J Exp Biol Advance Online Articles. First posted online on 15 April 2014 as doi:10.1242/jeb.103457 Access the most recent version at http://jeb.biologists.org/lookup/doi/10.1242/jeb.103457
1
Null point of discrimination in crustacean polarisation vision
2
Martin J. How1,2,3, John Christy3, Nicholas W. Roberts1 and N. Justin Marshall2
3
1 – School of Biological Sciences, Woodland Road, University of Bristol, Bristol, BS8 1UG, UK
4
2 - Queensland Brain Institute, University of Queensland, St Lucia, QLD 4072, Australia
5
3 - Smithsonian Tropical Research Institute, Panama City, Republic of Panama
The Journal of Experimental Biology – ACCEPTED AUTHOR MANUSCRIPT
6 7 8
Abstract
9
The polarisation of light is used by many species of cephalopods and crustaceans to discriminate
10
objects or to communicate. Most visual systems with this ability, such as that of the fiddler crab,
11
include receptors with photopigments that are oriented horizontally and vertically relative to the
12
outside world. Photoreceptors in such an orthogonal array are maximally sensitive to polarised light
13
with the same fixed e-vector orientation. Using opponent neural connections, this two-channel
14
system may produce a single value of polarisation contrast and, consequently, it may suffer from
15
null points of discrimination. Stomatopod crustaceans use a different system for polarisation vision,
16
comprising at least four types of polarisation-sensitive photoreceptor arranged at 0°, 45°, 90° and
17
135° relative to each other, in conjunction with extensive rotational eye movements. This
18
anatomical arrangement should not suffer from equivalent null points of discrimination. To test
19
whether these two systems were vulnerable to null points, we presented the fiddler crab
20
heteropleura and the stomatopod Haptosquilla trispinosa with polarised looming stimuli on a
21
modified LCD monitor. The fiddler crab was less sensitive to differences in the degree of polarised
22
light when the e-vector was at -45°, than when the e-vector was horizontal. In comparison,
23
stomatopods showed no difference in sensitivity between the two stimulus types. The results
24
suggest that fiddler crabs suffer from a null point of sensitivity, while stomatopods do not.
25 26
Keywords: polarisation distance, fiddler crab, mantis shrimp, discrimination threshold
© 2013. Published by The Company of Biologists Ltd
Uca
The Journal of Experimental Biology – ACCEPTED AUTHOR MANUSCRIPT
27
Introduction
28
The polarisation of light provides an independent channel of visual information that some animals
29
use to discriminate objects or for communication (Shashar et al., 1998; Wehner and Labhart, 2006;
30
Glantz, 2007; Chiou et al., 2011; How et al., 2012; Temple et al., 2012; Marshall et al., 2014b). Visual
31
systems that detect and identify objects using polarised light rely on comparative processing of the
32
signals generated by polarisation-sensitive photoreceptors distributed across parts of the visual field.
33
This is a process somewhat analogous to colour vision and adds to the well-known uses of the
34
polarisation of light for navigation, orientation and habitat localisation (Wehner, 1976; Schwind,
35
1983; Labhart and Meyer, 1999). Animals may use this channel to improve the detection of objects
36
through veiling light or glare (Schechner and Karpel, 2005; Alkaladi et al., 2013), to enhance the
37
contrast of transparent prey (Shashar et al., 1998; Tuthill and Johnsen, 2006; but see Johnsen et al.,
38
2011), to break camouflage (Shashar et al., 2000; Jordan et al., 2012; Temple et al., 2012) or to allow
39
the detection of polarised body patterns for communication (Shashar et al., 1996; Marshall et al.,
40
1999).
