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INTRODUCTION
Color patterns on animals affect their fitness in terms of reproductive success
and survivorship (Caro, 2005). For example, vivid colored ornaments can increase the
chance to be a potential mate by conspicuousness, and color patterns can reduce
predation risk by concealment. Therefore, the study of animal coloration is important
to understand animal behavior and evolution.
The function of color patterns depends on the sensory perception of the viewer.
Based on the colorblindness of humans in weak light, mammals (i.e., most are
nocturnal species) were previously assumed to lack color vision (Jacobs, 1993).
However, recent studies showed at least 24 species of non-primate mammals have
color vision, including 10 that were nocturnal (Kelber et al., 2003).
The finding that mammals can recognize color, suggests the possibility that they
also can see fluorescence, as has been found in some other taxa (Arnold et al., 2002;
Lim et al., 2007). Fluorescence is a by-product of excitation due to high energy
radiation such as ultraviolet. The excitation changes invisible radiation such as
ultraviolet to visible light. Although humans cannot recognize fluorescence under the
normal light conditions, in a dimly lit room with black lamps, humans can see the
fluorescence just like visible color. Fluorescent patterns are known to be important in
mate choice of some arachnids and birds (Arnold et al., 2002; Lim et al., 2007).
However, little is known about the occurrence, let alone function, of fluorescent color
patterns in mammals.
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In Metatherian mammals (marsupials), 29 species within the Family
Didelphidae (New world opossums) have fluorescent patterns on their pelage (Pine
and Abravaya, 1978; Pine, 1981; Meisner, 1983; Pine and Handley, 1984; Pine et al.,
1985; Macrini, 2004) although their functions are unknown. Moreover, the hair of 14
species of Order Diprotodontia (kangaroos and wallabies etc.) and Eastern Quoll
(Dasyurus viverrinus) (Bolliger, 1944; Nicholls and Rienits, 1971, 1973) contains
fluorescent substances. There are few data regarding fluorescence in Eutherian
(placental) mammals.
A second potential source of color is ultraviolet reflectance. Ultraviolet is
defined as an electronic radiation with a wavelength of 4 - 400 nm, but only the longer
wavelengths of ultraviolet (290 - 400nm) are available and reflected as potential
source of sensory information (Daniels, 1964; Koller, 1965; Robinson, 1966). Most
animals that have ultraviolet vision have peak sensitivity around 360 nm wavelengths
of ultraviolet (Jacobs, 1992; Tovée, 1995). As with fluorescent patterns (effectively),
humans are blind to ultraviolet reflectance patterns; the color vision of human is
restricted to the “visible spectrum” (380 – 760nm; Koller, 1965).
Ultraviolet vision and ultraviolet reflectance patterns also function in
mate-choice decisions for some animals, including some butterflies, spiders, fishes,
lizards and birds (Silberglied, 1973; Brunton and Majerus, 1995; Andersson and
Amundsen, 1997; Bennett et al., 1997; Hunt et al., 1999; Limbourg et al., 2004;
Boulcott et al., 2005; Mougeot and Arroyo, 2006; Kemp and Rutowski, 2007; Lim et
al., 2007). In contrast to “visible” (i.e., to humans) coloration and fluorescence,
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ultraviolet reflectance patterns are less permanent. For example, nutritive condition
can change the strength of ultraviolet reflectance (Lim and Li, 2006).
In addition to sexual display, ultraviolet reflectance patterns also facilitate
species discrimination. For instance, some species of birds that appear
indistinguishable based on the visible spectrum have different ultraviolet reflectance
patterns (Bleiweiss, 2004). This suggests that ultraviolet vision enables them to
differentiate their own species from other species. There is no apparent relationship
between ultraviolet reflectance patterns and visible color patterns (Bennett et al., 1997;
Lyytinen et al., 2004), suggesting that ultraviolet vision and ultraviolet reflectance
patterns confer additional (rather than redundant) information.
Although researchers believed, until recently, that mammals were blind to
ultraviolet radiation (Bennett et al., 1994), some mammals, such as the house mouse
(Mus musculus), Mongolian jird (Meriones unguiculatus), and Botta’s pocket gophers
(Thomomys bottae) were confirmed to possess ultraviolet vision (Jacobs, 1992).
