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FAU Institutional Repository FAU Institutional Repository http://purl.fcla.edu/fau/fauir This paper was submitted by the faculty of FAU’s Harbor Branch Oceanographic Institute. Notice: ©1992 Springer. This manuscript is an author version with the final publication available at http://www.springerlink.com and may be cited as: Herring, P. J., Widder, E. A., & Haddock, S. H. D. (1992). Correlation of bioluminescence emissions with ventral photophores in the mesopelagic squid Abralia veranyi (Cephalopoda: Enoploteuthidae). Marine Biology, 112(2), 293‐298. doi:10.1007/BF00702474 I I Marine Biology 112, 293- 298 (1992) Marine lntemattonat dournal llfSB~~7/ In on life Oceans B-Iology J--_--- () and Coastal Waters JJ-)P\J~ - © Springer-Verlag 1992 J Correlation of bioluminescence emissions with ventral photophores in the mesopelagic squid Ahralia veranyi (Cephalopoda: Enoploteuthidae) P. J. Herring I, E. A. Widder 2 and S. H. D. Haddock 3 1 Institute of Oceanographic Sciences, Deacon Laboratory, Brook Road, Wormley, Godalming GU8 5UB, Surrey, England 2 Harbor Branch Oceanographic Institution, 5600 Old Dixie Highway, Fort Pierce, Florida 34946, USA 3 Marine Science Institute, University of California, Santa Barbara, California 93106, USA Date of final manuscript acceptance: September 26, 1991. Communicated by 1. Mauchline, Oban Abstract. Specimens of the squid Abralia veranyi were spinosus and Systellaspis debilis is spectrally different collected off the Bahamas in 1989. The bioluminescence from that emitted by the photophores ofthe same species of the ventral photophores was recorded on videotape at (Herring 1983, Latz et al. 1988), and in many animals the 11 to 12°C and 24 °C, in conjunction with measurements emission spectra are determined, in part, by the effects of of the spectral emission at the same temperatures. At accessory optical structures such as filters (Denton et al. 11°C, the spectrum was unimodal, peaking at 490 nm 1985). with a narrow bandwidth. At the higher temperature a Reversible spectral changes in the bioluminescence shoulder at about 440 nm appeared in the emission spec­ emission ofa single individual have rarely been reported; trum. The short, bright flashes from the subocular pho­ the most detailed examples are those of the squids tophores had a broader bandwidth and a shorter wave­ Abraliopsis sp. and Abralia trigonura (Young and length emission maximum (475 nm) than that of the Mencher 1980, Young and Arnold 1982). These authors ventral photophores. Video recordings at the two tem­ suggested that the spectral changes observed (in response peratures showed no changes in either the identities ofthe to changes in ambient temperature or light intensity) re­ luminescing photophores or their relative intensities. One sulted both from recruitment of different photophores structurally distinct type of photophore was not illumi­ and from changes in the spectral emission of at least one nated. We conclude that the observed spectral changes class of photophore. were produced within one group of photophores, and We have recorded the ventral bioluminescence of the that recruitment ofthe unilluminated photophores would related squid Abralia veranyi on videotape and analysed produce an additional spectral component, previously the contributions of different photophores at different reported from another species of Abralia (A. trigonura). temperatures, while monitoring the associated spectral changes. The spectral changes we observed were not asso­ ciated with the recruitment of different classes of pho­ tophore. Introduction Certain species of bioluminescent animals are known to be able to produce different colours of light emission. In Materials and methods most of the cases so far investigated, this is achieved by the employment of different photophores, each of which Specimens of Abralia veranyi were obtained on a cruise of R.V. has a characteristic spectral emission. In some deep-sea "Edwin Link" in the Bahamas in November 1989. Squids were fishes the suborbital photophore produces red light, captured either by dipnetting at the surface or by capture at depth whereas the postorbital photophore produces blue light with the Johnson-Sea-Link submersible. They were brought into the (Widder et al. 1984). Among terrestrial arthropods the shipboard laboratory, where they usually emitted a spontaneous ventral glow. The most detailed observations were made on a spec­ red and green luminescence of the "railroad worm" imen (37.5 mm dorsal mantle length) captured at a depth of 602 m Phrixothrix sp. and the elaterid beetle Pyrophorus plagio- on 16 November at 26° 4.3'N, 77° 34.3'W The ambient temperature phthalmus similarly derive from different photophores at this depth was 12.5 °C. The morphology ofdifferent photophores (McElroy et aI., 1974). Even in cases where specific pho­ from this specimen was examined by embedding a small area of the tophores are not identifiable, different areas of the body ventral mantle in Taab (Reading, UK) premix medium resin. Thick may produce different