41
Object-based polarisation vision systems that have so far been studied are restricted to
42
cephalopods and crustaceans. In these examples, the photoreceptors that act as polarised light
43
detectors in the eye are aligned horizontally and vertically (Tasaki and Karita, 1966; Shaw, 1969;
44
Waterman, 1981) forming two channels of polarisation sensitivity. Furthermore, these animals
45
maintain precise alignment of their eyes relative to the visual world around them (Zeil et al., 1986;
46
Talbot and Marshall, 2011), thus ensuring that the polarisation-sensitive receptors remain horizontal
47
and vertical relative to the visual scene. Stomatopods are an exception. These crustaceans possess
48
an anatomically complex array of polarisation receptors with e-vector sensitivities arranged at 0°,
49
45°, 90° and 135° relative to each other (Marshall et al., 1991; Kleinlogel et al., 2003). They also have
50
receptors in rows 5 and 6 of the mid-band of the eye that are sensitive to left and right-handed
51
circularly polarised light (Chiou et al., 2008; Roberts et al., 2009). In addition to this anatomical
52
complexity, these animals regularly rotate their eyes around the axis of view (Cronin et al., 1988;
53
Land et al., 1990), thereby altering the orientation of the polarisation detectors relative to the
54
outside world. Such a system is likely, therefore, to have very different properties from the more
55
common two-channel polarisation vision.
56
An understanding of the underlying anatomy of polarisation vision opens the possibility for
57
modelling an animal’s sensitivity to polarised light cues. One approach, inspired by analogous
58
systems in colour vision (Vorobyev and Osorio, 1998), is to simulate the proposed neural
59
architecture of early visual processing. For simple systems, two orthogonally oriented polarisation
60
channels are assumed to have opponent connections (similar to dichromatic colour vision models)
61
and produce a single level of neural activity (Bernard and Wehner, 1977). Subsequent comparison of
62
this activity between two different parts of the visual field (one viewing an object and one viewing
63
the background) results in a measure of polarisation contrast, termed ‘polarisation distance’(How
64
and Marshall, 2014). Presumably this output is modulated at some stage by intensity variations, so
65
that intensity signals and polarisation signals are fused into a single measure of contrast; however
66
this falls beyond the scope of the current paper. Such models allow us to predict how well animals
67
will perform in a discrimination task, assuming that they are using a given neurosensory apparatus.
The Journal of Experimental Biology – ACCEPTED AUTHOR MANUSCRIPT
68
Previous studies using this modelling approach identified the problem of potential ambiguities
69
and null points in two-channel polarisation vision systems (Bernard and Wehner, 1977; How and
70
Marshall, 2014). For example, polarised light cues with e-vector axes oriented at +45° or -45°
71
stimulate horizontal and vertical polarisation receptors equally, and so are indistinguishable from
72
each other and from unpolarised light of the same intensity. This is widely accepted as a problem for
73
two-channel polarisation vision, yet, with the exception of some associative learning experiments
74
with cephalopods (Moody and Parriss, 1961; Shashar and Cronin, 1996), this has not been
75
investigated in detail at the behavioural level. To this end, we used a modified liquid crystal display
76
(LCD) monitor (Glantz and Schroeter, 2006; Pignatelli et al., 2011; How et al., 2012; Temple et al.,
77
2012) to present polarised looming stimuli to the two-channel polarisation vision system of the
78
fiddler crab Uca heteropleura (Smith, 1870) and to the dynamic, multi-channelled polarisation vision
79
system of the stomatopod Haptosquilla trispinosa (Dana, 1852). These looming stimuli differed in
80
the degree of polarisation, while the overall light intensity remained constant. We compared the
81
response probability of these two species to stimuli that fell, either within, or outside a predicted
82
null point of discrimination for a two-channel polarisation vision system.
