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LOW LIGHT, BAD FLIGHT
VISION AND VISUAL NAVIGATION IN
NOCTURNAL INSECTS
Prashant
PAL 0013
2
Compound eyes:
Insects recognize and react to conspecifics
 Distinguish and avoid predators
 Locate food sources and intercept prey
 Navigate
 Walk, swim or fly
Nocturnal insects:
Introduction
Light levels can be up to 11 orders of magnitude lower
3
 Behavioral modifications
 Visual system itself
How?
4
 Apposition compound eyes
Example: Nocturnal bees and
wasps
Nocturnal compound eyes
 High optical sensitivity- Superposition
compound eyes
Example: Nocturnal moths and beetles
5
Ommatidia
Hexagonal Circular Dome
Three basic models of the compound eye
6
Difference
Visual processing in nocturnal
insects
Vision
Eyes with an enhanced optical sensitivity to light
Visual neurons that sacrifice spatial and temporal resolution
to improve visual reliability for the slower and coarser
features of the world
EYES AND VISION IN NOCTURNAL INSECTS
Optics
Retina of the compound eye
8
A superposition eye can have
optical sensitivity 100–1000 times
higher than that of an apposition
compound eye
The Optical Designs of Nocturnal Compound Eyes
A
9
The ratio of the number of photons absorbed by a photoreceptor
to the number emitted per steradian of solid angle from a unit
area of an extended source
Where,
A-Diameter of eye operture
l - length of the rhabdom
K -peak absorption coefficient
of the visual pigment
 f -focal length of the
ommatidium
 d -diameter of the rhabdom.
Optical sensitivity
10
Good sensitivity to a spatially extended scene results from
a pupil of large area (π A2/4)
Photoreceptors that each view a large solid angle of visual
space (πd2/4 f 2 steradians)
Absorb a substantial fraction of the incident light (kl/2.3+kl).
This equation predicts
11
M. genalisA. mellifera
2 μm 8 μmRhabdum width
Facet size 36 μm20 μm
M. genalis an optical sensitivity that is roughly 27 times
greater than that of A. mellifera
Warrant et al., 2004
How nocturnal life has affected the optical structure
and sensitivity?
12
Warrant et al., 2006
Ocellar optics in nocturnal and diurnal bees and wasps
Nocturnal sweat bee, Megalopta genalis,
Nocturnal paper wasp, Apoica pallens
Diurnal paper wasp, Polistes occidentalis
13
Megalopta genalis Augochloropsis fuscognatha 14
Apoica pallens Polistes occidentalis15
Longitudinal light microscope sections of median ocelli
Apoica pallens (A), Megalopta genalis (B),
Polistes occidentalis(C)
l=lens
r=retina
p=screening
pigment
granules
16
Polistes occidentalis (C).
Megalopta genalis (A)
Apoica pallens (B)
The optical properties of median ocelli
17
General property of photoreceptors- Bumps
At higher intensities: the bump responses fuse to create a
graded response whose duration and amplitude are
proportional to the duration and amplitude of the light
stimulus
Photoreception and the Reliability of
Vision in Dim Light
18
At very low light levels: a light stimulus of constant intensity is
coded as a train of bumps
At somewhat higher light levels: the constant intensity is coded
by a graded potential of particular amplitude 19
 The major limitation for nocturnal vision in insects
 Arises from the stochastic nature of photon arrival and
absorption
Sources of Visual noise
 Photon shot noise
 Dark noise
 Transducer noise
Visual noise
20
• Photoreceptor absorbing a number of N photons
experiences an uncertainty (or photon shot noise) of √N
photons
(Land, 1981; Warrant and McIntyre, 1993)
• Decreasing photon catch in dim light results in an
increasing noise level
• As two visual channels need to detect sufficient photons in
order to reduce this noise level
PHOTON SHOT NOISE
21
 Consists of spontaneous thermal responses in the
absence of photons, which are indistinguishable from
membrane potentials (quantum bumps) produced by photons
(Barlow, 1956)
 These fluctuations are more frequent at higher
temperatures and introduce uncertainty at low light
intensities.
Even though dark noise is much lower in invertebrates than
in vertebrates
Dark noise
22
Photoreceptors are incapable of producing identical bumps
of fixed amplitude, latency and duration to each (identical)
photon of absorbed light.
