biology – pwoerpoint 2 slide
\nA deepwater fish with \u2018lightsabers\u2019 \u2013
\ndorsal spine-associated luminescence in
\na counterilluminating lanternshark
\nJulien M. Claes1
\n, Mason N. Dean2
\n, Dan-Eric Nilsson3
\n, Nathan S. Hart4 & Je\u00b4ro\u02c6me Mallefet1
\n1
\nLaboratoire de Biologie Marine, Earth and Life Institute, Universite\u00b4 catholique de Louvain, 1348 Louvain-la-Neuve, Belgium, 2
\nDepartment of Biomaterials, Max Planck Institute of Colloids and Interfaces, 14424 Potsdam, Germany, 3
\nLund Vision Group, Lund
\nUniversity, 22362 Lund, Sweden, 4
\nThe School of Animal Biology and The Oceans Institute, The University of Western Australia,
\nCrawley, WA 6009, Australia.
\nWe report the discovery of light organs (photophores) adjacent to the dorsal defensive spines of a small
\ndeep-sea lanternshark (Etmopterus spinax). Using a visual modeling based on in vivo luminescence
\nrecordings we show that this unusual light display would be detectable by the shark\u2019s potential predators
\nfrom several meters away. We also demonstrate that the luminescence from the spine-associated
\nphotophores (SAPs) can be seen through the mineralized spines, which are partially translucent. These
\nresults suggest that the SAPs function, either by mimicking the spines\u2019 shape or by shining through them, as
\na unique visual deterrent for predators. This conspicuous dorsal warning display is a surprising complement
\nto the ventral luminous camouflage (counterillumination) of the shark.
\nI
\nn the permanent darkness of the deep-sea a surprising diversity of organisms, from bacteria to fish, have
\nevolved the capability to produce a visible light1,2. This bioluminescence comes from a chemical reaction1\u20133 that
\noccurs either in the exterior environment or within cells; these photogenic cells (photocytes) are often
\nembedded in organs called photophores that can reach a high degree of sophistication, including reflectors, light
\nguides, wavelength-specific filters and optical lenses4\u20136. Numerous adaptive benefits have been suggested for
\nbioluminescent glows and flashes (light emission , 2 s), all falling in the three functional categories essential to an
\norganism\u2019s survival: predator evasion, food acquisition and reproduction1\u20133,7.
\nIn the mesopelagic zone (200\u20131000 m), many animals produce a continuous ventral glow to match downwelling
\nsunlight and conceal their silhouette from organisms swimming beneath them, a process called counterillumination2,8,9.
\nConversely, dorsal glows are rarely observed in this environment, probably because they are
\nhighly detectable against the darker background of deeper waters when viewed from above. As a consequence,
\nsuch conspicuous displays are usually of a predatory nature, produced by \u2018anatomical fishing lures\u2019 that attract
\nprey from a distance2,7. Probably because of the stark difference in the apparent roles of dorsal and ventral
\nluminescence, dorsal and ventral photogenic organs are rarely observed to glow concomitantly in the same
\nmesopelagic organism10. Here, however, we report a particular exception where the dorsal glows of a deepwater
\nshark might actually complement the counterilluminating luminescence produced by its ventral photophores.
\nThe velvet belly lanternshark, Etmopterus spinax, is a diminutive shark (# 60 cm in total length) that spends
\nmost of its time at mesopelagic depths11. Like other members of the Etmopteridae family, E. spinax harbours
\ndefensive mineralized spines in front of its dorsal fins and has a ventral surface covered by thousands of tiny (,
\n200 mm in diameter) photophores11,12. Stimulated by melatonin or prolactin, these organs produce a long lasting
\nblue-green luminescence13. This self-produced light, the chemistry of which remains unknown, provides this
\nlanternshark with a counterilluminating camouflage14 and perhaps aids in intraspecific communication15,16.
