Annurev-Ento-Via Lactea e Besouro

Annual Review of Entomology
How Dung Beetles

Steer Straight
Marie Dacke,1,2 Emily Baird,3 Basil el Jundi,4
Eric J. Warrant,1 and Marcus Byrne2
Annu. Rev. Entomol. 2021.66:243-256. Downloaded from www.annualreviews.org
Access provided by 138.117.176.20 on 03/26/23. For personal use only.
1
Department of Biology, Lund University, 223 62 Lund, Sweden; email: marie.dacke@biol.lu.se,
eric.warrant@biol.lu.se
2
School of Animal, Plant and Environmental Sciences, University of the Witwatersrand,
Johannesburg, South Africa; email: marcus.byrne@wits.ac.za
3
Department of Zoology, Stockholm University, 106 91 Stockholm, Sweden;
email: emily.baird@zoologi.su.se
4
Biocenter, University of Wuerzburg, 97074 Wuerzburg, Germany;
email: basil.el-jundi@uni-wuerzburg.de
Annu. Rev. Entomol. 2021. 66:243–56 Keywords

First published as a Review in Advance on
dung beetle, compass, orientation, navigation, central complex, celestial
August 21, 2020
The Annual Review of Entomology is online at Abstract

ento.annualreviews.org
Distant and predictable features in the environment make ideal compass cues
https://doi.org/10.1146/annurev-ento-042020-
to allow movement along a straight path. Ball-rolling dung beetles use a wide
102149
range of different signals in the day or night sky to steer themselves along
Copyright © 2021 by Annual Reviews.
a fixed bearing. These include the sun, the Milky Way, and the polarization
All rights reserved
pattern generated by the moon. Almost two decades of research into these
remarkable creatures have shown that the dung beetle’s compass is flexible
and readily adapts to the cues available in its current surroundings. In the
morning and afternoon, dung beetles use the sun to orient, but at midday,
they prefer to use the wind, and at night or in a forest, they rely primarily on
polarized skylight to maintain straight paths. We are just starting to under-
stand the neuronal substrate underlying the dung beetle’s compass and the
mystery of why these beetles start each journey with a dance.
243
DUNG BEETLES IN OUR PAST AND PRESENT
Placed over the heart, a carved amulet of a dung beetle was wrapped into the bindings of Egyp-
Scarab: refers to both tian mummies. Inscriptions on the underside of this sacred scarab implored the heart (the seat of
an amulet in ancient intelligence) to confirm the worthiness of the deceased for a place in the afterlife. The Egyptians
Egypt and a family linked the beetle’s role in resurrection to the disappearance of the sun in the West. Buried like a
(Scarabaeidae) of over
dung ball, the sun would be reborn again in the Eastern dawn. The Egyptians apparently believed
30,000 species of
beetles that the movement of the sun across the sky was dictated by a dung beetle (6). More than 3,000
years after the brief rule of the boy pharaoh Tutankhamun, we now know the opposite to be true:
Dung beetles: scarabs
It is the sun that dictates the movement of the beetle (5, 16, 24), and exactly a decade after that
that mostly feed on
feces (a few feed on discovery, we learned that this also holds true for the even more distant stars that form the Milky
plants, millipedes, or Way (10).
carrion); rollers form The sacred scarab (Scarabaeus sacer Linnaeus) is, in real life, a typical ball-rolling dung bee-
dung into balls tle. Of the approximately 600 species that can perform this easily observable feat, fewer than 10
species have been studied in any detail. Of those, the diurnal Scarabaeus lamarcki and the nocturnal
Scarabaeus satyrus account for the bulk of published research on dung beetle orientation behavior
(2, 3, 10, 11, 12, 14–16, 20–22, 24, 25, 33–35, 68).
Ball rolling has arisen several times, presumably from tunneling ancestors (63) that evolved
the ability to form dung into a ball, roll it away from the pat, and bury it underground for future
consumption. To avoid having its carefully manufactured ball stolen by other ball rollers foraging
at the same dung pat, a beetle with a ball will immediately push it away backwards, along a path
as linear as the terrain allows (2, 49). In this straight-line escape toward the unknown, with a ball
many times heavier than itself, the beetle naturally has to negotiate obstacles, holes, and other
hurdles but remains steadfast to its initial bearing for as long as it can (27, 49). If forced to take
a detour around an obstacle that cannot be climbed, the beetle soon continues along its initial
bearing again (5). This seemingly simple act of moving along a given bearing involves a complex
interplay of various sensory modalities, the motor system, and different neuronal circuits (69).
HOW TO GO STRAIGHT
When lost in the desert at night, or in a dense forest, humans cannot maintain a stable course, but
instead plod around in circles (69). Blindfolded, we will walk in circles as small as 20 m in diameter.
The possible effects of biomechanical asymmetries (such as having one leg shorter than the other)
and other general biases can be ruled out as a cause because the direction of this circling (left
or right) is not systematic (69). Deviation from the intended straight course under these circum-
stances is due instead to noise in the sensorimotor system and the unevenness of natural terrain.
Without any external directional references such as the sun or a distant landmark to continuously
recalibrate the system, these errors will accumulate (8). As a result, the intended directed walk will
soon approximate a logarithmic spiral (9).
The celestial compass employed by ball-rolling beetles to steer straight (Figure 1a,b) is visually
calibrated, generally with respect to the sun, the moon, or the stars (4, 5, 10, 12, 13, 16–18, 33, 35),
depending on the beetle’s period of activity. For a dung beetle, the equivalent of being blindfolded
is to roll a ball under an overcast sky, or in total darkness, or experimentally wearing a broad-
brimmed hat that prevents it from seeing the sky. The resulting paths are no longer straight, but
rather are curved and sometimes even describe small circles (10, 14, 15, 49, 68) (Figure 1c). Denied
a view of the sky, dung beetles will often travel back to the start of their journey, where they risk
encountering their ball-thieving relatives squabbling at the dung pile.
A beetle’s desire to transport its dung ball along a single bearing is so strong that it can be
evoked at any time, as long as the beetle is presented with a roughly spherical object (either a
244 Dacke et al.

