on the development of the californian hag-fish, bdellostoma stouti...

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DEVELOPMENT OF THE CALIFORNIAN HAG-FISH. 269 On the Development of the Californian Hag-fish, Bdellostoma Stouti, Lockington. By Bashford Dean, Ph.D., Columbia College, N.Y. (Preliminary Note.) With Plate 17. DR. HOWARD AYERS, in a lecture before the Wood's Holl Biological Laboratory, 1 has given a detailed account of the occurrence of the Pacific Hag-fish, Bdellostoraa Dombeyi ( = Stouti), in the Bay of Monterey. Its great abundance in this region gave promise of material for the study of the development of a Myxinoid; or, at all events, the chances to obtain these valuable stages seemed far more favorable here than in the European localities, mainly in the North Sea, where the eggs of Myxine had long been sought. Among the zoologists who endeavoured to secure hag-fish embryos in California Professor G\ C. Price, of the Leland Stanford, Junior, University, was the first to succeed, and he has already pub- lished two accounts of his studies. 2 During the past summer additional developmental stages, including a number of the earlier ones, were collected by the present writer during a visit (July, August, September) at the Hopkins Marine Laboratory. 1 1893, Ginn and Co., Boston. s " Zur Ontogenie eines Myxinoiden," ' Sitzungsberichten der mathematisch- physikalischen der K. Bayer. Akad. d. Wiss.,' Bd. xxvi, 1896, Heft 1, S. 67-74. " On some Points in the Development of a Myxinoid," ' Verhandlungen der Anat. Gesellscliaft.'

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DEVELOPMENT OF THE CALIFORNIAN HAG-FISH. 269

On the Development of the Californian Hag-fish,Bdellostoma Stouti, Lockington.

By

Bashford Dean, Ph.D.,Columbia College, N.Y.

(Preliminary Note.)

With Plate 17.

DR. HOWARD AYERS, in a lecture before the Wood's HollBiological Laboratory,1 has given a detailed account of theoccurrence of the Pacific Hag-fish, Bdellostoraa Dombeyi( = Stout i ) , in the Bay of Monterey. Its great abundance inthis region gave promise of material for the study of thedevelopment of a Myxinoid; or, at all events, the chances toobtain these valuable stages seemed far more favorable herethan in the European localities, mainly in the North Sea,where the eggs of Myxine had long been sought. Among thezoologists who endeavoured to secure hag-fish embryos inCalifornia Professor G\ C. Price, of the Leland Stanford, Junior,University, was the first to succeed, and he has already pub-lished two accounts of his studies.2 During the past summeradditional developmental stages, including a number of theearlier ones, were collected by the present writer during avisit (July, August, September) at the Hopkins MarineLaboratory.

1 1893, Ginn and Co., Boston.s " Zur Ontogenie eines Myxinoiden," ' Sitzungsberichten der mathematisch-

physikalischen der K. Bayer. Akad. d. Wiss.,' Bd. xxvi, 1896, Heft 1, S.67-74.

" On some Points in the Development of a Myxinoid," ' Verhandlungender Anat. Gesellscliaft.'

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270 BASHPORD DMAN.

At the request of Mr. J. T. Cunningham, well known for hisinterest in the study of the Myxinoids, the following paperhas been prepared, with a view of presenting in outline themain facts relating to the external development of this re-markable Chordate type.

The hag-fish finds a natural spawning ground in the Bay ofMonterey. Here the spawning appears to take place over awide area, since eggs have been secured at many and distantpoints. The embryos in the writer's collection, however, weretaken from one particular neighbourhood (about a mile offshore, in twelve fathoms of water, sp. gr. l'OSO, temp. 50°—60°F.), which represented doubtless a favorable spawning ground.About one fifth of the eggs here collected were found to yieldembryos, while eggs from other regions rarely contained them,the worthless eggs averaging nearly 98 per cent. In view ofthe present method of collecting, success in obtaining embryosis to a large degree a matter of accident; for the eggs canvery rarely be dredged, probably because they have beendeposited among rock fragments or deep in the mud, as Platesuggests.1 I t is upon trawl-line fishing, as Price has noted,that the collector must finally depend. By this means manyscores and even hundreds of hag-fishes may be caught duringa day's fishing; but among these there will only rarely be onewhich has entrapped an egg-string in its encasing slime.Such an instance is shown in the accompanying figure (fig. 1),from a water-colour sketch by the writer. The hag, reddishpurple in colour, has twisted itself into a knot around thetrawl-line; the slime mass enclosing it is ti'anslucent, whitish,here and there blood-stained; the eggs are tangled securelyin the meshes of the slime, suggesting a string of yellow beans.The eggs, as has often been noted, are fastened together ateither end by clumps of wiry filaments, whose tips interlock.The tips, shown in fig. 2, vary notably in size and form (con-

