Olfactory navigation versus olfactory activation: a controversy revisited

Journal of Comparative Physiology A, Jun 2018

In the early 1970s, Floriano Papi and colleagues proposed the olfactory-navigation hypothesis, which explains the homing ability of pigeons by the existence of an odor-based map acquired through learning. This notion, although supported by some observations, has also generated considerable controversy since its inception. As an alternative, Paulo Jorge and colleagues formulated in 2009 the olfactory-activation hypothesis, which states that atmospheric odorants do not provide navigational information but, instead, activate a non-olfactory path integration system. However, this hypothesis is challenged by an investigation authored by Anna Gagliardo and colleagues and published in the current issue of the Journal of Comparative Physiology A. In this editorial, the significance of the findings of this study is assessed in the broader context of the role of olfaction in avian navigation and homing, and experiments are suggested that might help to finally resolve the olfactory-navigation versus olfactory-activation controversy.

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Olfactory navigation versus olfactory activation: a controversy revisited

Journal of Comparative Physiology A https://doi.org/10.1007/s00359 Olfactory navigation versus olfactory activation: a controversy revisited Charles Walcott 0 1 Wolfgang Wiltschko 0 1 Roswitha Wiltschko 0 1 Günther K. H. Zupanc 0 1 0 Laboratory of Neurobiology, Department of Biology, Northeastern University , 360 Huntington Avenue, Boston, MA 02115 , USA 1 Fachbereich Biowissenschaften, J.W. Goethe-Universität Frankfurt am Main , 60438 Frankfurt am Main , Germany 2 Günther K. H. Zupanc In the early 1970s, Floriano Papi and colleagues proposed the olfactory-navigation hypothesis, which explains the homing ability of pigeons by the existence of an odor-based map acquired through learning. This notion, although supported by some observations, has also generated considerable controversy since its inception. As an alternative, Paulo Jorge and colleagues formulated in 2009 the olfactory-activation hypothesis, which states that atmospheric odorants do not provide navigational information but, instead, activate a non-olfactory path integration system. However, this hypothesis is challenged by an investigation authored by Anna Gagliardo and colleagues and published in the current issue of the Journal of Comparative Physiology A. In this editorial, the significance of the findings of this study is assessed in the broader context of the role of olfaction in avian navigation and homing, and experiments are suggested that might help to finally resolve the olfactorynavigation versus olfactory-activation controversy. Pigeon; Homing; Atmospheric odorants; Olfactory-navigation hypothesis; Olfactory-activation hypothesis Introduction As one of the editors of the Journal of Comparative Physiology A, I always take great pleasure in receiving and handling manuscripts on animal navigation, migration, and homing. This was also the case when Anna Gagliardo, Enrica Pollonara, and Martin Wikelski submitted the paper that is published in the journal’s current issue (Gagliardo et al. 2018) . In this study, the authors present findings that the authors interpret as inconsistent with the so-called olfactory-activation hypothesis. This hypothesis states that olfactory stimuli play a role in navigation of pigeons during homing, yet their function is restricted to the activation of navigational systems based on non-olfactory cues (Jorge et al. 2009, 2010) . Department of Neurobiology and Behavior, Cornell University, Ithaca, NY 14853, USA The olfactory-activation hypothesis has challenged earlier claims by other authors, most notably Floriano Papi and co-authors (Papi et al. 1971, 1972) , that pigeons learn at their home lofts to associate atmospheric odorants with the direction of winds, which serve as vehicles of these odorants. According to this hypothesis, which has become known as the olfactory-navigation hypothesis or olfactorymap hypothesis, pigeons use this information to construct an odor-based map. In combination with a compass system, this positional information enables them to return to their loft after displacement. Although some experimental data are in agreement with the olfactory-navigation hypothesis (for reviews see Wallraff 2004, 2005) , skepticism has persisted since the publication of Papi and colleagues’ paper in 1971. This skepticism was fueled more recently by the experiments conducted by Paulo E. Jorge and colleagues, in which they demonstrated that the orientation of pigeons exposed to artificial odorants that did not contain any navigational information was undistinguishable from the behavior of pigeons exposed to natural odorants, as long as the birds had access to these odorants during displacement (Jorge et al. 2009, 2010) . On the other hand, the pigeons were disoriented when they were deprived of odors during displacement. These observations prompted the authors to propose that odors do not provide navigational information but, instead, activate a non-olfactory path integration system. Exactly this hypothesis is challenged by the current paper of Gagliardo and colleagues. Based on GPS tracking experiments, their study has failed to find support for the idea of a mere activational role of olfactory stimuli, but seems to be in agreement with the olfactory-navigation hypothesis (Gagliardo et al. 2018) . Readers who have followed the development of avian navigation research may be puzzled at this point. Over nearly five decades, they have witnessed cycles of both support and disapproval of the olfactory-navigation hypothesis, leaving perhaps some of them wonder in which direction the pendulum might swing next. A weakness that prevents us from reaching a final verdict is that no experimental result published so far has proven the olfactory-navigation hypothesis (or an alternative to it) unambiguously. However, as history teaches us, controversies have preceded many scientific theories before they became widely accepted (Sherwood 2011) . Controversies did not stop Bill Keeton from inviting (...truncated)


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Charles Walcott, Wolfgang Wiltschko, Roswitha Wiltschko, Günther K. H. Zupanc. Olfactory navigation versus olfactory activation: a controversy revisited, Journal of Comparative Physiology A, 2018, pp. 1-4, DOI: 10.1007/s00359-018-1273-1