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Masters Theses Graduate School

6-1939

A Comparative Study of the Spiracle in Cyclostomata, Elasmobranchii and Pisces

Miser Russell Richmond University of Tennessee, Knoxville

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Recommended Citation Richmond, Miser Russell, "A Comparative Study of the Spiracle in Cyclostomata, Elasmobranchii and Pisces. " Master's Thesis, University of Tennessee, 1939. https://trace.tennessee.edu/utk_gradthes/4396

This Thesis is brought to you for free and open access by the Graduate School at TRACE: Tennessee Research and Creative Exchange. It has been accepted for inclusion in Masters Theses by an authorized administrator of TRACE: Tennessee Research and Creative Exchange. For more information, please contact [email protected]. To the Graduate Council:

I am submitting herewith a thesis written by Miser Russell Richmond entitled "A Comparative Study of the Spiracle in Cyclostomata, Elasmobranchii and Pisces." I have examined the final electronic copy of this thesis for form and content and recommend that it be accepted in partial fulfillment of the equirr ements for the degree of Master of Science, with a major in Animal Science.

Barton C. V. Ressler, Major Professor

We have read this thesis and recommend its acceptance:

Henry Meyer, A. C. Cole

Accepted for the Council: Carolyn R. Hodges

Vice Provost and Dean of the Graduate School

(Original signatures are on file with official studentecor r ds.) Kay 22, 1939

To the Committee on Graduate Study:. I am submitting to you a thesis written by Miser Russell Richmond entitled "A Comparative Study of the Spiracle in Cycloatomata, Elasmobranchii and Pisces." I reconmend that it be accepted for nine quarter hours credit in partial fulfillment of the requirements tor the degree of Master of Science with a major in Zoology.

.�®�Major Profeasor

We have read this thesis and recommend its acceptance:

Accepted for the Committee --- :; J De.;�(E�,�'the Graduate School c:;:::::,,,- - A COMPARATIVE STUDY OF THE SPIRACLE IN THE CYCLOSTOMATA, EIASMOBRANCHII AND PISCES

A THESIS Submitted to ..•... �- the Committee on Graduate Study . .;. ot . .... Q· • • : The University of Tennessee .; • 0 . in Partial Fulfillment ot the Requirements for the degree ot Master of Arts

by

Miser Russell Richmond June 1939 .&.CKNOWLEDGMENTS

I wish to express my appreciation to the Department of Zoology ot the· University of Tennessee tor the opportunity af'f'orded me to carry on this study.I am especially indebted to Professor Bartaa c.v.Ressler tor the suggestion of the problem, and for guidance. during . the study. I wiah,also, to thank the Library Staff of the University of Tennessee tor their cooperation in searoh tor litere.ture on the subject.

1.63524 IV

TABI.E OF CONTENTS

CHAPTER PAGE I. INTRODUCTION . • • • • • • • • • • • • • • • • • • • • • • 1 Statement of the purpose ••• ••••••••••••• 1 Importance of the investigation. • • • • • • • • • • • • 1 Plan of investigation. • • • • • • • • • • • • • • • • • 1 Classification of forms studied•• • • • • • • • • • • • l .II. LITERATURE • • • • • • • • • • • • • • • • • • • • • • • 3 Introductory statements. • • • • • • • • • • • • • • • • 3

Description of Cyolostomata. • • • • • • • • • • • • • • 3 The olfactory apparatus of Cyclostomata. • • • • • • • • 3 The Myxinoidei and Bdellostoma . • • • • • • • • • • • • 4 Gills of Cyclostomata. • • • • • • • • • • • • • • • • • 5 Spiracle or Elasmobre.nchii . • • • • • • • • • • • • • • 5 Description of visceral region of.Elasmobranchii . • • • 6 Diverticula of spiracle. • • • • • • • • • • • • • • • • 6

The spiracle in the Raji erinaceae . • • • • • • • • • • 8 Respiration of the Raji erinaoeae. • • • • • • • • • • • 8 Thymus-element of the spiracle . • • • • • • • • • • • • 9 The spiracle in the Teleostomi ••• • • • • • • • • • • 10 III. DISSECTION AND DISCUSSION••• • • • • • • • • • • • • • • • 12 Description and discussion of the nasal apparatus ot

Petromy1on marinua •••••••••• •• •••••• 12 Description and discussion of the spiracle of Squalus marinua•••• ••••• • • • • • • • • • • • • • • • 14

Description and discussion of the spiracle of Raji erinaceae. • • • • • • • • • • • • • • • • • • • • • • 23 V

CRA.PrER PAGE Description and discussion of the spiracle in the Teleosts •••• • • • • • • • • • • • • • • • • • • • 25

Description of the ear ot Petromyzon marinus • • • • • • 27 Description of the ear ot S3ualus aoanthiaa. • • • • • � 27 Description of the ear of Raji erinacea. • • • • • • • • 29 Description or the ear or Perea tlavesoena . • • • • • • 29 Formation of tympanum. • • • • • • • • • • • • • • • • • 31 IV. SUMMARY AND CONCLUSIONS. • • • • • • • • • • • • • • • • • 32 VI

LIST OF ILLUSTRATIONS

FIGURES PAGE 1. Petromyzon marinus, sagittal section ••• • • • • • • • • 13

2. Petromyzon marinus, sagittal section through olfactory apparatus x 3 •• • • •••••••• ••• ••••••• 13 3. Squalus acanthias. aide view of head ••• • ••••••• 16

4. Squalus acanthias, dorso-lateral view showing structures under the skin and skin muscles•• ••••••••••• 16

6. Squalus acanthias. dorso-lateral view showing structures. 1/4 inch below the surface • ••••• ••••• •••• 11

6. Squalus acanthias. dorso-lateral view sh01l'ing structures 1/2 inch belOW' the skin •••••••••••••••• • 17

7. Squalua acanthias. dorso-lateral view showing structures 3/4 inch below the surface •• • . •••••••••••• 19 s. Squalus acanthias, dorso-lateral view showing structures where spiracle meets the pharym •••••••••••• 19