\nWhen investigating this species\u2019 bioluminescence, we were surprised to observe glows from the frontal edges of
\nthe dorsal fins, forming conspicuous arcs immediately behind the spines (Fig. 1). This dorsal luminescent display
\nseems in direct conflict with the camouflage role of the ventral photophores. Here we document the structural
\nbasis of this intriguing display and investigate its functional significance. We examined the histology and light
\nemission of the dorsal photophores and determined the 3D structure and spectral transmittance of their associated
\nspines. Using these structural and in vivo luminescence data, ocular measurements from local fishes and
\nmarine mammals and a recent theory for visual detection in pelagic habitats17, we then determined the detection
\nSUBJECT AREAS:
\nBEHAVIOURAL ECOLOGY
\nICHTHYOLOGY
\nTHEORETICAL ECOLOGY
\nANIMAL BEHAVIOUR
\nReceived
\n9 January 2013
\nAccepted
\n4 February 2013
\nPublished
\n21 February 2013
\nCorrespondence and
\nrequests for materials
\nshould be addressed to
\nJ.M.C. (julien.m.
\nclaes@uclouvain.be)
\nSCIENTIFIC REPORTS | 3 : 1308 | DOI: 10.1038\/srep01308 1
\nrange of the luminescence produced by the spine-associated photophores
\n(SAPs) in the shark\u2019s environment, characterizing theirin situ
\nperformance and suggesting their ecological role.
\nResults
\nStructural basis. SAPs form two to four vertical rows on both sides of
\nthe dorsal fins, at a distance of about 1\u20133 mm behind the finspines
\n(Fig. 2a). These organs appear structurally similar to ventral
\nphotophores18, each organ comprising a pigmented sheath covered
\nby one or several lens cells, and enclosing a cluster of photogenic cells
\n(photocytes) containing fluorescent vesicles (Fig. 2b,c). Considering
\nthe relative orientation of lenses and photocytes, SAPs emit most of
\ntheir light laterally, forming sickle-shaped glows on the sides of the
\nleading edges of the dorsal fins, mimicking the curve of the spines
\nanterior to them. Given this intimate association of photophores and
\nspines (Fig. 2d) and that dorsal fins have been shown to rotate during
\nswimming in some shark species19, we examined the potential
\ninteraction of SAP luminescence and spines by measuring the
\nspectral transmittance of these structures. The spines could
\nhypothetically transmit about 10% of the SAP luminescence if the
\ndorsal fins were to rotate laterally during swimming (Fig. 2e).
\nFunctional significance. Ventral photophore and SAP luminescences
\nare long-lasting and their intensities are significantly correlated
\n(Fig. 3a), suggesting a common hormonal control for these
\nphotogenic structures. This information, combined with local
\nenvironmental data and the visual theory developed by Nilsson
\net al.17 allowed us to calculate the depth at which the ventral
\nphotophores provide an optimal counterilluminating camouflage for
\nthe brightest of our specimens (Fig. 3b). This theoretical depth should
\nreflect the preferred depth of the shark in its natural habitat. Using
\nNilsson et al. \u2019s theory again as well as the spine transmittance data and
\nocular anatomy of local fishes and marine mammals, we determined
\nthat, at theoretical counterillumination depth, SAPs can emit a close
\nrange luminescent signal, both around and through the spines, that
\nwould be detectable by most of the shark\u2019s potential predators\u2014but not
\nits main prey\u2014from several meters away (Fig. 3c).
\nDiscussion
\nIn the mesopelagic zone, where most animals\u2014including E. spinax\u2014
\nhave converged on camouflage strategies20, the dorsal long-lasting
\nluminescence produced by the shark\u2019s SAPs appears to be a paradoxical
\nand risky display. As a consequence, a strong adaptive benefit
\nof these intriguing photogenic structures might be expected.
\nWe explored the functional significance of SAP luminescence
\nusing an integrative method involving structural and performance
\ndata and a recent theoretical visual modeling17. This novel approach
\nappears particularly useful to test performance hypotheses involving
\ndeep-sea animals like E. spinax, which live in a largely inaccessible
\nenvironment and demonstrate a physiological fragility that considerably
\nrestricts their use in behavioral experiments. The validity of
\nour modeling was confirmed by the similarity between the theoretical
\ncounterillumination depth (164\u2013254 m deep, depending on
\nsurface light conditions), which suggests the occurrence depth of
\nthe shark, and the actual capture depth of our specimens (170\u2013
\n230 m). At this theoretical counterillumination depth, the particular
\nwindow of detection distances of SAP luminescence would not be
\neffective in prey attraction: our calculations predict that the main
\nprey of the shark (the pearlside fish Maurolicus muelleri)
\n21 can only
\nFigure 1 | Spine-associated bioluminescent display. (a) Location of
\nmineralized finspines in an adult Etmopterus spinax specimen. (b) Closeup
\nof first dorsal spine with SAPs in natural light. (c) Close-up of second
\ndorsal spine with spontaneously glowing SAPs in darkness. (d)
\nSpontaneous luminescence from another specimen of this species showing
\nthe glowing dorsal SAPs (white circles), counterilluminating ventral
\nphotophores14 (CVPs) and lateral photophore areas believed to be
\ninvolved in intraspecific communication15,16: ca, caudal; ic, infracaudal; la,
\nlateral; pe, pectoral. Scale bars, 5 cm.
