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Although ultraviolet (UV) sensitivity is widespread among animals it is considered rare in mammals, being restricted to the few species that have a visual pigment maximally sensitive (λmax) below 400 nm. However, even animals without such a pigment will be UV-sensitive if they have ocular media that transmit these wavelengths, as all visual pigments absorb significant amounts of UV if the energy level is sufficient. Although it is known that lenses of diurnal sciurid rodents, tree shrews and primates prevent UV from reaching the retina, the degree of UV transmission by ocular media of most other mammals without a visual pigment with λmax in the UV is unknown. We examined lenses of 38 mammalian species from 25 families in nine orders and observed large diversity in the degree of short-wavelength transmission. All species whose lenses removed short wavelengths had retinae specialized for high spatial resolution and relatively high cone numbers, suggesting that UV removal is primarily linked to increased acuity. Other mammals, however, such as hedgehogs, dogs, cats, ferrets and okapis had lenses transmitting significant amounts of UVA (315-400 nm), suggesting that they will be UV-sensitive even without a specific UV visual pigment.
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, 20132995, published 19 February 2014281 2014 Proc. R. Soc. B
R. H. Douglas and G. Jeffery
sensitivity is widespread among mammals
The spectral transmission of ocular media suggests ultraviolet
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Cite this article: Douglas RH, Jeffery G. 2014
The spectral transmission of ocular media
suggests ultraviolet sensitivity is widespread
among mammals. Proc. R. Soc. B 281:
Received: 15 November 2013
Accepted: 21 January 2014
Subject Areas:
vision, lens, transmission, mammal, ultraviolet
sensitivity, retina
Author for correspondence:
R. H. Douglas
Electronic supplementary material is available
at or
The spectral transmission of ocular media
suggests ultraviolet sensitivity is
widespread among mammals
R. H. Douglas
and G. Jeffery
Department of Optometry and Visual Science, City University London, Northampton Square,
London EC1V 0HB, UK
Institute of Ophthalmology, University College London, 11-43 Bath Street, London EC1V 9EL, UK
Although ultraviolet (UV) sensitivity is widespread among animals it is con-
sidered rare in mammals, being restricted to the few species that have a
visual pigment maximally sensitive (
) below 400 nm. However, even ani-
mals without such a pigment will be UV-sensitive if they have ocular media
that transmit these wavelengths, as all visual pigments absorb significant
amounts of UV if the energy level is sufficient. Although it is known that
lenses of diurnal sciurid rodents, tree shrews and primates prevent UV from
reaching the retina, the degree of UV transmission by ocular media of most
other mammals without a visual pigment with
in the UV is unknown.
We examined lenses of 38 mammalian species from 25 families in nine
orders and observed large diversity in the degree of short-wavelength trans-
mission. All species whose lenses removed short wavelengths had retinae
specialized for high spatial resolution and relatively high cone numbers,
suggesting that UV removal is primarily linked to increased acuity. Other
mammals, however, such as hedgehogs, dogs, cats, ferrets and okapis had
lenses transmitting significant amounts of UVA (315400 nm), suggesting
that they will be UV-sensitive even without a specific UV visual pigment.
1. Introduction
The range of wavelengths an animal perceives depends on the spectrum available
in the environment, the degree to which this is transmitted though the ocular
media and the visual pigments within the retina. The spectrum that humans
see during the day, using three cone visual pigments absorbing maximally
) at 420, 534 and 563 nm [1], spans approximately 400700 nm. Adult
humans are insensitive to shorter, ultraviolet (UV) wavelengths as these are
absorbed by the lens [25] and hence never reach the retina.
The range of wavelengths visible to other animals is often very different
from that of man due largely to their possession of visual pigments absorbing
elsewhere in the spectrum. Many species, for example, possess visual pigments
below 400 nm, and the resultant UV-sensitivity is relatively wide-
spread among invertebrates [68], birds, fish, reptiles and amphibians [9,10].
Among mammals, such UV-sensitive visual pigments are relatively rare and
have only been described in some rodents [1118], a mole [19], several marsu-
pials [2023] and some bats [2427]. Such animals have lenses that, unlike
those of humans, transmit short wavelengths well. UV sensitivity in mammals,
in comparison to other animals, is thus thought to be the exception.
Although visual pigments are usually characterized by their
, the wave-
length range absorbed by them is in fact broad and displays a secondary
absorption maximum in the UV (the cis-peak or b-band). Thus, all photo-
receptors can potentially absorb significant amounts of UV and any animal
with ocular media that are transparent to UV light will inevitably be sensitive
to these wavelengths even if they do not possess a visual pigment with
this part of the spectrum [9] (figure 1).
2014 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution
License, which permits unrestricted use, provided the original
author and source are credited.
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Therefor e, if the UV-absorbing lens of humans is remov ed
following catar a ct surgery or trauma tic injury, and not replaced
by a UV-absorbing prosthetic, they report vivid and detailed
vision in the UV [6,3133]. Similarly, despite the absence of a
visual pigment with
in the UV , the reindeer retina responds
electrophysiologically below 400 nm [34] and circadian rhythms
in the Syrian hamster can be entrained by wavelengths below
400 nm [3540], simply because they both hav e lenses that trans-
mit significant amount of light below 400 nm rather than a visual
pigment with
in the UV. Likewise, a phyllostomid flower
bat with a UV-transparent lens is able to respond behaviour ally
to UV even in scotopic conditions using the b-band of its rod
pigment [41]. A degree of UV sensitivity in the absence of a
photoreceptor absorbing maximally in this part of the spectrum
is therefor e not infrequent.
The spectral transmission of the ocular media (cornea, lens,
aqueous and vitreous humour) at short wavelengths is deter-
mined by their structural components, thickness and any
specific short-wave absorbing pigments they contain [42]. No
structure will transmit significant amounts of light below
about 300 nm owing to absorption by its nucleic acids and
structural protein components, for example aromatic amino
acids. With the exception of some fish corneas that absorb
blue/green light [4345], most corneas are thin and unpig-
mented, transmitting UV radiation down to around 300 nm.