9. Squalus acanthias, transverse section through the spiracle 20 10. Soyllium oanicula, advanced embryo, transverse section through the spiracle •••• ••••••••••••••20 11. Scyllium canicula, advanced embryo, transverse section through the spiracle ••••••••••••••••••21 12. Soyllium oanicula.. dorso-lateral view of skull shoring relation of-the poet-1piraoular ligaments and the dorsal apiracular caecum.•• ••••••••••••••••••21

13. ·Elaemobranch (Squalua aoanthias), horizontal section. • • 22 14. Teleost (Perea tlaveaoens) horizontal section. • • • • • • 22 15. Dorsal view of head region of Raji erinaceae •••••••26 VII

FIGURES PAGE

16. Ventral view of pectoral region of Raji erinaceae . • ••26

17. Raji erinaceae� cross section through the spiracles • ••26

18. Ear of Petromyzon marinua • •••••••••••••••28

19. Ear of &qualus acanthias • ••••••••••••••••28 20. Ear of Raji erinacea•• ••••••••••••••••• 30 21. Ear of Perea flavescens • • • • • • • • • • • • • • • • • 30 CHAPI'ER I

INTRODUCTION

Although scientists have been interested in the spiracle for a number of years, very little investigation has been done. In this study t�e writer shall endeavor to describe the structures and functions of the spiracle in the Cycloatomea, Elaamobrancha and Piacea as well as show the continuous development ot any structure as to its tunction in the animals studied. A• a. plan of study the epeoimena •ere divided into three general groups acoording to their olassitioation . The methods used in making the observa­ tions will be discussed later. The ,rork has been done either in the l�brary or laboratories ot the University o� Tennessee. Specimens tor study were supplied from. the stock of the University of Tennessee, .from the markets in Knoxville, or from fish­ ermen along the Tennessee River. Claaaitication of torma studied in this theaiaa Phylum-Chordata Sub-Phylum - Vertebrata. Class .l. Cyolostomata Sub-Class I. Myxinoidea--Hagtiahes Family - Kyxinidae Genus - 1. Bdellostoma--Pacific Form.a 2. Par&JQXine--Ooean Forms 3. Myxine--Pacitic, Atlantic Oceans Sub-C lau II . Petrc,av1ontia-Lampreya Family �-Petromyiontidae Genus - 1. Petr01111'zon-•Found in rivera and· seas of America, Europe and Asia

1 Cla1s B •. Ela1mobranchii Sub-Claaa I. Selachii Orcler l. S'quali--Sharka and Dogfish Sharks Order 2. Raji--Raya and Skates Sub-Class II. Holooeophali Order 1. Chimaeridae Class c. Pisces Sub-Class I. Teleostom.1--True Fishes Order 1. Croaaopterygii--Polypteridae Order 2. Chondrostei--Paddle-fiah am Sturgeons Family a. Polyoc:lontidae--Pa.ddletiahes Family b. Aoipenaeridae--Sturgeona Order 3. Holoatei--Oa.rpilces and Bowfina Family a. &miidae--Bowtina Family b. Lepiaoateidae--Oarpilce Order 4. Teleostei--Bony Fiahea . . Suborder (1) Cyprinitormes Family a. Cyprinidae--Carp, Minnows Family b. Catostomidae--Suokera Family c. Siluridae--Catfishea Suborder (2) Clupeiformes Family a. Salm.onidae--Trouts, Salmons Suborder (3) .loanthopterygii--s·piny-rayed Fishes Family a. Percidae--Perchea Sub-Cl.a.as II. Dipnoi - Lung Fishes Family a. Ceratodontidae - Australian Lung Fishes Family b. Lepidoeirenidae - South American and A.frioan Lung Fishes CHAPrER II

LITERATURE

The amount of literature on the apiracle ii limited to a few text­ books on C'ompara.tive .lnatom.y and a very limited number ot articles and reports in various sciantitic publications. No reoent reports were found.

The spiracle, known as the pituitary canal in the Cyoloatomata. does not come to the surface but ia &Hooiated with the nasal organ and runs from the nasal capsule downnrd and backward tothe reapiratory tube at the velum. Gill-Slitsi In Petromyzon •rinua there are seven pa.ire ot gill-elite and a lilce number ot pouches. The first gill-slit opens just opposite the entrance ot the pituitary canal. Water can enter the gill pouches either by the mouth or through the gill-alita. "The Lampreys differ from the other Vertebrata in the fact that the gills do not open directly into the enterio canal in the adult but into a respiratory tube lying below the gullet.•1 In the adult this tube extends from bucoal cavity to above the heart while in the larva it extend.a from. the intestine forward to the pharynx and during .-tamorphoais lo••• its connection with the intestine and the gullet ia formed. The gill-pouches have the shape of biconvex lenses. with numerous la­ mella on the inner surfaces. They are separated by inter-branohial septa. An additional cleft baa been totmd in the larva anterior to the tirat in 2 the adult aeries. The development of the olfactory sao, the pituitary pouoh and the pi­ tuitary body are closely related. In the embryo. betore the stomodeum

1 T. J. Parker and William Ju Haswell, .&. !ext-Book ot Zoology (Londona-MacKillan Company, 1928), PP• 126. 2 .ill!•• PP• 127-128. 3 connects with the 11e1enteron, two unpaiNd ectodermal invaginations appear in front ot the mouth. The first ia· the rudiment ot the oltaotory sac, the aecond the pituitary sac which opens just outdde the atomadeua. Ita blind end extends to the T8tltral surface ot the torebrain and ends below the in­ f'undibulum. .ls the embryo develops the olfactory and pituitary invaginationa beoOID.e depressed into a common pit whioh ahi:f'ts toward the top ot the head with the deTelopment of the thiok upper lip, the process causing an elongation ot the pituitary- sac into which the olfactory sac. opens posteriorly. Thus the entire passage of the Lamprey ia a persistent pituitary sac into which the 3 single oltaotory- organ opens.

