Ital. J. Zool., 68: 171-180 (2001)
Animal navigation at the end of the
century: a retrospect and a look
forward*
FLORIANO PAPI
Dipartimento di Etologia, Ecologia ed Evoluzione, Università di Pisa,
via A. Volta 6, I-56126 Pisa (Italy)
ABSTRACT
Around the middle of the 20th century the discovery of the biological compasses - solar, lunar, stellar and magnetic - marked a
fundamental breakthrough in the study of the orientation and
navigation of animals. This discovery attracted a great number of
scholars to this field of research, and contributed to our knowledge of frequently recurrent phenomena such as zonal maintenance in ecotonal environments and the guidance of migratory and
foraging movements. Several lines of research that emerged were
pertinent to and continue to stimulate the study of the genetic
and acquired components of orientation and its sensory foundations. The years in which the biological compasses were discovered also opened up the problem of the nature and function of
animal maps, which are often integrated with the use of one or
more compasses, and enable the animal to fix its position within
a relatively extensive territory. The maps can derive from a direct
knowledge of a geographical area, and are thus indicated as cognitive or mental, or they can extend beyond the places already
visited by the animal. Although this second type of map is probably widespread, it has been ascertained and analysed only in the
homing pigeon. The olfactory nature of the pigeon’s map has
found confirmation in neuroethological studies, and in the discovery that quantitative relations between certain organic substances
dispersed in the atmosphere characterise different geographical
areas and show enough persistency over space and time to allow
them to act as the material substrate for olfactory navigation. Obstacles to progress in the field of animal navigation include what
is still a poor level of knowledge about the mechanism of magnetic reception and about the physiological effects of experimental magnetic treatments, as well as the widespread but groundless
opinion that animals possess a magnetic map. Progress in telemetric recording of routes, even over long distances, have made it
possible to extend studies to new subjects and new environments. The satellite monitoring of the movements of ocean-crossing birds and sea turtles has begun to reveal a remarkable navigational capacity in both groups - a capacity based on mechanisms
which are still unknown.
KEY WORDS: Animal orientation - Animal navigation - Migration.
* Opening lecture presented at the 19th Congress of the “Società
Italiana di Etologia” (S. Giuliano, Pisa - October 4-6, 2000) held in
honour of the late professor Leo Pardi.
(Received 3 May 2001 - Accepted 28 May 2001)
INTRODUCTION
At this congress, held in honour of the scientific work
of Leo Pardi, many ethologists who are here were his
pupils in one or other of the two fields which he cultivated with great success and enthusiasm, animal orientation and the behaviour of social wasps. When I decided to pay homage to him by preparing the present contribution, I realised I would not be able to address all
the aspects of animal navigation, which are many and
varied, whether we consider the various animal groups,
the environments in which navigation takes place, or
the mechanisms and the orienting cues involved. The
present paper is not a review of the research on animal
navigation, but a choice of topics suggested by personal
experience and by contacts with colleagues, especially
Italian ones; and also by the greater fascination that certain phenomena hold - those still totally unexplained which are at the stage of research Gustav Kramer used
to call the ‘romantic phase’, perhaps because the large
number of possible solutions leaves more freedom for
the ingenuity and imagination of the experimenter,
while, when the problems are already circumscribed,
the solutions can almost be predicted, and they only require suitable verification.
A GLANCE AT THE PAST: THE DISCOVERIES OF THE
MYRMECOLOGISTS
We are at the end of a century of great scientific
achievements and there is the desire to look back, to
see how rapidly - or slowly? - we have proceeded in
our field, or in any case to consider the progress made
in the last hundred years. To do this I would like to recall some milestones. At the beginning of the century,
the first significant findings came from the myrmecologists. In 1904 a young French researcher, Henri Piéron,
carried out an extremely simple experiment on an ant,
which, leaving its nest, reached a point where it found
food and was about to return. Piéron moved the ant a
little bit further on, put it down again on the ground
and observed its behaviour. The ant set off and went on
a journey which was equal in length and direction to
the journey it would have made if it had not been
moved. In this way Piéron discovered that the ant was
able to return to its nest solely on the basis of the information it had collected on the journey out, regardless of
the surrounding landscape or local stimuli.
