Download Common Themes and Variations in Animal Orientation Systems1

AMER. ZOOL., 31:157-167 (1991)
Common Themes and Variations in Animal Orientation Systems1
KENNETH P. ABLE
Department of Biology, State University of New York, Albany, New York 12222
SYNOPSIS. Although only a small number of disparate taxa have been studied in detail,
there are some general themes that transcend the orientation and navigation mechanisms
of animals. I will identify some of these commonalities and illustrate them with data from
selected species. Nearly all species rely on multiple environmental cues in orientation and
these mechanisms seem often to be related hierarchically. Magnetic effects on orientation
are widespread. The various cue-based orientation mechanisms are not independent, but
influence one another during early development and later in life. The development of
orientation capabilities involves complex interactions of experience and endogenous rules
and learning predispositions. At the same time, considerable plasticity characterizes both
the development of orientation and the behavior of adults in response to environmental
situations requiring oriented movement.
and navigation become global. An enviMost mobile animals do not wander ran- ronmental cue employed in orientation
domly. Rather, their movements are orga- must be available and reliable over an
nized with respect to the environment in extensive area, and it may be necessary to
which they live such that they find food, rely on more than one cue.
Whereas the kinds of orientation problocate mates or avoid predators. Natural
selection should produce mechanisms to lems facing animals seem almost as numerinsure that these activities are carried on ous as the species, the means available for
in an efficient manner. Employing stimuli solving them are apparently much more
in the environment to orient their move- limited. This is suggested by the fact that
ments is a ubiquitous capability among ani- a number of common themes transcend
mals and the range in types of orientation orientation and navigation mechanisms
required is vast. For a relatively sedentary across a vast array of taxa. The assumption
animal that spends its life in a restricted has generally been made that functional
home range, learned local landmarks similarities in the orientation mechanisms
(visual, olfactory, etc.) might be sufficient of phylogenetically distant groups repreto control all its movements. In other cases, sent convergence, but in almost no group
more general capabilities will be required. (cf. Lindauer, 1956) do we have any inforAn amphibian living near a shoreline or a mation against which that assumption
sandhopper on a beach may need to know might be tested. Thus we should not ignore
the direction toward land or water. If the the possibility that some of the common
animals are not confined to a small area themes might exist because they represent
for their entire lives, problems can arise: primitive characters that have been long
landmarks will not be sufficient and shore- conserved in animal evolution.
lines can vary in their orientation. A mechMy objective in this paper will be to idenanism based on a ubiquitous cue such as tify some common threads in the orientathe sun or earth's magnetic field would be tion and navigation behavior of animals, I
better, especially if it was imbued with suf- hope without having to exercise too heavy
ficient plasticity to permit accommodation a hand in forcing data into preconceptions.
to new conditions. In species that migrate Any such attempt, however, necessarily
vast distances, the problems of orientation involves biases, conscious or otherwise, that
result in emphasizing some data at the
expense of others. While focusing on some
commonalities,
I shall at the same time
1
From the symposium on Recent Developments in the attempt to illustrate some of the adaptive
Study of Animal Migration presented at the annual
meeting of the American Society of Zoologists, 27— variability that characterizes different species' solutions to their particular orienta30 December 1988, at San Francisco, California.
INTRODUCTION
157
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KENNETH P. ABLE
tion problems. The number of species for
which we have sufficient data is embarrassingly small. Even so, I shall not attempt
a comprehensive review, but rather shall
rely on a few especially thoroughly studied
species and groups that illustrate the points
I wish to make.
the performance of what would seem like
a fairly simple task (Pardi and Ercolini,
1986). In the diurnal species, the sun compass seems to be the dominant mechanism,
but detailed studies of cue interactions have
not been done.
