Tetrachromacy, oil droplets and bird plumage colours

There is a growing body of data on avian eyes, including measurements of visual pigment and oil droplet spectral absorption, and of receptor densities and their distributions across the retina. These data are sufficient to predict psychophysical colour discrimination thresholds for light-adapted eyes, and hence provide a basis for relating eye design to visual needs. We examine the advantages of coloured oil droplets, UV vision and tetrachromacy for discriminating a diverse set of avian plumage spectra under natural illumination. Discriminability is enhanced both by tetrachromacy and coloured oil droplets. Oil droplets may also improve colour constancy. Comparison of the performance of a pigeon's eye, where the shortest wavelength receptor peak is at 410 nm, with that of the passerine Leiothrix, where the ultraviolet-sensitive peak is at 365 nm, generally shows a small advantage to the latter, but this advantage depends critically on the noise level in the sensitivity mechanism and on the set of spectra being viewed. Accepted: 3 July 1998     

Variations of colour vision in a New World primate can be explained by polymorphism of retinal photopigments

The squirrel monkey (Saimiri sciureus) exhibits a polymorphism of colour vision: some animals are dichromatic, some trichromatic, and within each of these classes there are subtypes that resemble the protan and deutan variants of human colour vision. For each of ten individual monkeys we have obtained (i) behavioural measurements of colour vision and (ii) microspectrophotometric measurements of retinal photopigments. The behavioural tests, carried out in Santa Barbara, included wavelength discrimination, Rayleigh matches, and increment sensitivity at 540 and 640 nm. The microspectrophotometric measurements were made in London, using samples of fresh retinal tissue and a modified Liebman microspectrophotometer: the absorbance spectra for single retinal cells were obtained by passing a monochromatic measuring beam through the outer segments of individual rods and cones. The two types of data, behavioural and microspectrophotometric, were obtained independently and were handed to a third party before being interchanged between experimenters. From all ten animals, a rod pigment was recorded with lambda max (wavelength of peak absorbance) close to 500 nm. In several animals, receptors were found that contained a short-wave pigment (mean lambda max = 433.5 nm): these violet-sensitive receptors were rare, as in man and other primate species. In the middle- to long-wave part of the spectrum, there appear to be at least three possible Saimiri photopigments (with lambda max values at about 537,550 and 565 nm) and individual animals draw either one or two pigments from this set, giving dichromatic or trichromatic colour vision. Thus, those animals that behaviourally resembled human protanopes exhibited only one pigment in the red-green range, with lambda max = 537 nm; other behaviourally dichromatic animals had single pigments lying at longer wavelengths and these were the animals that behaviourally had higher sensitivity to long wavelengths. Four of the monkeys were behaviourally judged to be trichromatic. None of the latter animals exhibited the two widely separated pigments (close to 535 and 567 nm) that are found in the middle- and long-wave cones of macaque monkeys.(ABSTRACT TRUNCATED AT 400 WORDS)     

Spectral mechanisms in the tree squirrel retina

Summary The retina of the gray squirrel (Sciurus carolinensis) contains rods and cones in a ratio of about 23. The spectral mechanisms in this retina were examined in behavioral and electrophysiological experiments. Tests of color vision revealed that this animal has a spectral neutral point at about 500 nm and, thus, dichromatic color vision. Recordings made from single optic nerve fibers and results obtained from an analysis of the flicker photometric electroretinogram (ERG) indicated that vision in the gray squirrel is based on three spectral mechanisms. One of these, presumably rod-based, has peak sensitivity at about 502 nm. The other two mechanisms reflect the presence of two classes of cone having average peak sensitivity of about 444 nm and 543 nm.     

The Absolute Threshold of Colour Vision in the Horse

Arrhythmic mammals are active both during day and night if they are allowed. The arrhythmic horses are in possession of one of the largest terrestrial animal eyes and the purpose of this study is to reveal whether their eye is sensitive enough to see colours at night. During the day horses are known to have dichromatic colour vision. To disclose whether they can discriminate colours in dim light a behavioural dual choice experiment was performed. We started the training and testing at daylight intensities and the horses continued to choose correctly at a high frequency down to light intensities corresponding to moonlight. One Shetland pony mare, was able to discriminate colours at 0.08 cd/m², while a half blood gelding, still discriminated colours at 0.02 cd/m². For comparison, the colour vision limit for several human subjects tested in the very same experiment was also 0.02 cd/m². Hence, the threshold of colour vision for the horse that performed best was similar to that of the humans. The behavioural results are in line with calculations of the sensitivity of cone vision where the horse eye and human eye again are similar. The advantage of the large eye of the horse lies not in colour vision at night, but probably instead in achromatic tasks where presumably signal summation enhances sensitivity.     