Moreover, Hut et al. (2000) concluded that nocturnal rodents are likely to have
ultraviolet vision.
Furthermore, it might be advantageous for nocturnal rodents to possess
ultraviolet signals. In butterflies, for example, ultraviolet reflectance patterns occur
more frequently in nocturnal species than diurnal species (Lyytinen et al., 2004),
which appears to be associated with predation. Diurnal birds tend to have ultraviolet
vision, whereas nocturnal birds tend not to (Koivula et al., 1997).
My research investigates the taxonomic distribution and particular nature (e.g.,
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sexual dimorphism, anatomical location) of ultraviolet reflectance patterns and
fluorescent patterns on rodents in an ecological hypothesis-driven framework to
investigate possible adaptive functions. Although many biologists have made detailed
examination of mammalian coloration with respect to the visible spectrum, there are
no data on 365nm ultraviolet-induced ultraviolet reflectance and fluorescent patterns
on rodents. If rodents possess these invisible (to humans) patterns, the effect of their
coloration could be different from that of visible coloration. Therefore, I will assess
the function of these invisible patterns by the association of life history and
environmental characters.
METHODS
Specimens
I examined 634 study skins (n = 2 per species) of 297 rodent species available at
the Museum of Vertebrate Zoology (University of California, Berkeley) during April
2008 to February 2009; Dr. James Patton graciously allowed use of these specimens for
this study. The specimens were chosen because they had associated collection location
data (latitude, longitude and elevation), represented both sexes, and phylogenetic
relationships (topology and branch lengths) had been previously assessed. Because
preservation of skins does not affect the existence of ultraviolet reflection and
fluorescence (Pine et al., 1985; Eaton and Lanyon, 2003; Hausmann et al., 2003), I was
able to use these specimens. To maximize the number of species, I examined only one
specimen of each sex from 292 species.
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However, to investigate the possibility of the individual variation within species, I
observed ultraviolet reflection and fluorescence of 10 individuals (5 males and 5
females) on five species, chose to represent four Rodentia suborders, including one
species each from Sciuromorpha, Castorimorpha and Hystricomorpha and two species
from Myomorpha.
When many specimens of the species from the same locality were available, I
chose the specimens with the best skin condition, collected at the highest elevation (to
maximize exposure to ultraviolet radiation, which is blocked by aerosol [e.g., cloud],
and favored most recently collected specimens.
Ultraviolet reflection and Fluorescent patterns
Both dorsal and ventral surfaces were examined on a non reflective plate in a
handmade dark box (26×60×52cm.) for eliminating unwanted spectra from the
environment (Plate 1).
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Plate 1
Dark box
60cm
52cm
26cm
Black vinyl cover
Non reflectance plate
Adjustable hooks
Ultraviolet lamp
UV protection goggle
Peep-hole
The filter
CCD camera
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The dorsal surface included head, ears, neck, body, fore-feet, hind-feet, fore-legs,
hind-legs and tail. The ventral surface included face, neck, body, fore-legs, hind-legs,
plantar tubercles and tail. In some individuals, I examined a lateral surface for
observations of legs and face patterns.
The plate was painted by Krylon ultra-flat camouflage Black #4290 to clearly
see ultraviolet reflection from specimens. The former version of this paint, ultra-flat
Black Krylon #1602, reflects 0.2 % at 350 nm (Wightman and Grum 1981). The box
was made by two thick wood panels stood parallel on a thin wood panel and the top
was covered by a thin wood panel. The remaining sides were covered by black vinyl
which allowed easy access to set specimens and flexibility for the length of specimens.
Because specimens’ size varied among species, the box had an adjustable plate with
hooks; for specimens too large for the box, I used a darkroom located in the Museum
of Vertebrate Zoology (UC Berkeley).
