THE SPECIES-REPERTOIRE OF WHISTLED SONGS IN THE EUROPEAN STARLING: SPECIES- SPECIFIC CHARACTERISTICS AND VARIABILITY

ABSTRACT

Observations of European starlings in France, Germany and Australia reveal surprising high similarities in the individual repertoires of whistled songs. The structure of the whistles enabled us to recognize a number of categories, in which some species-specific themes were found everywhere. They appear with the same general characteristics and variation ranges in all populations.

There seems therefore to be a basic species-specific repertoire common to all males, who have also a number of additional individual themes which characterize each male in its colony. These individual themes show also common characteristics in the different populations. The results suggest that a mechanism has evolved which canalizes the patterns to be learned. The existence of such a universal innate species-specific repertoire has also to be related to functional aspects and to the complicated dialects found in this species.     

Song Differentiation and Population Structure: the Example of the Whistled Songs in an Introduced Population of European Starlings Sturnus vulgaris in Australia

Whistled songs of male starlings were studied in Australia and results compared with previous ones in Europe. Starling whistle sonograms can be divided into general classes according to certain criteria. All or most males sing five whistled types (“species-specific” themes), plus other (“individual”) themes. The basic repertoire of species-specific themes is almost the same in Europe and Australia with the same characteristics and similar variation ranges. In both continents each male has a certain number of individual themes, but Australian repertoires tend to be smaller, with two species-specific themes less and fewer individual themes. In all study areas dialects were based on local variations in species-specific theme structure, but the Australian dialectal system is simpler than in Europe. Therefore basic characteristics seem to have been similarly transmitted across generations in both continents. But some of the differences (individual characteristics, repertoire size, frequencies) may stem from different habitat characteristics and also social structure, which could have greatly affected song differentiation.     

Isolation and characterization of polymorphic microsatellite loci in the plural cooperatively breeding superb starling,Lamprotornis superbus

Superb starlings (Lamprotornis superbus) are separate nesting plural cooperative breeders endemic to East Africa that show high levels of reproductive conflict and low reproductive skew. I isolated 31 polymorphic microsatellite loci from the superb starling genome and characterized them in approximately 31 individuals. The numbers of alleles per locus ranged from two to 16 and observed heterozygosities ranged from 0.03 to 0.88. Many of these loci amplified in other passerine species including the European starling, Sturnus vulgaris, and a variety of other starlings and mockingbirds.     

Sex-specific Activity Patterns in Periplaneta americana and their Relation to Mate-finding

The comparison of local song variations between a migratory and a sedentary population of starlings shows the species-specificity of the basic categories and of their variation range. Local variations were studied for different themes in the repertoire, near Kaiserslautern (West Germany) during the reproductive season of 1982. Results were compared with those previously obtained in Brittany (France). In the study area in Germany, 80 % of the individuals migrate in autumn whereas the Breton starlings remain near the colony all year. To compare the whistles of individuals of different regions, by examing the important variations in their frequency modulation, it is necessary to know the general basic features of the whistles. Using sonograms, the whistles of starlings can be divided into 8 general classes according to particular criteria: rhythmicity, modulation etc. Five themes, among these 8 classes, are sung by all or most of the individuals (“specific themes”). The analyses of whistles give us the following results:

• 1 The songs of the migratory population studied in W. Germany contain basic features corresponding to those known in the sedentary French population.
• 2 Like the Breton starlings, those in Germany show a “theme-specific” dialect distribution: the rhythmic theme shows several variants in an area of a few km², whereas the uniform simple theme presents only one variant over several 100 km². For the five themes, the dialectal mosaic is totally different: two birds can have the same variant of one given theme and sing different dialects of another.
• 3 The themes which, in France, show a great number of variants over a small area present the same tendency towards strong subdivision in dialects in Germany. In the two study areas, no correlation could be found between dialectal boundaries and ecological factors.
• 4 Considering that two starling populations with very different characteristics show such similarities in their basic song structures and also in their pattern of local variation (in the parameters concerned and in the sizes of the dialect areas) we may suppose that the basic structure of the specific themes could be determined by a genetic program. Some characteristics, like the precise details of the frequency modulation, may be due more to learning and may conform to the local dialect.

