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First published online May 19, 2008
Journal of Experimental Biology 211, 1737-1746 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.015396
Novel sensory modalities for navigation and other behaviours |
Seeing in the dark: vision and visual behaviour in nocturnal bees and wasps
Department of Cell and Organism Biology, Zoology Building, University of Lund, Helgonavägen 3, S-22362 Lund, Sweden
e-mail: eric.warrant{at}cob.lu.se
Accepted 12 February 2008
Summary
In response to the pressures of predation, parasitism and competition for limited resources, several groups of (mainly) tropical bees and wasps have independently evolved a nocturnal lifestyle. Like their day-active (diurnal) relatives, these insects possess apposition compound eyes, a relatively light-insensitive eye design that is best suited to vision in bright light. Despite this, nocturnal bees and wasps are able to forage at night, with many species capable of flying through a dark and complex forest between the nest and a foraging site, a behaviour that relies heavily on vision and is limited by light intensity. In the two best-studied species – the Central American sweat bee Megalopta genalis (Halictidae) and the Indian carpenter bee Xylocopa tranquebarica (Apidae) – learned visual landmarks are used to guide foraging and homing. Their apposition eyes, however, have only around 30 times greater optical sensitivity than the eyes of their closest diurnal relatives, a fact that is apparently inconsistent with their remarkable nocturnal visual abilities. Moreover, signals generated in the photoreceptors, even though amplified by a high transduction gain, are too noisy and slow to transmit significant amounts of information in dim light. How have nocturnal bees and wasps resolved these paradoxes? Even though this question remains to be answered conclusively, a mounting body of theoretical and experimental evidence suggests that the slow and noisy visual signals generated by the photoreceptors are spatially summed by second-order monopolar cells in the lamina, a process that could dramatically improve visual reliability for the coarser and slower features of the visual world at night.
Key words: nocturnal vision, compound eye, bee, wasp, landmark orientation, resolution, sensitivity, spatial summation
Introduction
To see reliably, an eye must capture sufficient light. For a diurnal
(day-active) animal, adapted for vision in bright sunlight, this basic
requirement is easily achieved. However, at night, or at tremendous depths in
the sea, where light levels may be many orders of magnitude lower, reliable
vision cannot be guaranteed. Indeed, many nocturnal and deep-sea animals have
simply ceased to rely on vision as their primary sense, depending instead on
olfaction, hearing, electroreception and mechanoreception to interpret their
environments (Warrant and Locket,
2004
; Warrant,
2008). This, however, is by no means the rule: many others have
invested heavily in vision, evolving remarkable adaptations to see well in dim
light (Laughlin, 1990;
Meyer-Rochow and Nilsson,
1998; McIntyre and Caveney,
1998; Warrant,
2004; Warrant,
2006; Warrant,
2008). This review showcases one particular group of such animals
– the nocturnal bees and wasps – a group that is starting to
reveal some of the basic principles used by animals to process visual
information in dim light.
To see well in dim light, a visual system needs to extract reliable
information from what may be an unreliable visual signal; that is, to extract
information from a visual signal that is contaminated by visual `noise'. Part
of this noise arises from the stochastic nature of photon arrival and
absorption: each sample of absorbed photons (or signal) has a certain degree
of uncertainty (or noise) associated with it. The relative magnitude of this
uncertainty is greater at lower rates of photon absorption, and these quantum
fluctuations set an upper limit to the visual signal-to-noise ratio
(Rose, 1942;
de Vries, 1943;
Land, 1981). As light levels
fall, the fewer the number of photons that are absorbed, the greater the noise
relative to the signal and the less that can be seen. Signal reliability in
dim light can thus be improved with an eye design of high sensitivity to
light. In nocturnal insects, including most moths and many beetles, this eye
design is typically a refracting superposition compound eye, a design that
allows single photoreceptors in the retina to receive focused light from
hundreds (and in some extreme cases, thousands) of corneal facet lenses
(Fig. 1B). This design
represents a vast improvement in sensitivity over the apposition compound eye
(Fig. 1A), a design in which
single photoreceptors receive light only from the single corneal facet lens
residing in the same ommatidium. Not surprisingly, apposition eyes are typical
of diurnal insects active in bright sunlight, and this includes all diurnal
bees and wasps. Strangely, apposition eyes are also found in several groups of
bees and wasps (and also ants) that have evolved a nocturnal lifestyle. Even
stranger, despite the poor sensitivity afforded by apposition eyes, these
insects invariably see quite well, with well-documented abilities to learn
visual landmarks and to use them during foraging and homing
(Warrant et al., 2004;
Greiner et al., 2007b;
Somanathan et al., 2008).
