Male European Starlings Research Articles

Male Starlings Sing Most in the Late Morning, Following Egg-Laying: A Strategy to Protect Their Paternity?

AbstractAccording to the 'fertility-announcement hypothesis', the song of paired males might function partly as a paternity guard strategy and partly to maximize their own extra-pair copulations (EPCs). A major prediction of this hypothesis is that males should sing most when the fertility of their mate reaches a temporal (both seasonal and diurnal) peak. We report some tests of this hypothesis from a study of monogamously paired male European starlings Stumus vulgaris. Mated males sang significantly more during the fertile period of their mate and most males even completely ceased singing after their mate's fertile period. During the ovulatory period mated males sang significantly more in the late morning (0900-1200 hours) following egg-laying, when most females may have reached peak diurnal fertility, than early in the morning (0600-0900 hours). For six females, we were able to determine precise laying times during their ovulatory period and we found that their mates had a significantly higher song rate within the insemination window (the first hour following egg-laying) than before egg-laying. Although male starlings sing most when their mate's fertility reaches a seasonal and diurnal peak, our observations suggest that post-pairing song in monogamous males does not function primarily to deter other males attempting EPCs, or to attract extra-pair mates. Our results rather suggest that post-pairing song in monogamous males is directed mainly towards their own female and functions to stimulate her to solicit copulations. This may be important in the context of sperm competition if frequent pair copulations result in a higher fertilization rate for the male when EPCs have occurred.

Plasma-luteinizing hormone and prolactin during circannual rhythms of gonadal maturation and molt in male and female European starlings.

Male European starlings held under constant 12-h days (LD 12:12) undergo circannual rhythms of gonadal maturation and molt. This study examined the temporal relationship of the different physiological phases of these rhythms and the associated endocrinology. The majority of males and about half of the females in this study showed evidence of rhythmicity in gonadal maturation under constant LD 12:12. These gonadal cycles were different from those under natural changes in day length in that the period of photorefractoriness, when birds are unresponsive to an increase in day length, was always much less and in some cases very short indeed. The relationship between molt and gonadal regression was similar to that during natural cycles: every bird that showed gonadal regression began to molt during regression, and molt did not occur except during gonadal regression. The plasma-luteinizing hormone showed rhythmicity related to gonadal maturation, although less clearly in females and much less pronounced than during natural annual rhythms. Plasma prolactin remained low in most males but varied erratically in females. There was no evidence of rhythmicity in prolactin in either sex. High prolactin was not related to gonadal regression or molt. The results suggest that II endogenous circannual rhythms have a role in the expression of natural annual cycles in this species, then they are highly modulated by ambient day length throughout the year rather than simply being synchronized by day length.

Polygynous male starlings allocate parental effort according to relative hatching date

In many polygynous bird species, males allocate most of their parental effort to their primary females’ broods. There are several hypotheses that may explain this: the relative reproductive value of the brood, the energetic demand of the brood, the genetic quality of the female and the certainty of fatherhood may all be higher for the primary females’ broods. Since these parameters may covary in nature, experiments are necessary to determine their importance. Bigynous male European starlings,Sturnus vulgarispredominantly incubated the eggs and fed the nestlings of their primary females. In an experiment we altered the order in which the clutches hatched by exchanging the primary and secondary females’ eggs before hatching. Even though experimental males mostly incubated their primary females’ clutches, they predominantly fed the nestlings of the secondary female. Experimental males fed secondary females’ nestlings significantly more than control males did. In fact, experimental males invested in their secondary females’ broods to the same extent as control males invested in their primary females’ broods. This result demonstrates that males use relative brood age to decide how to allocate their parental effort between their broods which has important implications for the evolution of the starling mating system.

Immunocytochemical localization of GnRH precursor in the hypothalamus of European starlings during sexual maturation and photorefractoriness.