Growing from the life-long work of Karl
von Frisch, the navigation system of the
honeybee (Apis mellifera) is the best underCOMMON THEMES
stood of any species on earth (von Frisch,
Multiple cues and hierarchies of mechanisms
1967). Indeed, it was von Frisch, working
In the early days of experimental with bees, who first demonstrated a hierresearch on animal orientation systems, it archical organization of orientation mechwas customary to adopt a unitary approach. anisms. Bees are central place foragers and
Based on the assumption that a single exploring workers often face the problem
mechanism would subserve a given behav- of seeking food in unknown locations and
ioral type, it was easy to arrive at the sim- then finding their way back to the hive.
plistic picture that developed for migra- Many of von Frisch's experiments showed
tory birds: a sun compass for diurnal that bees pay attention to and learn visual
migrants and a star compass for night landmarks and one might suppose that a
migrants. What more could one need? system of navigation based on familiarity
with landscape features might suffice over
Apparently, a great deal more.
As data have accumulated, it has become the distances that they travel (up to 10 km
apparent that probably no metazoan that or so). In fact, Gould (1986) has shown that
faces orientation tasks of any complexity honeybees can develop cognitive maps of
relies on a single orientation mechanism. the hive neighborhood that allow them to
The use of multiple cues appears to be the navigate along novel routes based on the
rule, a conclusion forced upon the field learned spatial relationships between landprimarily by studies of homing pigeons and marks. However, a more general system
migratory birds (Keeton, 1974; Emlen, has apparently been required.
1975). Soon the terms "hierarchy" and
The time-compensated sun compass, dis"redundant cues" became widespread, covered independently and simultaneously
often applied without regard to the exis- by von Frisch in bees and Kramer in birds,
tence of any data actually demonstrating provides the primary orientation mechahierarchical relationships or redundancy. nism. As in all other cases of sun compass
Indeed, without a full understanding of orientation that have been analyzed, the
how all the orientation mechanisms of an relevant stimulus information is the azianimal operate and interact with one muth of the sun: sun elevation is ignored.
another, it is logically impossible to con- Among other ways, this is clearly illusclude that any are redundant. At any rate, trated by clock shift experiments wherein
the existence of multiple orientation capa- animals can be induced to respond to a
bilities has now been demonstrated in those noon sun as if it were sunrise or sunset.
species that have been studied in detail, The details of sun compass orientation have
and some progress has been made in dis- been analyzed more thoroughly in bees
cerning the relationships among them, as than in any other animal. In numerous eleindicated by the following examples.
gant experiments, Gould and his colSandhoppers (Talitrus and Talorchestia) leagues showed that bees allow for the fact
orienting with respect to the shorelines on that the rate of change in such azimuth
which they live are known to employ a time- varies greatly during the day as well as with
compensated sun compass, polarized sky- season and latitude, although it averages
light, the magnetic field, slope of substrate, 15 per hr. The bees cope with this problem
landmarks, sky color differences over land by maintaining a running average of the
and sea, and perhaps a moon compass in sun's azimuth change based on their expe-
ANIMAL ORIENTATION SYSTEMS
rience during the past 40 min or so (see
Dyer and Gould, 1983).
Because bees rely on the sun, cloud cover
is a potentially serious problem. Von Frisch
(1948) discovered that when the sun is not
directly visible, bees use the patterns of
polarized skylight to extract that information. The relevant and most reliable
information is the pattern of e-vector
angles, viewed at UV wavelengths, in small
patches of blue sky (von Frisch, 1967;
Edrich and von Helverson, 1976; Brines
and Gould, 1979). Based on a complex
series of apparently innate rules, bees use
information about the UV content of light
from a patch of sky and its relative distance
from the sun to resolve inherent ambiguities involved in translating e-vector patterns into such azimuth (Brines and Gould,
1979; Rossel and Wehner, 1982).
In what to my knowledge were the first
cue conflict experiments, von Frisch pitted
polarized light patterns against the sun to
see which cue bees would use. The relationship is apparently not strictly hierarchical, but depends on the relative strengths
of the two stimuli. When bees were allowed
to view the real sun and a small patch of
sky through a polaroid, they danced as predicted by the sun. But the influence of
polarized light increased as the amount of
UV transmitted by the polaroid increased.
