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Marine Biological Laboratory Library 

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M.A., F.R.S. 






© Oxford University Press ig^ 2 
Library of Congress Catalogue Card Number: 62-21012 

First Edition 1950 
Second Edition 1962 

Printed in the United States of America 


My grateful thanks are due to the following, who spent much time reading and 
criticizing various parts of the manuscripts and proofs: 

E. H. Ashton, A. d'A. Bellairs, Q. Bone, B. B. Boycott, P. M. Butler, S. Crowell, 

D. H. Cushing, F. C. Fraser, R. B. Freeman, H. Greenwood, I. Griffiths, R. J. 
Harrison, R. A. Hinde, K. A. Kermack, J. Lever, N. B. Marshall, D. R. Newth, 
C. Nicol, F. R. Parrington, P. Robinson, A. J. Sutcliffe, H. G. Vevers, E. I. 
White, M. Whitear. 

Thanks for permission for reproductions of illustrations are due to: 

G. C. Aymar, E. J. W. Barrington, J. Berrill, T. H. Bullock, A. J. E. Cave, 
W. E. Le Gros Clark, E. Crosby, F. G. Evans, Helen Goodrich, A. Gorbman, 
J. Gray, W. K. Gregory, W. J. Hamilton, J. E. Harris, L. Hogben, A. Holmes, 

E. Hoskings, W. W. Howells, J. S. Huxley, F. Knowles, D. Lack, N. A. Mackin- 
tosh, G. H. Parker, A. T. Phillipson, R. J. Pumphrey, E. C. R. Reeve, A. S. 
Romer, E. S. Russell, F. K. Sanders, A. H. Schultz, G. G. Simpson, N. Tinber- 
gen, G. L. Walls, L. Waring, T. S. Westoll, E. I. White, F. F. Zeuner, 

and to the following publishers and other bodies: 

The American Museum of Natural History; Bailliere, Tindall and Cox; E. 
Benn, Ltd. ; Biological Reviezvs ; the British Medical Journal; the British Museum ; 
the Cambridge University Press; the Company of Biologists, Ltd.; Dodd, Mead 
& Co.; Editors of the Ibis; Longmans, Green & Co., Ltd.; the Physiological 
Society; Putnam, Ltd.; the Scientific Monthly; the Wilson Bulletin; the Wistar 
Institute; Zoological Society of London. 


For this edition every part of the book has been revised and corrected, 
but the basic plan and balance of interests have not been altered. 
Changes of arrangement and emphasis might have suited some types 
of reader but I have thought it better that the book should continue 
to show the idiosyncracies and interests of the author. One of the 
dangers of a textbook is, surely, that unsophisticated readers may sup- 
pose that they are getting the authentic and complete treatment of the 
subject. Some obvious imbalances may, therefore, even be an advan- 
tage as reminders of the relativity of all statements. 

Nevertheless, I have attempted to make the treatment rather more 
complete and systematic than before. For example, the descriptions 
of the parts of the body are now arranged more nearly similarly for all 
groups. With the help of many friends mistakes have been removed 
and accounts of recent work added. The anatomy of Mammals is not 
dealt with in the same detail as that of other groups, being covered 
separately in The Life of Mammals (Clarendon Press, 1957), where 
also there is a fuller account of the comparative embryology of 

During the revision I have become even more conscious of the 
defects of the work, both in general form and detailed treatment. It is 
still not possible to see more than the vaguest outlines of a proper 
science of comparative biology. We are faced with a great series of 
wonderful systems, differing slightly from each other and maintaining 
themselves in slightly different surroundings. But we have no proper 
scientific words with which to talk about them. For example, it is 
absurd that this book contains so little reference to genetics, bio- 
chemistry, or control theory. No doubt this is partly my fault, but the 
fact is that these more exact sciences have yet to show us how to treat 
the organization of a whole creature. 

Fortunately, the animals remain as fascinating as ever, indeed the 
search for exact ways of describing makes them even more so. Those 
of us who have revised the book will be well rewarded for our trouble 
if others arc helped to look and think for themselves. If they do they 
will find a really astonishing array of experiments made by natural 
selection with every part of the vertebrate organization. To take one 
example, we are offered the opportunity to learn how the endocrine 


control system works by examining hundreds of different variants of 
it. The more one thinks of it the more surprising it is that biology 
has made so little use of the experiments that have been done for us 
by nature. Surely soon someone will come along with sufficient know- 
ledge and logical and mathematical ingenuity to show us how to study 
vertebrate organization. 

Besides those mentioned below who have assisted in the revision of 
particular sections, I should like to thank the many people, including 
teachers and students, who have written about particular points, and 
especially Professor J. Lever of Amsterdam for his many detailed 
comments. My grateful thanks are also due to Mrs. J. Astafiev, who 
has redrawn many of the figures, Mr. C. Marmoy for assistance with 
the Bibliography, Mr. P. N. Dilly, who has helped throughout, also 
my secretaries and especially Miss S. Thistleton and Miss J. Everard, 
for continuous help with the manuscript. It is also a pleasure to thank 
the members of the Clarendon Press and in particular Miss M. Gregory 
for the help with the revision. 

J. Z. Y. 

February 1962 


The history of textbooks is often dismissed by the contemptuous 
assertion that they all copy each other — and especially each other's 
mistakes. Inspection of this book will quickly confirm that this is true, 
but there is nevertheless an interest to be obtained from such a study, 
because textbooks embody an attitude of mind; they show what sort 
of knowledge the writer thinks can be conveyed about the subject- 
matter. It may be that they are more important than at first appears 
in furthering or preventing the change of ideas on any theme. 

The results of the studies of scholars on the subject of vertebrates 
have been summarized in a series of comprehensive textbooks during 
the past hundred years. Most of these works are planned on the lines 
laid down by the books of Gegenbaur (1859), Owen (1866), and 
Wiedersheim (1883), lines that derive from a pre-evolutionary tradi- 
tion. This partly explains the curiosity that in spite of the great impor- 
tance of evolutionary doctrine for vertebrate studies, and vice versa, 
vertebrate textbooks often do not deal directly with evolution. They 
derive their order from something even more fundamental than the 
evolutionary principle. The essential of any good textbook is that it 
should be both accurate and general. As Owen puts it in his Preface: 
Tn the choice of facts I have been guided by their authenticity and 
their applicability to general principles.' The chief of the principles 
he adopted was 'to guide or help in the power of apprehending the 
unity which underlies the diversity of animal structures, to show in 
these structures the evidence of a predetermining Will, producing 
them in reference to a final purpose, and to indicate the direction and 
degrees in which organisation, in subserving such Will, rises from the 
general to the particular'. He confessed 'ignorance of the mode of 
operation of the natural law of their succession on the earth. But that 
it is an "orderly succession" — and also "progressive" — is evident 
from actual knowledge of extinct species.' 

These principles were essentially sound, and Owen's treatment was 
to a large extent the basis of the work that appeared after the Dar- 
winian revolution. In English, following the translation of Wieder- 
sheim's book by W. N. Parker (1886) we have H. J. Parker and 
Haswell's work, now in its 6th edition. The books of Kingsley and 
Neal and Rand are in essentially the same tradition, though they 


incorporate much new work, especially from the neurological studies 
of Johnston and Herrick. Further exact studies on these same general 
morphological lines made possible the books of Goodrich (1930) and 
de Beer (1935), which have provided the morphological background 
for the present work. Throughout these works on Comparative Ana- 
tomy the emphasis is on the evolution of the form of each organ 
system rather than on the change of the organization of the life of 
the animal as a whole. 

Meanwhile many other treatises appeared dealing with the life and 
habits of the animals, rather than with morphological principles. 
Among these we may mention Bronn's Tierreich (1859 onwards), the 
Cambridge Natural History, and many works dealing with particular 
groups of vertebrates. The palaeontologists produced their own series 
of textbooks, mainly descriptive, such as those of Zittel and Smith 
Woodward, culminating in Romer's admirably detailed and concise 
book, to which the present work owes very much. The results of 
embryological work have been summarized by Graham Kerr (191 9), 
Korscheldt and Heider (1931), Brachet (1935), Huxley and de Beer 
(1934), and Weiss (1939), among others. Unfortunately there has been 
little summarizing of what is commonly called the comparative physio- 
logy of vertebrates. Winterstein's great Handbuch der vergleichenden 
Physiologie (191 2) covers much detailed evidence, but comes no nearer 
than do the comparative anatomists to giving us a picture of the 
evolution of the life of the whole organism. 

All of these books deal in some way with the evolution of vertebrates, 
and vet curiously enough they speak of it very little. It is hardly an 
exaggeration to say that they leave the student to decide for himself 
what has been demonstrated by their studies. Huxley's Anatomy of 
Vertebrated Animals (1871) is an exception in that it deals with the 
animals rather than their parts, and at a more popular level. Brehm's 
Thierleben (1876) gives a picture of the life of the animals, though in 
this case not of their underlying organization. Kukenthal's great 
Handbuch der Zoologie has the aim of synthesizing a variety of know- 
ledge about each animal-group, and some of the volumes dealing with 
vertebrates make fascinating reading- — notably that of Streseman on 
birds. But the size of the work and the multiplicity of authors make 
it impossible for any general picture of vertebrate life to appear from 
the mass of details. 

The position is, then, that we have good descriptions of the struc- 
ture, physiology, and development of vertebrates, of the discoveries 
of the palaeontologists and accounts of vertebrate natural history, but 


that there is no work that attempts to define the organization of the 
whole life and its evolution in all its aspects. Indeed, none of these 
works defines what is being studied or tries to alter the direction of 
investigation — all authors seem prepared to agree that biological study 
is adequately expressed through the familiar disciplines of anatomy, 
physiology, palaeontology, embryology, or natural history. In passing, 
we may note the extraordinary fact that there are no detailed works on 
the comparative histology or biochemistry of vertebrates — surely most 
fascinating fields for the future, as is, indeed, hinted by the attempts 
that have been made in older works, such as that of Ranvier (1878), 
and the newer ones of Baldwin (1937 and 1945). 

The present book has gradually grown into an attempt to define 
what is meant by the life of vertebrates and by the evolution of that 
life. Put in a more old-fashioned way, this represents an attempt to 
give a combined account of the embryology, anatomy, physiology, 
biochemistry, palaeontology, and ecology of all vertebrates. One of 
the results of the work has been to convince me more than ever that 
these divisions are not acceptable. All of their separate studies are 
concerned with the central fact of biology, that life goes on, and I 
have tried to combine their results into a single work on the way in 
which this continuity is maintained. 

A glance through the book will show that I have not been successful 
in producing anything very novel — others will certainly be able to 
go much farther, and in particular to introduce to a greater extent facts 
about the evolution of the chemical and energy interchanges of verte- 
brates, here almost omitted! However, I have very much enjoyed the 
attempt, which has provided the stimulus to try to find out many 
things that I have always wanted to know. 

For any one person to cover such a wide field is bound to lead to 
inexactness and error in many places. I have tried to verify from 
nature as often as possible, but a large amount has been copied, no 
doubt often wrongly. Throughout, the aim has been to provide 
wherever possible an idea of the actual observations that have been 
made, as well as the interpretations placed upon them. A proper 
appraisal of general theories can only be reached if there is first a 
knowledge of the actual materials, which is the characteristic feature 
of scientific observation. A book such as the present has value only 
in so far as it leads the reader to make his own observations and helps 
him to know the world for himself. 

Mammalian organization requires more detailed treatment than 
that of other groups, and in providing this the work grew to beyond 


the length of a single book. Mammalian structure, function, and 
development will therefore be dealt with in a separate volume, which 
will also include a survey of comparative embryology. 

The original plan was that the palaeontological parts of the book 
would be written by J. A. Moy-Thomas. Had he lived this aspect of 
the work would have been very much better, and his common sense 
and laughter would have lightened the whole. I have tried to give 
some compensation at least by the speculation that is possible from a 
single point of view. To protect the reader against the limitations of 
my ignorance I have consulted specialists on every part of the work, 
and my deepest thanks are due to those who have helped in this way. 
They have done wonders in correcting mistakes, but, of course, are 
not responsible for any that remain, or for views expressed. Among 
those who have helped in this way with particular parts are Professor 
G. R. de Beer, Mr. R. B. Freeman, the late Professor W. Garstang, 
Dr. A. Graham, Professor J. B. S. Haldane, Professor W. Holling- 
worth, Dr. W. Holmes, Dr. J. S. Huxley, Dr. D. Lack, Mr. Maynard 
Smith, Dr. F. S. Russell, Dr. Tyndell Hopwood, Mr. H. G. Vevers, 
Professor D. M. S. Watson, and Professor S. Westoll. They have been 
patient and severe critics, and the reader and I owe them very much. 

One of the main problems of such a work is its illustration, and here 
I have been extraordinarily fortunate in having the help of Miss E. R. 
Turlington, who has not only provided brilliantly clear and beautiful 
pictures, but has taken extremes of care to ensure their accuracy by 
drawing from live animals, from dissections, and from skeletons, as 
well as by research into the illustrations of others. Miss J. de Vere 
has also given much help with drawing. We have borrowed good 
pictures unhesitatingly and should like to thank those who have given 
permission for their reproduction. 

I should also like to thank particularly my secretary, Miss P. Codlin, 
who has played a large part in making the book possible, and my 
daughter Cordelia for help with the index. 

Finally, I have to thank the Secretary and members of Oxford 
University Press for the care with which the book has been produced, 
and for their friendly co-operation, which has made the work a 

J. Z. Y. 





i. The need for generality in zoology, i ; 2. What do we mean by the life of an 
animal ? 2; 3. Li ving things tend to preserve themselves, 3; 4. What do we mean by 
awareness of life ? 5 ; 5. The influence of environment on life, 7 ; 6. What is it that 
heredity transmits ? 8 ; 7. The increasing complexity of life, 9 ; 8. The progression 
of life from the water to more difficult environments, 9; 9. Changes of climate and 
geological periods — (1) Changes of level of the continents, 11; (2) Changes of 
climate, 13; (3) Geological time, 16; (4) Classification of geological history, 18; 
10. Summary, 21. 



1. The variety of chordate life, 23; 2. Classification of chordates, 24; 3. Amphi- 
oxus, a generalized chordate, 24; 4. Movement of amphioxus, 26; 5. Skeletal 
structures of amphioxus, 29; 6. Skin of amphioxus, 29; 7. Mouth and pharynx 
and the control of feeding, 30; 8. Circulation, 33; 9. Excretory system of 
amphioxus, 35; 10. Nervous system, 36; 11. Gonads and development of 
amphioxus, 41; 12. Amphioxus as a generalized chordate, 46. 

1. Invertebrate relatives of the chordates, 47; 2. Subphylum Hemichordata 
(= Stomochordata), 50; 3. Class Pterobranchia, 58; 4. Subphylum Tunicata. 
Sea squirts, 60; 5. Development of ascidians, 66; 6. Various forms of tunicate, 
69; 7. Class Ascidiacea. 70; 8. Class Thaliacea, 70; 9. Class Larvacea, 72; 

10. The formation of the chordates, 74. 


1. Classification, 81; 2. General features of vertebrates, 81; 3. Agnatha, 83; 
4. Lampreys, 83; 5. Skeleton of lampreys, 85; 6. Alimentary canal of lampreys, 
88; 7. Blood system of lampreys, 91; 8. Urinogenital system of lampreys, 93; 
9. Nervous system of lampreys, 97; 10. The pineal eyes, 103; 1 1. Pituitary body 
and hypophyseal sac, 106; 12. Lateral line organs of lampreys, 108; 13. Vesti- 
bular organs of lampreys, 109; 14. Paired eyes of lampreys, no; 15. Skin photo- 
receptors, in; 16. Habits and life-history of lampreys, 112; 17. The ammocoete 
larva, 114; 18 Races of lampreys, a problem in systematics, 119; 19. Hag-fishes, 
order Myxinoidea, 122; 20. Fossil Agnatha, the earliest-known vertebrates, 125. 