1 "Ueber die Eier von Bdellostoma Bisclioffii, Schneider," 'Sitzungs-berichten der Gesellschaft naturlbrschender Freunde zu Berlin,' Jahrg.1896, No. 1, S. 17—21.

The writer's material was collected almost entirely from rocky bottom.

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DEVELOPMENT OP THE OALIKMiNIAN HAG-FISH. 271

trast Plate's fig. 3); they are typically flower-shaped, theirbroadly everted petal-like margins enabling them to interlock.

TIME AND MODE OF OVIPOSITION.

Both Ayers and Price have agreed that in the Bay ofMonterey the spawning season of Bdellostoma is an extendedone. These conclusions agree fully with the writer's observa-tions. He has obtained embryos of many ages from the samelocality at the same time; he notes, however, that during thepresent season the embryos were most abundant of a particularsize, a fact which suggests that a time of maximum spawninghad occurred. As to actual oviposition, the following note issuggestive:—A fisherman brought in (August 25th) twenty-three eggs, which he said had been spawned in the boatshortly after the mother, which he also brought, had beentaken. Each egg was encased in a transparent glisteningouter capsule, delicate but elastic. One would be inclined tobelieve that the fisherman had observed the normal method ofspawning, i. e. that the eggs were discharged at the same time,extruded from the abdominal pores the more readily on accountof the sheathing capsule. The rupture of the capsule at orbefore fertilisation would set free the fastening processes, andthus enable the eggs to become attached, either together or toother eggs in the neighbourhood. This view, as opposed tothat of Ayers, is supported by the fact that in a number ofcases embryos of widely different ages have been found in thesame egg-string.

GENERAL MODE OF DEVELOPMENT.

The material collected by the present writer includes analmost complete series of embryos from a stage in which theblastopore is closing, to one about the time of hatching;together with these are several possible stages of segmenta-tion. A few of the most typical of these embryos are shownin the accompanying figures (figs. 3—8), and afford a con-venient basis for an outline of the mode of Myxinoid develop-ment.

VOL. 4 0 , PART 2 . NEW BER. U

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272 BASHFORT) DEAN.

As Price has shown, and as others have indicated, thedevelopment of a Myxinoid is typically meroblastic j 1 it mightreasonably be surmised that the large amount of yolk-materialwould enable the embryo to attain an advanced stage beforethe period of hatching, and that the duration of developmentin the egg should be a long one. These conjectures areclearly confirmed by the writer's observations upon embryosreared for a time in aquaria; he believes that the eggs do nothatch within two months, and thinks it possible that severalmore months may be taken. By this time the young Bdello-stoma has attained a length of over 6 cm., and has outwardlythe characters of the adult. Price notes that a distinctlylarval period is absent.

There can be little doubt, as Price has noted, that Bdel-lostoma is not protandric in the sense demonstrated byCunningham in Myxine.3 The eggs are in all probabilityfertilised after deposition. An egg nucleus is then presentimmmediately below the single large micropyle at the opercu-lated (animal) pole of the egg.

Segmenta t ion . — Until the writer's material of theyoungest stages shall have been sectioned, he can refer butdoubtfully to a single egg. Of this transverse sections nearthe animal pole show on one side a number of nucleus-likestructures embedded in a clear peripheral germinal area.There are no cell outlines, although the stage is probablyearly. One cannot doubt, however, that a condition of asym-metry with reference to the longitudinal axis of the eggappears in very early stages. And from the conditions of thefollowing embryo it will be inferred that the dorsal lip of theblastopore appears on one side of the egg, not far from therim of the opercule, and that from this region it closes fissure-wise backward.