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Nocturnality in bees and wasps
Activity periods
Nocturnal and crepuscular (dusk and dawn) foraging activity in bees has
arisen independently in at least four of the seven recognised families of
bees, namely in the Colletidae, the Andrenidae, the Halictidae and the Apidae
(Hopkins et al., 2000;
Wcislo et al., 2004;
Taylor, 2007;
Warrant, 2007). Most species
are tropical or subtropical, but many are found in warmer arid areas at higher
latitudes. Only one species is known to be obligately nocturnal, and this is
the giant Indian carpenter bee Xylocopa tranquebarica (Apidae), a bee
capable of foraging even on the darkest moonless nights when light levels can
be as low as 10–5 cd m–2
(Burgett and Sukumalanand,
2000; Somanathan and Borges,
2001; Somanathan et al.,
2008). Many species are known to be crepuscular, such as
Xylocopa tabaniformis, Xenoglossa fulva, Ptiloglossa guinea and the
well-studied Central American sweat bee Megalopta genalis
(Linsley et al., 1955;
Janzen, 1968;
Roberts, 1971;
Warrant et al., 2004;
Kelber et al., 2006).
Megalopta genalis (Fig.
2A), for instance, is active under the thick rainforest canopy
during two short time windows shortly after dusk and before dawn
(Fig. 3)
(Warrant et al., 2004;
Kelber et al., 2006). Other
species, although primarily diurnal or crepuscular, are also capable of
foraging throughout the night if a moon half-full or larger is present in the
sky. Good examples include two species of honeybees (Apidae, genus
Apis) – the giant Asian honeybee Apis dorsata and the
African honeybee Apis mellifera adansonii – and the sweat bee
Lasioglossum (Sphecodogastra) texana
(Kerfoot, 1967a;
Kerfoot, 1967b;
Fletcher, 1978;
Dyer, 1985;
Kirchner and Dreller,
1993).
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Among the wasps, nocturnal activity has only arisen among the velvet ants
(family Mutillidae), and in two vespid genera, the neotropical Apoica
(Fig. 2B,C; Polistinae –
with nine species) and the southeast Asian Provespa (Vespinae –
with three species). Both Apoica and Provespa are active
nocturnal foragers, with both species collecting arthropod prey and pollen
(von Schremmer, 1972;
Maschwitz and Hänel,
1988; Hunt et al.,
1995; Martin,
1995; Matsuura,
1999). Hunt and colleagues
(Hunt et al., 1995) found that
Apoica forages during the first 4 h of the evening when the moon is
new or small, with another small peak of activity just before dawn (due to
wasps returning to the nest, possibly because it was too dark to find their
way home any earlier). As the moon waxes, Apoica also begins to
forage all night (Hunt et al.,
1995; Nascimento and
Tannure-Nascimento, 2005).
Why have some bees and wasps – and many other species of animals
– become nocturnal? Two main reasons have been hypothesised. The first
is reduced competition (Cockerell,
1923; Roubik,
1992; Hopkins et al.,
2000; Kronfeld-Schor and
Dayan, 2003; Wcislo et al.,
2004). In the forested habitats where nocturnal bees and wasps are
typically found, many species of trees and plants have flowers that open only
at night, or that produce nectar both day and night. Compared with diurnal
nectar sources, nocturnal flower resources are exploited by comparatively few
other animals – only bats and moths are notable competitors. The
abundance of nectar and pollen reserves probably drove bees to forage at
dimmer light levels, both later into the evening, to exploit the typically
generous nectar supplies of nocturnal flowers, and earlier in the morning,
when the nectar reserves of newly opened flowers are still relatively
untapped. The second probable reason why bees and wasps became nocturnal was
to avoid predation and parasitism (Bohart
and Youssef, 1976; Smith et
al., 2003; Kronfeld-Schor and
Dayan, 2003; Wcislo et al.,
2004). Diurnal bees and wasps are heavily attacked by predators
and parasites alike, and the nocturnal niche may have represented a convenient
escape route.
