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)