a b
c
Figure 1
(a) Twenty consecutive exits from the center of an experimental circular arena by three ball-rolling dung
beetles (blue and green tracks: Scarabaeus lamarcki; purple tracks: Sisyphus fasciculatus). Panel adapted with
permission from Reference 50. (b) The diurnal dung beetle S. lamarcki rolling its ball of dung. (c) The curved
tracks of 10 different beetles (Scarabaeus satyrus) when prevented from seeing the sky by the use of a
large-brimmed cap. Panel adapted with permission from Reference 10.
real or synthetic dung ball, either in the field or in the lab) of the right size and smell (25, 49,
68). When given a relevant compass cue, such as, for example, a point light source, and released
with a ball at the center of a circular arena, a beetle will swiftly roll the ball away along a stable
heading (Figure 1a). As soon as the beetle reaches the perimeter of the arena, it can be picked
up and temporarily separated from the ball. Then both can be placed back in the center of the
arena again. From this point, the beetle will set out with the ball in the same direction as before.
Experimentally, this can be repeated at least 100 times. From the rolling paths and exit bearings
recorded at the perimeter of the arena, we can determine (a) the initial rolling direction and (b) the
accuracy of the compass system. The latter is evaluated from the spread of the exit bearings (the
larger is the spread, the larger is the error) (49, 50) and from the tortuosity of the rolling paths (the
more winding or tortuous are the paths, the larger is the error) (12, 14, 68). Then, by manipulating
the sensory input between consecutive rolls from the center of the arena, we can also determine to
which compass cue the beetle is orienting. For example, using a mirror to cause the sun or moon
to appear on the opposite side of the sky, or repositioning a green LED by 180° in the lab, causes
the beetle to take a new direction opposite to its initial heading (16, 21, 25). According to its sun
compass (5), which has been found in all diurnal species tested to date, the beetle is still moving
in the same direction. Using the same logic, researchers have discovered that the beetles’ celestial
Snapshot: the state of
compass can also use the gradient of color or light intensity in the sky (21, 24), along with the a system at a particular
moon (12, 13, 25, 68), the polarization pattern around the sun or the moon (17, 18, 24, 25, 34), or point in time
the faint mist of stars that make up the Milky Way (10, 33, 35).
Linearly polarized
light: light that
oscillates mainly in
A CELESTIAL SNAPSHOT TO STEER BY one axis, perpendicular
El Jundi and colleagues (22) recently proposed that ball-rolling beetles record a celestial snapshot to its line of travel; can
be detected by most
of the sky’s features at the start of their journey, and then match this snapshot to their current
insects
celestial view to maintain a straight path. This conclusion was reached by studying the steering
response of beetles orienting under artificial skies with sources of unpolarized and/or linearly
polarized light presented in different combinations and at changing positions. On a clear day, the
www.annualreviews.org • The Dung Beetle Compass 245

