the same chronological age. The reduction of metabolic rate and resulting retarded development may account for the prolonged duration of incubation observed for both naturally and experimentally neglected auklet eggs.

Effects of low incubation temperatures during the pipped egg stage on hatchability and hatching times in domestic chickens and ring-billed gulls

Gulls and some other species of birds are known to neglect pipped eggs that remain within the clutch after the first egg(s) hatch. I examined the effects of incubation neglect at this stage of development by cooling eggs in the laboratory. Domestic white leghorn chicken (Gallus gallus) eggs had significantly reduced hatchability and delayed hatch times when incubated at 30 or 27 °C from pipping until hatching. Cyclic cooling for 4 or 7 h out of every 8-h period produced intermediate effects. Pip-to-hatch interval was delayed by as much as 60% in ring-billed gull (Larus delawarensis) eggs incubated from pipping onwards at 33 °C. To the extent that the laboratory results can be extrapolated to natural incubation, results suggest that egg neglect and low incubation temperatures during the critical final stages of hatching could have adverse effects upon the last egg(s) to hatch within a clutch. Depending on the species, low temperature and retardation could increase chances that a late-hatched young will be left behind when the rest of the brood leaves the nest. Where the hatch is typically asychronous, low incubation temperatures after the first eggs begin to hatch could increase the degree of asynchrony and hence the competitive disadvantage of the last-hatched young.