Navigational maps in homing pigeons: GPS-tracking experiments on the role of the stimuli involved in pigeons’ navigation

This projects aims at investigating the nature of the stimuli used in homing pigeons’ navigation over both unfamiliar and familiar areas by using GPS technology. The novel approach of this research project consisted in the investigation of old open questions by means of the use of the satellite technology. While the classical methods of investigation consisted in recording the initial orientation of birds at the release site and their homing time and success, the use of GPS loggers enabled the collection of detailed information on the behaviour of the pigeon during the entire homing journey. The analysis of the whole homing flight of birds subjected to experimental manipulations has highlighted behaviours and phenomena otherwise undetectable with traditional experiments. As concerning the true navigation behaviour, three investigations have been conducted: the olfactory lateralization in homing pigeons, the role of environmental odours on the navigational map and the role of geomagnetic information in a position finding mechanism. As regarding the analysis of the homing flight path of experienced pigeons receiving a unilateral olfactory input, the use of GPS-technique has allowed to highlight some of the effects of the right nostril occlusion, which remained undetected when observing only the initial orientation of the birds at vanishing. We have analysed the tracks of birds released with the left or the right nostril occluded and we have highlighted an important functional asymmetry in favour of the right nostril. In fact the birds processing the environmental olfactory information with the left nostril only, displayed a higher level of tortuosity in their flight path and stopped more frequently than both the unmanipulated controls and the birds using the right nostril. A further progress in the analysis of the birds navigational capabilities from unfamiliar places has been possible thanks to a newly developed GPS data loggers, that allows for a remote readout of the stored data, enabling therefore the acquisition of data of birds that do not home. With this specific technology we achieved a major advance in the understanding of the role of olfactory stimuli in pigeon navigation as we could test the performances of birds made anosmic by nasal anaesthesia. By using this kind of GPS we could test the olfactory activation hypothesis that predicts that olfactory stimuli prime the navigational capabilities of birds, and that the environmental odours are solely needed to activate a navigational system that, in turn, is based on non-olfactory cues. This hypothesis challenges the olfactory navigation hypothesis, which predicts that environmental odours constitute a specific component of the navigational map in homing pigeons. Therefore, we have analysed the GPS tracks of three groups of pigeons subjected to different olfactory conditions during transportation and at the release site and subjected to nasal anaesthesia prior release: controls birds exposed to environmental odours, birds transported in pure air and pigeons transported in pure air but stimulated with artificial odour of plant origin, before the release. The analysis of the tracks revealed that the birds exposed to the artificial odours displayed significantly poorer navigational performances than controls, suggesting a specific role of environmental olfactory information in pigeon navigation. Anatomical studies and conditioning experiments provided evidence that pigeons detect geomagnetic field intensity through the ophthalmic branch of the trigeminal nerve. Despite the fact that magnetic treatments and trigeminal nerve section do not disrupt the abilities of pigeons to home back to the colony, it has been proposed that pigeons tend to fly parallel or perpendicular to the steepest magnetic slope. We have analysed tracks of both intact and trigeminal sectioned pigeons in order to test if the pattern of the local magnetic gradient affect the birds’ flight paths. The analysis did not reveal a consistent effect of the local geomagnetic field in the birds’ homing trajectories. As concerning the navigation from familiar locations, we have conducted an investigation about the role of the topography in the landmark based navigation over familiar areas. It is known that pigeons are able to memorise landscape features of the over-flown areas. These features can be associated to a specific compass direction leading the bird home (site specific compass orientation). Alternatively the bird can learn the spatial relationships among the single landmarks so to build a familiar landmark based map used in a piloting strategy. The two different strategies can be put in conflict by shifting the birds’ internal clock, in order to asses which of the two strategies is preferentially adopted by the subject. This protocol has been used to assess which factors are determining the strategy preferentially used by an individual pigeon and the kind of landscape feature which are likely to be memorised as landmarks during piloting. The analysis of the tracks suggested that the characteristic features of the release site affect the level of reorientation after clock shift, and, in particular, it emerged that the sea might represent an important topographical feature, probably due to its strong chromatic component, that facilitates the ability of the birds to re-orient after a phase shift treatment. Therefore, the vicinity of the sea seems to determine a preference for the piloting strategy