1. The elasmobranchs : introduction, 131; 2. The swimming of fishes, 133; 
3. Equilibrium of fishes in water; the functions of the fins, 136; 4. Skin of 
elasmobranchs, 141; 5. The skull and branchial arches, 142; 6. The jaws, 145; 
7. Segmentation of the vertebrate head, 148; 8. The pro-otic somites and eye- 
muscles, 149; 9. The cranial nerves of elasmobranchs, 152; 10. Respiration, 157; 

11. The gut of elasmobranchs, 158; 12. The circulatory system, 159; 13. Urino- 
genital system, 162; 14. Endocrine glands of elasmobranchs, 164; 15. Nervous 
system, 167; 16. Receptor-organs of elasmobranchs, 170; 17. Autonomic nervous 
system, 173. 



i. Characteristics of elasmobranchs, 175; 2. Classification, 175; 3. Palaeozoic 
elasmobranchs, 176; 4. Mesozoic sharks, 180; 5. Modern sharks, 180; 6. Skates 
and rays, 182; 7. Chimaera and the bradyodonts, 184; 8. Tendencies in elasmo- 
branch evolution, 185; 9. The earliest Gnathostomes, Placoderms, 186. 


1. Introduction: the success of the bony fishes, 190; 2. The trout, 191; 3. The 
skull of bony fishes, 193; 4. Respiration, 196; 5. Vertebral column and fins 
of bony fishes, 199; 6. Alimentary canal, 201 ; 7. Air-bladder, 201 ; 8. Circulatory 
system, 201 ; 9. Urinogenital system and osmoregulation, 202; 10. Races of trout 
and salmon and their breeding habits, 204; 1 1. Endocrine glands of bony fishes, 
206; 12. Brain of bony fishes, 209; 13. Receptors for life in the water, 212; 
14. Eyes, 212; 15. Ear and hearing of fishes, 216; 16. Sound production in 
fishes, 218; 17. The lateral line organs of fishes, 218; 18. Chemoreceptors. 
Taste and smell, 220; 19. Touch, 222; 20. Autonomic nervous system, 222; 
21. Behaviour patterns of fishes, 225. 


1. Classification, 228; 2. Order 1. Palaeoniscoidei, 228; 3. Order 2. Acipen- 
seroidei, 234; 4. Superorder 2. Holostei, 234; 5. Superorder 3. Teleostei, 236; 

6. Analysis of evolution of the Actinopterygii, 237. 


I. Swimming and locomotion, 244; 2. Various body forms and swimming habits 
in teleosts, 248; 3. Structure of mouth and feeding-habits of bony fishes, 251; 
4. Protective mechanisms of bony fishes, 252; 5. Scales and other surface armour, 
252; 6. Spines and poison glands, 253; 7. Electric organs, 253; 8. Luminous 
organs, 254; 9. Colours of fishes, 255; 10. Colour change in teleosts, 258; 

II. Aerial respiration and the air-bladder, 261; 12. Special reproductive 
mechanisms in teleosts, 265. 


1. Classification, 268; 2. Crossopterygians, 268; 3. Osteolepids, 268; 4. Coela- 
canths, 271; 5. Fossil Dipnoi, 273; 6. Modern lung-fishes, 275. 



1. Classification, 296; 2. Amphibia, 296; 3. The frogs, 298; 4. Skin of Amphibia, 
298; 5. Colours of Amphibia, 299; 6. Vertebral column of Amphibia, 303; 

7. Evolution and plan of the limbs of Amphibia, 307; 8. Shoulder girdle of 
Amphibia, 309; 9. Pelvic girdle of Amphibia, 312; 10. The limbs of Amphibia, 
313; 1 1. The back and belly muscles of Amphibia, 318; 12. The limb muscles of 
Amphibia, 322; 13. The skull of Stegocephalia, 325; 14. The skull of modern 
Amphibia, 328; 15. Respiration in Amphibia, 332; 16. Respiration in the frog, 
333; I 7- Respiratory adaptations in various amphibians, 334; 18. Vocal appara- 
tus, 334; 19. Circulatory system of Amphibia, 335; 20. Lymphatic system of 
Amphibia, 338; 21. The blood of Amphibia, 339; 22. Urinogenital system of 
Amphibia, 340; 23. Digestive system of Amphibia, 342; 24. Nervous system 
of Amphibia, 344; 25. Skin receptors, 349; 26. The eyes of Amphibia, 350; 27. 
The ear of Amphibia, 353; 28. Behaviour of Amphibia, 354. 



i. The earliest Amphibia, 356; 2. Terrestrial Palaeozoic Amphibia. Embolomeri 
and Rhachitomi, 357; 3. Aquatic Amphibia of the later Palaeozoic, 359; 
4. Tendencies in the evolution of fossil Amphibia, 362; 5. Newts and Salaman- 
ders. Subclass Urodela, 364; 6. Frogs and Toads. Subclass Anura, 365; 7. Sub- 
class Apoda (— Gymnophiona = Caecilia), 366; 8. Adaptive radiation and 
parallel evolution in modern Amphibia, 366; 9. Can Amphibia be said to be 
higher animals than fishes ? 367. 


1. Classification, 369; 2. Reptilia, 371; 3. The organization of reptiles, 372; 
4. Skin of reptiles, 373; 5. Posture, locomotion, and skeleton, 373; 6. Feeding 
and digestion, 378; 7. Respiration, circulation, and excretion, 378; 8. Reproduc- 
tion of reptiles, 380; 9. Nervous system and receptors of reptiles, 383. 


1. The earliest reptile populations, Anapsida, 386; 2. Classification of reptiles, 
391; 3. Order 1. Chelonia, 392; 4. Subclass *Synaptosauria, 399; 5. Order 
*Ichthyopterygia, 401 ; 6. Subclass Lepidosauria, 401 ; 7. Order Rhynchocephalia, 
402; 8. Order Squamata, 404; 9. Suborder Lacertilia, 407; 10. Suborder 
Ophidia, 411; 11. Superorder Archosauria, 416; 12. Order *Pseudosuchia, 417; 
13. Order *Phytosauria, 417; 14. Order Crocodilia, 418; 15. The 'Terrible 
Lizards', Dinosaurs, 421; 16. Order *Saurischia, 422; 17. Order *Ornithischia, 
424; 18. Order *Pterosauria, 426; 19. Conclusions from study of evolution of the 
reptiles, 429. 


1. Features of bird life, 431 ; 2. Bird numbers and variety, 431 ; 3. The skin and 
feathers, 432; 4. Colours of birds, 436; 5. The skeleton of the bird. Sacral and 
sternal girders, 437; 6. The sacral girder and legs, 440; 7. Skeleton of the wings, 
447; 8. Wing muscles, 449; 9. Principles of bird flight, 450; 10. Wing shape, 
452; 1 1. Wing area and loading, 452; 12. Aspect ratio, 453; 13. Wing tips, slots, 
and camber, 453; 14. Flapping flight, 455; 15. Soaring flight, 458; 16. Soaring 
on up-currents, 458; 17. Use of vertical wind variations, 460; 18. Speed of 
flight, 461; 19. Take-off and landing, 462; 20. The skull in birds, 464; 21. The 
jaws, beak, and feeding mechanisms, 464; 22. Digestive system of birds, 468; 
23. Circulatory system, 470; 24. Respiration, 471; 25. Excretory system, 474; 
26. Reproductive system, 475; 27. The brain of birds, 477; 28. Functioning of the 
brain in birds, 479; 29. The eyes of birds, 482; 30. The ear of birds, 488; 31. 
Other receptors, 490. 


I. Habitat selection, 491; 2. Food selection, 491; 3. Recognition and social 
behaviour, 492; 4. Bird migration and homing, 493; 5. The stimulus to migra- 
tion, 495; 6. The breeding-habits of birds, 496; 7. Courtship and display, 497; 
8. Bird territory, 503; 9. Mutual courtship, 504; 10. Nest-building, 505; 

I I. Shape and colour of the eggs, 507; 12. Brooding and care of the young, 507. 


1. Classification, 509; 2. Origin of the birds, 510; 3. Jurassic birds and the 
origin of flight, 510; 4. Cretaceous birds. Superorder Odontognathae, 513; 


5. Flightless birds. Superorder Palaeognathae, 514; 6. Penguins. Superorder 
Impennae, 515; 7. Modern birds. Superorder Neognathae, 516; 8. Tendencies 
in the evolution of birds, 522 ; 9. Darwin's finches, 524 ; 1 o. Birds on other oceanic 
islands, 530; 11. The development of variety of bird life, 532. 


1. Classification, 533; 2. The characteristics of mammals, 534; 3. Mammals of 
the Mesozoic, 536; 4. Mammal-like reptiles, Synapsida, 539; 5. Order *Pely- 
cosauria (= Theromorpha), 540; 6. Order *Therapsida, 541; 7. Mammals from 
the Trias to the Cretaceous, 545; 8. Original cusp-pattern of teeth of mammals, 
548; 9. Egg-laying mammals. Subclass Prototheria (Monotremata), 549. 


1. Marsupial characteristics, 557; 2. Classification of marsupials, 562; 3. Opos- 
sums, 563; 4. Carnivorous marsupials, 565; 5. Marsupial ant-eaters and other 
types, 566; 6. Phalangers, wallabies, and kangaroos, 566; 7. Significance of 
marsupial isolation, 568. 


1. Eutherians at the end of the Mesozoic, 569; 2. The end of the Mesozoic, 569; 
3. Divisions and climates of the Tertiary Period, 571; 4. Geographical regions, 
572; 5. The earliest eutherians, 574; 6. Definition of a eutherian (placental) mam- 
mal) 575; 7- Evolutionary trends of eutherians, 575; 8. Conservative eutherians, 
577; 9. Divisions and classification of Eutheria, 577. 


1. Order 1. Insectivora, 581; 2. Order Chiroptera. Bats, 585; 3. Order Dermo- 
ptera, 592; 4. Order Edentata, 592; 5. Armadillos, 595; 6. Ant-eaters and sloths, 
597; 7. Order Pholidota: pangolins, 601. 


1. Classification, 602; 2. Characters of primates, 603; 3. Divisions of the pri- 
mates, 607; 4. Lemurs and lorises, 609; 5. Fossil Prosimians, 613; 6. Tarsiers, 
614; 7. Characteristics of Anthropoidea, 617; 8. New World monkeys, Ceboidea, 


1. Common origin of Old World monkeys, apes, and men, 623; 2. Old World 
monkeys, Cercopithecoidea, 623; 3. The great apes: Pongidae, 626; 4. The 
ancestry of man, 633; 5. Brain of apes and man, 633; 6. The posture and gait of 
man, 634; 7. The limbs of man, 635; 8. The skull and jaws of man, 637; 9. Rate 
of development of man, 640 ; 10. Growth of human populations, 641 ; 1 1 . Time of 
development of the Hominidae, 641; 12. The Australopithecinae, 643; 13. Early 
Hominids, *Pithecanthropus, 645; 14. Man, 646; 15. Human cultures, 648. 


1. Characteristics of rodent life, 652; 2. Classification, 653; 3. Order Rodentia, 
654; 4. Order Lagomorpha, 660; 5. Fluctuations in numbers of mammals, 663. 




i. Affinities of carnivores and ungulates: Cohort Ferungulata, 677; 2. Classifica- 
tion, 679; 3. Order Carnivora, 680; 4. The Cats, 680; 5. *Suborder Creodonta, 
683; 6. Suborder Fissipeda, 684; 7. Suborder Pinnepedia, 691. 


1. Origin of the ungulates, 694; 2. Ungulate characters, 695; 3. Classification, 699; 

4. Superorder Protoungulata, 700; 5. South American ungulates. *Order Notoun- 
gulata, 701; 6. *Order Litopterna, 703; 7. *Order Astrapotheria, 703; 8. Order 
Tubulidentata, 704. 


1. 'Near-ungulates', superorder Paenungulata, 706; 2. Classification, 706; 
3. Order Hyracoidea, 707; 4. Elephants. Order Proboscidea, 709; 5. *Order 
Pantodonta (Amblypoda), 717; 6. *Order Dinocerata, 718; 7. *Order Pyro- 
theria, 718; 8. *Order Embrithopoda, 718; 9. Order Sirenia, 720. 


1. Perissodactyl characteristics, 722; 2. Classification, 723; 3. Perissodactyl 
radiation, 724; 4. Suborder Ceratomorpha, tapirs and rhinoceroses, 727; 

5. Rhinoceroses, 728; 6. *Brontotheres (*Titanotheres), 730; 7. *Chalicotheres 
(= *Ancylopoda), 731; 8. Palaeotheres, 732; 9. Horses, 732; 10. Allometry in 
the evolution of horses, 737; 11. Rate of evolution of horses, 738; 12. Conclu- 
sions from the study of the evolution of horses, 739. 


1. Characteristics of artiodactyls, 741; 2. Classification, 745; 3. The evolution 
of artiodactyls, 746; 4. Pigs and hippopotamuses, 748; 5. *Oreodonts, 750; 

6. Camels, 751; 7. Ruminants, 753; 8. Chevrotains, 754; 9. Pecora, 755; 
10. Cervidae, 755; II. Giraffidae, 757; 12. Antilocapridae and Bovidae, 760. 


1. The life of the earliest chordates, 765; 2. Comparison of the life of early 
chordates with that of mammals, 767; 3. The increasing complexity and variety 
of vertebrates, 768; 4. The variety of evidence of evolutionary change, 769; 
5. Rate of evolutionary change, 770; 6. Vertebrates that have evolved slowly, 
771; 7. Varying rates of evolutionary changes, 774; 8. Vertebrates that have 
disappeared, 774; 9. Successive replacement among aquatic vertebrates, 775; 
10. Successive replacement among land vertebrates, 776; 11. Is successive re- 
placement due to climatic change?, 776; 12. Convergent and parallel evolution, 
777'. ! 3- Some tendencies in vertebrate evolution, 779; 14. Evolution of the 
whole organization, 780; 15. Summary of evidence about evolution of verte- 
brates, 781; 16. Conservative and radical influences in evolution, 783; 17. The 
direction of evolutionary change, 784; 18. The influences controlling evolutionary 
progress, 785. 


INDEX 797 





1 . The need for generality in zoology 

The aim of any zoological study is to know about the life of the ani- 
mals concerned. Our object in this book is, therefore, to help the 
reader to learn as much as possible about all the vertebrate animal life 
that has ever been. Thinking of the great numbers of types that have 
existed since the first fishes swam in the Palaeozoic seas, one might 
well be appalled by such a task: to describe all these populations in 
detail would indeed demand a huge treatise. However, in a well- 
developed science it should be possible to reduce the varied subject- 
matter to order, to show that all differences can be understood to have 
arisen by the influence of specified factors operating to modify an 
original scheme. Animal and plant life is so varied that it has not yet 
proved possible to systematize our knowledge of it as thoroughly as 
we should wish. Thinking, again, of the variety of vertebrate lives, 
it may seem impossible to imagine any general scheme and simple set 
of factors that would include so many special circumstances. Yet 
nothing less should be the aim of a true science of zoology. Too often 
in the past we have been content to accumulate unrelated facts. It is 
splendid to be aware of many details, but only by the synthesis of 
these can we obtain either adequate means for handling so many 
data or knowledge of the natures we are studying. In order to know 
life — what it is, what it has been, and what it will be — we must 
look beyond the details of individual lives and try to find rules govern- 
ing all. Perhaps we may find the task less difficult than expected. 
Even an elementary anatomical and physiological study shows that 
all vertebrates are built upon a common plan and have certain simi- 
larities of behaviour. Our object will be to come to know the nature 
of this plan of life, of structure, and action, to show how it is modified 
in special cases and how each special case is also an example of a 
general type of modification. 