Immunocytochemistry with quantitative image analysis, for both GnRH and its precursor proGnRH-GAP, was used in male European starlings (Sturnus vulgaris) to investigate four stages of a photoperiodically-induced reproductive cycle. Four different groups of birds were examined: photosensitive buy sexually immature, sexually mature, undergoing gonadal regression, and after the completion of regression and fully photorefractory. The size of cells staining for GnRH and proGnRH-GAP increased during gonadal maturation. A reduction in the number of cells staining for GnRH and the size of cells staining for both GnRH and proGnRH-GAP occurred during gonadal regression, though staining for GnRH and proGnRH-GAP in the median eminence remained high at this stage. Birds examined after completion of regression showed significantly reduced staining for both GnRH and its precursor. These observations suggest that photorefractoriness is promoted by a reduction in proGnRH-GAP production and in GnRH synthesis, rather than requiring inhibition of release of GnRH at the median eminence.

Photoperiodic Condition Modulates the Effects of Testosterone on Song Control Nuclei Volumes in Male European Starlings

Songbirds possess a specialized network of brain nuclei mediating song learning and production, the song system. In many species, the nuclei in this circuit are larger in volume in males housed on long photoperiods than in males housed on short photoperiods. Exposure to long days initially leads to increases in circulating levels of testosterone (T) and it is generally believed that volume changes in the song system are controlled by T-dependent effects of photoperiod. However, a growing body of evidence indicates that photoperiod can also have T-independent effects on song system morphology. Previous work in our laboratory suggested that photoperiodic condition may modulate the effects of exogenous testosterone on the volumes of song control nuclei in male European starlings (Sturnus vulgaris). In the present report, we tested the hypothesis that photorefractoriness attenuates the effects of T on the volumes of song control nuclei in starlings. One group of long-day photorefractory males (16L:8D) was exposed to exogenous T and two groups of short-day photosensitive birds (8L:16D) were either implanted with T or blank (control) capsules. After 8 weeks, T levels were elevated in both groups of T-implanted birds and were undetectable in control animals. Volumes of the high vocal center were larger in T-implanted photosensitive birds than in both T-implanted photorefractory and control photosensitive males, which did not differ. These results suggest that photorefractoriness renders the song nuclei of starlings less sensitive to stimulatory effects of T. Plasticity in the starling song system appears to require the coordination of the appropriate hormonal milieu with a permissive photoperiodic condition.

Age‐ and behavior‐related variation in volumes of song control nuclei in male European starlings

There is considerable interindividual variation in the volumes of song control nuclei. Sex and physiological condition appear to contribute to these differences; however, these factors alone do not account for all of the variation. Studies have attempted to relate differences in song behavior (i.e., song repertoire size) to variation in song nucleus volume, but have met with mixed success. In this article, two studies are presented that used male European starlings (Sturnus vulgaris) to explore the relationship between song nuclei volumes and age-related differences in song behavior and interindividual variation in song behavior in adults. The results of the first study showed that song repertoire size and song bout length were significantly greater in older adult than in yearling males. In addition, the volumes of the high vocal center (HVC) and nucleus robustus archistriatalis (RA) were significantly larger in older adults than yearlings. Area X of the parolfactory lobe did not differ significantly in volume between the two age classes. In the second study, both HVC and RA volume correlated positively with song bout length but not repertoire size among adult birds. Based on these results a new hypothesis is presented that states that variation in song nuclei volumes in starlings relates more to the amount of song produced than to the number of song types stored in memory. © 1996 John Wiley & Sons, Inc.

Age- and behavior-related variation in volumes of song control nuclei in male European starlings.

