Patterns of breeding behaviour and plasma levels of hormones in a free-living population of Pied flycatchers, Ficedula hypoleuca

Plasma levels of luteinizing hormone (LH) and steroid hormones were measured by radioimmunoassay in a series of plasma samples collected from a free-living population of Pied flycatchers, Ficedula hypoleuca. Both males and females have similar circulating levels of LH and testosterone when they arrive in the breeding area. However, as territories and pair bonds are established, and as courtship and nest-building ensue, the plasma levels of testosterone in males become elevated over those of females, although a lesser peak also occurs in females. As the egg laying phase and incubation begin, plasma levels of LH and testosterone decline sharply in both sexes. On the other hand polyterritorial males, that establish secondary territories, maintain higher levels of LH and testosterone than males remaining in the home-territory, at least until they return to the home-territory, usually at the middle part of the incubation period. By this time polyterritorial males also have basal levels of these hormones. Curiously, females on home-territories show a small, but significant, rise of circulating LH and testosterone at the time the males return.
In males, plasma levels of corticosterone are elevated from the time of arrival on the breeding grounds until the end of the nest-building period. Thereafter corticosterone levels decline in males staying on the home-territory but remain elevated in polyterritorial males until the latter return to the home-territory. In contrast, circulating levels of corticosterone in females are only elevated for brief period during egg laying.     

Modulation of gonadotrophin and prolacrin secretion by daylength and breeding behaviour in free-living starlings, Sturnus vulgaris

Plasma levels of luteinizing hormone (LH), follicle-stimulating hormone (FSH) and prolactin were measured by radioimmunoassay in plasma samples collected from free-living starlings, Sturnus vulgaris , trapped in nest-boxes. By leaving some nest-boxes undisturbed, and repeatedly destroying nests in others, birds from a single-brooded population were trapped whilst nest-building, incubating or feeding nestlings, at different times throughout the normal breeding season. In both males and females trapped whilst nest-building, plasma LH and prolactin levels increased progressively from mid March until late May. In females sampled during incubation, LH and FSH levels were high throughout May but decreased in early June. Prolactin levels were highest in late May. In both males and females trapped during mid May, LH levels were highest in these birds which were nest-building at this time and lowest in those feeding nestlings, FSH did not change significantly, and prolactin was low in those birds which were nest-building and high in those incubating or feeding nestlings. In female starlings from a double-brooded population, levels of LH and FSH were much lower whilst feeding the second brood than when feeding the first brood, whereas prolactin levels were similar. The results suggest that incubation and feeding behaviour inhibit the increase in LH secretion caused by increasing daylength, but stimulate prolactin secretion in excess of that caused by increasing daylength.     

Plasma levels of prolactin and gonadal steroids in relation to multiple-brooding and renesting in free-living populations of the song sparrow, Melospiza melodia

Plasma levels of testosterone (T), estradiol (E2), and prolactin were measured in samples collected from free-living song sparrows, Melospiza melodia. In males, plasma levels of T were elevated early in the season when territories were established and when females laid the first clutch of eggs. Thereafter, T levels declined and remained low throughout the remainder of the breeding cycle. However, if the first brood was lost to a predator, or by experimental removal of the nest, plasma levels of T increased as renesting, to replace the clutch, occurred. Circulating levels of prolactin in males began to rise during the egg-laying stage of the first brood, reached a maximum toward the end of the incubation stage, remained elevated until breeding was terminated, and then declined throughout the moulting stage to basal values in October. Prolactin levels remained high throughout the breeding season irrespective of whether a brood was raised successfully or whether the nest was lost and renesting occurred. In females, plasma levels of E2 were elevated prior to the egg-laying stage for each brood as is typical of multiple-brooded species. However, prolactin titers rose dramatically during egg-laying for the first clutch (slightly higher than in males) and were maximal by onset of incubation. Only females of this species incubate, although males do feed young. As in males, plasma prolactin in females remained high between broods and during experimentally induced renesting, and then declined to basal by the end of the moult stage in October. These data suggest that there are no differences in the temporal patterns of prolactin concentrations in blood between multiple-brooding and renesting. In a separate experiment, captive male song sparrows were transferred from a short day to artificial long days (18L 6D) and a control group was maintained on 9L 15D. In the long-day group, prolactin levels rose abruptly over the first 20 days, as the testes developed, and remained high well into postnuptial moult after the gonads had regressed. Prolactin remained basal in the control group. These data suggest that the temporal pattern of circulating prolactin levels throughout the breeding season is regulated at least partly by changing photoperiod. However, nonphotoperiodic factors are also important since photoperiodically induced increases in prolactin are significantly less than those seen in free-living individuals. These differences may be related to parental behavior.     