Since the problem arises from the variety of animals that have 
lived and live today, our central task is obviously to inquire into the 
reason for the existence of so much difference. If vertebrate life began 
as one single fish-like type, why has it not continued as such until 
now? Why, instead of numerous identical fishes, are there countless 


different kinds, while descendants of most unfish-like form are found 
living out of the water and even in the air and under the ground ? 

To put it in a way more familiar, though perhaps less clear: what 
are the forces that have produced the changes of animal form ? Know- 
ing these forces, and the original type, it would be possible to con- 
struct a truly general science of zoology, with sure premisses and 
deductions. Even if we cannot reach this end, we should at least try, 
hoping that after investigation of the biology of vertebrates it will be 
possible to retain something more than a mass of detailed information. 
At the end of such a study, if we deal with the subject right, we should 
surely be better able to answer some of the fundamental biological 
questions. We should be able to say something about the nature of 
evolution and of the differences between types, to know whether there 
have been rhythms of change at work to produce these differences, 
and also — the acid test of any true science — to forecast how these 
changes are likely to proceed in the future. 

2. What do we mean by the life of an animal? 

In biology we make much use of analogies, attempting to grasp the 
nature of the processes at work by comparison with man-made 
machines. We have a science of anatomy, which we are told is con- 
cerned with the 'structure' of animals, and we feel that we understand 
what 'structure' means. Physiology is the study of 'function', and 
this, too, we seem to understand. We take the analogies from our 
machines, which have what we call 'structure' and 'function'. How- 
ever, the difficulty at once arises that the living things make and control 
themselves. The whole scheme fails us when we ask what is it, then, 
that we call the 'life' of the animal, and what is it that is passed on 
from generation to generation, and that changes through the ages by 
the process we call evolution ? It has gradually become apparent that 
the body is not a fixed, definite 'structure' as it appears to casual 
observation or when dissected. In life there is ceaseless activity and 
change going on within the apparently constant framework of the body. 
The movement of the blood is one sign of this activity, and since 
Harvey's discovery of the circulation ( 1 628) we have learnt of innumer- 
able others. Everyone knows that the skin is continually being renewed 
by growth from below, and many other types of cell are similarly 
replaced; for instance, red blood-cells last only for a few weeks in 
man. Even in the cells that are not completely destroyed and replaced, 
such as the nerve-cells, there is continual change of the molecules that 
make up their substance. The full extent of this exchange has been 


shown by using isotopes to discover for how long individual atoms 
remain in the body; the work of Schoenheimer (1942), which by this 
means first clearly established the rapidity of the turnover, is a classic 
of modern biology. 

There are no man-made machines that replace themselves in this 
way, but in recent years there has been much study of machines that 
control their own operations. Such work provides us with new analo- 
gies and new mathematical techniques with which we can analyse 
the control of living systems (see Yockey and Quastler, 1958). As yet 
we have no means of grasping the enormously complicated network 
of activities that constitutes a single life. Throughout this book, how- 
ever, an attempt will be made to approach that end by use of certain 
clues to help us to concentrate on significant features, to see the 
rhythms or patterns common to the lives of the animals, and thus to 
carry in mind many details. It is possible in this way to bring together 
information collected by morphologists, geneticists, embryologists, 
physiologists, biophysicists, and biochemists to give a single view of 
the life of the organisms concerned. The task is admittedly a hard one 
and the success achieved only partial. Continually one slips into the 
discussion of particular structures, substances, or processes, forgetting 
the whole life. A detail of form or of chemical composition attracts, 
and thus distracts, attention; perhaps it can hardly be otherwise if we 
are to describe exactly. But it is surprising how practice improves the 
powers of selecting and emphasizing those patterns or details of 
knowledge that are significant for the study of each life as a whole. 

The first difficulty is to force oneself to remember all the time that 
a living animal or plant system is in a continual state of change. When 
making any observations, whether by dissection or with the micro- 
scope, with a test-tube, microelectrode, or respirometer, it is necessary 
continually to think back to the time when the tissue was active in the 
living body, and to frame the observation so that it shall reveal some- 
thing significant of that activity. This means that every biologist 
must know as much as possible of the life of the whole organism with 
which he deals ; indeed, something of the whole population from which 
the specimen was drawn. 

3. Living things tend to preserve themselves 

The clue by which we recognize significant features during any 
biological study is that living activity tends to ensure the continuance 
of its own pattern. The processes of life draw materials into the 
system, organize them there, and then send them out again, all in such 


a way that the arrangement or pattern of the processes remains almost 
unchanged as the molecules pass through it. We see analogies in the 
way that a waterfall or a human institution such as the Catholic 
Church remains the same, though its components change. Our 
business is to try to describe this arrangement or pattern of processes 
that is preserved. It is this pattern that we call the life of the species. 
The activities that go to make up one sort of life are not necessarily 
all to be found in any one individual, still less in any part of an in- 
dividual. The pattern is not to be seen in any single creature or 
part. Though we speak of 'individuals' they are no more the final 
units than are the cells, the heart, or the brain, the bones, hair, or 
nails. A whole interbreeding population is the unit of life that tends 
to preserve the type, assisted, in social species, by individuals that 
play a part in the life without participation in reproduction, such as 

A wide range of activities, therefore, goes to make up any one type 
of life, and we shall only appreciate these activities properly if we study 
that whole life as it is normally lived in its proper environment. The 
way to study animals or men is, first and foremost, to examine them 
whole, to see how their actions serve to meet the conditions of the 
environment and to allow preservation of the life of the individual and 
the race. Then, with this knowledge of how the animal 'uses' its parts 
we may be able to make more detailed studies, down to the molecular 
level, and show how together the activities form a single scheme of 

A living animal is continually doing things. Even when it is asleep 
it is breathing, its heart beating and brain pulsing, while countless 
chemical changes go on throughout its tissues. The waking life, of 
course, shows this restless action even more clearly. Animals may 
indeed sometimes be still, but they are never wholly inactive. It is not 
difficult to see startling glimpses of this activity if we watch animals 
alive, especially when they are in groups. A hawk wheeling, a pond 
full of tadpoles, or a crowd of people moving on a city street will 
remind us that if we are to see the interesting side of life we have to 
study activity and not, as is more easy to do and so often done, to 
spend all our time examining the 'structure' or 'chemistry' of the dead. 

The peculiarity of this activity of animals is that much, perhaps 
most, of it has the effect of maintaining the integrity of the body and, 
indeed, even of increasing the bulk, or of reproducing more bodies 
like the first (homeostasis). The search for food provides raw materials 
giving to the muscles energy for further search. If the situation 


demands still greater efforts these efforts will themselves lead to 
'hypertrophy', or increase in the muscle substance and power. Simi- 
larly, the muscular movements of respiration provide the oxygen by 
which these same movements and others are made possible. 

We could go on indefinitely describing how the activity of each part 
of the body tends, with some exceptions, to ensure the continuation 
of the whole. The mere statement of the existence of this tendency to 
self-maintenance does not, perhaps, sufficiently emphasize the power 
that it represents. It is one of the great 'forces' that control the 
matter of the earth. It causes huge masses of material to be moved 
annually to the tops of high trees and millions of wonderfully built 
animals to roam daily to find and consume uncounted tons of food 
or, not finding it, to search on and maintain their activity while any 
calorie remains available. The power of life is sufficient to bring about 
the incorporation of an appreciable part of the matter of the earth's 
surface into living things. Within the appropriate range of conditions, 
found chiefly near the surface of the sea and on the damper parts of 
the earth, life dominates the lifeless and provides a main influence on 
the matter present. 

Animals and plants are able to take these actions that tend to their 
own preservation because they contain stores of information about 
the conditions that are likely to be met with and the means by which 
adverse changes may be prevented. A fish is born with a body so 
shaped that it may swim, a gull can soar on air currents, and a monkey 
leap from branch to branch. Every type may thus be said to represent 
the environment in which it lives, that is to say, it has a hereditary 
store of information about it. Moreover, this hereditary store provides 
it with receptor organs and brain with which it can acquire further 
information during its lifetime. The study by engineers of the means 
by which information may be coded, transmitted, and stored has 
provided biologists with further means for study of the living memory 
stores, which are comparable in some ways with those of machines. 

4. What do we mean by awareness of life ? 

A man states that he is aware that he is alive. He says that he knows 
his needs and that he feels satisfaction when they are fulfilled. One 
of the most difficult problems of biology is to decide how to relate 
such statements about 'subjective experience' to what may be called 
the 'objective' descriptions of science. This is clearly a philosophical 
problem too large and important to be discussed properly here but 
it must be approached. Perhaps it begins to find a solution when we 


remember that in speaking of all these matters we are using the words 
of a conventional code, trying with them to convey information to 
our fellows or somehow to influence them. Then we shall stop 
asking such questions as 'what is consciousness ?' substituting 'what 
sort of information does he transmit when he says "I am conscious" ?' 

This will help with the particular aspect of the problem that con- 
cerns us here. In trying to define what we mean by the 'life' of an 
animal should we assume that, in addition to the actions of its body, 
which we describe, there are also actions of some other entity, its 
'mind' ? It is true that we should feel that any description of our own 
lives that left out 'awareness' was ludicrously incomplete. Since we 
have evolved from animals, so the argument runs, why should we 
deny that they have some form of 'consciousness' ? This seems logical 
but overlooks that the essential feature of statements such as T am 
aware that I am alive' or T feel pain' is that they are part of the 
means by which man, the communicating animal, controls and 
influences his environment. Statements are part of human life, just 
as swinging from branches is a feature of the life of monkeys and 
flying of birds. It will at once be objected that these animals also 
communicate, but the point is that communication must be considered 
as a part of the life system of each animal, like respiration, locomotion, 
or reproduction. 

This leaves us with the baffling problem of finding words with 
which to describe the describing system itself. Where indeed can we 
find a sure basis from which to start? Here, I think, we can only 
proceed by humbly admitting both ignorance and inadequacy. In 
our language we have a communication system with which we can 
convey to each other incomparably more information than passes 
between other animals. Our system is improving every year, but it is 
still grossly inadequate to describe the more subtle features of the 
world, and especially of living things. We may show the greatest 
respect for the depth of these mysteries by recognizing that they are 
still too great for us to describe in our simple language. To provide a 
good description of all the marvellous features of the life of a man or 
an animal requires a complicated and subtle terminology, for which 
we are striving. In pre-scientific language all such problems are 
simplified by supposing that the actions of any system are produced 
by some agent rather like a human being that resides within it. Thus 
a child says that the clouds move 'because they want to'. So we are 
accustomed to say that the body moves because it is guided by 'the 
mind'. This may indeed be the best way of speaking for some 


occasions, with our imperfect language, but it is a feeble descriptive 
technique. I do not believe that it is satisfactory for biology and 
especially not for zoology. By the life of an animal we mean all those 
activities that make a certain pattern and serve to maintain that 
pattern. In so far as we can describe this as a whole it is by comparing 
it with other self-maintaining systems and particularly with those 
self-controlling machines that we have made for ourselves. Biology 
today has a great opportunity to explore the means by which animals 
remain alive, using many sorts of descriptive technique, chemical, 
electrical and, not least, the means by which mathematicians and 
engineers describe whole complicated self-maintaining systems. It 
is in such language that a fuller and richer account of living things 
can be given. It is curious that objections to the use of scientific 
terminology often claim that it somehow 'reduces' or 'restricts' our 
view of life. Exactly the reverse is the case. Explaining human or 
animal life in terms of 'spirits', good or bad, is only describing them 
by comparison with themselves. Scientific description allows us to 
break out of our narrow prison and to show how each of the many 
aspects of life can be measured and compared with the forces that can 
be detected throughout the universe. 

5. The influence of environment on life 

Growth is the addition of material to that which is already organized 
into a living pattern. But the pattern is not fixed and invariate, even 
throughout any one life. Each individual changes through its lifetime, 
develops, as we say, and moreover is modified by the action upon it 
of its surroundings. Those parts that are exercised by the interaction 
of the animal's tendencies and the surrounding circumstances increase 
in amount (hypertrophy), while any disused parts undergo atrophy or 
reduction. The pattern is thus able to conform to a considerable 
extent to the exigencies of change in the external world. It could be 
imagined that a sufficiently plastic animal organization would be able 
in this way, if its tendencies to survival were strong enough, to mould 
itself to all the changes of climate through the millennia, so that a 
great variety of animal tvpes would arise by use and disuse alone. 
Only a limited degree of change is possible in this way, however, and 
it is not such changes either of development or by the direct influence 
of environment that we call 'evolution'. There is abundant evidence 
that the result of such interaction between organism and environment 
is not handed on in the genetic code. Acquired characters are not 


6. What is it that heredity transmit? 

What is passed on is a coded pattern or plan controlling the 
organization of the life processes of the next generation. The plan 
takes the physical form of a series of molecules of deoxyribose 
nucleotides (DNA) in the chromosomes. These by the specific 
arrangements of the four types of base that they contain somehow 
organize the proper linear sequences of the twenty or so amino-acids 
that make up the proteins of each species. By the emergence at the 
proper time during development of the appropriate proteins, enzyme 
systems are produced that ensure the development and functioning of 
the embryo and later the adult. We cannot fully understand how all 
these processes are regulated but we see in outline how it all follows 
if the DNA molecules provide a code from which natural selection 
has chosen in the past those items that are suitable to provide viable 
organisms for a particular environment. 

The organization of life is very rarely identical in any two indi- 
viduals; there is, therefore, a considerable range of potential patterns 
resident in all those animals of a population that are capable of mating 
together. The sum of those variants of the hereditary materials con- 
stitutes the pattern or mould, as it were, of the life of the whole species. 
Evolution consists in a change in this hereditary genotype, producing, 
of course, a new set of adults. The genotype probably rarely stays for 
long quite the same. Even in species that do not seem to be changing 
rapidly there are continual adjustments, for example in the power to 
produce antibodies or to manufacture enzymes. Evolution, proceeding 
by mutation, recombination, and selection, is not some remote or 
rare thing occurring only sporadically. It is a 'physiological' process as 
much as is a change in respiration rate or in number of red cells, but 
it has a longer time course than these. Evolution is the process by 
which the whole population adjusts its control system to meet chang- 
ing needs. Over long periods of years these adjustments produce the 
new forms of life that appear as, say, the first fishes, or land animals 
or mammals. Our aim is to try to discover the conditions under 
which each new main group of vertebrates arose and so to understand 
the processes that have been at work, modifying the basic organization. 

We must therefore direct our studies continually to populations, 
rather than to single individuals, thinking of all the creatures of a 
kind, spread out wherever a suitable habitat for them occurs. They 
will not all be alike genetically, and the circumstances of the lives of 
some members of the group may become sufficiently dissimilar to 


produce further divergences by use and disuse. Limitations of inter- 
mating may occur on account of limitation of movement, accentuated 
by partial and, perhaps, eventually complete geographical barriers. 
Such variations in external circumstance become matched by diver- 
gences in type, until two new races are produced, at first relatively 
and then absolutely infertile, so that there are then two separate 
populations or species instead of one. 