To detect fluorescent patterns, I used a handheld ultraviolet lamp (UVL-56,
6-watt, 365nm, 115V, UVP Inc.) as suggested by Pine (1981). To detect the ultraviolet
reflectance patterns, I used the ultraviolet lamp, an ultraviolet-transmitting,
visible-absorbing filter (U-360, Hoya Corporation; maximum transmittance 355 –
365nm) and a CCD Black and White Video Camera (Sony XC-EU50). Because
humans cannot see the ultraviolet spectrum, I used CCDs (Charge-coupled devices) in
the video camera which are specifically sensitive to ultraviolet radiation in the 360nm
range. The video camera with the filter recorded only the radiation corresponding to
the ultraviolet vision of rodents (355 – 365nm) (Jacobs, 1992; Tovée, 1995).
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Although some ultraviolet reflection is measured by spectrophotometers, these
machines are no better than human discrimination (Bowers, 1956). In addition,
spectrophotometers cannot detect ultraviolet reflectance patterns, chiefly because the
objective size on spectrophotometers is limited, for example, to 1mm in diameter (Lim
and Li, 2006), 2mm in diameter (Church et al., 1998) and 3mm² (Dresp et al., 2005;
Dresp and Langley, 2006). Without samples of known ultraviolet patterns, this
limitation prevents accurate results (Bowers, 1956).
Life history and Ecological characters
I used the classification of Mammal Species of the World (Carleton et al., 2005).
Life history characters were found in the Mammalian Species series and several
resources (i.e., Eisenberg, 1989; Emmons, 1997; Francis, 2008; Nowak and Paradiso,
1999; Parker, 1990; Reid, 1997; Smith and Xie, 2008; Strahan, 1983). Locomotion was
classified as Biped, Limited biped (the species can stand, but cannot walk bipedally),
and Quadruped. Activity of species was classified as Diurnal, Nocturnal (includes
crepuscular) and Diel (day and night). Predators were classified as Insects, Fish,
Reptiles, Aves, Mammals and None.
To classify species habitats, I used the life zone chart by Holdridge (1967). The 15
life zones (e.g., desert) were based on mean annual biotemperature, mean annual
precipitation and elevation. The mean annual biotemperature, the annual average
Celsius temperatures at which vegetative growth occurs, was calculated by following
the method of Holdridge (1967). The weather data were collected from World Weather
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Records (published by the Smithsonian Institution [-1940], by the United States
Weather Bureau [1941-1950] ) for specimens were collected before 1950 and Monthly
Climatic Data for the World (published by the National Climatic Center, Environmental
Data and Information Service, NOAA) for the specimens collected after 1951. I
compared the latitude and longitude of the specimens with that of available stations and
then I chose the nearest station and collected the weather data (i.e. temperature and
precipitation). According to Holdridge’s (1967) guidelines, each habitat fell into seven
altitudinal belts (Basal belt, Premontane, Lower Montane, Montane, Subalpine, Alpine,
Nival) and one of 12 humidity provinces (Semiparched, Superarid, Peratid, Arid,
Semiarid, Subhumid, Humid, Perhumid, Superhumid, Semisaturated, Subsaturated,
Saturated).
Data Analyses
Two binomial response variables regarding ultraviolet reflectance or fluorescence
were considered: whether or not the trait was conspicuous and, if so, whether the trait
could serve as a signal. Determination of whether ultraviolet reflection patterns were
conspicuous depended on environmental context (Fig. 1).
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Figure 1 Flowchart is describing the determination process of conspicuousness for
ultraviolet reflection patterns.
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In desert and snow habitats, assumed to strongly reflect ultraviolet radiation,
animals that reflected ultraviolet radiation were considered inconspicuous and those
that absorbed ultraviolet radiation were considered conspicuous (to observers that see
ultraviolet radiation). On the other hand, in habitats where ultraviolet radiation was
primarily absorbed by vegetation (e.g. forested habitats), animals that reflected
ultraviolet radiation were considered conspicuous and those that absorbed ultraviolet
radiation were considered inconspicuous.
Whether a conspicuous pattern constituted a potential signal further depended on
which body surface relative to the locomotory mode of the species (Fig. 2).
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Figure 2 Flowchart is showing how to classify conspicuous ultraviolet coloration and
fluorescence pattern as possible signals.
