Immunolabeling provides evidence for subregions in the songbird nucleus accumbens and suggests a context-dependent role in song in male European starlings (Sturnus vulgaris)

Birdsong is well known for its role in mate attraction during the breeding season. However, many birds, including European starlings (Sturnus vulgaris), also sing outside the breeding season as part of large flocks. Song in a breeding context can be extrinsically rewarded by mate attraction; however, song in non-breeding flocks, referred to here as gregarious song, results in no obvious extrinsic reward and is proposed to be intrinsically rewarded. The nucleus accumbens (NAc) is a brain region well-known to mediate reward and motivation, which suggests it is an ideal candidate to regulate reward associated with gregarious song. The goal of this study was to provide new histochemical information on the songbird NAc and its subregions (rostral pole, core, and shell), and to begin to determine subregion-specific contributions to gregarious song in male starlings. We examined immunolabeling for tyrosine hydroxylase (TH), neurotensin, and enkephalin (ENK) in NAc. We then examined the extent to which gregarious and sexually-motivated song differentially correlated with immunolabeling for the immediate early genes FOS and ZENK in each subdivision of NAc. We found that TH and ENK labeling within subregions of the starling NAc was generally similar to patterns seen in the core and shell of NAc in mammals and birds. Additionally, we found that gregarious song, but not sexually-motivated song, positively correlated with FOS in all NAc subregions. Our observations provide further evidence for distinct subregions within the songbird NAc and suggest the NAc may play an important role in regulating gregarious song in songbirds.

Unravelling the role of thyroid hormones in seasonal neuroplasticity in European Starlings (Sturnus vulgaris)

Thyroid hormones clearly play a role in the seasonal regulation of reproduction, but any role they might play in song behavior and the associated seasonal neuroplasticity in songbirds remains to be elucidated. To pursue this question, we first established seasonal patterns in the expression of thyroid hormone regulating genes in male European starlings employing in situ hybridization methods. Thyroid hormone transporter LAT1 expression in the song nucleus HVC was elevated during the photosensitive phase, pointing towards an active role of thyroid hormones during this window of possible neuroplasticity. In contrast, DIO3 expression was high in HVC during the photostimulated phase, limiting the possible effect of thyroid hormones to maintain song stability during the breeding season. Next, we studied the effect of hypothyroidism on song behavior and neuroplasticity using in vivo MRI. Hypothyroidism inhibited the photostimulation-induced increase in testosterone, confirming the role of thyroid hormones in activating the hypothalamic-pituitary-gonadal (HPG) axis. Surprisingly, apart from the myelination of several tracts during the photostimulated phase, most neuroplasticity related to song production was unaffected by hypothyroidism. Remarkably, T3 plasma concentrations were negatively correlated to the microstructural changes in several song control nuclei. Potentially, a global reduction of circulating thyroid hormones during the photosensitive period is necessary to lift the brake imposed by the photorefractory period, whereas local fine-tuning of thyroid hormone concentrations through LAT1 could activate underlying neuroplasticity mechanisms. Given the complexity of thyroid hormone effects, this study is a steppingstone to disentangle the influence of thyroid hormones on seasonal neuroplasticity.

Exposure to food insecurity increases energy storage and reduces somatic maintenance in European starlings ( Sturnus vulgaris )

Birds exposed to food insecurity—defined as temporally variable access to food—respond adaptively by storing more energy. To do this, they may reduce energy allocation to other functions such as somatic maintenance and repair. To investigate this trade-off, we exposed juvenile European starlings ( Sturnus vulgaris , n = 69) to 19 weeks of either uninterrupted food availability or a regime where food was unpredictably unavailable for a 5-h period on 5 days each week. Our measures of energy storage were mass and fat scores. Our measures of somatic maintenance were the growth rate of a plucked feather, and erythrocyte telomere length (TL), measured by analysis of the terminal restriction fragment. The insecure birds were heavier than the controls, by an amount that varied over time. They also had higher fat scores. We found no evidence that they consumed more food overall, though our food consumption data were incomplete. Plucked feathers regrew more slowly in the insecure birds. TL was reduced in the insecure birds, specifically, in the longer percentiles of the within-individual TL distribution. We conclude that increased energy storage in response to food insecurity is achieved at the expense of investment in somatic maintenance and repair.