snapshot can include the position of the sun, the circular pattern of polarized light that surrounds
it, and the gradients of color and light intensity that form across the sky, although there has been
no direct testing of whether beetles snapshot these last two cues (21, 22, 24). The snapshot strategy
is as simple as it is successful: The beetle will be sure to travel along a constant bearing as long
as the stored celestial snapshot matches the beetle’s current view of the sky. When these elements
do not match (that is, when the beetle is off course), the beetle simply needs to rotate until the
neuronal snapshot and the perceived celestial view are once again aligned and its orientation is
restored (15, 22).
Although we often describe the path of ball-rolling beetles as being a straight line, the truth
is that their trajectory is never completely straight. The evolutionarily acceptable—or noise-
limited—deviation between their stored and current views seems to be approximately 20°. This
estimate can be calculated from the mean difference between two consecutive exit bearings from
the center of a flat, circular arena when rolling under a clear blue sky (16). Interestingly, this ori-
entation error does not increase when the beetles are released in a highly artificial environment
that only offers a green LED as an ersatz sun to steer by (25). In fact, the same beetle will even
match the snapshot that it obtained in the visually rich outdoor environment to the solitary light
of a green LED in an otherwise dark and featureless lab (or vice versa) (25). In this situation, the
beetle reliably matches the position of the bright sun in its outdoor snapshot to the position of a
bright LED indoors.
While other insects, like bees and ants, show an innate ability to predict the positional rela-
tionships among the different elements of the sky, for example, the skylight polarization pattern
and the position of the sun (52, 81), dung beetles seem to accept any combination of these cues
for their snapshot (22). For example, a polarization pattern can be artificially presented together
with an ersatz sun in a way that is not physically possible in the real sky, without either cue losing
its utility for an orientating beetle (22). Such a navigational technique, which is both computa-
tionally straightforward and flexible, could explain the capacity of these insects to maintain their
orientation abilities under the many different types of skies or experimental setups that life, or the
researcher, presents to them.
THE ENIGMATIC BEETLE DANCE

At the start of its journey, once it has packed the dung into a neat sphere, the beetle climbs onto
the ball, pausing momentarily halfway up, with its hind legs still in contact with the ground, before
mounting the top of the ball. Once on top, the beetle rotates about its dorsal–ventral axis, occa-
sionally making brief pauses before climbing down head first and pushing the ball away backwards
(3) (Figure 2). This stereotypical behavior, known as the dance, seems to play an important—but
still somewhat puzzling—role in the orientation behavior of ball-rolling dung beetles.
Figure 2
Elements of the dung beetle dance. The beetle climbs halfway up onto the ball, making a brief pause before
climbing fully on top and starting to rotate. During the rotation, the beetle makes a series of brief pauses
before climbing down and rolling the ball away. Note the horizontal position of the head during the dance.
246 Dacke et al.

