The Luminescence of Some Deep-sea Fishes of the Families Gadidaeand Macrouridae

YATA HANEDAl

INTRODUCTION

WHILE STUDYING THE J APANESE FISH Pbysi­culus japonicum Hilgendorf, of the familyGadidae, Franz (1910) noticed a round blackpigmented spot situated ventrally and infront of the anus. He studied its structure, butwas unable to explain its physiological func­tion.

Later Kishitani (1930) examined this organand discovered it was an open type of lumi­nous organ containing symbiotic luminousbacteria. He described its structure and gavea specific name to the bacterium, Micrococcusphysiculus. He could not see any luminositywhile the fish was living under natural con­ditions, and concluded that the luminousorgan merely produced luminous bacteriawhich were ejected occasionally as a lumi­nous cloud into the surrounding sea water.

In August, 1936, I had an opportunity toobserve this fish in the dark in an aquariumtank at the Asamushi Marine BiologicalStation of Tohoku University. Among manyother fishes in the tank, I saw one which Ihad never seen before, which emitted lightfrom this ventral spot. It did not eject aluminous Cloud of matter .

In August, 1937, I observed another speciesof the Gadidae, Lotella phycis Temm. & Schl.,which also possessed a similar type of lumi­nous organ, from the duct ofwhich I was ableto culture luminous bacteria in artificialmedia.

The fishes of the family Macrouridae areclosely related to the Gadidae and have aluminous organ of the same type. Their

1 Tokyo J ikeikai Medica l College, Tokyo, J apan.Manuscript received Januaty 26, 1949.

luminosity was first recorded by Osorio(1912). One species of the family, Malaco­cephalus laevis (Lowe), has the same type ofluminous organ, similarly situated. Osoriostated that it was a practice of the Portuguesefishermen to force luminous matter from theorgan by pressing it against pieces of sharkflesh which they used as bait . In this way theflesh became luminous, and so was improvedas bait for their fishing. This led him to be­lieve that the luminous matter consisted ofluminous bacteria, but since he was unableto culture any he could not confirm his belief.

. Hickling (1925, 1926) described the struc-ture of the luminous organ of this fish, andstated that it was of a new type, the luminousmatter in the organ consisting of luminousgranules. In 1931 the same author describedthe lumino us gland of Coelorhynchus coelorhyn­chus Risso, also as a new type of luminousorgan containing a luminous granular sub­stance.

Yasaki and Haned·a (1936) reported thatthere were 10 species of the Macrouridae withlumin ous organs, from the ducts of whichthey cultured luminous bacteria in artificialmedia.

In 1938 I examined Malacocephalus laevis,described its luminous organ and the con­tents, and cultivated luminous bacteria fromit . Imai (1942) made bacteriological examina­tions of material from five species of theMacrouridae.

Recently Parr (1946) has studied manymacrourid fishes of the western North At­lantic and the Central American seas. Herecognized the outer aspect of the luminousorgans on the ventral regions of fishes of thegenera Hymenocephalus, Malacocephalus, Ven-

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Luminescence of Deep-sea Fishes- HANEDA

trifossa, Nezumia, Grenurus, Trachonurus, andCoelorhynchus as a lens-shaped body, or scale- .less "fossa" or naked area.

I have collected and studied the compara­tive structures of the luminous organs ofmany specimens of variou's-species, and Ihave also cultivated their bacteria in artificialmedia. The results of these observations arepresented here.

Acknowledgment: I wish to express my sin­cere gratitude to Dr. PIetsch, Scientific andTechnical Division, ESS, GHQ, SCAP, whohelped me in gaining publication of thispaper.

MATERIAL

Altogether I have examined material fromtwo species of the Gadidae and 14 species ofthe Macrouridae. .

The Gadidae are comparatively shallow­water fish. They may be caught close to thecoast of Japan. Physiculus japonicus occurs inwater varying in depthfrom 30 to 50 fathoms.Lotellaphycis is sometimes taken in extremelyshallow water near the surface. This enablesone to keep them in an aquarium tank whereeach can be observed in a natural state . Theymay be caught at any time of the year byhook and line, and their luminosity may beseen if they are taken during the darkness ofthe night. Physiculus japonicus is occasionallytaken by trawlers.

The Macrouridae are always caught bytrawlers since they are deep-water fishes livingin over 100 fathoms of water. They are takenmost abundantly during the winter in Japan.