Eye size, ocellus size and nocturnality
Despite being nocturnal, our discussion above indicates that light levels
– and by implication visual reliability – nonetheless limit
foraging activity in bees and wasps active at night
(Kelber et al., 2006). Some
species are clearly crepuscular, requiring slightly brighter twilight skies to
see well enough to negotiate obstacles during flight and to find their way
home following a foraging trip. Those that fly all night often require the
presence of bright moonlight. Light levels are thus limiting – a species
capable of visual foraging in the early dusk may be forced back to the nest
just a short time later before light levels have become unacceptably dim.
This light-level limitation has led to the evolution of proportionately
larger compound eyes and ocelli that have an improved capacity to capture
light. The ocelli, the three round eyelets located on the dorsal surface of
the head between the two compound eyes, are significantly larger relative to
body size in species that fly in dim light
(Kerfoot, 1967b;
Kelber et al., 2006;
Warrant et al., 2006). These
specialised eyes – which probably play a role in flight control
(Berry et al., 2007) –
are a tell-tale indicator of nocturnal behaviour in bees and wasps. In the
giant nocturnal Indian carpenter bee (Xylocopa tranquebarica) they
measure almost a millimetre across. The ocelli of the similarly sized
sympatric diurnal species X. ruficornis are significantly less than
half this size. While differing less dramatically, the compound eyes of the
nocturnal species are also relatively larger, and typically contain larger
numbers of ommatidia, than those of their diurnal relatives
(Jander and Jander, 2002).
Interestingly, the common European hornet Vespa crabro, which has
also been suggested to have nocturnal activity
(Blackith, 1958;
Spiewok and Schmolz, 2006),
lacks all such optical enlargements (F. Jonsson, A. Kelber and E.J.W., in
preparation).
Nocturnal visual behaviour in bees and wasps
Despite the fact that the visual systems of nocturnal bees and wasps are clearly operating near their limits, these insects are capable of quite sophisticated visual behaviours. Recent studies have shown that they are capable of visually learning landmarks around their nest entrances, and using them for homing, although the capacity to fly quickly and accurately in the vicinity of the nest is nevertheless affected by light level, and ultimately limited by it.
Homing, foraging and visual navigation
Bees and wasps are well known for their ability to forage at significant
distances from their nests, and to routinely and repeatedly return to the nest
with pollen and other provisions. In diurnal species this ability to `home' is
known to be a predominantly visual task. The location of the nest, and
favoured routes to flowers or other resources, are recognised by landmarks
that are learned visually and stored for later retrieval (reviewed in
Collett et al., 2003). The
directions and distances flown to and from the foraging site are also
determined visually (reviewed in
Srinivasan et al., 2006), and
in honeybees this information is transferred to other bees in the hive.
In order to locate and recognise its nest after returning from a foraging
trip, diurnal bees learn the arrangement of landmarks around the nest
entrance. This is done by performing an `orientation flight'
(Becker, 1958;
Zeil et al., 1996;
Lehrer, 1996;
Capaldi and Dyer, 1999): as a
bee flies from its nest, it turns to face the nest entrance and begins to fly
backwards in increasingly larger arcs to survey (and learn) the field of local
landmarks. In the sweat bee Megalopta genalis and the carpenter bee
Xylocopa tranquebarica, both active in extremely dim light, recent
behavioural investigations have revealed that both species perform such
orientation flights (Fig. 4A)
and use them to visually learn landmarks around the nest entrance at night
(Fig. 4B,C)
(Warrant et al., 2004;
Somanathan et al., 2008). For
experiments on Megalopta, five nest sticks were placed beside one
another on a small stand in the rainforest and, of these, only the middle nest
was occupied (marked by a stars in Fig.