\nFigure 2 | Structural basis and spatial organization of spine-associated
\nbioluminescent display. (a) Frontal edge of the second dorsal fin in
\ntransversal section (TS; 7 mm) showing the position of SAP rows (red
\narrows). ce, ceratotrichia; pl, pigmented layer. (b) Close-up of a SAP (TS;
\n7 mm) showing the position of photogenic cells (photocytes; white
\narrows). le, lens; ps, pigmented sheath. (c) Same SAP (TS; 7 mm) showing
\nthe autofluorescence of the photocyte vesicles (red arrows) under U.V.
\napplication. (d) Micro-CT of first and second dorsal finspines. Top inserts
\nare transversal sections situated close to the tip and the base. Note how the
\nspine cross-section in 2d have been rotated 90u anticlockwise relative to the
\ncross-section at the top of the figure. Scale bars correspond to 500 mm in
\n(a), (d) and to 150 mm in (b), (c). (e) Spectral transmittance of the spine
\n(grey line) with a superimposed Gaussian spectrum (dashed line) of shark
\nluminescence14. The spine can hypothetically transmit , 10% of SAP
\nluminescence frontally.
\nwww.nature.com\/scientificreports
\nSCIENTIFIC REPORTS | 3 : 1308 | DOI: 10.1038\/srep01308 2
\ndetect SAPs from short distance away (, 1.5 m); conversely potential
\npredators can detect them at several meters. This strongly suggests
\nthat dorsal bioluminescence in the lanternshark serves as a
\n\u2018\u2018predators-eyes-only\u2019\u2019 signal and therefore somehow functions as
\nan aposematic (warning) beacon to deter approaching predators
\n(or conspecifics), albeit without jeopardizing prey capture.
\nThe exact message of this aposematic signal remains unclear and
\nintriguing. Given the particular spatial organisation and close association
\nof SAPs with the defensive dorsal finspines, and the fact that
\nthe finspines are capable of transmitting a portion of SAP luminescence
\n(probably thanks to a reduced enameloid covering compared
\nto the spines of other non-bioluminescent squalid sharks12), we propose
\nthat SAPs evolved as a means of highlighting the spines themselves.
\nDorsal mineralized finspines, sometimes linked to venomous
\nglands, are found in chimaeras and a number of sharks9,22,23. While
\nstingray barbs can be easily whipped into defensive position in the
\nevent of a threat, the dorsal anchoring of the finspines largely restricts
\ntheir use to risky post-capture defensive events as a means of wounding
\nthe soft tissue in the mouth of a biting predator.
\nSAP \u2018\u2018advertisement\u2019\u2019 of these spines\u2014by luminescent strips mimicking
\nspine shape and\/or shining through the spines when the fins
\nrotate\u2014would be particularly advantageous, since it would allow the
\nshark to signal to potential predators from a distance the danger of
\nthe stinging appendages, maybe preventing attacks before they happen.
\nThe high density of E. spinax individuals present in Norwegian
\nfjords24 limit the time between encounters with this species, perhaps
\nfacilitating a predator\u2019s avoidance learning through a succession of
\nunsuccessful predation events.
\nBioluminescent aposematism has been experimentally demonstrated
\nin some terrestrial invertebrates25,26, and suggested for a number
\nof marine animals including cnidarians27, molluscs28, annelids29,
\ncrustaceans30, echinoderms31 and teleost fish32; this, however, is the
\nfirst suggestion of this behaviour in a cartilaginous fish.