The Cycloatcm..ta of the order Myxinoidei differ somewhat to Petr£Dll&ontea. The genera Kyxine has no true bucoal tunnel. 6r. velum separates the buccal cavity trom the pharym:. The noatril is a very large, unpaired opening lcoat­ ed 1n the doral •rgin ot the buccal apaoe and oontinuoua into the pituitary aao, whioh opens into the pharynx by an aperture which· appears late in the lite of the •bryo. Kyxinee live in mud and the respiratory current paase• through this naeal aperture to the gills. In different species of Bdelloatoma there·are trom six to fourteen small gill opening• on either side. Each of these connects by a tube with one ot the gill-pouchea which in turn conneot with the pharymt. Just be.ck ot the last gill-slit, on the left side, ia the opening of the oeaophageo­ cutaneous duct which leads to the pharynx. 4 Charles R. Stockard, Columbia University, in his observations ot Bdelloatoma atouti found that two post hyomandibular gills ooeur in the

3 T. J. Parker and William A. Haswell, A Text-Book 2£ ZooloQ' (Londona MacMillan Compe.cy, 1928), P• 129.

4 Charles R. Stockard, "The development or the Mouth and Gills ot Bdelloatoma. Stouti," American Journal ot hatomy ., Vol. V, pp. 481-511. 5 early embryos and are for some time in advance ot the true branchial gills in their state ot development. !hey then begin to degenerate and rapidly disappear.

In Myxine the gill-slits unite to form a single opening posteriorly. Also, in addition to these gill sacs. in the 14yxinoids a pharyngo-cutaneous duct passes from the pharynx along the left side to the exterior �ehind the last sac. Ite opening is adjacent to the laat gill pore. Breathing is accomplished by the expansion and contract ion of the mus­ cular 118.1.la of the sacs,· water being drawn in through the median nostril. which leads to the hypophyeial canal opening into the pharynx behind and ex­ pelled to the exterior along the expiratory tubes. The Gillsa

The gills of Cycloatomea are highly specialized structures, the lamellae being enclosed in rounded sacs with narrow ducts lead ing into them from. the pharynx and out of them to the e�erior. Due to their pouch-like shape this 5 group of gills ia called •raipobra.nchii. The gills are incloaed by the branohial ba.aket which is formed on each side ot nine curved vertlcal bars of cartilage the first just posterior to the atyloid cartilage, the second in front of the first gill-oleft and the remaining seven just behind their seven reepective gill-clef'ts. These bars are tied together longitudinally by four longitudinal rods.6 The respiratory system of the Elaamobranohii shows greater development, especially in the spiracle which now connects the pharynx with the outside through the epiracular canal. The oral cavity is wide and flattened dorao­ ventrally. The anterior pa.rt ii bounded by the jaws formed from the mandibular

5 Edwin s. Goodrich, Studies on the Structure and Development ot Vertebrates (Londona MacMillan Compaiiy-;-T930), PP• 492-493. 6 Parker and Haswell, .2E,• £!!•. PP• 124. 6 gill aroh. The tongue forms a small projection in the floor of the mouth. supported by the hyoid gill arch. The poaterior part of the cavity, the pharynx, is pierced by six in­ ternal gill-slits. The first, the spiracle, is a rounded opening in the roof of the mouth just posterior to the mandibular arch. The five remaining gill-alits connect with the visceral pouches which open to the outeide by •Y or the external gill-slits. The visceral pouches are aepe.rated by the visceral arches. The arches are ma.de up of a central portion, the inter• brachia! septum, each side of which ia covered with gill filaments, except for the first and last, constituting a demibra.noh. In Elamnobranohs and some Ganoids the anterior visoera.l ole�, the spiracle, is smaller than the others, and opens on the top of the head. Thie spiracle bears well developed gills in sharks such aa the Notidanidae but in those showing higher development it may contain only a vascular net­ work in its walls. In Ge.noida and Teleosts it is a pseudobranoh receiring blood from the opercular gill which is an ectodermal structure developed in the face of the operoulum. In typical Elaamobranchs the interbraohial septa extend to the outside of the body direatly, on the neck in Selachii and on the ventral aurtace in Raiea. The Teleoste and Ge.noida are similar except the operculum covers the whole external part ot the gilla. In El.asmobranoha the spiracle ia not merely aaimple tube paaaing from the pharynx to the surface of the body, but it has various outgrowths. Many of the Selachians have a caecal divertioulum on the dorso-internal •11 ot the spiracle, which passes inward, and, broadeniq in an antero-poaterior direction, becomes finaly attached to the auditory capsule, below the

7 J. s. Kingsley, !!!!..,ebrate Zoology (Bew Yorks Henry Holt & Company. 1911), PP• 22-23. ?

projecting ridge that marks the position of the horizonta l aemi-ciroular

canal , and immediately above the post-orbital groove. The opening ot the

caecum int o the spiracle is never closed. although in some genera (Ge.leus) 8 it may be very small. This caeoum waa first observed by Muller who thought

it was an accessory to the auditory organ. lluller described the caecum aa being present in Scyllium, Priaturua , Mustelus, Ga.leua and Batoida . Van

Bemm.e len9 added Aoanthias. Squat ina and Heptanchus to Muller's liat. In

A.canthias it is not the dorsal caecum, but the mucous memb rane of the spiracle

itself, that is bound to the auditory cartilage .

