Abstract

Giant clams utilize two mechanisms to produce white coloration analogous to that from RGB pixelated electro-optical displays. In the first, the mixed reflection from tight clusters of differently colored iridescent cells yields white. In the second, cells containing subcellular Bragg reflectors with heterogeneous lamellar spacings reflect multiple wavelengths to appear white at the macroscopic scale. Both mechanisms represent unique systems of structural color that produce white by color mixing.

© 2016 Optical Society of America

Animals exhibit a wide range of pigmented and structural coloration [13]. White coloration is most commonly produced by one of a few mechanisms: broadband reflectance from strong scattering within cells [4,5], variations in the lamellar dimensions and spacings of Bragg reflectors [68], or broadband scattering from wavelength-scale particles [6,9,10]. Giant clams (of the genera Tridacna and Hippopus) display vibrant colors in their exposed epithelia, which is the result of reflection from Bragg lamellae in specialized cells called iridocytes [11,12]. Constructive interference from the multiple, alternating lamellae of high and low refractive index within these spherical cells produces the intense blues, greens, and golds characteristic of these animals’ appearance [1315]. In some specimens, however, white regions or stripes also are evident. We describe here two mechanisms used by different species of giant clams to produce white coloration that prove to be directly analogous to the red-green-blue (RGB) pixel strategy of modern electro-optical technology. In the first, a collection of iridocytes in close proximity each reflects a different, specific color, with reflection from the assembly appearing white; in the second, some iridocytes are individually multicolored themselves as a result of subcellular variations in their Bragg lamellar dimensions.

Tridacna maxima and Tridacna derasa specimens were purchased live (LiveAquaria.com, Rhinelander, WI, USA) and shipped overnight to the University of California at Santa Barbara, where they were maintained in seawater at 24°C–26°C. Fresh specimens were photographed, the shells opened, and the tissue dissected (Fig. 1). Small samples (5mm×5mm) were cut from the mantle epithelium [e.g., from the region circled in red in Figs. 1(b) and 1(d)], placed on microscope slides, hydrated with buffered artificial seawater (ASW, 470 mM NaCl, 10 mM KCl, 27 mM MgCl2, 29 mM MgSO4, 11 mM CaCl2, 10 mM HEPES, pH 7.8) and covered with a #1 glass cover slip.

 figure: Fig. 1.

Fig. 1. (a) Juvenile T. maxima giant clam (6 cm) showing reflective epithelium of the mantle overlapping the shell. (b) Close-up of specimen shown in (a). (c) Dissected juvenile T. derasa (5 cm) showing numerous white stripes in mantle epithelium. (d) Close-up of the epithelium shown in (c); prominent white stripes are 12mm wide ×5mm long. Red circles indicate white areas analyzed.

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Samples thus prepared were placed on the stage of a Zeiss AxioObserver D1M inverted microscope (Carl Zeiss AG, Oberkochen, Germany) for imaging and microspectrophotometry (Fig. 2); a broadband halogen lamp (providing ample light in the measured range of 400–700 nm) provided illumination. For spectroscopy, a small region (1μm diameter) of the sample was imaged on the entrance slit (0.2 mm width) of an imaging spectrometer (Horiba JobinYvon iHR320, Horiba Group, Kyoto, Japan), with light entering the spectrometer dispersed horizontally by a grating (150 lines/mm, blazed for 500 nm) and the resulting image captured with a thermoelectrically cooled silicon charge-coupled device (Horiba JobinYvon Synapse detector) using an integration time of 0.05 s. Spectra were obtained from areas less than those of single iridocytes and normalized to a calibrated specular reflectivity standard (Ocean Optics STAN-SSH), and the normalized reflectivity was used for analyses. The 50× objective was a Zeiss EC EpiPlan-NEOFLUAR lens with numerical aperture of 0.8 and 3.8 μm depth of field; other details of the microspectrophotometer and the method of analysis were as described previously [16]. Noise in the short- and long-wavelength regimes is the result of low reflected signal at those wavelengths. Dark-field microscopy was performed in reflection mode with a 20× or 50× microscope objective and a Zeiss AxioCam ICC color camera.

 figure: Fig. 2.

Fig. 2. Schematic of illumination and light collection used to obtain bright-field images and high-resolution microspectrophotometric measurements [16].

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The regions of white reflectance observed in the epithelia of Tridacna maxima are typically broad and diffuse, while those in T. derasa are stripes (cf. Fig. 1). When reflectance from the white area in the T. maxima epithelium shown in Fig. 1(b) is examined at higher magnification (Figs. 3 and 4), it is clear that the apparent white coloration is the result of the aggregate reflection from a large cluster of iridocyte cells, each 510μm in diameter and each reflecting a specific color in the visible spectrum.

 figure: Fig. 3.

