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- Data packageData from: Deconstructing the flight paths of hippocampal-lesioned homing pigeons as they navigate near home offers insight into spatial perception and memory without a hippocampus(2022-08-30) Gagliardo, Anna; Cioccarelli, Sara; Giunchi, Dimitri; Pollonara, Enrica; Colombo, Silvia; Casini, Giovanni; Bingman, Verner P.The aim of this study was to exploit detailed analyses of GPS-recorded tracks to better characterise the impact of hippocampal (HF) lesion on spatial memory and perception in the context of homing pigeon navigation when reliant on familiar landscape features near the home loft following repeated releases from the same three locations. As reported previously, following HF lesion, a low spatio-temporal resolution analysis revealed that homing pigeons fly less direct paths home once near the loft. We now further show that 1) HF-lesioned pigeons are less likely to display fidelity to a particular flight path home when released from the same locations multiple times, 2) intact pigeons are more likely to exploit leading-line landscape features, e.g., a road or the border of a woodlot, in developing flight-path fidelity and 3) even when flying a straight path HF-lesioned homing pigeons are more likely to display relatively rapid, oscillatory heading changes as if casting about for sensory, presumably visual information. The flight behaviour differences between the intact and HF-lesioned pigeons persisted across the four releases from the three locations, although the differences became smaller with increasing experience. Taken together, the GPS-track data offer a detailed characterisation of the effects of HF lesion on landscape-based, homing pigeon navigation, offering new insight into the role of the hippocampal formation in supporting memory-related, e.g., fidelity to a familiar route home, and perhaps perceptual-related, e.g., oscillating headings, navigational processes.
- Data packageData from: Pigeons remember visual landmarks after one release and rely upon them more if they are anosmic(2020-09-24) Gagliardo, Anna; Pollonara, Enrica; Wikelski, MartinAnosmic birds' homing ability is impaired when challenged to navigate over unfamiliar areas. Nevertheless, anosmic pigeons, Columba livia, show unimpaired navigation when released within a familiar area, suggesting that they may rely on familiar visual landmarks for navigation. However, direct evidence for the reliance on familiar visual landmarks during homing in anosmic birds has never been provided. In this study we tracked pigeons subjected singly to one training flight from each of three locations. Prior to their second release from each site, half of the birds were made anosmic while the others were not manipulated. The level of route fidelity was analysed separately for three phases of the homing process, in which familiar visual cues may have different relevance and may be used within different cognitive strategies: (1) ‘Initial decision making’; (2) ‘En route navigation’; (3) ‘Local navigation around home’. Compared to control birds, the anosmic birds flew significantly closer to previously overflown locations in the ‘En route navigation’ phase, while no difference in route fidelity emerged during phases (1) and (3). Our results showed that a single experience is sufficient for pigeons to learn release site features, and that familiar visual landmarks constitute a critical source of navigational information in olfactorily deprived birds during the homing process.
- Data packageData from: Olfaction and topography, but not magnetic cues, control navigation in a pelagic seabird: displacements with shearwaters in the Mediterranean Sea(2015-10-27) Pollonara, Enrica; Luschi, Paolo; Guilford, Tim; Wikelski, Martin; Bonadonna, Francesco; Gagliardo, AnnaPelagic 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.
- Data packageData from: The homing pigeons’ olfactory map is affected by geographical barriers(2021-01-19) Gagliardo, Anna; Pollonara, Enrica; Wikelski, MartinThe factors affecting the olfaction-based navigational performances of homing pigeons released at relatively long distance (beyond 100 km from home) has in the past been subject to several investigations both in Germany and Italy using observations of vanishing bearing distributions. These studies highlighted the complexity of long-distance navigation in homing pigeons, which remains a poorly investigated aspect. In this tracking study we report how the homing performances of pigeons housed in Amino (Pisa, Italy) were affected by the presence/absence of a mountain range (the Northern Apennines) interposed between the home and the release site area (release sites: Trans = mountain barrier, Cis = no mountain barrier). We displaced unmanipulated control pigeons, anosmic pigeon, and pigeons transported in purified air to release sites located at a distance ranging between 95 and 246 km from home. There, birds were released without further manipulation. The navigational performances of anosmic pigeons were impaired at both Cis and Trans sites compared to both smelling groups. Both unmanipulated control pigeons and pigeons transported in purified air but allowed to smell environmental air at both the release site and after release displayed unimpaired navigational abilities at the Cis site, but impaired homing success and impaired homeward orientation at the Trans sites. Nevertheless, their homeward component was significantly greater than that of the anosmic birds at both geographical areas. This suggests that the Northern Apennine acts as a geographical barrier affecting the olfactory map accuracy of Amino pigeons, rather than totally reducing its spatial extent.