7. The increasing complexity of life 

The acquisition of new matter, and hence growth and reproduction, 
occurred in the earliest animals by relatively simple means, as it still 
does today in the bacteria, lower plants, and some protozoa. It is not 
easy to provide rigid criteria for the definition of 'simple'; perhaps 
some of the chemical changes involved may be quite complex, but the 
whole system can, with meaning, be said to be simple. The number 
of parts that it contains is relatively small and the number of 'adap- 
tive' actions that it can take is limited. A population of bacteria in a 
suitable culture medium obtains its raw materials by diffusion; the 
chief device that it uses to secure these materials is to provide a large 
number of spores, so that some may come to rest in suitable sur- 
roundings. Such a life can be said to be more simple than that of a 
vertebrate, whose system includes many special devices for obtaining 
access to the raw materials that it needs. We can say that a species of 
bacteria transmits less information than a vertebrate. LInfortunately 
there are no satisfactory counts of the number of genes available; the 
amount of DNA in bacteria is said to be about 0-05 mgm per gm 
and in rat liver 2 mgm per gm. Bacteria of any one species are able to 
alter their enzymes to suit the substrates available, but their life does 
not depend upon the differentiation into numerous cell types each 
with its special functions. The variety of information available in the 
'higher' genotypes enables them to take actions that ensure survival 
under conditions where the 'lower' organisms would die. Of course, 
each type has its own special 'niche' and the comparison of higher and 
lower is only possible if we can show exact quantitative differences. 

8. The progression of life from the water to more difficult environ- 

In general, the new environments colonized have involved ever 
wider departures from that watery one in which life first arose. This 
is shown most strikingly if we contrast the simple way in which the 
means of life are obtained by a marine bacterium with the complicated 


activities that go to maintain a man alive in a city. Yet all living 
systems, even those that have changed most markedly since their first 
origin, are still watery, and must have salt and nitrogenous com- 
pounds with which to make proteins and so on. Perhaps, indeed, the 
basic plan of the living activity differs less in the various types than 
one might suppose. 'Protoplasm' is certainly not identical in all 
creatures, but it may be that it differs less than do the outward forms 
that support it. 

In order to provide the conditions necessary for the maintenance of 
such a watery system, in very different environments, many auxiliary 
activities have been developed. It is these that give added complexity 
to the higher animals and plants, enabling them to undertake what 
can be called more difficult ways of life. In order to do this their 
activity must also be physically greater than is necessary in more 
lowly types. It may be presumed that more energy is transferred to 
maintain a given mass of living matter in the less 'easy' environments, 
and in this sense the higher animals are less efficient than the lower, 
by a very crude criterion of efficiency. 

According to this conception, then, evolution has involved a change 
in the relationship between organism and environment. Life has 
come to occupy places in which it did not exist before. Perhaps the 
total mass of living matter has thus been greatly increased. It must 
not, of course, be supposed that every evolutionary change has pro- 
duced an increase in complexity in this way; examples of 'degenera- 
tion' are too well known to need quoting. We have, however, a clear 
impression that through the years there has been, in general, some 
change in animals and plants and that in a sense some of the later 
organisms are 'higher' than the earlier. It is hardly possible to deny 
that there is some meaning in the assertion that man is a higher 
animal than amoeba. Our thesis attempts to specify more clearly what 
we can know about this evolutionary change, by saying that it con- 
sists of a colonization by life of environments more and more different 
from that in which life arose. This colonization was made possible 
by the gradual acquisition of a store of instructions enabling adjust- 
ments to be made by which life could be maintained in conditions not 
tolerable before. 

It is not easy to enumerate the complexity of any animal or to 
define quantitatively the nature of its relations with its environment, 
and for this reason it is difficult to prove our thesis rigorously. This 
book nevertheless makes an attempt to show how the organization of 
vertebrate life has become more complex since it first appeared, and 


that the increasing complexity is related to the adoption of modes of 
life continually more remote from the simple diffusion of substances 
from the sea. Of course, even the earliest vertebrates had already 
departed a long way from the first conditions of life and were quite 
complex organisms. However, in the history of their life through 
nearly 500 million years since the Ordovician period we can trace con- 
siderable further changes in complexity. During this time vertebrate 
life has left the sea to live in fresh water, on swampy land, and finally 
on dry land and in the air. It has produced special types able to sup- 
port life by such an astonishing variety of devices that we cannot 
possibly specify them all. We shall only direct attention to a few, and 
thus attempt to obtain an impression of the scheme of life of the vast 
hordes of vertebrate animals, which, in one shape or another, have 
swarmed and still swarm in the waters and over the earth. We shall 
try to discern whether there is reason to suppose that all this variety 
is related in some way to changes in the surrounding world and we 
may therefore finish this introduction by a brief survey of the evi- 
dences for climatic and geographical changes such as may have been 
responsible for the changes in organic life. 

9. Changes of climate and geological periods 

9.1. Changes of level of the continents 

Changes of geography are mostly so slow that they cannot in them- 
selves influence individual lives. On the other hand, nearly all living 
things must be suited to daily and annual cyclical changes, unless they 
live where no light enters. There is indirect evidence of further 
changes in climate and geography, occurring with such long periods 
that they are without appreciable effect on individual organisms, but 
may greatly affect the history of the race. 

The idea of geographical change is made familiar by the fact that 
coast-lines and river-courses have changed appreciably in historical 
times. We are familiar with stories of destruction of some houses or 
of a village by the sea, though it may come as a shock to learn that the 
sea-level has changed so much that England and France were con- 
nected by land 8,000 years ago, and that man-made instruments fished 
up from the Dogger Bank show that it was an inhabited peat bog 
6,000 years B.C. These changes in height of the land are signs of the 
'diastrophic movements', which are major features of long-period 
geological evolution. The earth forces that produce these movements 
are still obscure but they lead to repeated elevation and sinking of the 
land masses. The action of frost, wind, and rain continually breaks up 


and carries away the surface of the land, at a rate of the order of 1 ft 
per 4,000 years, the processes known as weathering and denudation. 
The material carried away is deposited in the river-beds and in the 
lakes and shallow seas around the river mouths (sedimentation) (Fig. 
1). Here it builds the sedimentary rocks, which may be many thou- 
sands of feet in thickness, the whole continental platform continuing 
to sink for long periods, perhaps with intervals during which it be- 
comes raised above the water. Fossil remains are usually the result of 




High mountain 

Average height ^ 
r of land tr X$ 


Fig. i. Curve showing the areas of the earth's solid surface in relation to the 
sea level. (From Holmes.) 

the preservation of the harder parts of animals in sedimentary deposits, 
and the most complete series of fossils are likely to be those of animals 
living in the seas. 

The surface crust of the earth is not a layer of uniform thickness and 
density but consists of irregular masses of lighter material, rich in 
silicon and aluminium (sial), forming the continents, and heavier 
material, rich in magnesium (sima), under the ocean beds. The reason 
for this non-uniform distribution is obscure, but it has the effect of 
making the continents stand higher, floating on the plastic denser 
medium beneath the crust. When material is removed from the con- 
tinents by denudation they rise; conversely the addition of millions 
of tons of ice will depress them. The continents are thus said to rest 
in isostatic equilibrium, and following the small changes in level the 
sea leaves more or less of the continental shelf uncovered. Such 
upward and downward movements profoundly influence the climate. 
Oceanic climatic influences tend to produce a damp, equable climate, 
with large areas of marsh and forest. When the land stands higher 


extremes of climate develop, some parts being cold, others forming 
large, dry interior plains. 

Besides changes in the balance produced by denudation and the 
advance of ice-caps there are also from time to time marked move- 
ments of uplifting or lowering of the land, which may be called 
independent earth movements. Such vertical movements of the con- 
tinental masses are produced by internal forces of unknown origin. 
They are doubtless related to a second series of major movements of 
crustal deformation that are due to tangential forces and lead to the 
formation of new mountain ranges (orogenesis) by compression, or to 
fracturing by tension. The upwelling of lava from the inside of the 
earth at these times makes the igneous rocks, usually devoid of fossils. 

Changes in geography are, then, mainly changes in the height of 
the land and the amount of it that is above water. Where the con- 
tinent is surrounded by a rather shallow continental shelf, this leads 
to considerable changes in appearance of the land-masses. The general 
opinion is that the main outline of the continental masses has remained 
much as at present, at least since Cambrian times. However there have 
probably been considerable movements of the land-masses in relation 
to each other. Some hold that the continents of lighter material are 
continually expanding, at least in certain directions, having grown 
from small centres to their present size. According to the hypothesis 
of Wegener, the continents have all been formed by the splitting up 
of one or a few land-masses. There is indeed evidence from both 
geophysics and biology that the continents have been drifting apart 
(Bullard, 1959). The direction of magnetization of rocks, which is 
determined at the time of their formation, shows that the land-masses 
must have changed their positions greatly. For example, such data 
show that during the Triassic period the British Isles lay in the tropics 
and in confirmation of this we find that many salt deposits (formed 
only in very warm climates) lie in the Triassic formation (Droitwich, 
Bath, Nantwich, &c). 

9.2. Changes of climate 

Evidence of marked changes of climate is the finding in England 
and other regions now temperate of animal and plant remains appro- 
priate to warmer or colder conditions (corals and woolly rhinoceros, 
for instance). There is thus every reason to think that there have been 
great changes from hot to cold and wet to dry conditions, in conjunc- 
tion with the changes in latitude and in level of the land. 

These fluctuations in geography and climate are obviously of great 


importance to the biologist. We can hardly expect to treat animals 
and plants as stable systems if the environment around them is 
changing. In order to be able to assess the influence of such changes 
on life we must know more about the rates at which they occur, and 
careful study shows that some of the climatic changes are rhythmic. 
Rhythmic changes of climate are, of course, very familiar to us in the 
cycles of days, months, and years, and the immense importance of 
these short-period changes for animal and plant life must not be 

Here we are more concerned with changes of longer periodicity, of 
which the best known are fluctuations of the amount of solar radiation 
received at any given part of the earth's surface. These are likely to 
be especially important since plants, and hence ultimately animals, 
depend for their energy on sunlight. The cycle of number of sun- 
spots (n*4 years) involves a change in amount of radiation, and this is 
associated with some biological cycles, for instance in the distribution 
of the rings of growth made by trees. Longer-period fluctuations in 
the amount of radiation received on any part of the earth's surface 
depend on the perturbations of the earth's orbit, particularly on 
changes in the obliquity of the ecliptic. The effect of these perturba- 
tions can be calculated, and the results show that at any one place 
there are rhythmical variations in the amount of radiation received, 
and in its seasonal distribution. The periodicity of these calculated 
changes is about 40,000 years, with considerable irregularities and 
variations in the sizes of the maxima (Fig. 2). 

During the last million years (the Pleistocene epoch) there has been 
a series of waves of glaciation (ice ages); the ice-caps have several 
times advanced towards the equator and then retreated again. These 
changes are usually classified into four periods of glaciation, separated 
by interglacial periods. However, the last (fourth Pleistocene) glacia- 
tion, of which we know the most, certainly had three separate climaxes 
of cold. The correspondence of these with especially marked minima 
in the curve of solar radiation is not perfect (Fig. 2), but it suggests 
that the basic periodicity may have been something like 40,000 years, 
and that the division of the whole Pleistocene period into four periods 
of glaciation obscures a change with much shorter periodicity. From 
about 120,000 to 180,000 years b.p. (Before Present) there were no 
marked minima in the solar radiation curve, and this agrees with other 
evidence of a long interglacial period (third Pleistocene interglacial). 
Two marked minima agree with the other signs of a penultimate (third 
Pleistocene) glaciation, and this was preceded by a very long warmer 


period, the second inter-glacial. As we go farther back the study 
becomes more and more difficult, but the available evidence suggests 
that fluctuations of climate considerable enough to alter the entire 
fauna and flora may have taken place at a periodicity of something 
over 40,000 years. It is a measure of the difficulty of geological 
science that we cannot yet give a systematic account of the chronology 
or climatic changes even of the relatively recent Pleistocene period 
(variously estimated at 600,000 to 1,800,000 years) during which these 
glaciations occurred. 

RM590 R.M550 
EGI 1 EGI 2 


RM476 RM 435 

ApGI I ApGI 2 


Fig. 2. Curve of solar radiation received at 65 ° N. lat. in the summer. The radiation is 
expressed in 'canonic units' (related to the solar constant in calories). Time in thousands 
of years. R.M. 25, &c, indicate the radiation minima. (From Zeuner, based on the tables 

of Milankovitch.) 

As we proceed to study times still more remote our vision becomes 
increasingly blurred. We can now only rarely distinguish periodicities 
as short as 40,000 years, though there is evidence that they existed, for 
instance from varved Cretaceous sediments. All we can see in the 
study of geological deposits are the very marked changes produced by 
the major movements of orogenesis and by the isostatic readjust- 
ments. The surprising thing is that these immensely slow changes 
have been sufficiently regular to leave layered deposits, allowing the 
development of a system of geological classification. The process of 
sedimentation was interrupted by periods when the continental shelf 
on which the rocks rest was raised above the water surface and under- 
went denudation for a while, before being again lowered below the sea 
and covered with a new deposit. During the interval, while the shelf 
was raised above the water, the animals and plants in the sea became 


changed; thus rather sharp breaks appear in the series of fossils. The 
occurrence of these breaks has been used by geologists to define the 
major geological periods, which thus correspond to cycles of elevation 
and depression of the continents. By comparing the fossils contained 
in the rocks major geological periods have been recognized in various 
parts of the world. The times of submergence and emergence differ 
from region to region, however, and no very close detailed comparison 
is possible. It is easy to forget that climates and land levels do not 
always change in the same direction in different parts of the world. 

9.3. Geological time 

Until recently most geologists assumed that there was a regular 
cycle of raising and lowering (diastrophism) and that comparable 
periods could be recognized everywhere. It is now widely doubted 
whether there has been any such 'pulse of the earth'. The rock series 
are not the same in all the continents. For example, in South Africa 
three long series, known as Cape, Karoo, and Cretaceous formations, 
occupy the time covered in Europe by the many elevations and depres- 
sions between Silurian and Cretaceous times. Probably the conditions 
under which rocks were formed have remained about the same 
throughout geological time but have been interfered with by periods 
of elevation, depression, and folding that are peculiar to each region. 

The study of fossils often establishes the order in which the rocks 
were laid down, but other methods have to be used to discover the 
period of time covered by each stage. This is especially important to 
the biologist, who wants to know the rate at which animals or plants 
have evolved. Reliable knowledge of the ages of the rocks has only 
begun to accumulate since the discovery of radioactivity. Uranium 
and thorium disintegrate, producing lead, at rates that are unaffected 
by any known conditions. The age of any rock since its deposition can 
therefore be calculated if we can estimate the amount of breakdown 
products of these elements present in it. The lead present in a rock is 
often not all derived from the uranium and thorium there, but separa- 
tion of the lead isotopes enables those of radioactive origin to be 
estimated, and the age of the deposit can then be determined, assum- 
ing that the breakdown of uranium to lead began when the rock was 
crystallized in its present position. Other methods of estimating the 
ages of rocks from isotope ratios have been developed. Especially 
promising is the determination of the ages of the deposition of sedi- 
mentary rocks from the ratio of A 40 /K 40 and Sr 87 /Rb 87 in deposits 
formed by erosion of micas or granites. 




The time at which the crust of the earth assumed its present form 
is now thought to have been 4,500 million years ago (Holmes, 1959) 
but the rocks laid down during the greater part of this long period 
contain no undoubted animal or plant remains. Cambrian rocks, 
when fossils become readily discernible, were laid down about 600 
million years ago. 

25 60 
11 40 70 

135 180 225 270 305 350 400 440 






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Fig. 3 shows the maximum thickness of sediment in each period plotted against estimates 
of the absolute date. The error attached to these determinations is shown by the 
marginal lines. Apparently the rate of sedimentation has not been constant (modified 

after Holmes). 