Very Ear ly E m b r y o (fig. 3).—At this stage the embryois thread-like. The very narrow neural cord, N, represents

1 Cunningham, Retzius (1889), 'Biol. Foren. Forhdgr.,' Bd. i, pp. 22—28.2 Cunningham, J. T., "Reproductive Elements in Myxine," 'Quart.

Journ. Micros. Sci.,' vol. xxvii, 1886.

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DEVELOPMENT OE TBE OALIFOBNIAN HAG-FISH. 273

the fused lips of the blastopore, whose fissure is still to bemade out behind the tail region, BP. Anteriorly the longnarrow brain mass, Bj is indicated, scarcely deeper and widerthan the myelon into which it merges. No canalis centraliscan be determined in surface view. Notochord and meso-blastic somites have not yet arisen. A mesoblastic thickeningis apparent in surface view only at *.

Early Embryo (fig. 4).—This embryo is scarcely longerthan the earlier one, but it is notably broader, and it has mademarked advances in organogeny. Anteriorly the neural cordhas acquired a lumen; its walls, thickened and folded asym-metrically, mark out vaguely the divisions of the brain. Au-ditory vesicles, AU, are prominent; optic vesicles present butvery indistinct. Mesoblastic somites, PS, about ninety innumber, appear close to the neural cord, and extend sidewaysbut a very short distance. They are here differentiated insitu, but surface view cannot demonstrate definitely that gutcavities are present.

Interesting is the condition of the fore-gut, which nowdilates under the definite head region, and is already, as far asone can judge from surface view, pierced with several gill-slits.The heart, H, is vaguely indicated in front of the head, extend-ing directly forward.

Moderately Early Embryo (fig. 5).—The trunk hasbecome outlined in this stage; on each side it is separatedfrom the yolk region by a marginal artery which passes back-ward as it breaks into branches in the neighbourhood of thetail. Body length has somewhat increased, due apparently togrowth in both directions, the head now extending under theoperculum, the tail somewhat nearer the opposite pole of theegg. Advances in the development of the neural cord includeanteriorly the enlargement and definite outlining of the brainparts which have now grown under the auditory vesicles andover the eyes, and the now prominent and fused nasal pouches,and posteriorly the extension of the canalis centralis into theregion of the tail. The asymmetry of the foldings of theneural tube is now visible only in the region of the medulla.

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274 BASHFOKD DEAN.

Somites are prominent, PS. Pronephric tubules are apparentin connection with all the mesoblastic somites, PN, each nar-rowing out laterally into a delicate contorted tube, but as yetthere has appeared no pronephric duct. In the gill regionabout the normal number of gill-slits have now been formed.The number increases from behind, but remarkably enoughthose latest formed (i. e. hindmost) are largest. The gillregion is marked out clearly on either side of the embryo as aconspicuous lappet-shaped outgrowth.

Late Embryo (figs. 6, 7).—Continued growth has carriedthe head of the embryo around the animal pole as far ou theventral side as past the rim of the operculum ; the tail, nownarrow and tapering, has elongated until it has almost reachedthe hind end of the egg. Head, neck, and tail are separatedbelow from the yolk-sac, although they lie in grooves, and aredeeply sunken into it. Again, a marginal artery, DA, separatesthe trunk from the yolk-sac. Somites are now clearly marked ;pronephric structures are prominent, PN, and a segmentalduct, SD, is found. In the head region the principal advancesinclude the enlarged size of the nasal pouch, N, the appearanceof supporting tissue and of mouth, the latter originating as asingle invagination. This is very definitely shown in one ofthe writer's preparations, who thus differs from the conclusionof Price as to its probable origin as a paired structure. Thegill-slits at this stage, GS, may be seen through the backwhen this region is viewed as a transparent object. Since thelast stage these have been drawn forward, and at the sametime inward toward the ventro-median line by the growth ofthe head. The heart is at this stage a well-marked tube,passing straight toward the head from the hinder pole of theegg; on either side it receives asymmetrically the vesselsfrom the yolk region, carrying the venous blood to the gills.The vessels are very conspicuous in the living object, thecrimson threads in brilliant contrast to the rich yellow of theunderlying yolk.