4B,C). The bee left its nest at 18:48 h (16 min after sunset),
performed an orientation flight for a few seconds (presumably learning the
spatial arrangement of the five nests), and then left
(Fig. 4B, upper panel). While
the bee was away, the positions of the bee's nest and an empty nest were
swapped (Fig. 4B, lower panel).
Upon return at 18:58 h, the bee flew without hesitation into the central
unoccupied nest – the `spatially correct' nest – but after a
couple of seconds flew out again. After re-surveying the nests, the bee
returned to the central nest, again immediately flying out. Presumably the
aroma or some other feature of the nest was repellent to the bee, and it was
not until the bee's actual nest was retuned to the central position that the
bee ceased to re-emerge. In a second experiment, a moveable white card was
instead used as a landmark – the bee's nest in this case remained in its
original location. Prior to the bee's departure, the landmark was placed over
the entrance of the central, occupied nest
(Fig. 4C, upper panel). The bee
departed its nest at 18:40 h, performed an orientation flight, and left. While
the bee was away, the white card was placed over the entrance of a
neighbouring unoccupied nest. The bee returned at 18:58 h and flew directly
into the landmarked unoccupied nest (Fig.
4C, lower panel). As before, the bee flew out almost immediately,
due to the foreign internal environment of the landmarked nest. This continued
until the landmark was returned to the bee's actual nest, after which it no
longer emerged. These two experiments show that Megalopta are capable
of using visually learned landmarks at night to find their way home, an
ability that nocturnal carpenter bees also share
(Somanathan et al., 2008).
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Just like their diurnal relatives (reviewed in
Collett et al., 2003),
nocturnal bees and wasps probably also have the ability to learn visual
landmarks along the foraging route. One possible system of landmarks is the
characteristic pattern of bright patches of sky visible through the canopy.
For a human observer standing in a dark rainforest at night this is the only
visible landmark! Its complexity – due to the overlapping silhouettes of
tens of thousands of small leaves and branches – is, however,
overwhelming, and it is difficult for a human observer to see any order or
pattern. However, if seen through the poor spatial resolution of an ocellus or
compound eye, this complexity disappears and the pattern becomes much more
obvious (H. Malm and E.J.W., in preparation). If, in addition, the pattern is
sufficiently different at different places in the rainforest, this would allow
its use as a landmark for an insect flying or walking beneath it. Indeed, it
has been found that both nocturnal
(Hölldobler and Taylor,
1983; Klotz and Reid,
1993; Taylor,
2007) and diurnal
(Hölldobler, 1980) ants
navigate to and from their nests using the rainforest canopy pattern as a
visual landmark.
The canopy patches also contain a second possible navigational cue –
polarised skylight, either due to the setting sun, or formed around the moon,
a cue used by other crepuscular and nocturnal insects for navigation
(Dacke et al., 2003a;
Dacke et al., 2003b;
Dacke et al., 2004). During
the hour directly after sunset or before sunrise, the sun's pattern of
skylight polarisation is very simple, with the dominant direction of
polarisation identical in all parts of the sky, and oriented roughly
north–south (Cronin et al.,
2006). The degree of polarisation is also very high
(Cronin et al., 2006). Thus,
in addition to its characteristic pattern, the patches of sky visible through
the canopy after dusk and before dawn are each rich in a single direction of
highly aligned polarised light. The two cues together – a spatial
pattern of canopy landmarks and a single directional compass cue defined by
the plane of polarised skylight – might be sufficient to allow homing in
nocturnal bees and wasps. This would require that the ocelli and/or the
compound eyes are sensitive to polarised light. The dorsal areas of compound
eyes in many insects have long been known to contain photoreceptors sensitive
to polarised light (Wehner and Labhart,
2006). Megalopta also has such a `dorsal rim' area, and
the ommatidia located there have enormous rhabdoms with photoreceptors that
are highly sensitive to polarised light (Greiner et al., 2007a).
Nocturnal flight performance
Foraging on foot at night, as many nocturnal ants do (e.g.
Klotz and Reid, 1993;
Greiner et al., 2007b), while
demanding, is nonetheless made easier by several sensory cues: olfactory,
mechanosensory and visual cues all cooperate to guide ground-based nocturnal
navigation (Klotz and Reid,
1993). A walking nocturnal insect can make use of navigational
guides provided by topographical landmarks in the substrate, or by scent
trails left there by conspecifics, whereas nocturnal flying insects rarely
experience such cues. Instead, they tend to rely on visual cues, a
considerable challenge in dim light. How well, then, do nocturnal bees and
wasps fly?