The phenomenon was immediately confirmed by others, but remained unexplained until Felix Sanschi (1911,
1923), a Francophone Swiss, doctor by profession and
amateur myrmecologist, set out in search of “a source
of stimulation that had a ubiquitous action like the magnetic pole for sailors” and could therefore guide the ant
in the opposite direction that of the outward journey,
even in an unfamiliar environment. In 1911 he discovered this source in the sun and demonstrated, with the
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famous mirror experiment, that ants are able to go in a
particular geographical direction by maintaining a fixed
angle with the sun. He also posed the question of
whether ants took into account the apparent movement
of the sun, and therefore actually possessed a compass,
but obtained negative results. The discovery of the phenomenon of compensation of the movement of the sun
and that of the other biological compasses did not occur until the middle of the century.
THE STUDY OF TAXES
Meanwhile, however, studies of the simpler and more
fundamental mechanisms of orientation flourished, the
tropisms of Jennings (1906) and Loeb (1918), later renamed taxes by Kühn (1919), classified and revised by
Fraenkel and Gunn (1940). This research was mainly
carried out in the laboratory, on animals with a low level of organisation, and the meaning of the findings is
often obscure, so that it was sometimes jokingly asked
if taxes were not a product of the laboratory, and therefore had no meaning in the life of the animal. This criticism is justified, partly because this approach to animal
orientation was based on the concept of a machine-like
animal that reacts to stimuli in a forced, stereotyped
manner. It was logical that, when phenomena of orientation in nature began to be studied and their biological
meaning to be understood - I refer to the discovery of
biological compasses - the study of taxes underwent a
crisis. Today, however, we are seeing a reassessment of
this approach, because the importance of taxes in the
study of the ontogenesis of more complex orientation
phenomena has been understood. Stereotypical tactic
reactions are often the innate endowment of the young
animal, which will modify and adapt them according to
experience, and, therefore, through learning processes
which will transform the machine-like animal into an
organism capable of providing responses which may be
individually and temporally different according to the
demands of the environment. This concept was amply
developed recently by Campan (1997), who exemplified
it on models taken from his own studies, the cricket
Nemobius campestris, and the sandhopper Talitrus
saltator, in so doing utilising the studies of the Pardi
school, above all those of Scapini and Ugolini (see
Campan, 1997, for references).
F. PAPI
1951 by Kramer in the starling. Very soon after, between
1952 and 1953 Pardi and I published data on the sun
and moon compass in the sandhopper, Talitrus saltator
(Pardi & Papi, 1952, 1953; Papi & Pardi, 1953), with
many new findings on the compensation of the apparent motion of the sun and on the functioning of the
time-compensated ‘chronometric’ compass. But what
was most important was the demonstration of the existence of this mechanism in an animal whose organisation and behaviour were much simpler than those of
the starling or the bee. Essentially it was an indication
that the mechanism of sun orientation must be much
more common in the animal kingdom than the early
discoveries - of von Frisch and Kramer - had led one to
believe. Von Frisch (1953) immediately draw attention
to this, as Pardi often recalled.
And here allow me to draw on a personal recollation.
Karl von Frisch, informed of what we had seen in the
sandhopper, came to Pisa and we gave him a demonstration of how sandhoppers placed in a dry place orientate themselves towards the sea and change direction
if they are made to see the sun from another direction
by means of a mirror. A photographic document (Fig. 1)
of that episode has remained, showing Karl von Frisch,
ANIMAL COMPASSES
Towards the middle of the century, over a time-span
of twenty years, four mechanisms were discovered by
which animals are able to orientate themselves in given
directions, independently of the presence of reference
points on the earth’s surface: the sun, moon, stars and
magnetic compasses. The compensated sun compass
was discovered in 1946 by von Frisch in the bee and
Fig. 1 - A photographic memento of the period of the discovery
of biological compasses: K. von Frisch, L. Pardi and F. Papi on the
beach at San Rossore, Pisa, intent on collecting sandhoppers (top
photo) and observing their orientation inside the recipient placed
on the sand (bottom photo). K. von Frisch is the first from the left
in both photos, L. Pardi is the last on the right in the bottom photo, F. Papi the last on the right in the top photo. October 1952.