Classical geology is based mainly on studies in Europe and North 
America. Although a terminology based on absolute time is beginning 
to emerge, it is still necessary to use that based mainly on stratigraphic 
studies, begun by William Smith in the British Isles early in the nine- 
teenth century. In this system, the time since the Cambrian is divided 
into eleven major periods, but several of these were double or triple 
periods of advance and retreat of the sea. Even the most carefully 
compiled radioactivity data are not yet adequate to provide us with 
definite estimates of the durations of the periods, though there is 
agreement on a total period of about 600 million years since the 
Cambrian. Fig. 3 shows the maximum thickness of sediment in each 
period plotted against estimates of the absolute dates. The error 


attached to these determinations is shown. Apparently the rate of 
sedimentation has not been constant. 

It is conventional to postulate a series of crustal revolutions. The 
extent of the movements has not been equal throughout and some of 
them, more marked than others, were times of building of great 
mountain chains such as the Alps or Andes (Fig. 4). There were also 
many lesser rises and falls and changes of climate with shorter periods, 

Table I 




































70 ± 2 





35± 5 





80 ± 5 





25± 5 



20 1 4 * 
26j 46 






70 ± 5 

• 350 ±10 





400 ±10 











600 ±20 


such as those of about 40,000 years that we can detect in the later part 
of the Pleistocene. Many modern geologists are sceptical about the 
existence of any regularities or rhythms in these changes (see Herbert, 
1952, and Gilluly, 1949). It is useful when trying to adjust the mind 
to periods of 30 million years to remember the frequent changes of 
level and climate that have occurred in the last 100,000 years. In 
spite of all that we know about the history of the earth's surface, it is 
necessary every time that we make statements about the influence of 
presumed climatic changes on organic evolution to remember how 
scanty our knowledge is. 

9.4. Classification of geological history 

The period isolated as 'Cambrian' by geologists lasted 100 million 
years and almost certainly included several inundations, perhaps 
three. The Ordovician lasted for 60 million years and included three 


floods in North America. There were powerful earth movements at 
the end of this period, at any rate in North America, known as the 
Taconian revolution. The Silurian, lasting for 40 million years, 
apparently included a single main cycle of inundation, ending in an 
elevation of the land, which though slight in America, was marked 
in Europe as the Caledonian revolution, producing the range of 
mountains stretching across Scandinavia to Scotland and Ireland. 







h-RiAssir iiiRA«if L0W U p PER 

Tai n 1- Acadian Appalachian Nevadian Laramidt Cascadian 

Fig. 4. Diagrams of main changes of areas of land and water and in climatic conditions 

since the Cambrian. The chief times of mountain-building (orogenesis) in America are 

also shown. (Redrawn by permission from Textbook of General Zoology, 2nd ed. by 

W. C. Curtis and M. J. Guthrie, John Wiley & Sons, Inc., 1933.) 

Throughout these early Palaeozoic periods the fossils are entirely 
those of aquatic animals, except for some traces of land plants and 
arthropods at the end of the Silurian. The oldest remains of verte- 
brates are fish-scales from the Ordovician (p. 125). Details of the 
Palaeozoic climatic changes are not clear, but the fact that corals, 
which can now live only in warm water, were alive over a considerable 
part of the earth's surface suggests that conditions were warmer than 
at present at least at some early Palaeozoic times. 

The Devonian is considered by some to include a single main 
period, about 50 million years long, with one flood at the middle and 
more arid conditions at the end, but other authorities divide it into 
several periods. The first forests appeared at this time, and here, also, 
are found tti3 first signs of vertebrate terrestrial life, in the form of 
fossil lung-fishes and amphibians (p. 296). The period recognized as 
Carboniferous in Europe includes two major periods of about 40 


million years each in America, the Mississippian and Pennsylvanian. 
Throughout this long time conditions varied widely in different parts 
of the world. In the early Mississippian there were many swamps in 
North America. In the northern hemisphere the Pennsylvanian was 
probably a time of warm, moist conditions, with no cold winters, 
but there are signs that for part of this time India and Africa were 
covered with an ice-sheet. The coal measures show us the remains of 
the forests of spore- and seed-bearing plants that were then pro- 
duced, and the land conditions evidently favoured the life of the 

The Permian probably constitutes a single 45-million-year period, 
with very active orogenesis, leading to a more arid climate, perhaps 
showing large seasonal changes, with deserts in some parts of the 
world and glaciation in others. These conditions continued into the 
Triassic, when the continents lay high. The reptiles, first found in 
the Permian, developed throughout the Triassic and flourished in the 
succeeding Jurassic period, which probably lasted 45 million years. 
The Cretaceous period, during which the thick chalk deposits were 
laid down, probably lasted for rather more than 60 million years, 
including two major cycles of inundation. The lower Cretaceous 
certainly included extensive periods of flooding, when there were 
large shallow seas. Then later, towards the end of the upper Creta- 
ceous, there were extensive orogenic movements, the Laramide 
revolution, producing the Rockies and the Andes. The temperature 
was warm until near the end of the Cretaceous, and we do not know 
what condition led to the break that is found between the animals of 
the Cretaceous and Eocene. Some groups of dinosaurian reptiles seem 
to have died out suddenly, but it is important to notice that not all 
disappeared at the same time, for instance, the stegosaurs and 
pterodactyls (p. 569) disappeared well before the end of the Cretaceous. 
However, it is probable that great changes went on at the end of this 
period, and we may guess that a factor leading to the development of 
the birds and mammals was the great rise of the continents, perhaps 
accompanied by a fall in temperature over wide areas that had enjoyed 
warmer weather. As always, when we look closely at such problems, 
we are appalled by the vast lengths of time involved and the scanty 
nature of our clues about them. The land lay very high at this time, 
and the apparent abruptness of the break between Cretaceous and 
Eocene fauna may be an artifact due to the scarcity of fossils. In 
North America there is evidence from terrestrial deposits of a long 
Paleocene period between the Cretaceous and Eocene. 


It is usual to divide the last main geological period, the Tertiary, 1 
into epochs, Paleocene, Eocene, Oligocene, Miocene, Pliocene, and 
Pleistocene, the names originally referring to the percentage of fossil 
genera surviving to the present day (see p. 571). Probably the whole 
time since the end of the Cretaceous has been about 70 million years. 
During the early part of the Tertiary period the climate was cold, but 
as erosion of the mountains that had been produced at the end of the 
Cretaceous proceeded the conditions became warmer, and throughout 
the Eocene and Oligocene there were large forests and humid con- 
ditions. Then during the Miocene there were marked earth move- 
ments, leading to elevation of the land and accompanied by more arid 
conditions, with wide areas of prairie and the widespread appearance 
of important new food plants — the grasses. The weather probably 
became gradually colder through the Pliocene, no doubt with many 
fluctuations, culminating in the ice ages of the Pleistocene. Here we 
come back to the period of which we have more detailed knowledge, 
and are reminded that the ice age was not continuous, but interrupted 
by many w r armer periods. 

This very brief survey of geological history in the northern hemi- 
sphere can hardly do more than remind us of the depths of our ignor- 
ance. We see enough to be sure that climatic conditions have varied 
throughout the millions of years, but we cannot yet see sufficient 
details to allow us to discover whether there is any rhythm of major 
cycles. It is easy to talk glibly of 'Carboniferous forests' or 'arid con- 
ditions of the Permian', forgetting that these periods lasted for a time 
that we can only roughly record in numbers and not properly imagine 
in terms of our experience, although we are among the longest lived 
of animals. The evidence suggests that conditions did not remain 
stable for such a vast length of time as a whole geological period, but 
fluctuated markedly, either irregularly or with complicated rhythms 
of greater and lesser magnitude. We must not forget that very pro- 
found 'climatic' changes occur every day, others every year, and some 
every eleven years. It is not impossible that these shorter-period 
changes, necessitating continual readjustment of animal and plant life, 
have been as important as the slower changes in producing evolution. 

10. Summary 

To reduce to order our knowledge of vertebrate life we shall try 
to discover its general organization and then examine the factors that 

1 This word is a survival from an old-fashioned classification of rocks, the Tertiary heing 
the period since the Cretaceous. 


have produced all the varied types. The pattern of organization we 
have to study is that of the animal as an active system maintaining 
itself in its environment. This tendency to maintenance and growth 
is the central 'force' that produces the variety of life. The opportunity 
for change is provided by the fact that reproduction seldom produces 
an exact copy of the parent, and thus a range of types is provided. 
The tendencies to grow and to vary lead animals to colonize new en- 
vironments and produce the variety of life. As evolution has proceeded 
animals have come to occupy environments differing ever more widely 
from the sea in which life probably arose. Life in these more difficult 
environments is made possible by the development of special devices, 
making the later animals more complex than the earlier and in this 
sense 'higher'. It remains uncertain what influences have been respon- 
sible for producing the changes in organic form. Geological evidence 
shows that there have been many changes in climate and geography, 
some of them proceeding at very slow rates in comparison with the 
rhythms of individual animal lives. It is uncertain whether evolution- 
ary changes follow these slow geological changes, or are a result of 
the instability imposed on living things by climatic rhythms with 
shorter periods, such as those of days, years, and the sunspot cycles. 



1 . The variety of chordate life 

The Chordata occupy a greater variety of habitats and show more 
complicated mechanisms of self-maintenance than any other group in 
the whole animal kingdom. They and the arthropods and the pulmon- 
ate molluscs have fully solved the problem of life on the land — which 
they now dominate. This domination is achieved by most delicate 
mechanisms for resisting desiccation, for providing support, and for 
conducting many operations that are harder in the air than in water. 
By even more wonderful devices the body temperature is raised and 
kept uniform and thus all reactions accelerated. Finally, use is made of 
this high rate of living for the development of the nervous system into 
a most delicate instrument, allowing the animal not only to change its 
response to a given stimulus from moment to moment, but also to 
store up and act upon the fruits of past experience. 

Besides these more developed types of chordate that dominate the 
land and air there are also great numbers of extremely successful 
aquatic and amphibious types. The frog is often referred to as a some- 
what lowly and unsuccessful animal, but frogs and toads are found all 
over the world. The sharks and bony fishes share with the squids and 
whales the culminating ecological position in the food chains of the 
sea, while the bony fishes are the only animals that have achieved con- 
siderable size and variety in fresh water. Among the still more lowly 
chordates the sea-squirts take a very important, though not dominant, 
position among the animal and plant communities that occupy the 
sea bottom, but they have never entered fresh water. 

One could continue indefinitely with particulars of the amazing 
types produced by this most adaptable phylum. Yet through all their 
variety of structure the chordates show a considerable uniformity of 
general plan, and there can be no doubt that they have all evolved 
from a common ancestor of what might be called a 'fish-like' habit. 
In the very earliest stages only the larva was fish-like, and the life- 
history probably also included a sessile adult stage, such as the tuni- 
cates still show today (p. 66). This bottom-living phase was then 
eliminated by paedomorphosis, the larvae becoming the adults. There- 
fore the essential organization of a chordate is that of a long-bodied, 


free-swimming creature. All the other types can be derived from such 
an ancestor, though in some cases only by what is often called 

2. Classification of chordates 

We may conveniently divide the Phylum Chordata into four 
subphyla : 

Subphylum i. Hemichordata 

Balanoglossus; Cephalodiscus; Rhabdopleura 
Subphylum 2. Cephalochordata (= Acrania) 

Subphylum 3. Tunicata 

Ciona, Sea-squirts 
Subphylum 4. Vertebrata 

The Vertebrata, the largest of these groups, may be subdivided: 
Subphylum Vertebrata 
Superclass 1. agnatha 

Class 1. Cyclostomata. Lampreys and hag- fishes 

Class 2. *Cephalaspidomorphi. *Cephalaspis 

Class 3. # Pteraspidomorphi. *Pteraspis 

Class 4. *Anaspida. *Birkenia, *Jamoytius 

Superclass 2. gnathostomata 

Class 1. *Placodermi. *Acanthodes 

Class 2. Elasmobranchii. Dogfishes, skates, and rays 

Class 3. Actinopterygii. Bony fishes 

Class 4. Crossopterygii. Lung-fishes 

Class 5. Amphibia 

Class 6. Reptilia 

Class 7. Aves 

Class 8. Mammalia. 

3. Amphioxus, a generalized chordate 

It has long been realized that through their great variety all these 
types show certain common features, often referred to as the typical 
chordate characters. It is better to regard these not as a list of isolated 
'characters' but as the signs of a certain pattern of organization that 
is characteristic of the group. There is much reason to suppose that 
this basic chordate organization was that of a free-swimming marine 
animal, probably feeding by the collection of minute particles. We 
are fortunate in having still alive a little animal, amphioxus, the 

ii. 3 AMPHIOXUS 25 

lancelet, which shows nearly all of these features in diagrammatic form. 
Study of amphioxus will go a long way to show the basic plan on which 
all later chordates are built, and, indeed, gives us a strong indication 
of what the early chordates must have been like. 

Though it can swim freely through the water, amphioxus is essenti- 
ally a burrowing animal, and many of its special features are connected 
with this habitat. It lives in the sand, at small depths, and has been 
found all round the oceans of the world. Evidently, in spite of its 
simplicity, it is a successful type. It is found on British coasts and, 
indeed, the first individual described was sent (preserved) from Corn- 
wall to the German zoologist Pallas, who supposed it to be a slug and 
called it Limax lanceolatus (1774). It was first figured and given the 
name Amphioxus lanceolatus by Yarrell in 1836. However, the name 
Branchiostoma had been given in 1834 by Costa and by the rules of 
priority this is the official name of the genus. We may keep amphioxus 
as a common name. Some eight species of Branchiostoma are recog- 
nized, and in addition there is a group of six species referred to the 
genus Asymmetron. These resemble Branchiostoma in general organi- 
zation, but they have gonads only on the right side. 

The adult Branchiostoma lanceolatum is rather less than 2 in. long 
and has the typical fish-like organization, whose main external 
features are related to the methods of locomotion and feeding (Fig. 
5). The body is elongated, and flattened from side to side. The skin 
has no pigment, and the muscles can be easily seen as a series of 
blocks, the myotomes, serving to bend the body into folds. As the 
name implies, the body is pointed at both ends; there is no recogniz- 
able head separated from the body. Indeed, there are no separate eyes, 
nose, or ears, and no jaws, so that the fundamental plan of chordate 
organization appears in almost its fullest simplicity from one end of 
the body to the other. The front end is, however, marked by a series 
of buccal cirri, which form a sieve around the opening of the oral hood 
and are provided with receptor cells. 

Although the animal is provided with a large number of gill-slits 
these do not appear externally, being covered by lateral folds of the 
body, which enclose a ventral space, the atrium, opening posteriorly 
by an atriopore. The outside edges of the atrium project as a pair of 
metapleural folds, giving the body a triangular shape in transverse 
section. The alimentary canal opens posteriorly by an anus, in front 
of the hind end of the body, thus leaving a definite tail — a region of 
the body not containing any part of the alimentary canal. 

The general arrangement of the organs can best be understood by 


considering the body as consisting of two tubes, the outer skin 
(ectoderm) and the inner alimentary canal (endoderm), with a space 
between (the coelom) lined by a third layer (the mesoderm). This 
arrangement is actually found during the course of the development 
(Fig. 18). The mesoderm at first forms thin layers, the somatopleure 
applied to the outer body wall and the splanchnopleure to the gut. 
Very soon the inner layer becomes much thickened where it is applied 
to the nerve-cord and notochord, and here it forms the myotomes, or 
muscle-blocks. In this dorsal part of the mesoderm the coelom, 
known here as the myocoele, soon becomes obliterated, leaving the 
ventral splanchnocoele around the gut. Besides the muscle that forms 
in the myotomes, non-myotomal muscles develop in the somatopleure 
and splanchnopleure. These are not divided into segments and are 
innervated by the dorsal nerve-roots, the ventral roots supplying only 
the myotomes. 