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Ultraviolet reflection patterns and fluorescence patterns on plantar tubercles or
ventral surface of tail were never considered signals because these surfaces are rarely
visible to other organisms.
Before assessing possible adaptive significance of ultraviolet or fluorescent
signal with respect to life history or environmental characters I assessed their
phylogenetic independence using the Runs Test (Abouheif, 1999). The Runs Test was
conducted in the program, Phylogenetic Independence Version 2.0 (Reeve and
Abouheif, 2003) with completed phylogeny data modified from the super tree of
Bininda-Emonds et al. (2007) in program Mesquite Version 2.6 (Maddison and
Maddison, 2009).
Phylogenetically non-independent data need to be tested for an association
between traits (e.g., ultraviolet reflectance signal) and life history (i.e. activity and
predators) or environmental (i.e. altitudinal belts, life zones, humidity provinces and
elevation) variables among species by phylogenetic comparative methods (PCMs),
which have been developed to reduce the effect of phylogenetic inertia (Janson, 1992).
The association was tested by Generalized Estimating Equations (GEE)
approach (Paradis and Claude, 2002), one of the PCMs can analyze not only
non-independent data but also independent data (Paradis and Claude, 2002; Paradis,
2006). Moreover, the GEE approach can analyze binominal traits and continuous and
categorical characters. The GEE approach was run using the APE package in R
language (Paradis et al., 2004).
When the GEE approach was applied, binominal variables were transformed to
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“0” for absent and “1” for present. Some multi-nominal characters (i.e. altitudinal belts,
life zones and humidity provinces) were reclassified to reduce the number of dummy
variables (Table 1).
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Table 1 Reclassification of multi-nominal variables for GEE approach
Altitudinal
belts
Life zones
Humidity
provinces
1)Basal belt
2)Premontane, Lower Montane
3)Montane, Subalpine
1)Wet Tundra, Wet Forest, Rain Forest, Moist Forest
2)Steppe, Dry Forest, Thorn Steppe, Thorn Woodland, Very Dry Forest
3)Dry Scrub, Desert Scrub, Desert;
1)Perarid, Arid
2)Semiarid, Subhumid
3)Humid, Perhumid, Superhumid.
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RESULTS
Individual variation
I observed little individual variation on the presence of ultraviolet reflection and
fluorescence (Table 2).
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Table 2 Individual variation of the presence of ultraviolet reflection and fluorescence
among five rodent species was shown. Number of specimens with character present /
total number of specimens, UV = ultraviolet, Dorsal = dorsal surface, Ventral = ventral
surface
Suborder
Species
Sciuromorpha
Castorimorpha
Myomorpha
Myomorpha
Hystricomorpha
Tamiasciurus douglaasii
Liomys salvini
Zapus princeps
Rattus steini
Ctenomys haigi
UV
reflection
Dorsal
0 / 10
0 / 10
8 / 10
0 / 10
9 / 10
UV
reflection
Ventral
1 / 10
8 / 10
10 / 10
0 / 10
10 / 10
Fluoresc
ence
Dorsal
0 / 10
9 / 10
0 / 10
10 / 10
10 / 10
Fluoresc
ence
Ventral
0 / 10
10 / 10
10 / 10
9 / 10
10 / 10
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Phylogenetic independence
Ultraviolet signal was significantly phylogenetically correlated (P=0.0003) as
was sexual dimorphism in this trait (P=0.0003).
Fluorescent signal was also significantly phylogenetically correlated (P=0.0003).
However, sexual dimorphism in this trait was not significantly phylogenetically
correlated (P=0.086).
Ultraviolet signal
One hundred ninety-eight species (67%) exhibited an ultraviolet signal.
Ultraviolet signal was significantly associated with elevation (P < 0.001) (Fig. 3, Table
3). However, associations with life history characters (i.e. activity and predators) and
other environmental variables (i.e. altitudinal belts, life zones and humidity provinces)
were not significant. Among the species that exhibited ultraviolet signal, 51 species
were sexually dimorphic with respect to this trait.
