Metric Analysis of Threshold Spectral Sensitivity in the Honeybee

AbstractBehavioral spectral sensitivity curves are frequently used to characterize peripheral stages of visual processing. We test specific hypotheses about the physiology underlying honeybee spectral sensitivity by approximating published sensitivity curves with several metric models. The analysis shows that: (1) models assuming no interactions between different receptor types do not explain the behavioral data. Similarly, neither simple luminance mechanism models (sum of receptor excitations), nor models in which only the most sensitive receptor determines sensitivity fit the data. (2) The minimum number of postreceptoral mechanisms mediating discrimination is two. (3) Both mechanisms are of the chromatic type. Adding an achromatic mechanism decreases the accuracy of approximation. Copyright © 1997 Elsevier Science Ltd

Are fruit colors adapted to consumer vision and birds equally efficient in detecting colorful signals?

Reproduction in plants often requires animal vectors. Fruit and flower colors are traditionally viewed as an adaptation to facilitate detection for pollinators and seed dispersers. This long-standing hypothesis predicts that fruits are easier to detect against their own leaves compared with those of different species. We tested this hypothesis by analyzing the chromatic contrasts between 130 bird-dispersed fruits and their respective backgrounds according to avian vision. From a bird's view, fruits are not more contrasting to their own background than to those of other plant species. Fruit colors are therefore not adapted toward maximized conspicuousness for avian seed dispersers. However, secondary structures associated with fruit displays increase their contrasts. We used fruit colors to assess whether the ultraviolet and violet types of avian visual systems are equally efficient in detecting color signals. In bright light, the chromatic contrasts between fruit and background are stronger for ultraviolet vision. This advantage is due to the lesser overlap in spectral sensitivities of the blue and ultraviolet cones, which disappears in dim light conditions. We suggest that passerines with ultraviolet cones might primarily use epigamic signals that are less conspicuous to their avian predators (presumably with violet vision). Possible examples for such signals are carotenoid-based signals

Approach Direction Prior to Landing Explains Patterns of Colour Learning in Bees

Gaze direction is closely coupled with body movement in insects and other animals. If movement patterns interfere with the acquisition of visual information, insects can actively adjust them to seek relevant cues. Alternatively, where multiple visual cues are available, an insect’s movements may influence how it perceives a scene. We show that the way a foraging bumblebee approaches a floral pattern could determine what it learns about the pattern. When trained to vertical bicoloured patterns, bumblebees consistently approached from below centre in order to land in the centre of the target where the reward was located. In subsequent tests, the bees preferred the colour of the lower half of the pattern that they predominantly faced during the approach and landing sequence. A predicted change of learning outcomes occurred when the contrast line was moved up or down off-centre: learned preferences again reflected relative frontal exposure to each colour during the approach, independent of the overall ratio of colours. This mechanism may underpin learning strategies in both simple and complex visual discriminations, highlighting that morphology and action patterns determines how animals solve sensory learning tasks. The deterministic effect of movement on visual learning may have substantially influenced the evolution of floral signals, particularly where plants depend on fine-scaled movements of pollinators on flowers

Visual ecology of the Australian lungfish (Neoceratodus forsteri)

