Wild hummingbirds can use the geometry of a flower array.

Animals use cues from their environment to orient in space and to navigate their surroundings. Geometry is a cue whose informational content may originate from the metric properties of a given environment, and its use has been demonstrated in the laboratory in nearly every species of animal tested. However, it is not clear whether geometric information, used by animals typically tested in small, rectangular boxes, is directly relevant to animals in their natural environment. Here we present the first data that confirm the use of geometric cues by a free-living animal in the wild. We trained rufous hummingbirds to visit a rectangular array of four artificial flowers, one of which was rewarded. In some trials a conspicuous landmark cued the reward. Following array translocation and rotation, we presented hummingbirds with three tests. When trained and tested with the landmark, or when trained and tested without it, hummingbirds failed to show geometric learning. However, when trained with a landmark but tested without it, hummingbirds produced the classic geometric response, showing that they had learned the geometric relationships (distance and direction) of several non-reward visual elements of the environment. While it remains that the use of geometry to relocate a reward may be an experimental artefact, its use is not confined to the laboratory.

Wild, free-living rufous hummingbirds do not use geometric cues in a spatial task.

In the laboratory, many species orient themselves using the geometric properties of an enclosure or array and geometric information is often preferred over visual cues. Whether animals use geometric cues when relocating rewarded locations in the wild, however, has rarely been investigated. We presented free-living rufous hummingbirds with a rectangular array of four artificial flowers to investigate learning of rewarded locations using geometric cues. In one treatment, we rewarded two of four flowers at diagonally opposite corners. In a second treatment, we provided a visual cue to the rewarded flower by connecting the flowers with "walls" consisting of four dowels (three white, one blue) laid on the ground connecting each of the flowers. Neither treatment elicited classical geometry results; instead, hummingbirds typically chose one particular flower over all others. When we exchanged that flower with another, hummingbirds tended to visit the original flower. These results suggest that (1) hummingbirds did not use geometric cues, but instead may have used a visually derived cue on the flowers themselves, and (2) using geometric cues may have been more difficult than using visual characteristics. Although hummingbirds typically prefer spatial over visual information, we hypothesize that they will not use geometric cues over stable visual features but that they make use of small, flower-specific visual cues. Such cues may play a more important role in foraging decisions than previously thought.

The influence of chromatic background on the photosensitivity of tilapia erythrophores.

Non-mammalian vertebrates and invertebrates use extraretinal photoreceptors to detect light and perform diverse non-image-forming functions. Compared to well-studied visual systems, the effect of ambient light conditions on photosensory systems of extraretinal photoreceptors is poorly understood. Chromatophores are photosensitive dermal pigment cells that play an important role in the formation of body color patterns to fit the surrounding environment. Here, we used tilapia erythrophores to investigate the relationship between environmental light and chromatophore photoresponses. All erythrophores from three spectral conditions aggregated their pigment granules in UV/short wavelengths and dispersed in middle/long wavelengths. Unlike retinal visual systems, environmental light did not change the usage of the primary opsins responsible for aggregation and dispersion. In addition, short wavelength-rich and red-shifted background conditions led to an inhibitory effect on erythrophore photoresponses. We suggest that, as extraretinal photoreceptors for non-image-forming functions, chromatophores directly adjust their photoresponse sensitivity via changes in opsin expression levels rather than opsin types when environmental light changes.

Feedback from horizontal cells to cones mediates color induction and may facilitate color constancy in rainbow trout.

Color vision is most beneficial when the visual system is color constant and can correct the excitations of photoreceptors for differences in environmental irradiance. A phenomenon related to color constancy is color induction, where the color of an object shifts away from the color of its surroundings. These two phenomena depend on chromatic spatial integration, which was suggested to originate at the feedback synapse from horizontal cells (HC) to cones. However, the exact retinal site was never determined. Using the electroretinogram and compound action potential recordings, we estimated the spectral sensitivity of the photoresponse of cones, the output of cones, and the optic nerve in rainbow trout. Recordings were performed before and following pharmacological inhibition of HC-cone feedback, and were repeated under two colored backgrounds to estimate the efficiency of color induction. No color induction could be detected in the photoresponse of cones. However, the efficiency of color induction in the cone output and optic nerve was substantial, with the efficiency in the optic nerve being significantly higher than in the cone output. We found that the efficiency of color induction in the cone output and optic nerve decreased significantly with the inhibition of HC-cone feedback. Therefore, our findings suggest not only that color induction originates as a result of HC-cone feedback, but also that this effect of HC-cone feedback is further amplified at downstream retinal elements, possibly through feedback mechanisms at the inner plexiform layer. This study provides evidence for an important role of HC-cone feedback in mediating color induction, and therefore, likely also in mediating color constancy.

Modulation of environmental light alters reception and production of visual signals in Nile tilapia.

Signal reception and production form the basis of animal visual communication, and are largely constrained by environmental light. However, the role of environmental light in producing variation in either signal reception or production has not been fully investigated. To chart the effect of environmental light on visual sensitivity and body colouration throughout ontogeny, we measured spectral sensitivity, lens transmission and body pattern reflectance from juvenile and adult Nile tilapia held under two environmental light treatments. Spectral sensitivity in juveniles reared under a broad-spectrum light treatment and a red-shifted light treatment differed mostly at short wavelengths, where the irradiance of the two light treatments differed the most. In contrast, adults held under the same two light treatments did not differ in spectral sensitivity. Lens transmission in both juveniles and adults did not differ significantly between environmental light treatments, indicating that differences in spectral sensitivity of juveniles originated in the retina. Juveniles and adults held under the two environmental light treatments differed in spectral reflectance, and adults transferred to a third, white light treatment differed in spectral reflectance from their counterparts held under the two original treatments. These results demonstrate that environmental light plays a crucial role in shaping signal reception in juveniles and signal production throughout ontogeny, reinforcing the notion that environmental light has the capacity to influence animal communication, and suggesting that the characteristics of environmental light should be considered in models of ecological speciation.