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ANIMAL NAVIGATION AT THE END OF THE CENTURY
Leo Pardi and myself intent on digging sandhoppers out
of the damp sand and then observing their orientation
in a bowl with a glass lid over it. Pardi and I had welcomed the Herr Professor in jacket and tie, but the seventy-year-old future Nobel Prize winner surprised everyone by taking a swim in the cold waters of the Tyrrhenian in October.
The discovery of the four biological compasses gave
great impetus to research into orientation and navigation, and into their neurobiological foundations. The
spin-off from the discovery of the solar compass was
the most important result: the knowledge gained about
the compensation of the motion of the sun and of the
biological rhythm that depends on it, about the perception of polarised light and about the innate and learned
components of solar orientation are now the common
cultural heritage of all zoologists. The moon compass
has been clearly demonstrated only in sandhoppers
(Wallraff, 1981), but has raised the important problem
of the biorhythm on which it is based and its co-existence with the biorhythm of the sun compass: two
rhythms each with its own period in the same animal.
From recent research on moon orientation it should be
mentioned that Marchetti and Baldaccini (1997) observed moon orientation in the willow warbler, but
have had negative results with other species.
Regarding the star compass we should remember that
it is well known only in birds and that the acquisition
mechanism was clarified thanks to Emlen (1970), whereas things are different for the magnetic compass. Magnetic orientation in the sense of the ability to recognise
the compass directions is certainly widespread in the
animal kingdom, but lack of knowledge of the receptor
and the reception mechanism continues to complicate
the matter. Recently the group led by Walker (Walker et
al., 1997) has produced findings regarding a receptor
functioning with magnetite crystals in cells of the olfactory lamellae of the trout, but this is clearly an initial result. There has been a long discussion about whether
the magnetic field is used to determine geographical
position, but so far there is no evidence for this
(Wiltschko & Wiltschko, 1995).
In the field of sun and moon compasses there are
many open problems because of the very nature of the
orientation mechanism, which is based on reference
points - the sun and the moon - whose geographical direction varies continuously. For a correct orientation the
animal must have the solar or lunar ephemeris, or both,
in its head, by heredity and/or ontogenetic acquisition.
The sun compass functions by communicating to the
animal the angle to keep, not with the sun, but with its
projection on the horizon, i.e. with the solar azimuth.
Now, while the sun moves in the sky at a constant velocity - 15° per hour - its azimuth does not do the same,
as it varies with a velocity that depends on the time of
day, the latitude and the season. The azimuth of the
sun shifts more quickly in the noon hours than in the
morning or afternoon hours (Fig. 2), and the phenomenon varies in degree at different latitudes (Fig. 3).
Fig. 2 - This diagram of the motion of the sun and its azimuth is
intended to show that the azimuth of the sun moves at a different
velocity in the course of the day. The arc of the sun is represented for 45° of latitude north at the equinoxes. The positions of the
sun are represented at midday (1), at mid-afternoon (2) and at
sunset (3) with the corresponding azimuths (A1, A2, A3). Note that
the time taken by the sun’s azimuth to move from A1 to A2 is
equal to that from A2 to A3 and that the velocity is therefore different. The arrows at the bottom indicate the direction of movement of the sun’s azimuth.
Bees and ants manage to master this situation by
completing basic genetic information through experience. In an experiment by Dyer and Dickinson (1994),
bees that had come out into the open to gather only in
local time
Fig. 3 - The sun’s azimuth as a function of local time. The picture
refers to the situation at different latitudes in the northern hemisphere on the days of the equinoxes. Only at the pole does the
sun’s azimuth move at a constant velocity; otherwise it is always
faster during the noon hours than during the morning or afternoon
hours, up to the extreme situation at the equator, where the sun is
in the east until midday, and then passes immediately to the west.
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the second half of the afternoon were incapable, with
such limited experience, of calculating the position of
the sun at various times of the day at the site of the experiment, while the genetic information that they possess seems to induce them to calculate positions of the
sun that are valid for equatorial latitudes (Fig. 4).
If the solar ephemerides are complicated, the lunar
ephemerides are no less so, and the relative information
is perhaps too complex to be learnt, at least by animals
at the level of crustaceans. In sandhoppers, Ugolini and
his colleagues demonstrated that the young born in the
laboratory and prevented from seeing the sky until the
moment of the experiment, orientated themselves perfectly, as soon as they were exposed to the light of the
moon (Ugolini et al., 1999). Figure 5 shows the results
with experienced adults and inexperienced young, and
an extraordinary similarity in the orientation of the two
groups. Since the inexpert young orient themselves perfectly, it can be assumed that the mechanism of lunar
orientation is completely innate.