There is considerable interindividual variation in the volumes of song control nuclei. Sex and physiological condition appear to contribute to these differences; however, these factors alone do not account for all of the variation. Studies have attempted to relate differences in song behavior (i.e., song repertoire size) to variation in song nucleus volume, but have met with mixed success. In this article, two studies are presented that used male European starlings (Sturnus vulgaris) to explore the relationship between song nuclei volumes and age-related differences in song behavior and interindividual variation in song behavior in adults. The results of the first study showed that song repertoire size and song bout length were significantly greater in older adult than in yearling males. In addition, the volumes of the high vocal center (HVC) and nucleus robustus archistriatalis (RA) were significantly larger in older adults than yearlings. Area X of the parolfactory lobe did not differ significantly in volume between the two age classes. In the second study, both HVC and RA volume correlated positively with song bout length but not repertoire size among adult birds. Based on these results a new hypothesis is presented that states that variation in song nuclei volumes in starlings relates more to the amount of song produced than to the number of song types stored in memory.

Adoption or infanticide: options of replacement males in the European starling

The behaviour of a male bird towards a potential mate and her clutch may depend both on his expected paternity and on the likelihood that she will produce a replacement clutch if he commits infanticide. In this study we evaluate the choices made by replacement male European starlings Sturnus vulgaris. By removing males before and during laying, we induced other males, mainly neighbours, to mate with the reproductively active females. When the original male was removed before laying, a new male adopted the subsequent clutch in 14 out of 15 cases. When ten females were widowed during their laying period, replacement males never adopted their clutches. The paternity of replacement males was a function of when they replaced the former male. When replacement occurred more than 3 days before egglaying, the new male fathered nearly all offspring; when it occurred the day before laying, the new male still fathered more than every second young. When the original male was removed during his mate’s laying period, in five out of ten cases a replacement male committed infanticide by throwing out the eggs, but this only occurred in one out of 15 cases when removal took place before laying. The evidence for infanticide actually being committed by the replacement male was circumstantial. Four out of six of the females affected by apparent infanticide produced replacement clutches in which the male presumably had higher paternity than in the original clutch. In all cases, the male adopted the replacement clutch. In five cases when the original male was removed during laying, the neighbours neither adopted the brood nor committed infanticide, although they sometimes were seen courting the widowed female and copulating with her. These cases occurred later during laying than those were males comitted infanticide. The time from infanticide to the laying of the replacement clutch tended to increase as infanticide was committed later in the laying sequence. We conclude that strategies of potential replacement males are influenced by their expected paternity in the current brood and the probability that the female will produce an early replacement clutch.

Female choice for complex song in the European starling: a field experiment

Male European starlings Sturnus vulgaris sing long complex songs that appear to be important in the courtship of females but which also influence competitive interactions between males. We tested the hypothesis that females choose mates on the basis of the complexity of their songs, rather than on the quality of the territories the males defended. In order to determine whether certain territories were preferred over others, the first set of birds to settle in the experimental nest-boxes was removed and a second set allowed to settle. Consistent preferences for certain nest-boxes were indicated by correlations between the settlement patterns of the first and second sets of birds. However, males with the most complex song did not necessarily occupy the most preferred nest sites. Males with more complex song acquired mates faster. This relationship remained significant when nest-site preference was statistically controlled, indicating that female starlings chose males with complex song rather than those that defended preferred nest sites. A number of morphological variables were also found to be uncorrelated with female choice. Song complexity in European starlings increases with age, and the evolution of song complexity in this species is consistent with an age-indicator model of sexual selection. Males with larger repertoires were also in better condition, indicating that females obtain high-quality mates by choosing on the basis of male song.

Two histological markers reveal a similar photoperiodic difference in the volume of the high vocal center in male European starlings.