Projecting inward and forward from the imler wall of the spirac le , at

it s pharyngeal opening ., is another diverticulum, much shallower in extent and

with a wide mouth. It ia located below the level of the pre-apiracular carti­

lage and immediately in front of the pr oximal end of the hyomandibular. An­

teriorly it ia bounded by the levator maxillae auperioria musc le. and pos­

teriorly by the anterior surface of the hyomandibular cartilage and t�e inte­

rior poat-1piraoular ligament. The blind end of this caecum is separat ed only 10 by mucous membrane from the orbital blood sinus .

11 Norria and Hughes (1895) found an opening on the anterior m.eaial wall

of the apiracular oleft of Squalua aoanthias both in the Embryo and adult . The

veey small pore in the spiracular wall leads into a CUP-like organ with three

diverticula. They seem to be modified ampullae ot Lorenzini.

The spirac le in sharks represents only the upper part of the byoid clett,

8 11'. C. Ridewood, "The apiraole and aaaooiated atruoturea in Blaamobranoh Fishes," .Anatomischer .&.nzeiger , Vol. XI . Dec. 1896.

9 Ibid ., P• 431

lO Ibid., P• 430.

11 G. Pinkus , "The apirac ular sense organ in Blaamobrancha, G&noid Dipnoan." Anatomy Record, Vol. XVIII, PP • 208-209. 8 the middle and lower portions being obliterated. The pit thus formed ia the . 12 atructure regarded as the internal part ot the hyoid cleft by Dorhn in 1886. Garman (1874) pointed out that the spiracle ia ot greater importance to the rays than the abarka , due to the fact that rays live on the bottom and this places their mouth at a di•dvantage aa an incurrent respiratory opening.

The apiracle ia uaed as the incuJTent opening and is therefore larger than in the 1harka. Be, also• pointed · out that sting rays had a valve in the spiracle which allowed the current to paH inward only. However, in the common skate there 11 no valve and water may pass either way. It uaually goes only inward. but if sand or other toreign material gets into the spiracle, the skate spout s 13 out through the spiraole to remove it. "When tully open the external opening of the spiracle in the coDDnon skate is almost elliptical in outline, but the curvature of ita anterior •rgin ia much greater than that of its posterior margin. The anterior lip of the open­

ing bears a rudimentary gill and the closing of the spiracle is ef'feoted mainly by the contraction of this gilled lip, while the posterior lip. being nearly

straight when relaxed contracts but little.tt l4 In respirat ion the spiracle opens and closes regularly. During rest the movements are slow and the opening is much narrower, but during active respi­ ration the anterior lip of the spiracle moves back and forth quickly and the spiracle opens it s maximum width. When the spiraoular valve opens the branohial region expands and a strong current ot water is drawn through the spiracle, the

12 G. Pinkus , •The apiracula.r sense organ in Elamnobrancha. Ganoid, Dipnoan," Anatomy Record, Vol. XVIII , P• 433. 13 · Herbert W. Rand , "Funotiona of the Spiracle in the Skate," -The American Naturalist. Vol • .XXXXI, Kay 1907. PP• 288-289.

14 .ill!•, P• 389. 9 external branchial apertures being closed. The movement of the mouth ii practically the same. Some water entered the mouth, however, the greater volume enters the spiracle. The action of the mo_uth is always a little slow as com.pa.red with the action ot the spiracle . The mouth and spiracle cloae together, but the mouth opens alightly later than the apiraoles. When the apiraole and mouth are closed, the water ia forced out through the gill cletts. Inspirations occur trom twenty to thirty per minute and normal ,pouting every five to ten minutes. Spouting is caused by insufficient oxygen aupply, irri• tation, exercise or induction of bulk material• .ll so, any irritation to the 15 eye will cause the animal to spout. 16 Van Bemmelen (1884) searched for a thymus element in the spiracle ot rays and in his study observed the ventral apiraoular follicle but could not determine its_ thymua element . In his conclusion Van Bemmelen aaid, "I in• cline certainly to the view, which would consider both the vesicular follicle of the spiracle and that of the angle of the mouth as possibly the rudimentary equivalents or thymus-element or these pa.rte. 17 Ten years later Beard found ,. in the ray embryo ot aeventeen mm., a thy- mus placode in the 1pira.cle. It consisted of but a single regular epithelium. ot colUJDJlllr cells containing very few leuoooytes. In larger embryos the leu­ cocyte count increased, though the structure ot the epithelium changed very little. However, Beard found in some embryos that the placode gr ows and spreads into a flattened plate of epithelial cells and in others a cone ot epithelial cell• were formed.

5 1 J. Frank Daniel, The Elasmobranoh Fishes (Berkley, University ot Californi• Presa, 1928) ,. p7"'!&1. 16 J. Beard ,. "Thymus-Element of the Spiracle in Raja, n Anatomhcher Anzeiger , Vol. XVIII. Nov. 1900. (Jena: Verlag von Gustav Fischer, 1909) PP• S58-359. 7 1 �., P• 363. 10

In the Soyllium the thymus-elements arise as those of the Raj i and for a ti:m.e their plaoodes remain very simple, only increasing in area. Later the epi thelium beoom.es tubular and vasoular.

Beard made the following oonclusions in regard to the thymus-elements a

11 1. It arises as a pla oode of the gill-pouch, and _with the rupture of this latter it comes to be epiblastio .in position.

2. In late phases it acquired a covering of ordinary epiblast.

3. Connective-tissue septa grow into it.

,. Blood oapillaries penetrate it.

5. Its epithelium gives or igin to leucooytes. 6. At a la ter period it becomes more or less constricted off fran the 17 branchial epi theliwn, but apparently unlike a thymus-element, not oompletely. "

The external opening of the gills, direotly to the ou tside in the

Cyclostames, and Elasmobranohs, is replaced by operoular covering of the gill­ olefts in the Teleostomi and Dipnoi.