Photoreceptor Spectral Sensitivity in the Bumblebee,Bombus impatiens (Hymenoptera: Apidae)

The bumblebee Bombus impatiens is increasingly used as a model in comparative studies of colour vision, or in behavioural studies relying on perceptual discrimination of colour. However, full spectral sensitivity data on the photoreceptor inputs underlying colour vision are not available for B. impatiens. Since most known bee species are trichromatic, with photoreceptor spectral sensitivity peaks in the UV, blue and green regions of the spectrum, data from a related species, where spectral sensitivity measurements have been made, are often applied to B impatiens. Nevertheless, species differences in spectral tuning of equivalent photoreceptor classes may result in peaks that differ by several nm, which may have small but significant effects on colour discrimination ability. We therefore used intracellular recording to measure photoreceptor spectral sensitivity in B. impatiens. Spectral peaks were estimated at 347, 424 and 539 nm for UV, blue and green receptors, respectively, suggesting that this species is a UV-blue-green trichromat. Photoreceptor spectral sensitivity peaks are similar to previous measurements from Bombus terrestris, although there is a significant difference in the peak sensitivity of the blue receptor, which is shifted in the short wave direction by 12–13 nm in B. impatiens compared to B. terrestris.     

Spectral sensitivities including the ultraviolet of the passeriform bird Leiothrix lutea

Spectral sensitivity functions of a passeriform bird, the Red-billed Leiothrix Leiothrix lutea (Timalidae) were determined in a behavioural test under different background illuminations.

Visual pigments, oil droplets, ocular media and cone photoreceptor distribution in two species of passerine bird: the blue tit (Parus caeruleus L.) and the blackbird (Turdus merula L.)

The spectral absorption characteristics of the retinal photoreceptors of the blue tit (Parus caeruleus) and blackbird (Turdus merula) were investigated using microspectrophotometry. The retinae of both species contained rods, double cones and four spectrally distinct types of single cone. Whilst the visual pigments and cone oil droplets in the other receptor types are very similar in both species, the wavelength of maximum sensitivity (λ_max) of long-wavelength-sensitive single and double cone visual pigment occurs at a shorter wavelength (557 nm) in the blackbird than in the blue tit (563 nm). Oil droplets located in the long-wavelength-sensitivesingle cones of both species cut off wavelengths below 570–573 nm, theoretically shifting cone peak spectral sensitivity some 40 nm towards the long-wavelength end of the spectrum. This raises the possibility that the precise λ_max of the long-wavelength-sensitive visual pigment is optimised for the visual function of the double cones. The distribution of cone photoreceptors across the retina, determined using conventional light and fluorescence microscopy, also varies between the two species and may reflect differences in their visual ecology. Accepted: 8 January 2000     

Phototaxis in water fleas (Daphnia magna) is differently influenced by visible and UV light

The effects of vertical illumination with monochromatic lights on phototaxis of Daphnia magna in a test chamber were determined at five levels of equal quantal flux density (between 188 and 6.42 · 10⁻⁵ nEinstein). Visible adaptation light (500 nm) and subsequent spectral test light had the same quantal flux density. The animals reacted to ultraviolet light (260–380 nm) with negative phototaxis, whereas visible light (420–600 nm) caused positive phototaxis. Action spectra were determined, based on the evaluation of different parameters of phototactic behavior. The maximum spectral sensitivity in the ultraviolet was found at 340 nm. The maximum spectral efficiency in the visible varied in dependence on light intensity. Ecological consequences of the results are discussed. Accepted: 3 August 1998     

Spectral sensitivity of ground squirrel cones measured with ERG flicker photometry

Summary Ground squirrels have dichromatic color vision. The spectral sensitivities of the two classes of cones found in the retinas of two species of ground squirrel were measured using ERG flicker photometry. The spectral sensitivity curves for these cone classes were closely fit by curves from wavelength-dependent visual pigment nomograms. One cone type had an average peak sensitivity of 518.9 nm (California ground squirrels,Spermophilus beecheyi) or 517.0 nm (thirteen-lined ground squirrels,Spermophilus tridecemlineatus). The second type of cone found in these ground squirrels had an average peak sensitivity of 436.7 nm. An examination of the variation in spectral sensitivity among individual animals suggests that the sensitivity peaks for the middle-wavelength cone cover a range of not greater than 4 nm.     