STRUCTURE OF LUMINOUS ORGANS

Studies made up to the present time showthat the Gadidae and Macrouridae possessthe same open type of luminous organs.These organs may consist of the followingfour components: (a) A luminous gland; (b)its canals and their openings; (c) lenses withan external ventral aperture covered with athin transparent skin through which light istransmitted; and (d) a reflector and chroma-tophores. .

373

In some species the luminous gland maybe so small as to be almost invisible. Thecanal leading from the gland may be eithervery short or very long. The structure of thelens may be very complicated, or very simpleand inefficient. The reflector may vary also inits efficiency according to its structure.

The external ventral aperture · throughwhich light is transmitted is visible externallyand may be comparatively large, or verysmall, or it may be absent. It may be bean­shaped, or circular, or very long and filiform,and in some species there may be two ex­ternal apertures . The figures illustrate themany forms which , can be seen. In the firsttype the luminous organ is very small andbarely visible (as in Coelorhynchus anatirostris).It has a very short luminous duct, and issituated very close to the anus ·lying ven­trally in the muscles, and has neither reflector,lens, nor externalaperture. The organ cannotbe seen externally, and gives the impressionthat it does not exist. Only when the fish issectioned longitudinally and a cut is madethrough the organ can it be seen that thereis a luminous duct which is extremely smalland inefficient. In this duct are luminousbacteria . Although it is vestigial, it is never­theless a true luminous organ, difficult as itis to determine.

Coryphenoides garmani and . C. misakius aretwo other species which have very short andinefficient luminous ducts . The lenses andexternal apertures are inefficient, and from acasual inspection it is difficult to say whetherthey are luminous or not. However, luminousbacteria live in the duct of the gland.

In what may be considered the normal typeor the typical luminous organ-such as thatfound in Physiculus japonicus, Lotella phycis,Abyssicola macrochir, Coelorhynchus kishinouyei,Coelorhynchus japonicus, and Nezumia condylura-the organ consists of a rather large lumi­nous gland, the reflector, the lenses, and ascaleless external aperture covered with thintransparent skin . The canal in some speciesis rather long and in others very short; for

374

FIG•. 1. Diagrams of rhe luminous organs of someM acrouri dae. a, Coryphaenoides garmani; b, A byssico/amacrochir; c, Coe/orhynchus japonicus; d, Coelorbyncbushubbsi. ph or, lum ino us organ; an , anus.

example , C. japonicus has a very short canalwith the external aperture close to the anus .

Some species have two scaleless externalventral apertures. Examples of this type areMalacocephalus laevis (Lowe) and Malaco­cephalus nipponensis, each of which has twoexternal apertures, one bean-shaped and oneround . The inner structure is of the normaltype, i.e., it has a large luminous gland , a re­flector, two lenses, and two external aper­tures. Their structure has been described byboth Dr. Hickling and myself.

The canal is very long in some species,such as CoelorhynchusparalMus and C. tokiensis.The canal itself functions as a lum inou s glandwith a long reflector, a poor lens substance,and no external aperture. However, one cansee the long luminous duct through thetransparent scales on the lowest part of thesbdomen.

PACIFIC SCIENCE, Vol. V, October, 1951

~W. pliot Y

FI G. 2. M a/acocepha/us /aevis (Lowe). phot , lurni­nous orga n; an, anus.

In their young stages these fishes are verystrange, and only in this stage are theystrongly luminous, the luminosity beingvisible ventrally as a single line . When fullgrown, this thin duct is covered with blackpigment, which renders it useless as a lumi­nous comp onent in spite of the fact thatluminous bacteria are living within it . Theluminosity of Coelorbyncbus coelorhynchus, asdescribed by Hickling (1931), may be due tothe fact that perhaps he saw a young speci­men , as it is probable that this species is verysimilar to the two species under discussion.

Coelorhynchus hubbsi Matsub ara has an ex­tremely thin, long canal, each end of whichis swollen into a club-shaped gland . The

FI G. 3. Diagram of rhe luminous organ of Coelor­byncbns para//e/us and its lon gitu din al section. phor,lum inous gland ; refl, reflector; cond, .conduit; chr ,chromatophore; an, anus; recr, rectum.