83 84
Results
85
Fiddler crabs U. heteropleura responded to polarised looming stimuli in a number of ways similar to
86
those reported for U. vomeris (How et al., 2012), including cessation of all movement (freeze),
87
drawing of the legs or claw closer to the body (tuck), a jerk or twitch, and a sprint. A small number
88
of crabs responded to the zero contrast stimulus (Fig. 1a, dotted line) as a result of coincidental
89
changes in behaviour during stimulus presentation. These therefore estimate the probability of false
90
positive responses during the experiment. A significant response was recorded for crabs viewing the
91
horizontally polarised stimuli down to differences in degree as low as 8% (linear mixed effects model
92
(lmer) for 8% stimulus vs. background: family binomial, number of crabs (n) = 22, df = 1, χ 2 = 18.7, p
1
Null point of discrimination in crustacean polarisation vision
2
Martin J. How1,2,3, John Christy3, Nicholas W. Roberts1 and N. Justin Marshall2
3
1 – School of Biological Sciences, Woodland Road, University of Bristol, Bristol, BS8 1UG, UK
4
2 - Queensland Brain Institute, University of Queensland, St Lucia, QLD 4072, Australia
5
3 - Smithsonian Tropical Research Institute, Panama City, Republic of Panama
The Journal of Experimental Biology – ACCEPTED AUTHOR MANUSCRIPT
6 7 8
Abstract
9
The polarisation of light is used by many species of cephalopods and crustaceans to discriminate
10
objects or to communicate. Most visual systems with this ability, such as that of the fiddler crab,
11
include receptors with photopigments that are oriented horizontally and vertically relative to the
12
outside world. Photoreceptors in such an orthogonal array are maximally sensitive to polarised light
13
with the same fixed e-vector orientation. Using opponent neural connections, this two-channel
14
system may produce a single value of polarisation contrast and, consequently, it may suffer from
15
null points of discrimination. Stomatopod crustaceans use a different system for polarisation vision,
16
comprising at least four types of polarisation-sensitive photoreceptor arranged at 0°, 45°, 90° and
17
135° relative to each other, in conjunction with extensive rotational eye movements. This
18
anatomical arrangement should not suffer from equivalent null points of discrimination. To test
19
whether these two systems were vulnerable to null points, we presented the fiddler crab
20
heteropleura and the stomatopod Haptosquilla trispinosa with polarised looming stimuli on a
21
modified LCD monitor. The fiddler crab was less sensitive to differences in the degree of polarised
22
light when the e-vector was at -45°, than when the e-vector was horizontal. In comparison,
23
stomatopods showed no difference in sensitivity between the two stimulus types. The results
24
suggest that fiddler crabs suffer from a null point of sensitivity, while stomatopods do not.
25 26
Keywords: polarisation distance, fiddler crab, mantis shrimp, discrimination threshold
© 2013. Published by The Company of Biologists Ltd
Uca
The Journal of Experimental Biology – ACCEPTED AUTHOR MANUSCRIPT
27
Introduction
28
The polarisation of light provides an independent channel of visual information that some animals
29
use to discriminate objects or for communication (Shashar et al., 1998; Wehner and Labhart, 2006;
30
Glantz, 2007; Chiou et al., 2011; How et al., 2012; Temple et al., 2012; Marshall et al., 2014b). Visual
31
systems that detect and identify objects using polarised light rely on comparative processing of the
32
signals generated by polarisation-sensitive photoreceptors distributed across parts of the visual field.
33
This is a process somewhat analogous to colour vision and adds to the well-known uses of the
34
polarisation of light for navigation, orientation and habitat localisation (Wehner, 1976; Schwind,
35
1983; Labhart and Meyer, 1999). Animals may use this channel to improve the detection of objects
36
through veiling light or glare (Schechner and Karpel, 2005; Alkaladi et al., 2013), to enhance the
37
contrast of transparent prey (Shashar et al., 1998; Tuthill and Johnsen, 2006; but see Johnsen et al.,
38
2011), to break camouflage (Shashar et al., 2000; Jordan et al., 2012; Temple et al., 2012) or to allow
39
the detection of polarised body patterns for communication (Shashar et al., 1996; Marshall et al.,
40
1999).