Avian colour vision and avian video playback experiments

Video playback potentially allows the presentation, manipulation, and replication of realistic moving visual stimuli, in a way that is impossible with real animals or static dummies, and difficult even with mechanical models. However, there are special problems attached to the use of this technology; this article concentrates on the problem of accurate colour rendition. Video and television simulate the colour of objects rather than reproduce the spectrum of light that they naturally emit, transmit, or reflect. This simulation is achieved by using relatively narrow waveband light to stimulate the cone cells in the retina in a similar pattern to that produced by the natural object. However, species differ in the spectral tuning of their photoreceptors, so a faithful colour rendition for a human is unlikely to be achieved for another species. This problem is discussed with special reference to birds, a taxon renown for its colourfulness and frequent use in behavioural experiments but which has a very different colour vision from that of humans. We stress that the major pitfalls that can arise when using video playback with avian subjects can also occur in ’normal’ behavioural experiments. However, the problems of faithful colour rendition are particularly severe with video, and the major benefits that the technology brings will only be realised under a limited range of circumstances, with careful validation experiments. Received: 24 January 2000 / Received in revised form: 28 March 2000 / Accepted: 1 April 2000     

The contribution of single and double cones to spectral sensitivity in budgerigars during changing light conditions

Bird colour vision is mediated by single cones, while double cones and rods mediate luminance vision in bright and dim light, respectively. In daylight conditions, birds use colour vision to discriminate large objects such as fruit and plumage patches, and luminance vision to detect fine spatial detail and motion. However, decreasing light intensity favours achromatic mechanisms and eventually, in dim light, luminance vision outperforms colour vision in all visual tasks. We have used behavioural tests in budgerigars (Melopsittacus undulatus) to investigate how single cones, double cones and rods contribute to spectral sensitivity for large (3.4°) static monochromatic stimuli at light intensities ranging from 0.08 to 63.5 cd/m². We found no influences of rods at any intensity level. Single cones dominate the spectral sensitivity function at intensities above 1.1 cd/m², as predicted by a receptor noise-limited colour discrimination model. Below 1.1 cd/m², spectral sensitivity is lower than expected at all wavelengths except 575 nm, which corresponds to double cone function. We suggest that luminance vision mediated by double cones restores visual sensitivity when single cone sensitivity quickly decreases at light intensities close to the absolute threshold of colour vision.     

Comparative study of the spectral sensitivities of mesopelagic crustaceans

The spectral sensitivities of 12 species of mesopelagic crustaceans were studied by means of electrophysiological recordings. Nine of the species are vertical migrators, while 3 are not, and 9 species possess bioluminescent organs, while 3 are not bioluminescent. All species had a single peak of spectral sensitivity with maxima between 470 nm and 500 nm. There was no apparent correlation between sensitivity maxima and daytime depth distribution, migratory behavior, or the presence or absence of bioluminescent organs. With the exception of the hyperiid amphipod Phronima sedentaria, the spectral sensitivities of these mesopelagic crustaceans demonstrate a better match for maximum sensitivity to bioluminescence than to downwelling light. Accepted: 29 June 1999     

Fruits, foliage and the evolution of primate colour vision

Primates are apparently unique amongst the mammals in possessing trichromatic colour vision. However, not all primates are trichromatic. Amongst the haplorhine (higher) primates, the catarrhines possess uniformly trichromatic colour vision, whereas most of the platyrrhine species exhibit polymorphic colour vision, with a variety of dichromatic and trichromatic phenotypes within the population. It has been suggested that trichromacy in primates and the reflectance functions of certain tropical fruits are aspects of a coevolved seed-dispersal system: primate colour vision has been shaped by the need to find coloured fruits amongst foliage, and the fruits themselves have evolved to be salient to primates and so secure dissemination of their seeds. We review the evidence for and against this hypothesis and we report an empirical test: we show that the spectral positioning of the cone pigments found in trichromatic South American primates is well matched to the task of detecting fruits against a background of leaves. We further report that particular trichromatic platyrrhine phenotypes may be better suited than others to foraging for particular fruits under particular conditions of illumination; and we discuss possible explanations for the maintenance of polymorphic colour vision amongst the platyrrhines.     