Experiments in which the bees viewed the
natural blue sky and a reflected image of
the sun resulted in compromise directions
(von Frisch, 1967). In nature, of course,
bees and other animals are not often confronted with situations in which orientation cues give conflicting information and
there is no a priori reason to expect independent, hierarchical relationships. In fact,
in the real world, pooling information from
multiple cues would usually result in
reduced error in a directional decision.
Bees also need to be able to cope with
completely cloudy situations when neither
the sun nor polarized skylight is available.
Yet the dance is still coded with respect to
the sun, so the bees require some system
that provides sun azimuth indirectly. A logical candidate might seem to be a magnetic
compass. Although there is evidence of
magnetic effects on the orientation of comb
159
building (Lindauer and Martin, 1972;
Dejong, 1982), small errors in dances performed on vertical comb (Misswelsung) (von
Frisch, 1967), a tendency for horizontal
dances performed in the absence of visual
cues to be oriented in cardinal directions
(Lindauer and Martin, 1972), and some
conditioning experiments not directly
involving orientation (Walker and Bitterman, 1985), attempts to demonstrate a
magnetic compass involved in food-finding
have not been successful (Towne and
Gould, 1985). Rather, the bees rely on a
learned relationship between the diurnal
path of the sun and local landmarks near
the hive, extrapolating the position of the
sun given the time of day (Dyer and Gould,
1981).
In vertebrates, multiple cues in orientation are the rule and an emerging trend
has been the ubiquity of magnetic orientation (see review volumes by Kirschvink
et al., 1985; Maret et al., 1986). While the
experimental results are sometimes not as
robust as one might wish, carefully controlled studies are now so numerous that I
find it impossible not to accept the widespread occurrence of magnetic orientation
capabilities. Most of the negative data have
come from attempts to condition various
species to magnetic stimuli (see e.g., Griffin,
1987, and other papers in the same issue).
As with any negative data, these results are
inherently uninterpretable. They are as
likely to be a reflection of the experimenters' failure to devise a system in which
the animal can or is motivated to express
a relevant response, as was demonstrated
in attempts to replicate the magnetic effect
on comb-building in honeybees (Dejong,
1982), as they are to be indicators of a real
inability to perceive the stimulus.
Sockeye salmon (Oncorhynchus nerka) fry
and smolts exhibit population specific
migration directions within river and lake
systems (Brannone^ al., 1981). Under clear
daytime skies these movements are oriented by visual cues, although it is not clear
whether the sun or polarized light patterns
predominate (Groot, 1965; Dill, 1971).
Tested in orientation tanks in a shifted
magnetic field, the fish orient with respect
to visual cues when those are available. At
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KENNETH P. ABLE
night or when the tanks were covered with
opaque material, the orientation of the fish
shifted as predicted by the change in magnetic directions (Quinn, 1980; Quinn and
Brannon, 1982). In the smolts, orientation
became axially bimodal in tests under
opaque covers, a phenomenon that occurs
frequently in species performing orientation in response to magnetic cues.
Amphibians perform oriented movements with respect to the axis of the shorelines along which they live (Y-axis orientation: Ferguson, 1971). Individuals learn
the orientation of new natural or artificial
shorelines and Y-axis orientation has been
extensively exploited in studies of orientation mechanisms (Adler, 1976). When
visual cues from the daytime sky are available, the sun compass and polarized skylight patterns prevail. The latter are mediated by an extra-optic photoreceptor
(pineal complex). The relative weighting
of the two cues is not entirely clear, but
circumstantial evidence suggests that the
sun takes precedence (Adler, 1976; review
in Able, 1980). Recent studies on the newt,
Notophthalmus viridescens, have shown that
in the absence of meaningful visual cues,
Y-axis orientation is accomplished via a
magnetic compass (Phillips, 1986a, b, 1987).