- Data packageData from: Productivity changes in the Mediterranean Sea drive foraging movements of yelkouan shearwater Puffinus yelkouan from the core of its global breeding range(2021-12-10) Pezzo, Francesco; Zenatello, Marco; Cerritelli, Giulia; Navone, Augusto; Giunchi, Dimitri; Spano, Giovanna; Pollonara, Enrica; Massolo, Alessandro; Gagliardo, Anna; Baccetti, NicolaPelagic seabirds are tied to their breeding colonies throughout their long-lasting breeding season, but at the same time, they have to feed in a highly dynamic marine environment where prey abundance and availability rapidly change across space and seasons. Here, we describe the foraging movements of yelkouan shearwater Puffinus yelkouan, a seabird endemic to the Mediterranean Sea that spends its entire life cycle within this enclosed basin and whose future conservation is intimately linked to human-driven and climatic changes affecting the sea. The aim was to understand the main factors underlying the choice of foraging locations during the reproductive phases. A total of 34 foraging trips were obtained from 21 breeding adults tagged and tracked on Tavolara Archipelago (N Sardinia, Italy). This is the largest and most important breeding area for the species, accounting for more than 50% of the world population. The relationships between foraging movements during two different breeding stages and the seasonal changes of primary productivity at sea were modeled. Movements appeared to be addressed toward inshore (<20 km), highly productive, and relatively shallow (<200 m) foraging areas, often in front of river mouths and at great distances from the colony. During incubation, the Bonifacio Strait and other coastal areas close to North and West Sardinia were the most preferred locations (up to 247 km from the colony). During the chick-rearing phase, some individuals reached areas placed at greater distances from the colony (up to 579 km), aiming at food-rich hotspots placed as far north as the Gulf of Lion (France). The need for such long distance and long-lasting foraging trips is hypothesized to be related to unfavorable conditions on the less productive (and already depleted) Sardinian waters.
- Data packageData from: GPS tracking technology and re-visiting the relationship between the avian visual wulst and homing pigeon navigation(2024-04-02) Cioccarelli, Sara; Giunchi, Dimitri; Pollonara, Enrica; Casini, Giovanni; Bingman, Verner P.; Gagliardo, AnnaWithin their familiar areas homing pigeons rely on familiar visual landscape features and landmarks for homing. However, the neural basis of visual landmark-based navigation has been so far investigated mainly in relation to the role of the hippocampal formation. The avian visual Wulst is the telencephalic projection field of the thalamofugal pathway that has been suggested to be involved in processing lateral visual inputs that originate from the far visual field. The Wulst is therefore a good candidate for a neural structure participating in the visual control of familiar visual landmark-based navigation. We repeatedly released and tracked Wulst-lesioned and control homing pigeons from three sites about 10-15 km from the loft. Wulst lesions did not impair the ability of the pigeons to orient homeward during the first release from each of the three sites nor to localise the loft within the home area. In addition, Wulst-lesioned pigeons displayed unimpaired route fidelity acquisition to a repeated homing path compared to the intact birds. However, compared to control birds, Wulst-lesioned pigeons displayed persistent oscillatory flight patterns across releases, diminished attention to linear (leading lines) landscape features, such as roads and wood edges, and less direct flight paths within the home area. Differences and similarities between the effects of Wulst and hippocampal lesions suggest that although the visual Wulst does not seem to play a direct role in the memory representation of a landscape-landmark map, it does seem to participate in influencing the perceptual construction of such a map.
- Data packageData from: GPS-profiling of retrograde navigational impairments associated with hippocampal lesion in homing pigeons(2021-06-15) Gagliardo, Anna; Colombo, Silvia; Pollonara, Enrica; Casini, Giovanni; Rossino, Maria Grazia; Wikelski, Martin; Bingman, Verner P.The avian hippocampal formation (HF) is homologous to the mammalian hippocampus and plays a central role in the control of spatial cognition. In homing pigeons, HF supports navigation by familiar landmarks and landscape features. However, what has remained relatively unexplored is the importance of HF for the retention of previously acquired spatial information. For example, to date, no systematic GPS-tracking studies on the retention of HF-dependent navigational memory in homing pigeons have been performed. Therefore, the current study was designed to compare the pre- and post-surgical navigational performance of sham-lesioned control and HF-lesioned pigeons tracked from three different sites located in different directions with respect to home. The pre- and post-surgical comparison of the pigeons’ flight paths near the release sites and before reaching the area surrounding the home loft (4 km radius from the loft) revealed that the control and HF-lesioned pigeons displayed similarly successful retention. By contrast, the HF-lesioned pigeons displayed dramatically and consistently impaired retention in navigating to their home loft during the terminal phase of the homing flight near home, i.e., where navigation is supported by memory for landmark and landscape features. The data demonstrate that HF lesions lead to a dramatic loss of pre-surgically acquired landmark and landscape navigational information while sparing those mechanisms associated with navigation from locations distant from home.