4. Movement of amphioxus 

The adult myotomes are blocks of striated muscle-fibres, running 
along the body, separated by sheets of connective tissue, the myo- 
commas. This repetition or segmentation is characteristic of the 
organization of all chordates. The myocommas do not run straight 
down the body from dorsal to ventral side but are V-shaped (Fig. 5). 
However, each muscle-fibre runs straight from before backwards, and 
the contraction of the whole myotome therefore bends the body. A 
full discussion of the means by which forward motion is achieved by 
such a system will be given later (p. 133). Essentially, contraction of 
the myotomes results in transverse motion of the body inclined at 
varying angles in such a way as to result in forward propagation. Each 
myotome must therefore contract after that in front of it — the effect 
being to produce an S-bend that moves backwards through the water 
as the fish moves forward. 

For our present purpose the point is that the contraction is serial, 
that is to say, it depends on the breaking up of the longitudinal muscle 
into blocks. It was probably the need for division of the musculature 
that led to the development of the segmentation, and this, affecting 
primarily the muscles, has come to influence a great part of chordate 

Contraction of the longitudinally arranged muscle-fibres will only 
produce a sharp bending of the body if there is no possibility of short- 
ening of the whole. To prevent telescoping, an incompressible and 
elastic rod, the notochord, runs down the centre of the body. It 

II. 4 



is usually stated that this is a 
'supporting structure', but, of 
course, an animal such as a fish in 
water needs no 'support'. Nor is 
the notochord a lever to which 
muscles are attached, as they are 
to the bones of many higher forms. 
No muscles pull on it directly, 
though the myocommas are at- 
tached to its sheath. Its function 
is to prevent the shortening of the 
body that would otherwise be the 
result of contraction of longitudi- 
nal muscles. In fact, it serves to 
make that contraction efficient in 
bending the body; its elasticity 
may also play an important 

The notochord is composed of 
a series of flattened plates sur- 
rounded by a fibrous sheath. The 
plates are arranged in a regular 
manner with their flat surfaces in 
the transverse plane of the body. 
They are of two sorts, fibrous 
and homogeneous, which alternate 
with each other. Each plate de- 
velops as a highly vacuolated cell, 
the nuclei being later pushed aside 
to the dorsal or ventral edge. This 
structure is well suited by the 
turgidity of its cells enclosed in 
the sheath to resist forces tending 
to shorten the body. The cord of 
amphioxus is peculiar in that it 
extends from the very tip of the 
head to the end of the tail, pro- 
jecting, that is to say, beyond the 
level of the myotomes, a condition 
presumably associated with the 
burrowing habit. 






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Amphioxus probably does not often swim free in the water and the 
body is not adapted for fast movements. It has no elaborate fins such 
as those of later fishes, which ensure static stability like the feathers 
on an arrow, or are movable, to allow active control of the direction 

Fig. 6. Transverse section through amphioxus in the region of the pharynx. 

atr. atrium; d.a. dorsal aorta; d. coel. dorsal portion of coelom; div. intestinal diverticulum; 
d.n. 1 and d.n. 2 , branches of the dorsal nerve-root; end. endostyle; epipharyngeal groove; 
/. fin-ray box; g. gonad; I y.b. primary gill bar containing coelom; my. myotome; metapl. 
nietapleural fold; n. notochord; n.c. nerve-cord; ph. pharynx; sub. end. coel. subendostylar 
coelom; t.b. tongue bar; v. a. ventral aorta; v.n. ventral nerve-root. (After Krause.) 

of swimming (p. 136). There is a low dorsal ridge, which continues 
behind as a small caudal fin. There are no definite paired fins, but the 
metapleural folds might perhaps be considered comparable to the 
lateral fin folds from which all vertebrate limbs are probably derived. 
They are distended with coelomic fluid and, with the dorsal ridge, 

II. 6 



probably serve to protect the body during the rapid dives by means of 
which the creature enters the sand. The habit of swimming with the 
front end downwards suggests the presence of a gravitational receptor 
mechanism. The larvae of lampreys swim in a similar way (p. 114). 


Fig. 7. Section of the skin of amphioxus. 

b.v. blood-vessel; cut. cutis; ep. epidermis; n. nerves; s.cut. sub-cutis. 
(After Krause.) 

5. Skeletal structures of amphioxus 

Around the notochordal sheath is a further layer of gelatinous 
material containing fibres. There are no cells within this material 
but it is secreted by cells around the outside, which retain the epithe- 
lial arrangement of the mesoderm from which they were derived. 
This connective tissue continues as a sheath around the nerve-cord 
and above this into a series of structures known as fin-ray boxes, 
which support the median ridge. These are more numerous than the 
segments and each contains a more rigid material referred to as 
'cartilage'. The relationship of these structures to the fin supports of 
vertebrates is obscure. Other skeletal rods occur in the cirri around 
the mouth and in the gill bars. 

6. Skin of amphioxus 

The epidermis differs from that of vertebrates in being very thin, 
composed of a single layer of cells, ciliated in the young, and with the 
outer border slightly cuticularized in the adult (Fig. 7). It is not 


known whether this cuticle contains a substance similar to the keratin 
produced by the many-layered skin of later forms. There are receptor 
cells but no glands or chromatophores in the skin. 

Below the epidermis is a fibrous cutis, and below this again a 
gelatinous material containing fibres, the sub-cutis. Both these layers 
are secreted by scattered cells having some similarity to the fibroblasts 

Fig. 8. Anterior end of amphioxus, from a stained and cleared preparation 
of a young animal. 

b.c. buccal cirri;/, fin-ray box; II. p. Hatschek's pit; my. myotome; n. notochord; 
n.c. nerve-cord; p. pigment spot; ph. pharynx; v. velar tentacles; zi.o. wheel organ. 

of higher forms. They contain a system of cutaneous canals, with 
endothelial lining (Fig. 14). 

7. Mouth and pharynx and the control of feeding 

Amphioxus obtains its food by extracting small particles from a 
stream of water, which it draws in by means of cilia. In all animals 
that use cilia for this purpose a very large surface is provided (e.g. 
lamellibranchs, ascidians), and the pharynx and gill bars of amphioxus 
occupy more than one-half of the whole surface area of the body. 
Special arrangements are made for the support and protection of this 
ciliated surface, the wall of the pharynx being so greatly subdivided 
that it needs the protection of an outer layer, the atrium. 

The mouth lies covered by an oral hood whose edges are drawn out 
into buccal cirri, provided with sense-cells (Fig. 8). When feeding the 
cirri are curved to form a funnel-like sieve preventing the entry of 
large particles. Around the mouth itself there is a further ring of 

ii. 7 



sensory tentacles, the velum. The oral hood contains a complex set of 
ciliated tracts, the 'wheel organ' of Miiller, and this plays a part in 
sweeping the food particles into the mouth (Figs. 8 and 9). Near its 
centre is a groove, Hatschek's pit, formed as an opening of the left 
first coelomic sac to the exterior (p. 44). 

The main operation of food collec- 
tion is performed by the pharynx, a 
large tube, flattened from side to side, 
whose walls are perforated by nearly 
200 oblique vertical slits, the number 
increasing as the animal gets older. 
The slits are separated by bars con- 
taining skeletal rods and further sub- 
division is provided by cross-bars 
(synapticulae). Since the bars slope 
diagonally many of them are cut in a 
single transverse section, but it must 
be remembered that they are essen- 
tially the vertical portions of the main 
walls of body and pharynx, where 
these have not been perforated by a 
gill-slit. Such a portion of the body 
wall must contain a coelomic space 
and this can in fact be seen in the 
original or primary gill bars. How- 
ever, an increase of the ciliary surface 
is produced by downgrowth of secon- 
dary or tongue bars from the upper 
margin, dividing each primary slit; 

these secondary bars contain no coelom. The coelomic spaces in the 
primary bars, of course, communicate above and below with con- 
tinuous longitudinal coelomic cavities (Fig. 6). 

There are cilia on the sides and inner surfaces of the gill bars, the 
lateral ones being mainly responsible for driving the water outwards 
through the atrium and thereby drawing the feeding current of water 
in at the mouth. In the floor of the pharynx lies the endostyle, con- 
taining columns of ciliated cells, alternating with mucus-secreting 
cells, which produce sticky threads in which food particles become 
entangled. Various currents then draw the sticky material along until 
it reaches the mid-gut. The frontal cilia of the gill bars produce an 
upward current, driving the mucus from the endostyle into a median 

Fig. 9. Transverse section through 
front end of amphioxus. 

b.c. buccal cirri; e. eyespot; H.p. Hats- 
chek's pit; ?i. notochord; n.C. nerve-cord. 


dorsal epipharyngeal groove, in which it is conducted backwards. 
The cilia of the endostyle also move mucus along the peripharyngeal 
ciliated tracts, behind the velum, to join the epipharyngeal groove. 
Radioactive iodine is concentrated by one of the columns of the endo- 
style and secreted with the mucus. Barrington (1958) suggests that 
these may be regarded as the precursors of the thyroid cells, serving 
to produce iodinated mucoproteins, which are then absorbed farther 
down the gut (see p. 119). 

The pharynx narrows at its hind end to open dorsally into a region 
best known as the mid-gut, the name stomach being inappropriate. 

£{■ nig. ant. (cft 

/ Ag 

T ^^^' |l ^ | i | Mii)iifmiTn^ r . y 

Fig. 10. Currents in the mid-gut of amphioxus, showing the appearance when an 
animal is placed in a medium containing carmine particles. Arrows show the chief 

ciliary currents. 

div. diverticulum ;f.c. food cord; h.g. hind-gut; i.c.r. ileo-colon ring; m.g.ant. and 

anterior and posterior parts of mid-gut; oes. oesophagus. (After Barrington.) 

A large mid-gut diverticulum reaches forward from this region on the 
right-hand side of the pharynx. From its position this organ is often 
called the liver, but Barrington has given reasons for supposing that 
it is the seat of the production of digestive enzymes. Zymogen cells, 
similar to those of the mid-gut, are found in its walls. Its strong dorsal 
and ventral ciliation maintains in it a circulation of food materials and 
secretion, and its cells are capable of phagocytosis as well as secretory 
activity. Amphioxus thus combines intracellular with extracellular 
digestion, doubtless in connexion with its microphagous habit. 
Particles placed in the diverticulum are swept backwards and join the 
main food cord that passes through the mid-gut (Fig. 10). 

The hind end of the mid-gut is marked by a specially ciliated region, 
the ileo-colon ring, whose cilia rotate the cord of mucus and food. The 
movement is transmitted to the portion of the food cord in the mid- 
gut and presumably assists in the taking up of the enzymes that 
emerge from the diverticulum. Extracellular digestion takes place in 
the mid-gut and the enzymes responsible have been studied by Bar- 
rington. The pH of the contents varies from 67 to 7-1. An amylase is 
present in extracts of the diverticulum, mid-gut, and hind-gut, but 
not in those of the pharynx. Lipase and protease are present in the 


same regions, the latter having an optimum action at about pH 8-o, 
being, that is to say, a tryptic type of enzyme. There is no sign of 
any protease with an acid optimum, similar to the pepsin of higher 

Behind the ileo-colon ring the intestine runs as a straight hind-gut 
to the anus. Absorption of food takes place here, and perhaps also 
in the mid-gut, apparently partly by intracellular digestion, since 
ingested carmine particles are taken into the cells. 

The feeding current is regulated by the rate of beat of the cilia and 
the degree of contraction of the inhalent and exhalent apertures. The 
walls of the atrium contain an elaborate system of afferent and 
efferent nerve-fibres. The receptors include a set of large peripheral 
nerve-cell bodies, lying beneath the atrial epithelium and sending 
axons in by way of the dorsal roots. The motor fibres also pass through 
the dorsal roots and run without synapse to the cross-striated fibres 
of the pterygial muscle, which forms the floor of the atrium. The 
stream flowing into the pharynx is tested by the receptors of the velum 
and atrium, and if noxious material is present, the water is expelled by 
closing the atriopore and contracting the pterygial muscle, producing 
a 'cough'. The system can distinguish between suspensions of food 
material and inorganic particles. When sufficient food has been taken, 
collection is suspended until it has been digested (Bone, i960). 

The atrial nervous system probably regulates spawning as well as 
feeding. It has often been compared with the sympathetic system of 
craniates but there are almost no close similarities. The nerve cells in 
it are receptors and there is no sign of the peripheral synapse on 
the efferent pathway that is so characteristic of the true autonomic 
system. The atrial system is developed in relation to filter feeding 
and has perhaps been completely lost in higher forms that feed by 
other methods and have developed new methods to control them 
(p. 117). 

8. Circulation 

The blood-vessels of amphioxus show in diagrammatic form the 
fundamental plan on which the circulation of all chordates is based 
(Fig. 11). Slow waves of contraction occur in various separate parts 
in such a way as to drive the blood forwards in the ventral vessels, 
backwards in the dorsal ones. Below the hind end of the pharynx 
there is a large sac, the sinus venosus, into which blood from 
all parts of the body is collected. From this there proceeds for- 
wards a large endostylar artery (truncus arteriosus or ventral aorta) 



II. 8- 

ant. card- 

d. cuv. 


d ao: 

post, card' 

from which spring vessels carrying blood up the branchial arches. 
At the base of each primary bar there is a little bulb, functioning as 

a branchial heart. From the gill bars 
blood is collected into paired dorsal 
aortae, which join behind the pha- 
rynx. From the paired and median 
aortae blood is carried to the system 
of lacunae that supplies the tissues. 
There are no true capillaries. From 
the lacunae blood is collected into 
veins, the most important of which 
are the caudals, cardinals, and a 
plexus on the gut. The cardinals are 
a pair of vessels in the dorsal wall of 
the coelom, and they collect blood 
from the muscles and body wall. 
They lead to the sinus venosus by 
a pair of vessels, ductus Cuvieri, 
which pass ventrally and across the 
coelom to join the sinus venosus on 
the floor of the gut. The caudal 
veins join the plexus on the gut, 
from which blood is collected by 
a large subintestinal vein running 
on to the liver; from here another 
plexus leads to the sinus venosus. 

Contractions arise independently 
in the sinus venosus, branchial 
bulbs, subintestinal vein, and else- 
where. The rhythms are very slow 
(once in two minutes), irregular, 
and apparently not coordinated by 
any control system. 

The blood is colourless and is not 
known to contain any respiratory 
pigment. It contains no cells. Pre- 
sumably the tension of dissolved 
oxygen acquired by simple solution 
is sufficient for the small energy needs of the animal, w r hich spends 
most of its life at rest. It is by no means certain that any oxygenation 
of the blood takes place in the gills. Orton has suggested that since 




i i. Diagram of the circulation of 

aff.d. afferent vessel of diverticulum; ant. 
card, anterior cardinal vein; br.a. bran- 
chial arch; dorsal aorta; d.cuv. ductus 
Cuvieri; eff.d. efferent vessel of diver- 
ticulum; post. card, posterior cardinal 
vein; sin. sinus venosus; subint. subin- 
testinal vein; v. a. ventral aorta. (After 
Grobben and Zarnik.) 

II. Q 



these, through their cilia, do much of the work of the body, the 
blood actually leaves the gills less rich in oxygen that when it enters 
them. Oxygenation probably takes place chiefly in the lacunae close 
to the skin, perhaps especially those of the metapleural folds. 

