The ontogeny of the homing pigeon navigational map: evidence for a sensitive learning period

Homing pigeons can learn a navigational map by relying on the heterogeneous distribution of atmospheric odours in the environment. To test whether there might be a sensitive period for learning an olfactory-based navigational map, we maintained a group of young pigeons in an aviary screened from the winds until the age of three to four months post-fledging. Subsequently, the screens were removed and the pigeons were exposed to the winds and the environmental odours they carry for three months. One control group of pigeons was held in a similar aviary but exposed to the winds immediately upon Hedging, while another control group of pigeons was allowed free-flight. When the pigeons from the three groups were released from two distant release sites at about six months of age post-fledging, the two control groups were found to be equally good at orientating and returning home, while the experimental pigeons held in the shielded aviary for the first three months post-fledging were unable to orientate homeward and they were generally unsuccessful in returning home. This result supports the hypothesis that environmental experience during the first three months post-fledging is critical for some aspect of navigational map learning and that navigational map learning displays sensitive period-like properties.     

Positional entropy during pigeon homing II: navigational interpretation of Bayesian latent state models

In these two companion papers we introduce a new approach to the analysis of bird navigation which brings together several novel mathematical and technical applications. Miniaturized GPS logging devices provide track data of sufficiently high spatial and temporal resolution that considerable variation in flight behaviour can be observed remotely from the form of the track alone. We analyse a fundamental measure of bird flight track complexity, spatio-temporal entropy, and explore its state-like structure using a probabilistic hidden Markov model. The emergence of a robust three-state structure proves that the technique has analytical power, since this structure was not obvious in the tracks alone. We propose the hypothesis that positional entropy is indicative of underlying navigational uncertainty, and that familiar area navigation may break down into three states of navigational confidence. By interpreting the relationship between these putative states and features on the map, we are able to propose a number of hypothetical navigational strategies feeding into these states. The first of these two papers details the novel technical developments associated with this work and the second paper contains a navigational interpretation of the results particularly with respect to visual features of the landscape.     

Pigeon homing along highways and exits

BACKGROUND: Anecdotal observations and early airplane and helicopter tracking studies suggest that pigeons sometimes follow large roads and use landmarks as turning points during their homeward journey. However, technical limitations in tracking pigeon routes have prevented proof. RESULTS: Here, we present experimental and statistical evidence for this strategy from the analysis of 216 GPS-recorded pigeon tracks over distances up to 50 km. Experienced pigeons released from familiar sites during 3 years around Rome, Italy, were significantly attracted to highways and a railway track running toward home, in many cases without anything forcing them to follow such guide-rails. Birds often broke off from the highways when these veered away from home, but many continued their flight along the highway until a major junction, even when the detour added substantially to their journey. The degree of road following increased with repeated releases but not flight length. Significant road following (in 40%-50% of the tracks) was mainly observed from release sites along northwest-southeast axis. CONCLUSIONS: Our data demonstrate the existence of a learned road-following homing strategy of pigeons and the use of particular topographical points for final navigation to the loft. Apparently, the better-directed early stages of the flight compensated the added final detour. During early and middle stages of the flight, following large and distinct roads is likely to reflect stabilization of a compass course rather than the presence of a mental roadmap. A cognitive (roadmap) component manifested by repeated crossing of preferred topographical points, including highway exits, is more likely when pigeons approach the loft area. However, it might only be expected in pigeons raised in an area characterized by navigationally relevant highway systems.     

Development of the navigational map in homing pigeons: effects of flight experience on orientation performance

Experiments have shown that pigeons, Columba livia, are able to develop navigational abilities even if reared and kept confined in an aviary, provided that they are exposed to the natural winds. In contrast, pigeons reared in a wind-screened aviary do not learn to navigate. Pigeons kept confined in a screened aviary when young do not learn to navigate even if, once they become adult, the screens are removed and the birds are exposed to natural winds for a period sufficiently long for map learning. In all of these experiments, pigeons were kept confined until the day of test release. In the present study we found that pigeons reared in a wind-screened aviary developed navigational abilities if, once adult, they were allowed to perform spontaneous flights around the loft. Nevertheless, their navigational performance never reached the level of controls.Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.      