Aqueous and vitreous humours are similarly transparent.
Lens transmission, however, is very variable. In some species,
the lens lets through almost as much UV as the cornea, while
in others it can remove all UV and some of the blue, appearing
visibly yellow. Thus, although oil droplets in birds, for example,
prevent short wavelengths from reaching the outer segments of
some cones, and pigments such as the human macular pigment
absorb blue light, the lens is the filter that determines the cut-off
in the UV in almost all species (see the electronic supplementary
material, S1).
Unfortunately, detailed informationabout the spectral trans-
mission of most mammalian lenses is lacking. The only ones that
have been examined are those that seem obviously interesting.
At one extreme, the lenses of diurnal primates [5,4649], tree
shre ws [50,51] and sciurid rodents [12,39,5258] are various
shades of yellow, removing all radiation below 420470 nm.
At the other extreme, species with visual pigments with
in the UV have lenses maximally transparent to UV radiation,
transmitting mos t light down to 320340 nm [3,4,12,16,18,
19,23,25,36,37,5964]. How ev er, little is known about the w a ve-
lengths transmitted by the lenses of mammals between these
two extremes. Although the lenses of some have been reported
as containing no short-wa velength-absorbing pigment [54],
reliable quantitative transmission data from intact lenses are
only available only for the Syrian hamster (Mesocricetus auratus)
[3539], pig (Sus scrofa) [4], rabbit (Oryctolagus cuniculus)
[3,6568] and reindeer (Rangifer tarandus)[34].
Here, we examine the spectral transmission of the lenses of
38 mammalian species belonging to 25 families in nine orders,
most never examined before, and show a variety of degrees
of shortwave transmission. Perhaps surprisingly, many let
through significant amounts of shortwave radiation, suggesting
that a degree of UV sensitivity is widespread among mammals.
2. Material and methods
Animals were obtained from various sources such as abattoirs,
zoos, veterinary practices and scientific establishments (see
Acknowledgements). They had either been used for other scien-
tific procedures, sacrificed for food production, died naturally or
were put down owing to injury or illness. No animals were killed
specifically for this project. Eyes were obtained either immedi-
ately following death, or soon thereafter, and were either used
immediately or frozen dry for several days before thawing. Vari-
able numbers of lenses were available for each species and in
four species a range of lens sizes/ages were examined (see
table 1 for details).
Lenses, and usually corneas, were removed from the eye,
briefly rinsed in phosphate-buffered saline (PBS) and mounted
in purpose-built holders in air in front of an integrating sphere
within a Shimadzu 2101 UVPC spectrophotometer. Vitreous
humour was also removed from the eyes of some animals with
a syringe and placed in a standard quartz cuvette within the
same apparatus. Transmission at 700 nm was set to 100% and
ocular media scanned at 1 nm intervals from 300 to 700 nm.
To determine the effect of freezing on lens transmission, three
fresh bovine lenses were scanned soon after death, frozen in air at
2258C for 4 days, thawed and rescanned.
The pigments responsible for lens pigmentation were also
extracted and spectrally characterized for six species (see the
electronic supplementary material, S4).
3. Results
Although the cornea and vitreous humour were not exam-
ined in all species, when they were, in line with previous
observations [42], the lens always removed more short-
wavelength radiation than either the cornea or the vitreous
(see the electronic supplementary material, S1).
Freezing had no significant effect on lens transmission,
allowing data from both fresh and previously frozen lenses
to be compared (figure 2).
The spectral transmission of the lenses of some of the
species studied here had been examined previously; pig [4],
tree shrew (Tupaia glis) [50], rabbit [3,6568], mouse (Mus mus-
culus) [3,4,63,64], brown rat (Rattus norvegicus) [3,4,12,36,37,60],
grey squirrel (Sciurus carolinensis) [54,58], prairie dog (Cynomys
ludovicianus) [5556], flying squirrel (Glaucomys volans) [56],
marmoset (Callithrix jacchus )[49],squirrelmonkey(Saimiri
300 400 500 600 700
% transmission
normalized absorbance
wavelength (nm)
Figure 1. The absorption spectra of the visual pigments of the ferret and the
spectral transmission of its lens. The absorption maxima of the visual
pigments (rods—505 nm; cones—430 and 558 nm) are taken from
Calderone & Jacobs [28] and the visual pigments templates of Govardovskii
et al. [29] (solid lines) have been fitted to them using the methods described
in Hart et al. [30]. The lens transmission (dotted line) is taken from this
study. As all the visual pigments absorb significant amounts of UV radiation
and the lens transmits in this part of the spectrum, the ferret is likely to
perceive such short wavelengths. Proc. R. Soc. B 281: 20132995
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Table 1. Summary of mammalian lenses examined ranked by the amount of UVA they transmit. ‘50%T’ is the wavelength at which the lens transmits 50% of
the incident illumination. ‘%UVA transmitted’ is a measure of the proportion of light between 315 and 400 nm that is transmitted by the lens (see the
electronic supplementary material, S2). For most species, lens transmission and axial diameter (pathlength) varied little between individuals and averages are
shown. Where there were significant differences between individuals, ranges are given. Where the transmission of the lens varied with lens size/age, the % UVA
on the retina was calculated using specific ages/lens sizes as described in footnotes.