9. Excretory system of amphioxus 

One of the most mysterious features about the organization of 
amphioxus is that there are flame-cells, comparable with those found 

Fig. 12. Solenocytes of amphioxus, showing the nuclei, long flagella, and the openings 
into the main excretory canal, which leads to the atrium. (After Goodrich.) 

in platyhelmia, molluscs, and annelids. The excretory organs, there- 
fore, do not conform to the basic chordate plan, and are in fact very 
different from those not only of all other chordates but also from any 
found in the remote invertebrate allies of the chordates which, as we 
shall presently see, include the echinoderms, brachiopods, and polyzoa. 
The nephridia lie above the pharynx. To each primary gill bar 
there corresponds a sac, opening by a pore to the atrium and studded 
with numerous elongated flame-cells (solenocytes) (Fig. 12). These 


flame-cells do not open internally, but are in close contact with special 
blood-vessels (glomeruli) whose walls separate the flame-cells from 
the coelomic epithelium. Assuming that there are 200 of these nephri- 
dia, each with 500 solenocytes 50 \x long, Goodrich, who has provided 
the most accurate information about these organs, shows that the total 
length available for excretion is no less than 5 metres. It is assumed 
that excretion takes place by diffusion through the flame-cell wall, the 
liquid being driven down the tube by cilia. Coloured particles injected 
into the blood-stream are not excreted by the nephridia. 

In development these remarkable organs arise from groups of cells 
close to the meeting-place of ectoderm and endoderm; almost cer- 
tainly they are derived from the former. They have no relation what- 
ever to the mesoderm and this fact alone sufficiently indicates that 
they are in no way comparable to the pronephros of vertebrates, as is 
sometimes stated. There is no organ in vertebrates with which they 
can be compared, nor is there any trace in amphioxus of organs com- 
parable to the vertebrate kidney system. In fact we have here a 
remarkable case of an isolated feature; evidently separate items of the 
genotype may vary independently, and the whole bodily organization 
does not necessarily change together. 

The brown funnels are blind sacs at the front of the atrium, 
invaginating into the epibranchial coelom. They are probably receptor 
organs. Some parts of the atrial wall may perform excretory functions. 
Masses of cells in the atrial floor, the atrial glands, contain granules 
that may be excretory but may have been taken up from the food 

In the gonads, especially the testes, there are large yellow masses, 
containing uric acid, which are extruded with the gametes. 

10. Nervous system 

Amphioxus possesses a hollow dorsal nerve-cord similar to that of 
vertebrates. Though this is somewhat modified at the front end, it is 
not there enlarged into an elaborate brain. The nervous system is con- 
nected with the periphery by a remarkably simple set of nerve-roots, 
a dorsal and a ventral on each side in each segment. The roots do not 
join (Fig. 13): the ventral roots lie opposite the myotomes, to which 
they carry motor-fibres, and these end on the muscle-fibres with 
motor end-plates. The dorsal root runs out between the myotomes 
and carries all the afferent fibres of the segment and motor-fibres for 
the non-myotomal muscles of the ventral part of the body. This is the 
fundamental pattern of the roots in all vertebrates. 





Fig. 13a. Nerve-cord of amphioxus. 
d.n. dorsal nerve-root; g. 'giant' nerve-fibres; v.n. ventral nerve-root. (After Retzius.) 




s.m c 

median giant fibre 

Fig. 13ft. Stereogram illustrating the structure of the spinal cord in an adult amphioxus. 

The receptor system is made up of a more or less continuous column of bipolar cells of 
Retzius (Ret.), together with smaller cells of various types (rec). According to Johnston 
these receptor cells (1,2 and 3) can be regarded as equivalent to the dorsal root ganglion 
cells of vertebrates. The other type of receptor cell is the giant Rohde cell (Roh.), which has 
a large axon and elaborate dendritic system. It is probable that at least some of these cells 
possess a peripheral axon running in the dorsal root. I.e. longitudinal connective cell. 

The visceral motor cells (v.m.c.) are arranged segmentally, one per segment. 

The somatic motor cells (s.m.c.) lie at a different level in the cord from the ventral 

Other cells in the cord are internuncials of various types. (After Bone.) 

The fibres of the peripheral nerves differ from those of vertebrates 
in that they have no thick myelin sheath that will blacken with 
osmium tetroxide. The nerve trunks are surrounded by an epineurium 
with connective tissue cells but there seem to be no Schwann cells 
accompanying the nerve-fibres (Bone, 1958). 



The afferent fibres of the dorsal roots are unique among chordates 
in that the cell bodies are not collected into spinal ganglia but mostly 
lie within the central nervous system. At least three types of central 
neuron send fibres that terminate as free nerve endings in the skin. In 
addition, on the head and tail there are peripheral receptor cells, 
sending fibres centrally, also complicated encapsulated organs in the 
metapleural folds (Bone, i960). There are numerous large multipolar 
nerve-cells, presumably afferent, just beneath the atrial epithelium. 

5 cut. 

bucc. ep 

Fig. 14. Sagittal section through the front end of amphioxus. 
bucc.ep. buccal epithelium; cer. cerebral vesicle, with large nerve-cells; ep. epidermis; 
my. myotome; n. notochord; p. pigment spot; s.cut. subcutis; vent, ventricle of cerebral vesicle. 

(After Krause.) 

These cells have many branched dendrites and an axon that runs 
through a dorsal root to the spinal cord. Their status is discussed on 


The spinal cord has only a narrow lumen and its elements are 

arranged as in vertebrates, namely, ependyma close to the canal, cell 
layer ('grey matter'), and outer fibrous layer ('white matter'). The cells 
are not arranged clearly in horns as they are in vertebrates. The most 
conspicuous cells are the giant cells, which lie dorsally in the anterior 
and posterior parts but are absent from about the 13th to 39th seg- 
ments. Each of these cells has many dendrites, branching in the region 
of entry of the dorsal root fibres, and a single axon, which runs back- 
wards in the front part of the body, forwards in the hind, passing in 
each case for the whole length of the cord. A median giant fibre, 
which runs ventrally for the length of the cord, lies close to the 
viscero-motor cells that probably produce the 'coughing' movements 
of the atrium (p. 33). 




Ten Cate has investigated the movements of amphioxus and found 
that it responds to all stimuli by movements of 'flight'. There are no 
isolated or local movements; the effect of any stimulus such as touch 
on the side of the body is to produce waves of myotomal contraction. 
These may, however, vary from strong waves going the whole length 




B o.c. t.po.h 

Fig. 15. Diagram of (a) the anterior end of the nervous 
system of amphioxus and (b) the brain of a fish 

A. Amphioxus. g.ep. granulated ependyma in the wall of the 'dorsal 
central canal'; i.o. infundibular organ; p.sp. pigment spot; r.f. 
Reissner's fibre in the central canal; s.ep. sensory epithelium, 
u. Polypterus, a.c. anterior commissure; aq.s. aqueductus Sylvii; cer. 
cerebellum; ep. epiphysis; m. medulla spinalis; n.h. neurohypophysis; nucleus praeopticus; o.c. optic chiasma; r.f. Reissner's fibre in 
fourth ventricle; s.c.o. subcommissural organ; s.d. saccus dorsalis; 
s.v. saccus vasculosus with primary sense cells; t.po.h. tractus praeop- 
tico-hypophyseus. (After Olson and Wingstrand.) 

of the body to single rapid twitches. The giant cells participate in the 
spread of these waves. It seems likely that the arrangement ensures 
that touch on the anterior part of the body, normally exposed when 
feeding, produces backward movement (i.e. withdrawal into the sand) 
but touch on the hind part the reverse movement of emergence and 

At the front end the central canal is enlarged to form a cerebral 
vesicle (Fig. 14). The whole neural tube is hardly wider here than in 
the region of the spinal cord and there is no thickening of the walls, 


which are indeed mostly formed of a single layer of ciliated epithelial 
cells (Fig. 15). This is a striking indication of the lack of cephalization 
of the animal. From the region of the cerebral vesicle spring the first 
two dorsal roots, to which there are no corresponding ventrals. These 
roots carry impulses from the receptors of the oral hood and its 

A B C 

Ifls jT^o*~r$5fc 

Fig. 16. Diagram to show the direction of the eye-spots of amphioxus. 
A, anterior, B, middle, and c, posterior regions of the body. The eyes are shown as if seen from 
behind. D shows the direction of spiralling of the animal when swimming — as seen from in front. 

(After Franz.) 

The infundibular organ (Fig. 15) is composed of tall cells with long 
cilia, which beat in the opposite direction to those of the rest of the 
vesicle. From them fibres run backwards down the cord. The organ 
is also the site of origin of Reissner's fibre (Fig. 15). This is a thread 
of non-cellular material, present in all vertebrates at the centre of the 
neural canal. It is secreted at the front end and then passed backwards 
and is often collected and absorbed in a sac at the hind end of the 
spinal cord. In vertebrates it arises from secretory ependymal cells of 
the subcommissural organ, lying dorsally in the diencephalon (Fig. 
1 5). The infundibular organ of amphioxus is clearly not exactly similar, 
yet the Reissner's fibres are clearly comparable ; an interesting problem 
in homology. 

A further complication is that the cells of the infundibular organ 
contain material that stains with the Gomori method, and is similar to 
the neurosecretory material found in the fibres of the hypophysial tract 
(Fig. 15). The organ thus seems to occupy a central position in the 
control system as a receptor, originator of nerve-fibres, and of two 
sorts of secretion. There is clearly much to be learned from this about 
the origin and significance of the control systems of the diencephalon. 

In young stages the cerebral vesicle opens by an anterior neuro- 
pore, and at the point where the closure takes place there develops a 
depression of the skin, lined by special epithelium, and known as 
Kolliker's pit. It is said to receive no special innervation. The cells 
at the front end of the cerebral vesicle contain pigment and there have 


been attempts to show that this represents an eye. More probably 
it serves to prevent rather than to receive photic stimulation; there 
are other cells lying in the spinal cord that are clearly photoreceptors 
(Fig. 9). In the front part of the body these are unprotected by pig- 
ment, whereas more posteriorly they are so pigmented as to be pro- 
tected asymmetrically from the light (Fig. 16). This asymmetry may 
be connected with the fact that when swimming free in the water 
amphioxus moves spirally about its axis, turning clockwise as seen 
from behind. It was established by Parker that a small beam of light 
produces movements of amphioxus only when it is directed on to the 
region of the body or tail, not when it shines on the head. Since the 
animal normally lies with the head protruding we may suppose that 
the pigment spot serves to prevent light that strikes down vertically 
from stimulating the photoreceptors in the cord. 

Amphioxus is therefore provided with receptor and motor systems 
that serve to keep it in its sedentary position, able to collect food from 
the current that it makes by the cilia (p. 33). There are mechanisms 
that help it to make appropriate movements of escape when it is 
touched or when the body (but not head) is illuminated. The touch 
receptors of the buccal cirri produce rejection of large particles and 
those of the velum are chemo-receptors. The infundibular organ may 
be some form of gravity or pressure receptor. By means of these 
receptor organs and its simple movements of swimming, burrowing, 
and closing the oral hood, the animal is maintained, probably mainly 
by trial and error (phobotactic) behaviour, in an environment suitable 
for its life. There are none of those elaborate mechanisms that we find 
in higher chordates for 'seeking' special environments or for so 
'handling' or managing them that they may prove habitable by the 
animal. Amphioxus must take and leave the world very much as it 
finds it. The 'correct' environment is chosen for it by the selective 
settling of the larvae. 

1 1 . Gonads and development of amphioxus 

The gonads of amphioxus are hollow segmental sacs with no com- 
mon duct. Each sac develops from mesoderm cells, perhaps originally 
from a single cell, at the base of the myotomes in the branchial region, 
the genital cells themselves developing on the walls (Fig. 6). The sexes 
are separate and the genital products are shed by dehiscence into the 
atrium, the aperture by which they escape closing and the gonad 
developing afresh. 

Extrusion of the gametes occurs in spring, on warm evenings 



following stormy weather. Fertilization is external and development 
then occurs free in the water. Numerous eggs are produced and they are 
small but yolky. Complex flowing movements take place in them after 
fertilization, and cleavage is then rapid and complete, producing a 
blastula composed of a dome of somewhat smaller and a floor of rather 
larger cells (Fig. 17). These latter then invaginate to make the archen- 
teron, opening by a wide blastopore, which later becomes the anus. 
At about this stage the gastrula becomes covered with flagella, by 
which it rotates within the egg case. 

Fig. 17. Three stages in the development of amphioxus as seen in stained 

a, the blastula; b, early, and C, later gastrula. 

The creature now elongates and its dorsal side flattens and eventu- 
ally sinks in to form the neural tube (Fig. 18 a). At about this time 
the dorsal side of the inner layer begins to fold near to the front end, 
in such a way as to make a pair of lateral pouches. The walls of these 
pouches are the future mesoderm and the cavity is the coelom. As in 
other early chordates, therefore, the coelom is continuous at first 
with the archenteron. The roof of the archenteron also arches up 
dorsally and forms the notochord, the gut wall being completed by the 
approximation of the edges of the remaining portion of the inner 
layer, which is now the definitive gut wall or endoderm. 

The analysis of the processes of development now enables us to say 
something of the forces by which these formative foldings and cell 
movements are produced. The formation of the neural tube, meso- 
derm and notochord and the completion of the gut roof all involve an 
upward movement of cells towards the mid-dorsal line. This process 
of 'convergence' is a very marked feature of the development of all 
chordates (Young, 1957, p. 609). 

As the animal elongates, further mesodermal pouches are produced, 
each separating completely from the endoderm and from its neigh- 




bours. The cells of each pouch push down ventrally on either side of 
the gut, the outer ones applying themselves to the body wall to form 
the somatopleure, the inner to the gut wall as splanchnopleure (Fig. 
1 8 d). The inner wall of the mesoderm on either side of the nerve- 
cord thickens to form the myotome, and a tongue of cells growing up 
between this and the nerve-cord forms the sheaths of the latter and 


my coel. 

A B C D 

Fig. i 8. Further stages in the development of amphioxus as seen in transverse 

A, stage of three somites; B, six somites; c, nine somites; D, eleven somites, arch, archenteron; 
coel. coelom; tries, mesoderm; my. myotome; my. coel. myocoele; n. notochord; n.c. nerve-cord; somatopleure; splanchnopleure; spl.coel. splanchnic coelom. (After Hatschek.) 


g. ioo u. 

Fig. 19. Young amphioxus, soon after hatching. 
g. gut; «. notochord; n.c. nerve-cord; nenr.c. neurenteric canal; neur.p. neuropore. 

probably also the fin-ray boxes and other 'mesenchymal' tissues. The 
upper part of the coelomic cavity, the myocoele, becomes separated 
from the ventral splanchnocoele. Whereas the former becomes almost 
completely obliterated, the latter expands to form the adult coelom, 
the cavities between the adjacent sacs breaking down. 

While this differentiation of the mesoderm has been proceeding the 
animal has elongated into a definitely fish-like form. The neural tube 
is a small dorsal canal, opening by an anterior neuropore and con- 
tinuous behind through a neurenteric canal with the gut (Fig. 19). 
The larva hatches when only two segments have been formed and 
swims at the sea surface by means of its ciliated epidermis, turning on 
its axis from right to left as it proceeds with the front end forwards. 