Birds have been more extensively studied than any other vertebrate group. Sun,
star and magnetic compasses were first discovered in birds and in recent years much
efFort has been devoted to working out the
relationships among these multiple capabilities. In the homing pigeon it is clear
that the sun provides the compass of first
choice. Under solid overcast, the magnetic
compass is used (reviews, Able, 1980;
Wiltschko and Wiltschko, 1988). The many
species of migratory birds exhibit a diversity of strategies, and only a few species
have been examined in detail. The sun
compass was discovered in the starling
(Sturnus vulgaris), a diurnal migrant, but
the problems involved in eliciting demonstrably migratory activity from caged diurnal migrants has discouraged work on those
species.
Nocturnal songbird migrants have a host
of orientation capabilities at hand: magnetic, sun and star compasses, and sunset
cues including polarized skylight. Cue conflict experiments have been performed on
a number of species, but the results have
not been completely consistent. Tests of
birds in a planetarium where the sky can
be rotated provide the best evidence supporting a star compass {e.g., Emlen's 1967
experiments with indigo buntings, Passerina cyanea). In many instances, stellar and
magnetic directions must have been in conflict and the birds shifted as predicted by
the stars. The indigo bunting has been
shown to perform magnetic orientation
(Emlen et al., 1976) and the planetarium
experiments were not specifically designed
as cue conflict tests, so the apparent conclusion that stellar cues override magnetic
ones in this species should probably be
viewed with caution. Using a similar design,
bobolinks (Dolichonyx oryzivorus) appeared
to rely preferentially on magnetic directions (Beason, 1986). Wiltschko and
Wiltschko (1975a, b) performed outdoor
tests with warblers (Sylvia) and European
robins (Erithacus rubecula) under starry skies
within a shifted magnetic field. Although
sometimes involving a delay in response,
the birds shifted directions as predicted by
the magnetic field. This experiment has
been replicated with European robins
(Bingman, 1987), and these results provide
strong evidence that in these species magnetic cues take precedence over stars, but
the birds do not always respond immediately to the cue conflict.
Investigations with several species of
North American emberizine night migrants
have shown that visual cues around the time
of sunset are sufficient, if not indeed necessary, for meaningful migratory orientation (reviews, Able and Cherry, 1985;
Moore, 1987). Experiments in which both
magnetic directions and sunset position
were shifted (the latter with mirrors) have
been performed outdoors with Savannah
sparrows (Passerculus sandwichensis) (Moore,
1985a). Each bird was subjected to only
two tests, so their cumulative exposure to
the cue conflict was only about 4 hr. The
results showed clearly that visual cues at
sunset overrode both magnetic and stellar
directions.
Determining precisely what cue is
ANIMAL ORIENTATION SYSTEMS
responsible for the visual sunset orientation has been complicated by the fact that
polarized skylight at dusk also serves as an
orientation stimulus in the same species
(Able, 1982a, 1989). Because of the technical difficulties involved in simulating
accurately the patterns of polarized light
occurring in the natural sky, it has been
difficult to determine whether sunset orientation is preferentially responsive to the
sun or to the polarization patterns. The
best attempts (Moore and Phillips, 1988;
experiments with hand-raised Savannah
sparrows, Able, unpublished data) suggest
that polarized light is the primary cue. Our
hand-raised Savannah sparrows exhibited
no ability to perform migratory orientation at sunset independent of polarized
light.