order family species
number of
Rodentia Muridae mouse (Mus musculus) 29 1.9 2.8 313337 81.4
Rodentia Muridae black rat (Rattus rattus) 11 3.7 5.2 317372 80.5
Erinaceomorpha Erinaceidae hedgehog (Erinaceus
4 3.0 326 65.5
Carnivora Canidae dog (Canis lupus familiaris)
2 5.0 335 61.3
Chiroptera Pteropodidae Livingstone’s fruit bat
(Pteropus livingstonii)
4 5.0 6.0 332422 60.8
Carnivora Felidae cat (Felis catus) 6 7.0 345 58.9
Carnivora Mustelidae ferret (Mustela putorius furo) 4 3.9 344 56.1
Rodentia Muridae brown rat (Rattus norvegicus) 2 4.2 339 55.8
Artiodactyla Giraffidae okapi (Okapia johnstoni) 2 7.0 355 53.4
Artiodactyla Suidae pig (Sus scrofa) 5 5.5 375 43.6
Rodentia Caviidae guinea pig (Cavia porcellus) 11 3.7 377 34.6
Carnivora Ailuridae red panda (Ailurus fulgens) 1 5.8 386 30.2
Rodentia Sciuridae flying squirrel
(Glaucomys volans)
2 4.9 423 29.3
Chiroptera Pteropodidae Rodrigues flying fox
(Pteropus rodricensis)
1 4.8 388 28.1
Artiodactyla Cervidae reindeer (Rangifer tarandus) 5 10.1 384 26.5
Artiodactyla Cervidae pudu
(Pudu puda) 2 7.0 386 25.0
Artiodactyla Bovidae cattle (Bos primigenius) 8 11.1 384 22.1
Artiodactyla Bovidae sheep (Ovis aries) 4 7.7 393 15.2
Rodentia Dasyproctidae agouti (Dasyprocta punctata) 1 6.1 406 15.0
Lagomorpha Leporidae rabbit (Oryctolagus cuniculus) 2 6.7 392 12.7
Artiodactyla Tragulidae java mouse deer
(Tragulus javanicus)
2 9.0 403 12.4
Artiodactyla Bovidae Arabian oryx (Oryx leucoryx) 1 10.3 400 8.5
Artiodactyla Camelidae alpaca (Vicugna pacos) 5 10.2 405 6.0
Perissodactyla Equidae horse (Equus ferus caballus) 1 12.0 416 4.6
Primates Cebidae squirrel monkey
(Saimiri sciureus sciureus)
2 4.6 420 2.8
Primates Lemuridae ring-tailed le
(Lemur catta)
1 6.5 425 2.0
Carnivora Herpestidae meerkat (Suricata suricatta) 3 2.4 3.4 420436 1.7
Primates Callitrichidae marmoset (Callithrix jacchus) 1 3.0 427 0.9
Artiodactyla Bovidae lowland anoa
(Bubalus depressicornis)
1 8.0 478 0.6
Rodentia Sciuridae ground squirrel
(Urocitellus richardsonii)
2 3.1 462 0.6
Primates Cercopithecidae macaque (Macaca fascicularis) 5 3.3 424 0.5
(Continued.) Proc. R. Soc. B 281: 20132995
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sciureus sciureus)[46]andmacaque(Macaca fascicularis)[48].Our
data for these species agreed with the previously published spec-
tra. They are presented here to validate our method, facilitate
direct comparison with novel data and allow further analysis.
The spectral transmission of representative lenses is shown in
figure 3 and equivalent scans for all species are shown in the elec-
tronic supplementary material, S3. The spectral properties of the
mammalian lenses examined ranged from those in young murid
amounts of UV r adia tion (50% transmission 310320 nm), to
those of prima tes, sciurid rodents, meerka ts and tree shre ws
that wer e visibly yellow and prev ented UV r adia tion from reac h-
ing the retina (50% transmission 424465 nm). All other
mammals had lenses whose spectral tr ansmission la y betw een
these two extremes (table 1 and figure 3; also see the electr onic
supplementary material, figure S3ad).
The degree of UV radia tion transmitted by the lens is
traditionally expressed as the wa v elength of 50% transmission.
How e v er, this measur e can be misleading as the short-wa v e-
length cut-off is sometimes steep, but at other times gentle.
Thus, although the flying squirrel and the macaque both have
a similar wa v elength of 50% transmission (423424 nm), their
spectral chara cteristics at short wav elengths are in fact quite
different (see the electronic supplementary material, figure 3c).
A better indica tion of the potential for UV vision is given by
the proportion of UVA (315400 nm) tha t is transmitted by the
lens (table 1; see the electronic supplementary material, S2).
Forfourspecies(Pteropus livingstonii, Rattus ra ttus, Mus mus-
culus and Suricata suricatta), lenses from a range of ages/sizes
were available and exhibited decreased short-wavelength trans-
mission in older/larger lenses. Data are shown only for the rat
lenses wer e available for them. Similar trends wer e shown by
lesser numbers of Livingston’s bats (n ¼ 4) and meerkats (n ¼ 3).
The eyes of the Alaotran gentle lemur and the ring-tailed
lemur, apart from containing a distinctly yellow coloured
Table 1. (Continued.)
order family species
number of
Primates Atelidae red-faced spider monkey
(Ateles paniscus)
1 3.8 438 0.4
Primates Callitrichidae golden lion tamarin
(Leontopithecus rosalia)
1 3.0 441 0.4
Scandentia Tupaiidae Tree shrew (Tupaia glis) 1 3.2 435 0.3
Primates Lemuridae Alaotran gentle lemur
(Hapalemur alaotrensis)
1 5.9 425 0.3
Rodentia Sciuridae grey squirrel
(Sciurus carolinensis)
2 3.6 441 0
Rodentia Sciuridae prairie dog
(Cynomys ludovicianus)
7 3.6 463 0
Primates Cebidae capuchin (Cebus apella) 1 3.9 426 0
Aged 69 72 days with lens pathlength 2.2 mm.
Pathlength 3.8 mm.
Pathlength 5.0 mm.
Pathlength 3.4 mm.
300 400 500 600 700
% transmission
th (nm)
Figure 2. Average spectral transmission of three bovine lenses before (solid
line) and after (dashed line) four days of freezing.
300 350 400 450 500
% transmission
th (nm)
Figure 3. Representative average spectral transmission curves at short wave-
lengths of the lenses from 10 mammalian species. Most curves are the
averages of all available lenses. However, for the black rat and meerkat indi-
viduals of a variety of lens sizes were scanned; the data shown for the two
species are for young and old animals, respectively. From left to right at 50%
transmission they are (n, lens axial diameter in millimetres); young black rats
(2, 3.8), cat (6, 7.0), okapi (2, 7.0), cattle (8, 11.1), rabbit (2, 6.7), Arabian
oryx (1, 10.3), squirrel monkey (2, 4.6), Alaotran gentle lemur (1, 5.9), adult
meerkat (1, 3.4) and prairie dog (7, 3.6). All scans were zeroed at 700 nm. Proc. R. Soc. B 281: 20132995
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lens, on dissection revealed a bright yellow substance within
the eye. Strepsirrhine primates are known to have yellow ribo-
flavin-based tapeta [69], which is almost certainly the source of
this pigmentation.