This source of noise, originating in the biochemical
processes leading to signal amplification
To maximise the photon catch or signal-to-noise ratio to
enhance sensitivity
Transducer noise
23
 Photoreceptor responses to single photons (i.e bumps)
are much larger in nocturnal insects
Retinal adaptations for nocturnal
vision
Large bumps have been demonstrated
Nocturnal crane flies
Cockroaches
Bees
Spiders
24
Quantum bumps of nocturnal M. genalis and diurnal L.
leucozonium 25
Contrast gain of the bees M. genalis and L. leucozonium
Fredriksen et al., 200826
 A large number of animals are known to use colour to
detect, discriminate and recognise objects
 Food sources
 Mating partners
 Landmarks or their homes
Nocturnal Color Vision
An animal needs to possess and use at least two types of photoreceptors,
with different spectral sensitivities, to look at an object
27
Simple 4-stage model of colour discrimination with two
spectral types of receptors.
28
Natural light levels and limits of colour vision 29
 UV
 Violet
 Green
Kelber, 2003
Deilephila elpenorMacroglossum stellatarum
Colour Vision in Diurnal and
Nocturnal Hawkmoths
Three different spectral classes of photoreceptors
30
Schematic drawings of the structure of the rhabdom of
Deilephila elpenor
Schlecht et al., 1978
31
Color vision in D. elpenor is color-constant
 This moth can not only be trained to associate a sugar
reward with a blue disc at starlight
 Discriminate this blue disk from other discs in various
shades of gray with a choice frequency of at least 80%.
Kelber, 2003
32
Colour vision in Deilephila elpenor
Kelber et al., 2002
33
Colour constancy 34
 Many nocturnal insects have evolved sufficiently
sensitive visual systems
Celestial cues
Terrestrial visual Cues
Nocturnal Navigation and
Orientation
35
At night, the brightest and most easily discernable cue in
the sky is undoubtedly the moon
Navigation and orientation using
celestial cues
Its bright disk is used for orientation and navigation in a number of
different nocturnal insects
Ants Earwigs
Moths
Beetles
36
 A much dimmer and more subtle cue associated with the
moon is its pattern of polarized light.
 This circular pattern, centered around the moon, arises
because of the atmospheric scattering of moonlight as it
travels toward Earth
 Light is most polarized around a circular celestial locus
90◦ from the moon, and the circular pattern of polarized
light moves with the moon
Cont….
37
 On full moon nights
 On four nights before and after this event
Dacke et al., 2003
Lunar orientation in a beetle
38
The path taken by a ball-rolling Scarabaeus zambesianus
0 to 90 90 or 180
39
Circular diagrams of turns made by Scarabaeus zambesianus
rolling under the night sky.
40
 Visual detection of optic flow is also clearly necessary for
controlling nocturnal flight
Navigation and orientation using
terrestrial cues
 Dim light gypsy moths
 Mosquitoes
 Locust
41
Landmark orientation in sweat bee
Warrant et al., 2004 42
 X. leucothorax is diurnal
 X. tenuiscapa is largely diurnal and
occasionally crepuscular
 X. tranquebarica is truly nocturnal
Somanathan et al., 2008
Flight activity in three species of carpenter bees
in relation to light intensities
43
Somanathan et al., 2008
Flight activity in all three species as a function of light
intensity
44
Two-dimensional reconstruction of flight paths of X. tranquebarica
at a nest site 45
X. leucothorax X. tenuiscapa
X. tranquebarica
46
Scanning electron micrograph of heads
Canopy or Individual trees
As the animal moves under the tree canopy, the brighter
sky in the gaps of the canopy, together with the darker
area under the canopy
Ex: Nocturnal shield bug, Parastrachia japonensis
Insects living in forests
47
Schematic drawing of the displacement test
48
A nocturnal provisioning path and the distribution of foraging
and homing directions 49
Homing path and distribution of homing directions in a
nocturnal displacement test 50
Nocturnal homing using canopy cues in the shield bug
Parastrachia japonensis
Hironaka et al., 2008
51
Reid et al., 2011
Myrmecia pyriformis Smith
Landmark panorama provide night-active bull
ants with compass information during route
following
52
Landmark-blocking experiment
53
A) initial orientation of individual ants at the nest the
B) time taken to exit the 30cm circle and
C) the proportion that crossed the 1.2m reference line 54
Displacement experiment. 55
Neural adaptations
 An increase in the response gain of the
photoreceptors with decreasing light intensity can
further enhance sensitivity but does not improve
photon capture itself