If one looks at all the data from night
migrants, there is clearly no consensus concerning the cue hierarchy. Perhaps this
reflects real behavioral differences among
species or perhaps it is an artifact of differences in experimental design. To
attempt to force the data into a single
framework requires arbitrarily emphasizing some experimental results and ignoring others, but perhaps it is a worthwhile
exercise if only to highlight how much more
we need to know. I would suggest that the
magnetic compass is the primary source of
directional information for adult migratory birds (based on the data of Wiltschko
and Wiltschko, 1975a, b, and Bingman,
1987). Perhaps for reasons that will not
become clear until we know the sensory
basis of magnetoreception in birds, the
magnetic compass may be consulted only
infrequently (data from European robins
suggest only every few days or so). In the
short term, then, visual stimuli might take
precedence in a cue conflict experiment,
only to be overridden once a magnetic fix
has been taken. In those species where
appropriate experiments have been performed, visual cues at sunset take priority
over stars, and the relevant stimulus at sunset may be a polarized skylight compass. In
the immediate absence of visual cues, many
night migrants resort to downwind orientation (Able, 19826).
The magnetic compass of birds has been
161
shown to be an inclination compass (i.e., it
does not detect the polarity of the field)
(Wiltschko and Wiltschko, 1972, 1988).
Reversing either the horizontal or vertical
component of the magnetic field induces a
reversal in the orientation of the birds.
Similarly, a reversal of Y-axis orientation
in newts was induced by inverting the vertical component of the magnetic field (Phillips, 19866), indicating that they too possess an inclination compass. However, in
the only other adequate test of which I am
aware, lake-migrating sockeye salmon fry
persisted in northward orientation in a
magnetic field with the vertical component
pointing upward (Quinn et al., 1981). This
suggests that they could detect the polarity
of the field. Data of this sort are rare
because so few species have been induced
to exhibit an oriented response to magnetic fields, but such functional aspects of
the magnetic compass are important in
evaluating models of mechanisms of magnetic field perception (Wiltschko and
Wiltschko, 1988; Kirschvink and Kirschvink, 1991).
Transfer of information among
orientation systems
Life would be simpler for the student of
animal orientation mechanisms if each of
the multiple capabilities described above
was an independent channel. That has not
turned out to be the case: at least some of
the orientation capabilities influence one
another in various ways, both during the
ontogeny of the mechanisms as well as in
"mature" individuals.
In honeybees, information about the
daily pattern of change in sun azimuth
(including apparently the variable rate of
azimuth change during the day) is transferred onto landmarks in the vicinity of the
hive (Dyer and Gould, 1983). This enables
the bees to communicate in the currency
of sun direction even when the sky is solidly
overcast. In migratory birds, Wiltschko and
Wiltschko (1976) showed that European
robins calibrated an artificial star pattern
to magnetic directions. The orientation
directions observed when the birds were
tested in the presence of both the "stars"
and the magnetic field was maintained on
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KENNETH P. ABLE
subsequent nights when the birds were
tested in a magnetic field too weak to provide directional information. In this case,
the "stars" were no more than celestial
landmarks that derived their directional
meaning from the magnetic field. Although
this experiment showed that information
may be transferred in this way, the situation in nature is more complicated, as
examination of interactions during ontogeny has shown.
All animals that perform sun compass
orientation must learn the path of the sun.
This has been studied in honeybees and
homing pigeons (reviews, Dyer and Gould,
1983; Able and Bingman, 1987). The sun
arc must obtain directional significance
with respect to some other frame of reference. What provides this information in
honeybees is not known, but it could be
local landmarks. In pigeons, a system that
is functional over a large area is required,
so some more universal calibration is necessary. Wiltschko et al. (1983) and
Wiltschko and Wiltschko (1988) have studied the homing orientation of young
pigeons allowed to view the daytime sky
only within a shifted magnetic field. The
vanishing bearings of the birds relative to
controls suggested that magnetic directions played a calibrating role in the process of learning the sun compass. Phillips
and Waldvogel (1988) have proposed that
polarized skylight patterns may be involved
in the calibration of the pigeon's sun compass.