In Holocephali, spiracles are absent in the adult but present in the young of Chimaera. The interbraohial septum is al so muoh reduoed and in Teleostomi the reduction is carried still further, the whole gill structure 18 being covered by a movable operoulum.. Open spiracles are wanting in most Teleostami but are retained .in the

Crossopterygii (Polypterus) and Chondrostei (Aoipenser and Polyodon). In the embryos of salmon the spiracle is present but degenerates in the adult.

The spiracle in the sturgeon (Aeipenser) is a slit-like structure just above the eye. It is a hemibranoh of the hyoid arch and is a true gill serving the

17 Beard. �·�·• p. 363. 18 T. W. Bridge and G. A. Boulanger, Fishes, Ascidians, etc. , (Londona MacMillan & Company, 1922, pp. 278-279. 11

same purpose in the circulatory system as in Elasmobranch. Polyodon (Spoonbill) and Polypterus have a suppressed hemibranch while Lepidosteus' (Ga.rpike) has two series of lamellae on the inner surface of the operoulurn. The ventral seotion is supplied with venous blood, the dorsal with arterial, so that the latter is 19 a definite pseudobranoh. 20 Goodrich tound a pseudobranch to be deyeloped in Ac ipenser, Polyodon6

Lepidostens, � and most Teleosts. Von Baer (1827) tormd two pseudobrancha

in Acipenser. In 1831 those of Lepisdoste� were worked out by Va lentin. Hyrth (1838 ) proved they were supplied with arterial blood. J. Muller (1839)

classified the teleostean psuedobranohs as, (1) free, with gill-lamella pro­ jecting into the sub operoular cavity, and (2) glandular, sunk below the epithelium. Granel di stinguished £our adult types of pseudobranchs, n(l) a

free pseudobranoh with lamella set along the axis and bearing secondary la­ mella all covered with eotoderrnal epithelium.. Ex. Tra.ohimus ; (2) lamella free but epithelium covers them without sinking between the seoondary la.mella,· Ex.

Chrysophrys; (3) the lamella do not project and have sunk below the covering of eotodermal epithelium, Ex. Ph oxinus; (�) t�e whole organ is separated £ran. n21 the superficial epithelium by an overgrowth of tissue. Ex. G� ., Cyprinus. Pinkus 22 in his study of Protopterus found a peculiar vesicular sense­ organ imbedded in cartilage near the anterior end of the ear capsule , inner­ vated by a sma ll nerve that arises fr om the main lateral line of the facial nerve.

19 Bridge and Boulanger., �· .ill!., pp. 283-28�. 20 E. s. Goodrich, Loe. Cit., P• 519. 21 Ibid. , P• 521. 22 G. Pinkus, nThe spiracular sense organ in llamnobranohs, Ge.noid, Dipnoan," Anatomy Record, Vol. XVIII, pp. 208-209. CHA.PrER III

DISSECTION AND DISCUSSION

Cyoloatomata:

The specimens used to dissect tor a study ot the Cycloatomata were Petromyzon marinus. a speoiea which is common in ·the waters of the rivers. aeas and oceans in and around Ameri ca. Europe andAsia . This animal is long and ee. �-like. having two dor sal fins but no lateral f'ina. The body ia o overed with a el imy akin with out scales. The mouth is at the bottom of a ciroular auctor ial funnel . the inside of which is armed with horny teeth which aid in holding on to the fish on which they feed. The naaal organ ia a single median organ placed at the posterior side ot the hypophya ial duct . the opening to which serves as the nostril opening upon the top of the head. The deeper end of' the hypophyais expands into a sac which ends blindly at a point even with the first gill­ alit. The gill-slits are tubular. and the folded gills are borne on the walls of pouch-like regions of these tubes.

It is the nasal apparatus in Cyclostomes that is the forerunner of the spiracle in the Elasmobrancha. To show these structures and the related structures the specimens were dissected by .making a sagittal section. from dorsal to ventral beginning with the anterior of the buccal tunnel and con­ tinuing in a mid-line to a point even with the last gill-slit. This repre­ sents ab out 1/5 of the total body length. (Figures 1 and 2) The nasal aperture opens externall7 in the mid-dorsal line slightly anterior to the eyes . The nasal opening runs downward to the nasal capsule.

12 13

/

A ,o, --1.. ..,. c. ��t.,,, , ..

. R:,. 1. A pouch-like divertioulum separates it from the nasal aperture by mucous mem ­ brane and it contains the nasal glands and olfactory nerve endings, then it curves slightly upwa rd a.nd oontinues on baokward ending in a blind pouch just bel ow the notocord at a point even with the first gill-slit. The posterior part of the pouch is known as the pituitary pouch . The whole nasal .aperture is tube-like with alight convolutions in the walls running

'longitudinally. No rudimentary gill structures are present. The nasal aperture is primarily used in the sense of smell which is located in the olfactory sac which lies in the nasal capsule. When the pi­ tuitary sac comes in contact with the. infundibulum of the brain, it gives off numerous follicles which form the pituitary body. The nerve supply to the naaal aperture is the superior opthalmio to the dcrsal region and the facial to the pituitary region. The blood comes from the internal carotid artery through the basilar artery. Selachii: The Elasmobranchii include several orders but in this investigation , the_ dogfiah ahark (Squalua aoanthiaa) and the common skate (Raji erinacea) 'rire used as basic specimens with others referred to for oom.pa.riaon . In �he Elaamobranohii the spiracle is definitely a part of the res­ piratory ayatem. The apira.ole opens to the exterior through the apiraoular aperture and to the interior into the pharynx.