(Laughlin, 1981)
 The ultimate solution to optimise sensitivity at
low light intensities is to process the incoming
visual signal using a strategy of neural summation
in space and time
56
Temporal Summation
 Visual systems can also improve image reliability
at night by slowing vision down
 Lengthening the eye’s visual integration time at
night
 Signal-to-noise ratio of lower temporal
frequencies is improved
57
 Temporal summation results in a slower but more reliable
visual world
 Extremely long photoreceptor integration times
 Sit-and-wait predators and slowly moving animals,
temporal summation is certainly a good strategy
Cont…
58
Theory of spatial summation
Spatial Summation
59
 Photons are integrated over wider visual fields,
which is similar to a widening of the angular
sensitivity function
 Only when neural summation is matched to the
extent of the visual overlap present in the eye
60
Warrant, 2004
A Possible Mechanism for Spatial Summation in Megalopta’s Eye
61
Greiner et al., 2004 and Ribi, 1975
Comparison of the First-Order Interneurons, L-fiber types L3
and L4, of the M. genalis female (left) and the worker
honeybee A. mellifera (right)
62
 Nocturnal insects have excellent night vision
 With the capacity to discriminate colors
 Orient themselves using faint celestial cues fly unimpeded
through a complicated habitat
 Navigate to and from a nest using learned visual
landmarks
Conclusion
63
 The photoreceptors of nocturnal insects respond more
slowly and have a higher contrast gain
 A neural strategy of spatial and temporal summation at a
higher level in the visual system is hypothesized as the
necessary bridge between retinal signaling and
visual behavior.
Cont…
64
65
66

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Vision and visual navigation in nocturnal insects

  • 1. 1
  • 2. LOW LIGHT, BAD FLIGHT VISION AND VISUAL NAVIGATION IN NOCTURNAL INSECTS Prashant PAL 0013 2
  • 3. Compound eyes: Insects recognize and react to conspecifics  Distinguish and avoid predators  Locate food sources and intercept prey  Navigate  Walk, swim or fly Nocturnal insects: Introduction Light levels can be up to 11 orders of magnitude lower 3
  • 4.  Behavioral modifications  Visual system itself How? 4
  • 5.  Apposition compound eyes Example: Nocturnal bees and wasps Nocturnal compound eyes  High optical sensitivity- Superposition compound eyes Example: Nocturnal moths and beetles 5
  • 6. Ommatidia Hexagonal Circular Dome Three basic models of the compound eye 6
  • 8. Visual processing in nocturnal insects Vision Eyes with an enhanced optical sensitivity to light Visual neurons that sacrifice spatial and temporal resolution to improve visual reliability for the slower and coarser features of the world EYES AND VISION IN NOCTURNAL INSECTS Optics Retina of the compound eye 8
  • 9. A superposition eye can have optical sensitivity 100–1000 times higher than that of an apposition compound eye The Optical Designs of Nocturnal Compound Eyes A 9
  • 10. The ratio of the number of photons absorbed by a photoreceptor to the number emitted per steradian of solid angle from a unit area of an extended source Where, A-Diameter of eye operture l - length of the rhabdom K -peak absorption coefficient of the visual pigment  f -focal length of the ommatidium  d -diameter of the rhabdom. Optical sensitivity 10
  • 11. Good sensitivity to a spatially extended scene results from a pupil of large area (π A2/4) Photoreceptors that each view a large solid angle of visual space (πd2/4 f 2 steradians) Absorb a substantial fraction of the incident light (kl/2.3+kl). This equation predicts 11
  • 12. M. genalisA. mellifera 2 μm 8 μmRhabdum width Facet size 36 μm20 μm M. genalis an optical sensitivity that is roughly 27 times greater than that of A. mellifera Warrant et al., 2004 How nocturnal life has affected the optical structure and sensitivity? 12
  • 13. Warrant et al., 2006 Ocellar optics in nocturnal and diurnal bees and wasps Nocturnal sweat bee, Megalopta genalis, Nocturnal paper wasp, Apoica pallens Diurnal paper wasp, Polistes occidentalis 13
  • 15. Apoica pallens Polistes occidentalis15
  • 16. Longitudinal light microscope sections of median ocelli Apoica pallens (A), Megalopta genalis (B), Polistes occidentalis(C) l=lens r=retina p=screening pigment granules 16
  • 17. Polistes occidentalis (C). Megalopta genalis (A) Apoica pallens (B) The optical properties of median ocelli 17