Pigeon navigation: Effects upon homing behaviour by reversing wind direction at the loft

Summary In order to test the nature of the information acquired by pigeons at home and utilized as map component in their navigational mechanism, groups of birds were kept since fledging time in glass corridors, which had their main axis oriented E-W (or ESE-WNW). Referring to the quadrants centered by these directions as experimental quadrants, the treatment of the birds was as follows. Whenever a wind was blowing from one of the experimental quadrants, C1-and C-birds were subjected to an artificial air current blowing from the center of the same quadrant, and E-birds to air currents from the center of the opposite quadrant. C2-birds, reared in a corridor which was unscreened at both ends, were not treated with artificial winds and could perceive the natural winds from the experimental quadrants. Finally, S-birds were never exposed to either natural or artificial winds.When released from directions comprised in the xperimental quadrants, C-, C1-, and C2-birds were homeward oriented, while E-birds oriented themselves toward the opposite direction (Fig. 7), and S-birds' bearings were random. The homing performances of E-birds were poorer than those of the other birds, and on some releases, disastrous.It is concluded that the information that pigeons acquire at home and then use for navigational purposes is wind borne and can be conveyed by an artificial air current. This confirms previous results which indicated the olfactory nature of the information.Dedicated to Prof. Dr. H. Autrum, on occasion of his seventieth birthdayThis study was supported by the Cosiglio Nazionale delle Ricerche. We thank the Command of the Brigata Paracadutisti Folgore, Italian Army, which kindly allowed us to use a power boat for the releases from over the sea. We also wish to thank Dr. R.F. Hartwick for valuable help with some experiments and for stimulating discussions, Mr G. Mela and Mr D. Moretti for constructing the control drices for the fans.     

Backtracking behaviour in lost ants: an additional strategy in their navigational toolkit

Ants use multiple sources of information to navigate, but do not integrate all this information into a unified representation of the world. Rather, the available information appears to serve three distinct main navigational systems: path integration, systematic search and the use of learnt information—mainly via vision. Here, we report on an additional behaviour that suggests a supplemental system in the ant''s navigational toolkit: ‘backtracking’. Homing ants, having almost reached their nest but, suddenly displaced to unfamiliar areas, did not show the characteristic undirected headings of systematic searches. Instead, these ants backtracked in the compass direction opposite to the path that they had just travelled. The ecological function of this behaviour is clear as we show it increases the chances of returning to familiar terrain. Importantly, the mechanistic implications of this behaviour stress an extra level of cognitive complexity in ant navigation. Our results imply: (i) the presence of a type of ‘memory of the current trip’ allowing lost ants to take into account the familiar view recently experienced, and (ii) direct sharing of information across different navigational systems. We propose a revised architecture of the ant''s navigational toolkit illustrating how the different systems may interact to produce adaptive behaviours.     

Pigeon homing and magnetic fields: a response to Luschi et al. (1996)

This paper comments on an article ''Pigeon homing: evidence against reliance on magnetic information picked up en route at release sites'' by P. Luschi, C. del Seppia, E. Crosio and F. Papi, which appeared in this journal. It is pointed out that the particular effects which these authors show to be stress-induced artefacts are restricted to their specific strain of homing pigeons. The same effects could not be observed in pigeons from two other lofts: a difference in response that was shown to have a genetic base. In view of this, conclusions drawn from the results of Luschi et al. must be restricted to their own findings; they cannot be generalized to the other findings which indicate the use of magnetic outward journey information in young homing pigeons.     

iCatch:a new strategy for capturing large DNA fragments using homing endonucleases