A pigment absorbing maximally at 357369 nm was
extracted from the lenses of six species with yellow lenses
and identified as 3-hydroxykynurenine glucoside in two
(see the electronic supplementary material, S4).
4. Discussion
(a) Diversity of ultraviolet transmission by
mammalian lenses
As expected, the transmission of short wavelengths by the
mammalian lens varies considerably between species. At one
extreme, as has previously been reported, species with visual
pigments absorbing maximally in the UVfor example murid
rodentstransmit up to 80% of UVA radiation (figure 3 and
table 1; see also the electronic supplementary material, S3).
The most UV-transparent lens observed outside of such animals
belongs to the European Hedgehog (Erinaceus europeus;seethe
electronic supplementary material, figure S3b). Interestingly,
preliminary evidence suggests that the closely related Southern
white-breasted hedgehog (Erinaceus concolor) may in fact pos-
sess a visual pigment with
below 400 nm (M. Glo
2013, personal communication). In stark contrast, the lenses of
mature diurnal primates, sciurid rodents, tree shrews and
meerkats contain a pigment absorbing maximally around
360370 nm (see the electronic supplementary material, S4).
Consequently, they absorb all UV radiation and a considerable
amount of blue light, appearing visibly yellow (figure 3 and
table 1; see also the electronic supplementary material, S3).
Although it is well established that sciurid rodents and diurnal
primates have yellow lenses, we have expanded the number of
species within these orders known to have such lenses, and
their presence in meerkats is a novel observation.
However, most mammals appear to have lenses between
these two extremes that transmit variable amounts of short-
wave radiation (figure 3 and table 1; see also the electronic
supplementary material, S3). Relatively large lenses like those
of the horse (Equus ferus caballus), alpaca, oryx, anoa (Bubalus
depressicornis) and mouse deer remove the vast majority of
the UV, although as they remove little visible radiation, they
do not appear obviously yellow. On the other hand, animals
such as the cat, dog, ferret and okapi have lenses that transmit
only slightly less UVA than those of some murid rodents
(figure 3 and table 1; see also the electronic supplementary
material, S3).
As expected, species that are at least partially nocturnal
generally have lenses transmitting UV, while those that
are mainly diurnal prevent such wavelengths reaching the
retina. For example, while diurnal sciurid rodents have
yellow lenses that remove all UV, the nocturnal flying squirrel
has a clear lens [56] that transmits significant amounts of
UVA (table 1; see also the electronic supplementary material,
figure S3c). However, such a demarcation is not absolute and
some animals, like the okapi, can be exposed to relatively
high amounts of daylight while having lenses that transmit
relatively large amounts of UV.
(b) Lens transmission indicates that a degree of
ultraviolet sensitivity may be widespread among
Only species with UV-transparent lenses and a visual pig-
ment with
below 400 nm are usually considered UV
sensitive. However, as all visual pigments have a degree of
photosensitivity at such short wavelengths, an animal with
a lens transmitting UV radiation will inevitably be sensitive
in this part of the spectrum, even in the absence of a specific
UV-absorbing visual pigment.
Species are ranked according to the amount of UVA trans-
mitted by the lens in table 1. A previous study has shown that
the reindeer, whose lens transmits 26.5% of UVA and which
does not have a visual pigment with
below 400 nm,
nevertheless responds electrophysiologically to 372 nm light
[34]. It therefore seems likely that species with similar or
300 400 500 600 700
% transmission
wavelength (nm)
3.5 4.0 4.5 5.0 5.5
50% transmission
pathlength (mm)
50% transmission
0 100 200 300 400 500 600
e (da
Figure 4. Lens transmission as a function of lens size/age in rodents. (a) Spectral
transmission of 11 black rat (R. rattus) lenses ranging in axial length between
3.7 and 5.2 mm. (b) Wavelength of 50% transmission as a function of lens
size for all the lenses shown in (a). The data are fit by y ¼ 43.992x þ
149.68 (R
¼ 0.9062). The dashed line is an approximation of the relationship
expected if pathlength were the only factor affecting transmission. (c)Average
wavelength of 50% lens transmission (+1 s.d.) of mice (M. musculus)of
known age; 40 (n ¼ 3), 70 (n ¼ 8), 265 (n ¼ 4) and 564 (n ¼ 6) days.
The data are fit by y ¼ 0.0443x þ 311.1 (R
¼ 0.9634). Proc. R. Soc. B 281: 20132995
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more UV lens transmission, such as cattle, pig, ferret, dog,
okapi and cat, for example, will also be sensitive at these
short wavelengths (table 1).
The realization that many mammals have some UV sensi-
tivity may be important for understanding aspects of their
behaviour as they could be responding to visual signals
undetectable to humans. It may also have implications for
the lighting conditions of captive and domestic species. On
the one hand, some UV may be required for normal behav-
iour, while on the other, excessive UV exposure might put
species with UV-transparent ocular media at increased risk
of retinal damage (see below).
(c) The nature of ultraviolet sensitivity without a
at short wavelengths
It might be argued that UV perception not mediated by a
visual pigment with
in this part of the spectrum is in
some way not ‘real’ UV sensitivity. However, nobody ques-
tions a human’s ability to see red light with a wavelength
of 700 nm, despite the fact that our long-wavelength sensitive
cone absorbs maximally at wavelengths more than 100 nm
removed from this.
Although all visual pigments can absorb UV radiation, the
way the signals generated by the photoreceptors to such wave-
lengths are processed is not known. Thus, animals without a
visual pigment with
in the UV will probably be unable
to distinguish UV as a separate colour. Aphakic humans, for
example, report UV as appearing like a desaturated (whitish)
blue-violet [6].
