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Bioluminescence of the Poecilostomatoid Copepod Oncaea Conifera

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Bioluminescence of the Poecilostomatoid Copepod Oncaea Conifera l MARINE ECOLOGY PROGRESS SERIES Published April 22 Mar. Ecol. Prog. Ser. Bioluminescence of the poecilostomatoid copepod Oncaea conifera Peter J. Herring1, M. I. ~atz~,N. J. ~annister~,E. A. widder4 ' Institute of Oceanographic Sciences, Deacon Laboratory, Brook Road Wormley, Surrey GU8 5UB, United Kingdom 'Marine Biology Research Division 0202, Scripps Institution of Oceanography, La Jolla, California 92093, USA School of Biological Sciences, University of Birmingham, Edgbaston. Birmingham B15 2TT, United Kingdom Harbor Branch Oceanographic Institution, 5600 Old Dixie Highway, Fort Pierce, Florida 34946, USA ABSTRACT: The small poecilostomatoid copepod Oncaea conifera Giesbrecht bears a large number of epidermal luminous glands, distributed primarily over the dorsal cephalosome and urosome. Bio- luminescence is produced in the form of short (80 to 200 ms duration) flashes from withrn each gland and there IS no visible secretory component. Nevertheless each gland opens to the exterior by a simple valved pore. Intact copepods can produce several hundred flashes before the luminescent system is exhausted. Individual flashes had a maximum measured flux of 7.5 X 10" quanta s ', and the flash rate follows the stimulus frequency up to 30 S" Video observations show that ind~vidualglands flash repeatedly and the flash propagates along their length. The gland gross morphology is highly variable although each gland appears to be unicellular. The cytoplasm contains an extensive endoplasmic reticulum. 0. conifera swims at Reynolds numbers of 10 to 50, and is normally associated with surfaces (e.g. marine snow). We suggest that the unique anatomical and physiological characteristics of the luminescent system arc related to the specialised ecological niche occupied by this species. Flashing is interpreted as a defensive response to potential predators. INTRODUCTION Bioluminescence is not secretory but is confined within the glands (Herring 1988) Bioluminescence is a common attribute in the crus- This investigation was undertaken to clarify the tacean order Copepoda, occurring in at least 7 families characteristics of the luminescence of Oncaea conifera (Herring 1988). It is found in most, if not all, species and to compare these with the luminescent systems of of the calanoid families Metridinidae, Lucicutiidae, other copepods. 0.conifera is a widespread and abun- Heterorhabdidae and Augaptilidae. Oncaea conifera dant species in the world oceans, albeit in a variety of Giesbrecht (family Oncaeidae) is, however, the only morphological forms (Moulton 1973, Malt 1983a). It is poecilostomatoid species known to be luminescent. found at epi- meso- and bathypelagic depths (Malt The luminescence of this species was first reported 1983b) and may contribute a significant proportion by Giesbrecht (1895) in specimens from the Gulf of of the potential luminescence of the zooplankton com- Naples (Italy). He noted that the females had at least munity. 70 luminous glands of variable shape and that those of the smaller males were similar but fewer in number. The luminescence of calanoid copepods is visibly MATERIALS AND METHODS secretory in nature and is dispersed into the water by the movements of the animal (Bowlby & Case 1991a, Copepods were obtained mainly from the eastern Widder 1992, Widder & Herring unpubl.). The glands North Atlantic, on cruises of RRS 'Discovery' between are usually large and the secretory material is vesicu- 1981 and 1990, using a rectangular midwater trawl lar or granular in nature (Bannister & Herring 1990, with a 1 m2 mouth area (RMT1) and a mesh of 330 pm Bowlby & Case 1991b). Giesbrecht (1895). however, (Roe & Shale 1979). Additional specimens were ob- noted that those of Oncaea conifera were different. tained from the Santa Barbara Channel and Monterey O Inter-Research 1993 298 Mar. Ecol. Prog. Ser. 94: 297-309, 1993 Bay (Pacific Ocean) in 1989. Specimens for quantum Quantum emission. Measurements of quantum emission measurements were collected in the Alboran emission and kinetics of mechanically stimulated Sea (western Mediterranean Sea) in April 1991 and in flashes were made in a 6 in (= 152 mm) diameter inte- the eastern North Atlantic in May 1991, using 0.5 or grating sphere collector (Labsphere, Inc.) coupled to a 0.75 m diameter conical nets towed for 15 min at 2 in (= 51 mm) diameter Burle 8850 photon-counting approximately 0.5 m S-'. Specimens were obtained photomultiplier tube (see Latz et al. 1990 for details). from a depth of 30 m in April 1991 and 100 to 170 m in Because the integrating sphere is a 4.rr collector it May 1991, and were individually sorted into vials of measures total flux. Flashes were elicited