Francesco Bonadonna

Sensitivity to dimethyl sulphide suggests a mechanism for olfactory navigation by seabirds

Petrels, albatrosses and other procellariiform seabirds have an excellent sense of smell, and routinely navigate over the worlds oceans by mechanisms that are not well understood. These birds travel thousands of kilometres to forage on ephemeral prey patches at variable locations, yet they can quickly and efficiently find their way back to their nests on remote islands to provision chicks, even with magnetic senses experimentally disrupted. Over the seemingly featureless ocean environment, local emissions of scents released by phytoplankton reflect bathymetric features such as shelf breaks and seamounts. These features suggest an odour landscape that may provide birds with orientation cues. We have previously shown that concentrated experimental deployments of one such compound, dimethyl sulphide (DMS), attracts procellariiforms at sea, suggesting that some species can use it as a foraging cue. Here we present the first physiological demonstration that an Antarctic seabird can detect DMS at biogenic levels. We further show that birds can use DMS as an orientation cue in a non-foraging context within a concentration range that they might naturally encounter over the ocean.

FORAGING FLIGHTS OF BREEDING THICK-BILLED MURRES (URIA LOMVIA) AS REVEALED BY BIRD-BORNE DIRECTION RECORDERS

A bird-borne data logger, which stores flight directions at regular intervals, was used to reveal the foraging patterns of Thick-billed Murres (Uria lomvia) breeding at Latrabjarg in northwestern Iceland. Tracked birds traveled 10 to 168 km one-way to foraging sites in a narrow sector to the northwest of the breeding colony. The pattern of foraging activity was rather constant. Outbound birds stopped briefly several times, possibly testing prey availability. The longest stops occurred at sites close by the turning point of the out- bound journey. During the inbound flight, stops were less frequent and shorter than on the outbound flight, suggesting that the sequence of stops was not the expression of a distur-

Individual Odor Recognition in Birds: An Endogenous Olfactory Signature on Petrels' Feathers?

A growing body of evidence indicates that odors are used in individual, sexual, and species recognition in vertebrates, and may be reliable signals of quality and compatibility. Petrels are seabirds that exhibit an acute sense of smell. During the breeding period, many species of petrel live in dense colonies on small oceanic islands and form pairs that use individual underground burrows. Mates alternate between parental duties and foraging trips at sea. Returning from the ocean at night (to avoid bird predators), petrels must find their nest burrow. Antarctic prions, Pachyptila desolata, are thought to identify their nest by recognizing their partner’s odor, suggesting the existence of an individual odor signature. We used gas chromatography and mass spectrometry to analyze extracts obtained from the feathers of 13 birds. The chemical profile of a single bird was more similar to itself, from year to year, than to that of any other bird. The profile contained up to a hundred volatile lipids, but the odor signature may be based on the presence or absence of a few specific compounds. Our results show that the odor signature in Antarctic prions is probably endogenous, suggesting that in some species of petrels it may broadcast compatibility and quality of potential mates.

Kin recognition and inbreeding avoidance in wild birds: the first evidence for individual kin-related odour recognition

Identification of family members plays a primary role in the evolution of social behaviours such as nepotism, altruism and mate choice. The process is particularly important for philopatric species in which the encounter rate of kin-related conspecifics is high. Olfactory-based recognition of individual kin has been identified in most species, with the exception of birds; historically, birds were thought to have poor olfactory abilities, so the use of olfactory cues was ruled out a priori. Here, we show that European storm petrels, Hydrobates pelagicus, are able to distinguish kin from nonkin odours. Using special cotton swabs, like those used in forensic police procedures, we offered birds a binary choice in a Y-maze. Birds significantly preferred odours of unrelated individuals. Olfactory imprinting on a ‘family olfactory template’ or self-referent phenotype matching may be the mechanism underlying this effect. This choice behaviour may allow these highly philopatric birds to avoid inbreeding and select an appropriate mate. Our results suggest that sophisticated olfactory communication is relevant in birds, and leads to important behavioural traits such as philopatry.

Recognition of burrow's olfactory signature in blue petrels, Halobaena caerulea: an efficient discrimination mechanism in the dark

Previous work has shown that blue petrels need olfaction to home. We investigated whether they also recognize an olfactory signature of their own nest. We performed T-maze experiments in which maze arms were connected with the subject birds burrow and with the burrow of a conspecific neighbour. Of 23 birds, 16 were able to recognize the arm leading to their own burrow. In a second experiment, we positioned the maze in front of the subjects burrow but the maze arms were closed and did not enter the burrow. Consequently, no burrow odours could be sensed by the bird. In this case, 85% of birds (17 of 20) failed to choose, suggesting that petrels were not motivated to choose by positional cues in the absence of odour cues. We explored this idea further by performing a homing experiment whereby homing birds had to relocate an artificially displaced burrow entrance. Blue petrels homed, ignoring the natural burrow entrance and using the new artificial one. The ability to smell their own burrow allows blue petrels to return to the colony at night and to find the correct nest.

Evidence for nest-odour recognition in two species of diving petrel.