In the lab, a beetle can be presented with a single new orientation cue (for example, a UV
light spot or polarized light), in addition to a green light spot mimicking the sun, during or af-
ter the performance of a dance (22). The beetle will steer by the additional cues only if they
are added while it is dancing and will ignore them if they are added once it has begun to roll.
These results suggest that some component, or combination of elements, of the dance facili-
tates the formation of the celestial snapshot (15, 22). Whether this snapshot is formed during ball
mounting, while pausing or rotating during the dance, or during all of these actions remains to be
determined.
Dung beetles are not the only animals that stop and rotate. During their initial forays from
the nest, ants will stand and perform pirouettes where they rotate about their dorsal axis while
occasionally pausing in the direction of the nest (30–32, 59, 85). A recent study of Cataglyphis
noda has shown that the direction of these pauses can even be guided by the earth’s magnetic
field (30a). The terrestrial snapshots of the nest and its surroundings that the ants obtain by these
rotations help them to locate their home as they return. However, as far as we can understand from
experiments in which we systematically move the dung pile, rotate overhead objects, or displace
individuals to novel terrain—all while the beetle is in the process of rolling its ball—dung beetles
do not need terrestrial landmarks to successfully roll along a constant bearing (14). This is not
surprising, considering that they are transient visitors to ephemeral dung pats who will not benefit
from memorizing landmarks in each novel location. The dung beetle dance therefore does not
appear to be involved in landmark learning.
The rotational component of the beetles’ dance could potentially play an important role in
enabling them to compare the rotation of their body with the relative movement of celestial
cues in the visual scene. This comparison would enable beetles to determine which celestial
cue is most reliable at that time and, in this way, set these signals in a hierarchy of usefulness
(5, 24, 25, 50). Another potential function of the dance could also be a practical one: Climb-
ing up onto the ball enables the beetle to easily align itself along its chosen bearing by rotating
about its dorsal axis, then descending into a head-down position to begin (or continue) pushing
the ball in the chosen direction. The rotation on top of the ball could also potentially help to
raise the beetle above the ground so that it has a better view of the sky while simultaneously being
able to defend its food parcel from other hungry marauding beetles.
It is important to note that a beetle will also dance if it loses control of its ball, deviates from
its intended course, or experiences large changes in the apparent position of the sun (3). This
indicates that, en route, the dance may play a role in enabling beetles to reorient after experiencing
disturbances to their rolling path. Any self-induced stop, such as when climbing onto the ball
to escape the scorching heat of the midday ground (67), will also warrant a dance, and beetles
sometimes dance for no apparent reason—to the frustration of observers trying to understand the
dance’s function.
THE CELESTIAL COMPASS: CHALLENGES, BACK-UPS,

AND ADAPTATIONS
We have noted that objects such as tripods, the experimenter, or even the dung pile can be reposi-
tioned without causing a change in the beetles’ behavior or choice of direction. Even if transferred
to a different site mid-roll, the beetles do not change their direction (14). For researchers, this dis-
regard of landmarks is beneficial because it makes it easier to design experiments. For the beetles, it
removes the potential of having a stable back-up for their celestial compass system. Consequently,
this creates some challenges for the ball roller, particularly when the sun is at, or close to, its
zenith.

Wind Augments Ambiguous Celestial Cues in the Middle of the Day
As the sun approaches the top of its daily path, it becomes increasingly unreliable as an orientation
Azimuth: angular cue (58). This is because any small change in heading has little effect on the position of the sun
distance from North on the retina, making it difficult for beetles to reliably match the scene to the stored snapshot. As
to the point at which a the sun’s elevation increases, the 20° error between consecutive rolls recorded at low and medium
perpendicular line
solar elevations increases to above 40° (16). At such times, when the directional information from
passing through the
celestial object celestial cues is less reliable, the dung beetles’ compass instead takes directional information, if
intersects the horizon available, from the wind (11).
Recent experiments show that, when the sun is higher than 75° in the sky, diurnal dung beetles
Sisyphus: refers to
both a mythological will change direction by 180° if the direction of the wind changes by 180° (11). This can be easily
Greek king punished simulated by alternating the wind direction between a pair of fans facing each other across the
to push a large rock up ball-rolling arena. It is important to note that the diurnal dung beetle is able to orient in any
a hill for eternity and a direction with respect to the wind. This means that dung beetles, like the desert ant Cataglyphis
dung beetle genus

(58, 82–84), and the fruit fly Drosophila melanogaster (59a), carry a wind compass. As the sun sinks
closer to the horizon and once again becomes a reliable orientation cue (16), any switch in wind
direction is ignored (11).