Energetics of offspring production: a comparison of a marsupial (Monodelphis domestica) and a eutherian (Mesocricetus auratus)

This study compares the energetic cost of reproduction during gestation and lactation of a eutherian, the golden hamster (Mesocricetus auratus), and a similar-sized (60–120 g) marsupial, the gray short-tailed opossum (Monodelphis domestica). Food consumption was monitored in 20 reproductively active (RA) opossums and 16 RA hamsters from conception to weaning and at equivalent intervals in 19 non-reproductive (NR) opossums and 21 NR hamsters, all maintained within their zone of thermoneutrality (30 °C). Total energy assimilated from conception to weaning [opossums: 1261.3 ± 28.0 Kcal (1 Kcal = 4.1868 J) and hamsters: 1647.5 ± 60.6 Kcal] was positively correlated with litter size and mass per young in both species. Maternal mass-specific assimilated energy was significantly greater in hamsters than in opossums during gestation (P < 0.001), but not during lactation or from conception to weaning (P > 0.05). Efficiency of offspring production (energy stored in young/incremental energy in RA females) was higher in hamsters than in opossums and, in both species, it was higher during lactation than in gestation. The energetic cost of reproduction (per young per day) was higher in hamsters than in opossums. The marsupial mode of reproduction, as seen in opossums, yields young at lower cost but requires a longer reproductive period than is the case for a similar-sized eutherian. Accepted: 8 September 1998     

Bat Eyes Have Ultraviolet-Sensitive Cone Photoreceptors

Mammalian retinae have rod photoreceptors for night vision and cone photoreceptors for daylight and colour vision. For colour discrimination, most mammals possess two cone populations with two visual pigments (opsins) that have absorption maxima at short wavelengths (blue or ultraviolet light) and long wavelengths (green or red light). Microchiropteran bats, which use echolocation to navigate and forage in complete darkness, have long been considered to have pure rod retinae. Here we use opsin immunohistochemistry to show that two phyllostomid microbats, Glossophaga soricina and Carollia perspicillata, possess a significant population of cones and express two cone opsins, a shortwave-sensitive (S) opsin and a longwave-sensitive (L) opsin. A substantial population of cones expresses S opsin exclusively, whereas the other cones mostly coexpress L and S opsin. S opsin gene analysis suggests ultraviolet (UV, wavelengths <400 nm) sensitivity, and corneal electroretinogram recordings reveal an elevated sensitivity to UV light which is mediated by an S cone visual pigment. Therefore bats have retained the ancestral UV tuning of the S cone pigment. We conclude that bats have the prerequisite for daylight vision, dichromatic colour vision, and UV vision. For bats, the UV-sensitive cones may be advantageous for visual orientation at twilight, predator avoidance, and detection of UV-reflecting flowers for those that feed on nectar.     

Photoreceptor spectral sensitivity in island and mainland populations of the bumblebee, <Emphasis Type="Italic">Bombus terrestris</Emphasis>

Most species of flower-visiting Hymenoptera are trichromatic, with photoreceptor spectral sensitivity peaks in the UV, blue and green regions of the spectrum. Red flowers, therefore, should be relatively difficult to detect for such insects. Nevertheless, in population biological studies in the bumblebee, Bombus terrestris, the Sardinian island population (B. t. sassaricus) displayed significantly higher responses to red artificial flowers (in tests of innate colour choice and detectability) than several mainland populations of the same species (Chittka et al. in Cognitive ecology of pollination, pp 106–126, 2001; Popul Ecol 46:243–251, 2004). Since there is relatively little physiological data on population differences in sensory systems, we used intracellular recording to compare photoreceptor spectral sensitivity in B. t. sassaricus and the southern European and Mediterranean population, B. t. dalmatinus. The results show both populations to be UV–blue–green trichromats, but with a small but significant increase in long-wave sensitivity in island bees. Spectral peaks were estimated at 348, 435 and 533 nm (B. t. dalmatinus) and 347, 436 and 538 nm (B. t. sassaricus) for UV, blue and green receptors, respectively. There were no significant differences in UV and blue receptor sensitivities. We found no photoreceptors maximally sensitive to red spectral light in the Sardinian population and model calculations indicate that the behavioural population differences in colour responses cannot be directly explained by receptor population differences. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Animal colour vision--behavioural tests and physiological concepts