     

Elevated testosterone levels affect female breeding success and yolk androgen deposition in a passerine bird

Although it is well documented that testosterone (T) is an important mediator in the regulation of behaviour in male vertebrates, its functional significance in females is less understood. Experimentally increased T in adult female birds has been found to have both advantageous and detrimental effects on behaviour and fitness. In addition, T may also mediate maternal effects when it is deposited into the egg yolk, and variations in androgen concentration between eggs contribute to differences in offspring phenotype and fitness. In this study we examined the effects of experimentally elevated female T on reproductive success and yolk androgen deposition in the spotless starling. The administration of exogenous T in female spotless starlings before egg laying caused negative effects on reproductive performance: when compared to control females T-females laid fewer eggs and raised fewer chicks. We also found an effect of elevated female T on yolk androgen deposition: T-females laid eggs with greater amounts of yolk T than control females, whereas yolk androstenedione levels were not affected. Although some of these effects likely involved a direct interference of female T with female reproductive function, some of them could be due to effects operating in eggs through maladaptive high T levels.     

同域分布下丝光椋鸟与灰椋鸟的繁殖行为

2011年3—6月,通过悬挂巢箱人工招引丝光椋鸟(Sturnus sericeus)及同域分布下的灰椋鸟(Sturnus cineraceus),并对其繁殖生态进行了初步研究。共设置椋鸟式巢箱40个,其中椋鸟的入住率是84.6%,营巢成功率是51.5%,利用摄像机对其中3巢丝光椋鸟与3巢灰椋鸟进行了系统的繁殖行为观察。结果显示:丝光椋鸟窝卵数为6～7枚,灰椋鸟窝卵数5～7枚,后者的卵显著大于前者;丝光椋鸟的育雏期(20d)较灰椋鸟(16d)长,且亲鸟的递食率明显较高;育雏期丝光椋鸟亲鸟的警戒频次也明显高于灰椋鸟。因此,相比于灰椋鸟,丝光椋鸟具有更完善的育雏行为机制。另外,本文还首次报道了丝光椋鸟的种内巢寄生现象。     

Perineuronal nets and vocal plasticity in songbirds: A proposed mechanism to explain the difference between closed‐ended and open‐ended learning

Perineuronal nets (PNN) are aggregations of chondroitin sulfate proteoglycans surrounding the soma and proximal processes of neurons, mostly GABAergic interneurons expressing parvalbumin. They limit the plasticity of their afferent synaptic connections. In zebra finches PNN develop in an experience‐dependent manner in the song control nuclei HVC and RA (nucleus robustus arcopallialis) when young birds crystallize their song. Because songbird species that are open‐ended learners tend to recapitulate each year the different phases of song learning until their song crystallizes at the beginning of the breeding season, we tested whether seasonal changes in PNN expression would be found in the song control nuclei of a seasonally breeding species such as the European starling. Only minimal changes in PNN densities and total number of cells surrounded by PNN were detected. However, comparison of the density of PNN and of PNN surrounding parvalbumin‐positive cells revealed that these structures are far less numerous in starlings that show extensive adult vocal plasticity, including learning of new songs throughout the year, than in the closed‐ended learner zebra finches. Canaries that also display some vocal plasticity across season but were never formally shown to learn new songs in adulthood were intermediate in this respect. Together these data suggest that establishment of PNN around parvalbumin‐positive neurons in song control nuclei has diverged during evolution to control the different learning capacities observed in songbird species. This differential expression of PNN in different songbird species could represent a key cellular mechanism mediating species variation between closed‐ended and open‐ended learning strategies. © 2017 Wiley Periodicals, Inc. Develop Neurobiol 77: 975–994, 2017     