·Luminescence of Deep-sea Fishes - HANEDA

TABLE 1

D ATA ON C OLLECTIONS OF L UMINOUS GADIDAE AND MACRO URIDA E

375

SPECIES PLACE OF COLLECTION DAT E OF COLLECT ION

Coryphaenoides garmani Jordan and GilbertSagarni-Sok odara * _

Coryphaenoides misakius J ord an and GilbertMi saki-Sokodara*

Abyssicola macrochir Gunther ' .Ten aga-dara*

Coelorhynchus anatirostris J ordan and GilbertNe zumi-Hige "

Ch6 shi fish marker, Chiba Prefectu re . . N ov., Dec., 1934Mimase fish marker , K6chi Prefecrure J an., Mar., 1935

Choshi fish marker. . . . . . . . . . . . . . . . . . . N ov., Dec. , 1934J an., Mar., 1935Jan., 1936

Ch6shi fish market . . . . . . . . . . . . . . . . . . . Ocr., N ov., Dec ., 1934Feb., Mar., 1935

Ch6shi fish marker. . . _ _. . . . . . Nov., D ec., 1934Feb., 1938

C.[aponicusTemm. and Schl. . ." . . . . . . . . . . .. M imase fish market : . . . . . M ar., 1935Tojin * Feb., 1938

C. kiJhillOuyei J ord an and Snyder . . _. . . . . . . . Numazu fish market, Shizuoka Prefecture Mar., 1935Mu gu ra-hige * He ra fishing village, Shizuok a Prefecture Mar., 1938

C. para/Mus Gu nth er. . . . . . . . . . . . . . . . . . . .. Mimase fish marker. . . . . . . . . . . . . . . . . . J an., Mar., 1935Soroi-hige * - Mar., 1938

C. tokiensis Steindachner and D iiderlein ', M imase fish marker. J an., Mar., 1935Nezumi*

C. bubbsi Matsubara , . . . . . . . . . . . . . . . . . . . . Mimase fish market .. ... _. . . . . . . . . . . . N ov., 1934M oyo-Hige" Mar., 1935

Mar., 1938

N ezumia condy/ura J ordan and Gilbert . . . . . . Ch6 shi fish marker . . . . . . . . . . . . . . . . . . . Nov. , Dec ., 1934Nezurni- dara* Mar., 1935

M a/acocepha/uJ laeuis (Lowe) ' .' . . . . . .. Mimase fish market ' " Apr., 1935J an., Apr ., 1936

Hymenocepha/uJJtriatiJJimuJJordan and Gilbert Mimase fish marker. _. . . . . . . . . . . . . . .. Apr ., 1935Suji-dara* Apr., 1938

H. Kuronumai Karnohara _. .. Mimase fish marker. _. . . . . . . . . . . . . Mar., Apr. , 1938Yari-dara*

H. gracilis Gilbert and Hubbs . . . . . . . . . . . .. Mimase fish market . . __ . _. .. _. . . . . . . . Mar., Apr ., 1938H oso-suji-dara*

Pbysiculus japonicus Hilgend orf. .Chigo -dara*

Mimase fish market .Choshi fish markerAsamu shi Marine Biological Station ,

Aomori PrefecrureM isaki fish market, Kanagawa Prefecture

J an., Apr ., 1935Apr. , i 937Aug ., 1938

Aug., 1938

L otella pbycis Te mm. and SchI.. . . . . . . . . . . . Misaki M arine Biolo gical Station , Kana- Aug. , 1938gawa Prefecture

* J apanese name.

376

ventral area is scaleless and there are two ex­ternal apertures . Behind the swelling at theposterior end is a reflector. By examiningfresh material in the dark, two luminouspoints can be seen.

The combination of a very long canal anda compound lens occurs in some species, suchas Hymenocepbalus striatissimus Jordan andGilbert, H. gracilis Gilbert and Hubbs, andH. kuronumai Kamohara. In these there is along, thin canal at the end of which is a club­shaped luminous gland to which is attached ,ventrally, a swollen pouch-shaped body. Thisis a lens. Just behind and below it in the skinof the abdomen is a swelling which is doublyconvex. This is a second lens which directsthe light ventrally to the outside. It is a verycomplex organ . This type of luminous organhas already been reported , by Vinciguerra(1932) .

~ .

Q ' ""'I~

--=--~;....--'_...,""\,~l:~st an .

~;:='~~~):~~ . . , an

\ . l\.nt dond .l.~st.