Squalus acanthias adults reaoh a length ot about three feet. In this investigation various sizes . from unborn embryos •t 5 iliohes� t. 2.5 ;nohes ­ long were studied. The illu stration s shown in Figures 3, 4, 5, 6, 7 and 8 were-made from a apeoimen twenty-five inches long to get the various cross 16

aeotions or the spiracle at different depths. A apeoimen twenty-one_ inch•• long was uaed in making the cross section of the body through the apiraolea. The spiracle is located posterior to �nd slightly toward the dorsal line from the eye. in the middle of an imaginary line drawn from the mouth to the nearest point on a mid-dorsal line . (Figure 3) The opening ot the spiracle is somewhat longer than wide with the long axil running horbontal to the eye . Anteieior and adjacent to the 1piraole is the apiraoular pit and just dorsal to the apiraoular canal ia the rather �rge spiraoular muscle . From an external view the lamella of the paeudo­ branoh may be observed attached to the anterior muscular wall. This muaou• lar wall serves as a valve in controlling the ai&e of the opening of the apiraoular canal . The fi�st plane observed below the aurfaoe was fraa a dorao-lateral viewwith the skin and superficial muscles removed. (l'igure 4) In thia and the illustrationa ot this aeries the eye is used aa a point of orientation. In this illustration the spiracle appears almost ova l with the lamella more distinct on the anterior aide. The apiracula.r pit ia still present. The spiracle is pro tected by the hyoid and mandibular arches on either side and dorsally by the supra-orbital crest. The second plane of observation (Figure 5) below the surface was made from the same position as the previous one and shows the structures one­ fourth of an inch below the sur:ta.ce. This illustration shows the ap1raole to be pressed down by the dorsal ·apiracular muscle, the apiraoula.r pit 11 not evident andthe lamella of the paeudobranch are somewhat flattened. , In Figure 6 the spiracle has become enlarged slight ly and stretched 16

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If W 1 S - Do y <.. D � L, t,..,..i t i e f; J , &I. Sq_ v.. ,i l u s. R c; ,dJi�,. bt-Lov.i sKirJ. �now;N� �tr' 1A tL,1. ttS ,;,, �.,_ ... t�<- 18 toward the ba.ae ot the supra-orbital orest. The dorsal spiracular muaol• has disappeared. The hyomandibular branch of the facial nerve is seen coming from the supra-orbital crest and running aoross the anterior wall ot the apir­ ac le . The lame llae have become greatly reduced in size and now appear more as ridges of vaaoularized tissue. The apiraoular artery supplies the paeuclo­ branoh with blood tram the first afferent artery. Figure 7 shows the structures exposed on a plane three-fourtha of an inch below the surface. The spiracle has been somewhat flattened by the hyoid and mandibular arches. The hyoid and mandible are exposed. The base of the supra-orbital cartilage ha.a pushed downward ani backward causing the spiracle to appear to have two protrusions in a or&niad direction.

The final illustration in thi s aeries, Figure 8, shows the base of the apiraole as it enters the pharynx. The walls are irregular and contain man.y irregular folds tilled with mucous. There is a posterior-ventral diverticulua between the mandible and the hyoid whi ch appears to be due to pres sure rather than being a true diver ticulum. The front of the spiracle widens ton.rd the oral groove. Tb.rough the opening , the tloor of . the pharynx may be observed covered with mucous and having the gill rakers and gill bars opening to the gill pouches in a ventro-lateral direction. Since Squalua aoanthia.s was the only type available for disseotion the investigator has uaed two illustration•, one from Goodrich and one from

Ridnood of Soyllium. canicula (Figures 10 and 11) as a means ot comparieon.

In a tranaverae section th rough the spiracles it was Qbaerved that the epiraoular canal of Squalua aoanthiaa ia praotioally straight with only alight l>ulgt1 in the inside walls and a paeudobra.nch with poorly developed lamella on_the anterior wall. In Soyllium oanicula . however, the apiraole 19

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- . .-t----.1-.L---C.-5 d ,,J.A 1" S 2S shows two divert icula (Figures 10 arid 11). The dorsal diverticulum. projects from the antero-medial wall ot the apiracular pocket toward the auditory cap­ sule and may be attached to it above the post-orbital groove. At ita begin• ning the diverticulum is almost closed but beoome a enlarged as it approaches the auditory capsule. The embryonic specimen s studied were little different from e th adult ex­ cept that the spiracle was larger in proportion to the total body size and assumed more · of a wedge shape with the blade pointing toward the mouth. The lamellae appeared as very amall ridges almost covered with mucous.

Norris and Hughes (1920) claimed the dorsal divertioulum in Squalus acanthias is divided into two or three small diverticula each ot wh ich is supplied by a branch of the ramus oticua VII nerve. He considered it a modified ampulla of L�renzini. The second diverticulum on the anterior medial wall of the apiraoular canal is located ventrally near the union of the canal with the pharynx. It is more shallowthan the doreal diverticulum and is connected to the canal by a short neck. · The apiracular pocket is supplied by the hyomandibular branch of the facial nerve and by the epiracular artery.

In the Squali the spiracle functions as an aoceuory respiratory organ, water being taken into the spiracle a.s well as the mouth . It is thought by 2 some that the apiraoular diverticula form a part ct the auditory syatea. Raji s

The common skate (Raji erinacae) used tor atudy waseleven inches wide and nineteen inches long .