L a t e s t Embryo (fig. 8).—The figure illustrates the lateststage in the writer's material. The young Bdellostoma

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DEVELOPMENT OF THE CALIFORNIAN HAG-FISH. 275

measures 6 cm. in length, and will (probably) shortly hatch.It exhibits occasional writhing, and its mode of growth sug-gests that in the process of hatching the operculum will bedetached by movements of the tail. The colour at this stageis purplish, save in the region of the yolk-sac. This, as before,is bright yellow, closely traversed by vitelliue blood-vessels.The yolk-sac is now attached to the embryo only in the middleportion of its trunk; both the anterior and posterior trunkregions seen in the figure are separate, therefore, from the yolk-sac, although pressed tightly against it, and embedded in deepgrooves. The tail lies on its right side, and is growing overthe head toward the opercular end of the egg. The head,lying somewhat on its left side, has now grown backward tillit has nearly reached the posterior pole of the egg. Struc-turally this late embryo closely resembles the adult; cirriare present around the mouth as in the adult condition,although they cannot be seen in the figure, the mouth beingpressed far backward on the ventral side. The anus is indi-cated at A, segmental mucous pits at M. Dermal-fin rays arewell developed. The gills, GS, are now the characteristicpouches with infolded walls and with external tubular ducts.Their final position will be seen to be far backward of the head.It is evident, accordingly, when figs. 4, 5, 6, and 8 are con-trasted, that the gills have not been growing forward at auequal rate with the head region. They early arise near thefirst slit even in front of the auditory sacs (fig. 4) ; they areseen later (fig. 5) in the process of being drawn forward underthe head, but are now well behind the ear capsules ; still later(fig. 6) they are seen in their normal position on the ventralside of the throat, but further back behind the ear sacs, sepa-rated from them by a distance of several somites; and finally(fig. 8) they appear in their adult conditions, still furthercaudad, now separated from the ear sacs by ten or moresomites. By the process of unequal growth, therefore, thechange in the position of the gills is explained.1 As at no

1 As has also been shown to be the case in Amphioxus by Lsmkester andWilley. (Editor.)

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276 BASHFOBD DEAN.

stage in the writer's material has he found any traces of eitheranterior or posterior gill-slits to increase the normal number,he is unable to accept Price's suggestion based upon thenumber of spinal ganglia and the change in the position of thegills, that the embryos of Bdellostoma have as many as thirty-five pairs of gill-slits.

CONCLUSIONS.

The Myxinoid differs widely from all other Chordates in itsdevelopmental type. Its sharply marked differences from themode of development of the lamprey emphasise the widedivergence of these branches of the Marsipobranchian stem;and this alone forms a strong ground for belief in the antiquityof the Cyclostomes, and for rejecting even a most remoteTeleostean ancestry. Developmentally the two branches cer-tainly differ as widely as sharks and Ganoids. There can beno doubt, furthermore, that the embryonic conditions ofBdellostoma are not to be derived directly from those of thelamprey. To what degree the converse is to be accepted mustremain for further study. We may now reasonably believe thatthe ontogeny of a Myxinoid, when fully studied, will enable theinterrelationships of the Marsipobranchs to be broadly out-lined : and it is possible that many valuable suggestions willfollow as to the general relations of these to Protochordateson the one hand, and on the other to the ancestral Gnatho-stome.

Some of the more striking features in the development ofBdellostoma, as above described, may finally be summarised.

I. The neural tract is laid down, nearly in its entire length,before the appearance of somites, and without any indicationof neuromeres.

II. The neural tract, as in Petromyzon, acquires a lumenby dissociation of cells (as shown by sections), proceedingantero-posteriorly.

III . The brain is distinctly a tubular structure, and differslittle in calibre from the spinal cord up to a relatively lateperiod in development, i. e. to the time of the appearance of

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DEVELOPMENT OF THE UALIFOBNIAN HAG-FISH. 277

paired sense-organs, of gill-slits, and of nearly the adultnumber of somites.

IV. The brain portion of the early neural tube is of verygreat length, one fifth the entire length of the nerve-tube(one quarter if the foldings in the brain wall be taken intoaccount), at a stage when nearly the adult number of somitesare present. It is to be inferred, therefore, that the craniotebrain is composed of a far longer region of the anterior neuraltract than has hitherto been supposed. It is thus probablyhomologous with the branchial region of the cord, as well aswith the so-called brain of Amphioxus.