Most studies of seasonal changes in the avian song control system have used Nissl stains to characterize the nuclei. More recent work has indicated that changes in nucleus volume evident in Nissl-stained tissue are not always apparent when investigated with other histochemical criteria. In this experiment, we used two different markers (Nissl stain and alpha 2-adrenergic receptor autoradiography) to characterize changes in the song system of European starlings (Sturnus vulgaris). Fluctuating levels of circulating testosterone (T) appear to be causally related to seasonal changes in the song system. Therefore, we used photoperiod manipulations to place male starlings into different physiological conditions. Photosensitive male starlings were placed on 11L:13D or 16L:8D photoperiods for at least 5 months. Birds on 11L:13D have enlarged gonads and circulating T. In contrast, starlings maintained on 16L:8D initially show marked gonadal growth. However, after about 6-8 weeks the birds are photorefractory (i.e., the gonads are regressed and T falls to undetectable levels). The volume of the high vocal center (HVC) was 44% larger in the 11L:13D than in 16L;8D birds in Nissl-stained tissue. The density of alpha 2-adrenergic receptors as determined by in vitro receptor autoradiography with [3H]p-amino-clonidine (PAC) is higher in HVC than in the surrounding neostriatum, clearly delineating the boundaries of the nucleus. We reconstructed the volume of HVC using PAC stained tissue. Thus, two histochemical markers indicate a photoperiodic difference in HVC volume of male starlings.

Experimental demonstration of a trade-off between mate attraction and paternal care

Males should invest in mate attraction, mate guarding and paternal care in relation to the marginal fitness value of each of those behaviours. Since time and energy are limited, trade-offs between these activities are expected. This study demonstrates that monogamous male European starlings (Sturnus vulgaris) decrease their paternal effort in response to increased opportunities to attract additional mates and instead invest in mate attraction. Monogamous males' probabilities of attracting additional females were increased by providing them with additional nestboxes. This resulted in both the rate at which males were visited by prospecting females and the probability that they would obtain secondary mates increasing. Males with an additional nestbox sang more than males with only one nestbox, both before laying and during incubation. Males with two nestboxes spent more time at their nest sites when their fertile females were away before, but not during, egg laying. The experiment affected how much males incubated during the early, but not during the late, part of the incubation period. This makes sense, because males can attract additional females mainly during the early part of the incubation period. Male feeding of nestlings was unaffected by the experiment. The fact that the potential to attract mates affects males' investment in parental care suggests that variation in this potential may contribute to the variation in paternal care between bird species.

Response of Male European Starlings To Experimental Removal of Their Mate During Different Stages of the Breeding Cycle

Abstract We experimentally removed females from monogamous European starling Sturnus vulgaris pairs during different stages of the breeding cycle and recorded the effect of these removals on male behaviour and on offspring survival in order to assess the possibilities for female mate desertion. Removal of the female during the laying, incubation and early nestling stage (1- to 5-day-old nestlings) invariably resulted in complete failure of the brood. The survival of the nestlings improved slightly if the female was removed during the middle nestling stage (6- to 10-day-old nestlings), but mortality rate of nestlings was still significantly higher than in control two-parent broods. About 80% of the males widowed during the laying/incubation period removed all eggs from the nest, while only 49% of all males widowed during the early and middle nestling stage removed all dead nestlings. Removal of eggs/dead nestlings by a widowed male starling probably functions to increase the chance on a successful re-mating, since replacement clutches were found only in nests whereof the clutch/brood was removed. We recorded one definite and at least nine suspected cases of parental infanticide, the killing of own offspring, by experimentally widowed male starlings. After nestlings reached 10 days of age (late nestling stage), there was no longer a significant difference in nestling mortality rate between male-only and two-parent broods. This crucial point coincides with the time when (1) the nestlings are functionally homeothermic, and (2) the exponential growth of the nestlings begins to moderate. Moreover, at this time, late in the season, the only viable option for deserted males is to care for the young because the probability of renesting successfully is low. Our results thus indicate that after nestlings reach 10 days of age, female starlings may have the opportunity to desert their mate. However, at that time, the benefits of female mate desertion are reduced as opportunities for renesting succesfully are low.