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Fig.3
Association between ultraviolet signal and elevation
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Table 3 Association between ultraviolet signal and life history or environmental
variables by Generalized Estimating Equations (GEE) approach was shown. n =
number of species, dfP = phylogenetic degrees of freedom, S.E. = standard error, *Test
of the significance: F = 8.1459, df = 1, p=0.001
Variable
Activity
n
284
dfP
49.78
Reptilian predators
Avian predators
Mammalian predators
Altitudinal belts
101
101
101
297
21.98
21.98
21.98
51.25
Life zones
297
51.25
Humidity provinces
297
51.25
Elevation
297
51.25
Estimate
0.3077
0.2145
0.5708
1.3434
-0.2760
-0.1794
-0.0112
0.2625
-0.3471
0.9709
0.6261
0.0002
S.E.
0.1665
0.3326
0.3961
0.2406
0.2417
0.1687
0.2728
0.1968
0.2762
0.1907
0.1993
6.1606
t
1.8481
0.6448
1.4411
5.5847
-1.1419
-1.0634
-0.0410
1.3336
-1.2570
5.0915
3.1422
2.8541
p
0.0708
0.5221
0.1643
1.5344
0.2664
0.2928
0.9675
0.1885
0.2147
5.5888
2.8374
0.0063*
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Fluorescent signal
Two hundred fifty-eight species (87%) exhibited a fluorescent signal that was
significantly associated with avian predators (P < 0.01) (Fig. 4, Table 4). However,
associations with other life history characters (i.e. activity, reptilian predators and
mammalian predators) and environmental variables were not significant. Among the
species that exhibited a fluorescent signal, 11 species were sexually dimorphic with
respect to this trait.
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Fig.4
Association between fluorescent signal and avian predators
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Table 4 Association between fluorescence signal and life history or environmental
variables by Generalized Estimating Equations (GEE) approach was shown. n =
number of species, dfP = phylogenetic degrees of freedom, S.E. = standard error, *Test
of the significance: F = 6.1536, df = 1, p = 0.01
Variable
Activity
n
284
dfP
49.78
Reptilian predators
Avian predators
Mammalian predators
Altitudinal belts
101
101
101
297
21.98
21.98
21.98
51.25
Life zones
297
51.25
Humidity provinces
297
51.25
Elevation
297
51.25
Estimate
0.4976
-0.6607
-0.1822
0.7067
0.0120
-0.1070
0.0518
-0.1833
0.3349
-0.6559
-0.4496
-0.0001
S.E.
0.5081
0.3664
0.4441
0.2849
0.2875
0.2405
0.3202
0.2295
0.4340
0.2203
0.3334
0.0001
t
0.9795
-1.8031
-0.4103
2.4806
0.0418
-0.4451
0.1619
-0.7986
0.7718
-2.9772
-1.3485
-0.9464
p
0.3323
0.0777
0.6858
0.0217*
0.9670
0.6582
0.8721
0.4283
0.4439
0.0045
0.1837
0.3485
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DISCUSSION
Ultraviolet signal
Among other taxa, conspicuous ultraviolet coloration is used for intra- or
inter-specific communication like visual coloration (ex. Avilés et al., 2006; Viitala et
al., 1995). However, ultraviolet coloration may be more influenced by radiation
condition than visual coloration because ultraviolet is more scattered than longer
wavelength, light (Bennett and Cuthill, 1994).
“Altitude effect”, the increase in solar radiation with increasing altitude, could
be expected to affect the presence of ultraviolet signal due to the increases in visibility
at higher altitudes. In particular, radiation of 370 nm wavelength increases nine
percent per 1000 m (Blumthaler et al., 1997). Consistent with this hypothesis, I found
a trend toward increasing frequency of species with ultraviolet signal at increasing
elevations. The rodents possessing ultraviolet signal may choose their habitat to
maximize the conspicuousness of the signal. For example, some lek birds {i.e.,
cock-of-the rocks (Rupicola rupicola), white-throated manakins (Corapipo gutturalis),
and white-fronted manakins (Lepidothrix serena)} apparently choose specific light
conditions for their display to maximize visual contrast (Endler and Théry, 1996). On
the contrary, the solar radiation stimulated the employment of ultraviolet signal among
rodents living in high elevation. For example, among gonodactyloid stomatopods, the
visual system of each species adapts its habitat light condition respectively (Cronin et
al., 2000).