FIG. 4. Diagram of the luminous organ of Hymen­ocephalus kuronumai and its longitudinal section. phor, .luminous gland; Lest, external lens; Lint, internal lens ;cond , conduit ; an, anus; rect, rectum ; op, opening ofconduit,

All of these are luminous glands and theirinnermost surfaces are lined with a layer ofepithelial cells. Within the cavities formed by

.the folds of the glands resting on the inner

PACIFIC SCIENCE, Vol. V, October, 1951

ends of the epithelial cells are other cellswhich contain capsules in which are massesof bacteria, variously arranged. Some of thesecapsules are entire and contain the bacteria,others are ruptured and have allowed thebacteria to escape into the fluid of the glandducts. Hickling says these masses are gran­ules of luminous matter and thar they existin four states, viz.: (a) as closely packedmasses filling their capsule; (b) as closelypacked masses, but only half filling their cap­sule; (c) as loosely packed individuals in aruptured capsule ; and (d) as dispersed in­dividuals free from their now empty capsule.

Both Kishitani and I, however, considerthese so-called luminous granules to bemasses of luminous bacteria. We have ex­amined a great amount ofmaterial from manyspecies and it all shows the same character­istics.

LUMINOUS PHENOM ENA OF THESE ORGANS ,

WHEN SEEN IN DARKNESS

Inasmuch as Lotell« phycis and Physiculusjaponicus live in comparatively shallow water,they can be kept in aquaria where their lu­minosity, if visible, could be seen in the dark.I have kept many specimens under observa­tion but almost all of them displayed noluminosity which could be seen externally.

In August, 1936, while working at the. Asamushi Marine Biological Station , I had a

further opportunity to observe these fishes inthe dark. Among many specimens of Pbysi­culusjaponicus in an aquarium tank , I saw onefish with a luminous ventral aperture . Thisaperture could be seen only when the fishswam upwards and thus showed its ventralsurface. It could not be seen when it swamdownwards from the top of the tank, show­ing only its dorsal surface, or when it swamhorizontally , showing either one of itslateral surfaces.

I could not see any luminous, cloudy dis­charge from the opening, as had been sug­gested, and this led me to believe that theluminosity arose from a true luminous organ,

Luminescence of Deep-sea Fishes- HANEDA

and that the difficulty in seeing it was due tothe expansion of the chromatophores in thetransparent, scaleless skin which covers ' theoutside of the aperture. When these chroma­tophores expand they shut off the light andwhen they contract the light is transmittedand can be seen. Possibly the expansion andcontraction may be determ ined by the watertemperature, the degree of darkness or light,or by other factors , but I did not determinethe effects of these factors upon the func­tioning of the chromatophores.

However, from my observations I am ofthe opinion that when these fishes are swim­ming in natural conditions at the bottom ofthe sea they are normally luminous, emittinglight through these ventral apertures.

I have never been able to observe anymacrourid fish in a natural condition sincethey are all deep-sea fish and cannot be kept inan aquar ium . I have been able to examine onlydead and living material freshly caught bytrawlers from deep water . When examiningthis freshly caught material I could see theluminosity of some, but not of others. Whenthe glands were cut open, however, they were

. always luminous.The luminosity of young Coelorhynchus

parallelwmay be seen as a beautiful greenfiliform line on .the ventral surface. Coelo­rhynchus hubbsihas two luminous spots on theventral surface, and I am of the opinion thatthese fishes, when in their natural conditions,normally display their luminosity.

I cannot agree with the opinion that thesefishes, through the opening of the canal inthe anal region, discharge a luminous cloudinto the surrounding sea water.

CONTENTS OF THE LUMINOUS DUCTS

Emulsions of the contents of the ducts weremade in sterile sea water and were examined inthe dark.

When first made, the emulsion was uni­formly luminous. After standing in verticaltubes and settling for 20 minutes, the lumi­nosity had collected as an upper layer. When

377

shaken up , it was again uniformly distributedin the tube. If it was centrifuged, the lumi­nosity was concentrated in the sediment at thebottom of the tube and the fluid above wasclear and not luminous. If this precipitate waswell mixed with sterile sea water the wholemixture became uniformly luminous, but ifit was mixed with sterile distilled water, itfailed to show any luminosity.

Changes of temperature showed the fol­lowing results. Luminosity was greatest be­tween 15 and 23°C. and this is the optimumtemperature; at 0° C. it ceased; at 3--4° C. itwas very weak ; at temperatures between 23°and 45° C. it decreased; above this point itfinally ceased and could not be reactivatedwhen cooled again to 15-23° C.

The reactions were those of luminous bac­teria and an examination under the micro­scope showed bacteria and segments of thegland duct cells. The bacteria stained red withZiehl's solution and I was able to culturethem by the usual bacteriological methods.Samples were taken from the organs of everyfish studied. The characteristics of the lumi ­nous bacteria from the luminous ducts ofmany species of fishes of the Gadidae and theMacrouridae were investigated by the usualmethods of culture in artificial media .