STUDIO DEI MOVIMENTI DI FORAGGIAMENTO DI TARTARUGHE COMUNI (CARETTA CARETTA)IN RELAZIONE A VARIABILI AMBIENTALI

RIASSUNTO: Durante il loro ciclo vitale, le tartarughe marine compiono vari spostamenti, sia su piccola che su ampia scala. Nelle tartarughe comuni il periodo che segue l’abbandono della spiaggia dove sono nate e prima del raggiungimento della maturità sessuale, è poco conosciuto. Dopo alcuni anni di vita pelagica, si ritiene che i giovani si spostino in ambiente neritico, dove foraggiano completando il loro sviluppo. Di recente, l’evoluzione delle tecniche di telemetria satellitare ha consentito di seguire, con buona accuratezza, anche i movimenti di questi giovani, permettendo così di ricostruire le rotte seguite da questi animali durante il loro prolungato soggiorno in ambiente neritico. Lo scopo di questo lavoro è stato quello di elaborare dati ottenuti tramite telemetria satellitare sul comportamento di giovani di tartaruga comune e di integrare gli stessi con informazioni su vari parametri ambientali ed oceanografici, per studiare la possibile relazione tra questi importanti fattori ed i movimenti delle tartarughe monitorate. A questo scopo, sono stati presi in considerazione cinque esemplari di tartaruga comune che erano stati catturati accidentalmente da pescherecci, riabilitati da appositi centri di recupero e rilasciati in varie zone dei mari italiani (a Lampedusa, a Livorno e Rimini). Trasmettitori satellitari connessi col Sistema Argos incollati sul loro carapace hanno permesso di seguire gli animali per 4-11 mesi dopo il rilascio. I dati di localizzazione giornalieri ottenuti dai satelliti Argos sono stati analizzati e filtrati sulla base di apposite procedure, fino ad ottenere un set di dati affidabile con cui ricostruire le rotte seguite da questi animali. In modo analogo, sono stati elaborati dati inviati dalle trasmittenti sulla temperatura dell’acqua in cui si trova la tartaruga e sul numero, la durata massima e media delle immersioni da essa compiute in un determinato lasso di tempo. Queste informazioni sono state analizzate e successivamente integrate con altri dati satellitari, ottenuti da database in rete, relativi a parametri ambientali ed oceanografici come la temperatura superficiale dell’acqua e la concentrazione di clorofilla

Homing Pigeons Only Navigate in Air with Intact Environmental Odours: A Test of the Olfactory Activation Hypothesis with GPS Data Loggers

A large body of evidence has shown that anosmic pigeons are impaired in their navigation. However, the role of odours in navigation is still subject to debate. While according to the olfactory navigation hypothesis homing pigeons possess a navigational map based on the distribution of environmental odours, the olfactory activation hypothesis proposes that odour perception is only needed to activate a navigational mechanism based on cues of another nature. Here we tested experimentally whether the perception of artificial odours is sufficient to allow pigeons to navigate, as expected from the olfactory activation hypothesis. We transported three groups of pigeons in air-tight containers to release sites 53 and 61 km from home in three different olfactory conditions. The Control group received natural environmental air; both the Pure Air and the Artificial Odour groups received pure air filtered through an active charcoal filter. Only the Artificial Odour group received additional puffs of artificial odours until release. We then released pigeons while recording their tracks with 1 Hz GPS data loggers. We also followed non-homing pigeons using an aerial data readout to a Cessna plane, allowing, for the first time, the tracking of non-homing homing pigeons. Within the first hour after release, the pigeons in both the Artificial Odour and the Pure Air group (receiving no environmental odours) showed impaired navigational performances at each release site. Our data provide evidence against an activation role of odours in navigation, and document that pigeons only navigate well when they perceive environmental odours

Examples of tracks.

<p>Other explanations as in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0022385#pone-0022385-g001" target="_blank">Figure 1</a>.</p

Mean vector distributions relative to the sections of the tracks recorded in the first hour after release.

<p>Further explanations as in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0022385#pone-0022385-g007" target="_blank">Figure 7</a>.</p

Examples of tracks.

<p>Other explanations as in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0022385#pone-0022385-g001" target="_blank">Figure 1</a>.</p

Examples of tracks.

<p>Other explanations as in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0022385#pone-0022385-g001" target="_blank">Figure 1</a>.</p

Pooled efficiency index of the section of the track recorded in the first hour after release.

<p>The filled and open symbols represent the data included and not included in the pooled analysis respectively. The median values of the data included in the pooled analysis are indicated by the unbroken lines. The dotted lines indicate the median values of the whole data set.</p

Mean vector distributions relative to the sections of the tracks recorded in the first three hours after release from Bolgheri (home direction 336°) and Montespertoli (home direction 270°), respectively.

<p>Outer arrows: home direction. Inner arrows: individual mean vectors (see Material and methods for further explanations). The open triangles at the periphery of the circle represent the directions of the individual mean vectors. Confidence ellipses of the distributions are reported. The second order mean vector lengths and directions are reported inside the circles. Asterisks indicate the significance level of the one sample Hotelling test: * p<0.05; ** p<0.01; *** p<0.001.</p