Temporal Dynamics of Dialects in the Whistled Songs of Starlings

Previous studies revealed that whistled songs of starlings can be separated into different categories, among which five themes are found in the repertoires of all (or most) individuals. These “specific” themes show local variations but the different themes have different sizes of dialect areas. This study investigates the temporal evolution of this complex dialectal system. Observations were made in an area where dialects were mapped three years earlier. They reveal an obvious temporal evolution of dialects, although the degree of variation differs according to the theme. No structural change was observed for two themes (CC and ST), but some temporal dynamics in their dialect boundaries did appear. There were changes in the structures and boundaries of two other themes (IT and HT). However, they showed:

• — a relationship between new and old structures, either with persistence of the old variants or with an apparent drift. Almost no really new structures were observed.
• — all the 1980 variants recorded in 1983 were found at sites not far from the original one. The main changes consisted of extensions or regressions of variants along boundaries.

Lastly, the temporal evolution of RT dialects is unusual in that the changes are more sudden. The variants have been replaced by different ones in some cases, but in others they have remained stable. The complexity of the dialectal system is persistent on a temporal level, varying from stability for ST to sudden changes for RT, with IT and HT intermediate.     

Seasonal variation in the whistles of the Starling Sturnus vulgaris

Observations of sedentary male Starlings at two sites in Brittany from December 1979 to December 1980 showed that the amount of whistled song varies during the year, principally from March to July during the reproductive season. Whistles are not numerous in summer but increase from September. These results suggest a link between whistled songs and testosterone titers. The different whistle types present different evolutions of their relative frequencies. Some are abundant during the nest building phase, others during the feeding phase. The curves were similar at the two sites for a given theme, showing that each theme constitutes an entity and that the different themes are influenced differently by environmental factors. The significance to the learning process in young birds is discussed.     

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.     

Realized vs apparent reduction in enemies of the European starling

Release from parasites, pathogens or predators (i.e. enemies) is a widely cited ‘rule of thumb’ to explain the proliferation of nonindigenous species in their introduced regions (i.e. the ‘enemy release hypothesis’, or ERH). Indeed, profound effects of some parasites and predators on host populations are well documented. However, some support for the ERH comes from studies that find a reduction in the species richness of enemies in the introduced range, relative to the native range, of particular hosts. For example, data on helminth parasites of the European starling in both its native Eurasia and in North America support a reduction of parasites in the latter. However, North American ‘founder’ starlings were likely not chosen randomly from across Eurasia. This could result in an overestimation of enemy release since enemies affect their hosts on a population level. We control for the effects of subsampling colonists and find, contrary to previous reports, no evidence that introduced populations of starlings experienced a reduction in the species richness of helminth parasites after colonization of North America. These results highlight the importance of choosing appropriate contrast groups in biogeographical analyses of biological invasions to minimize the confounding effects of ‘propagule biases’.     

Daily Laying Time in Free‐Living European Starlings: Solar Noon,a Potential Synchronizer

Reproduction is generally controlled by important temporal constraints involving complex adaptive mechanisms. Birds, in temperate zones, present marked breeding seasonality as well as marked daily organization of reproductive behavior, especially laying. Intra‐specific variability and determinants of this pattern have been investigated mainly in domestic non‐passerine birds. The present study analyzed the daily temporal organization of laying in a free‐living species, the European starling, Sturnus vulgaris. Breeding in a starling colony was monitored for five consecutive years using a non‐invasive method (infrared video camera) to precisely estimate laying times. European starlings present a marked daily laying rhythm, ovipositions occurring only during a morning species‐specific temporal window. Inside this laying window, time intervals between successive eggs varied greatly among females. Contrary to many species, the light/dark cycle did not appear to control laying time in European starlings, but daily variations of the ultraviolet composition of the solar spectrum appeared to be a possible Zeitgeber of this behavior.     