SUMMARY In nearly every procellariiform species, the sense of smell appears to be highly adapted for foraging at sea, but the sense of smell among the diving petrels is enigmatic. These birds forage at considerable depth and are not attracted to odour cues at sea. However, several procellariiform species have recently been shown to relocate their nesting burrows by scent, suggesting that these birds use an olfactory signature to identify the home burrow. We wanted to know whether diving petrels use smell in this way. We tested the common diving petrel Pelecanoides urinatrix and the South-Georgian diving petrel Pelecanoides georgicus to determine whether diving petrels were able to recognise their burrow by scent alone. To verify the efficacy of the method, we also tested a bird that is known to use olfaction for foraging and nest recognition, the thin-billed prion Pachyptila belcheri. In two-choice T-maze trials, we found that, for all species, individuals significantly preferred the odour of their own nest material to that of a conspecific. Our findings strongly suggest that an individual-specific odour provides an olfactory signature that allows burrowing petrels to recognize their own burrow. Since this ability seems to be well developed in diving petrels, our data further implicate a novel adaptation for olfaction in these two species that have been presumed to lack a well-developed sense of smell.

Oceanic navigation in Cory's shearwaters: evidence for a crucial role of olfactory cues for homing after displacement

SUMMARY Pelagic birds, which wander in the open sea most of the year and often nest on small remote oceanic islands, are able to pinpoint their breeding colony even within an apparently featureless environment, such as the open ocean. The mechanisms underlying their surprising navigational performance are still unknown. In order to investigate the nature of the cues exploited for oceanic navigation, Corys shearwaters, Calonectris borealis, nesting in the Azores were displaced and released in open ocean at about 800 km from their colony, after being subjected to sensory manipulation. While magnetically disturbed shearwaters showed unaltered navigational performance and behaved similarly to unmanipulated control birds, the shearwaters deprived of their sense of smell were dramatically impaired in orientation and homing. Our data show that seabirds use olfactory cues not only to find their food but also to navigate over vast distances in the ocean.

Orientation in the wandering albatross: interfering with magnetic perception does not affect orientation performance

After making foraging flights of several thousands of kilometres, wandering albatrosses (Diomedea exulans) are able to pinpoint a specific remote island where their nests are located. This impressive navigation ability is highly precise but its nature is mysterious. Here we examined whether albatrosses rely on the perception of the Earths magnetic field to accomplish this task. We disturbed the perception of the magnetic field using mobile magnets glued to the head of nine albatrosses and compared their performances with those of 11 control birds. We then used satellite telemetry to monitor their behaviour. We found that the ability of birds to home to specific nest sites was unimpaired by this manipulation. In particular, experimental and control birds did not show significant differences with respect to either foraging trip duration, or length, or with respect to homing straightness index. Our data suggest that wandering albatrosses do not require magnetic cues to navigate back to their nesting sites.

Major histocompatibility complex class II compatibility, but not class I, predicts mate choice in a bird with highly developed olfaction.

Mate choice for major histocompatibility complex (MHC) compatibility has been found in several taxa, although rarely in birds. MHC is a crucial component in adaptive immunity and by choosing an MHC-dissimilar partner, heterozygosity and potentially broad pathogen resistance is maximized in the offspring. The MHC genotype influences odour cues and preferences in mammals and fish and hence olfactory-based mate choice can occur. We tested whether blue petrels, Halobaena caerulea, choose partners based on MHC compatibility. This bird is long-lived, monogamous and can discriminate between individual odours using olfaction, which makes it exceptionally well suited for this analysis. We screened MHC class I and II B alleles in blue petrels using 454-pyrosequencing and quantified the phylogenetic, functional and allele-sharing similarity between individuals. Partners were functionally more dissimilar at the MHC class II B loci than expected from random mating (p = 0.033), whereas there was no such difference at the MHC class I loci. Phylogenetic and non-sequence-based MHC allele-sharing measures detected no MHC dissimilarity between partners for either MHC class I or II B. Our study provides evidence of mate choice for MHC compatibility in a bird with a high dependency on odour cues, suggesting that MHC odour-mediated mate choice occurs in birds.

Scent of a nest: discrimination of own-nest odours in Antarctic prions, Pachyptila desolata

Petrels and albatrosses evolved well-developed olfactory anatomical structures comparable to those of mammals. To date it has been demonstrated that petrels are attracted by food-related odours, and that some hypogean species have decreased homing performances if anosmic. The ability to distinguish between familiar and unfamiliar odours had not been demonstrated. Here we show that the Antarctic prion, Pachyptila desolata, is able to distinguish between its own nest and that of a conspecific, relying on olfactory cues only. When tested in a maze, only prions with an intact sense of smell made a choice and recognized their own burrow whereas anosmic birds did not. In the absence of leading odours in the maze prions behaved similarly to anosmic birds. These results suggest the mechanism used in the short-range homing process of this species as an olfactory beaconing and suggest the skill of recognising individually distinctive odours. Evolving an efficient identification system in the dark allowed these hypogean petrels to return to their colony at night and recognise their own burrow without singing. This behaviour protects them from predation by skuas, Catharacta skua lönnbergi, that hunt petrels by vision and hearing.