Fig. 3. Magnified views of a white region in T. maxima epithelium, shown in Fig. 1(b), imaged in dark-field reflectance mode. (a) Low-magnification, with each individual bright spot revealing an individual iridocyte. (b) Higher-magnification view of the same region. Dotted circles indicate sample areas of light collection for microspectrophotometric analysis of reflectance from individual iridocytes.

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 figure: Fig. 4.

Fig. 4. Examples of iridocytes of various colors from the white region shown in Fig. 1(b) from which spectra were obtained.

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Individual iridocytes from the white region indicated in Fig. 1(b) were selected for spectral analysis, with representative areas of light collection as indicated in Fig. 3(b). Examples of well-separated iridocytes selected for these analyses, permitting spectroscopic measurements from individual iridocytes free of confounding reflectance from neighboring cells, are shown in Fig. 4. A typical spectrum of reflectance from one of these iridocytes [Fig. 5(a)] exhibits a well-defined peak in the visible wavelength range. The wide range of wavelengths and reflectance maxima from such reflectance peaks from multiple iridocytes are shown in Fig. 5(b), with peak wavelengths varying over most of the visible range from 420 to >600nm.

 figure: Fig. 5.

Fig. 5. (a) Typical spectrum from single iridocyte from a white region in T. maxima mantle epithelium. (b) Peak reflectivity and wavelength from spectra from multiple isolated iridocytes from the white region as analyzed in (a).

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Results of comparable analyses of the white stripes on T. derasa are quite different. Microscopic images in dark-field reflectance mode show that individual iridocytes become resolvable at successively increasing levels of magnification (Fig. 6). These iridocytes are positioned close together [Figs. 6(b) and 6(c)]; isolated iridocytes, while rare, can be seen on the edges of the white stripe.

 figure: Fig. 6.

Fig. 6. Iridocytes in a white stripe from T. derasa, imaged at increasing levels of magnification in dark-field reflectance mode.

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Spectra from regions 1μm in diameter were obtained from individual iridocytes from the white stripe of the T. derasa in the same manner as described above (Fig. 7). Each panel in Fig. 7 shows multiple spectra collected from different areas within a single iridocyte. Care was taken to ensure that each set was from a single iridocyte by only using spectra from regions that were separated by less than a single cell diameter (spectral location separation <5μm, cell diameter 5–10 μm). As seen from the spectral peaks in Figs. 7(a)7(e), the small diameter of the collection spot allowed us to analyze multiple areas of different, single colors within single iridocytes. However, an example of the very dense spatial variation in color is seen in Fig. 7(f), where the small but finite size of the spectrometer’s entrance slit results in spectra with multiple peaks corresponding to multiple Bragg stacks contributing to the reflection observed.

 figure: Fig. 7.

Fig. 7. Spectra from individual iridocytes from a white stripe from T. derasa, as seen in Fig. 6. Spectra with single peaks are rare because each iridocyte displays multiple colors.

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Figures 1(b) and 1(d) show representative regions of the epithelia of two species of giant clams that both appear white. But when examined in detail, these reveal very different origins of their white reflectance.

The white region in T. maxima in Fig. 3 (and the accompanying spectral peaks in Fig. 5) is shown to consist of a collection of iridocytes that each reflects a single, specific color, the collection of iridocytes which spans the visible spectrum. Figure 5(b) clearly shows that the spectral peaks of the individual iridocytes span most of the visible spectrum, ranging from 400 to beyond 600 nm.

In contrast, the white areas of T. derasa are shown in Fig. 6 to be composed of a collection of iridocytes in which each individual iridocyte displays spectra of multiple colors (Fig. 7), each originating from spatially distinct subcellular regions. Figure 7(a) shows two spectra from one iridocyte, with individual peaks at 500 and 550 nm. Similarly, Fig. 7(b) shows four spatially resolvable reflectance spectra from another single iridocyte, with peaks at 460, 500, 550, and 575 nm. Similar variations in spectra from single iridocytes are seen in Figs. 7(c)7(e). While spectra from individual Bragg stacks within a single iridocyte were thus often visible and separable, this was not always the case. For example, Fig. 7(f) shows spectra from a single iridocyte in which each individual spectrum displays not one but multiple peaks at 525, 565, 585, and 600 nm, originating from variations in the lamellar spacings of Bragg stacks in very close proximity within a single iridocyte.

