Partner-Specific Odor Recognition in an Antarctic Seabird

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Science  29 Oct 2004:
Vol. 306, Issue 5697, pp. 835
DOI: 10.1126/science.1103001


Among birds, the Procellariiform seabirds (petrels, albatrosses, and shearwaters) are prime candidates for using chemical cues for individual recognition. These birds have an excellent olfactory sense, and a variety of species nest in burrows that they can recognize by smell. However, the nature of the olfactory signature--the scent that makes one burrow smell more like home than another--has not been established for any species. Here, we explore the use of intraspecific chemical cues in burrow recognition and present evidence for partner-specific odor recognition in a bird.

Individual odor recognition has been recognized in mammals for decades, yet the ability to discriminate individuals by scent alone has rarely been investigated in birds (1). Procellariiform seabirds are prime candidates for such studies. These birds have an excellent sense of smell (2), breed in colonies, and are monogamous for life (3). Although several burrowing species can relocate their nests by smell, the nature of the olfactory signature of the burrow remains unclear (4). Here we explore the use of intraspecific chemical cues in burrow recognition in Antarctic prions, Pachiptila desolata (Fig. 1A), and present evidence for partner-specific odor recognition in a bird.

Fig. 1.

Evidence for personal odor recognition. (A) An Antarctic prion, Pachiptila desolata, from Ile Verte (wingspan, 60 cm). About 1 million pairs breed throughout Kerguelen. (B to D) Each histogram shows the percentage of birds that sought out a particular odor in three Y-maze experiments performed at Ile Verte: (B) personal (Per) versus conspecific (CS) odor; (C) partner (P) versus conspecific (CS) odor; (D) personal (Per) odor versus control (C). NC, no choice. P values were determined with a binomial test (Supporting online text).

We performed our study in a breeding colony on a remote, sub-Antarctic island (Ile Verte, 49°51′S, 70°05′E, ∼1 km in diameter) in the gulf of Morbihan, Kerguelen Archipelago. To examine whether prions could discriminate between conspecific odors, we presented them with odor choices in a Y-maze. Prions have a musky scent that tends to permeate cotton bags used for transporting birds. Cotton bags were thus used as odor sources in the arms of the maze. A controlled, regulated airflow improved odor delivery to the bird making a choice (5).

In our first experiment, we wanted to determine whether birds could distinguish their own odor from that of a conspecific selected at random from the colony. If this were the case, then birds might use their own odor as a cue to recognize their nests. Contrary to our expectations, 17 of 22 birds oriented to the odor of a conspecific, whereas only 3 birds preferred their own odor (P < 0.01, binomial test) (Fig. 1B). This result was surprising because incubating birds do not typically explore other burrows. Pairs are philopatric to specific burrows, and predation on roving birds is extreme (3).

Because prions spend up to 2 weeks foraging at sea between incubation shifts, nests probably smell most like the most recent nest occupant. If returning birds could recognize their partner's scent, then perhaps they could use this cue to relocate their home burrow. To test this second hypothesis, we waited until the mates of our initial test subjects exchanged places with them. We then presented these new birds with a choice between their partner's odor and the odor of another conspecific. Here, 17 of 20 birds preferred the odor of their partner to the odor of another conspecific, whereas only 3 birds oriented to the odor of a conspecific (P < 0.01, binomial test) (Fig. 1C).

A final test verified that prions could detect their own odor. Here we gave birds a choice between bags scented with personal odor and one of three different clean bags. Sixteen of 21 birds chose their personal odor, and 4 birds chose the control (P < 0.05, binomial test) (Fig. 1D).

Our results show that Antarctic prions are able to recognize and discriminate individual odor cues that likely contribute to the olfactory signature of their burrows. Prions may also use scents for sex discrimination, but this hypothesis was not directly tested and needs to be further explored (Supporting online text).

Although prions can recognize their own personal odor, we also found they choose to avoid it in the presence of a conspecific odor. Aversion to personal scents has been linked to inbreeding avoidance through kin recognition, and, in rodents, self-referential phenotype matching is implicated as a mechanism for assessing relatedness (6). Like many procellariiforms, Antarctic prions are philopatric to remote islands. Their demography suggests that kin recognition may be critical for discriminating between potential mates. How scent plays a role in kin recognition or subsequent mate choice in procellariiforms is not known (7), but this topic is ripe for further investigation among these and other birds.

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