Avian retinal oil droplets: dietary manipulation of colour vision?

Abstract

Avian vision is highly developed, with bird retinas containing rod and double-cone photoreceptors, plus four classes of single cones subserving tetrachromatic colour vision. Cones contain an oil droplet, rich in carotenoid pigments (except VS/ultraviolet-sensitive cones), that acts as a filter, substantially modifying light detected by the photoreceptor. Using dietary manipulations, we tested the effects of carotenoid availability on oil droplet absorbance properties in two species: Platycercus elegans and Taeniopygia guttata. Using microspectrophotometry, we determined whether manipulations affected oil droplet carotenoid concentration and whether changes would alter colour discrimination ability. In both species, increases in carotenoid concentration were found in carotenoid-supplemented birds, but only in the double cones. Magnitudes of effects of manipulations were often dependent on retinal location. The study provides, to our knowledge, the first experimental evidence of dietary intake over a short time period affecting carotenoid concentration of retinal oil droplets. Moreover, the allocation of carotenoids to the retina by both species is such that the change potentially preserves the spectral tuning of colour vision. Our study generates new insights into retinal regulation of carotenoid concentration of oil droplets, an area about which very little is known, with implications for our understanding of trade-offs in carotenoid allocation in birds.

Figure 1.

Effect in P. elegans subjects of carotenoid-supplemented (solid black line), energy-restricted (light grey line) and control (light grey dashed line) treatments on (a) weight and (b) plasma carotenoid concentration. (c) Taeniopygia guttata plasma carotenoid concentration for each treatment at the beginning of the experimental treatments and sacrifice at six weeks: carotenoid group (solid black line) and control group (light grey line). Error bars in both panels represent ±1 s.e.

Figure 2.

Normalized absorbance spectra of P. elegans oil droplets: (a) single cones and (b) double cones. In (a), C-type (light grey line); Y-type (dark grey line); R-type (solid black line). In (b), single peak (light grey dashed line); double peak (dark grey dashed line); 100% absorbance double peak (solid black line). Single-cone spectra from (a) are also representative of those measured in T. guttata. In (b), only single-peak spectra (light grey dashed line) were measured in double cones of T. guttata.

Figure 3.

Mean difference in λ_cut (Δλ_cut) of carotenoid (black shaded boxes) and energy-restricted (grey shaded boxes) treatments from control (treatment minus control) shown separately for each droplet type in P. elegans. Single cones: (a) R-type, (b) Y-type and (c) C-type; double cones: (d) single-peak P-type and (e) double-peak P-type. Data are grouped by retinal sector (anterior, dorsal, posterior and ventral). Error bars represent ±1 s.e.

Figure 4.

Difference in mean λ_cut (Δλ_cut) between carotenoid and control treatments (carotenoid minus control) shown separately for each droplet type in T. guttata: (a) R-type, (b) Y-type, (c) C-type and (d) P-type. Data are grouped by retinal sector (dorsal and ventral). Error bars represent ±1 s.e.

Figure 5.

Effect of oil droplet filtering on visual pigment spectra for R-type droplets for each treatment: Govardovskii template curve for P. elegans LWS visual pigment (black dashed line); cone sensitivity spectrum after filtering by mean λ_cut from carotenoid-supplemented treatment (dark grey line); cone sensitivity spectrum after filtering by mean λ_cut from energy-restricted treatment (light grey line). The curves shown are for mean λ_cut values from P. elegans posterior sector, which showed the largest difference in λ_cut after the experimental treatments (figure 3).

Figure 6.

P-type oil droplet spectra from P. elegans: single peak (light grey line); double peak (dark grey line); 100% absorbance double peak (solid black line), with associated Govardovskii template curve for P. elegans LWS visual pigment spectrum (black dashed line).