The beetle wind compass is an impressive product of evolution because it seems so beautifully
matched to the habitat in which researchers discovered this phenomenon: The Kalahari wind
blows strongest around midday (when the sun is highest), driven by heat rising from the semiarid
landscape after a morning baking in the sun (11). Even more impressive is that this directional
information can be transferred from the wind compass to the sun compass and vice versa (11),
each providing a back-up for the other cue. The prevalence of the wind compass across other
species has yet to be determined.
An additional challenge for a solar compass is that the sun moves, changing its azimuthal po-
sition (relative to North) during the day. Consequently, an animal maintaining a given bearing to
the sun for an extended amount of time will move along a curved track. Many insects compensate
for this by using an internal clock (36, 53, 57, 80); however, this movement of the sun is most
likely not a concern for dung beetles during their brief, six-minute (on average) food-transporting
excursions (11).
Forest Beetles Are Guided by Their Polarization Compass

Forests are demanding for any celestially guided creature to travel through. The beetles are con-
stantly forced off course by vegetation and have limited information about their orientation, as
the canopy prevents a clear view of various celestial cues. Ants, along with many forest species,
memorize the local canopy pattern formed by the dark foliage silhouetted against the bright
sky and use it to locate their nest (19, 43, 44, 60). A similar strategy is employed by nocturnal
shield bugs (41, 42). This type of localized compass cue is, however, only effective if the insect
has had the opportunity to learn and remember the spatial relationship between the overhead
canopy pattern and its nest site. Dung beetles, which direct their movements over unfamiliar ter-
ritory toward an undefined goal, must instead rely on more global cues, the most ubiquitous be-
ing the celestial signals discussed above. To understand how dung beetles have adapted to the
forest challenge, researchers have turned their attention to the woodland-living beetle Sisyphus
fasciculatus.
In a set of experiments with these delicate, spidery, long-legged beetles, Khaldy and colleagues
(50) showed that moving the sun to the opposite side of the sky (using a mirror) has no effect on
the beetles’ roll bearings. This stands in direct contrast to the well-documented 180° change in
bearing recorded in savanna-living beetles (5, 16, 24, 25, 68) tested under the same experimental
248 Dacke et al.

condition. Khaldy and colleagues thus concluded that the sun is not the primary cue for orienta-
tion in Sisyphus. This makes sense, as movement under an overhead canopy will cause the sun to
frequently be hidden from direct view. Provided that patches of clear sky are visible, the wide-field
Polarizing filter:
celestial pattern of polarized light will remain just as reliable under a canopy as under the open sky converts incident
(37, 66). Not surprisingly, as soon as a polarizing filter is turned above these beetles, they turn with unpolarized light (that
it (50). This suggests that the hierarchy of orientation cues used in the snapshot compass network oscillates in all
of the beetle is closely adapted to the habitat in which the user is active. More comparisons among directions) into
linearly polarized light
dung beetle species active in different types of visual habitats are currently underway to put this
(that oscillates mainly
theory to the test. in one axis)
Central complex:
Nocturnal Beetles Rely on Sky-Wide Cues for Orientation brain area that (among
Nocturnal dung beetles, like many other nocturnal insects, face a particular challenge for vi- other functions)
encodes the
sual orientation at night—the small pupils of their compound eyes have difficulty collecting
orientation of its
enough light to sustain reliable vision (76, 77). Nonetheless, due to the high optical sensitiv- owner in relation to
ity of their superposition compound eyes (7, 55, 56, 73, 78, 79) (Figure 3a,b), and by employ- the external world
ing neural summation strategies that significantly improve visual reliability in dim light (70, 71,
74), nocturnal insects, including nocturnal dung beetles, can acquire remarkable visual capacities
(75).
It is this excellent night vision that allows nocturnal dung beetles to see several features of the
night sky that turn out to be critical compass cues for their orientation. These insects are, for
instance, the only animals known to use the broad, faint pattern of polarized light formed around
the moon to keep a straight-line course (17, 18, 25, 34) (Figure 3c). They have the ability to orient
by the moon itself (12, 13, 68), but it is the moon’s polarization pattern that is the preferred cue,
possibly because this cue can be integrated across the entire night sky (25).
When the moon is not present for all or most of the night, nocturnal dung beetles can revert to
the Milky Way for orientation (10, 33, 35) (Figure 3d). This broad bright extended stripe of light,
arching across the dome of the night sky, is easily visible to their sensitive superposition eyes, even
if few individual stars are sufficiently bright to be seen. The essential feature of the Milky Way
that allows unambiguous orientation is its internal gradient of light intensity (33)—the Milky Way
is noticeably brighter in the southern half of the night sky than in the northern half (Figure 3d).
Had this not been the case, and were the Milky Way evenly bright in both halves of the sky,
then a 180° orientation ambiguity could potentially arise (33). Dung beetles are the only animals
known to use the Milky Way for short-range straight-line orientation, but other nocturnal animals
probably use it too. For all of these animals, the ever-increasing presence of anthropogenic light
pollution (see the sidebar titled The Disadvantages of Enlightenment?) could begin to obscure
the essential features of the night sky needed for orientation, thereby threatening the ability of
nocturnal animals to efficiently carry out the tasks of their daily life.
THE INTERNAL COMPASS