The extent of UV sensitivity in animals with UV-transpar ent
ocular media but without a specific UV visual pigment is also
uncertain. However, it is probable that such animals will be
less sensitive at these wavelengths than species that do have
such a visual pigment, although the photopic sensitivity of
aphakic humans [6] and reindeer [34] to UV light is surprisingly
high. Such sensitivity will be influenced by several factors.
For example, as the absorptance spectrum of a visual pigment
is influenced by pigment density, the degree of UV sensitivity
will depend in part on the length of a species’ outer segments
and the presence of a tapetum (which would effectively double
the pathlength of the outer segment). Furthermore, the nature
of the inter a ctions between the different photor eceptor types a t
short wavelengths and the effectiveness of short wav elengths
at triggering the transduction cascade, neither of which are
known, will also influence the degree of shortwave sensitivity.
(d) Function of ultraviolet sensitivity in mammals
It is tempting to seek a specific function for UV sensitivity,
although similar questions are rarely asked about other
parts of the spectrum. The functions proposed include;
mate choice, ‘secret’ intraspecific communication, navigation,
prey detection and foraging. However, UV light is little
different from other parts of the spectrum and its perception
need have no specific function beyond simply extending the
spectral range of the animal and improving its sensitivity.
Indeed, although UV has a role to play in both foraging
and mate choice in birds, longer wavelengths have been
shown to be more important [70,71]. Although in some
instances, UV may have a specific function, such as increas-
ing the visibility of the white fur of predatory polar bears
within a snowy landscape for reindeer [34] or enhancing
the visibility of urine trails for rodents [15,16], UV is normally
just a part of a wider spectrum of wavelengths all of which
are important for an animal’s behaviour.
Perhaps, the reason why there is a tendency to attribute
some special importance to UV sensitivity is simply that
humans are not able to see it [72].
(e) What is the function of preventing ultraviolet
radiation from reaching the retina?
Shortwave-sensitive visual pigments come in two forms:
violet-sensitive or UV-sensitive (UVS). Molecular evidence
suggests the UVS visual pigments are the ancestral form
[73]. Logically therefore, UV-transmitting lenses are also
ancestral and animals must have been subjected to selective
pressure to lose both UVS visual pigments and UV lens trans-
mission. Therefore, rather than seeking a specific function for
UV vision in mammals, it might be more pertinent to ask,
what is the function of animals having lenses that prevent
short wavelengths reaching the retina? Blocking UV could
be either protective or an aid to spatial resolution [42].
These different functions are by no means mutually exclusive
and both would explain the presence of UV-absorbing lenses
in mainly diurnal animals.
Removing short wavelengths, especially in long-lived
diurnal species, could protect the retina as the degree of reti-
nal light damage is considerably increased at shorter
wavelengths [74]. There is some experimental evidence for
such a function. For example, when the UV-absorbing
lenses of grey squirrels were removed, the retinae of these
eyes suffered more retinal damage than intact companion
eyes [75]. It has therefore been suggested that the reason noc-
turnal rodents, for example, can have UV-sensitive visual
pigments (and a UV-transparent lens) is that they are rela-
tively short-lived and habitually exposed to low light levels.
However, the lens cannot have a protective role in all species.
The reindeer, for example, lives in an extremely UV-rich
environment and can reach ages of up to 20 years, yet it
seems to suffer no ill effects from allowing UV to reach the
retina [34]. Similarly, some UV-sensitive parrots can live to
be over 50 years old with no apparent damage [76]. Either
species such as reindeer and parrots have mechanisms
to prevent the harmful effects of UV, or some species are
particularly sensitive to its deleterious consequences.
Short-wave absorbing filters will also increase image
quality as both the degree of Rayleigh scatter and chromatic
aberration are increased in this part of the spectrum [52],
although such a function is difficult to prove experimentally.
Interestingly, species such as diurnal primates and sciurid
rodents, whose lenses do remove short wavelengths, either
have a large proportion of cones (more than 20%) within
the retina and/or areas of very high cone density (more
than 100 000 cones mm
; see the electronic supplementary
material, table S5), which is consistent with a function of
such filters being to increase image quality. Interestingly,
the same argument has very recently been suggested to
account for the UV-absorbing ocular media of diurnal rap-
tors, which have extremely high visual acuity to facilitate
the capture of moving prey on the wing [77].
For species active that are at night, on the other hand,
the primary visual requirement is high absolute sensitivity
rather than spatial acuity, which will be facilitated by a
UV-transparent lens. Such animals generally have a lower Proc. R. Soc. B 281: 20132995
on February 19, 2014rspb.royalsocietypublishing.orgDownloaded from
proportion of cones in their retina and no areas of increased
cone density, but often have areas of increased rod density
consistent with maximizing absolute sensitivity (see the
electronic supplementary material, table S5).
(f) Size(age)-related changes in lens transmission
It is not possible to characterize the spectral transmission of a
species’ lens by a single curve, as it will inevitably change as
a function of lens size. In some species, such as man, the lens
grows throughout life [78], and its size can be used to age the
animal [79]. In other species, lens growth levels off in older ani-
mals [80]. Generally, as shown by the four species in this study
for whom a range of lens sizes were available (P. livingstonii,
R. rattus, M. musculus and S. suricatta), the relative transmission
of short wavelengths decreases with increased lens size and
age (figure 4).
Some age-related change in lens transmission is an inevi-
table consequence of increased pathlength in older animals.
An approximate indication of the effect of lens size on
spectral transmission can be obtained by squaring the trans-
mission spectrum of a small lens to give a theoretical curve
for a lens twice the diameter [81,82]. For both the rat
(figure 4b) and mouse (data not shown), increased size is
insufficient to account for the decreased transmission
observed. The causes for the frequently described age-related
yellowing of the lens of primates [5,83] are complex [78] but
are in part the result of the attachment of the major
tryptophan-derived, short-wave absorbing lens pigment
(see the electronic supplementary material, S4) to lens pro-
teins [47,84]. The proximate causes of the decreased
shortwave transmission in other species, for example those
described here, that cannot be the result of a simple increase
in pathlength, are unclear.