  • 18. General property of photoreceptors- Bumps At higher intensities: the bump responses fuse to create a graded response whose duration and amplitude are proportional to the duration and amplitude of the light stimulus Photoreception and the Reliability of Vision in Dim Light 18
  • 19. At very low light levels: a light stimulus of constant intensity is coded as a train of bumps At somewhat higher light levels: the constant intensity is coded by a graded potential of particular amplitude 19
  • 20.  The major limitation for nocturnal vision in insects  Arises from the stochastic nature of photon arrival and absorption Sources of Visual noise  Photon shot noise  Dark noise  Transducer noise Visual noise 20
  • 21. • Photoreceptor absorbing a number of N photons experiences an uncertainty (or photon shot noise) of √N photons (Land, 1981; Warrant and McIntyre, 1993) • Decreasing photon catch in dim light results in an increasing noise level • As two visual channels need to detect sufficient photons in order to reduce this noise level PHOTON SHOT NOISE 21
  • 22.  Consists of spontaneous thermal responses in the absence of photons, which are indistinguishable from membrane potentials (quantum bumps) produced by photons (Barlow, 1956)  These fluctuations are more frequent at higher temperatures and introduce uncertainty at low light intensities. Even though dark noise is much lower in invertebrates than in vertebrates Dark noise 22
  • 23. Photoreceptors are incapable of producing identical bumps of fixed amplitude, latency and duration to each (identical) photon of absorbed light. This source of noise, originating in the biochemical processes leading to signal amplification To maximise the photon catch or signal-to-noise ratio to enhance sensitivity Transducer noise 23
  • 24.  Photoreceptor responses to single photons (i.e bumps) are much larger in nocturnal insects Retinal adaptations for nocturnal vision Large bumps have been demonstrated Nocturnal crane flies Cockroaches Bees Spiders 24
  • 25. Quantum bumps of nocturnal M. genalis and diurnal L. leucozonium 25
  • 26. Contrast gain of the bees M. genalis and L. leucozonium Fredriksen et al., 200826
  • 27.  A large number of animals are known to use colour to detect, discriminate and recognise objects  Food sources  Mating partners  Landmarks or their homes Nocturnal Color Vision An animal needs to possess and use at least two types of photoreceptors, with different spectral sensitivities, to look at an object 27
  • 28. Simple 4-stage model of colour discrimination with two spectral types of receptors. 28
  • 29. Natural light levels and limits of colour vision 29
  • 30.  UV  Violet  Green Kelber, 2003 Deilephila elpenorMacroglossum stellatarum Colour Vision in Diurnal and Nocturnal Hawkmoths Three different spectral classes of photoreceptors 30
  • 31. Schematic drawings of the structure of the rhabdom of Deilephila elpenor Schlecht et al., 1978 31
  • 32. Color vision in D. elpenor is color-constant  This moth can not only be trained to associate a sugar reward with a blue disc at starlight  Discriminate this blue disk from other discs in various shades of gray with a choice frequency of at least 80%. Kelber, 2003 32
  • 33. Colour vision in Deilephila elpenor Kelber et al., 2002 33
  • 35.  Many nocturnal insects have evolved sufficiently sensitive visual systems Celestial cues Terrestrial visual Cues Nocturnal Navigation and Orientation 35
  • 36. At night, the brightest and most easily discernable cue in the sky is undoubtedly the moon Navigation and orientation using celestial cues Its bright disk is used for orientation and navigation in a number of different nocturnal insects Ants Earwigs Moths Beetles 36
  • 37.  A much dimmer and more subtle cue associated with the moon is its pattern of polarized light.  This circular pattern, centered around the moon, arises because of the atmospheric scattering of moonlight as it travels toward Earth  Light is most polarized around a circular celestial locus 90◦ from the moon, and the circular pattern of polarized light moves with the moon Cont…. 37
  • 38.  On full moon nights  On four nights before and after this event Dacke et al., 2003 Lunar orientation in a beetle 38
  • 39. The path taken by a ball-rolling Scarabaeus zambesianus 0 to 90 90 or 180 39
  • 40. Circular diagrams of turns made by Scarabaeus zambesianus rolling under the night sky. 40
  • 41.  Visual detection of optic flow is also clearly necessary for controlling nocturnal flight Navigation and orientation using terrestrial cues  Dim light gypsy moths  Mosquitoes  Locust 41
  • 42. Landmark orientation in sweat bee Warrant et al., 2004 42