Over a century ago workers such as J. Lubbock and K. von Frisch developed behavioural criteria for establishing that non‐human animals see colour. Many animals in most phyla have since then been shown to have colour vision. Colour is used for specific behaviours, such as phototaxis and object recognition, while other behaviours such as motion detection are colour blind. Having established the existence of colour vision, research focussed on the question of how many spectral types of photoreceptors are involved. Recently, data on photoreceptor spectral sensitivities have been combined with behavioural experiments and physiological models to study systematically the next logical question: ‘what neural interactions underlie colour vision ?‘This review gives an overview of the methods used to study animal colour vision, and discusses how quantitative modelling can suggest how photoreceptor signals are combined and compared to allow for the discrimination of biologically relevant stimuli.     

Thermoregulatory differences between phenotypes in the speckled wood butterfly: hot perchers and cold patrollers?

Males of the speckled wood butterfly Pararge aegeria L. (Satyrinae), actively search for females (“patrolling”) or wait for them at particular places (“perching”). Darker males are more likely to patrol than pale ones, which are mainly territorial perchers. We studied whether this morphological variation relates to thermoregulatory differences. The relationship between thoracic temperature and ambient temperature differed between the colour types under natural conditions: darker males had on average lower body temperatures than paler males. Different activities (e.g. resting, flying) and behavioural strategies (perching or patrolling) were associated with differences in thoracic temperature: patrolling males which mainly engaged in long flights and periods of basking afterwards, had lower thoracic temperatures than perching males which engaged in very short flights, fights and basking. When resting for a while thoracic temperatures did not differ between males practising different strategies. Under laboratory conditions, darker males heated up faster than pale males but there was no difference in the thoracic temperature at which they started to fly. These results indicate that thermal requirements (or general conditions) differ between the behavioural strategies, and that behavioural differences between phenotypes (colour types) relate to differences in thermal ecology. This supports the idea that darker males are better adapted to patrolling. There is no evidence that one mate-locating strategy is always superior to the other, which coincides with the observation that both strategies co-exist. More generally, this study shows that relatively small differences in colour can have a considerable effect on thermoregulation and hence on the behavioural strategies a heliothermic insect will adopt. Received: 15 August 1997 / Accepted: 15 December 1997     

Cone pigments in a North American marsupial, the opossum (Didelphis virginiana)

Only two of the four cone opsin gene families found in vertebrates are represented in contemporary eutherian and marsupial species. Recent genetic studies of two species of South American marsupial detected the presence of representatives from two of the classes of cone opsin genes and the structures of these genes predicted cone pigments with respective peaks in the ultraviolet and long-wavelength portions of the spectrum. The Virginia opossum (Didelphis virginiana), a profoundly nocturnal animal, is the only marsupial species found in North America. The prospects for cone-based vision in this species were examined through recordings of the electroretinogram (ERG), a commonly examined retinal response to photic stimulation. Recorded under flickering-light conditions that elicit signals from cone photoreceptors, the spectral sensitivity of the opossum eye is well accounted for by contributions from the presence of a single cone pigment having peak absorption at 561–562 nm. A series of additional experiments that employed various chromatic adaptation paradigms were conducted in a search for possible contributions from a second (short-wavelength sensitive) cone pigment. We found no evidence that such a mechanism contributes to the ERG in this marsupial.     

<Emphasis Type="Italic">Protungulatum</Emphasis>, Confirmed Cretaceous Occurrence of an Otherwise Paleocene Eutherian (Placental?) Mammal

Neither pre-Cenozoic crown eutherian mammals (placentals) nor archaic ungulates (“condylarths”) are known with certainty based on the fossil record. Herein we report a new species of the Paleocene archaic ungulate (“condylarth”) Protungulatum from undisputed Late Cretaceous aged rocks in Montana USA based on an isolated last upper premolar, indicating rare representatives of these common early Tertiary mammals appeared in North America a minimum of 300 k  years before the extinction of non-avian dinosaurs. The other 1200 mammal specimens from the locality are characteristic Late Cretaceous taxa. This discovery overturns the current hypothesis that archaic ungulates did not appear in North America until after the Cretaceous/Tertiary (K/T) boundary and also suggests that other reports of North American Late Cretaceous archaic ungulates may be correct. Recent studies, including ours, cannot determine whether Protungulatum does or does not belong to the crown clade Placentalia.