\nTransmission of bioluminescent signals by mineralized structures,
\nsuch as the spines of the velvet belly lanternshark, are rare in nature,
\nhaving only been observed in several organisms including opisthoproctid
\nfishes33 and a marine snail (Hinea brasiliana)
\n27. Further
\nexamination of E. spinax\u2019s spines may provide insights into evolutionary
\nco-opting of structural biomaterials for optic functions.
\nAlthough SAPs appear structurally and physiologically similar to
\nthe other photophores harbored by the velvet belly lanternshark,
\ntheir dorsal glow represents a unique bioluminescent display. This
\n\u2018abnormal\u2019 luminescence might also be found in other lanternsharks
\n(Etmopteridae), which harbor similar dorsal finspines and ventral
\nphotophores11. Even though the function of these organs remains
\nhypothetical, they clearly demonstrate that warning luminescence
\nand counterillumination, two apparently contradictory strategies,
\ncould surprisingly operate in a single organism at the same time.
\nMethods
\nSharks. Adult sharks were collected using longlines in the Raunefjord (Norway)
\nbetween December 2009 and October 2012, transferred to Espeland Marine Station
\nand housed in tanks placed in a dark cold room. Our protocol, including fish sacrifice,
\nwas in accordance with national guidelines for experimental fish care (fish handling
\napproval #1664 was given by the National Committees for Research Ethics of
\nNorway).
\nPhotographs of spontaneous luminescence were taken in complete darkness with a
\nCanon 7D camera (whole shark, sensitivity 6400 ISO, objective 20 mm; dorsal fins,
\n12800 ISO, 60 mm; both with an aperture of 2.8 and an exposure time of 30 s). For
\nvisibility purpose, a post adjustment of brightness and contrast was applied to the
\nentire pictures using Adobe PhotoshopH. Other pictures were taken with the same
\ncamera in natural light.
\nLuminescence recording. A Berthold FB12 luminometer coupled to an optical fibre
\nwas used to record in vivo intensity of dorsal and ventral continuous luminescence
\nfrom several live specimens according to Claes et al.14. Values were corrected for fiber
\nabsorption and angular losses. Ventral photophore spacing\/density and mean
\nintensity of specimens was estimated according to Claes and Mallefet15, by counting
\nthe photophores present in standard (0.25 cm2
\n) ventral skin patches under a
\nbinocular microscope.
\nSpine structure. Dorsal finspines were removed from dead specimens wrapped in
\nplastic wrap with a small amount of fluid for hydration, and packed tightly with paper
\ntowels into plastic tubes for micro-CT scanning (1174 scanner, SkyScanH, Kontich,
\nBelgium). The X-ray source was set at 50kVp (peak kilovoltage) and 800 mA; 220
\nproject ( help with nursing paper writing from experts with MSN & DNP degrees)ions were acquired over an angular range of 360degrees. Samples were scanned
\nwith an isotropic voxel size of 16.8 mm, an integration time of 4500ms, and a 0.25mm
\naluminum filter to decrease beam-hardening effects. Scans were reconstructed using
\ncommercial software (NReconH SkyScanH software, version 1.6.1.2) then visualized
\nin 3d and segmented virtually in multiple planes using Amira software (Mercury
\nComputer Systems) to examine spine structure and morphology.
\nHistology. Skin tissues containing SAPs from dorsal fins of freshly dead specimens
\nwere excised and fixed in a 3.5% formaldehyde solution for two weeks. Tissues were
\nprogressively dehydrated (50, 70, 2 3 90%, 1 hour each), placed 1 h in 100% butanol
\nand left overnight in 100% butanol at 60uC. Tissues were then submerged in paraffin
\nwax for different periods (12 h, 1 h and 3 h) at melting temperature (58uC). Sections
\nwere performed with a metal knife microtome, stained using Masson\u2019s trichrome, and
\nphotographed under a light\/fluorescence microscope (Leitz Diaplan, Leitz, Wetzlar,
\nGermany).
\nSpine transmission. The second dorsal finspines of freshly dead specimens were
\nremoved and their anterior-posterior spectral transmittance was measured near the
\ntip, at 75% of the exterior spine length, using an Ocean Optics S2000
\nspectroradiometer. Broadband white light from an Ocean Optics PX-2 pulsed xenon
\nlamp was delivered to the caudal surface of the spine via an optical fibre terminated
\nwith a quartz lens. Light transmitted anteriorly by the spine was collected via a second
\nquartz lens coupled to an optical fibre connected to the spectroradiometer.