For a dung beetle to move its ball along a desired course, external compass information needs to
be adequately processed and turned into a steering command. This happens in the Y-shaped brain
at the center of its flat, shovel-shaped head (48). From the eyes—via the optic lobe and the anterior
optic tubercle—celestial information is transferred to a small, easily identifiable neuropil in the
central brain known as the bulb (26, 48). From this point, the compass information is transmitted
to the neurons in a higher brain center, the central complex (25) (Figure 4). It is there that we find
the internal compass of dung beetles and all other migrating and navigating insects investigated
to date (23, 25, 38, 39, 45, 62, 64, 72).

a b
0.5 mm
c Moon
d
1.0
0.8
0.6
0.4
0.2
0.0
Figure 3
(a,b) The size of the eye and the dark-adapted optical pupil (known as the superposition aperture) (white
circles) in two species of dung beetles from the same genus (Onitis): (a) the diurnal Onitis belial and (b) the
nocturnal Onitis aygulus. The superposition aperture contains several hundred ommatidial facets, each
collecting and focusing light on a single photoreceptor (i.e., rhabdom) in the underlying retina—the larger is
this pupil, the more sensitive is the eye. The dashed circles represent effective apertures, theoretically
derived apertures in which each facet contributes light equally (79). In reality, facets near the edge of the real
aperture contribute less light than those near the center. Note how the eye and superposition aperture are
larger in the beetle from the dimmer habitat. Panels a and b are adapted with permission from Reference 56.
(c,d) Fisheye images of the sky in rural South Africa. In panel c, the moon is near the horizon, causing the
maximum degree of polarization band to cross the sky at an angular distance of 90° from the moon itself.
Estimated degrees of linear polarization are relative to the color map to the right of the image; redder hues
indicate high degrees of polarization, and blue hues indicate low degrees of polarization. In panel d, the
moon is well below the horizon, revealing the bright band of the Milky Way. Note the difference in intensity
across this faint band of light. Panel c adapted with permission from Reference 34.
Central Coding of Compass Cues