Natural genetic materials contain many biosynthetic gene clusters encoding potentially valuable natural products,many of which can be used directly without codon optimization or other manipulations.With the development of synthetic biology,several DNA assembly standards have been proposed,conveniently facilitating the reuse of natural materials.Among these standards,the iBrick assembly standard was developed by our laboratory to manipulate large DNA fragments,employing two homing endonucleases.Considering the difficulty of cloning large iBrick parts using conventional endonuclease-mediated restriction and ligation methods,we herein present a new method,known as iCatch,which readily captures biosynthetic gene clusters.As the clusters cloned by iCatch have the prefix and suffix of the iBrick standard,they serve as new iBrick parts and are therefore conducive to further editing and assembly with the iBrick standard.iCatch employs the natural homologous recombination system to flank the region of interest with I-Scel and PI-Pspl recognition sites,after which the genome is digested with I-Scel or PI-Pspl and the fragments are then self-ligated to clone the target DNA fragments.We used this method to successfully capture the actinorhodin biosynthetic cluster from Streptomyces coelicolor and then heterologously expressed this cluster in a thermophilic Streptomyces strain.We propose that iCatch can be used for the cloning of DNA sequences that are dozens of kilobases in length,facilitating the heterologous expression of microbial natural products.Moreover,this cloning methodology can be a complementary tool for the iBrick standard,especially in applications requiring the manipulation of large DNA fragments.     

The orientation of homing pigeons in relation to change in sun declination

Summary The sun navigation hypothesis ofMatthews is briefly reviewed with special reference to his sun occlusion experiment which supports this hypothesis. The results of a similar experiment are presented in which 13 young pigeons were kept from sight of the sun during a seven day period including the fall equinox while the sun height at noon decreased 3° 6.7. When the birds were released from a point 93 km. south of their loft they were exposed to a noon sun height equal to that of a point north of their home loft eight days earlier. Nevertheless they showed a northward orientation as did the 10 control birds with no difference in homing performance between the experimental and control groups. These results are not in agreement with those ofMatthews and do not support his sun navigation hypothesis.

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Zusammenfassung Die Sonnennavigations-Hypothese vonMatthews wird kurz besprochen, besonders im Hinblick auf den Warte-Versuch (Sun occlusion experiment), der unter anderem zur Prüfung der Hypothese angestellt wurde. Die Ergebnisse eines im Wilhelmshavener Gebiet angestellten Warteversuchs werden mitgeteilt: 13 Tauben wurden um die Herbst-Tagundnachtgleiche für 7 Tage ohne Sicht der Sonne gehalten, deren Mittagshöhe in dieser Zeit um 3° 6,7 abnahm. Als die Vögel 93 km südlich ihres Heimatorts aufgelassen wurden, befanden sie sich im Gebiet einer Mittags-Sonnenhöhe gleich der, welche vor der Warteperiode etwa 2° nördlich vom Heimatort herrschte. Trotzdem flogen sie gleich den Kontrollen nordwärts ab. Auch im Heimkehrerfolg bestand kein Unterschied zwischen Versuchs-und Kontrolltauben. Diese Ergebnisse stimmen mit den vonMatthews berichteten nicht überein und stützen seine Sonnen-Navigations-Hypothese nicht.

     

The ontogeny of territoriality during maturation

Territoriality drives the evolution of many mating systems, yet has remained an extremely difficult trait to measure in the wild. Classic studies rely on the theoretical framework of resource holding potential (RHP) as a predictor of success in territory acquisition. However, mounting evidence suggests that an individual's RHP may change over short time scales. Previous studies suggest that RHP is best understood by considering two categories of territoriality, resource defending and resource usurping potential (RDP and RUP, respectively). In a population of the side-blotched lizard, Uta stansburiana, blue-throated males defend territories near their natal site (RDP) while mature orange-throated males use their RUP to sequester high quality territories from defending territorial males. We tested differences in territoriality by releasing pairs of maturing male lizards onto experimentally altered territories that had improved thermal qualities owing to the addition of rock piles. Dyads of males competed for these thermal resources and the females that were released on rock piles. Early in the season, when throat colors were not yet fully expressed, large male body size predicted contest victories irrespective of throat color. This pattern changed however, with the onset of the breeding season and maturation of throat color. Orange males tended to usurp territories from blue males within 2 weeks of contest initiation. Large male body size still influenced these contests, but after one more week, throat color was the sole factor explaining variance in territory ownership. We demonstrate the ontogeny of territoriality relating to body size and throat color during maturation, and suggest a novel approach to assessing territoriality and aggression in the wild.     