  • 43.  X. leucothorax is diurnal  X. tenuiscapa is largely diurnal and occasionally crepuscular  X. tranquebarica is truly nocturnal Somanathan et al., 2008 Flight activity in three species of carpenter bees in relation to light intensities 43
  • 44. Somanathan et al., 2008 Flight activity in all three species as a function of light intensity 44
  • 45. Two-dimensional reconstruction of flight paths of X. tranquebarica at a nest site 45
  • 46. X. leucothorax X. tenuiscapa X. tranquebarica 46 Scanning electron micrograph of heads
  • 47. Canopy or Individual trees As the animal moves under the tree canopy, the brighter sky in the gaps of the canopy, together with the darker area under the canopy Ex: Nocturnal shield bug, Parastrachia japonensis Insects living in forests 47
  • 48. Schematic drawing of the displacement test 48
  • 49. A nocturnal provisioning path and the distribution of foraging and homing directions 49
  • 50. Homing path and distribution of homing directions in a nocturnal displacement test 50
  • 51. Nocturnal homing using canopy cues in the shield bug Parastrachia japonensis Hironaka et al., 2008 51
  • 52. Reid et al., 2011 Myrmecia pyriformis Smith Landmark panorama provide night-active bull ants with compass information during route following 52
  • 54. A) initial orientation of individual ants at the nest the B) time taken to exit the 30cm circle and C) the proportion that crossed the 1.2m reference line 54
  • 56. Neural adaptations  An increase in the response gain of the photoreceptors with decreasing light intensity can further enhance sensitivity but does not improve photon capture itself (Laughlin, 1981)  The ultimate solution to optimise sensitivity at low light intensities is to process the incoming visual signal using a strategy of neural summation in space and time 56
  • 57. Temporal Summation  Visual systems can also improve image reliability at night by slowing vision down  Lengthening the eye’s visual integration time at night  Signal-to-noise ratio of lower temporal frequencies is improved 57
  • 58.  Temporal summation results in a slower but more reliable visual world  Extremely long photoreceptor integration times  Sit-and-wait predators and slowly moving animals, temporal summation is certainly a good strategy Cont… 58
  • 59. Theory of spatial summation Spatial Summation 59
  • 60.  Photons are integrated over wider visual fields, which is similar to a widening of the angular sensitivity function  Only when neural summation is matched to the extent of the visual overlap present in the eye 60
  • 61. Warrant, 2004 A Possible Mechanism for Spatial Summation in Megalopta’s Eye 61
  • 62. Greiner et al., 2004 and Ribi, 1975 Comparison of the First-Order Interneurons, L-fiber types L3 and L4, of the M. genalis female (left) and the worker honeybee A. mellifera (right) 62
  • 63.  Nocturnal insects have excellent night vision  With the capacity to discriminate colors  Orient themselves using faint celestial cues fly unimpeded through a complicated habitat  Navigate to and from a nest using learned visual landmarks Conclusion 63
  • 64.  The photoreceptors of nocturnal insects respond more slowly and have a higher contrast gain  A neural strategy of spatial and temporal summation at a higher level in the visual system is hypothesized as the necessary bridge between retinal signaling and visual behavior. Cont… 64
  • 65. 65
  • 66. 66

Notas del editor

  1. The large rhabdoms of Megalopta are clearly an adaptation for improved sensitivity at night, and the interesting observation that the equally nocturnal Apoica has small rhabdoms suggests that some of their sensitivity may have been offered in favour of spatial resolution. This conclusion is reinforced by calculations of the occupation ratio of rhabdoms in the retina (the percentage cross-sectional area of rhabdoms within a unit cross-sectional area of retina). The occupation ratios of the wasps Apoica and Polistes are quite small (9.5% and 6.1%, respectively: Table 1). Even though Apoica is nocturnal, its rhabdom occupation ratio is only slightly larger than that of its diurnal relative. In contrast, the nocturnal bee Megalopta has a rhabdom occupation ratio over three times greater (33.6%: Table 1).
  2. At the level of the photoreceptors, the reliability of vision is determined by the repeatability of this response
  3. They were then displaced either 2m to the left or 2m to the right of the nest-to-tree line (R). Normal foraging paths are shown in grey, displaced paths are in black.