White coloration in the epithelia of mollusks was previously shown to be produced by two general mechanisms. One involves Bragg reflectors composed of lamellae that vary significantly in dimension, resulting in either flat white [8] or silvery [17,18] broadband reflection. The second involves not reflective interfaces but scattering structures in cells [9,10]. These latter systems include both fixed and tunable intracellular vesicles, 510μm in diameter, that scatter light over a broad wavelength range. The white reflectance from giant clam epithelia reported here results from the mixing of colors from closely located punctate sources, either comprising discrete cells or within single cells. As described in detail elsewhere, the apparent physiological functions of this reflectance from cells in the epithelia of giant clams includes protection from high solar photon flux [11,12] and a recently discovered Mie-scattering augmentation of the photosynthetic capacity of the animal’s symbiotic microalgae [15]. Detailed simulations supporting these observations are in review for publication elsewhere (Ghoshal et al., unpublished observations). The mechanisms of white reflectance we have analyzed can contribute to both of these functions.

We conclude that the white color of the epithelial cells of two species of giant clams is produced by two different mechanisms, both based on the reflectance of multiple colors. In Tridacna maxima, clusters of iridocytes that reflect different colors, like clusters of RGB pixels, produce the white color. In T. derasa, the same effect is produced from iridocytes that each contain multiple Bragg stacks with different lamellar spacings, reflecting multiple colors seen as white in aggregate. While variations of this second mechanism have been seen in other types of mollusks [8], this is the first observation of biological RGB-like pixelation to yield white reflectance of which we are aware.

Funding

Institute for Collaborative Biotechnologies; U.S. Army Research Office (ARO) (W911NF-09-0001, W911NF-10-1-0139).

Acknowledgment

This research was supported by the Institute for Collaborative Biotechnologies through grants W911NF-09-0001 and W911NF-10-1-0139 from the U.S. Army Research Office.

REFERENCES

1. T. W. Cronin, S. Johnsen, N. J. Marshall, and E. J. Warrant, Visual Ecology (Princeton University, 2014).

2. S. Berthier, Iridescences (Springer, 2007).

3. H. Simon, The Splendor of Iridescence: Structural Colors in the Animal World, 1st ed. (Dodd, Mead & Company, 1971).

4. P. Vukusic, B. Hallam, and J. Noyes, Science 315, 348 (2007). [CrossRef]  

5. S. M. Luke, B. T. Hallam, and P. Vukusic, Appl. Opt. 49, 4246 (2010). [CrossRef]  

6. L. M. Mäthger, E. J. Denton, N. J. Marshall, and R. T. Hanlon, J. R. Soc. Interface 6, S149 (2009). [CrossRef]  

7. T.-H. Chiou, L. M. Mäthger, R. T. Hanlon, and T. W. Cronin, J. Exp. Biol. 210, 3624 (2007). [CrossRef]  

8. G. R. R. Bell, L. M. Mäthger, M. Gao, S. L. Senft, A. M. Kuzirian, G. W. Kattawar, and R. T. Hanlon, Adv. Mater. 26, 4352 (2014). [CrossRef]  

9. L. M. Mäthger, S. L. Senft, M. Gao, S. Karaveli, G. R. R. Bell, R. Zia, A. M. Kuzirian, P. B. Dennis, W. J. Crookes-Goodson, R. R. Naik, G. W. Kattawar, and R. T. Hanlon, Adv. Funct. Mater. 23, 3980 (2013). [CrossRef]  

10. D. G. DeMartini, A. Ghoshal, E. Pandolfi, A. T. Weaver, M. Baum, and D. E. Morse, J. Exp. Biol. 216, 3733 (2013). [CrossRef]  

11. S. Kawaguti, Biol. J. Okayama Univ. 12, 81 (1966).

12. D. Griffiths, H. Winsor, and T. Luongvan, Aust. J. Zool. 40, 319 (1992). [CrossRef]  

13. P. A. Todd, J. H. Lee, and L. M. Chou, Hydrobiologia 635, 37 (2009). [CrossRef]  

14. M. R. A. Naguit, Threshold 4, 17 (2009).

15. A. L. Holt, S. Vahidinia, Y. L. Gagnon, D. E. Morse, and A. M. Sweeney, J. R. Soc. Interface 11, 20140678 (2014). [CrossRef]  

