Gap detection in the European starling (Sturnus vulgaris)

Summary Gap-detection thresholds were determined for single units in the cochlear ganglion and in auditory nerve fibres of the starling from responses to two broad-band noise bursts separated by a temporal gap of between 0.4 and 204.8 ms. All 35 units showed a threshold within the range of gap sizes tested. The median minimum-detectable gap was 12.8 ms with the minimum being 1.6 ms. A multiple regression analysis revealed that the size of the minimum-detectable gap was not significantly correlated with the neuron's CF, with its sharpness of tuning as given by its bandwidth 10 dB above threshold, or with its Q_10dB value. Only the level of stimulation above the neuron's threshold showed a significant negative correlation with the size of the minimum-detectable gap. These results are discussed with respect to theoretical considerations of limits posed on temporal resolution by the characteristics of peripheral filters. These findings are also discussed in the context of the coding of gaps at different levels of the starling's auditory system and in relation to psychoacoustic results in the starling on gap detection and time resolution described by temporal modulation transfer functions.     

Azimuthal sound localization in the European starling (Sturnus vulgaris)

Summary The physical measurements reported here test whether the European starling (Sturnus vulgaris) evaluates the azimuth direction of a sound source with a peripheral auditory system composed of two acoustically coupled pressure-difference receivers (1) or of two decoupled pressure receivers (2).A directional pattern of sound intensity in the freefield was measured at the entrance of the auditory meatus using a probe microphone, and at the tympanum using laser vibrometry. The maximum differences in the soundpressure level measured with the microphone between various speaker positions and the frontal speaker position were 2.4 dB at 1 and 2 kHz, 7.3 dB at 4 kHz, 9.2 dB at 6 kHz, and 10.9 dB at 8 kHz. The directional amplitude pattern measured by laser vibrometry did not differ from that measured with the microphone. Neither did the directional pattern of travel times to the ear. Measurements of the amplitude and phase transfer function of the starling's interaural pathway using a closed sound system were in accord with the results of the free-field measurements.In conclusion, although some sound transmission via the interaural canal occurred, the present experiments support the hypothesis 2 above that the starling's peripheral auditory system is best described as consisting of two functionally decoupled pressure receivers.Abbreviations CM cochlear microphonics - ITD interaural time difference - IID interaural intensity difference - MRA minimum resolvable angle - dB SPL sound-pressure level (re 0.00002 Pa)     

Metabolic costs of egg production in the European starling (Sturnus vulgaris)

The energy cost of egg production in passerine birds has typically been estimated to be 45%-60% of basal metabolic rate (BMR), but this is based on theoretical models using data on energy content of eggs and reproductive tissue; there are still very few empirical data on egg production costs. In this study, we directly measured resting metabolic rate (RMR) in egg-laying female European starlings (Sturnus vulgaris) over 3 yr. We compared these data with RMR of nonbreeding and chick-rearing birds and with estimated energy expenditure generated from a typical energy content model by using empirically derived data from body composition analysis for this species. We found marked variation in RMR between years and between reproductive stages, which complicates comparisons among breeding stages for the assessment of relative egg production costs. On the basis of this method, RMR during egg laying varied from +74% to -13% of nonbreeding RMR and from +20% to -7% of chick-rearing RMR. We therefore used an alternate approach: measuring changes in RMR through the complete cycle of follicle development and ovulation. The increase in RMR from the beginning of prelaying to the six-follicle stage (before first ovulation) when birds have a complete developing follicle hierarchy was 22.4%. This value is still much lower than that estimated from our energy content model. We discuss conceptual problems associated with the theoretical energy content approach but also suggest, on the basis of earlier work done in our lab, that the measured increase in RMR might still underestimate the actual cost of egg production if birds reallocate energy between different physiological systems.     