Background. The transition from water to land was a key event in the evolution of vertebrates that occurred over a period of 15-20 million years towards the end of the Devonian. Tetrapods, including all land-living vertebrates, are thought to have evolved from lobe-finned (sarcopterygian) fish that developed adaptations for an amphibious existence. However, while many of the biomechanical and physiological modifications necessary to achieve this feat have been studied in detail, little is known about the sensory adaptations accompanying this transition. In this study, we investigated the visual system and visual ecology of the Australian lungfish Neoceratodus forsteri, which is the most primitive of all the lungfish and possibly the closest living relative to the ancestors of tetrapods. Results. Juvenile Neoceratodus have five spectrally distinct retinal visual pigments. A single type of rod photoreceptor contains a visual pigment with a wavelength of maximum absorbance (max) at 540 nm. Four spectrally distinct single cone photoreceptors contain visual pigments with max at 366 (UVS), 479 (SWS), 558 (MWS) and 623 nm (LWS). No double cones were found. Adult lungfish do not possess UVS cones and, unlike juveniles, have ocular media that prevent ultraviolet light from reaching the retina. Yellow ellipsoidal/paraboloidal pigments in the MWS cones and red oil droplets in the LWS cones narrow the spectral sensitivity functions of these photoreceptors and shift their peak sensitivity to 584 nm and 656 nm, respectively. Modelling of the effects of these intracellular spectral filters on the photoreceptor colour space of Neoceratodus suggests that they enhance their ability to discriminate objects, such as plants and other lungfishes, on the basis of colour. Conclusion. The presence of a complex colour vision system based on multiple cone types and intracellular spectral filters in lungfishes suggests that many of the ocular characteristics seen in terrestrial or secondarily aquatic vertebrates, such as birds and turtles, may have evolved in shallow water prior to the transition onto land. Moreover, the benefits of spectral filters for colour discrimination apply equally to purely aquatic species as well as semi-aquatic and terrestrial animals. The visual system of the Australian lungfish resembles that of terrestrial vertebrates far more closely than that of other sarcopterygian fish. This supports the idea that lungfishes, and not the coelacanth, are the closest living relatives of the ancestors of tetrapods

Enhanced UV-Reflection Facilitated a Shift in the Pollination System of the Red Poppy, Papaver rhoeas (Papaveraceae)

Evolutionary change is considered a major factor influencing the invasion of new habitats by plants. Yet, evidence on how such modifications promote range expansion remains rather limited. Here we investigated flower color modifications in the red poppy, Papaver rhoeas (Papaveraceae), as a result of its introduction into Central Europe and the impact of those modifications on its interactions with pollinators. We found that while flowers of Eastern Mediterranean poppies reflect exclusively in the red part of the spectrum, those of Central European poppies reflect both red and ultraviolet (UV) light. This change coincides with a shift from pollination by glaphyrid beetles (Glaphyridae) to bees. Glaphyrids have red-sensitive photoreceptors that are absent in bees, which therefore will not be attracted by colors of exclusively red-reflecting flowers. However, UV-reflecting flowers are easily detectable by bees, as revealed by visual modeling. In the North Mediterranean, flowers with low and high UV reflectance occur sympatrically. We hypothesize that Central European populations of P. rhoeas were initially polymorphic with respect to their flower color and that UV reflection drove a shift in the pollination system of P. rhoeas that facilitated its spread across Europe

The variable colours of the fiddler crab Uca vomeris and their relation to background and predation

Colour changes in fiddler crabs have long been noted, but a functional interpretation is still lacking. Here we report that neighbouring populations of Uca vomeris in Australia exhibit different degrees of carapace colours, which range from dull mottled to brilliant blue and white. We determined the spectral characteristics of the mud substratum and of the carapace colours of U. vomeris and found that the mottled colours of crabs are cryptic against this background, while display colours provide strong colour contrast for both birds and crabs, but luminance contrast only for a crab visual system. We tested whether crab populations may become cryptic under the influence of bird predation by counting birds overflying or feeding on differently coloured colonies. Colonies with cryptically coloured crabs indeed experience a much higher level of bird presence, compared to colourful colonies. We show in addition that colourful crab individuals subjected to dummy bird predation do change their body colouration over a matter of days. The crabs thus appear to modify their social signalling system depending on their assessment of predation risk

An Ishihara-style test of animal colour vision

ABSTRACT Colour vision mediates ecologically relevant tasks for many animals, such as mate choice, foraging and predator avoidance. However, our understanding of animal colour perception is largely derived from human psychophysics, and behavioural tests of non-human animals are required to understand how colour signals are perceived. Here, we introduce a novel test of colour vision in animals inspired by the Ishihara colour charts, which are widely used to identify human colour deficiencies. In our method, distractor dots have a fixed chromaticity (hue and saturation) but vary in luminance. Animals can be trained to find single target dots that differ from distractor dots in chromaticity. We provide MATLAB code for creating these stimuli, which can be modified for use with different animals. We demonstrate the success of this method with triggerfish, Rhinecanthus aculeatus, which quickly learnt to select target dots that differed from distractor dots, and highlight behavioural parameters that can be measured, including success of finding the target dot, time to detection and error rate. We calculated discrimination thresholds by testing whether target colours that were of increasing colour distances (ΔS) from distractor dots could be detected, and calculated discrimination thresholds in different directions of colour space. At least for some colours, thresholds indicated better discrimination than expected from the receptor noise limited (RNL) model assuming 5% Weber fraction for the long-wavelength cone. This methodology could be used with other animals to address questions such as luminance thresholds, sensory bias, effects of sensory noise, colour categorization and saliency