16. A. Ghoshal, D. G. DeMartini, E. Eck, and D. E. Morse, J. R. Soc. Interface 10, 20130386 (2013). [CrossRef]  

17. E. J. Denton and M. F. Land, Proc. R. Soc. London B 178, 43 (1971). [CrossRef]  

18. A. L. Holt, A. M. Sweeney, S. Johnsen, and D. E. Morse, J. R. Soc. Interface 8, 1386 (2011). [CrossRef]  

References

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  1. T. W. Cronin, S. Johnsen, N. J. Marshall, and E. J. Warrant, Visual Ecology (Princeton University, 2014).
  2. S. Berthier, Iridescences (Springer, 2007).
  3. H. Simon, The Splendor of Iridescence: Structural Colors in the Animal World, 1st ed. (Dodd, Mead & Company, 1971).
  4. P. Vukusic, B. Hallam, and J. Noyes, Science 315, 348 (2007).
    [Crossref]
  5. S. M. Luke, B. T. Hallam, and P. Vukusic, Appl. Opt. 49, 4246 (2010).
    [Crossref]
  6. L. M. Mäthger, E. J. Denton, N. J. Marshall, and R. T. Hanlon, J. R. Soc. Interface 6, S149 (2009).
    [Crossref]
  7. T.-H. Chiou, L. M. Mäthger, R. T. Hanlon, and T. W. Cronin, J. Exp. Biol. 210, 3624 (2007).
    [Crossref]
  8. G. R. R. Bell, L. M. Mäthger, M. Gao, S. L. Senft, A. M. Kuzirian, G. W. Kattawar, and R. T. Hanlon, Adv. Mater. 26, 4352 (2014).
    [Crossref]
  9. L. M. Mäthger, S. L. Senft, M. Gao, S. Karaveli, G. R. R. Bell, R. Zia, A. M. Kuzirian, P. B. Dennis, W. J. Crookes-Goodson, R. R. Naik, G. W. Kattawar, and R. T. Hanlon, Adv. Funct. Mater. 23, 3980 (2013).
    [Crossref]
  10. D. G. DeMartini, A. Ghoshal, E. Pandolfi, A. T. Weaver, M. Baum, and D. E. Morse, J. Exp. Biol. 216, 3733 (2013).
    [Crossref]
  11. S. Kawaguti, Biol. J. Okayama Univ. 12, 81 (1966).
  12. D. Griffiths, H. Winsor, and T. Luongvan, Aust. J. Zool. 40, 319 (1992).
    [Crossref]
  13. P. A. Todd, J. H. Lee, and L. M. Chou, Hydrobiologia 635, 37 (2009).
    [Crossref]
  14. M. R. A. Naguit, Threshold 4, 17 (2009).
  15. A. L. Holt, S. Vahidinia, Y. L. Gagnon, D. E. Morse, and A. M. Sweeney, J. R. Soc. Interface 11, 20140678 (2014).
    [Crossref]
  16. A. Ghoshal, D. G. DeMartini, E. Eck, and D. E. Morse, J. R. Soc. Interface 10, 20130386 (2013).
    [Crossref]
  17. E. J. Denton and M. F. Land, Proc. R. Soc. London B 178, 43 (1971).
    [Crossref]
  18. A. L. Holt, A. M. Sweeney, S. Johnsen, and D. E. Morse, J. R. Soc. Interface 8, 1386 (2011).
    [Crossref]

2014 (2)

G. R. R. Bell, L. M. Mäthger, M. Gao, S. L. Senft, A. M. Kuzirian, G. W. Kattawar, and R. T. Hanlon, Adv. Mater. 26, 4352 (2014).
[Crossref]

A. L. Holt, S. Vahidinia, Y. L. Gagnon, D. E. Morse, and A. M. Sweeney, J. R. Soc. Interface 11, 20140678 (2014).
[Crossref]

2013 (3)

A. Ghoshal, D. G. DeMartini, E. Eck, and D. E. Morse, J. R. Soc. Interface 10, 20130386 (2013).
[Crossref]

L. M. Mäthger, S. L. Senft, M. Gao, S. Karaveli, G. R. R. Bell, R. Zia, A. M. Kuzirian, P. B. Dennis, W. J. Crookes-Goodson, R. R. Naik, G. W. Kattawar, and R. T. Hanlon, Adv. Funct. Mater. 23, 3980 (2013).
[Crossref]

D. G. DeMartini, A. Ghoshal, E. Pandolfi, A. T. Weaver, M. Baum, and D. E. Morse, J. Exp. Biol. 216, 3733 (2013).
[Crossref]

2011 (1)

A. L. Holt, A. M. Sweeney, S. Johnsen, and D. E. Morse, J. R. Soc. Interface 8, 1386 (2011).
[Crossref]

2010 (1)

2009 (3)

L. M. Mäthger, E. J. Denton, N. J. Marshall, and R. T. Hanlon, J. R. Soc. Interface 6, S149 (2009).
[Crossref]

P. A. Todd, J. H. Lee, and L. M. Chou, Hydrobiologia 635, 37 (2009).
[Crossref]

M. R. A. Naguit, Threshold 4, 17 (2009).

2007 (2)

T.-H. Chiou, L. M. Mäthger, R. T. Hanlon, and T. W. Cronin, J. Exp. Biol. 210, 3624 (2007).
[Crossref]

P. Vukusic, B. Hallam, and J. Noyes, Science 315, 348 (2007).
[Crossref]

1992 (1)

D. Griffiths, H. Winsor, and T. Luongvan, Aust. J. Zool. 40, 319 (1992).
[Crossref]

1971 (1)

E. J. Denton and M. F. Land, Proc. R. Soc. London B 178, 43 (1971).
[Crossref]

1966 (1)

S. Kawaguti, Biol. J. Okayama Univ. 12, 81 (1966).

Baum, M.