In the only study of nocturnal flight performance in insects
(Theobald et al., 2007), the
nocturnal bee Megalopta was filmed returning to the nest at different
times relative to sunrise or sunset (and thus at different light intensities).
Several interesting things were discovered. Firstly, bees always flew quickly,
irrespective of the level of illumination. This is surprising because one
might have suspected that as light levels fell, failing visual reliability and
longer visual integration times may have demanded slower flight [as seen in
honeybees (Menzel, 1981;
Rose and Menzel, 1981)]. This,
however, is apparently not the case. Secondly, at brighter light levels,
Megalopta was typically found to return to the nest and to enter it
quickly and confidently (Fig.
5B,C) whereas at dimmer light levels, returns were usually found
to be more circuitous (thus taking longer) and less confident, often involving
several aborted landing attempts (Fig.
5A,D). Thus, decreasing light level does indeed seem to worsen
flight performance and landing success, but remarkably at all intensities,
even at the dimmest, there were exceptions: some bees flew quickly and
confidently into the nest without hesitation. These exceptional individuals
may, by chance, have succeeded in landing on their first attempt.
Alternatively, these bees may have reliably detected large-scale landmarks,
such as the canopy pattern or larger (or closer) bushes and trees,
successfully relaying the sequence of retinal images required to match the
stored memory `snap-shots' that allow the bee to accurately home in on the
otherwise invisible nest entrance
(Cartwright and Collett, 1983;
Stürzl and Zeil, 2007).
Thus, even though light level clearly affects flight performance, bees are
capable of accurate visual navigation at all light levels within their normal
range. Interestingly, an analogous situation has also been found in
bumblebees: at lower light levels bumblebees spend more time visually
searching for flowers than at higher light levels
(Skorupski et al., 2006).
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Visual adaptations for reliable nocturnal vision
Our discussions above clearly indicate that nocturnal bees and wasps are
able to see well in very dim light. What visual adaptations have allowed this?
Part of the answer is embodied in the optical sensitivity (S) of an
eye to an extended source of broad-spectrum light. S, expressed in
units of µm2 sr, is given by
(Kirschfeld, 1974;
Land, 1981;
Warrant and Nilsson, 1998):
 | (1) |
A2/4) and photoreceptors that each view a
large solid angle of visual space
(d2/4f2 sr) and absorb a
substantial fraction of the incident light [kl/(2.3+kl)].
The apposition eyes of nocturnal bees and wasps show all three trends.
Moreover, recent work has shown that even their photoreceptors have special
neural adaptations for life in dim light.
Optical adaptations in the compound eyes and ocelli
To see how nocturnal life has affected the optical structure, and
sensitivity, of the apposition eyes and ocelli of bees and wasps, we can
compare nocturnal and diurnal species. For instance, the nocturnal sweat bee
Megalopta has larger eyes and larger facets (diameters up to 36
µm) than the strictly day-active European honeybee Apis mellifera
(diameters up to 20 µm). Moreover, in Apis the rhabdoms have a
width of only 2 µm, whereas in Megalopta they reach an
extraordinary 8 µm, resulting in a receptive field of more than 7 times
greater solid angular extent (Greiner et
al., 2004a; Warrant et al.,
2004). Similar differences are also seen in the ocelli: nocturnal
bees and wasps have much larger ocellar lenses and rhabdoms than their diurnal
relatives (Warrant et al.,
2006). In the compound eyes, these differences in receptive field
and facet size allow Megalopta an optical sensitivity that is roughly
27 times greater than in Apis: 2.7 µm2 sr
versus 0.1 µm2 sr. Similar differences in sensitivity
can be seen in the apposition eyes of nocturnal and diurnal carpenter bees (H.