Effects of Testosterone On Nest-Box Occupation and Associated Behaviours By Male European Starlings (Sturnus Vulgaris)

Abstract In an aviary experiment carried out at the beginning of the breeding season in March and April, nest-box occupation and associated behaviours were observed in a group of 18 adult and 18 first-year male European starlings. Nine birds of each group carried a testosterone implant (T-males) and the other 9 an empty implant (C-males). When analyzed for effects of age, first year birds were significantly more active with regard to nest-box inspection and nest-building than adults. When analyzed for effects of treatment, T-males occupied more nest-boxes and visited their nest-boxes more often than C-males. Other activities like singing, nest-box inspection, nest-building and aggressive behaviour were not significantly different between T-males and C-males. We suggest that the absence of a significant effect of T on aggression may be related to the colonial nesting habits of the starling. Since T-males tended to be more active with regard to all behaviours studied testosterone may have led to a general increase in frequency and persistence of behaviour which in turn facilitated nest-box occupation.

Relations between song repertoire size and the volume of brain nuclei related to song: comparative evolutionary analyses amongst oscine birds

Song and brain structure are compared amongst 41 species of oscine birds by using the method of independent evolutionary contrasts. We find a significant correlation between the relative volume of the song control centre, the high vocal centre (HVC), and the number of song types typically found in the repertoire. Relative HVC volume is not correlated with the number of different syllable types per song bout. The relative volume of a second song nucleus, area X, is not significantly correlated with either measure. Relative HVC volume is uncorrelated with relative volume of the hippocampus, a brain area involved in other forms of memory. This is the first evidence for repeated independent evolution of an association between complexity of learned song and the relative volume of one of the song control nuclei though to be involved in song learning.

Function of the Song and Song Repertoire in the European Starling (Sturnus Vulgaris) : an Aviary Experiment

AbstractWe confronted individually-caged male European starlings, Sturnus vulgaris, with conspecifics of both sexes in order to study singing behaviour during intrasexual and intersexual encounters. Males spent more time at the nestbox, sang more songs and more song types during female presentations than during control periods (observation periods with no conspecifics). Males also sang more songs in the nestbox and flew more to the nestbox with green nest material. During male presentations, only the time spent at the nestbox and the carrying of nest material increased significantly. Males spent more time at the nestbox, sang more songs and more song types in response to a female stimulus than to a male stimulus. Males also sang more songs in the nestbox and flew more to the nestbox with nest material during female than during male presentations. These results suggest that the song and song repertoire of male starlings serve primarily an intersexual rather than an intrasexual function. However, in contrast to a previous study, our results suggest that singing also serves as an intrasexual signal to deter rivals at close encounter. We also tested the hypothesis that the 'whistles' and the 'warbling song' have separate intrasexual and intersexual functions, as has been suggested in the literature. We found no evidence for a specialized intrasexual function of the whistles nor for a specialized intersexual function of the warbling song. From this study it also appears that variations in the size of the aviary can modify the behavioural responses of starling males. New information with regard to the use of green nest material by male starlings is given.

Song acquisition in photosensitive and photorefractory male European starlings

We tested the ability of 1-year-old European starlings ( Sturnus vulgaris) to acquire songs while in different physiological states. Photorefractory males, with low testosterone levels, learned songs as completely and as accurately as photosensitive males in full reproductive condition. This indicates that song acquisition in 1-year-old males does not depend on high levels of androgens. The ability to learn songs during the nonbreeding season may reflect the high song output of potential tutors through most of the year, including the photorefractory period, and may facilitate increases in song repertoire size in adulthood.

Photoperiodic time measurement during the termination of photorefractoriness in the starling ( Sturnus vulgaris L.)

Groups of photorefractory male European starlings have been kept under Nanda-Hamner LD schedules ranging from LD 6:6 to LD 6:54 for about 6 weeks. Subsequently, when transferred to LD 13:11, all birds of groups LD 6:18 and LD 6:42 went through a complete cycle of testicular growth and regression. Furthermore, they carried out a postnuptial molt, indicating that they have been able to terminate photorefractoriness under these LD schedules. In contrast, no positive responses could be detected in groups LD 6:6, LD 6:30, LD 6:36, and LD 6:54. Groups LD 6:12, LD 6:24, and LD 6:48 were intermediate in their reactions. Only part of these birds showed gonadal recrudescence when tested for photosensitivity. Changes in plasma testosterone levels were closely related to variations in testicular diameter. These results clearly suggest a strong circadian component in photoperiodic time measurement during the termination of photorefractoriness in the starling. Positive or negative responses were completely in line with predictions derived from the model of external coincidence. A comparison with the results of a similar experiment previously done with photosensitive birds failed to detect basic differences in the interpretation of the various LD cycles. These findings suggest that the same photoperiodic time measurement system is used at both phases of the starling's annual cycle.