D. G. DeMartini, A. Ghoshal, E. Pandolfi, A. T. Weaver, M. Baum, and D. E. Morse, J. Exp. Biol. 216, 3733 (2013).
[Crossref]

Bell, G. R. R.

G. R. R. Bell, L. M. Mäthger, M. Gao, S. L. Senft, A. M. Kuzirian, G. W. Kattawar, and R. T. Hanlon, Adv. Mater. 26, 4352 (2014).
[Crossref]

L. M. Mäthger, S. L. Senft, M. Gao, S. Karaveli, G. R. R. Bell, R. Zia, A. M. Kuzirian, P. B. Dennis, W. J. Crookes-Goodson, R. R. Naik, G. W. Kattawar, and R. T. Hanlon, Adv. Funct. Mater. 23, 3980 (2013).
[Crossref]

Berthier, S.

S. Berthier, Iridescences (Springer, 2007).

Chiou, T.-H.

T.-H. Chiou, L. M. Mäthger, R. T. Hanlon, and T. W. Cronin, J. Exp. Biol. 210, 3624 (2007).
[Crossref]

Chou, L. M.

P. A. Todd, J. H. Lee, and L. M. Chou, Hydrobiologia 635, 37 (2009).
[Crossref]

Cronin, T. W.

T.-H. Chiou, L. M. Mäthger, R. T. Hanlon, and T. W. Cronin, J. Exp. Biol. 210, 3624 (2007).
[Crossref]

T. W. Cronin, S. Johnsen, N. J. Marshall, and E. J. Warrant, Visual Ecology (Princeton University, 2014).

Crookes-Goodson, W. J.

L. M. Mäthger, S. L. Senft, M. Gao, S. Karaveli, G. R. R. Bell, R. Zia, A. M. Kuzirian, P. B. Dennis, W. J. Crookes-Goodson, R. R. Naik, G. W. Kattawar, and R. T. Hanlon, Adv. Funct. Mater. 23, 3980 (2013).
[Crossref]

DeMartini, D. G.

D. G. DeMartini, A. Ghoshal, E. Pandolfi, A. T. Weaver, M. Baum, and D. E. Morse, J. Exp. Biol. 216, 3733 (2013).
[Crossref]

A. Ghoshal, D. G. DeMartini, E. Eck, and D. E. Morse, J. R. Soc. Interface 10, 20130386 (2013).
[Crossref]

Dennis, P. B.

L. M. Mäthger, S. L. Senft, M. Gao, S. Karaveli, G. R. R. Bell, R. Zia, A. M. Kuzirian, P. B. Dennis, W. J. Crookes-Goodson, R. R. Naik, G. W. Kattawar, and R. T. Hanlon, Adv. Funct. Mater. 23, 3980 (2013).
[Crossref]

Denton, E. J.

L. M. Mäthger, E. J. Denton, N. J. Marshall, and R. T. Hanlon, J. R. Soc. Interface 6, S149 (2009).
[Crossref]

E. J. Denton and M. F. Land, Proc. R. Soc. London B 178, 43 (1971).
[Crossref]

Eck, E.

A. Ghoshal, D. G. DeMartini, E. Eck, and D. E. Morse, J. R. Soc. Interface 10, 20130386 (2013).
[Crossref]

Gagnon, Y. L.

A. L. Holt, S. Vahidinia, Y. L. Gagnon, D. E. Morse, and A. M. Sweeney, J. R. Soc. Interface 11, 20140678 (2014).
[Crossref]

Gao, M.

G. R. R. Bell, L. M. Mäthger, M. Gao, S. L. Senft, A. M. Kuzirian, G. W. Kattawar, and R. T. Hanlon, Adv. Mater. 26, 4352 (2014).
[Crossref]

L. M. Mäthger, S. L. Senft, M. Gao, S. Karaveli, G. R. R. Bell, R. Zia, A. M. Kuzirian, P. B. Dennis, W. J. Crookes-Goodson, R. R. Naik, G. W. Kattawar, and R. T. Hanlon, Adv. Funct. Mater. 23, 3980 (2013).
[Crossref]

Ghoshal, A.

A. Ghoshal, D. G. DeMartini, E. Eck, and D. E. Morse, J. R. Soc. Interface 10, 20130386 (2013).
[Crossref]

D. G. DeMartini, A. Ghoshal, E. Pandolfi, A. T. Weaver, M. Baum, and D. E. Morse, J. Exp. Biol. 216, 3733 (2013).
[Crossref]

Griffiths, D.

D. Griffiths, H. Winsor, and T. Luongvan, Aust. J. Zool. 40, 319 (1992).
[Crossref]

Hallam, B.

