The effects of dietary carotenoid intake on carotenoid accumulation in the retina of a wild bird, the house finch (Carpodacus mexicanus)

doi:10.1016/j.abb.2010.06.033

Archives of Biochemistry and Biophysics

Volume 504, Issue 1, 1 December 2010, Pages 161-168

https://doi.org/10.1016/j.abb.2010.06.033 Get rights and content

Abstract

Carotenoid pigments accumulate in the retinas of many animals, including humans, where they play an important role in visual health and performance. Recently, birds have emerged as a model system for studying the mechanisms and functions of carotenoid accumulation in the retina. However, these studies have been limited to a small number of domesticated species, and the effects of dietary carotenoid access on retinal carotenoid accumulation have not been investigated in any wild animal species. The purpose of our studies was to examine how variation in dietary carotenoid types and levels affect retinal accumulation in house finches (Carpodacus mexicanus), a common and colorful North American songbird. We carried out three 8-week studies with wild-caught captive birds: (1) we tracked the rate of retinal carotenoid depletion, compared to other body tissues, on a very low-carotenoid diet, (2) we supplemented birds with two common dietary carotenoids (lutein + zeaxanthin) and measured the effect on retinal accumulation, and (3) we separately supplemented birds with high levels of zeaxanthin – an important dietary precursor for retinal carotenoids – or astaxanthin – a dominant retinal carotenoid not commonly found in the diet (i.e. a metabolic derivative). We found that carotenoids depleted slowly from the retina compared to other tissues, with a significant (∼50%) decline observed only after 8 weeks on a very low-carotenoid diet. Supplementation with lutein + zeaxanthin or zeaxanthin alone significantly increased only retinal galloxanthin and ε-carotene levels, while other carotenoid types in the retina remained unaffected. Concentrations of retinal astaxanthin were unaffected by direct dietary supplementation with astaxanthin. These results suggest highly specific mechanisms of retinal carotenoid metabolism and accumulation, as well as differential rates of turnover among retinal carotenoid types, all of which have important implications for visual health maintenance and interventions.

Research highlights

► House finches accumulate high levels of carotenoids in their retinas. ► Retinal carotenoids are relatively stable to depletion. ► Supplementation with dietary zeaxanthin increased the retinal accumulation. ► Only specific retinal carotenoid types (galloxanthin) responded to supplementation. ► These results suggest specific mechanisms of retinal carotenoid uptake and metabolism.

Introduction

Diet-derived carotenoids acting as provitamins, immunomodulators, antioxidants, and/or photoprotectants play an important role in the health and normal physiological function of humans and a diversity of animals [1], [2]. Carotenoids are particularly important for visual health, and increased retinal carotenoid accumulation is associated with a reduced risk of age-related macular degeneration (AMD)¹ and cataract in humans [3], [4]. Carotenoid accumulation in the retina is influenced by carotenoid intake [5], [6], raising the possibility of dietary interventions to promote visual health. However, testing such interventions in humans is difficult, and thus birds have been proposed as a model system for the study of the controls and functions of retinal carotenoids because they accumulate levels of retinal carotenoids comparable to humans [7], [8], [9]. In young quail (Coturnix japonica), for example, dietary carotenoid supplementation elevates retinal carotenoid concentrations, enhances photoprotection, and reduces the accumulation of A2E – a marker of eye disease [8], [9], [10]. However, the mechanisms of accumulation and functions of carotenoids in the avian retina differ from humans in several important aspects. The avian retina contains metabolically derived apo- and keto-carotenoids not found in the human retina, and the majority of carotenoids in the avian retina accumulate in an esterified form [11]. Therefore carotenoid accumulation in the avian retina may be subject to constraints that are not shared by humans.

In the avian retina, carotenoids accumulate within cone oil droplets that are located between the inner and outer segments of the cone photoreceptors. In this position the light absorbance of carotenoids modifies the spectrum and intensity of light reaching the visual pigment. The types and concentrations of carotenoids in the oil droplets are specific to the type of photoreceptor. For example, the long-wavelength-sensitive cone contains a red oil droplet pigmented with astaxanthin, while the short-wavelength sensitive cone oil droplets contain galloxanthin that absorbs light at shorter wavelengths [12]. Thus carotenoid-pigmented oil droplets act as matched filters, enhancing color discrimination and improving color constancy [13]. This specific and matched carotenoid accumulation is achieved through the metabolism and selective accumulation of dietary carotenoids. Avian retinal carotenoids, like galloxanthin, are found only in the eye, suggesting highly localized carotenoid metabolism [11], [14], [15].