It seems likely that such age-related changes in lens trans-
mission are the inevitable result of both increased lens size
and light exposure. Nonetheless, they might protect the
retina of older animals from the harmful UV radiation and,
for example, slow the rate of photoreceptor loss.
We are grateful to the following who helped in the
procurement of eyes: Stewart Thompson (Imperial College, University
of London); Ilse Pedler (Mercer and Hughes Veterinary practice, Saf-
fron Walden); Jim Bowmaker and Astrid Limb (University College
London); Margaret Stafford and John Lawrenson (City University
London); Wendy Steel (Royal Veterinary College, Potters Bar); Clare
Brazill-Adams (MRC National Institute for Medical Research, Mill
Hill); the Horniman Museum (London), Edmund Flach and Belinda
Clark (Zoological Society of London); Kellie Wyatt, Adina Valentine,
Christoph Schwitzer and Michelle Barrow (Bristol Zoo); Helen
Schwantje and Caite Nelson (Fish, Wildlife and Habitat Management
Branch state government BC, Canada). Especial thanks to Andrea
Bowden (ne
e Thorpe) for allowing use of some unpublished data
from her PhD. Professors Julian Partridge, Roger Truscott, Leo Peichl
and Martin Glo
smann are thanked for helpful discussion.
Funding statement. G.J. was supported by the BBSRC for some of this
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Supplementary resource (1)

... Vertebrate corneas and humours are typically highly transmissive from the infrared to ca. 300 nm (e.g., [36]), but some lenses contain pigments that prevent shorter-wavelength light reaching the retina. As far as we are aware, transmission data for snake corneas have Table 15.1. ...
... Some diurnal snakes have similarly transmissive lenses across a broad range of wavelengths, whereas others block some or all light <400 nm ( Fig. 15.4N). Evidence for the latter is thus far restricted to caenophidians, mostly highly visual hunters, consistent with the hypothesis that blocking UV enhances acuity (e.g., [36]) as well as perhaps protecting retinal cells from damage. Data are scant but, as far as is known, snakes with UV-blocking lenses have visual pigments with peak sensitivities >400 nm. ...
Snakes comprise nearly 4,000 extant species found on all major continents except Antarctica. Morphologically and ecologically diverse, they include burrowing, arboreal, and marine forms, feeding on prey ranging from insects to large mammals. Snakes are strikingly different from their closest lizard relatives, and their origins and early diversification have long challenged and enthused evolutionary biologists. The origin and early evolution of snakes is a broad, interdisciplinary topic for which experts in palaeontology, ecology, physiology, embryology, phylogenetics, and molecular biology have made important contributions. The last 25 years has seen a surge of interest, resulting partly from new fossil material, but also from new techniques in molecular and systematic biology. This volume summarises and discusses the state of our knowledge, approaches, data, and ongoing debates. It provides reviews, syntheses, new data and perspectives on a wide range of topics relevant to students and researchers in evolutionary biology, neontology, and palaeontology.
... Different factors such as price and durability must be calculated in order to determine the best marker (Janss and Ferrer, 1998). There are also many researches available that showed by using Ultraviolet lights, the collision of birds may be minimized as described in Bischof et al. (2011) and May et al. (2017) A detailed study carried out by Douglas and Jeffery (2014) confirmed that the discharges of UV rays on power lines happened as standing corona adjacent to cables and random flashes on insulator and this discharge spectrum (200nm-400nm) was below the standard lower limit of human vision. ...
... The presence of UV-driven traits could result from a range of processes such as being a byproduct of physiology, an enhancement of individual physiology, or serving an ecological role by enhancing communication or concealmentmost are untested hypotheses. It should be noted that some ecologically functional roles likely depend on the optical sensitivity of organisms involved in intraspecific or interspecific interactions [23][24][25][26][27][28]18]. Alternatively, while biofluorescence may be physiologically or ecologically adaptive in some species, in others, it might be a biochemical pathway with specific, unknown, or insignificant impacts on individual fitness [27,5,29,17]. ...
Ultraviolet (UV) induced biofluorescence is being discovered with increasing frequency across the tree of life. However, there is not yet a standardized, low-cost, photographic methodology used to document, quantify, and minimize sources of bias that often accompany reports made by researchers new to fluorescence imaging. Here, a technique is described to create accurate photographs of biofluorescent specimens as well as how to use these images to quantify fluorescence via color quantization, using open-source code that utilizes K-means clusters within the International Commission on Illumination L*a*b* (CIELAB) color space. The complexity of photographing different excitation and emission wavelengths and methods to reduce bias from illumination source and/or camera color sensitivity (e.g., white balance) without the use of modified equipment is also addressed. This technique was applied to preserved southern flying squirrel (Glaucomys volans) specimens to quantify the color shift between illumination under visible and UV light and analyze variation among specimens. This relatively simple methodology can be adapted to future studies across a range of fluorescent wavelengths and project goals, and assist future research in which unbiased photographs and analyses are key to understanding the physiological and ecological role of biofluorescence.
... Many birds, perhaps the majority of species, achieve spectral resolution across a broad light spectrum, from ultraviolet to far red (Cuthill et al. 2000). However, it should be noted that contrary to popular belief, birds are not exceptional in this, the same broad spectral range of vision is found in many mammals (Douglas and Geffery 2014) and invertebrates (Cronin 2008). Furthermore, vision in the ultraviolet region of the spectrum, is not a property of vision in all birds. ...
Full-text available
Natural England Commissioned Report NECR432
... Another enigma concerns the reindeer's cornea and lens. Overexposure to ultraviolet (UV) light can cause irreversible damage to retinal photoreceptors [3], so most diurnal mammals have UV-filtering ocular media [4]. In reindeer, however, the cornea and lens transmit up to 60% of available UV light [5], which is enough to excite the photoreceptors responsible for vision [5]. ...