Somanathan, R. M. Borges, A. Kelber and E.J.W., in preparation), wasps
(Greiner, 2006) and ants
(Menzi, 1987;
Moser et al., 2004;
Greiner et al., 2007b). Even
though nocturnal species experience a significant improvement in optical
sensitivity over diurnal species, it is still very modest compared with that
found in a typical superposition eye, such as those of the nocturnal moth
Deilephila elphenor (S=69 µm2 sr). This shows
up the inherent limitations of the apposition design for vision in dim light,
and begs the question – how can nocturnal bees and wasps nonetheless
navigate using landmarks at night? Part of the answer lies in the properties
of the photoreceptors, the topic to which we turn next.
Neural adaptations in the photoreceptors
Slowly flying nocturnal crane flies
(Laughlin and Weckström,
1993), and slowly walking nocturnal ants
(de Souza and Ventura, 1989),
tend to have slow vision, with photoreceptors having long integration times
compared with the photoreceptors of faster moving and distantly related
species active in bright light. These studies conclude that the slow vision of
the nocturnal species might be correlated with a slower locomotory speed, or a
dimmer habitat, or both.
What is the situation in fast-flying nocturnal bees? Do their
photoreceptors reveal properties that are uniquely suited to a life in dim
light? This question was investigated by intracellularly recording the
responses of photoreceptors to Gaussian-distributed white-noise light stimuli
in closely related nocturnal and diurnal sweat bees: the nocturnal
Megalopta genalis and the diurnal Lasioglossum leucozonium
(Frederiksen et al., 2008).
Two important differences in photoreceptor performance were found between
these two species, each of which highlights an adaptation for vision in dim
light.
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;
Laughlin and Weckström,
1993; Heimonen et al.,
2006; Pirhofer-Walzl et al.,
2007)] indicate that the photoreceptor's gain of transduction is
greater in Megalopta than in Lasioglossum. This higher
transduction gain manifests itself as a higher contrast gain; that is, in a
greater photoreceptor voltage response per unit change in light intensity (or
contrast). Contrast gain is plotted as a function of temporal frequency in
Fig. 6C–F: at all levels
of light and dark adaptation, for the frequency range both species can
discriminate, the visual gain of Meglopta is always higher than that
of Lasioglossum, and at the lowest intensities
(Fig. 6E,F) is up to five times
higher. This higher gain results in greater signal amplification.
Unfortunately, it also amplifies the noise, and thus on its own, the higher
gain does not alter the visual signal-to-noise ratio. However, because the
noise (including photon shot noise, the noise associated with the random
nature of photon absorption in the retina) is uncorrelated between different
photoreceptors and ommatidia, a subsequent spatial summation – as we
propose for nocturnal bees (see below) – has the potential to average
out the noise and amplify the signal even further, thereby greatly improving
the visual signal-to-noise ratio. Thus, a high visual gain, followed by
spatial summation, could represent a significant strategy for vision in dim
light.
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). In diurnal Lasioglossum, the dark-adapted corner
frequency is nearly three times the value found in Megalopta, at
around 20 Hz (Fig. 6F), a value
that is nonetheless considerably less than that typical of the diurnal, highly
manoeuvrable and rapidly flying higher flies [50–107 Hz
(Laughlin and Weckström,
1993)]. Since the two bees fly at similar speeds, their difference
in temporal properties – most probably due to different photoreceptor
sizes, and different numbers and types of ion channel in the photoreceptor
membrane (Laughlin, 1996)
– can only be related to the difference in light intensity experienced
by the two species. The nocturnal Megalopta has clearly evolved
slower vision, and this must be beneficial at night. Indeed, van Hateren
(van Hateren, 1993) has
convincingly shown that slower vision in dim light – despite
compromising temporal resolution – is beneficial because it increases
the visual signal-to-noise ratio and improves contrast discrimination at lower
temporal frequencies by suppressing photon noise at frequencies that are too
high to be reliably resolved. Despite comprising temporal resolution, this
low-pass filtering (which is evident in
Fig. 6C–F), improves
visual reliability in dim light. However, the narrower bandwidth possessed by
nocturnal Megalopta (Fig.
6C–F) has a devastating effect on the visual information
rate (calculated in bitss–1): at all intensities, the
intrinsic rate of visual information in the photoreceptors of
Lasioglossum is significantly greater than in those of
Megalopta (Fig. 7A).