41
Object-based polarisation vision systems that have so far been studied are restricted to
42
cephalopods and crustaceans. In these examples, the photoreceptors that act as polarised light
43
detectors in the eye are aligned horizontally and vertically (Tasaki and Karita, 1966; Shaw, 1969;
44
Waterman, 1981) forming two channels of polarisation sensitivity. Furthermore, these animals
45
maintain precise alignment of their eyes relative to the visual world around them (Zeil et al., 1986;
46
Talbot and Marshall, 2011), thus ensuring that the polarisation-sensitive receptors remain horizontal
47
and vertical relative to the visual scene. Stomatopods are an exception. These crustaceans possess
48
an anatomically complex array of polarisation receptors with e-vector sensitivities arranged at 0°,
49
45°, 90° and 135° relative to each other (Marshall et al., 1991; Kleinlogel et al., 2003). They also have
50
receptors in rows 5 and 6 of the mid-band of the eye that are sensitive to left and right-handed
51
circularly polarised light (Chiou et al., 2008; Roberts et al., 2009). In addition to this anatomical
52
complexity, these animals regularly rotate their eyes around the axis of view (Cronin et al., 1988;
53
Land et al., 1990), thereby altering the orientation of the polarisation detectors relative to the
54
outside world. Such a system is likely, therefore, to have very different properties from the more
55
common two-channel polarisation vision.
56
An understanding of the underlying anatomy of polarisation vision opens the possibility for
57
modelling an animal’s sensitivity to polarised light cues. One approach, inspired by analogous
58
systems in colour vision (Vorobyev and Osorio, 1998), is to simulate the proposed neural
59
architecture of early visual processing. For simple systems, two orthogonally oriented polarisation
60
channels are assumed to have opponent connections (similar to dichromatic colour vision models)
61
and produce a single level of neural activity (Bernard and Wehner, 1977). Subsequent comparison of
62
this activity between two different parts of the visual field (one viewing an object and one viewing
63
the background) results in a measure of polarisation contrast, termed ‘polarisation distance’(How
64
and Marshall, 2014). Presumably this output is modulated at some stage by intensity variations, so
65
that intensity signals and polarisation signals are fused into a single measure of contrast; however
66
this falls beyond the scope of the current paper. Such models allow us to predict how well animals
67
will perform in a discrimination task, assuming that they are using a given neurosensory apparatus.
The Journal of Experimental Biology – ACCEPTED AUTHOR MANUSCRIPT
68
Previous studies using this modelling approach identified the problem of potential ambiguities
69
and null points in two-channel polarisation vision systems (Bernard and Wehner, 1977; How and
70
Marshall, 2014). For example, polarised light cues with e-vector axes oriented at +45° or -45°
71
stimulate horizontal and vertical polarisation receptors equally, and so are indistinguishable from
72
each other and from unpolarised light of the same intensity. This is widely accepted as a problem for
73
two-channel polarisation vision, yet, with the exception of some associative learning experiments
74
with cephalopods (Moody and Parriss, 1961; Shashar and Cronin, 1996), this has not been
75
investigated in detail at the behavioural level. To this end, we used a modified liquid crystal display
76
(LCD) monitor (Glantz and Schroeter, 2006; Pignatelli et al., 2011; How et al., 2012; Temple et al.,
77
2012) to present polarised looming stimuli to the two-channel polarisation vision system of the
78
fiddler crab Uca heteropleura (Smith, 1870) and to the dynamic, multi-channelled polarisation vision
79
system of the stomatopod Haptosquilla trispinosa (Dana, 1852). These looming stimuli differed in
80
the degree of polarisation, while the overall light intensity remained constant. We compared the
81
response probability of these two species to stimuli that fell, either within, or outside a predicted
82
null point of discrimination for a two-channel polarisation vision system.
83 84
Results
85
Fiddler crabs U. heteropleura responded to polarised looming stimuli in a number of ways similar to
86
those reported for U. vomeris (How et al., 2012), including cessation of all movement (freeze),
87
drawing of the legs or claw closer to the body (tuck), a jerk or twitch, and a sprint. A small number
88
of crabs responded to the zero contrast stimulus (Fig. 1a, dotted line) as a result of coincidental
89
changes in behaviour during stimulus presentation. These therefore estimate the probability of false
90
positive responses during the experiment. A significant response was recorded for crabs viewing the
91
horizontally polarised stimuli down to differences in degree as low as 8% (linear mixed effects model
92
(lmer) for 8% stimulus vs. background: family binomial, number of crabs (n) = 22, df = 1, χ 2 = 18.7, p