... Vision characteristics Reference Dog Red-green color blind; more sensitive to object movement; two types of photoreceptors, blue and yellow but not red and green; can see UV Neitz et al., 1989;Davis, 1998;Douglas and Jeffery, 2014 Bee See orange, yellow, green, blue, violet, and even UV, but no red. UV, blue and green photoreceptors Menzel and Backhaus, 1989;Chittka and Menzel, 1992;Peitsch et al., 1992 Mantis shrimp Up to 12 photoreceptors that can detect UV, visible, and polarized light; perceive depth with each eye Thoen et al., 2014;Cronin and Marshall, 2001 Crab Mäthger et al., 2006;Shashar et al., 1996 Bat Use echolocation to locate and catch its prey; also see with polarized light. ...
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Traditional supervised classifications for remote sensing-based water quality monitoring count on a set of classifiers to retrieve features and improve their prediction accuracies based on ground truth samples. However, many existing feature extraction methods in remote sensing are unable to exhibit multiple-instance nonlinear spatial pattern recognition at scales via ensemble learning. This paper designed for lake algal bloom monitoring presents intelligent feature extraction for harmonizing local and global features via tensor flow-based ensemble learning with integrated biomimetic and computational intelligence. To explore such complexity, an Integrated Biomimetic and Ensemble Learning Algorithm (IBELA) was developed to synthesize the contribution from different classifiers associated with the biomimetic philosophy of integrated bands. It leads to strengthened multiple-instance spatial pattern recognition in lake algal bloom monitoring via image fusion at the decision level. With the implementation of IBELA, a case study of a eutrophic freshwater lake, Lake Managua, for water quality monitoring leads to demonstrate six input visual senses showing different impacts on retrieving Chl-a concentrations in the dry and wet season, respectively. The input of total nitrogen from the watershed plays the most important role in water quality variations in both seasons in a watershed-based food-water nexus. Although ultraviolet and microwave bands are important in the dry season, Secchi disk depth is critical in the wet season for water quality monitoring.
Snakes comprise nearly 4,000 extant species found on all major continents except Antarctica. Morphologically and ecologically diverse, they include burrowing, arboreal, and marine forms, feeding on prey ranging from insects to large mammals. Snakes are strikingly different from their closest lizard relatives, and their origins and early diversification have long challenged and enthused evolutionary biologists. The origin and early evolution of snakes is a broad, interdisciplinary topic for which experts in palaeontology, ecology, physiology, embryology, phylogenetics, and molecular biology have made important contributions. The last 25 years has seen a surge of interest, resulting partly from new fossil material, but also from new techniques in molecular and systematic biology. This volume summarises and discusses the state of our knowledge, approaches, data, and ongoing debates. It provides reviews, syntheses, new data and perspectives on a wide range of topics relevant to students and researchers in evolutionary biology, neontology, and palaeontology.
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Lynn et al., (2019) accused fellow scientists of misrepresenting free-roaming cats (Felis catus) by framing them as a global threat to biodiversity, rather than a localised threat to specific ecosystems. These authors asserted that the narrative created a ‘moral panic’ over free-roaming cats, which is escalated by emotive journalistic pieces read by audiences around the world. To test this empirically, I performed a thematic discourse analysis of user comments responding to five news articles, a magazine, and a YouTube video related to the topic of freeroaming cats. The discourses examined flow between conservationists, the media, and the public, and reflect the confused and convoluted ways in which people think about cats. Here I discuss how well the data fits the moral panic theory. I analyse how labels such as ‘feral’ serve to ‘other’ cats, rendering them objects of distain and creating ‘folk devils’ that are deemed more killable than beloved companion animals of the same species.
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In this work, we for the first time report the identification of UV filters in the bird eye lens. We found that lenses of some raptors (black kite, common buzzard) and waterfowl (birds from Podicipedidae family) contain unusually high levels of reduced nicotinamide adenine dinucleotide (NADH)—a compound with high absorption in the UV-A range with a maximum at 340 nm. The lens metabolome of these birds also features an extremely low [NAD +]/[NADH] ratio. Chemometric analysis demonstrates that the differences between the metabolomic compositions of lenses with low and high NADH abundances should be attributed to the taxonomic features of bird species rather to the influence of the low [NAD +]/[NADH] ratio. We attributed this observation to the low metabolic activity in lens fiber cells, which make up the bulk of the lens tissue. Photochemical measurements show that properties of NADH as a UV filter are as good as that of UV filters in the human lens, including strong absorption in the UV-A spectral region, high photostability under both aerobic and anaerobic conditions, low yields of triplet state, fluorescence, and radicals under irradiation. Lenticular UV filters protect the retina and the lens from photo-induced damages and improve the visual acuity by reducing chromatic aberrations; therefore, the results obtained contribute to our understanding of the extremely high acuity of the raptor vision.
Purpose: To determine the spectral transmittance of artificial intraocular lenses (IOLs) designed for various species (dog, cat, chinchilla, eagle, tiger) and compare them to the spectral properties of the biological lenses of these species. Methods: Twenty-seven IOLs were scanned with a spectrophotometer fitted with an integrating sphere. Results: All IOLs transmitted long wavelengths well before cutting off sharply at short wavelengths, with insignificant transmission below ca. 340 nm. In comparison with the IOLs, the biological lenses of the cat, dog, and probably the chinchilla transmitted significantly more short wavelengths. The spectral properties of the biological lenses of eagles and tigers, while uncertain, may be a closer match to the IOLs made for these species. Conclusion: It is not known if there are any visual or behavioral consequences for animals caused by a mismatch between the spectral properties of their biological lenses and IOLs. However, following IOL implantation there might be a change in the perceived hue of objects due to the removal of UV wavelengths which form a normal part of the visible spectrum for these species and/or a decrease in sensitivity.
