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Fluorescent Enhancement of Signaling in a Mantis Shrimp

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Science  02 Jan 2004:
Vol. 303, Issue 5654, pp. 51
DOI: 10.1126/science.1089803

Visual signals based on colored pigments can be unreliable in aquatic environments, because the optical properties of water spectrally filter both the incident and the reflected light. Fluorescence has more potential to contribute to color underwater than in terrestrial situations, because the spectrum of the emitted light can contrast effectively with that of the predominantly blue illumination (1). Many corals have striking fluorescent coloration (2), and some vision-centered marine organisms such as squids have fluorescent patches (3). Though a behavioral function has been shown for fluorescence in budgerigar plumage (4), the use of fluorescent colors as signals has not been shown in the sea. Here, we show that fluorescent coloration used in postural signaling by the mantis shrimp Lysiosquillina glabriuscula contributes to signal brightness and visibility, particularly at greater depths.

Several species of mantis shrimp (stomatopod crustaceans) have strongly fluorescent yellow markings. In L. glabriuscula, these appear as patches on the antennal scales and carapace (Fig. 1A). This species is large (up to 22 cm long) and is found throughout the western Atlantic from South Carolina to Brazil. Burrowing in sandy substrates at depths from the low intertidal to 60 m, monogamous adults rarely leave their burrows except to search for new mates. A common threat display involves raising the head and thorax, spreading the striking appendages and other maxillipeds, and extending the prominent, oval antennal scales laterally (Fig. 1A). We have observed such displays directed toward males of the same species as they approached a burrow entrance and toward potential predators when encountered in the open. The display increases the apparent size of the animal and accentuates both its weapons and the yellow markings.

Fig. 1.

Fluorescent markings in display mode: (A) reflected by white light and (B) stimulated by blue light. Scale bar, ∼1 cm. (C) Reflectance (thick line) and normalized fluorescence excitation (thin line) and emission (dashed line) spectra for the fluorescent pigment (5). (D) Normalized spectral sensitivities of medium-wavelength photo-receptors in compound eyes of L. glabriuscula (thick line, row 2 distal tier; thin line, row 2 proximal tier), together with the fluorescence emission spectrum (dashed line).

To human eyes, the patches appear yellow due to combined reflectance and fluorescence when illuminated by white light, and they have a strong yellow fluorescence when illuminated by ultra-violet or blue light (Fig. 1B) (5). The excitation spectrum (Fig. 1C) peaks in the blue (440 nm, 365 to 495 nm at half-maximum) and is well matched to the wavelength range of maximum illumination (5). The wavelengths of the fluorescence emission (524 nm at peak, 500 to 575 nm at half-maximum) transmit well through seawater, so the emitted light would be visible at distances at which animal-to-animal interactions occur.

The spectrum produced by the yellow patches under ambient illumination at any depth is a combination of the reflectance and fluorescence components (2, 5). At moderate depths, the interaction of reflectance and ambient light produces a broad peak in the 475- to 575-nm (cyan to yellow) range. The fluorescence overlays and intensifies this peak (fig. S1). We estimate that, throughout the depth range from 2 to 40 m, the fluorescence accounts for 7 to 10% of the total (reflected plus fluoresced) photons leaving the yellow patches.

The fluorescence contribution gains significance when we consider the photoreceptors used by stomatopods. Mantis shrimp have a complex system of color vision, based on at least eight primary spectral receptor classes operating at wavelengths from 400 to 700 nm. Colored markings play a critical role in visual communication (6). The fluorescence spectrum is well placed to stimulate receptor classes that are tuned to middle wavelengths (5) (Fig. 1D), so it should be highly recognizable in a species-specific signaling system. For the pair of receptors with the closest spectral match, the modeling indicates that, at depths of 20, 30, and 40 m, the fluorescence contributes approximately 9, 11, and 12%, respectively, of the photons stimulating the shorter-wavelength receptor, and 15, 22, and 30%, respectively, of those stimulating the longer-wavelength receptor. Thus, the fluorescence enhances and spectrally identifies a color signal in the variable lighting over the depth range inhabited by this species.

Supporting Online Material

www.sciencemag.org/cgi/content/full/1089803/DC1

Materials and Methods

SOM Text

Fig. S1

References

References and Notes

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