Immunohistochemical demonstration of marked changes in the LHRH system of photosensitive and photorefractory European starlings (Sturnus vulgaris).

Immunocytochemistry was used to determine the effects of photoperiod on the LHRH neurosecretory system in the brain of male European starlings. In this species, as in other birds, reproduction is triggered by long daylengths but continued exposure leads to photorefractoriness and to a complete shut-down of the reproductive system. These effects are thought to be mediated through changes in the secretion of LHRH. In starlings exposed to a photoperiod of 11 h light:13 h darkness (11L:13D) and with fully developed testes there was strong immunostaining of both LHRH perikarya (n = 522 +/- 43 S.E.M.) and fibres. Photosensitive short-day (8L:16D) starlings with undeveloped testes had an almost identical distribution of strongly immunoreactive perikarya (n = 523 +/- 62) but there were fewer fibres. In the median eminence, fibre number was reduced significantly (P less than 0.01) by some 30%. In long-day (18L:6D) photorefractory starlings with fully regressed testes there was an even more obvious change in the LHRH system. Perikarya were only weakly immunoreactive and there was a significant (P less than 0.01) reduction in mean diameter from 10 to 6.5 micron. In addition, there was a significant (P less than 0.05) reduction in cell number (312 +/- 62), although this may well result from the fact that some weakly stained cells fell below the limits of resolution and could not be counted. LHRH fibres disappeared almost entirely from the median eminence, and were not visible elsewhere in the brain. The higher neural pathways regulating photorefractoriness induced by long days are unknown but clearly both production of LHRH in the perikarya and release/storage of LHRH in the terminals is being profoundly modified.

Circannual variations in plasma luteinizing hormone levels in castrated male European starlings (Sturnus vulgaris).

Intact and castrated male European starlings were held for about 2 years in a constant 12-hr photoperiod and constant temperature conditions. At 1- to 2-month intervals, testicular width was measured by laparotomy, and blood samples were taken for analysis of plasma luteinizing hormone (LH). Most of the control birds went through at least one circannual cycle of testicular width and plasma LH concentration. In the castrates, a similar proportion of birds went through circannual LH cycles with periods indistinguishable from those of the controls. It is concluded that the testes and their hormones are not essential components of the mechanism that generates circannual gonadal cycles in male European starlings.

Effects of Nestboxes On LH, Testosterone, Testicular Size, and the Reproductive Behavior of Male European Starlings in Spring

AbstractThe effect of nestboxes on the vernal increase and decrease in reproductive activity was investigated in male European starlings (Sturnus vulgaris), held in outdoor aviaries. Male-only groups with (group 1) and without (group 2) availability of nestboxes were compared for the amount of song, for testicular size and plasma titers of luteinizing hormone (LH) and testosterone. Testicular size and LH differed significantly between the 2 groups, being higher in males with nestboxes. Similar differences, as well as differences in nestbox-related behaviors (sitting in front of a nestbox, inspecting it, and nestbuilding) were also found when individuals of group 1, in possession of a nestbox, were compared to those without. In another group (2), the seasonal dependence of nestboxes as a modifying factor was investigated. These males were given access to nestboxes later in the season, than the males of group 1, after April 7. The effects on physiological parameters at this time of year were negligible in that only a transient increase in LH was seen compared to group 3. Nestbox-oriented behaviors did not reach the same intensities as in group 1. These results demonstrate the importance of nest-site availability in modifying behavioral and physiological functions during the vernal reproductive cycle. At the same time they indicate a seasonal dependence in these modifying effects.