SUMMARYPelagic 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, Cory's shearwaters, Calonectris borealis, nesting in the Azores were displaced and released in open ocean at about 800km 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. Supplementary material available online at
SummaryForty years ago, Papi and colleagues discovered that anosmic pigeons cannot find their way home when released at unfamiliar locations. They explained this phenomenon by developing the olfactory navigation hypothesis: pigeons at the home loft learn the odours carried by the winds in association with wind direction; once at the release site, they determine the direction of displacement on the basis of the odours perceived locally and orient homeward. In addition to the old classical experiments, new GPS tracking data and observations on the activation of the olfactory system in displaced pigeons have provided further evidence for the specific role of olfactory cues in pigeon navigation. Although it is not known which odours the birds might rely on for navigation, it has been shown that volatile organic compounds in the atmosphere are distributed as fairly stable gradients to allow environmental odour-based navigation. The investigation of the potential role of olfactory cues for navigation in wild birds is still at an early stage; however, the evidence collected so far suggests that olfactory navigation might be a widespread mechanism in avian species.
When given repeated training from a location, homing pigeons acquire the ability to use familiar landmarks to navigate home. Both control and hippocampal-lesioned pigeons succeed in learning to use familiar landmarks for homing. However, the landmark representations that guide navigation are strikingly different. Control and hippocampal-lesioned pigeons were initially given repeated training flights from two locations. On subsequent test days from the two training locations, all pigeons were rendered anosmic to eliminate use of their navigational map and were phase- or clock-shifted to examine the extent to which their learned landmark representations were dependent on the use of the sun as a compass. We show that control pigeons acquire a landmark representation that allows them to directly use landmarks without reference to the sun to guide their flight home, called "pilotage". Hippocampal-lesioned birds only learn to use familiar landmarks at the training location to recall the compass direction home, based on the sun, flown during training, called "site-specific compass orientation." The results demonstrate that for navigation of 20 km or more in a natural field setting, the hippocampal formation is necessary if homing pigeons are to learn a spatial representation based on numerous independent landmark elements that can be used to directly guide their return home.
SUMMARYThe identification of the sensory cues and mechanisms by which migratory birds are able to reach the same breeding and wintering grounds year after year has eluded biologists despite more than 50 years of intensive study. While a number of environmental cues have been proposed to play a role in the navigation of birds, arguments still persist about which cues are essential for the experience based navigation shown by adult migrants. To date, few studies have tested the sensory basis of navigational cues used during actual migration in the wild: mainly laboratory based studies or homing during the non-migratory season have been used to investigate this behaviour. Here we tested the role of olfactory and magnetic cues in the migration of the catbird (Dumetella carolinensis) by radio tracking the migration of birds with sensory manipulations during their actual migratory flights. Our data suggest that adult birds treated with zinc sulphate to produce anosmia were unable to show the same orientation as control adults, and instead reverted to a direction similar to that shown by juveniles making their first migration. The magnetic manipulation had no effect on the orientation of either adults or juveniles. These results allow us to propose that the olfactory sense may play a role in experience based migration in adult catbirds. While the olfactory sense has been shown to play a role in the homing of pigeons and other birds, this is the first time it has been implicated in migratory orientation. Supplementary material available online at
Domestic chicks bilaterally or unilaterally lesioned to the hippocampus were trained to search for food hidden beneath sawdust by ground-scratching in the centre of a large enclosure, the correct position of food being indicated by a local landmark in the absence of any extra-enclosure visual cues. At test, the landmark was removed or displaced at a distance from its original position. Results showed that sham-operated chicks and chicks with a lesion of the left hippocampus searched in the centre, relying on large-scale geometric information provided by the enclosure, whereas chicks with a lesion of either the right hippocampus or both hippocampi were completely disoriented (landmark removed) or searched close to the landmark shifted from the centre (landmark displaced). These results indicate that encoding of geometric features of an enclosure occurs in the right hippocampus even when local information provided by a landmark would suffice to localize the goal; encoding based on local information, in contrast, seems to occur outside the hippocampus. These findings provide evidence that the left and right avian hippocampi play different roles in spatial cognition, a phenomenon which had been documented previously only for the human hippocampus.
During migratory journeys, birds may become displaced from their normal migratory route. Experimental evidence has shown that adult birds can correct for such displacements and return to their goal. However, the nature of the cues used by migratory birds to perform long distance navigation is still debated. In this experiment we subjected adult lesser black-backed gulls migrating from their Finnish/Russian breeding grounds (from >60°N) to Africa (to < 5°N) to sensory manipulation, to determine the sensory systems required for navigation. We translocated birds westward (1080 km) or eastward (885 km) to simulate natural navigational challenges. When translocated westwards and outside their migratory corridor birds with olfactory nerve section kept a clear directional preference (southerly) but were unable to compensate for the displacement, while intact birds and gulls with the ophthalmic branch of the trigeminal nerve sectioned oriented towards their population-specific migratory corridor. Thus, air-borne olfactory information seems to be important for migrating gulls to navigate successfully in some circumstances.
Pelagic seabirds wander the open oceans then return accurately to their habitual nest-sites. We investigated the effects of sensory manipulation on oceanic navigation in Scopoli’s shearwaters (Calonectris diomedea) breeding at Pianosa island (Italy), by displacing them 400 km from their colony and tracking them. A recent experiment on Atlantic shearwaters (Cory’s shearwater, Calonectris borealis) breeding in the Azores indicated a crucial role of olfaction over the open ocean, but left open the question of whether birds might navigate by topographical landmark cues when available. Our experiment was conducted in the Mediterranean sea, where the availability of topographical cues may provide an alternative navigational mechanism for homing. Magnetically disturbed shearwaters and control birds oriented homeward even when the coast was not visible and rapidly homed. Anosmic shearwaters oriented in a direction significantly different from the home direction when in open sea. After having approached a coastline their flight path changed from convoluted to homeward oriented, so that most of them eventually reached home. Beside confirming that magnetic cues appear unimportant for oceanic navigation by seabirds, our results support the crucial role of olfactory cues for birds’ navigation and reveal that anosmic shearwaters are able to home eventually by following coastal features.
SUMMARY The ability of pigeons to find their way home from unfamiliar sites located up to hundreds of kilometers away is well known, but the mechanisms underlying this ability remain controversial. One proposed mechanism is based on the suggestion that pigeons are equipped with magnetoreceptors that can enable the detection of either the earth's magnetic field and/or magnetic field anomalies in the local terrain over which the pigeons fly. Recent reports have suggested that these magnetoreceptors are located in the upper beak where they are innervated by the ophthalmic branch of the trigeminal nerve. Moreover, this nerve has been shown to mediate pigeons' ability to discriminate the presence versus the absence of a magnetic field anomaly in a conditioning situation. In the present study, however, we show that an intact ophthalmic branch of the trigeminal nerve is neither necessary nor sufficient for good homing performance from unfamiliar locations, but that an intact olfactory nerve is necessary.
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