P. Vukusic, B. Hallam, and J. Noyes, Science 315, 348 (2007).
[Crossref]

Hallam, B. T.

Hanlon, R. T.

G. R. R. Bell, L. M. Mäthger, M. Gao, S. L. Senft, A. M. Kuzirian, G. W. Kattawar, and R. T. Hanlon, Adv. Mater. 26, 4352 (2014).
[Crossref]

L. M. Mäthger, S. L. Senft, M. Gao, S. Karaveli, G. R. R. Bell, R. Zia, A. M. Kuzirian, P. B. Dennis, W. J. Crookes-Goodson, R. R. Naik, G. W. Kattawar, and R. T. Hanlon, Adv. Funct. Mater. 23, 3980 (2013).
[Crossref]

L. M. Mäthger, E. J. Denton, N. J. Marshall, and R. T. Hanlon, J. R. Soc. Interface 6, S149 (2009).
[Crossref]

T.-H. Chiou, L. M. Mäthger, R. T. Hanlon, and T. W. Cronin, J. Exp. Biol. 210, 3624 (2007).
[Crossref]

Holt, A. L.

A. L. Holt, S. Vahidinia, Y. L. Gagnon, D. E. Morse, and A. M. Sweeney, J. R. Soc. Interface 11, 20140678 (2014).
[Crossref]

A. L. Holt, A. M. Sweeney, S. Johnsen, and D. E. Morse, J. R. Soc. Interface 8, 1386 (2011).
[Crossref]

Johnsen, S.

A. L. Holt, A. M. Sweeney, S. Johnsen, and D. E. Morse, J. R. Soc. Interface 8, 1386 (2011).
[Crossref]

T. W. Cronin, S. Johnsen, N. J. Marshall, and E. J. Warrant, Visual Ecology (Princeton University, 2014).

Karaveli, S.

L. M. Mäthger, S. L. Senft, M. Gao, S. Karaveli, G. R. R. Bell, R. Zia, A. M. Kuzirian, P. B. Dennis, W. J. Crookes-Goodson, R. R. Naik, G. W. Kattawar, and R. T. Hanlon, Adv. Funct. Mater. 23, 3980 (2013).
[Crossref]

Kattawar, G. W.

G. R. R. Bell, L. M. Mäthger, M. Gao, S. L. Senft, A. M. Kuzirian, G. W. Kattawar, and R. T. Hanlon, Adv. Mater. 26, 4352 (2014).
[Crossref]

L. M. Mäthger, S. L. Senft, M. Gao, S. Karaveli, G. R. R. Bell, R. Zia, A. M. Kuzirian, P. B. Dennis, W. J. Crookes-Goodson, R. R. Naik, G. W. Kattawar, and R. T. Hanlon, Adv. Funct. Mater. 23, 3980 (2013).
[Crossref]

Kawaguti, S.

S. Kawaguti, Biol. J. Okayama Univ. 12, 81 (1966).

Kuzirian, A. M.

G. R. R. Bell, L. M. Mäthger, M. Gao, S. L. Senft, A. M. Kuzirian, G. W. Kattawar, and R. T. Hanlon, Adv. Mater. 26, 4352 (2014).
[Crossref]

L. M. Mäthger, S. L. Senft, M. Gao, S. Karaveli, G. R. R. Bell, R. Zia, A. M. Kuzirian, P. B. Dennis, W. J. Crookes-Goodson, R. R. Naik, G. W. Kattawar, and R. T. Hanlon, Adv. Funct. Mater. 23, 3980 (2013).
[Crossref]

Land, M. F.

E. J. Denton and M. F. Land, Proc. R. Soc. London B 178, 43 (1971).
[Crossref]

Lee, J. H.

P. A. Todd, J. H. Lee, and L. M. Chou, Hydrobiologia 635, 37 (2009).
[Crossref]

Luke, S. M.

Luongvan, T.

D. Griffiths, H. Winsor, and T. Luongvan, Aust. J. Zool. 40, 319 (1992).
[Crossref]

Marshall, N. J.

L. M. Mäthger, E. J. Denton, N. J. Marshall, and R. T. Hanlon, J. R. Soc. Interface 6, S149 (2009).
[Crossref]

T. W. Cronin, S. Johnsen, N. J. Marshall, and E. J. Warrant, Visual Ecology (Princeton University, 2014).

Mäthger, L. M.