Superposition
aperture: the To begin to understand how different skylight cues are coded in the brain, we have recorded
diameter of the region neuronal activity in the beetle central complex while simulating a beetle turning 360° under a
of facets that accepts natural sky. This is achieved by recording the activity of neurons while rotating a polarizer in
light for superposition the dorsal visual field (mimicking a turn in the celestial polarization pattern) or circling a green
on a single rhabdom
light spot at a certain elevation (simulating the sun or moon) above a constrained beetle (25). This
Rhabdom: type of recording reveals that at least four types of central complex neurons are highly sensitive to
light-absorbing part of polarized light and to the position of a single light source (i.e., the sun or the moon) (15, 20, 25). In
the visual receptor in
locusts, this dual input is considered to give rise to a map-like representation of polarization angles
the eye of an
arthropod; contains (39, 40) and sun directions (61). Combined, they provide the insect with an unambiguous compass
visual pigments signal throughout the day. Given the similarity in neuroarchitecture and encoding of sky compass
cues in the locust’s and dung beetle’s central complex (46), a similar map-like representation of
compass cues probably guides the beetle on its straight travels.
250 Dacke et al.

THE DISADVANTAGES OF ENLIGHTENMENT?
Light pollution describes the swamping of natural nighttime light by anthropogenic sources of light. Currently,
more than 80% of the world’s population lives under light polluted night skies, and one-third of humankind can no
longer see the Milky Way (28). This addition of light to the night sky fundamentally alters the visual world for many
species of our nocturnal fauna. Newly hatched turtles crawl to lights and away from the safety of the ocean (54),
and migrating and local birds can be attracted to night lights (47). Such phenomena result in hundreds of millions
of wildlife deaths each year. Light pollution also masks the moon, the stars, and the celestial pattern of polarized
light in the night sky. The rapid growth of cities makes it increasingly important to understand the mechanisms
behind animal orientation and navigation at night. We can use dung beetles to determine how a celestial compass
is affected by these changes in the night sky. This knowledge can then be used to find ways to minimize the effects
of light pollution. In contrast to many other anthropogenic threats to our planet, this type of pollution could easily
be reduced or even eliminated by simply switching it off.
It remains to be shown if orientation in response to wind cues is also processed by the central
Celestial polarization
complex of the beetle brain. Given the recent description of central-complex neurons that inte-
pattern: a pattern of
grate wind and visual cues in Drosophila (59a), and the fact that beetles can transfer the desired partially linearly
heading direction from the wind to the sun compass and vice versa (11), it would be surprising if polarized light in the
this is not the case. The recent discovery of yet another set of central-complex neurons that re- sky created by the
spond to the rotation of a (simulated) starry sky in the night-migrating Bogong moth (1) supports scattering of sunlight
or moonlight
our belief that this dim light compass cue is also processed in this highly integrative part of the
insect brain.
Moonrise
Lun
ar M
12 am po
ay
oo ized
l
n
W
ar
y period of S. sa
tivit
lky
Ac tyr
us
Mi
ligh
t
Sunset
6 pm 6 am
Sunrise
February 13, 2020
S ola
r po ind
Ac i
rc k
Su ize d
t iv
p e rio d o f S. la m a
it y
n
lar
W
lig 12pm
ht
Moonset
Figure 4
The main compass cues (arrows) used by dung beetles (Scarabaeus lamarcki and Scarabaeus satyrus) to steer
straight across the savanna will change over a 24-h period. We believe that this change in cue preference is
encoded by the brain’s central complex (center), driven by the changing reliability of the different compass
cues. This could be analyzed by the beetle during the rotational part of its dance.