Song as an honest signal of past developmental stress in the European starling (Sturnus vulgaris)

Bird song is a sexually selected male trait where females select males on the basis of song quality. It has recently been suggested that the quality of the adult male song may be determined by nutritional stress during early development. Here, we test the 'nutritional-stress hypothesis' using the complex song of the European starling. Fledgling starlings were kept under experimental treatment (unpredictable short-term food deprivations) or control conditions (ad libitum food supply), for three months immediately after independence. We measured their physiological and immune responses during the treatment and recorded song production during the following spring. Birds in the experimental group showed increased mass during the treatment and also a significantly suppressed humoral response compared with birds in the control group. There was no difference between the groups in the cell-mediated response. Next spring, males in the experimental group spent less time singing, sang fewer song bouts, took longer to start singing and also sang significantly shorter song bouts. These data support the hypothesis that both the quality and quantity of song produced by individual birds reflect past developmental stress. The results also suggest the 'nutritional-stress hypothesis' is best considered as a more general 'developmental-stress hypothesis'.     

Intraspecific nest parasitism in the European starling Sturnus vulgaris

Biochemical genetic markers were used along with conventional methods (abnormal laying sequence/clutch size, unusual egg shape/pigmentation) to identify intraspecific nest parasitism at two British nestbox colonies of the European starling. Between 11 and 37% of first clutches were parasitized during 1977–1979. Parasitic females probably comprised all of the following categories: (1) paired females contesting a nestbox occupied by another pair; (2) previously paired females who had laid a clutch but had been unsuccessful; (3) unpaired females who had copulated with males that already had a mate and nest site; and (4) ‘professional’ nest parasites who distributed at lest some of their eggs in one or more nests other than their own. Although parasitized nests had higher clutch sizes, parasitism led to fewer host young fledging per egg laid, mainly through the eviction of eggs and subsequent nest desertion. Number of parasitic young fledged per egg laid was highest when eggs were laid synchronously with the host, when host clutches were larger, or a smaller number of parasite eggs were added to a nest, thus favouring parasites that distribute their eggs amongst a number of nests. A greater pressure on nest sites may have accounted for the higher levels of parasitism at the Aberdeen colony and for the greater number of parasite eggs laid in a nest. Although most parasitic female starlings appeared to be much less successful than non-parasitic ones, nest parasitism in the starling might evolve directly when one or more of the following advantages are present. (1) There are no constraints on the number of eggs a female may lay but there are constraints on the number of young she may feed adequately. (2) Female survival is increased by having fewer or no eggs/young to care for. (3) Current feeding conditions favour the survival of more young than would be produced by the most common clutch size. Intraspecific nest parasitism is considered to be a first stage in the evolution of interspecific nest parasitism.     

Sleep pattern in the starling (Sturnus vulgaris)

Electrographic and behavioural observations were conducted on two male and two female captive starlings (Sturnus vulgaris) under natural illumination conditions during autumn. Polygraphically sleep and wakefulness of starling were similar to those of other birds. Starling's total sleep (TS) and slow wave sleep (SWS) lasted 39.0 +/- 1.4% and 38.3 +/- 1.7% of the 24-h period respectively. Paradoxical sleep (PS) was 1.8 +/- 0.2% of the total sleep time. The mean durations individual of TS, SWS and PS episodes were 6.8 +/- 0.2 min, 5.0 +/- 1.0 min and 18 +/- 3 s respectively. The daily percentage of SWS was correlated with the mean episode duration while that of PS was correlated with the number of episodes rather than with the mean episode duration. Starling females spent in sleep a greater percentage of the 24-h period than males.     

Gap detection in the starling (Sturnus vulgaris)

Summary Gap-detection thresholds of single units were determined from auditory forebrain neurons of the awake starling. Nine different response types were statistically defined from the discharge pattern to a 400 ms broadband noise stimulus. The gap stimuli consisted of two broadband noise bursts which were separated by a gap ranging from 0.4 to 204.8 ms duration. The median minimumdetectable gap for 121 out of 145 units that had a significant threshold 204.8ms was 12.8 ms; 20% of the neurons showed thresholds between 0.4 and 3.2 ms. The neurons of the nine response types differed significantly in their minimum-detectable gaps; neurons with phasic-tonic and phasic excitation exhibited the best (i.e. shortest) minimum-detectable gaps. The neurons of the three different recording areas (field L, NCM and HV) were significantly different in their minimumdetectable gaps; field L neurons showed the best temporal resolution for gaps in broadband noise. Gap-detection thresholds are compared with psychophysical thresholds determined with the same stimuli and the relevance of forebrain units for temporal resolution is discussed.Abbreviations CS control stimulus - HV hyperstriatum ventrale - HVc hyperstriatum ventrale pars caudalis - NB noise burst - NCM neostriatum caudale pars medialis - NS noise stimulus - SGS standard gap series - TW time window     