I was able to obtain 10 strains of luminousbacteria from each of these fishes-Lotellaphycis, Malacocephalus laevis, Hymenocepbalasgracilis; 20 strains of luminous bacteria fromCoelorhynchus kish'inouyei and Nezumia ron­dylura; and 14 strains from the other species.

These strains of bacteria were taken fromvarious species of fish taken at different timesand in different localities. All had the samegeneral biological characters but the optimumtemperature, that is, the temperature at whichthe luminosity was greatest, varied. In somecases it was higher than others, but it nevervaried much . The optimum temperature forluminosity was lower for the bacteria of thosefishes which live in 'deep and therefore colderwater than for those ' living in the shallowerand warmer water. A more complete discus-

378

sion of these bacteria will be presented in aseparate paper.

SUMMARY

Some of the fishes belongin g to the familiesGadidae and Macrouridae are luminous andpossess the "open type" of luminous organcontaining luminous symbiotic bacteria. Itconsists of a gland in the ventral muscles lyingin a scaleless depression between the pelvicfins. This is a characteristic of these fishes.Their luminescence is controlled by means ofchromatophores. Normally they are deep-seafishes although at times some of the Gadidaemay be caught in shallow water. Observationswere made on 14 species of the Macrouridaeand 2 species of the Gadidae. Their luminousducts are very similar but vary in size. In somespecies they are very long , in others very

, short, and in others extremely small and notvisible from the outside. Some of the lumin­ous ducts are ora comparatively simple con­struction while others are extremely complex.

I consider the luminous symbiotic bacteriawhich were cultured from th ese many fishesto be a species of the new group of luminousbacteria, but a more complete discussion willbe presented later in a separate paper.

REFERENCES

FRANZ, V. 1910. Die japanischen Knochen­fische der Sammlungen Haberer und Do­flein . Abhandl. Wiss. 11 kl. Sitzber. 4 : 28.

HICKLING, C. F. 1925. A new type of lumi­nescence in fishes. J our. Mar. Biol. Assoc.(0. K.) (n. s.) 13(4): 914-929.

- - - 1926. A new type of luminescence infishes.J our. Mar. Biol. Assoc. (0. K.) (n. s.)14: 495- 506.

PACIFIC SCIENCE, Vol. V, October, 1951

--- 1931. A new type of luminescence infishes, 'III . The gland in Coelorbyncbuscoelorbyncbus Risso. J our. Mar. Biol. Assoc.(Plymouth) 17: 853-875.

HANEDA, Y. 1938. Ueber den Leuchtfisch ,M alacocephalus laevis (Lowe) . J ap. J our.Med. Sci. III. Biophysics Trans. and Abs.5(3) : 355-366.

IMAI, H . 1942. Studies on luminous symbioticbacteria. Seiikai Zasshi 61(4) : 454-467. (I nJapanese.)

KISHITANI, T. 1930. Studien tiber die Leucht­symbiose in Physiculusjaponicus Hilgendorf,mit der Beilage der zwei neuen Arten derLeuchtbakrerien. Tohoku Imp. Univ. Sci.Rpts., 4 Series, Bioi. 5(4): 801-823.

--- 1932. Studien tiber Leuchtsymbi osevon japanischen Sepien. Folia A natomicaJaponica 10(3): 315-413.

M EISSNER, G . 1926. Bakteriologische Unter­suchungen tiber die symbiontischen Leucht­bakterien von Sepien aus dem Golf vonNeapel. Zentbl. f Bakt. , Abt. II. 67(8):194- 238.

PARR, A. E. 1946. The M acrouridae of theWestern North A tlantic and Central AmericaSeas. Bingh am Oceanogr. ColI. Bul. 10: 1­99.

VINCIGUERRA, D . 1932. D el genere Hymeno­cepbalus (H italicus, Gigl. ) An n. M us. a«di Storie Na t. Genova, Estratto 56: 1-13.

YASAKI, Y. 1928. On the nature of theluminescence of the knightfish (Monocen­iris japonicus (Houttuynj) . Jour. Expt . Zool.50(3): 495- 502.

--- and Y. HANEDA. 1935. On the lumi­nescence of the deep sea fishes, familyMacrouridae.OhyoDobutsugaku Zasshi [jour.Appl. Zool.] 7(4) : 165-176. (In J apanese.)