MAPS
Much research subsequent to the discovery of biological compasses has shown that the performances in the
Fig. 4 - In this experiment of Dyers and Dickinson (1994), the bees
were trained to gather on clear days, in the second half of the afternoon (indicated as ‘Training time’). At a later stage they were allowed to gather with an overcast sky at any time of day; on the basis of the bees’ dances on the honeycomb, the experimenters
recorded how they estimated the variation of the sun’s azimuth in
the course of the day. The single estimates of the sun’s azimuth are
indicated by crosses. If the bees had correctly calculated the variations in the position of the azimuth, the points would have been
found on the sinusoidal dashed curve, as happens in bees that have
seen the sun all the day. In reality, the experimental bees calculated
positions of the azimuth that are constant for almost the whole
morning and then jump abruptly to a value that is different by about
180°. As the information available to bees is almost exclusively genetic, they seem to be pre-adapted to an equatorial astronomic situation, which can be seen here on the continuous light grey curve.
Only if bees see the sun all day do they adjust their orientation to
the local latitude. From Dyers and Dickinson (1994), modified.
F. PAPI
Fig. 5 - Orientation of Talitrus saltator exposed to moonlight. The
experiments were carried out in parallel on inexperienced young
(a), which had been born and reared in the laboratory and on
adults collected in nature (b). Each point represents a mean for 10
specimens; the internal arrow represents the average vector, the
external arrow the expected direction. The experiments were carried out during different lunar phases, at different times, and with
different positions of the moon. From data by Ugolini et al. (1999).
spatial field of many animals cannot be explained by
the sole possession of one or more compasses. In certain cases - in many cases - it is necessary to attribute to
the animal the possession of an instrument of orientation which, again using a metaphor, has been called a
map. Psychologists often add to the term map the adjective ‘cognitive’, even if they then admit that speaking
of a cognitive map is a source of error, because both
terms can be understood in several ways. The problem
of the map has been addressed by psychologists and
zoologists in different ways. When Tolman (1948)
spoke of a map in animals, what he meant was, precisely, a cognitive map and he was thinking of an inner
representation of spatial relations between known landmarks, whereas when Kramer (1961) expressed the
concept of ‘map and compass’, in using the term map
he was simply having recourse to a metaphor without
any claim to be indicating what the map might be in
physiological or psychological terms. Kramer had in
mind the navigation of the homing pigeon, and was
well aware that the pigeon is able to return from unknown places and that its map, extending beyond the
places already flown over, was not referable to a collage of familiar landmarks. Many other zoologists subsequently proceeded with this idea in mind. The zoological and the psychological approaches, however, ended
up by bringing the positions of the researchers in the
two fields together, so that today spatial orientation, together with the production and perception of acoustic
signals and the use of symbolic systems of communication, is a field in which ethological and cognitive programmes (Kamil, 1998) converge, giving substance to
Cognitive Ethology, which has become a fully developing branch of the science of animal behaviour.
It is certain that not all animals that cover large distances in foraging or migratory flights are capable of
building up their own spatial map and using it for new
spatial solutions, for example, finding a short cut to
shorten the journey. After long discussions, the opinion
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ANIMAL NAVIGATION AT THE END OF THE CENTURY
prevailed that bees, like ants, do not possess a real map
(Wehner, 1992), and it is admitted in more general
terms, that Hymenoptera make up for this deficiency
with a combination of an egocentric and a geocentric
orientation, which makes possible a good spatial orientation performance, as can also be demonstrated experimentally (Fig. 6).
The inability of Hymenoptera to develop a map has
been attributed to the modest size of their brain. If this is
the reason, arthropods of larger dimensions may possess
such an ability, for example, the decapod crustaceans.
There is some evidence of this (Vannini & Cannicci, 1995).