T h e primary magnetic compass of
migratory birds develops in the absence of
any experience with visual orientation
stimuli (reviews, Able and Bingman, 1987;
Wiltschko and Wiltschko, 1988). Growing
up in the earth's magnetic field is sufficient
to produce this capability. On the other
hand, in birds raised with exposure to day
and night skies within a shifted magnetic
field, the magnetic compass became calibrated with respect to geographic directions (reviewed by Able and Bingman,
1987). In recent experiments with handraised Savannah sparrows we have found
that visual cues in either the day or night
sky are capable of producing this modification of the primary magnetic compass
(Able and Able, unpublished data). This
suggests that the axis of celestial rotation
provides the basic frame of reference containing information about geographic
directions, but the specific mechanisms
remain to be worked out.
The star compass of night-migrating
birds develops independently of the other
systems. The axis of stellar rotation confers
directionality upon the star patterns, the
pole point taken as north (Emlen, 1970).
The magnetic directions experienced during the young bird's first exposure to star
patterns have no influence on its development (Wiltschko et al, 1987a).
Migratory Savannah sparrows make their
directional decisions around the time of
sunset (review, Moore, 1987). Hand-raised
sparrows given controlled exposure to the
daytime sky under manipulated relationships of skylight polarization patterns and
sun azimuth learned to perform orientation at dusk based on the e-vector of polarized light. Similar manipulations performed with birds exposed within a shifted
magnetic field showed that this polarized
light compass was calibrated by the magnetic field (Able and Able, unpublished
data).
Thus in both the development of orientation capabilities in young birds and in
the performance of orientation in mature
animals, there exist complex routes of
interaction among the various cue-based
mechanisms. We can expect similar situations to be revealed by future studies on
other taxa. The adaptive value of these
complex webs of interaction is not clear,
although it has been suggested that they
provide means of coping with spatial and
temporal variability of the relevant orientation cues.
"Programs" and developmental plasticity
It is obvious from the foregoing discussion that experience and learning play
strong roles in the development of orientation behavior. On the other hand, those
roles are constrained by learning rules and
predispositions that define what constitutes relevant experience and the ways in
which that experience can modify behavior. Many examples are evident in the
ANIMAL ORIENTATION SYSTEMS
163
ontogeny of avian compass mechanisms. 1980). Because the birds were tested under
For example, during the development of the same conditions throughout the season
stellar orientation, the axis of celestial rota- (constant 12:12 photoperiod, same magtion is taken to be a north-south axis and netic field), the change in orientation
the pole point is defined as north. These direction would seem to be based on an
conventions are surely innate, so labeling internal time-dependent program.
them tells us nothing about how the rules
The pied flycatcher (Ficedula hypoleuca)
actually work.
has a migration route that is basically simFor solitary animals, especially those that ilar to the garden warbler, first moving
must travel long distances unaccompanied southwest, then south and southeast into
by individuals familiar with the route, there Africa. Recent studies by Beck suggest that
may be little opportunity to learn the nec- the mechanisms controlling its first migraessary information. On their first migra- tion are astoundingly complex. When
tion, many birds travel alone, attempting tested in a constant photoperiod and the
to reach an appropriate but unfamiliar magnetic field of Germany these birds
wintering area. How do they know what showed the southwest direction characterdirection to fly and how far to go? At least istic of the beginning of fall migration. As
some of the relevant information seems to the season progressed, unlike the garden
be genetically transmitted in the form of warblers, the flycatchers ceased to show
an endogenous time-based program oriented hopping. Remarkably, flycatchers
(reviewed in Gwinner, 1986). In long-dis- tested in magnetic fields that simulated the
tance migrant European warblers (genera intensity and inclination values encounSylvia and Phylloscopus), the amount of noc- tered along the migration route did show
turnal restlessness {Zugunruhe) exhibited in the shift to southeast at the appropriate
captivity was closely correlated with the time in the migration season (Beck, 1984;
species' migration distance. The same pat- Beck and Wiltschko, 1988). These results
tern was true in several populations of the can only be explained by a scheme in which
blackcap (S. atricapilla) that differed in some measure of seasonal time (indepenmigration distance, and F1 hybrids between dent of photoperiod) interacts with magdifferent populations showed intermediate netic field information indicating latitude
levels of Zugunruhe (Berthold and Quer- (at least) to induce the proper directional
ner, 1981). This quantitative behavioral orientation. Only if the "correct" magcharacter thus shows a high degree of her- netic field value(s) are perceived at the
itability and has been proposed to some- proper time will the migratory program be
how provide a first time migrant with a activated and appropriate orientation
means of traveling approximately the cor- occur. This remarkably intricate control
rect distance to reach the wintering area may represent an extreme case, but it illusof its population.