The functional anatomy of the shoulder in the European starling (Sturnus vulgaris)

The excursions of wing elements and the activity of eleven shoulder muscles were studied by cineradiography and electromyography in European starlings (Sturnus vulgaris) flying in a wind tunnel at speeds of 9–20 m s^?1. At the beginning of downstroke the humerus is elevated 80–90° above horizontal, and both elbow and wrist are extended to 90° or less. During downstroke, protraction of the humerus (55°) remains constant; elbow and wrist are maximally extended (120° and 160°, respectively) as the humerus passes through a horizontal orientation. During the downstroke-upstroke transition humeral depression ceases (at about 20° below horizontal) and the humerus begins to retract. However, depression of the distal wing continues by rotation of the humerus and adduction of the carpometacarpus. Humeral retraction (to within about 30° of the body axis) is completed early in upstroke, accompanied by flexion of the elbow and carpometacarpus. Thereafter the humerus begins to protract as elevation continues. At mid-upstroke a rapid counterrotation of the humerus reorients the ventral surface of the wing to face laterad; extension of the elbow and carpometacarpus are initiated sequentially. The upstroke-downstroke transition is characterized by further extension of the elbow and carpometacarpus, and the completion of humeral protraction. Patterns of electromyographic activity primarily coincide with the transitional phases of the wingbeat cycle rather than being confined to downstroke or upstroke. Thus, the major downstroke muscles (pectoralis, coracobrachialis caudalis, sternocoracoideus, subscapularis, and humerotriceps) are activated in late upstroke to decelerate, extend, and reaccelerate the wing for the subsequent downstroke; electromyographic activity ends well before the downstroke is completed. Similarly, the upstroke muscles (supracoracoideus, deltoideus major) are activated in late downstroke to decelerate and then reaccelerate the wing into the upstroke; these muscles are deactivated by mid-upstroke. Only two muscles (scapulohumeralis caudalis, scapulotriceps) exhibit electromyographic activity exclusively during the downstroke. Starlings exhibit a functional partitioning of the two heads of the triceps (the humerotriceps acts with the pectoralis group, and does not overlap with the scapulotriceps). The biphasic pattern of the biceps brachii appears to correspond to this partitioning.     

Dominance, competition, and energetic reserves in the European starling, Sturnus vulgaris

We investigated the relationships between social dominance,competition for food, and strategies of body mass and fat regulationin the European starling (Sturnus vulgaris). In birds housedin groups of three, subdominant birds stored more fat than dominants.A removal experiment established a causal link between socialdominance and fat reserves; in groups that had the dominantindividual removed, the remaining birds reduced body mass andfat, relative to control groups that had the subordinate removed.In a second experiment, we investigated the influences of degreeof competition for food and dominance on body mass and fat reserves.Birds under high competition increased fat reserves and tendedto have higher body mass than birds under low competition. Theincrease in fat reserves was higher in the subdominants thanin the dominants. These results are consistent with hypothesesconcerning dominance-dependent access to food; subdominant birds,or birds under increased competition, may store more fat asan insurance against periods when food cannot be obtained. However,relations between dominance, body mass, and fat reserves mayalso arise through other proximate factors relating to dominance-dependentcosts and benefits of fat storage, such as predation risk andenergetic expenditure.     

Behavioural and hormonal effects of social isolation and neophobia in a gregarious bird species, the European starling (Sturnus vulgaris)

Separating gregarious individuals from their group members often results in behavioural and physiological changes, like increased levels of corticosterone. Testosterone and corticosterone, in particular, have been implicated in the response of mammals to novelty. Data in birds are, however, rare. The presence or absence of group members may also influence an individual's response to novel stimuli. We assessed the behaviour and hormonal response of European starlings (Sturnus vulgaris) to a novel object in two different situations and seasons: each starling was tested when separated and when in contact with its group members in May/June (breeding season) and again in September/October (non-breeding season). Starlings are gregarious throughout the year, but as foraging flocks are small during the breeding season and large during the non-breeding season, we assumed that non-breeding starlings would be more affected by social isolation. Overall, starlings had higher levels of corticosterone, lost more body mass, and were more active when they were separated from their group. Isolated individuals, however, did not show a greater neophobic response than individuals in the presence of their group members in either season. Circulating levels of testosterone and corticosterone were higher after a test with novel object than after a test with only the familiar feeding dish in both sexes and seasons. However, control tests for handling effects confirmed only the increase in testosterone. Our study shows that social isolation is stressful for unrelated and unpaired members of a wild flocking bird species and demonstrates that novelty can lead to a rise in testosterone in birds.     

