Neural Correlates of Behavioural Olfactory Sensitivity Changes Seasonally in European Starlings

Geert De Groof,Helga Gwinner,Annemie Van der Linden,Silke Steiger,Bart Kempenaers,Michael Hendricks

doi:10.1371/journal.pone.0014337

Geert De Groof, Helga Gwinner + Show 4 more

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https://doi.org/10.1371/journal.pone.0014337

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Abstract

BackgroundPossibly due to the small size of the olfactory bulb (OB) as compared to rodents, it was generally believed that songbirds lack a well-developed sense of smell. This belief was recently revised by several studies showing that various bird species, including passerines, use olfaction in many respects of life. During courtship and nest building, male European starlings (Sturnus vulgaris) incorporate aromatic herbs that are rich in volatile compounds (e.g., milfoil, Achillea millefolium) into the nests and they use olfactory cues to identify these plants. Interestingly, European starlings show seasonal differences in their ability to respond to odour cues: odour sensitivity peaks during nest-building in the spring, but is almost non-existent during the non-breeding season.Methodology/Principal FindingsThis study used repeated in vivo Manganese-enhanced MRI to quantify for the first time possible seasonal changes in the anatomy and activity of the OB in starling brains. We demonstrated that the OB of the starling exhibits a functional seasonal plasticity of certain plant odour specificity and that the OB is only able to detect milfoil odour during the breeding season. Volumetric analysis showed that this seasonal change in activity is not linked to a change in OB volume. By subsequently experimentally elevating testosterone (T) in half of the males during the non-breeding season we showed that the OB volume was increased compared to controls.Conclusions/SignificanceBy investigating the neural substrate of seasonal olfactory sensitivity changes we show that the starlings' OB loses its ability during the non-breeding season to detect a natural odour of a plant preferred as green nest material by male starlings. We found that testosterone, applied during the non-breeding season, does not restore the discriminatory ability of the OB but has an influence on its size.

Highlights

IntroductionDuring the past 20-30 years many studies have shown the complexity of avian olfactory structures, in species with larger olfactory bulbs (OB) like vultures, petrels and albatrosses and in species with much smaller OB such as pigeons, quail, robins, hummingbirds and starlings (for review see [1,2,3])
It has long been thought that birds lack a well-developed sense of smell
Post hoc pair-wise comparisons of telencephalon volume for the three seasons found that it was significantly larger for spring (1238641 mm3) compared to summer (1228640 mm3; P = 0.028) and compared to fall (1220638 mm3; P = 0.002) (Fig. 2), a trend was observed between the volume of summer compared to that of fall (P = 0.063)

Summary

Introduction

During the past 20-30 years many studies have shown the complexity of avian olfactory structures, in species with larger olfactory bulbs (OB) like vultures, petrels and albatrosses and in species with much smaller OB such as pigeons, quail, robins, hummingbirds and starlings (for review see [1,2,3]) Birds use their sense of smell in navigation, in avoidance of insects, in nest identification, in detection of chemical signals during courtship, in food searching and in avoiding predators [4]. Due to the small size of the olfactory bulb (OB) as compared to rodents, it was generally believed that songbirds lack a well-developed sense of smell This belief was recently revised by several studies showing that various bird species, including passerines, use olfaction in many respects of life. During courtship and nest building, male European starlings (Sturnus vulgaris) incorporate aromatic herbs that are rich in volatile compounds (e.g., milfoil, Achillea millefolium) into the nests and they use olfactory cues to identify these plants. European starlings show seasonal differences in their ability to respond to odour cues: odour sensitivity peaks during nest-building in the spring, but is almost non-existent during the non-breeding season

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Conclusion