Daily laying time in free-living European starlings: solar noon, a potential synchronizer

Reproduction is generally controlled by important temporal constraints involving complex adaptive mechanisms. Birds, in temperate zones, present marked breeding seasonality as well as marked daily organization of reproductive behavior, especially laying. Intra-specific variability and determinants of this pattern have been investigated mainly in domestic non-passerine birds. The present study analyzed the daily temporal organization of laying in a free-living species, the European starling, Sturnus vulgaris. Breeding in a starling colony was monitored for five consecutive years using a non-invasive method (infrared video camera) to precisely estimate laying times. European starlings present a marked daily laying rhythm, ovipositions occurring only during a morning species-specific temporal window. Inside this laying window, time intervals between successive eggs varied greatly among females. Contrary to many species, the light/dark cycle did not appear to control laying time in European starlings, but daily variations of the ultraviolet composition of the solar spectrum appeared to be a possible Zeitgeber of this behavior.     

Female European starling preference and choice for variation in conspecific male song

Data from several field studies support the hypothesis that female European starlings, Sturnus vulgaris, attend to variation among the songs of conspecific males when making mate-choice decisions. However, for a variety of methodological reasons, direct evidence for female preferences based on song in starlings has been lacking. This study presents a novel technique for assaying directly female preference and choice in European starlings by using the presentation of conspecific male song as an operant reinforcer in a controlled environment. Using an apparatus in which the playback of songs from different nestboxes is under the operant control of the subject, we demonstrate how the reinforcing properties of conspecific song can be used to measure female preference and choice. The results of the study suggest three conclusions. First, female starlings prefer naturally ordered conspecific male songs over reversed songs. Second, female starlings display robust preferences for longer compared with shorter male song bouts. Behaviour in the operant apparatus varied directly with male song bout length. Third, preferences based on song bout length are sex specific. Male starlings failed to respond differentially to the same stimuli for which females showed strong preferences. These results suggest that male-male variation in song bout length is important for mate choice among starlings. In addition, we detail the use of a novel behavioural assay for measuring female preferences that can be applied to similar behaviours in other species of songbirds. Copyright 2000 The Association for the Study of Animal Behaviour.     

The effect of egg size and habitat on starling nestling growth and survival

In spite of the fact that hatchling size and energy reserves in birds are affected by egg size, many studies have failed to find an effect of egg size on offspring fitness. One possibility is that this is because they have been performed in areas with high food availability and that effects of egg size on offspring fitness are most apparent in areas of low food availability. To investigate this, egg size,␣offspring mass and survival of European starlings (Sturnus vulgaris) were measured in an agricultural landscape with a low but variable amount of pasture, the preferred foraging habitat of parent starlings. Offspring mass was related to egg size, but egg size explained a declining proportion of the variation in nestling mean mass as nestlings grew older. Offspring survival during the early, but not during the late nestling period was related to egg size. Throughout the nestling␣period, survival was related to the mass of the nestlings. It is suggested that the effect of egg size on␣offspring survival is through the effect of egg size on offspring mass, this effect declining as offspring grow older. Offspring survival during the early part of the nestling period was related to egg size when availability of pasture was low, but not when it was high. However, the interaction was not significant. Selection for␣larger egg size is discussed in relation to the structuring␣of starling populations into sources and sinks. Received: 22 September 1997 / Accepted: 22 January 1998     

SONGS OF BLUE TITS PARUS CAERULEUS PALMENSIS FROM LA PALMA (CANARY ISLANDS)—A TEST OF HYPOTHESES

ABSTRACT

Parus major and Parus caeruleus palmensis have some song types in common. They consist of whistled element-types in different frequency ranges. Both species show territorial reactions to playback of the song-types belonging to the other species. P.c. palmensis does not share any songtypes with Central European Parus caeruleus. This is confirmed by playback experiments with the different song types, which do not elicit any territorial behaviour. The songs of P.c. palmensis also differ from those of blue tits from any other Canary Island. They may be derived from contact calls of the Lanzarote population. They have been developed by young birds that had not yet learnt their songs when they colonized La Palma from Lanzarote without reaching any of the other Canary Islands. It is suggested that the uniform song repertoire was developed by adapting the already learned contact calls to each other. The similarities to song types of P. major are due to convergence rather than character displacement. All other Canary Island tit populations share the main features of their songs, which are characterized by quick frequency changes. It seems most likely that these islands have been colonized by birds which had already learnt their songs. Differences in song repertoires are mainly caused by drift events which happen to occur because of population bottlenecks during the colonization process.     