Predation by sparrowhawks Accipiter nisus on male and female pied flycatchers Ficedula hypoleuca in relation to their breeding behaviour and foraging

Bright plumage, song display, and aggressive resource defence in males may cause higher predation on males than on females during the breeding season. However, in birds, higher predation on females is sometimes observed. Parental investment may be high in females (egg-laying, incubation and feeding of offspring), which might lead to a high risk of predation. We studied predation by sparrowhawks Accipiter nisus in relation to behaviour in pied flycatchers Ficedula hypoleuca where breeding males are more conspicuous than females in plumage and behaviour. Male pied flycatchers generally occupied more exposed perches than females. Females were more mobile and foraged more than males, especially prior to and during incubation. During the incubation and nestling stages, when predation on the sexes could be directly compared, sparrowhawks took about the same number of male and female pied flycatchers. During incubation, however, females spent about 77% of the day in the nest and were 4.7 times more vulnerable than males per unit of time available (i.e. outside the nest). A comparison with the chaffinch Fringilla coelebs , where hawks took more females than males, indicates that timing of breeding, foraging behaviour and parental roles of males and females affect predation risk.     

Serum prolactin levels and crop-sac development in ring doves during a breeding cycle

Using a turkey prolactin radioimmunoassay, the serum prolactin levels of male and female ring doves (Streptopelia risoria) during the breeding cycle were measured and their circulating prolactin levels were compared to crop-sac weight on a within-bird basis. During the early phase of the incubation period, crop weight showed a delayed response to prolactin stimulation and there was no correlation; during the midincubation period when prolactin and crop-sac weight were increasing, there was a strong positive correlation; around hatching, when prolactin was at its peak, there was no correlation. There were again strong positive correlations at later samples, when squabs were developing and both prolactin and crop-sac weight were declining. Thus, it appears that the correlation between the circulating prolactin level and crop-sac development depends on the stage of the breeding cycle. While males and females showed similar pattern of circulating prolactin during the period of incubation and parental care, only females consistently showed a postovulatory rise of prolactin. These results were discussed in the context of the role of prolactin in the breeding cycle.     

Handicapped females receive more feedings during incubation from their mates: support for the female nutrition hypothesis

The female nutrition hypothesis posits that provisioning intensity of incubating females by their mates may depend on female needs and ensure proper incubation and a corresponding high hatching and breeding success of breeding pairs. Here, we have handicapped female pied flycatchers Ficedula hypoleuca at the beginning of incubation by clipping two primaries on each wing and filmed nests during incubation and later nestling provisioning to estimate male involvement in incubation feeding at the nest and in offspring care. Incubation feeding was more frequent at late nests. Correcting for this seasonal effect, incubation feeding was significantly affected by treatment and twice as high at experimental as at control nests. There was no effect of the experiment on female incubation attendance. The handicap did not result in any effect on hatching and breeding success, nestling growth and male or female provisioning and mass at the end of the nestling period. Males adjust their incubation feeding activity at the nest to female energetic requirements during incubation.     

Aggressiveness in king penguins in relation to reproductive status and territory location

King penguins, Aptenodytes patagonicus, vigorously defend small territories in very dense colonies. The egg-laying season lasts approximately 4 months, but only pairs that reproduce during the first half of the period succeed in fledging a chick. I examined various factors affecting aggressiveness of king penguins during the breeding season and focused on the differences between central and peripheral territories. Pairs on peripheral territories experienced twice as many encounters with avian predators as did central birds. The vast majority of peripheral birds were late breeders, indicating that reproductive success was very low among penguins defending a territory on the edge of the colony. Time invested in territory defence and rate of agonistic encounters between breeding neighbours increased from the incubation to the brooding period. Parents gave most threat displays to territorial neighbours when the chick was very young and just before crèche formation. Distance to colony edge was not related to aggressiveness in incubating birds, however, the rate of pecking and flipper blows increased from the edge to the centre during brooding. In addition, aggressiveness of breeding penguins towards travelling birds trespassing into their territory increased with distance to edge. Early breeders were not more aggressive than late breeders but the proportion of time spent in territory defence increased with the number of days a bird had spent incubating. As expected, I did not detect any sex difference in aggressive behaviour. Birds occupying territories on the beach were generally more aggressive during the incubation period than those located on the valley sides. Reproductive status (incubating versus brooding) and territory location were the main factors explaining the various levels of aggressiveness observed in breeding king penguins. Copyright 2000 The Association for the Study of Animal Behaviour.     