THE TWO MAPS OF THE HOMING PIGEON
In certain cases the navigation map extends well beyond the area known to the animal and this is demonstrated by the rapid returns home of animals transferred
to distant and unknown places. Probably many species
have maps of this type, but the nature of the map is
known only for the homing pigeon. The homing pigeon has inherited good homing abilities from its wild
ancestor, as was demonstrated many years ago (Alleva
Fig. 6 - An ant that has completed a journey from its nest to the
point where it has found food, is moving back to its nest and is
about to reach it. In the return trip it could rely on both the egocentric and geocentric mechanism (a). If on its departure from the
point where it has found food, it is moved to a flat area devoid of
landmarks, the ant moves in a straight line and, thanks to the
egocentric path-integration mechanism, reaches the position of
the fictive nest. Thereafter, it circuits in the area looking for the
nest (b). If, however, when it reaches the nest, it is carried back
to the same departure point on the flat area without landmarks, it
will look for the nest without moving too far away, because, having completed the return programme, it thinks it is near home (c).
If, on the other hand, this same ant is placed at the beginning of
a route marked by the same landmarks as those found on the
path that leads home, it will stay on the route until it reaches
home, guided by the geocentric mechanism, even if it has shortly
before completed the return programme (d). From Wehner
(1998), modified.
et al., 1975), and has improved these abilities as a message-carrier for man. The map that enables the pigeon
to return from unknown places is of an olfactory nature
and is acquired by associating the smells carried by the
wind with its direction of origin. This olfactory theory
was put forward 30 years ago by Pisan ethologists (Papi
et al., 1972), and mention has frequently been made of
the relevant research in the congresses of our Society.
The pigeon is the animal that has been most studied
from the point of view of navigation, and today we
know that in actual fact it possesses not one, but two
maps, the visual map of known places and the olfactory
map, which is more extensive and superimposed on the
visual one. In the zone of superimposition of the two
maps, the pigeon has a double certainty: it can head for
home both with the sense of smell and with that of
sight, as Anna Gagliardo and Poalo Ioalé also demonstrated recently with an elegant experiment (Gagliardo
et al., 2001). As Chelazzi and Pardi (1972) discovered
many years ago, pigeons placed in a cage in an open
place show that they can orientate homewards. Using a
new type of cage, Gagliardo and Ioalé saw that pigeons
orientate in a familiar place even if they are rendered
temporarily anosmatic, provided they can see the surrounding landscape. If, on the other hand, they are prevented from seeing the landscape by a series of vertical
screens, orientation towards home remains correct if the
pigeons’ smelling capacity is intact, but becomes random if they are anosmatic.
The existence of two maps is also shown by the neuroethological experiments which attempted to establish,
using the lesion method, which areas of the brain are
involved in the acquisition and use of the navigation
maps. Recently some progress has been in this field and
it can be concluded that while the hippocampus is the
seat of the processing of data relative to visual navigation, the pyriform cortex - also called the olfactory cortex on account of the projections that it receives from
the olfactory bulbs - is fundamental for purposes of acquisition and use of the olfactory map, while the map
itself seems to be preserved and read - pardon the
metaphors - in the caudolateral neostriatum (Bingman
et al., 1998b, for references). The research in this field
has been going on now for many years and is an example of how neuroethological research can achieve fundamental improvements in the knowledge of the cognitive processes occurring in natural conditions.
THE DEBATE ON OLFACTORY NAVIGATION
As everyone knows, the hypothesis of the olfactory
map of the homing pigeon has met with criticism and
opposition which I would not have imagined would be
so insistent, even after the considerable amount of evidence presented by the Pisan group, and after Hans
Wallraff and other German researchers of the MaxPlanck-Institut of Seewiesen had confirmed, consolidat-
176
ed and considerably extended knowledge of the olfactory navigation of the pigeon (see Wallraff, 1990, 2001
for references). One of the arguments most often put
forward against the olfactory theory is that pigeons, and
birds in general, rely on a redundant series of orientating factors used flexibly, so that it is unlikely that a single source of spatial information is essential for navigation (Keeton, 1979; Wiltschko, 1991, and also recently
Wehner, 1998).