The Dynamic Dung Beetle Compass
From years of work with such pliable subjects, it has become apparent that the dung beetle compass
is not preprogrammed. Rather, it continuously adapts to the visual ecology of its owner: In the
morning or the afternoon, dung beetles primarily orient with the sun; at midday, they react to the
wind; and at night (or in a forest), they favor the celestial polarization pattern (Figure 4). This
dynamic coding has been recorded in the central complex, where the same neurons switch their
response from a single light source at high light intensities to a broad-field polarized light stimulus
at low light intensities (25).
While this adaptability most likely reflects the relative reliability of each compass cue at any
given point in time, we do not yet understand how this flexible hierarchy of cues is established in
the beetle’s brain. One possibility is that it could be created during the rotational component of the
dance: A high signal modulation during rotation would indicate a high reliability for that signal.
This mechanism would require the insect to correlate its body orientation with visual input from
the sky (or mechanosensory input from the wind). In flies, the central complex has been shown to
combine visual information with motor feedback from the legs (65) and to possess the potential
to switch the cue hierarchy within a short period of time (29, 51). The central complex, as a highly
integrative part of the brain, thus may potentially process all dimensions of the dynamic dung
beetle compass.
FUTURE ISSUES
1. The rapid growth of cities makes it increasingly important to understand the mecha-
nisms behind animal orientation and navigation at night. This knowledge will be valu-
able in current and future efforts to reduce the negative effects of light pollution on
nocturnal fauna.
2. Studies of homing dung beetles in Africa (Scarabaeus galenus and Pachysoma spp.) and
South America (Eucranium spp.) could broaden our understanding of navigation in in-
sects. Comparisons with the straight-line, orienting dung beetles (e.g., S. lamarcki and
E. satyrus), which only ever depart and never return to the same dung pat, might also
provide useful insights into the evolution of navigation.
3. Recent evidence for context-dependent modulation of the central complex makes it crit-
ical to study the compass networks of insects that actively orient in their natural envi-
ronment. This can be accomplished using recordings from tethered or completely un-
constrained insects.
4. Several hypothetical neural circuits have been proposed as models for biological compass
systems. Modeling how celestial compass signals are selected, processed, and integrated
(including the neuronal processes that dictate what cue or cues should be followed at
any given moment) will represent an important and informative step toward a full un-
derstanding of how a robust compass system can be designed.
DISCLOSURE STATEMENT
The authors are not aware of any affiliations, memberships, funding, or financial holdings that
might be perceived as affecting the objectivity of this review.
252 Dacke et al.

ACKNOWLEDGMENTS
We would like to thank Clarke Scholtz for introducing many of us to the wonderful world of dung
beetles, the Harvey family and Adventures with Elephants for access to their farms and beetles,
and Inger Ekström for illustrations.
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Preference Provides a Plethora of Problems (Don’t Panic)

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A Century of Synergy in Termite Symbiosis Research: Linking the Past
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Annual Review of Entomology

How Dung Beetles

Annu. Rev. Entomol. 2021. 66:243–56 Keywords

The Annual Review of Entomology is online at Abstract

244 Dacke et al.

www.annualreviews.org • The Dung Beetle Compass 245

THE ENIGMATIC BEETLE DANCE

246 Dacke et al.

THE CELESTIAL COMPASS: CHALLENGES, BACK-UPS,

www.annualreviews.org • The Dung Beetle Compass 247

dung beetle genus

direction is ignored (11).

Forest Beetles Are Guided by Their Polarization Compass

248 Dacke et al.

THE INTERNAL COMPASS

www.annualreviews.org • The Dung Beetle Compass 249

Central Coding of Compass Cues

250 Dacke et al.

www.annualreviews.org • The Dung Beetle Compass 251

252 Dacke et al.

LW Simmons, J Ridsdill-Smith. Oxford, UK: Wiley-Blackwell

beetles for orientation. J. Comp. Physiol A 189:411–18

www.annualreviews.org • The Dung Beetle Compass 253

of learning walk elements in Cataglyphis ants. J. Exp. Biol. 220:2426–35

254 Dacke et al.

J. Comp. Physiol. A 183:45–60 evolution molds the

www.annualreviews.org • The Dung Beetle Compass 255

after sunset. Experientia 27:1364–66

256 Dacke et al.

Contents Volume 66, 2021

Preference Provides a Plethora of Problems (Don’t Panic)

Michael E. Scharf and Brittany F. Peterson p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p23

Chemical Ecology, Biochemistry, and Molecular Biology of Insect

Spider Diversification Through Space and Time

Navigation Along Windborne Plumes of Pheromone and

An online log of corrections to Annual Review of Entomology articles may be found at

From the Annual Review of Animal Biosciences, Volume 8 (2020)

Arthropod Origins: Integrating Paleontological and Molecular Evidence

From the Annual Review of Microbiology, Volume 74 (2020)

From the Annual Review of Phytopathology, Volume 58 (2020)

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