V. The numerous foldings (asymmetrical) of the brain wall,by which the regions come to appear, indicate a primitivecondition of- the craniote brain, i. e. that the latter wasoriginally a tube of many vesicles1 (eight of these at leastbetween cerebellum and thalamus), which in the ontogeny ofhigher forms have become merged into fewer and larger ones.

VI. There is an almost entire absence of cranial flexure.VII. Although the developmental type of Bdellostoma is

distinctly meroblastic, it is noteworthy that there appears notrace of a germ ring j except in the immediate region of thetail, the somites arise in situ at the sides of the neural axis.

VIII. The early appearance in each segment of pronephrictubules, similar to each other in essential characters, demon-strates, as Price has shown, that the entire excretory system ofMyxinoids must, from the standpoint of ontogeny, be regardedas uuivalent. If we accept, therefore, Spengel's criticisms ofthe results of Semon on the morphology of the excretorysystem in Myxine, we must nevertheless admit Semon's aprior i view as to its homology as a pronephros.

Note on the above by J. T. Cunningham, M.A.—It is,I think, of some interest that the method of fishing by whichalone eggs of a Myxinoid have been obtained in California is

1 Tbe writer believes that these may be distinguished from the neuromeresof Locy and receut authors, which arc not distinctly vesicular, and whichoccur in cord as well as in brain.

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278 BA8HF0RD DEAN.

commonly practised off the mouth of the Firth of Forth, andelsewhere along the east coasts of Scotland and England,although eggs of Myxine have never been obtained by thatmethod. Some years ago I made strenuous endeavours toobtain fertilised eggs of Myxine, and received grants fromthe Royal Society to defray the expenses of the investigation.I frequently made excursions on fishing-boats engaged in fish-ing for haddocks with long lines, which the Americans calltrawl-lines. On these lines large numbers of Myxine werealways taken on the hooks, just as in the fishing described inthe Bay of Monterey. But no extruded or fertilised eggswere ever seen by me entangled in the slime of the Myxine.The only explanation of this which seems possible is that offthe English coast the fishing-lines have not been shot on aground where Myxine spawn, all endeavours to obtain theeggs from the lines or from the fishermen having hithertofailed. I cannot agree with Mr. Bashford Dean in his re-marks on the mode of oviposition. The sheathing capsules towhich he refers as enclosing the spawned eggs observed by afisherman must be, I think, the follicular capsules belongingto the ovary, in which the eggs are developed. I have fre-quently seen the eggs of Myxine enclosed in these capsulespressed from the fish, but I showed in my paper on the gene-rative organs that the eggs normally escaped from the ovaryby the rupture of these capsules, and the separation of thecapsules without rupture is due to some violence or pressurein the capture or handling of the female. In Myxine it iscertain that the eggs when extruded are enclosed only in theegg membrane provided with threads at the poles, this mem-brane being of the nature of a chorion produced in the folli-cular capsule. It is probable that in this respect the eggs ofBdellostoma S tou t i are quite similar to those of Myxineglutinosa.

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DEVELOPMENT OP THE OALIFORNIAN HAG-FISH. 279

DESCRIPTION OF PLATE 17,

Illustrating Dr. Bashford Dean's paper " On the Developmentof the Californian Hag-fish, B d e l l o s t o m a S t o u t i ,Lockington."

FIG. 1.—Bdellostoma taken on trawl-line, showing egg.string entangled inencasing slime. X f.

FIG. 2.—Tips of horn-like filaments of eggs, x about 30.

FIGS. 3, 4, 5.—Stages of early embryos. X 4J. AB. Anterior end ofbrain. AU. Auditory vesicle. B. Brain, BF. Blastopore. GS.Gill-slits, H. Heart, u. Spinal cord. o. Rim of operculum. OP.Optic vesicle, PN. Pronephric tubules. PS. Somites. UDT. Uu-differentiated tail mass. * Appearance of mcsoblast.

FIGS. 6, 7, 8.—Two stages of late embryos. X 4J. A. Anus. ATJ. Audi-tory vesicle. DA. Dorsal aorta. GS. Gill-sacs. H. Heart. M.Mucous pouch, OP. Eye. u. Nasal sac. PN. Pronephric tubule.SD. Pronephric duct.

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Fio. S.

f Hulk, Lift1 EdinT