Immimohistochemical localization of corticotropin-releasing factor in selected brain areas of the European starling (Sturnus vulgaris) and the song sparrow (Melospiza melodia)

Summary Corticotropin-releasing factor (CRF) was localized in the brains of two passerine species, the European starling (Sturnus vulgaris) and the song sparrow (Melospiza melodia), by means of immunohistochemistry. The hypothalamic distribution of this peptide in these species includes a complex of immunoreactive perikarya observed in the paraventricular nucleus (PVN), in both its medial and lateral divisions. Nerve fibers were also seen running from these areas to the anterior median eminence (AME) where a terminal field is apparent. A wide variety of extra-hypothalamic nuclei containing CRF-immunoreactive cells and fibers were identified. An apparent CRF terminal field can be visualized in the lateral septum. A dense fiber plexus is present in the nucleus accumbens (Ac) and more caudally in the nucleus of the stria terminalis (nST). In colchicinepretreated animals, it was revealed that these areas also contain CRF-stained perikarya. The pattern of CRF immunoreactivity in the Ac-nST complex is continuous, with no distinction apparent between the nuclei. The medial preoptic area (mPOA) and the adjacent diagonal band of Broca contain CRF-fibers, while cells are apparent in the mPOA. In the mesencephalon, cells were visualized in the midbrain central gray; a terminal field and scattered positively stained perikarya were found in areas more ventral to the central grey that are adjacent to the third cranial nerve. Scattered cells were also seen at the border of the nucleus intercollicularis-nucleus mesencephalicus lateralis, pars dorsalis complex. In contrast to mammalian studies, no immunoreactive nerve fibers or perikarya were observed in telencephalic areas homologous to the mammalian neocortex. These studies confirm the presence of a CRF path-way regulating pituitary function and suggest a broad role played by CRF as a neuromodulator or neurotransmitter in autonomic and possibly behavioral activities in these species.     

Dynamics of Campylobacter colonization of a natural host, Sturnus vulgaris (European starling)

Wild European Starlings ( Sturnus vulgaris ) shed Campylobacter at high rates, suggesting that they may be a source of human and farm animal infection. A survey of Campylobacter shedding of 957 wild starlings was undertaken by culture of faecal specimens and genetic analysis of the campylobacters isolated: shedding rates were 30.6% for Campylobacter jejuni , 0.6% for C. coli and 6.3% for C. lari. Genotyping by multilocus sequence typing (MLST) and antigen sequence typing established that these bacteria were distinct from poultry or human disease isolates with the ST-177 and ST-682 clonal complexes possibly representing starling-adapted genotypes. There was seasonal variation in both shedding rate and genotypic diversity, both exhibiting a maximum during the late spring/early summer. Host age also affected Campylobacter shedding, which was higher in younger birds, and turnover was rapid with no evidence of cross-immunity among Campylobacter species or genotypes. In nestlings, C. jejuni shedding was evident from 9 days of age but siblings were not readily co-infected. The dynamics of Campylobacter infection of starlings differed from that observed in commercial poultry and consequently there was no evidence that wild starlings represent a major source of Campylobacter infections of food animals or humans.     