1 J. Frank Daniel, �· £!!•, p. 149. 2 Ibid .• P• 14 9 . 24

The spiracles are located immediately posterior and slightly lateral to the eyes. (Figure 16) From an external view the spiracle appears to slant (as a ChinamanI s eye a). On the anterior wall at the opening. the muscular spiracular valve is located and immediately below th is structure the pseudobranoh may be seen when the spiracle is open. The apiracular valve is composed ot a atitf creacentic told ot connective ti ssue which 1, · constantly opening and closing during respiration . This told is held in place by the crescentic apiracular cartilage wh ich is attached at each end by ligament. The closure of the spiracular 'Valve is by the dorsal constrictor muscles . The spiracle. in the Raji• is the main opening tor the entrance ot water into th e pharyngeal cavity since the mouth is against t�e bottom ot the stream most ot the time. (Figure 16) At the posterior ot the pharyngeal cavity aix internal gill-slits break th e lateral wall of the cavity into the visceral pouches which open to the outside through the external gill-slits. The visceral arches separating the visceral pouohea are made of a central interbranchial aepta with branchial filaments on either side. These are supplied with blood from the ventral aorta which gives off branches to each demi.branch through the afferent ar­ teries. The blood trom the gill filament is collected by the poet-trematioa on the anterior face of the gill-arch and the pre-trematics on the posterior face of each gill-arch which join to torm th e efferent bra.nchial arteries which connect with the dorsal aorta.. The hyoidean artery arises near the middle ot the tront pre-trematic and g oes forward to 1upply the rudimentary gill ot the spiracle and the ad­ jacent tP,Uscles. The branches to the spiracle reunite forming the ventral 26 carotid which joins the internal carotid. The spiracle, beside being supplied by the intra-orbital canal of the lateral line system, is supplied by the hyomandibular branch of the facial nerve. A cross section through the spiracles (Figure17) shows them. with re­ lated structures . The body is much flattened, the lateral sides being the muscular lateral fins. The spiracular canals run from the orbital crest at the eye downward and inwa rd into the pharynx. The muscular valve and paeudo­ branch appear near the exterior opening of the apiracular canal. Below and to the side of the pharynx is the large pectoral muscle s.

Teleostomia The spiracle in the Teleoats is either greatly modified or entirely ab­ sent. The salmon (Salm.o) have a apiraole in the embryo but as adults they have a small rudimentary paeudobra.nch left under the operculum.. Sturgeons

(Aoipenaer) have a small spi�ole opening from. a small slit-like opening above' the eye and running downward and inwardto connect with · the pharynx. No paeudobranch is present on either anterior or posterior wall . The spoon­ bill (Polyodon) has a sn:all apiraole behind the eye. The operoulum contains no opercular bones and is extended into a pointed process. There are no branchiostegal rays in the spoonbill. The writer examined specimens of the catfish, sucker, trout, perch. carp and branch minnows, chiefly ailversides. and found the .spiracle to be absent. Gills in the Teleoats are covered with a partially ossified structure, the operculum. which is a new structure in the· bony fishe s. (Figure 14 )

The spiracle in moat Teleosts is closed on the outside by the operculum., 26

c:::::=- AG-: \ l «.l ; fi. � � t::::::::> �

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_,-� 'H � t fY'\ \AH.le_ JI ' S ta,·_.,. e...,� , l r , ) rt.. 't' ill, N : f\\ C. \A. O \:,...., ) "'4(..� 1\1� C $,(4 J � C p � d C i\ vt. · C. A J ;,t� 27 the inside structure from the throat ending in a pouch-like diverticulum just beneath opercular roots. This divertioulum has a protuding arm toward the labyri�h of the ear. This protru eion does not appear to penetrate the auditory capaule but the circulating water within affects the sensitive part of the ear. This bliDd .spiracular canal is the primitive Eustachian tube, but, since there is no middle ear in fish the tube is not a true Eustachian tube. In the Amphibians the middle ear appears in .&.nura and we find a definite Eustachian tube connecting the vestible of' the middle ear wi th the throat.

Ear: Since the ear is so closely related to the spiracle the writer observed the ear in the specimens of' Petro.myzon marinua , Squalua acanthias, Raji erinacea, and Perea flavescena and will describe to some detail their atructurea.

Petromzon marinus (Figure 18) has an ear which is ver-y simple and could be called a neuromaat of the lateral line system. It does not serve the pur­ pose of hearing but of equilibrium. The ear is paired taking the form ot sacs located on each side of the brain behind the eyes in the cartilaginous skeleton. The labyrinth bears two semicircular canals, anterior and posterior, each ot which beara an am.pulla containing atatoliths. The statoliths contain calcium. particles in a mucous substance wh ich when moved produce a sensation on the auditory nerve . Connection to the outside is maintained through the endolymph­ atic duot which emerges in a pit just back of the median nostril. The canals and the auditory sac are filled with elldolymph. The Elasmobranchii, also, have a latere.l line system in connection with the auditory appa.ratua .

The ear of Squalus acanthias (Figure 19 ) shows a marked advance over P.

•rinus in having -three semicircular canals. Each of these canals has an 28

Al'lh�; • v­ �e.rwi:C'-t TC. \A.\9',f" C�Nl\ L- 29 ampulla containing a number ot hair cells innervated by the auditory nerve.

The cavity of the atatooyst retains its connection to the outside through the endolymphatic duct which contains water instead or endolyaph. The sac­ culua has become further separated trom the utriculus and is connected only by the canalh reuniens. The sacpulus has developed an outgrowth. the lagena.

The lagena does not function and it is believed that the ear is chiefly an. or­ gan of equilibrium. The whole apparatus ia located in a cartilaginous capsule fused with the cranium.

The ear of Raji erinaoea (Figure 20) is similar to that of Squalua acanthias in the naber of semicircular canals, ampulla and hair cells . A crystalline stone is present in the utrioulus. The connection to the outside is through the endolymph duct and elldolymphatic vestibule. The ear with its canals tilled with perilymph and the ducts and vestibule with endolymph func­ tion both in hearing and be.lance. A.a in Squa.lua the whole auditory apparatus ia enclosed in a cartilaginous cranium 'Which appears as an elevation between the spiracles and mid-line. Perea flavescens (Figure 21) has the same number of 1emi-oircular cam.la aa the Raji. However, the Perea has a large utrioulua and a much larger sac­ culus than previously found . The endolymphatio duct now grcnr1 out of the sao­ culus to the exterior. The bony auditory capsule is connected with the cranial cavity. In tu.notion the auditory apparatus ia for hearing and equilibrium.