This argument is based on a confusion between natural situations and experimental situations, whose persistence in the debate is surprising. Certainly the pigeon, which leaves its loft spontaneously in search of
food, has at its disposal, on its return, a redundant series of navigational cues: memory of the direction maintained on the journey out and recorded with the sun
compass and maybe also with the magnetic compass,
the angle maintained with respect to the wind, and the
visual and olfactory characteristics of the places flown
over. It has to choose, integrate and mediate. But if the
pigeon has been transported, inside a vehicle, to a
place that is certainly a long way from any area previously flown over and has been deprived during the
journey of access to the most obvious information regarding the direction of movement (e.g. transporting it
under general anaesthetic), it is logical to expect that
the cues it has at its disposal to orientate in the direction of home might be very few in number or even totally unavailable, given that the most obvious information useful for homing derive either from knowledge of
the places or, in the case of a journey into an unknown
area, from the information gathered on the outward
journey. And yet pigeons, at least in many zones, are
able to orient homewards, even if they are released after a journey of this type and it is this phenomenon that
has for many years been the mystery yet to be revealed.
It should not however surprise us that, in the situation
we have described, depriving pigeons of a single type
of cue - the olfactory cue - is sufficient to render them
incapable of orientating homewards. What should be
emphasised is that we do not assert that pigeons only
navigate by smell, but that olfactory cues are essential
for orientation homewards in pigeons transported passively to an unfamiliar place.
The olfactory theory is not only supported by experiments with olfactory deprivation; there is not enough
space here to mention all the other experiments of various kinds that confirm it. Whoever would like further
information can find it in the various reviews (Wallraff,
1990, 2001; Papi, 1991, 1995) in which the history of the
debate for and against the olfactory theory is reported.
Today we can look forward to the outcome of this debate with optimism. The rival hypothesis to the olfactory theory, that of magnetic navigation, was abandoned
by its main supporter, Charlie Walcott (1991), who declared that he no longer believed it and even a recent
attempt by Michael Walker (1998) to advance once
again the theory of a magnetic map for the pigeon, was
F. PAPI
easily refuted by Wallraff (1999). Moreover, it has been
demonstrated that certain disorientating effects, obtained with magnetic treatments, were not due to interference with navigation, but to the emotional state of
the animal (Luschi et al., 1996, 1999). Lastly, new research has been carried out in Ohio (Bingman & Mackie, 1992), Arizona (Bingman et al., 1998a), Georgia, USA
(Bingman & Benvenuti, 1996), Great Britain (Guilford et
al., 1998) and the state of New York (Benvenuti &
Brown, 1989), that has confirmed the ubiquity of the
phenomenon of olfactory navigation. The effect of
these findings has been that the scientific community is
recognising the validity of the olfactory theory and one
sign of this fact is the position taken by two researchers
who are outside the fray, Ken Able (1996) and Tim
Roper (1999), the first warning that those who do not
believe that smell guides pigeons have to carry the burden of proof, the second asserting that it is now time to
identify the physical substratum that makes olfactory
navigation possible. This hope is now on the way to
fulfilment, as we shall now see.
THE PHYSICAL SUBSTRATUM OF OLFACTORY
NAVIGATION
The hypothesis of the olfactory navigation of the
homing pigeon assumes that there are substances dispersed in the atmosphere that characterise different regions - otherwise navigation would not be possible and that these substances are fairly stable in time, in
spite of the dynamic phenomena of the atmosphere.
This has long been denied, but recently H. G. Wallraff
has obtained positive results, and this is perhaps the
most important recent discovery in the field of animal
navigation (Wallraff, 2000; Wallraff & Andreae, 2000).
He set out with the assumption that there are gradients
of concentration for odorous substances and that pigeons base themselves not on the absolute concentrations of these substances, but on the quantitative relations between them, just as man does in distinguishing
between the scents of flowers and fruit, given that their
specificity is based precisely on the quantitative relations of the component substances.
With these assumptions, Wallraff proceeded with the
experimental approach and, for three years in succession, collected a large number of samples of air in 96
localities distributed over an area with a diameter of 400
km, with its centre in the city of Würzburg in Bavaria,
where he keeps the pigeons with which he works. The
samples were analysed with gas-chromatography, and
the result was that for six organic substances, the most
frequent and abundant, the quantitative relation of each
to the other five has a pattern that varies geographically, but is stable over time. These data have made it possible to simulate on a computer how a model pigeon
would behave when released from 196 localities situated in the area studied, with the result that it orientates
ANIMAL NAVIGATION AT THE END OF THE CENTURY
177
homewards with the same precision (or, rather, imprecision) of a real pigeon (Fig. 7).