colours of bioluminescence, as in ("" 2 urn) serial sections were cut on a Huxley Ultratome with glass knives and stained with 1% toluidine blue in 1% borax. the green and blue luminescence of the cnidarian Umbel­ An intensified video camera (ISIT Dage 66) was used to record lula huxleyi (Herring 1983, Widder et al. 1983). The secre­ the bioluminescence on !" (12.7 mm) video tape. Computer image­ tory bioluminescence of the decapod shrimps Oplophorus analysis ofphotophore patterns was carried out using a Megavision 294 P.J. Herring et al.: Bioluminescence of Abralia 1024XM system . A photograph of the formalin-preserved specimen that were not brightly luminescent could often be stimu­ was scanned into the computer system using a Hewlett Packard lated by briefexposure to the illumination ofa hand-held ScanJet Plus scanner for comparison with digitized video frames of flashlight. Luminescence was mostly of relatively con­ bioluminescence. Images of Abralia veranyi at 12 and 24 °C were compared with each other and with the digitized photograph of the stant intensity and any changes that did take place were preserved specimen using geometric correction algorithms to cor­ gradual. Any manipulation of the squid was liable to rect for scale differences and geometric distortions between images . induce a very rapid and bright flash from one or more of Comparisons ofimages were made by subtraction. Possible intensi­ the subocular photophores (usually the large posterior ty or size differences between emitting photophores at the two organ). The pattern of visible mantle photophores temperatures were examined using object analysis algorithms as changed regularly with the respiratory pulsations of the well as by real-time pseudocolour analysis ofvideo playback. Biolu­ minescence images were enhanced and sharpened prior to pho­ mantle musculature (Fig. 1). This pattern change is prob­ tographing digitized images from a high-resolution video monitor. ably exaggerated in the experimental situation by virtue Bioluminescence spectra were measured with an EG & G Prince­ of the fact that the squid is unnaturally flattened against ton Applied Research Model 1460 optical multichannel analyser the bottom of the dish during the inhalant pulse. The (OMA) using a linear array detector consisting of 700 intensified respiratory pulse rate at 24°C was substantially higher photodiodes (Model 1420 detector). Details of the OMA operation than that at 12"C. and calibration have been described by Widder et al. (1983). Specimens were maintained in a glass crystallizing dish in sea water at the experimental temperature and mounted above the vid­ Spectral measurements eo camera, which therefore viewed the squids from below. The bioluminescence of the ventral mantle was passed through a quartz Flashes from the subocular photophore (only measured glass-fibre optic of 5 mm diameter to the collection optics of the at 24 °C) had a unimodal emission maximum at OMA. Water-temperature changes were achieved by changing the ~475 nm, with a full width at half maximum (FWHM) sea water in the dish rather than by transferring the specimen . A short ( - 5 min) period of acclimatization preceded each set of ob­ of 82 to 83 nm (Fig. 2A). The array of ventral mantle servations. photophores at 24°C had a Am • x at 489 to 492 nm and an FWHM of47 to 66 nm, with a distinct shoulder at about 440 nm. At 11°C there was no short-wavelength shoul­ Results der, }'m.x was between 487 and 494 nm and FWHM was 54 to 75 nm (Fig. 2 B). The main distinction between the Visual observations two temperatures was the appearance of the short-wave­ In most cases, Abralia veranyi was spontaneously lu­ length shoulder at the higher temperature. This spectral minescent when brought into the dark room. Individuals change was easily and repeatedly reversible. Fig. 1. Abralia veranyi (life size) at 12°C. (A) Photophore pat­ tern with mantle contracted; (B) 10 video frames later, mantle ex­ panded; (C) 10 frames later, mantic contracted; (D) 10 frames later, mantle expanded P.1. Herring et al.: Bioluminescence of Abralia 295 A 350 400 450 550 600 650 700 Wavelength (nm) B Fig. 3. Abralia veranyi ( x 1.3) at 12°e (lower) and 24°e (upper). Note extr a rows of later al tentacular photophores in lower video­ 350 400 450 500 550 600 650 700 frame. This was also seen in some frames at 24"C, and was probably Wavelength (nm) a function of tent acle orientation Fig. 2. Abralia veranyi. Spectral distribution of biolum inescence emission of (A) posterior ocular photophore at 24°e and (B) ven­ tral mantle at 11 and 24°e to 6, and smaller, much more numerous ones. The larger photophores are further separable into refractive and non-refractive types, each horizontal band being com­ Video recordings of photophore illumination posed of one type only. The smaller photophores are less regularly arranged and also comprise two visibly differ­ Images of the pattern of photophores illuminated at 12 ent types, one of simple appearance and with an opaque and 24 °C are shown in Figs.
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