Because of their essential role in color vision and photoprotection in the avian eye, variation in retinal carotenoid accumulation could impact color vision, retinal health, and have consequences for an individual’s survival and fitness. However, the influence of diet on retinal carotenoid accumulation is not known for any wild bird or other wild animal species. There have been a number of comparative microspectrophotometric studies of the carotenoid-pigmented cone oil droplets of wild birds [16], and the majority of experimental studies of retinal carotenoid dynamics have been limited to young birds of domesticated species like the chicken (Gallus domesticus) and quail. Studying these selectively bred domesticated species makes it difficult to place these results in a natural context and limits our ability to examine the evolutionary forces shaping retinal carotenoid accumulation.

To expand these investigations to wild birds, we have initiated a series of studies on retinal carotenoids in the house finch (Carpodacus mexicanus), a common North American passerine bird. This species is sexually dimorphic, with sexually selected carotenoid-based male plumage coloration, and has become a model species for the study of carotenoid physiology in wild birds [17]. We have found that carotenoid levels in the retinas of wild house finches vary among seasons, and positively correlate with body condition and male coloration [18]. The purpose of the current study is to examine how dietary carotenoid intake affects accumulation of specific retinal carotenoids and may shape the variation we have seen in the wild population. We carried out three separate experiments with captive wild-caught house finches to determine: (1) the time course of retinal carotenoid depletion, as animals are being fed a very low-carotenoid diet, (2) how supplemental levels of two common dietary carotenoids (lutein and zeaxanthin) affect retinal carotenoid accumulation, and (3) the effect of separate high doses of two abundant carotenoids in the avian retina – zeaxanthin (the main carotenoid in medium-wavelength-sensitive cones and precursor of other metabolically derived carotenoids in the quail retina [11]) or astaxanthin (the metabolic derivative that pigments the oil droplets associated with the long-wave-sensitive cones) – on retinal carotenoid accumulation.

Section snippets

Chemicals

Solvents for carotenoid extraction and high-performance liquid chromatography (HPLC) analyses were purchased from Fisher Scientific (Waltham, MA). Purified standards of lutein and β-carotene were acquired from CaroteNature (Lupsingen, Switzerland), astaxanthin from Sigma–Aldrich (St. Louis, MO), and zeaxanthin from DSM (Heerlen, Netherlands). A diet supplement of combined lutein and zeaxanthin (OroGlo-15® containing 15 g/kg of 8.2:1, lutein:zeaxanthin) was donated by Kemin Inc. (Des Moines, IA).

Retina and plasma carotenoid types

Consistent with our previous studies [18], [22], we observed six major carotenoid types in house finch retinas from all three experiments (Table 1). The retinal carotenoid profile was dominated by astaxanthin and galloxanthin, together making up on average >75% of total retinal carotenoids. The plasma carotenoid profile of wild house finches was dominated by lutein and zeaxanthin, with small amounts of β-cryptoxanthin and β-carotene making up <5% of total at the time of capture (Table 1). On

Carotenoid types and concentration

The carotenoid profile of the wild house finch retina was dominated by astaxanthin and galloxanthin, making up 42% and 35% of total, respectively. This is roughly similar to the turkey (Meleagris gallopavo), consisting of 23% astaxanthin and 28% galloxanthin [14], but contrasts with results from domesticated chickens (Gallus domesticus) with 71% and 7%, respectively and quail with 29% and 13%, respectively. These species-specific differences could stem from: (1) variation in the frequency of

Conclusion

Carotenoid accumulation in the retina varies significantly among adult wild house finches and correlates with condition and male carotenoid-based plumage coloration [18]. The studies presented here suggest that, although dietary carotenoid access does affect retinal accumulation, diet is not the primary source of variation observed among wild birds. Compared to other body tissues, retinal accumulation in adult house finches is relatively stable to dietary changes over time, and carotenoid

Acknowledgments

This work was supported financially by the National Science Foundation (IOS-0910357 and 0923694), the American Ornithologist Union, and the Animal Behavior Society. Birds were captured and housed under United States Fish and Wildlife Service permit #MB088806-1, and Arizona State Game and Fish scientific collecting permit SP727468. All experimental procedures were approved by the Institutional Animal Care and Use Committee at Arizona State University (protocol #09-1054R and 06-874R). We would

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The effects of dietary carotenoid intake on carotenoid accumulation in the retina of a wild bird, the house finch (Carpodacus mexicanus)

Abstract

Research highlights

Introduction

Section snippets

Chemicals

Retina and plasma carotenoid types

Carotenoid types and concentration

Conclusion

Acknowledgments

Arch. Biochem. Biophys.

Exp. Eye Res.

Arch. Biochem. Biophys.

Vision Res.

Prog. Retin. Eye Res.

Vision Res.

Vision Res.

Comp. Biochem. Physiol.

Exp. Eye Res.

Exp. Eye Res.

Annu. Rev. Nutr.

J. Nutr.

J. Nutr.

Invest. Ophthalmol. Vis. Sci.

Nutr. Metab.

Invest. Ophthalmol. Vis. Sci.

Invest. Ophthalmol. Vis. Sci.

Biochemistry

Proc. R. Soc. B