trates the lengths to which natural selection may go to solve the problem of getting
To reach this wintering place, the young a first-time migrant to a suitable wintering
birds must not only move the proper dis- area.
tance, they must fly in the right direction.
Here, too, there is evidence of a considIt is important to recognize that refererable degree of genetic control. Naive ring to these various phenomena as
hand-raised garden warblers show orien- "endogenous migratory programs" and
tation in the appropriate migratory direc- "innate directional information" can
tion when tested in the earth's magnetic engender a false sense that we understand
field during their first autumn of life. This the mechanisms involved. In fact, we know
species makes a substantial turn in direc- very little indeed about the physiology of
tion in the course of its migration south- these "programs," what environmental
ward into sub-Saharan Africa, and birds parameters drive or modulate them, and
tested in Germany throughout the migra- to what extent and how they are heritable
tion season showed this seasonal shift in (see Scapini, 1988).
direction (Gwinner and Wiltschko, 1978,
While a fairly rigid, heritable control sys-
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KENNETH P. ABLE
tern may be the only viable way to solve
the problem of orientation and migration
in situations in which following or learning
from conspecifics is not possible, there
would seem to be clear advantages to having some plasticity built into the system.
Some of that plasticity is created by the
interactions that occur during the development of orientation mechanisms
described above, and the still controversial
basis of the navigational map in homing
pigeons provides another instructive lesson.
After more than four decades of intensive work, the means by which homing
pigeons determine their location upon
release is not understood to the satisfaction
of workers in the field (see e.g., Wallraff,
1983; Schmidt-Koenig, 1987). In theory
there are two conceptually different ways
in which a pigeon might solve this problem.
On the one hand, the pigeon (or other animal) might rely on information perceived
during the outward journey to infer the
direction and distance of displacement.
There is evidence that pigeons and other
animals use such information when it is
available, but for pigeons there are good
data to suggest that this so-called routebased information is not necessary for
homeward navigation. The other alternative is the existence of some kind of extensive map. There is very little evidence that
animals other than birds possess maps that
extend beyond areas of immediate familiarity (review, Able, 1980).
The search for the sensory basis of the
map sense in pigeons has been generally
characterized by a unitary approach, most
recently with some research groups propounding an olfactory basis for the map
while others propose magnetic maps. There
is a large volume of evidence supporting
the former, some of it quite strong (Wallraff, 1983), and a compelling case can be
made for some involvement of the magnetic field (review, Gould, 1985). The main
basis of controversy has been the fact that
pigeons from research lofts in different
locations behaved differently and results
obtained at one site could often not be replicated convincingly at others (Wiltschko et
al., 1987c). We may just now be beginning
to see the way out of this conundrum by
recognizing that some of these differences
may result from experience-dependent
plasticity in the development of navigation
behavior. Put simply, pigeons may come to
rely preferentially on those factors that
provide the most reliable information at a
given time and place. If true, searching for
a unitary map basis will be sterile, and differences in the environment or rearing
procedures experienced by young pigeons
could have large effects on the map that
develops. Wiltschko et al. (19876) have begun
to make some progress in this direction.
They raised two groups of young pigeons,
one in their normal loft which is quite
shielded from wind, the other in an exposed
loft on the roof of a nearby building.