Female presence affects male behavior and testosterone levels in the European starling (Sturnus vulgaris)

In this study, we confronted individually housed male European starlings (Sturnus vulgaris) with a female conspecific for 60 min to study the consequences on behavior and plasma testosterone (T) concentrations. Control males experienced a similar procedure, the only difference being that they were tested in the absence of a female. Female presence significantly affected both behavior and plasma T levels of male starlings. Experimental males spent significantly more time singing in the nest box and flew significantly more into the nest box with green nesting material during female presentations than during control periods. Control males never showed these mate attraction behaviors. In total 5 of the 16 experimental males did not respond behaviorally to the female stimulus bird (NR males). In contrast to T levels of control males, plasma T concentrations of both experimental males that did respond to the female (R males) and of NR males (which only perceived the female stimulus) were positively influenced by female presentation. The time spent singing in the nest box by experimental males (R and NR males combined) during female presence tended to be positively correlated with changes in plasma T levels. Finally, before introduction of a female, plasma T levels of R males were significantly higher than those of NR males indicating that individually housed males respond to the presence of a female conspecific by increasing their mate attraction behaviors only when a threshold plasma T concentration has been reached.     

Isolation and characterization of polymorphic microsatellites isolated from the spotless starling (Sturnus unicolor) and cross‐species amplification in the European starling (Sturnus vulgaris)

Spotless and European starlings (Sturnus unicolor and Sturnus vulgaris) have attracted attention from researchers interested in sexual selection, evolution of parental care and reproductive strategies. Both species show high levels of intraspecific nest parasitism and extra‐pair paternity, but research in this area is hampered by a lack of molecular markers specific for these species. Here, we describe a set of primers for nine microsatellite loci in spotless starlings, eight of which are highly polymorphic (7.37 alleles in average). These microsatellites are also polymorphic in European starlings (6.75 alleles in average).     

Azimuthal sound localization in the European starling (Sturnus vulgaris): II. Psychophysical results

Small songbirds have a difficult analysis problem: their head is small compared to the wavelengths of sounds used for communication providing only small interaural time and level differences. Klump and Larsen (1992) measured the physical binaural cues in the European starling (Sturnus vulgaris) that allow the comparison of acoustical cues and perception. We determined the starling’s minimum audible angle (MAA) in an operant Go/NoGo procedure for different spectral and temporal stimulus conditions. The MAA for broadband noise with closed-loop localization reached 17°, while the starling’s MAA for open-loop localization of broadband noise reached 29°. No substantial difference between open-loop and closed-loop localization was found in 2 kHz pure tones. The closed-loop MAA improved from 26° to 19° with an increase in pure tone frequency from 1 to 4 kHz. This finding is in line with the physical cues available. While the starlings can only make use of interaural time difference cues at lower frequencies (e.g., 1 and 2 kHz), additional interaural level difference cues become available at higher frequencies (e.g., 4 kHz or higher, Klump and Larsen 1992). An improvement of the starling’s MAA with an increasing number of standard stimulus presentations prior to the test stimulus has important implications for determining relative (MAA) localization thresholds.     

Lesions to the medial preoptic area affect singing in the male European starling (Sturnus vulgaris)

The aromatization of testosterone (T) in the medial preoptic nucleus (POM) is known to regulate male courtship and sexual behaviors expressed prior to, and in anticipation of, copulation. Singing in male European starlings is used to attract mates prior to physical sexual contact, suggesting that the POM might be involved. The present study was performed to examine the effects of lesions targeting the POM on singing and courtship behavior in reproductively active male starlings. A significant decrease in song output and the gathering of green nest materials was observed in males with lesions to the POM compared to males with damage to brain areas outside of the POM. Lesions did not affect a male's tendency to remain near a female or to occupy a nestbox, suggesting that the effects of POM lesions were specific to courtship behaviors. Behavioral differences were not related to testis mass or volume, and GnRH immunoreactivity was observed within the hypothalamus and median eminence for each male, suggesting that the effects of POM lesions were related specifically to POM involvement in song expression rather than to a disruption of the GnRH axis. These results suggest a general role for the POM in the expression of behaviors related to sexual arousal or anticipation, including song.     

Innervation of the parathyroid in the european starling (Sturnus vulgaris)

Anatomical studies were conducted to characterize the source, type, and distribution of parathyroid gland innervation in European starlings. Denervation experiments demonstrated that the parathyroid glands and adjacent carotid bodies are innervated by nerve fibers originating in the nodose ganglion of the vagus nerve. In the parathyroid parenchyma, these fibers terminate adjacent to chief cells or near vascular smooth muscle. Vagal fibers also form synapses with catecholamine-containing glomus cells of the carotid body. Blood that first perfuses the carotid body subsequently perfuses the parathyroid parenchyma. These observations suggest that vagal innervation may influence parathyroid function in starlings either through direct chief cell innervation or through alteration of vascular perfusion. A neurohemal relationship also may exist between the carotid body and parathyroids.     