Pharmacological inhibition of caspase and calpain proteases: a novel strategy to enhance the homing responses of cord blood HSPCs during expansion

Background

Expansion of hematopoietic stem/progenitor cells (HSPCs) is a well-known strategy employed to facilitate the transplantation outcome. We have previously shown that the prevention of apoptosis by the inhibition of cysteine proteases, caspase and calpain played an important role in the expansion and engraftment of cord blood (CB) derived HSPCs. We hypothesize that these protease inhibitors might have maneuvered the adhesive and migratory properties of the cells rendering them to be retained in the bone marrow for sustained engraftment. The current study was aimed to investigate the mechanism of the homing responses of CB cells during expansion.

Methodology/Principal Findings

CB derived CD34⁺ cells were expanded using a combination of growth factors with and without Caspase inhibitor -zVADfmk or Calpain 1 inhibitor- zLLYfmk. The cells were analyzed for the expression of homing-related molecules. In vitro adhesive/migratory interactions and actin polymerization dynamics of HSPCs were assessed. In vivo homing assays were carried out in NOD/SCID mice to corroborate these observations. We observed that the presence of zVADfmk or zLLYfmk (inhibitors) caused the functional up regulation of CXCR4, integrins, and adhesion molecules, reflecting in a higher migration and adhesive interactions in vitro. The enhanced actin polymerization and the RhoGTPase protein expression complemented these observations. Furthermore, in vivo experiments showed a significantly enhanced homing to the bone marrow of NOD/SCID mice.

Conclusion/Significance

Our present study reveals another novel aspect of the regulation of caspase and calpain proteases in the biology of HSPCs. The priming of the homing responses of the inhibitor-cultured HSPCs compared to the cytokine-graft suggests that the modulation of these proteases may help in overcoming the major homing defects prevalent in the expansion cultures thereby facilitating the manipulation of cells for transplant procedures.     

Major cranial changes during Triceratops ontogeny

This is the first cranial ontogenetic assessment of Triceratops, the well-known Late Cretaceous dinosaur distinguished by three horns and a massive parietal-squamosal frill. Our analysis is based on a growth series of 10 skulls, ranging from a 38 cm long baby skull to about 2 m long adult skulls. Four growth stages correspond to a suite of ontogenetic characters expressed in the postorbital horns, frill, nasal, epinasal horn and epoccipitals. Postorbital horns are straight stubs in early ontogeny, curve posteriorly in juveniles, straighten in subadults and recurve anteriorly in adults. The posterior margin of the baby frill is deeply scalloped. In early juveniles, the frill margin becomes ornamented by 17-19 delta-shaped epoccipitals. Epoccipitals are dorsoventrally compressed in subadults, strongly compressed and elongated in adults and ultimately merge onto the posterior frill margin in older adults. Ontogenetic trends within and between growth stages include: posterior frill margin transitions from scalloped to wavy and smooth; progressive exclusion of the supraoccipital from the foramen magnum; internal hollowing at the base of the postorbital horns; closure of the midline nasal suture; fusion of the epinasal onto the nasals; and epinasal expansion into a morphologically variable nasal horn. We hypothesize that the changes in horn orientation and epoccipital shape function to allow visual identity of juveniles, and signal their attainment of sexual maturity.     

The antibody response during amphibian ontogeny

The maturation of the anti DNP-response in adult and larval amphibians has been compared in two species of anurans,Rana catesbeiana andXenopus laevis. IgM responses were very similar in larvae and adults of both species. Specific IgG antibody synthesis, studied inRana catesbeiana only, was not obvious in larval primary response but was easily detectable in adults. Although metamorphosis results in profound changes in the lymphoid system associated with the apparent acquisition of self tolerance to new antigens, immunological memory of antigens injected during larval life ofRana andXenopus persists after the metamorphosis period.