by motor filtered seawater and dark acclimated at 13 or 8OC, stirring, using either brief (< 1 S) pulses or a constant respectively, for 18 to 23 h prior to testing to allow re- speed of 2000 rpm. Photomultiplier output was con- covery of bioluminescence reserves (Latz et al. 1990). verted to square wave (TTL) pulses by an amplifier/ Video recording. Characterization of the biolurni- discriminator (Pacific Instruments, model AD6). Pulses nescence requires information on the quantum yield were counted in 10 ms time bins by an EG & G Ortec and kinetics of individual flashes, the flash capabilities ACE multichannel scalar operating in an IBM com- of individual copepods and the responses of individual patible PC. Records were of 40 S duration and were glands. The latter information can only be obtained stored on disk for later analysis. Quantum calibration from videorecordings of flashing copepods; these allow was determined by using an NIST-referenced multi- the time course of the luminescence of individual spectral source (Optronic Laboratories, model 310) to glands to be followed. measure the spectral responsivity of the system. Based Three systems (available at different times and on the emission spectrum of Oncaea conifera (see places) were employed for recording bioluminescence below) a responsivity value of ca 5.8X lo3photons TTL or swimming patterns. One system, used at sea, was pulse-' was calculated. the Mixed Light Imaging System (MLIS) which uses Flashes were analyzed for the following variables strobed infra-red illumination with an exposure time (Latz et al. 1990): rise time, maximum flux, E-folding of 13 to 33 vs at a frequency of 60 Hz (Widder 1992). time (time from maximum flux to l/e of maximum; its Earlier video microscopy recordings of biolumines- reciprocal gives the rate of exponential decay), decay cence were also made at sea with a Delnocta triple time (based on 97 % decay), total duration, flash quan- stage image-intensifier mounted on a Vickers M41 tum emission, total stimulable luminescence (TSL) for Photoplan microscope and coupled to a National all flashes specimen-', proportion of TSL in a single Panasonic Newicon videocamera. In the laboratory at flash, and total flashes specimen-'. Because these Santa Barbara (California,USA), a Dage 66 ISIT video- variables displayed a lognormal rather than a normal camera mounted on a Zeiss IM35 inverted microscope distribution, values represent the geometric means was used. For the MLIS recordings the copepods were and error based on the antilogarithms of the confi- free-swimming in aquaria (35 X 15 X 60 mm). Video dence limits of the log-transformed data (Sokal & Rolf microscopy recordings were made with the specimen 1981). Statistical significance is based on the 5% held in a drop of seawater on a microscope slide. probability level. Video recordings of swimming pattern were analyzed Spectral emission and fluorescence. The emission with a Megavision 1024XM image-analysis system. spectra of mechanically stimulated specimens were Each video frame was separated into individual fields obtained with an EG & G Princeton Applied Research and missing interlace lines filled as a mathematical Model 1460 optical multichannel analyser (OMA) average of the lines above and below them. For each operated and calibrated as described by Widder et swimming track 96 consecutive fields were mathemati- al. (1983). cally combined and thresholded, producing a cumula- Fluorescence observations on live copepods were tive image of 96 strobes at a frequency of 60 Hz. made with a Vickers Photoplan microscope and long Electrical stimulation and recording. Copepods wavelength ultraviolet incident illumination, viewed were placed between 2 platinum electrodes and stimu- through a GG40 + 2E barrier filter. Photographs lated electrically with a Grass square-wave stimulator. were taken on Tri-X film. Fluorescence spectra The luminous responses were either videorecorded were recorded with the same system coupled by a as described above or detected with an EM1 6097s fibre optic to the spectral analysis system described photomultiplier operated at 1200 V and an analogue by Herring (1983). recording made on an S. E. Laboratories ultraviolet Microscopy. Specimens were fixed for light and oscillograph. Electrical stimulation provides a quanti- electron microscopy in 2.5 % glutaraldehyde in phos- tatively repeatable and defined stimulus of short phate buffer pH 7.4, postfixed in 1 O/o osmium tetroxide, duration, allowing a clearer analysis of the flash para- dehydrated in a graded ethanol series and taken into meters. Taab Ltd Prernix medium grade resin via propylene Herring et al.: Bioluminescence of Oncaea conifera 299 oxide. Light microscope sections were cut on a Huxley The luminous glands could usually be readily identi- Ultratome and stained with 1 % toluidine blue
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