G. R. R. Bell, L. M. Mäthger, M. Gao, S. L. Senft, A. M. Kuzirian, G. W. Kattawar, and R. T. Hanlon, Adv. Mater. 26, 4352 (2014).
[Crossref]

L. M. Mäthger, S. L. Senft, M. Gao, S. Karaveli, G. R. R. Bell, R. Zia, A. M. Kuzirian, P. B. Dennis, W. J. Crookes-Goodson, R. R. Naik, G. W. Kattawar, and R. T. Hanlon, Adv. Funct. Mater. 23, 3980 (2013).
[Crossref]

L. M. Mäthger, E. J. Denton, N. J. Marshall, and R. T. Hanlon, J. R. Soc. Interface 6, S149 (2009).
[Crossref]

T.-H. Chiou, L. M. Mäthger, R. T. Hanlon, and T. W. Cronin, J. Exp. Biol. 210, 3624 (2007).
[Crossref]

Morse, D. E.

A. L. Holt, S. Vahidinia, Y. L. Gagnon, D. E. Morse, and A. M. Sweeney, J. R. Soc. Interface 11, 20140678 (2014).
[Crossref]

A. Ghoshal, D. G. DeMartini, E. Eck, and D. E. Morse, J. R. Soc. Interface 10, 20130386 (2013).
[Crossref]

D. G. DeMartini, A. Ghoshal, E. Pandolfi, A. T. Weaver, M. Baum, and D. E. Morse, J. Exp. Biol. 216, 3733 (2013).
[Crossref]

A. L. Holt, A. M. Sweeney, S. Johnsen, and D. E. Morse, J. R. Soc. Interface 8, 1386 (2011).
[Crossref]

Naguit, M. R. A.

M. R. A. Naguit, Threshold 4, 17 (2009).

Naik, R. R.

L. M. Mäthger, S. L. Senft, M. Gao, S. Karaveli, G. R. R. Bell, R. Zia, A. M. Kuzirian, P. B. Dennis, W. J. Crookes-Goodson, R. R. Naik, G. W. Kattawar, and R. T. Hanlon, Adv. Funct. Mater. 23, 3980 (2013).
[Crossref]

Noyes, J.

P. Vukusic, B. Hallam, and J. Noyes, Science 315, 348 (2007).
[Crossref]

Pandolfi, E.

D. G. DeMartini, A. Ghoshal, E. Pandolfi, A. T. Weaver, M. Baum, and D. E. Morse, J. Exp. Biol. 216, 3733 (2013).
[Crossref]

Senft, S. L.

G. R. R. Bell, L. M. Mäthger, M. Gao, S. L. Senft, A. M. Kuzirian, G. W. Kattawar, and R. T. Hanlon, Adv. Mater. 26, 4352 (2014).
[Crossref]

L. M. Mäthger, S. L. Senft, M. Gao, S. Karaveli, G. R. R. Bell, R. Zia, A. M. Kuzirian, P. B. Dennis, W. J. Crookes-Goodson, R. R. Naik, G. W. Kattawar, and R. T. Hanlon, Adv. Funct. Mater. 23, 3980 (2013).
[Crossref]

Simon, H.

H. Simon, The Splendor of Iridescence: Structural Colors in the Animal World, 1st ed. (Dodd, Mead & Company, 1971).

Sweeney, A. M.

A. L. Holt, S. Vahidinia, Y. L. Gagnon, D. E. Morse, and A. M. Sweeney, J. R. Soc. Interface 11, 20140678 (2014).
[Crossref]

A. L. Holt, A. M. Sweeney, S. Johnsen, and D. E. Morse, J. R. Soc. Interface 8, 1386 (2011).
[Crossref]

Todd, P. A.

P. A. Todd, J. H. Lee, and L. M. Chou, Hydrobiologia 635, 37 (2009).
[Crossref]

Vahidinia, S.

A. L. Holt, S. Vahidinia, Y. L. Gagnon, D. E. Morse, and A. M. Sweeney, J. R. Soc. Interface 11, 20140678 (2014).
[Crossref]

Vukusic, P.

S. M. Luke, B. T. Hallam, and P. Vukusic, Appl. Opt. 49, 4246 (2010).
[Crossref]

P. Vukusic, B. Hallam, and J. Noyes, Science 315, 348 (2007).
[Crossref]

Warrant, E. J.

T. W. Cronin, S. Johnsen, N. J. Marshall, and E. J. Warrant, Visual Ecology (Princeton University, 2014).

Weaver, A. T.

D. G. DeMartini, A. Ghoshal, E. Pandolfi, A. T. Weaver, M. Baum, and D. E. Morse, J. Exp. Biol. 216, 3733 (2013).
[Crossref]

Winsor, H.

D. Griffiths, H. Winsor, and T. Luongvan, Aust. J. Zool. 40, 319 (1992).
[Crossref]

Zia, R.