1:{earing in any of the fishes is the perception ot m.eohanioal vibrations of low frequency. Fish are capable of hearing with their auditory organs but not to the extent that land vertebrates are which are subject to vibrations of the air.

When forms leav,e the water tor a land habitat , they no longer breath by 30

£t1e.fol M ph�i-:c. V�d,b�\c. j -to e.1t�vi ov- ,______N Jo /,� /titpJ, J t,•e.,. d CA�t S,M;Ci°UIA h., C ;\ 1t l l

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-::....------+-,�-- HoY", · l- o tit..l l S C.h\� (: ive.l4.,'Ii"'

Eustachian tube and the columella (stapes) respectively. The incus develops from the quadrate of the lower vertebrates while the �lleus crune from t�e proximal end of Meokel 's cartilage which was cut off fr om the tatial structure. CHAPTER IV

SUMMARY AND CONCLUSIONS

1. The Cyclostomata, Elaamobranchii. and Pisces ha.ve reapiratory­ ayatema uaing gilla 'to take the oxygen tram the water.

2. All forms live in wat er during their entire life.

3. All forms have a atructure related to the respiratory system usually known as spiracle, or a deri'V8.tive from it .

4. The spiracle in its typical form is a modified gill-olett derived

:tram the first pharyngeal pouoh and containing a rudimentary gill structure as in the Elasmobranchii. through this canal water passes from the exterior to the pharynx.

6. '?he Cyoloetomata posseu a primitive form of apiracle in the median nasal canal . In Petromyzon marinua the nasal capsule ends as a blind sac• the pituitary pouch, which opens only to the exterior, while 14yxines maintain a connection with the.pharynx.

e. In the Raji the spiracle is equipped with a valve which regulates the flow of the water into the pharyngeal canal.

7. The Teleosts, except .A.oipenser and , Polyodon, have no apiraoular opening to the exterior. The upper end has been closed off' by the formation of the operoulum (Salmon haa a rudimentary paeudobra.noh under the operoulua) .

8. The apirac le is related to the aui itory appa.ra'tua . Diverticula were found protruding from the apiraoularr canal toward and in aom.e oasea

32 33 connecting with the aud itory- structures.

9. When the · tympanum is formed it originatea trOlll atruoturea around the 1piraoular canal and closes the opening to the exterior• the lower part forming the Euataohian tube.

10. The development of the tympanum and the Eustachian tube parallels the development of the auditory receiving mechanism which appears in the land torma that must adjust themaelve s to recording air waves. The first true tympanum and Eustachian tube appear in the .Anura.

...•.. .:• . • ,J .J • . : •• • ,

BIBLIOGRAPHY 35

BIBLIOGRAPHY

Adams, Leverett .l.llen, An Introduction --to the Vertebrates, New Yorks John Wiley & Sons, Irie ., 1938 .

Beard , J., "A Thymus-Element of the Spiracle in Ra!1,• Anatomischer Anzeiger, November 1900 , Vol. XVIII, Jena , Ver ag_von Gustav Fischer, 1§61.

Daniel, J. Fr&Dk, � Elasmobranch Fishes, Berkleya University ot Cal ifornia Press, 1928 .

DeBeer, G. R., Vertebrate Zoology, New York: The :MacMillan Company, 1928 . Goodrich, Edwin s., Studies on the Structure � Development 2!_ Vertebrates, New York: The MacMillan Company, 1930.

Ho rner, S. F. and Shipley, A. E., Fishes and Aseidians, Etc •• The Cam.bridge Natural History Series, Vol. VII, NewYork: The MaeMill�n Company, 1922.

Hegner, R. W ., College Zoology, Fourth Edition, New York : The MacMillan Compaey-, 1936 .

Hyman, Libbie, H., A La.borato Manual com rative Vertebrate Anatcmw:, 7 � 5 �hicago1 The University o Chicago Press, 922.

Kingsley, J. s., Textbook !:! Vertebrate Zoology, NewYork s Henry Holt and Company, 1911.

Kulme, Eugene R., A Guide to the Fishes of Tennessee and the Mid-South, · Nashville, Tennessee Dep8. rtment of Conservation, 1939:--

Neal, Herbert V. and Rand , Herbert W., Com. rati ve Anatom , Philadelphia a U y . P. Blakiston' s Son and Company , Inc . , 9S6.

NorTia, H. W. and Hughes. · Sally P., "The Spiracular Sense-Organ in Elasmobranohs, Ge.noid, Dipnoan,a _Anatomy Reoord, .Vol. XVIII, PP • 205-209. Owen, Richard, Anatomy of Vertebrates, Vol. I,"F ishes and Reptiles.!'Lond on: Longman' s, Green and Company , l866 . _

Parker, T. Jeffrey and H�swell, 'William A., A Text�Book of Zoology, Fourth Edition, Londona MacMillan and Canpany , T928 . - ·

Ridewood, W. G., "On the Spiracle and Associated Structures in Elasmobranch Fishes," A:natomisoher Anzeiger. December 1895, Vol. XI, Jena.a Verlag Yon Gustav Fischer, 1896. Stockard, Charle s R., •rhe Development ot the Mout h and Gills ot Bdelloatoma Stouti," American Journal � Anatomy:. Vol . v. pp. 481-617. 36

Wilder� Harris ·H., The Hi story 2£ � Human Body, New Yorks Henry Holt and Company, 19'ff': ·

Wieman, H. L., An Introduction to Vertebrate Embryology, New York s McGraw­ Hill Book Company, Ino �, _19�. Woodruff, Lorande Loss , Animal Biology, New York s The MacMillan Company, 1938.