Of course, it is not necessarily the case that the substances studied by Wallraff are those that orientate pigeons. Of the six hydrocarbons considered, one only,
isoprene, is found in nature, the other five being anthropogenic. The identification of the substances that
orientate pigeons will not be easy, partly because pigeons might adapt themselves to using different substances according to their availability and distribution.
But a big step forward has certainly been taken, because it has been proved that, as predicted by the olfactory theory, there are organic substances in the atmosphere whose quantitative relations are sufficiently stable
to be used for establishing position with respect to a
particular place. With this the main objection to the theory of olfactory navigation falls.
NAVIGATION OF OCEANIC ANIMALS
The phenomena of navigation have been studied
above all in land animals, which, in addition to the four
biological compasses, can use all the visual and chemical
information provided by a polymorphous environment,
such as that of the earth. On the other hand, we know
very little about how animals that move on and under
the ocean, in an apparently uniform, featureless environment, navigate. And yet marine animals are capable of
performances, in the field of navigation, worthy of an
Olympic Medal. Let us take as an example the recent
documentation on the albatrosses obtained with satellite
telemetry (Jouventin & Weimerskirsch, 1990; Prince et al.,
1992; Weimerskirch et al., 1993, 1997). Albatrosses make
foraging flights of hundreds or thousands of kilometres
with outward and return journeys that are sometimes almost perfectly superimposable on each other, even if the
route is composed of several stretches effected in different directions (Fig. 8a, b). In certain cases it has been
seen that albatrosses are able to pinpoint their destination (Fig. 8c), from a distance of more than 1000 km.
Similar examples can be given for other birds, sea-lions,
otaries, and cetaceans. All these performances are based
Fig. 7 - Result of a simulation of the orientation of a pigeon
which, in the area of Würzburg, chooses the direction of home
on the basis of the quantitative relations between six chemical
compounds diffused in the atmosphere (see text). The orientation
for 196 different places was calculated. In each circle one radius
points towards home and the other indicates the direction chosen; the area in black between the two radii provides the measure
of error, which in 94% of cases is less than 90°. The diameter of
the circles is proportional to the agreement between the indications of direction of the six substances considered. α indicates the
mean deflection from the expected direction, r gives the length of
the mean vector. From Wallraff (2000), modified.
on unknown navigation mechanisms: we are in the romantic phase of research that I mentioned earlier and
there will certainly be much to do and to collect for
those who wish to dedicate themselves to the subject.
Sea turtles are also excellent navigators. Paolo Luschi
and I began not many years ago to study their routes by
applying satellite transmitters to the migrating females
(Papi et al. 1995, 1997; Papi & Luschi, 1996; Luschi et al.,
1997). The most famous and most interesting journey
Fig. 8 - Tracks of foraging trips of wandering albatrosses as revealed by satellite telemetry. From Weimerskirch et al. (1993), modified.
178
from the point of view of navigation is that made by
green turtles that live on the coasts of Brazil, but go to
Ascension Island, in the middle of the Atlantic Ocean, to
nest. How do green turtles manage to reach this small
remote island, only 13 km wide, situated more than
2000 km from the Brazilian coast? So far there are three
hypotheses and no certainties. The first hypothesis is
that the turtles, knowing the route from Brazil to Ascension, travel until they come within seeing distance of the
island, then correct their route and orientate themselves
definitively towards their destination. This first and most
economic hypothesis, which has no paternity, poses the
problem of how turtles are able, on such a long journey,
to compensate for the drift phenomena due to currents
and storms, as well as the probable imprecisions of the
animal in maintaining its route.
The second hypothesis is that of magnetic navigation,
which exploits the particular situation of the earth’s
magnetic field in this area of the Atlantic. As Lohmann
and Lohmann (1996) have pointed out, the isolines of
intensity and those of inclination of the field, i.e. the
isodynamics and the isoclinics, cross each other at almost a right angle: if the animal was capable of determining the values of inclination and intensity of the
field, it could at any moment establish its own position
and navigate with a system of bicoordinates.
The third hypothesis, already more than thirty-five years
old (Carr, 1965; Koch et al., 1969), envisages the possibility that the Atlantic equatorial current, which moves in a
westerly direction, on contact with Ascension, washes
away substances that give rise to a chemical plume which
could be used by the animals both in orientating themselves towards Ascension and in returning to Brazil.