Annual variation in the timing of breeding and moulting in male and female Pied Flycatchers Ficedula hypoleuca

During five breeding seasons, the timing of breeding and moulting was studied in the Pied Flycatcher Ficedula hypoleuca. In central Sweden, on average 67% of the males and 41% of the females started moulting before the young fledged. The proportion of individuals with an overlap between breeding and moulting varied considerably between years, with the highest proportion of moulting males being recorded in the year when the females started egg-laying on the latest date. Despite a large annual variation in the proportion of individuals showing a moult/breeding overlap, the duration of this overlap varied insignificantly between years. The onset of moult in males seemed to be related to both calendar date and timing of the current breeding attempt. Most females postponed their moult until just before or just after the fledging of their young, independent of calendar date. There was no significant relationship between male and female moult scores and nestling weight at fledging or fledging success of their brood. Thus, in long-distance migrants such as Pied Flycatchers, it may be adaptive to have some overlap between reproduction and moult, but there seems to be a limit to how early in the breeding cycle they are able to start moulting.     

Endocrine correlates of parental care in an Antarctic winter breeding seabird, the emperor penguin, Aptenodytes forsteri

Plasma levels of luteinizing hormone (LH) and prolactin associated with parental behavior were measured in the Antarctic winter breeding emperor penguin, Aptenodytes forsteri. Males exclusively incubate the egg while females exclusively brood the nonhomeothermic young; both sexes alternate in rearing the homeothermic young. Birds were sampled on arrival from the sea through egg laying, incubation, and brooding. All parent birds lost their chicks at the end of the brooding period due to harsh weather but sampling continued. In females, LH titers dropped after egg laying but levels were restored when the birds returned from the sea to brood the chicks and were not depressed by high prolactin levels. Plasma prolactin remained low in males captured on arrival and kept until the free-living males finished incubation. In breeders, prolactin secretion increased during the prelaying period when day length decreased. Prolactin levels stayed elevated in males during incubation and in brooding females returning after a 2-month absence at sea. Prolactin values were higher in brooding females than in males ending incubation or returning in late brooding. These levels did not drop after chick loss, and the sexual difference in prolactin values was maintained after breeding failure. In emperor penguins, increased prolactin secretion appears to be triggered around the time of egg laying and continues, driven by an endogenous mechanism, through incubation and brooding until rearing is completed. Prolactin secretion independent of external stimuli may have evolved in pelagic seabirds to maintain parental care despite long absences at sea from the breeding colony.     

Effects of presence of squabs upon plasma concentrations of prolactin and LH and length of time of incubation in ringdoves on "extended" incubatory patterns

The effects of a brief exposure to newly hatched squabs upon the concentrations of plasma prolactin and LH secretion and length of incubation time in ring doves were investigated using a novel experimental procedure. After 5 days of incubation birds were deprived of their nests for 3 days. On return to their nests, the birds immediately resumed incubation and laid a second clutch of eggs after 5 days at which time the first clutch was removed. A consequence of this procedure was that at the time of hatching, concentrations of plasma prolactin had passed their peaks and were falling to baseline values, while concentrations of plasma LH were beginning to increase. This experimental manipulation made it possible to demonstrate that brief exposure to newly hatched squabs significantly affects the concentration of plasma prolactin, an effect which was more pronounced in females than in males. This increased secretion of prolactin was associated with a reduction of plasma LH which reached significance in females but not in males. Birds exposed to squabs spent a significantly longer period of time on their nests as compared to those birds not exposed to squabs. This observation is consistent with a role for prolactin in maintaining readiness to incubate.     