\nVisual modeling. The visibility ranges of both ventral and dorsal glows were
\ncalculated according to the theory developed by Nilsson et al.17. This range depends
\non the intensity of down-welling daylight and thus on depth in the sea. Etmopterus
\nspinax was assumed to occur at \u2018counterillumination depth\u2019 where its silhouette,
\nFigure 3 | In vivo recordings and visual modeling of Etmopterus spinax luminescence. (a) Correlation between SAP (from the second dorsal fin) and
\ncounterilluminating ventral photophore (CVP) luminescence intensity (I). Mq s21
\n, megaquanta (106 photons) per second. (b) Detection of CVP
\nluminescence as a function of the shark\u2019s occurrence depth for heavy overcast and clear skies (sun at 45u). Counterillumination occurs when detection 5
\n0. (c) Detection distance of SAP luminescence at counterillumination depth as a function of the pupil diameter of the observer. This distance is calculated
\n(1) around or (2) through the spine, assuming 10% transmission. Dots represent pupil diameter of the shark (grey), its main prey (the pearlside fish
\nMaurolicus muelleri; white) and its potential predators (piscivorous fishes and marine mammals; black).
\nwww.nature.com\/scientificreports
\nSCIENTIFIC REPORTS | 3 : 1308 | DOI: 10.1038\/srep01308 3<\/p>\n","protected":false},"excerpt":{"rendered":"
biology – pwoerpoint 2 slide A deepwater fish with \u2018lightsabers\u2019 \u2013 dorsal spine-associated luminescence in a counterilluminating lanternshark Julien M. Claes1 , Mason N. Dean2\u2026<\/p>\n","protected":false},"author":1,"featured_media":0,"comment_status":"open","ping_status":"open","sticky":false,"template":"","format":"standard","meta":{"footnotes":""},"categories":[8827,10099,10540,10536,10892,10538,10539,10537,10891],"tags":[10549,10616,10615,7687,10627,8857,10552,10295,10548,10622,8907],"class_list":["post-130387","post","type-post","status-publish","format-standard","hentry","category-australia-essays","category-buy-essay","category-cheap-essay-writers","category-get-assignments-done","category-page-paper","category-phd-essay-writers","category-research-paper-writing-service-for-any-topic","category-study-bay-essay","category-write-my-assignment-ireland","tag-ai-plagiarism-free-essay-writing-tool","tag-australian-best-tutors","tag-best-trans-tutors","tag-buy-essay-uk","tag-cheap-dissertation-writer","tag-help-with-writing-an-essay","tag-help-write-my-paper-ai-free","tag-homework-for-you","tag-online-essay-writers","tag-phd-essays","tag-write-my-essay-for-me"],"_links":{"self":[{"href":"https:\/\/www.studyproessays.com\/help\/wp-json\/wp\/v2\/posts\/130387","targetHints":{"allow":["GET"]}}],"collection":[{"href":"https:\/\/www.studyproessays.com\/help\/wp-json\/wp\/v2\/posts"}],"about":[{"href":"https:\/\/www.studyproessays.com\/help\/wp-json\/wp\/v2\/types\/post"}],"author":[{"embeddable":true,"href":"https:\/\/www.studyproessays.com\/help\/wp-json\/wp\/v2\/users\/1"}],"replies":[{"embeddable":true,"href":"https:\/\/www.studyproessays.com\/help\/wp-json\/wp\/v2\/comments?post=130387"}],"version-history":[{"count":0,"href":"https:\/\/www.studyproessays.com\/help\/wp-json\/wp\/v2\/posts\/130387\/revisions"}],"wp:attachment":[{"href":"https:\/\/www.studyproessays.com\/help\/wp-json\/wp\/v2\/media?parent=130387"}],"wp:term":[{"taxonomy":"category","embeddable":true,"href":"https:\/\/www.studyproessays.com\/help\/wp-json\/wp\/v2\/categories?post=130387"},{"taxonomy":"post_tag","embeddable":true,"href":"https:\/\/www.studyproessays.com\/help\/wp-json\/wp\/v2\/tags?post=130387"}],"curies":[{"name":"wp","href":"https:\/\/api.w.org\/{rel}","templated":true}]}}