Some avian predators such as Eurasian kestrels (Falco tinnunculus),
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rough-legged buzzards (Buteo lagopus) and great grey shrikes (Lanius excubitor)
detect their prey by using ultraviolet cues (Viitala et al., 1995; Koivula and Viitala,
1999; Probst et al., 2002). Although I found that more than half of the rodent species
investigated possessed ultraviolet signal, this trait was not associated with avian or
other predators, suggesting ultraviolet signal may not affect risk of predation.
Although ultraviolet signal is an important cue for mate choice in some animals
such as jumping spiders (Cosmophasis umbratica), zebra finches (Taeniopygia
guttata), bluethroats (Luscinia s. svecica) and starlings (Sturnus vulgaris) (Bennett et
al., 1996; Andersson and Amundsen, 1997; Bennett et al., 1997; Lim et al., 2007), only
51 species out of 198 species showed sexual dimorphism, suggesting ultraviolet signal
was not primarily related to sexual ornamentation. However, most of the 51 species
are promiscuous like other taxa which have conspicuous sexual dimorphism.
Fluorescent signal
The function of fluorescent signal is not clear especially in the terrestrial
environment (Andrews et al., 2007; Mazel and Fuchs, 2003). Although fluorescent
signal was considered as a warning against predators (orchid bees (Eufriesea
niveofasciata); Nemésio, 2005), a threat to other males and predators (Mantis shrimp
(Lysiosquillina glabriuscula); Mazel et al., 2004), a lure for prey (deep-sea
siphonophores (Erenna); Haddock et al., 2005), and a cue for species recognition or
intraspecific communication (loliginid squid (Alloteuthis subulata and Loligo
vulgaris); Mäthger and Denton, 2001; reef fishes; Michiels et al., 2008), only the
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function for courtship among jumping spiders (Cosmophasis umbratica) and
budgerigars (Melopsittacus undulatus) (Arnold et al., 2002; Lim et al., 2007) was
experimentally tested.
Most rodents possessed fluorescent signal, especially those with avian predators.
Avian hunting can be divided into visual hunting by diurnal species and acoustic
hunting by nocturnal species (Mikkola, 1983; Sherman, 1985; Honkavaara et al.,
2002). Therefore, not only the presence of avian predators but also the activity pattern
of avian predators may affect predation risk.
Interestingly, the species, either male or female has fluorescence on dorsal body,
which I consider the most conspicuous fluorescent pattern, are likely the prey of
diurnal avian species. This finding was somewhat counterintuitive and suggests the
presence of a trade-off. If signal increases vulnerability to predators, it must also
confer some benefit exceeding this cost such as ornamentation. Indeed, the species
displaying sexual dimorphism in fluorescent signal more frequently had diurnal avian
predators.
Moreover, the species that fluoresced its dorsal body in both sexes tended to
have nocturnal avian predators or not to have avian predators. This suggested that, like
loliginid squid (Alloteuthis subulata and Loligo vulgaris) ( Mäthger and Denton, 2001),
rodents may use fluorescent signal for species recognition or intraspecific
communication in the absence of the pressure of predation risk.
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CONCLUSION
This research clearly showed that ultraviolet signal and fluorescent signal exist
among rodents. The evolution of ultraviolet signal is probably encouraged more
strongly in the presence of greater ultraviolet radiation especially in the reduced
predation risk. Therefore, although the adaptive function of ultraviolet signal in
rodents is probably different from that in other taxa, ultraviolet coloration in rodents,
as with birds (Finger and Burkhardt, 1994; Parker, 2005), may be caused by the
structure of hair or skin. My findings point to the possibility that fluorescence among
rodents emerged by predator-prey interaction like spiders (Andrews et al., 2007).
Therefore, rodents may mainly use fluorescent signal as a communication tool hidden
from their predators.