L. M. Mäthger, S. L. Senft, M. Gao, S. Karaveli, G. R. R. Bell, R. Zia, A. M. Kuzirian, P. B. Dennis, W. J. Crookes-Goodson, R. R. Naik, G. W. Kattawar, and R. T. Hanlon, Adv. Funct. Mater. 23, 3980 (2013).
[Crossref]

Adv. Funct. Mater. (1)

L. M. Mäthger, S. L. Senft, M. Gao, S. Karaveli, G. R. R. Bell, R. Zia, A. M. Kuzirian, P. B. Dennis, W. J. Crookes-Goodson, R. R. Naik, G. W. Kattawar, and R. T. Hanlon, Adv. Funct. Mater. 23, 3980 (2013).
[Crossref]

Adv. Mater. (1)

G. R. R. Bell, L. M. Mäthger, M. Gao, S. L. Senft, A. M. Kuzirian, G. W. Kattawar, and R. T. Hanlon, Adv. Mater. 26, 4352 (2014).
[Crossref]

Appl. Opt. (1)

Aust. J. Zool. (1)

D. Griffiths, H. Winsor, and T. Luongvan, Aust. J. Zool. 40, 319 (1992).
[Crossref]

Biol. J. Okayama Univ. (1)

S. Kawaguti, Biol. J. Okayama Univ. 12, 81 (1966).

Hydrobiologia (1)

P. A. Todd, J. H. Lee, and L. M. Chou, Hydrobiologia 635, 37 (2009).
[Crossref]

J. Exp. Biol. (2)

D. G. DeMartini, A. Ghoshal, E. Pandolfi, A. T. Weaver, M. Baum, and D. E. Morse, J. Exp. Biol. 216, 3733 (2013).
[Crossref]

T.-H. Chiou, L. M. Mäthger, R. T. Hanlon, and T. W. Cronin, J. Exp. Biol. 210, 3624 (2007).
[Crossref]

J. R. Soc. Interface (4)

L. M. Mäthger, E. J. Denton, N. J. Marshall, and R. T. Hanlon, J. R. Soc. Interface 6, S149 (2009).
[Crossref]

A. L. Holt, S. Vahidinia, Y. L. Gagnon, D. E. Morse, and A. M. Sweeney, J. R. Soc. Interface 11, 20140678 (2014).
[Crossref]

A. Ghoshal, D. G. DeMartini, E. Eck, and D. E. Morse, J. R. Soc. Interface 10, 20130386 (2013).
[Crossref]

A. L. Holt, A. M. Sweeney, S. Johnsen, and D. E. Morse, J. R. Soc. Interface 8, 1386 (2011).
[Crossref]

Proc. R. Soc. London B (1)

E. J. Denton and M. F. Land, Proc. R. Soc. London B 178, 43 (1971).
[Crossref]

Science (1)

P. Vukusic, B. Hallam, and J. Noyes, Science 315, 348 (2007).
[Crossref]

Threshold (1)

M. R. A. Naguit, Threshold 4, 17 (2009).

Other (3)

T. W. Cronin, S. Johnsen, N. J. Marshall, and E. J. Warrant, Visual Ecology (Princeton University, 2014).

S. Berthier, Iridescences (Springer, 2007).

H. Simon, The Splendor of Iridescence: Structural Colors in the Animal World, 1st ed. (Dodd, Mead & Company, 1971).

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Figures (7)

Fig. 1.
Fig. 1. (a) Juvenile T. maxima giant clam (6 cm) showing reflective epithelium of the mantle overlapping the shell. (b) Close-up of specimen shown in (a). (c) Dissected juvenile T. derasa (5 cm) showing numerous white stripes in mantle epithelium. (d) Close-up of the epithelium shown in (c); prominent white stripes are 1 2 mm wide × 5 mm long. Red circles indicate white areas analyzed.
Fig. 2.
Fig. 2. Schematic of illumination and light collection used to obtain bright-field images and high-resolution microspectrophotometric measurements [16].
Fig. 3.
Fig. 3. Magnified views of a white region in T. maxima epithelium, shown in Fig. 1(b), imaged in dark-field reflectance mode. (a) Low-magnification, with each individual bright spot revealing an individual iridocyte. (b) Higher-magnification view of the same region. Dotted circles indicate sample areas of light collection for microspectrophotometric analysis of reflectance from individual iridocytes.
Fig. 4.
Fig. 4. Examples of iridocytes of various colors from the white region shown in Fig. 1(b) from which spectra were obtained.
Fig. 5.
Fig. 5. (a) Typical spectrum from single iridocyte from a white region in T. maxima mantle epithelium. (b) Peak reflectivity and wavelength from spectra from multiple isolated iridocytes from the white region as analyzed in (a).
Fig. 6.
Fig. 6. Iridocytes in a white stripe from T. derasa, imaged at increasing levels of magnification in dark-field reflectance mode.
Fig. 7.
Fig. 7. Spectra from individual iridocytes from a white stripe from T. derasa, as seen in Fig. 6. Spectra with single peaks are rare because each iridocyte displays multiple colors.

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