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Biofluorescence in Catsharks www.nature.com/scientificreports OPEN Biofuorescence in Catsharks (Scyliorhinidae): Fundamental Description and Relevance for receie: 22 anuar 2016 ccepte: 05 pri 2016 Elasmobranch Visual Ecology Puise: 25 pri 2016 David F. Gruber1,2,3, Ellis R. Loew4, Dimitri D. Deheyn5, Derya Akkaynak6,7, Jean P. Gafney1, W. Leo Smith8, Matthew P. Davis9, Jennifer H. Stern8, Vincent A. Pieribone10 & John S. Sparks3,11 Biofuorescence has recently been found to be widespread in marine fshes, including sharks. Catsharks, such as the Swell Shark (Cephaloscyllium ventriosum) from the eastern Pacifc and the Chain Catshark (Scyliorhinus retifer) from the western Atlantic, are known to exhibit bright green fuorescence. We examined the spectral sensitivity and visual characteristics of these reclusive sharks, while also considering the fuorescent properties of their skin. Spectral absorbance of the photoreceptor cells in these sharks revealed the presence of a single visual pigment in each species. Cephaloscyllium ventriosum exhibited a maximum absorbance of 484 ± 3 nm and an absorbance range at half maximum (λ1/2max) of 440–540 nm, whereas for S. retifer maximum absorbance was 488 ± 3 nm with the same absorbance range. Using the photoreceptor properties derived here, a “shark eye” camera was designed and developed that yielded contrast information on areas where fuorescence is anatomically distributed on the shark, as seen from other sharks’ eyes of these two species. Phylogenetic investigations indicate that biofuorescence has evolved at least three times in cartilaginous fshes. The repeated evolution of biofuorescence in elasmobranchs, coupled with a visual adaptation to detect it; and evidence that biofuorescence creates greater luminosity contrast with the surrounding background, highlights the potential importance of biofuorescence in elasmobranch behavior and biology. Although biofuorescence has been extensively examined in cnidarians, particularly corals1–3, the phenomenon has only recently been shown to be phylogenetically widespread and phenotypically variable in both cartilaginous and bony marine fshes4. Biofuorescence has even recently been observed in sea turtles5. Tis revelation leads to many new questions regarding the biological and ecological role of biofuorescence in the marine realm, because fshes and sea turtles, unlike cnidarians, possess advanced visual systems6–9. Marine organisms biofuoresce by absorbing the dominant higher energy ambient blue light via fuorescent compounds, and reemit it at longer, lower energy wavelengths, visually resulting in green, orange, and red fuo- rescence to the human visual system. With increasing depth in the ocean, the spectral quality of sunlight becomes restricted to a narrow range of wavelengths of blue light and intensity decreases in an approximately exponential 1aruc oee it niersit of ew or Department of atura ciences ew or 10010 . 2it niersit of ew or e rauate enter roram in ioo ew or 10016 . 3merican useum of atura istor acer Institute for omparatie enomics ew or 10024 . 4College of eterinar eicine orne niersit Itaca 14853 . 5University of California, San Diego, Scripps Institution of Oceanorap a oa 203 . 6University of Haifa, Charney School of Marine Sciences aifa 348838 Israe. 7Interuniersit Institute of arine ciences iat 88103 Israe. 8University of Kansas, ioiersit Institute an Department of coo an outionar ioo awrence 6604 . t. ou tate niersit Department of iooica ciences t. ou 56301 . 10e on . ierce aorator euar an oecuar sioo ae niersit coo of eicine ew aen 0651 . 11merican useum of atura istor Diision of erterate ooo Department of Ictoo ew or 10024 . orresponence an reuests for materias sou e aresse to D.. emai: Dai.rueraruc.cun.eu Scientific RepoRts | 6:24751 | DOI: 10.1038/srep24751 1 www.nature.com/scientificreports/ Figure 1. (a) Microspectrophotometry data from Celphaloscyllium ventriosum and Scyliorhinus retifer. Maximum absorbance of 484 and 488 nm, respectively. (b) Long rods of S. retifer (scale = 10 μm). manner10. In clear ocean water the light spectrum bandwidth progressively narrows with increasing depth, reach- ing a wavelength peak of 465 nm and a narrow bandwidth of ~20 nm at the maximum depth of penetration11. Tus, biofuorescence adds photons in a spectral region (i.e., longer wavelengths of the visible spectrum) not oth- erwise represented at depth, which has been shown to drive evolutionary shifs in light absorbance across many taxa, such as the evolution of divinyl-chlorophyll a in marine micro algae12. Green Fluorescent Protein (GFP) was discovered in a hydrozoan jellyfsh, Aequorea victoria, coupled to the bioluminescent apparatus, where it converts blue bioluminescent light to green light13. Te GFP family has since proven to be one of the most useful tools in biomedical