It is only when the approximately 27 times greater optical sensitivity of the
apposition eyes of Megalopta is accounted for
(Fig. 7B) that the rate of
information transmission in Megalopta is greater than that in
Lasioglossum, but then only at the very lowest intensities.
Information, it seems, has been sacrificed in Megalopta for a greater
absolute sensitivity. Again, this sacrifice only makes sense in the light of a
subsequent strategy of spatial summation, the topic to which we turn next.
Spatial and temporal summation
As we saw above, the apposition eyes of nocturnal bees and wasps are not
especially sensitive to light. Even if the eyes of nocturnal species have 10
to 50 times the optical sensitivity of those in diurnal species
(Eqn 1), this may still not be
enough to guarantee reliable vision. There is, however, an additional
strategy, thought to reside in the neural circuits processing the incoming
visual signal, which can potentially solve the problem: the neural summation
of light in space and time (Snyder,
1977; Snyder et al.,
1977a; Snyder et al.,
1977b; Laughlin,
1981; Laughlin,
1990; Warrant,
1999). We have already discussed summation in time above: when
light gets dim, the visual systems of nocturnal animals can improve visual
reliability by integrating signals over longer periods of time
(Laughlin, 1990;
van Hateren, 1993). In the
eye, this can be achieved by having slower photoreceptors. Even slower vision
could be obtained by neurally integrating (summing) signals at a higher level
in the visual system. This temporal summation only comes at a price: it can
drastically degrade the perception of fast-moving objects, potentially
disastrous for a fast-flying nocturnal animal (like a nocturnal wasp or bee)
that needs to negotiate obstacles. Not surprisingly, temporal summation is
more likely to be employed by slowly moving animals.
Summation of photons in space can also improve image quality. Instead of each visual channel collecting photons in isolation (as in bright light), the transition to dim light could activate specialised laterally spreading neurons that couple the channels together into groups. Each summed group – themselves now defining the channels – could collect considerably more photons over a much wider visual angle, albeit with a simultaneous and unavoidable loss of spatial resolution. Despite being much brighter, the image would become necessarily coarser.
Evidence for laterally spreading neurons has been found in the first optic
ganglion (lamina ganglionaris) of nocturnal cockroaches
(Ribi, 1977), fireflies
(Ohly, 1975) and hawkmoths
(Strausfeld and Blest, 1970),
and these have been interpreted as an adaptation for spatial summation
(Laughlin, 1981). The
nocturnal bee Megalopta genalis also appears to have such neurons
(Greiner et al., 2004b;
Greiner et al., 2005)
(Fig. 8A). The wide lateral
branches of its laminar monopolar cells L2, L3 and L4, which spread to 12, 11
and 17 lamina cartridges, respectively, are considerably wider than the
homologous cells of Apis, which spread to 2, 0 and 4 cartridges,
respectively (Ribi, 1981;
Greiner et al., 2004b;
Greiner et al., 2005)
(Fig. 8A).
Even though their role in summation is yet to be shown, the morphologies of
these cells in Megalopta are well suited to the task of summation. If
one investigates the possible improvement afforded by optimal spatial and
temporal summation using theoretical methods
(Warrant, 1999), then both
Megalopta (Fig. 8B)
and Apis (Fig. 8C) are
able to resolve spatial details in a scene at much lower intensities with
summation than without it (Theobald et
al., 2006). These theoretical results assume that both bees
experience a rotational velocity during flight of 240°
s–1, a value that has been measured from high-speed films of
Megalopta fixating the nest entrance during orientation flights at
night. At the lower light levels where Megalopta is active, the
optimum visual performance shown in Fig.
8B is achieved with an integration time of about 30 ms and
summation from about 12 ommatidia (or cartridges). This integration time is
close to the photoreceptor's dark-adapted integration time
(Warrant et al., 2004), and
the extent of predicted spatial summation is very similar to the number of
cartridges to which the L2 and L3 cells branch
(Greiner et al., 2004b), thus
strengthening the hypothesis that the lamina monopolar cells are involved in
spatial summation.