Sexual dimorphism and bilateral asymmetry of syrinx and vocal tract in the European starling (Sturnus vulgaris)

Sexually dimorphic vocal behavior in zebra finches (Taeniopygia guttata) is associated with a 100% larger syrinx in males and other morphological adaptations of the sound source. The songbird syrinx consists of two independent sound sources, whose specialization for different spectral ranges may be reflected in morphological properties, but the morphology of labia and syringeal skeleton have not been investigated for lateralized specializations. Similarly, little is known whether the morphology of the songbird vocal tract reflects differences in vocal behavior. Here, we tested the hypothesis that different vocal behavior and specialization is reflected in the morphology. We investigated syringeal and upper vocal tract morphology of male and female European starlings (Sturnus vulgaris). Female starlings exhibit smaller vocal repertoires and sing at lower rates than males. In males, the left syrinx produces mostly low frequencies, while the right one is used for higher notes. Macroscopic and histological techniques were used to record nineteen measurements from the syrinx and the vocal tract which were tested for sexual differences in syrinx and vocal tract and for lateral asymmetry within the syrinx. Sexually dimorphic vocal behavior is reflected in the morphology of the starling syrinx. Males have a larger syrinx with the size difference attributable to increased muscle mass and three enlarged elements of the syringeal skeleton. The upper vocal tract, however, does not differ between males and females. Distinct lateralization was found in two elements of the syringeal skeleton of females, and the labia in the left syrinx are larger than those on the right in both sexes. The sexual dimorphism of the syringeal size is smaller in starlings (35%) than in zebra finches (100%), which is consistent with the different vocal behavior of females in both species. The morphological differences between the two sound sources are discussed in relation to their vocal performance. J. Morphol., 2011. © 2011 Wiley‐Liss, Inc.     

Melatonin and the circadian rhythms of feeding and perch-hopping in the European starling,Sturnus vulgaris

Summary The role of melatonin plasma titers in the control of free-running circadian rhythms was investigated in European starlings,Sturnus vulgaris, held in continuous dim light. Simultaneous recordings of plasma melatonin, perch-hopping and feeding activity revealed synchronous circadian variations in all three functions with high melatonin titers during resting and low titers during activity periods. Implanting birds with melatonin silastic capsules resulted in a 100-fold increase in plasma concentrations and an abolition of the endogenous melatonin rhythm. Feeding rhythms persisted during this treatment, although the activity time () was lengthened and the circadian period () shortened. Similar changes were found in perchhopping activity, but in some birds, this activity was more or less suppressed. These data demonstrate that although melatonin plasma titers freerun synchronously with other circadian parameters, fluctuations in peripheral melatonin are not essential for the expression of circadian activity.     

Breeding-context-dependent relationships between song and cFOS labeling within social behavior brain regions in male European starlings (Sturnus vulgaris)

Male European starlings (Sturnus vulgaris) sing throughout the year, but the social factors that motivate singing behavior differ depending upon the context in which song is produced. In a non-breeding context (when testosterone concentrations are low), starlings form large, mixed-sex flocks and song is involved in flock cohesion and perhaps maintenance of social hierarchies. In contrast, in a breeding context (when testosterone concentrations are high), male song plays a direct role in mate attraction. How the nervous system ensures that song production occurs in an appropriate context in response to appropriate stimuli is not well understood. The song control system regulates song production, learning, and, to some extent, perception; however, these nuclei do not appear to regulate the social context in which song is produced. A network of steroid hormone sensitive nuclei of the basal forebrain and midbrain regulates social behavior. The present study used the immediate early gene cFOS to explore possible involvement of these regions in context-dependent song production. Numbers of cFOS-labeled cells in the medial bed nucleus of the stria terminalis, anterior hypothalamus, and ventromedial nucleus of the hypothalamus related positively only to song produced in a breeding context. In contrast, numbers of cFOS-labeled cells in three zones of the lateral septum related positively only to song produced in a non-breeding context. Taken together, these data suggest differential regulation of male starling song by social behavior nuclei depending upon the breeding context in which it is produced.