Prolactin and parental behavior in Adélie penguins: effects of absence from nest, incubation length, and nest failure

Adélie penguin (Pygoscelis adeliae) males and females, nesting in Antarctica, alternate attendance at the nest with absences of many days to forage at sea. We investigated the importance of tactile input from egg and chicks on prolactin levels by observing nest attendance patterns and obtaining blood samples (1) during the first nest exchange of the incubation stage, (2) from birds whose incubation period was artificially increased or decreased by about 10 days, and (3) from birds whose nests had failed. Prolactin levels in females after 8 to 11 days of absence from the breeding colony did not differ from those in incubating males and did not change after females resumed incubation. Moving eggs between nests resulted in nests in which chicks hatched after about 26, 36 (normal), or 46 days. Duration of incubation did not affect prolactin levels in the parents measured during incubation, at the pip stage, hatch stage, or early brood stage. Adults first left their chicks unguarded on about the same calendar date, regardless of chick age. However, chicks from long incubation nests averaged 8 days younger when they were left unguarded than chicks from control or short-incubation nests. In females, there was no effect of nest failure on prolactin levels. In males, prolactin levels were slightly lower after nest failure than in males tending nests. Testosterone was significantly higher in males after nest failure than in males still tending nests. Prolactin is elevated in Adélie penguins as part of the program of cyclical hormonal changes that accompany the lengthy reproductive season and is relatively independent of tactile input. Sustained prolactin secretion is probably required for the maintenance of parental behavior in offshore feeding species that must be absent from the nest for many days at a time.     

Effects of testosterone implants on pair behaviour during incubation in the Yellow-legged Gull Larus cachinnans

The Yellow-legged Gull Larus cachinnans is monogamous with bi-parental incubation. In this study, the effects of high levels of plasma testosterone in male Yellow-legged Gulls during the incubation period were analysed. Free-living male gulls were implanted with testosterone (T-males), and their sexual behaviour within the pair was observed and compared with that of control pairs. Egg temperatures, length of incubation and hatching success were also analysed. T-males and their mates displayed more sexual behaviour than the controls. T-males engaged in mounting behaviour with their mates, whereas control males did not. Proportionally less time was spent incubating (in relation to time present in the colony) by T-males than control males. However, the mates of T-males did not spend more time incubating than control females to compensate for male neglect, although they did spend more time on the territory. Egg temperature in T-male nests was significantly lower than in control nests, but no significant difference in the length of incubation or hatching success between the two groups was found. In birds, the effects of high testosterone levels on male behaviour during incubation have only been analysed in a polyandrous species whose females usually do not contribute to incubation. The present results thus suggest that those males of a monogamous species with bi-parental incubation that sustain high testosterone levels after laying, thus reducing their contributions to incubation, will be confronted with a lack of compensation from their mates during incubation. Finally, this lack of female compensation seems to be mediated by behavioural interactions with the male rather than by her absence from the colony.     

Evidence from hatching success and DNA fingerprinting for the fertility of hybrid Pied × Collared Flycatchers Ficedula hypoleuca × albicollis

The Pied and Collared Flycatchers Ficedula hypoleuca and F. albicollis hybridize on the Baltic islands of Öland and Gotland. Field studies of hatching success in clutches from 36 breeding hybrid males indicate that male hybrids reproduce successfully. In comparison, 25 hybrid females had normal clutch sizes but failed to hatch nestlings, suggesting female hybrid sterility. The paternity of seven hybrid males was investigated by DNA fingerprinting using two hypervariable minisatellite probes. Of these hybrid males, six were assessed as fertile. Three of the hybrid male families (43%) contained nestlings with extra-pair paternity and the frequency of extra-pair fertilization among 37 nestlings was 22%. One nestling originated from intraspeciflc female nest parasitism. The sterility pattern in hybrids between these two flycatchers with sterile female and fertile male hybrids is in agreement with Haldane's rule.     

Individual differences in aggressiveness of adelie penguins

The number of pecks per minute given by individual Adelie penguins to an artificial model is used as a measure of aggressiveness. Penguins without eggs or chicks are less aggressive than thoes with eggs or chicks. Aggressiveness increases after egg-laying, and reaches a peak at about chick hatching. Prior to egg-laying, males are more aggressive towards the model than females, but after egg-laying there is no difference between them (on average). Most penguins with above average aggressiveness are located at territories in the centre of a colony, whereas those with below average aggressiveness tend to occur at the periphery. Penguins with high aggressiveness also have a higher breeding success than less aggressive ones.     

Sex roles in the monogamous Purple Sandpiper Calidris maritima in Svalbard

The Purple Sandpiper Calidris maritima, an Arctic shorebird, displays unusual sex roles during breeding. In a 5-year study in Svalbard, in the Norwegian high Arctic, data were collected on the roles of the sexes in this species. Purple Sandpipers were similar to most shorebirds in that males actively courted females, established territories and vigorously defended their territories from intruders. Both sexes shared incubation duties approximately equally over the entire 21-day incubation period. Males incubated very little initially, but increased their effort significantly during the first 11 days of incubation to over 50% of the time from days 11–21. However, Purple Sandpipers contrasted with most other shorebird species in that females discontinued their breeding efforts at hatching. In nearly all cases, broods were attended solely by the male until the chicks reached fledging age (or even longer). Nonetheless, the pair bond must be described as monogamous because neither males nor females were found to re-mate or lay a second clutch during a season. This pattern of parental care, which is found only in very few other shorebird species, is discussed in an evolutionary context.     