Even in the honeybee Apis, summation can improve vision in dim
light (Fig. 8C). As we
mentioned above, the Africanised race, Apis mellifera scutellata, and
the closely related south-east Asian giant honeybee Apis dorsata,
both forage during dusk and dawn, and even throughout the night, if a moon
half-full or larger is present in the sky. Behavioural experiments show,
however, that even the strictly day-active European honeybee is capable of
seeing course habitat features, like large pale flowers, at moonlight
intensities. This ability can be explained only if bees optimally sum photons
over space and time (Warrant et al.,
1996), and this is also revealed in
Fig. 8C (for an angular
velocity of 240° s–1). At the lower light levels where
Apis is active, the optimum visual performance shown in
Fig. 8C is achieved with an
integration time of about 18 ms and summation from about three or four
cartridges. As in Megalopta, this integration time is close to the
photoreceptor's dark-adapted value
(Warrant et al., 2004), and
the extent of predicted spatial summation is again very similar to the number
of cartridges to which the Apis L2 and L3 cells actually branch.
In addition to simply capturing more light, spatial summation in nocturnal bees is ideally suited to take advantage of the special signal characteristics of the photoreceptors. As we mentioned above, the high voltage gain present in the photoreceptors amplifies both the signal and the noise. Because the noise is uncorrelated across ommatidia, spatial summation could effectively average out the noise, and dramatically increase the visual signal-to-noise ratio in dim light, albeit for a lower range of spatial frequencies. Whether the cellular circuits of the nocturnal bee lamina actually perform this task remains to be seen.
Finally, it must be pointed out that all of these nocturnal visual
investments – larger eyes, more numerous ommatidia, larger corneal
lenses, wider rhabdoms and more extensively branching lamina monopolar cells
– are unavoidably costly, in terms of both the extra weight (payload)
that must be carried during flight, and the extra energy (measured in terms of
ATP molecules consumed) that is required to power (and maintain) an improved
nocturnal visual capacity (Laughlin et
al., 1998; Laughlin,
2001; Niven et al.,
2007). Even though the cost per bit of nocturnal visual
information remains to be determined, it is likely to be high, and almost
certainly higher than the equivalent cost of diurnal visual information. This
greater cost – like the significant visual investments described in this
review – all indicate that for bees and wasps, and certainly for many
other nocturnal animals, the evolutionary benefits associated with seeing well
at night are significant indeed.
Conclusions
Despite their tiny and relatively insensitive apposition eyes, several groups of bees and wasps have successfully conquered the nocturnal niche, and taken advantage of the benefits that this niche provides for foraging and the avoidance of enemies. Like their diurnal relatives, these insects successfully learn visual landmarks and use them for homing, a feat that requires reliable vision in dim light. This reliability is the result of the combined action of a variety of adaptations within the eyes, and also most probably in the optic lobes, particularly in the lamina. Greatly enlarged corneal facets and rhabdoms, and slow photoreceptors with high contrast gain, ensure that visual signal strength is maximal as it leaves the eye and travels to the lamina. Even though it remains to be shown conclusively, anatomical and theoretical evidence suggests that once the visual signals from large groups of ommatidia reach the lamina, they are spatially summed by the second-order monopolar cells, resulting in an enhanced signal and reduced noise. The greatly improved signal-to-noise ratio that this strategy could afford, whilst confined to a narrower range of spatial and temporal frequencies, would ensure that nocturnal visual reliability is maximised for the slower and coarser features of the world. Those features that are faster and finer – and inherently noisy – would be filtered out. However, for a nocturnal bee or wasp struggling to find its way home in the dark, the ability to see a slow and coarse world, rather than nothing at all, would probably mean the difference between a successful return to the nest and becoming hopelessly lost.
Acknowledgments
I wish to thank Dan-Eric Nilsson, Almut Kelber, Michael Pfaff, Jamie Theobald, Gillian Little and Daniel Marlos for graciously allowing me to reproduce their figures and images in this review. I am also extremely grateful for the ongoing support of the Swedish Research Council (Vetenskapsrådet) and the Royal Physiographic Society of Lund.
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max) is plotted as a function of
light intensity. When bees sum photons optimally in space and time (continuous
lines), vision is extended to much lower light intensities (non-zero