Let us now consider the health of these three hypotheses after the most recent experiments we carried
out using satellite telemetry and in collaboration with
researchers at the Universities of Wales and Lund
(Luschi et al., 1998; Papi et al., 2000). The reconstruction of the route of the turtles from Brazil to Ascension
would be very useful for obtaining evidence from them
about the methods of navigation used, but it is very difficult to capture the females in the sea on their outward
journey from Ascension. We therefore started to record
the return journeys from Ascension to the coast of
Brazil, with the result that we saw the animals moving
initially in a narrow corridor pointing in a WSW direction (instead of W) and parallel to the current, almost a
confirmation of the hypothesis of the chemical plume,
and then diverge from each other and finally correct
and head towards the easternmost part of the Brasilian
continent (Fig. 9a). The result of another experiment
was more indicative. It was carried out by attaching
powerful magnets to the animals departing for Ascension. These made magnetic navigation based on isodynamics and isoclinics impossible. However, the animals
reached Brazil along routes that were very similar to
those of the controls (Papi et al., 2000, Fig. 9b). With
this the hypothesis of magnetic navigation falls.
F. PAPI
Fig. 9 - Plots of routes of green turtles (Chelonia mydas) in the
postreproductive migration from Ascension Island towards the
feeding grounds on the Brazilian coasts. In a the plots of the control turtles, in b those of turtles that carried magnets attached to
their body. The arrow indicates the position of Ascension Island.
From Papi et al. (2000), modified.
Our most recent experiments were carried out to test
the ability of turtles to compensate for passive dislocation
and therefore their real capacity for true navigation
(Luschi et al., 2001). Eighteen females captured at Ascension were released well out to sea at various distances
(between 60 and 450 km) from the island (Fig. 10). Of
the 18 turtles moved, 4 departed at once for Brazil, while
another 4 did so after trying for different lengths of time
to find the island again. It is noteworthy that one of them
passed 20 km S of the island without, however, heading
towards it. The remaining 10 females reached Ascension,
nearly all of them following tortuous routes that indicated a difficult search: suffice it to say that the routes are,
on average, double the distance of the routes as the crow
flies. In general, the turtles released from farther away
had more difficulty in reaching the island.
Certainly, these results favour neither the hypothesis
of magnetic navigation, which assumes a reliable map
from any distance, nor that of the chemical plume, given that the turtles released in the presumed plume also
followed tortuous routes and came out of the plume
before reaching the island. Beside these negative conclusions there is, however, a positive one: nearly all the
turtles that reached the island did so by arriving from
the NW (Fig. 11). This suggests that a sensorial contact
with the island could have been made from that direction and that this was more difficult from other directions. Now, while there is no reason why the island
179
ANIMAL NAVIGATION AT THE END OF THE CENTURY
be perceived, according to their intensity and the sensitivity of the sense of smell of the animal, even before
the island becomes visible. In addition turtles are notorious for having an excellent sense of smell.
In conclusion, but for the moment it is a hypothesis,
it might be thought that turtles leave Brazil knowing the
direction and distance of the island. Aided by their
compasses they might orientate a little N of the island
in order to meet the scents of the island carried by the
trade wind. This is an ad hoc explanation for the turtles
of Ascension: other populations might use other mechanisms. We shall see, or others will see.
****
Fig. 10. Scheme of the displacements of nesting green turtles from
Ascension Island to different points in the ocean. Figures in the
circles indicate the number of turtles released.
should be visible at a greater distance from the NW, the
fact should be considered that trade winds from the SE
constantly blow over Ascension. Even if the intensity of
the wind can vary, its direction is almost constant. It follows that NW of the island, at a distance that varies according to the intensity and turbulence of the wind,
smells coming from the island are present, which could
In concluding this reflection, I would particularly like
to invite the younger ethologists to consider the interest
of the studies of animal navigation, at whatever level
they are carried out: the descriptive level regarding the
reconstruction and study of routes, the sensorial level regarding the study of the ways of acquiring the information on which navigation is based, and the physiological
level, which interprets the phenomena observed in neurobiological terms. Innumerable problems remain open:
their solution, often unexpected, rewards the effort made
in asking nature a crucial question in the right way.
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α = 317°
r = 0.82
P < 0.001
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