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We investigated the reactions of four bat species from four different lineages to UV light: Hipposideros armiger (Hodgson, 1835) and Scotophilus kuhlii Leach, 1821, which use constant frequency (CF) or frequency modulation (FM) echolocation, respectively; and Rousettus leschenaultii (Desmarest, 1820) and Cynopterus sphinx (Vahl, 1797), cave and tree-roosting Old World fruit bats, respectively. Following acclimation and training involving aversive stimuli when exposed to UV light, individuals of S. kuhlii and C. sphinx exposed to such stimuli displayed conditioned reflexes such as body crouching, wing retracting, horizontal crawling, flying and/or vocalization, whereas individuals of H. armiger and R. leschenaultii, in most cue-testing sessions, remained still on receiving the stimuli. Our behavioral study provides direct evidence for the diversity of cone-based UV vision in the order Chiroptera and further supports our earlier postulate that, due to possible sensory tradeoffs and roosting ecology, defects in the short wavelength opsin genes have resulted in loss of UV vision in CF bats, but not in FM bats. In addition, Old World fruit bats roosting in caves have lost UV vision, but those roosting in trees have not. Bats are thus the third mammalian taxon to retain ancestral cone-based UV sensitivity in some species.
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Ultraviolet (UV)-sensitive visual pigments are widespread in the animal kingdom but many animals, for example primates, block UV light from reaching their retina by pigmented lenses. Birds have UV-sensitive (UVS) visual pigments with sensitivity maxima around 360-373 nm (UVS) or 402-426 nm (violet-sensitive, VS). We describe how these pigments are matched by the ocular media transmittance in 38 bird species. Birds with UVS pigments have ocular media that transmit more UV light (wavelength of 50% transmittance, λT0.5, 323 nm) than birds with VS pigments (λT0.5, 358 nm). Yet, visual models predict that colour discrimination in bright light is mostly dependent on the visual pigment (UVS or VS) and little on the ocular media. We hypothesize that the precise spectral tuning of the ocular media is mostly relevant for detecting weak UV signals, e.g. in dim hollow-nests of passerines and parrots. The correlation between eye size and UV transparency of the ocular media suggests little or no lens pigmentation. Therefore, only small birds gain the full advantage from shifting pigment sensitivity from VS to UVS. On the other hand, some birds with VS pigments have unexpectedly low UV transmission of the ocular media, probably because of UV blocking lens pigmentation.
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Recent years have seen an upsurge of interest in the study of ultraviolet vision in vertebrates. The presence of retinal photopigments that allow for ultraviolet vision appear to be relatively common among birds and fishes, and there is evidence that such pigments are to be found in some species from each of the following classes: amphibians, reptiles, and mammals. Following a review of the distribution and nature of ultraviolet vision in vertebrates the issue of the utility of this capacity is discussed.
purpose. To determine the eye’s spectral sensitivity in three species of the genus Octodon (order Rodentia; infraorder Caviomorpha), O. degus, O. bridgesi, and O. lunatus, as well as the spectral properties of the animals’ fur and urine and of objects in their habitat. The genus is endemic in Chile and contains species with different habitats and circadian patterns (diurnal versus nocturnal). methods. The electroretinogram (ERG) was used to record scotopic and photopic spectral sensitivity. The reflectance of ventral and dorsal body parts, urine, and other objects from the natural microhabitat were measured with a fiber-optic spectrometer. results. In scotopic conditions, the maxima of sensitivity (λmax) were at 505.7 ± 7.7 nm in O. degus, 501 ± 7.4 nm in O. bridgesi, and 510.1 ± 7.4 nm in O. lunatus, representing the rod mechanism. In photopic conditions, only the diurnal species O. degus (common degu) was studied. The degu’s photopic sensitivity had a λmax at 500.6 ± 1.2 nm and contained two cone mechanisms with λmax at 500 nm (green, medium-wavelength–sensitive [M] cones) and approximately 360 nm (ultraviolet, short-wavelength–sensitive [S] cones). In all three Octodon species, dorsal body parts were more cryptically colored than ventral ones, and ventral body parts had a significant UV reflectance. The fresh urine of O. degus, used for scent marking in various behavioral patterns, was also high in UV reflectance. conclusions. It is suggested that territorial urine marks are visual as well as pheromone cues for UV-sensitive species and hence may have favored the evolution of UV-cones in rodents.
Direct spectral transmittance data over the wave band 200–2500 nm were obtained for the ocular media of the thirteen-lined ground squirrel (Spermophilus tridecemlineatus) using a Zeiss (Oberkochen) DMR-21 dual-beam recording spectrophotometer. These data were used to calculate cumulative transmittance curves for each of the interfaces between optical media in the ground squirrel eye. Although radiation in the wave band 300–2500 nm can penetrate the cornea, our data show that the yellow pigment of the crystalline lens absorbs all wavelengths below 410 nm, while the vitreous humour absorbs most radiation longer than 1400 nm. The ground squirrel retina is, therefore, effectively protected from both near ultraviolet and infrared radiation, both of which are known to have deleterious effects on retinal photoreceptors.
The near ultraviolet (UVA) is a band of radiation that is invisible to us but not to a wide range of other creatures. Its discovery and properties are outlined, together with techniques for examining it. Its significance in flowers, butterflies and birds is reviewed and the position within the mammals is discussed.
We characterized Fos-like expression patterns in the primary visual cortex (V1) by binocular flicking stimulation with UV light to investigate cone-based UV vision in four bat species representing four lineages: Hipposideros armiger and Scotophilus kuhlii, insectivores using constant frequency (CF) or frequency modulation (FM) echolocation, respectively, and Rousettus leschenaultii and Cynopterus sphinx, cave-roosting and tree-roosting fruit bats, respectively. The optic centre processing the visual image, V1, appears more distinctly immunostaining in S. kuhlii and C. sphinx after 1h of UV light stimuli while in H. armiger and R. leschenaultii, staining was no more distinct than in corresponding controls. Our immunohistochemical evidence supports differences in the distribution of cone-based UV vision in the order Chiroptera and supports our earlier postulate that due to possible sensory tradeoffs and roosting ecology, defects in the short wavelength opsin genes have resulted in loss of UV vision in CF but not in FM bats. In addition, fruit bats roosting in caves have lost UV vision but not those roosting in trees. Our results thus confirm that bats are a further mammalian taxon that has retained cone-based UV sensitivity in some species.