- Data packageData from: Evidence for pre-mnemonic, perceptual neglect of environmental features in hippocampal lesioned pigeons during homing(2014-07-31) Gagliardo, Anna; Pollonara, Enrica; Coppola, Vincent J; Santos, Carlos David; Bingman, Verner P.The importance of the vertebrate hippocampus in spatial cognition is often related to its broad role in memory. However, in birds, the hippocampus appears to be more specifically involved in spatial processes. The maturing of GPS-tracking technology has enabled a revolution in navigation research, including the expanded possibility of studying brain mechanisms that guide navigation in the field. By GPS-tracking homing pigeons released from distant, unfamiliar sites prior to and after hippocampal lesion, we observed, as has been reported previously, impaired navigational performance postlesion over the familiar/memorized space near the home loft, where topographic features constitute an important source of navigational information. The GPS-tracking revealed that many of the lost pigeons, when lesioned, approached the home area, but nevertheless failed to locate their loft. Unexpectedly, when they were hippocampal-lesioned, the pigeons showed a notable change in their behaviour when navigating over the unfamiliar space distant from home; they actually flew straighter homeward-directed paths than they did prelesion. The data are consistent with the hypothesis that, following hippocampal lesion, homing pigeons respond less to unfamiliar visual, topographic features encountered during homing, and, as such, offer the first evidence for an unforeseen, perceptual neglect of environmental features following hippocampal damage.
- Data packageData from: Unilateral hippocampal lesions and the navigational performance of homing pigeons as revealed by GPS-tracking(2022-12-13) Gagliardo, Anna; Pollonara, Enrica; Bingman, Verner P.; Casini, GiovanniThe left and right hippocampal formation (HF) of the avian brain have been reported to control some different aspects of homing in pigeons. In the current study, we employed GPS-tracking technology and unilateral HF lesions to further explore what if any aspects of a pigeon’s homing flight might be under dominant control by either the left or right HF. Pigeons were released from three locations prior to any experimental manipulation and released repeatedly from the same three sites as sham-lesioned control, right HF-lesioned and left HF-lesioned treatment groups. Analyses of homing performance and virtual vanishing bearings revealed no effect of either lesion treatment. A more in-depth analysis of path efficiency during the initial decision-making, en route and near home phases of a homing flight also revealed no effect of either lesion treatment. A last analysis on the learning and memory for positions along a previously flown route, a proxy for investigating the development of route fidelity, also revealed no effect of either unilateral lesion. However, independent of treatment group, some statistically significant effects were observed with respect to changes in performance across training and the different release sites. The current study revealed no detectable difference between the left and right HF-lesioned pigeons with respect to several navigational parameters of a homing flight. Although in need of supporting experimentation, the results are consistent with the hypothesis that both the left and right HF are similarly able to support several aspects of homing pigeon navigation.
- Data packageData from: Only natural local odours allow homeward orientation in homing pigeons released at unfamiliar sites(2018-08-30) Gagliardo, Anna; Pollonara, Enrica; Wikelski, MartinAccording to the olfactory navigation hypothesis, birds are able to exploit the spatial distribution of environmental odourants to determine the direction of displacement and navigate from non-familiar locations. The so-called “olfactory activation hypothesis” challenged the specific role of olfactory cues in navigation by suggesting that olfactory stimuli only activate a navigational system that is based on non-olfactory cues, predicting that even artificial odourants alone are sufficient to allow unimpaired navigation. In this experiment, we compared tracks of experimental birds exposed to different olfactory stimuli before being made anosmic at the release site prior to release. One group of pigeons was exposed to purified air enriched with artificial odourants, while a second group was exposed to environmental air. The birds stimulated with artificial nonsense odourants displayed several behavioural differences from both untreated controls and anosmic pigeons exposed to environmental air prior to release: nonsense odourants birds were unable to determine the home direction, they mostly flew within a space outside the homeward oriented quadrant, and they flew shorter distances on the day of release. Our data failed to support a mere activational role of olfactory stimuli in navigation, and are consistent with the olfactory navigation hypothesis.