science14. GFP orthologs have also been reported in non-bioluminescent anthozoans2,15,16, planktonic copepods17, and lancelets18. In fshes, a novel bilirubin-binding fuorescent protein (FP) was found in Anguilla japonica19,20, and it has been shown that bilirubin-binding FPs also occur in cryptic marine eels of the genus Kaupichthys21. Tis new family of eel FPs evolved as the sister group to brain fatty acid-binding proteins21. Some fshes exhibit strong interspecifc variation in fuorescent emission patterns (e.g., members of the liz- ardfsh genus Synodus and the goby genus Eviota), which has led to the hypothesis that biofuorescence functions as a form of species recognition4, akin to the unique bioluminescent signals produced by both shallow water and deep-sea fsh lineages22–24. Tere are also many fshes known to possess yellow intraocular (lenses or cor- nea) flters25, which potentially function as long-pass flters and enable enhanced perception of fuorescence. Biofuorescence has also been shown to play a role in the behavior of marine organisms: fuorescence at the tips of the tentacles in the hydromedusa Olindias formosa attracts juvenile rockfshes of the genus Sebastes26; the fairy wrasse, Cirrhilabrus solorensis, responds to red biofuorescence27; and fuorescence in the mantis shrimp, Lysiosquillina glabriuscula, enhances signaling 28. Although recent work has demonstrated that biofuorescence is widespread in marine cartilaginous and ray-fnned fshes4,21, very few studies have examined the fuorescent properties of these lineages. Further assess- ment of these spectral properties is critical to advancing our understanding of the evolution of biofuorescence in marine vertebrates and its potential impact on their evolution, behavior, diversifcation rate, and the composition of marine ecosystems in general. Here we focus on cartilaginous fshes and examine the photoreceptor cells in two species of catsharks (Scyliorhinidae: Cephaloscyllium ventriosum and Scyliorhinus retifer) that exhibit bright green fuorescence patterns resulting from the presence of fuorescent compounds in their skin. We performed hyper- spectral imaging of their skin and investigated how the green-dominated fuorescence afected the appearance of these sharks to conspecifcs given their spectral sensitivity and the blue ambient water background. We also assembled a “shark-eye” camera and imaged catsharks in their natural environment with flters closely matching the absorbance spectrum of the measured visual pigment, as well as with underwater fuorescence photography. Models for estimating the lightness perception of these monochromatic sharks do not exist, therefore, we used models developed for the human visual system to gain insight into how biofuorescence changes the appearance of the sharks in the eyes of their conspecifcs, compared to the way they appear under white light. Results Microspectrophotometry (MSP) conducted on the retina of Cephaloscyllium ventriosum revealed a single visual pigment with an absorbance maximum (λ max) at 484 ± 3 nm and an absorbance range at half maximum (λ 1/2max) of 440–540 nm. Scyliorhinus retifer was also found to possess a single visual pigment with a λ max of 488 ± 3 nm and a λ 1/2max of 440–540 nm (Fig. 1). C. ventriosum and S. retifer were imaged and epidermal tissue from the fattened dorsal side of their head spectrally analyzed using a hyperspectral imager in fuorescence mode (Figs 2 and 3). Te dermal patches of C. ventriosum and S. retifer that were imaged always included one of the darker/ black reticulated patches (in bright feld) and light beige areas, which is the typical repeating, reticulated pigmen- tation pattern characteristic of these catsharks (Figs 4 and 5). Fluorescence images clearly showed that at 355 nm excitation, bright blue fuorescence (455 nm emission [em.] with a shoulder towards 500 nm; Figs 2 and 3a) was associated with the darker areas of the skin, whereas some dim blue-green fuorescence (455–505 nm em.; Figs 2 and 3b) was observed in the lighter beige regions of the skin. When excited at 390 and 470 nm, the fuorescence images show that only intense green fuorescence (525–535 nm em.) was generated from both the darker and lighter pigmented areas of the skin. Green fuorescence was most intense from the lighter beige colored areas Scientific RepoRts | 6:24751 | DOI: 10.1038/srep24751 2 www.nature.com/scientificreports/ Figure 2. Spectral characterization of C. ventriosum. (a) Fluorescence spectra following excitation at 355, 390, and 470 nm from black areas of the skin, using hyperspectral imaging analysis. (b) Same analysis from beige areas of the skin. (C) Excitation emission matrix (log scale representation) afer extraction of fuorescent compounds
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  • Identifying Sharks and Rays
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