Nest site attributes and temporal patterns of northern flicker nest loss: effects of predation and competition

To date, most studies of nest site selection have failed to take into account more than one source of nest loss (or have combined all sources in one analysis) when examining nest site characteristics, leaving us with an incomplete understanding of the potential trade-offs that individuals may face when selecting a nest site. Our objectives were to determine whether northern flickers (Colaptes auratus) may experience a trade-off in nest site selection in response to mammalian nest predation and nest loss to a cavity nest competitor (European starling, Sturnus vulgaris). We also document within-season temporal patterns of these two sources of nest loss with the hypothesis that flickers may also be constrained in the timing of reproduction under both predatory and competitive influence. Mammalian predators frequently depredated flicker nests that were: lower to the ground, less concealed by vegetation around the cavity entrance and at the base of the nest tree, closer to coniferous forest edges and in forest clumps with a high percentage of conifer content. Proximity to coniferous edges or coniferous trees increased the probability of nest predation, but nests near conifers were less likely to be lost to starlings. Flickers may thus face a trade-off in nest site selection with respect to safety from predators or competitors. Models suggested that peaks of nest predation and nest loss to eviction occurred at the same time, although a competing model suggested that the peak of nest loss to starlings occurred 5 days earlier than the peak of mammalian predation. Differences in peaks of mammalian predation and loss to starlings may constrain any adjustment in clutch initiation date by flickers to avoid one source of nest loss.     

A case of cooperative breeding in the European Starling,Sturnus vulgaris

Cooperative breeding, where individuals other than the parents help to raise offspring, occurs in only ~9% of bird species. Although many starlings (Sturnidae) are cooperative breeders, the European starling (Sturnus vulgaris) has rarely been observed exhibiting this behavior. Only two other records exist, one of which was limited to a juvenile giving food to chicks that had already been collected by a parent (and hence providing limited help). Herein, we report a case of cooperative breeding by a juvenile European starling, which represents the second with any evidence of the juvenile collecting food independently and the first to document the extent of such help in the form of feeding rates. Over a period of at least 3 days, a juvenile starling assisted two parents to feed their second brood of the year, and it fed the chicks at the same rate as the adults (~3.5 feeds per hour). In considering potential explanations for this behavior, we conducted an ancestral state estimation of cooperative breeding across starlings and were able to eliminate the possibility that this is a rarely expressed behavior inherited from cooperatively breeding ancestors. Instead, we propose that our observations point to a behavioral innovation, which may be in response to environmental change such as climate change (which has previously been associated with cooperative breeding). Researchers working on birds should be alert to such behavior to determine whether this apparently new breeding strategy will increase as a potential adaptation to environmental change.     

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).     

Pollutants increase song complexity and the volume of the brain area HVC in a songbird

Environmental pollutants which alter endocrine function are now known to decrease vertebrate reproductive success. There is considerable evidence for endocrine disruption from aquatic ecosystems, but knowledge is lacking with regard to the interface between terrestrial and aquatic ecosystems. Here, we show for the first time that birds foraging on invertebrates contaminated with environmental pollutants, show marked changes in both brain and behaviour. We found that male European starlings (Sturnus vulgaris) exposed to environmentally relevant levels of synthetic and natural estrogen mimics developed longer and more complex songs compared to control males, a sexually selected trait important in attracting females for reproduction. Moreover, females preferred the song of males which had higher pollutant exposure, despite the fact that experimentally dosed males showed reduced immune function. We also show that the key brain area controlling male song complexity (HVC) is significantly enlarged in the contaminated birds. This is the first evidence that environmental pollutants not only affect, but paradoxically enhance a signal of male quality such as song. Our data suggest that female starlings would bias their choice towards exposed males, with possible consequences at the population level. As the starling is a migratory species, our results suggest that transglobal effects of pollutants on terrestrial vertebrate physiology and reproduction could occur in birds.