Reproductive endocrinology of free-living nestling and juvenile starlings, Sturnus vulgaris; an altricial species

Plasma concentrations of luteinizing hormone (LH), prolactin and testosterone, and pituitary content of LH and prolactin, were measured in free-living starlings, Sturnus vulgaris , from hatching until 12 weeks of age.
Plasma LH concentrations were elevated in both sexes until four days after hatching, then they decreased. Throughout the period, plasma LH levels were low compared to those in breeding adults but were comparable to levels in post-breeding photorefractory adults. Pituitary LH content increased until 12 days after hatching, but this increase was due to physical growth during this period. Plasma prolactin concentration and pituitary prolactin content increased dramatically during the nestling period. The increase in pituitary prolactin content was in excess of that accounted for by increasing size. Plasma prolactin remained high during the immediate post-fledging period, but had started to decrease by 12 weeks after hatching. Plasma testosterone concentrations were lower than those in breeding adults, but generally higher than in post-breeding photorefractory adults. The gonads of both sexes remained regressed.
These results suggest that the reproductive system of nestling and juvenile starlings is in a similar state to that of post-breeding photorefractory adult starlings. The comparatively high levels of testosterone may reflect involvement in sexual differentiation.     

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.     

Change in body mass in relation to breeding phase in bull-headed shrikes

Changes in body mass of both sexes of the bull-headed shrike, Lanius bucephalus, were investigated over the six breeding phases of this species. Standardized body mass (SBM), which was defined as body mass divided by the length of the tarsus, of the males was relatively constant over the phrases, while the SBM of the females changed drastically. In the females, the SBM during egg-laying was higher than the SBM in all the other breeding phases. The SBM of the females did not differ between the incubation and early-nestling phases, and was lowest during the fledgling phase. Mass loss in bull-headed shrikes did not correspond to an adaptive adjustment of body mass to permit a reduction in the power required for flight in the nestling period. It is likely that incubating females constantly maintain their body mass to invest in parental efforts from the incubating to nestling periods.     

Double-nesting behaviour and sexual differences in breeding success in wild Red-legged Partridges Alectoris rufa

Double-nesting behaviour, a rare breeding system in which females lay in two nests, one incubated by herself and the other one by her mate, could be considered an intermediate stage in the evolutionary trend from biparental to uniparental care of single clutches. We examined the occurrence and success of double-nesting behaviour in Red-legged Partridges Alectoris rufa in Central Spain. Clutch size and hatching success were recorded, as well as the variation in these between years and between incubating sexes. Participation in incubation was higher for females (94.76%) than males (41.0%), and the proportion of incubating males varied markedly between years, with no incubating males in one dry year and approximately 50% of males incubating in other years. There was significant variation among years and between sexes in laying date, clutch size and hatching success. Clutch size decreased with later laying date in males and females. The probability of clutch loss to predation differed between sexes, being much higher for nests incubated by females. Our results suggest that both rainfall and predation influence the occurrence and success of double-nesting.     

Blood concentrations of gonadotrophins, prolactin and gonadal steroids in males and in non-pregnant and pregnant female African elephants (Loxodonta africana)

No seasonal variation in any of the hormones measured was apparent in males or females. Testosterone levels in males increased around puberty (10-11 years) and remained significantly higher in adult than prepubertal males. This was not accompanied by any significant change in levels of LH, FSH or prolactin. In non-pregnant females there was no apparent difference in levels of LH, FSH or prolactin with age. There was a significant increase in progesterone around puberty (12 years) but there was considerable overlap in values between prepubertal and adult females. During pregnancy, progesterone levels were significantly higher than in non-pregnant females with maximum levels occurring at mid-pregnancy (9-12 months). However, there was considerable overlap in values between non-pregnancy and pregnancy. Concentrations of LH and FSH decreased significantly during mid-pregnancy while prolactin levels increased dramatically during pregnancy; after 7 months of gestation until term levels were always at least 8 ng/ml greater than in any non-pregnant female. It is suggested that this consistent increase in plasma/serum levels of prolactin can be used to diagnose pregnancy in the elephant.