Avian influenza A virus susceptibility, infection, transmission, and antibody kinetics in European starlings

Avian influenza A viruses (IAVs) pose risks to public, agricultural, and wildlife health. Bridge hosts are spillover hosts that share habitat with both maintenance hosts (e.g., mallards) and target hosts (e.g., poultry). We conducted a comprehensive assessment of European starlings (Sturnus vulgaris), a common visitor to both urban and agricultural environments, to assess whether this species might act as a potential maintenance or bridge host for IAVs. First, we experimentally inoculated starlings with a wild bird IAV to investigate susceptibility and replication kinetics. Next, we evaluated whether IAV might spill over to starlings from sharing resources with a widespread IAV reservoir host. We accomplished this using a specially designed transmission cage to simulate natural environmental transmission by exposing starlings to water shared with IAV-infected mallards (Anas platyrhynchos). We then conducted a contact study to assess intraspecies transmission between starlings. In the initial experimental infection study, all inoculated starlings shed viral RNA and seroconverted. All starlings in the transmission study became infected and shed RNA at similar levels. All but one of these birds seroconverted, but detectable antibodies were relatively transient, falling to negative levels in a majority of birds by 59 days post contact. None of the contact starlings in the intraspecies transmission experiment became infected. In summary, we demonstrated that starlings may have the potential to act as IAV bridge hosts if they share water with IAV-infected waterfowl. However, starlings are unlikely to act as maintenance hosts due to limited, if any, intraspecies transmission. In addition, starlings have a relatively brief antibody response which should be considered when interpreting serology from field samples. Further study is needed to evaluate the potential for transmission from starlings to poultry, a possibility enhanced by starling’s behavioral trait of forming very large flocks which can descend on poultry facilities when natural resources are scarce.

SOCIAL INFORMATION AND BIOLOGICAL INVASIONS: CHORUS SONGS ARE MORE ATTRACTIVE TO EUROPEAN STARLINGS IN MORE RECENTLY ESTABLISHED POPULATIONS.

When biological invasions by animals occur, the individuals arriving in novel environments can be confronted with unpredictable or unfamiliar resources and may need social interaction to improve survival in the newly colonized areas. Gathering with conspecifics and using social information about their activities may reveal the location of suitable feeding and breeding sites. This could compensate for the absence of individual information about new habitats and constitute an advantage for new settlers. If a tendency to gather in response to social stimuli is transmitted from one generation to the next, and if the benefit of gathering is lower in long time established populations, there should be behavioural differences in receptivity to social cues in populations with different colonizing histories. We hypothesized that individuals of a social species like the European starling from relatively recently-established populations would be more responsive to social cues than individuals belonging to long-established populations. We conducted playback experiments using a starling chorus to test its acoustic attractiveness to populations of starlings with different colonizing histories. We compared the reaction of individuals from two populations in rural Brittany, western France, established for a long time, with three more recently settled ones: two populations from a propagation front in southern Italy and one urban population from Rennes city in Brittany. Our data supported our hypothesis: individuals from more recent populations were more responsive to the acoustic stimulus, and gave more calls in flight than individuals from populations with an older settlement history. We discuss the different behavioural responses we observed in the different populations and the potential effects of habitat characteristics and starling densities.

Population colonization history influences behavioral responses of European starlings in personality tests

To understand the processes involved in biological invasions, the genetic, morphological, physiological and behavioral characteristics of invasive populations need to be understood. Many invasive species have been reported to be flying species. In birds, both invaders and migrants encounter novel situations, therefore one could expect that both groups might react similarly to novelty. Here we analyzed the behavioral responses of individuals from three populations of European starling Sturnus vulgaris: a population settled for centuries in a rural region, a population that recently colonized an urban area, and a population of winter migrant birds. We conducted a social isolation test, a novel environment test, a novel food test and a novel object test to explore their reactions towards novelty. We identified and characterized different behavioral profiles for each test. The group of migratory adults appeared to be less anxious in social isolation than the group of urban young. Urban and migrant groups entered the novel environment sooner than rural birds. Shy, bold and intermediate individuals were observed in all three groups when presented with novel food. Finally, the proportion of shy individuals which did not touch the novel object was higher than the proportion of bold individuals in the rural group. Our study emphasizes that neophilia or boldness present in migrant and invasive populations may facilitate the occupation of novel habitats. Our analysis also suggests that mixed reactions of neophobia ensure behavioral flexibility in a gregarious invasive species.