Colour discrimination thresholds vary throughout colour space in a reef fish (Rhinecanthus aculeatus)

Animals use colour vision in a range of behaviours. Visual performance is limited by thresholds, which are set by noise in photoreceptors and subsequent neural processing. The receptor noise limited (RNL) model of colour discrimination is widely used for modelling colour vision and accounts well for experimental data from many species. In one of the most comprehensive tests yet of colour discrimination in a non-human species, we used Ishihara-style stimulus patterns to examine thresholds for 21 directions at five locations in colour space for the fish Rhinecanthus aculeatus. Thresholds matched RNL model predictions most closely for stimuli near the achromatic point, but exceeded predictions (indicating a decline in sensitivity) with distance from this point. Thresholds were also usually higher for saturation than for hue differences. These changes in colour threshold with colour space location and direction may give insight into photoreceptor non-linearities and postreceptoral mechanisms of colour vision in fish. Our results highlight the need for a cautious interpretation of the RNL model – especially for modelling colours that differ from one another in saturation (rather than hue), and for highly saturated colours distant from the achromatic point in colour space

Complementary shifts in photoreceptor spectral tuning unlock the full adaptive potential of ultraviolet vision in birds

Color vision in birds is mediated by four types of cone photoreceptors whose maximal sensitivities (λmax) are evenly spaced across the light spectrum. In the course of avian evolution, the λmax of the most shortwave-sensitive cone, SWS1, has switched between violet (λmax > 400 nm) and ultraviolet (λmax < 380 nm) multiple times. This shift of the SWS1 opsin is accompanied by a corresponding short-wavelength shift in the spectrally adjacent SWS2 cone. Here, we show that SWS2 cone spectral tuning is mediated by modulating the ratio of two apocarotenoids, galloxanthin and 11',12'-dihydrogalloxanthin, which act as intracellular spectral filters in this cell type. We propose an enzymatic pathway that mediates the differential production of these apocarotenoids in the avian retina, and we use color vision modeling to demonstrate how correlated evolution of spectral tuning is necessary to achieve even sampling of the light spectrum and thereby maintain near-optimal color discrimination

Importance of Achromatic Contrast in Short-Range Fruit Foraging of Primates

Trichromatic primates have a ‘red-green’ chromatic channel in addition to luminance and ‘blue-yellow’ channels. It has been argued that the red-green channel evolved in primates as an adaptation for detecting reddish or yellowish objects, such as ripe fruits, against a background of foliage. However, foraging advantages to trichromatic primates remain unverified by behavioral observation of primates in their natural habitats. New World monkeys (platyrrhines) are an excellent model for this evaluation because of the highly polymorphic nature of their color vision due to allelic variation of the L-M opsin gene on the X chromosome. In this study we carried out field observations of a group of wild, frugivorous black-handed spider monkeys (Ateles geoffroyi frontatus, Gray 1842, Platyrrhini), consisting of both dichromats (n = 12) and trichromats (n = 9) in Santa Rosa National Park, Costa Rica. We determined the color vision types of individuals in this group by genotyping their L-M opsin and measured foraging efficiency of each individual for fruits located at a grasping distance. Contrary to the predicted advantage for trichromats, there was no significant difference between dichromats and trichromats in foraging efficiency and we found that the luminance contrast was the main determinant of the variation of foraging efficiency among red-green, blue-yellow and luminance contrasts. Our results suggest that luminance contrast can serve as an important cue in short-range foraging attempts despite other sensory cues that could be available. Additionally, the advantage of red-green color vision in primates may not be as salient as previously thought and needs to be evaluated in further field observations