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Bioluminescent and Red-Fluorescent Lures in a Deep-Sea Siphonophore

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Science  08 Jul 2005:
Vol. 309, Issue 5732, pp. 263
DOI: 10.1126/science.1110441

Abstract

Bioluminescence (light production) and fluorescence (re-emission of absorbed radiation as light) are found in an unaccountably diverse array of marine organisms, where their functions are largely unknown. Here we report a deep-sea siphonophore that twitches glowing lures to attract fish. This is rare evidence of bioluminescence used for prey attraction among nonvisual marine organisms. The lures also contain red fluorescent material that shifts the wavelength of emitted light. The existence of a red-luminescent invertebrate suggests that long-wavelength light plays a greater role in marine interactions than previously suspected.

Examples of bioluminescent lures in the sea are quite rare, posited only for a few fish and cephalopods (1). In many marine organisms, including siphonophores, luminescence is thought to serve defensive purposes. Siphonophores are colonial hydrozoans (phylum Cnidaria) that are dominant predators in the ocean, some reaching tens of meters in length. Nearly all members of this group are luminous (2), but because of their fragility, they are rarely observed alive.

Using a submersible at depths between 1600 m and 2300 m (3), we collected three specimens of an undescribed species in the genus Erenna (Fig. 1A and movie S1). Unlike most siphonophores, Erenna do not feed on crustaceans but prey instead upon fish (4), remnants of which were found inside two of our specimens. At great depths where chance encounters with vertebrates are rare, it is unclear how they obtain prey. Here we show that the nonvisual Erenna sp. we captured possesses redemitting bioluminescent appendages that may act as lures for fish prey.

Fig. 1.

(A) Erenna sp. at 1662 m. Scale bar, 2 cm. (B) Scanning electron micrograph of immature photophore (pi) and cnido-band (cn). Scale bar, 200 μm. (C) Live tentilla with mature photophores (pm). Scale bar, 1 mm. (D to F) Fluorescence emission spectra of (D) a live mature photophore (excitation wavelength λex = 410 nm), (E) unpurified extract (λex= 473 nm), and (F) purified extract (λex = 410 nm). Dashed vertical lines show primary conserved emission peaks. (G) The absorbance spectrum of purified photophore extract.

Erenna tentacles have numerous side branches (tentilla), each consisting of a large cnido-band (an array of ∼3000 stinging cells) attached to a central stalk (Fig. 1, B and C). The transparent stalk terminates in a bulb containing white spots, historically called “ocelli” (4). We found that, when ruptured in CaCl2, these spots produced luminescence, indicating that they are in fact photophores filled with Ca2+-regulated photoproteins. Unlike typical cnidarian photocytes, these terminal photophores did not readily flash upon direct stimulation.

Photophores of young tentilla (Fig. 1B) contained only bioluminescent tissue, but when mature, they were surrounded by red fluorescent material (Fig. 1C). This substance produced a multimodal fluorescence emission, spanning yellow to red (583, 620, and 680 nm) (Fig. 1, D and E). These mature tentilla also displayed a unique rhythmic flicking behavior (movie S1).

We observed blue-green (immature) and orange-red (mature) in vivo emission by eye, but we were unable to record bioluminescence emission spectra because of the scarcity of specimens and the small size of the photophores. We expect bioluminescence spectra to be similar to fluorescence emissions, as is the case in other cnidarians (2).

Among all marine organisms, only the rare scaleless dragonfishes (Stomiidae) have been known to produce red luminescence (1), but red fluorescent substances have been noted in several marine phyla (57). The fluorescent material of Erenna does not appear to belong to the green fluorescent protein family (5), nor does it resemble the biliproteins of the siphonophore Physalia (6). On the basis of emission and absorption spectra, with a Soret band at 406 nm and secondary Q bands at 570 and 583 nm (Fig. 1, F and G), the main constituents are most similar to porphyrins found in medusae and fish (7).

Given the characteristic flicking of the bioluminescent and fluorescent filaments, we concluded that the siphonophore Erenna uses them as lures to attract fish. Fluorescent structures may serve as lures in a diverse assemblage of nonluminous taxa, from cnidarians to crustaceans, and we have found examples of putative lures in several other siphonophores and medusae. In shallow waters, fluorescence could be excited by ambient blue light rather than by bioluminescence as in deep-dwelling Erenna.

The assertion that red light acts as an attractant is at odds with the prevailing view that deep-living creatures cannot detect long wavelengths; however, our knowledge of deep-sea visual abilities is limited. For example, the eyes of Cyclothone, an abundant deep-sea fish, have not yet been studied, and evidence for red sensitivity in a deep myctophid fish has been presented only recently (8). Our findings suggest that the role of long-wavelength light in marine visual ecology merits a closer look.

Supporting Online Material

www.sciencemag.org/cgi/content/full/309/5732/263/DC1

Materials and Methods

Movie S1

References and Notes

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