Deprived of olfactory information both
during displacement and at release, the
birds from the normal loft were unaffected
{i.e., they flew in homeward directions like
their controls), whereas the birds raised on
the roof were not homeward oriented when
deprived of odors. These experiments
involved no direct manipulations of potential environmental factors used in navigation, and the experience of the two groups
differed in other ways, but the results do
show that early experience has a strong
influence on the selection and/or weighting of cues used later for navigation. I think
this approach may point the way toward a
final understanding of how the pigeon's
navigational map works.
Behavioral flexibility later in life
We have just begun to explore the ways
in which the orientation behavior of mature
individuals may be variably responsive to
environmental conditions (Moore, 19856).
In our attempts to understand basic orientation mechanisms we have surely looked
upon the animals too much as automatons.
Variability in orientation behavior is usually a nuisance to our experimental designs,
but to understand fully the adaptive value
of orientation systems, we will have to pay
increasing attention to that variability and
the ways in which it can be explained by
environmental conditions—an ecology of
orientation behavior.
There are numerous examples of flexi-
165
ANIMAL ORIENTATION SYSTEMS
ble behavior. Amphibians can learn to perform Y-axis orientation with respect to a
new shoreline, a capability of obvious adaptive value if animals move to new sites.
Likewise, pigeons can establish a new navigational map if their loft is moved to a
new location later in life. Typical nocturnal
bird migrants sometimes move in the early
morning hours (Gauthreaux, 1978; Bingman, 1980), and they may employ some of
the same orientation mechanisms used at
sunset (Moore, 1986). Honeybees constantly update information about the sun's
movement and relate that information to
landmarks near the hive. If the hive is
moved, new relationships are quickly
established.
In studies of magnetic orientation in the
eastern red-spotted newt, Phillips (1986a,
b, 1987) found that the type of orientation
exhibited (bimodal versus unimodal; shoreward versus toward the home pond) could
be influenced by manipulations of the water
temperature in the tanks in which the newts
lived. The behavior of the newts in response
to the temperature changes was at least
consistent with the expected behavior of
animals experiencing similar environmental contingencies in nature.
A simplistic view would predict that most
birds of the same species, migrating
through the same region at the same season, would exhibit similar orientation
directions. Sandberge<a/. (1988) tested the
orientation of European robins captured
at two sites (about 300 km apart) in southern Sweden. In autumn, birds from the two
places oriented in different directions,
especially when tested under conditions in
which they should have been using magnetic cues. The directions of orientation in
the cages were consistent with recoveries
of birds banded at the two stations. A reasonable scenario to account for these differences is that the fatter, southward orienting birds were expressing a motivation
to continue migration across the Baltic Sea
whereas the leaner birds from the other
site, having reached the coast, reoriented
to find suitable habitats for building up fat
reserves prior to embarking on an overwinter flight.
Discovering the ways in which orienta-
tion behavior responds to environmental
variability in ways that are advantageous
to individuals will require large sample sizes
and clever experimental designs if we are
to move beyond correlational studies. On
the other hand, it represents a new and
wide open area of behavioral ecology that
has the potential to yield exciting new
insights.
CONCLUSIONS
I have tried to discover some generalizations about orientation systems across
animal taxa. The cases I have made are
tentative because they are based on so little
data. One of the things we desperately need
now are studies on a variety of species,
employing similar experimental procedures.
Only in this way can we determine whether
behavioral strategies that seem similar
across animal groups are really based on
common mechanisms, and whether apparent differences in orientation behavior are
real and not a product of differences in
experimental design. At the other end of
this continuum, we need to look at the orientation behavior of a few species under a
variety of conditions to begin to explore the
adaptive variability that will enable us to
relate behavior and ecology in an evolutionary framework.
ACKNOWLEDGMENTS
My orientation studies have been generously supported by the National Science
Foundation. I thank Frank Moore and
Hugh Dingle for helpful comments on the
manuscript.
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