The mouth now appears as a circular opening and then moves 
over to the left side and becomes very large. From this time onward 
the whole development is markedly asymmetrical, presumably in 



ii. ii 

connexion with the spiral movement and method of feeding. The first 
gill-slit also forms near the midline but moves up on to the right side 
(Fig. 20). At about the same time the right side of the pharyngeal wall 
develops into a V-shaped thickening, the endostyle. Behind this there 
forms a tube, the club-shaped gland, joining the pharynx to the 
outside and formed by the closure of a groove in the side of the 
pharynx. The significance of this organ is still obscure ; it is presum- 
ably connected with the feeding process, which begins at this stage. 
It has been thought to represent a gill-slit. 

Fig. 20. Larval amphioxus before metamorphosis. 

an. anus; c.s.g. club-shaped gland; end. endostyle; g. gill-slits lying on right 

side, which will later move over to the left. H.p. Hatschek's pit (left first 

coelomic sac); m. lower edge of mouth, lying on left side; n. notochord; 

p. pigment spot. 

The first two coelomic pouches differentiate, asymmetrically, at 
this time. That on the right becomes the coelomic cavity of the head 
region, while the left one acquires an opening to the exterior and a 
heavily ciliated surface. This is perhaps also connected with the feed- 
ing-systems and becomes developed into Hatschek's pit of the adult. 
Its interest to the morphologist lies in the fact that the first coelomic 
cavity opens to the exterior in other early chordates and in some 
vertebrates (p. 206). The pit has thus some claim to be considered the 
equivalent of the hypophyseal portion of the pituitary gland. 

Further gill-slits develop in the mid-ventral line and move over on 
to the right side until fourteen have been so formed. Meanwhile, a 
further row of eight slits appears above that already formed. These are 
the definitive slits of the right side and presently the larva proceeds to 
become symmetrical by movement of eight of the first row of slits 
over to the left side, the remainder disappearing. At this 'critical 


stage' with eight pairs of slits the larva pauses for some time before 
further changes. It is interesting that this is the time at which it most 
nearly represents what might have been an ancestral craniate, with 
eight branchial arches (p. 145). Further slits are then gradually added 
in pairs on both sides. Each slit becomes subdivided, soon after its 
formation, by the downgrowth of a tongue bar. The atrium is absent 
from the early larva. Metapleural folds then appear on either side and 
are united from behind forwards to form a tube below the pharynx. 
During the later stages of development the larva sinks and finally rests 
on the bottom while undergoing the migration of gill-slits that con- 
stitutes its metamorphosis. In other species the larva remains longer 
in the plankton, becoming large and even showing quite large gonad 
rudiments. These were at first thought to be adults of a new genus 

The development of amphioxus, like its adult organization, shows 
us many features of the plan that is typical of all chordates and was 
presumably present in the earliest of them. Thus the cleavage, in- 
vagination, and mesoderm formation recall those of echinoderms and 
other forms similar to the ancestors of the chordates, and also show a 
pattern from which all later chordate development can be derived. 
Unfortunately we cannot pursue this study as far as we should like 
because of the difficulty of investigating the development of am- 
phioxus. Modern embryologists aim at tracing the morphogenetic 
movements by which the organism is built, and ultimately at dis- 
covering the forces responsible for these processes. We still remain 
ignorant of the details of these morphogenetic movements, and can 
only guess that the system of cell activities by which an amphioxus 
is built represents quite closely the original set of morphogenetic 
processes of vertebrates (Young, 1957, p. 633). 

There are, of course, some special features connected with the 
method of life of the larva, and especially with its asymmetry. The 
strange sequence of gill formation, the immense left-sided larval 
mouth, perhaps the club-shaped gland, and Miiller's organ, may show 
considerable modifications of relatively recent date. However, the 
earliest chordates probably fed by means of cilia and were planktonic, 
so we must not too hastily assume that even these asymmetrical features 
are novelties. 

The division of the mesoderm of amphioxus into a series of sacs 
presents an interesting problem. The segmentation of the mesoderm 
of vertebrates is restricted to the dorsal region. In the lowest chord- 
ates (see p. 51), as in their pre-chordate ancestors, there are three 


coelomic cavities, but it is probable that the many segments of verte- 
brates arose in order to provide a set of muscles able to contract in a 
serial manner for the purpose of swimming. Their segmentation would 
thus be a relatively late development, not related to the segmentation 
of annelids, which divides the whole body into rings. Accordingly the 
ventral part of the vertebrate coelom usually remains unsegmented. 
But in amphioxus (and in the lamprey) it is subdivided from its first 
appearance and only becomes continuous later. The best interpreta- 
tion of this condition is to suppose that in order to provide a series of 
myotomes a rhythmic process subdividing the mesoderm was adopted. 
In its earliest stages this affected the whole mesoderm, ventral as well 
as dorsal, but later became restricted to the dorsal region. New 
morphogenetic processes may often pass through stages of refinement 
and simplification in such ways. 

12. Amphioxus as a generalized chordate 

Amphioxus provides us, then, with a valuable example of a chordate 
that retains the habit of ciliary feeding, which was probably that of the 
earliest ancestors of our phylum. No doubt in connexion with this, 
and the bottom-living habit, there are many specializations; the 
enormously developed pharynx with its atrium, the asymmetry, and 
so on; but the general arrangement of the body is almost diagram- 
matically simple, and it may well be that amphioxus shows us a stage 
very like that through which the ancestors of the craniates evolved. 
Perhaps next the larva remained longer in the plankton and became 
mature there. The Amphioxides larvae show signs of such a change. 

This might give rise to a suspicion that amphioxus is not an 
ancestral type but a simplified derivative of the vertebrates, perhaps 
a paedomorphic form. It possesses, however, sufficient peculiar 
features to make this view unlikely. Neoteny might explain the 
regular segmentation, separate dorsal and ventral roots, and other 
features, but can hardly account for the method of obtaining food, 
for the condition of the skin, or for the presence of nephridia. It may 
be, therefore, that amphioxus shows us approximately the condition 
of the early fish-like chordates, living in the Silurian some 400 million 
years ago, and that it has undergone relatively little change in all the 
time since. 



1 . Invertebrate relatives of the chordates 

We have seen in the organization of amphioxus the plan of chordate 
structure as it may have existed in Palaeozoic times. Before proceeding 
to discuss the later forms that evolved from animals of this sort we may 
first look yet farther backwards to discuss the origin of the whole 
chordate phylum from still earlier ancestors. The great difficulty of 
such an inquiry is itself a stimulus and a challenge. Typical fish-like 
chordates were undoubtedly established by the Ordovician period, 
but we have no good fossil record of their earliest form and this must 
therefore be deduced from study of amphioxus and later animals. No 
fossils that suggest chordate affinities have been found in the still 
earlier rocks. There are, however, certain strange animals alive today 
which, though not of fish-like type, show undoubted relationship with 
our group. These might, of course, be degenerate offshoots from later 
periods, but careful comparison suggests that they have been separa- 
ted for a very long time and provide us with relics of some of the early 
stages of our history. 

The first step in our inquiry, however, before discussing these 
forms, should be to find out, if possible, which of the main lines of 
invertebrate animals shows the closest affinity with the chordates. 
Almost every phylum in the animal kingdom has been suggested, 
including the nemertines. Many still suppose that the annelids and 
arthropods, because of their metameric segmentation, are related to 
the chordates, but closer examination shows that the similarities are 
superficial. The segmentation of these annulate animals is an almost 
complete division of the whole body into rings, and all the organ 
systems are affected by it to some extent. In chordates only the dorsal 
myotomal region is segmented; even the mesoderm is not divided in 
its ventral region in most animals. Moreover, the whole orientation 
of the body differs in the two groups. The vertebrate nerve-cord is 
dorsal to the gut, in annulates the nerve-cord is below and the 'brain' 
above. The blood circulates in opposite directions, the limbs are 
based on quite different plans, and so on. Attempts have been made 
to get over these difficulties by turning the invertebrate upside down! 
Patten and Gaskell carried such theories to extremes and tried to 


show a relationship of chordates with the eurypterids, heavily ar- 
moured arachnids of the Cambrian and Silurian. These animals show 
a certain superficial resemblance to some early fossil fishes, the cepha- 
laspids of the Devonian (Fig. 83), and these workers, with great 
ingenuity, claimed to find in them evidence of the presence of many 
chordate organs. 

The safest evidence of affinity is a similarity of developmental pro- 
cesses : animals that develop very differently are unlikely to be closely 
related. The development of modern annulates is utterly different 
from that of chordates. The cleavage by which the fertilized egg is 
divided into blastomeres follows in annulates a 'spiral' plan, in which 
every blastomere arises in a regular way and the future fate of each 
can be exactly stated. In later annulates, such as the arthropods, this 
plan is complicated by the presence of much yolk, but even in these 
animals the cleavage does not resemble that of chordates, which is 
radial or 'irregular', the cells not forming any special pattern. This 
characteristic has been used to divide the whole animal kingdom into 
two major groups, Spiralia and Irregularia. 

The next stage of development, gastrulation, by which the ball of 
cells is converted into a two-layered creature, also occurs very differ- 
ently in the two groups. Our knowledge of the mechanics of the pro- 
cesses by which this change is produced is still imperfect, in spite of 
recent advances, but in lower chordates it occurs by invagination, the 
folding in of one side of the ball of cells to form an archenteric cavity 
communicating with the exterior. In annulates this is never seen; 
the cells that will go to form the gut migrate inwards either at one 
pole or all round the sphere and only later form themselves into a 
tube, which comes to open secondarily to the outside. It is probable 
that when we know more of the forces by which the gastrulation is 
produced the difference will appear even more marked than it does 
from this crude and formal statement that gastrulation in chordates is 
by invagination, in annulates by immigration. 

The same applies to the method by which the mesoderm and coelom 
are formed. In lower chordates the third layer is produced by separa- 
tion from the endoderm, so that the coelom is continuous with the 
archenteron and is said to be an enterocoele. In annulates cells 
separate in various ways to form the mesoderm and a coelom then 
arises within this solid mass as a schizocoele. It is true that in some, 
indeed many, of the higher chordates the coelom is never continuous 
with the archenteron, but its method of development shows it to be 
a modified enterocoele. 


In all these points of development the chordates differ from the 
annulates, but resemble the echinoderms and their allies. Further 
features support this latter relationship. One of the most important 
of these is that the echinoderm-like animals, and some of the early 
chordates, have a larva with longitudinal ciliated bands, very different 
from the trochophore larva, in which the bands run transversely 
round the body, which is found in the other line of animals. The 
nervous system of annulates consists of a set of ganglionated cords, 
whereas in echinoderm-like animals it is a diffuse sheet of cells and 
fibres below the epidermis. The nerve-cord of the chordates can be 
derived from the latter but not easily from the former condition. 
Many further points could be cited, for instance, the presence of a 
mesodermal skeleton in both chordates and echinoderms, but not in 
annulates. It may be that there are also fundamental biochemical 
differences. Most of the spirally cleaving types of animal conduct their 
energy transfers with arginine phosphate, whereas vertebrates, 
amphioxus, ascidians, and ophiuroid echinoderms use creatine phos- 
phate. Balanoglossus and echinoids have both. 

In the study of evolution it is not sufficient merely to make formal 
comparisons, we must try to find out and compare the plan of develop- 
ment and structure common to all members of two groups, a technique 
often requiring great knowledge and good sense. When this is done in 
the present case it will be found that the essential plan of development 
of annulates involves spiral cleavage, gastrulation by immigration, 
and a coelom formed as a schizocoele, a trochophore-like larva, and 
full segmentation of the mesoderm. It is exceedingly unlikely that 
such animals have given rise to chordates with their very different 
development, which we may crudely define as showing radial cleavage, 
gastrulation by invagination, and larva of echinoderm type. 

Extending this method we may divide the whole world of Metazoa 
by similar criteria into Spiralia or Polymera and Irregularia or Oligo- 
mera. The former include besides the annulates the molluscs and 
platyhelmia, whereas the latter group contains, in addition to the 
chordates, the echinoderms, brachiopods, polyzoa (ectoprocta), grap- 
tolites, pogonophora, and Phoronis. The animals in this latter group 
seem at first sight to be very different from the chordates in outward 
form, but the farther we look into their fundamental organization, the 
more we become convinced that the ancestors of the fish-like animals 
are to be found here. By study of the relics of the early chordates it is 
possible to trace the history of this strange change with some plausi- 
bility, though its full details will probably never be known. 



III. 2 

2. Subphylum Hemichordata (= Stomochordata) 

Class i. Enteropneusta 

Balanoglossus ; Glossobalanus ; Ptychodera; Saccoglossus 
Class 2. Pterobranchia 

Cephalodiscus ; Rhabdopleura 

Fig. 21. Balanoglossus, removed from its tube and seen from the dorsal side. 
abd. abdomen; atr. atrium; an. anus; c. collar; h.c. hepatic caeca; p. proboscis; ph. pharynx. 

(From van der Horst.) 

Fig. 22. Balanoglossus in its tube in the sand. (After Stiasny.) 

In the Hemichordata are placed animals of two types, the worm- 
like Balanoglossus and its allies (Enteropneusta) and two sedentary 
animals, Cephalodiscus and Rhabdopleura (Pterobranchia). The Entero- 
pneusta are mostly burrowing animals (Figs. 21 and 22) varying in 
different species from 2 cm to over 2 metres long. Several genera are 
recognized (e.g. Balanoglossus, Saccoglossus, Ptychodera) and they 
occur in all seas. Saccoglossus occurs around the British coast. The 
body is soft, without rigid skeletal structures, and divided into 
proboscis, collar, and trunk. The animals are very fragile and it is 
difficult to collect specimens in which the hind part of the trunk 

III. 2 



('abdomen') is intact. The proboscis, collar, and trunk each contain 
a coelomic cavity, and the coeloms of the proboscis and collar are 
distensible by intake of water through a single proboscis pore and 
paired collar pores. The skin is richly ciliated all over the body. The 
outer epithelium is thus unlike the squamous, layered skin of higher 
forms (Fig. 23). It contains numerous gland-cells, whose secretion 
is very copious, so that the animals are always covered with slime. 


Fig. 23. Section of the epidermis of an enteropneust. 
h.m. basement membrane; ep. epidermal cell; gl. I and 2, different types of gland cell; 
neur. neuron; neur.s. neuro-sensory cell; n.g.p. process of epidermal cell acting as neuro- 
glia in the nerve net. (After Bullock, v. der Horst and Grasse.) 

A characteristic feature is an unpleasant smell, resembling that of 
iodoform, which possibly serves, like the mucus, as a protection. 

Below the skin is a nerve plexus receiving the inner processes of 
receptor cells and containing ganglion cells (Fig. 23). Deep to this are 
muscles running in various directions. It is said that the animal moves 
by first pushing the proboscis and collar forward through the sand 
and then drawing the body after it. Protrusion of the proboscis can- 
not, however, be very vigorous. It may perhaps be produced by ciliary 
action distending the coelom as is usually stated — more probably by 
circular muscles, but these are weak. Numerous longitudinal muscles 
are present, however, in the proboscis and trunk and are partly 
attached to a plate of skeletal tissue in the collar. This tissue is 
attached to the ventral side of a forwardly directed diverticulum of 
the pharynx. The wall of this is thick, composed of vacuolated cells, 
and bears a certain resemblance to a notochord (Fig. 24). A notochord 
extending throughout the length of the body would clearly be dis- 
advantageous for an animal whose main movements are lengthening 



and shortening. It is possible that the diverticulum and plate found 
in the collar represent the remains of a notochord, serving as a 
fixed point by which the body is drawn forward on to the proboscis. 
However, many prefer to call it a 'stomochord' to avoid too close a 


Fig. 24. Diagrammatic section of front end of Balanoglossus. 
c. collar coelom ; card.s. sac around heart ; div. pharyngeal diverticulum ('stomochord') ; dn 
dorsal nerve-root ; dv. dorsal vessel ; gl. glomerulus ; £s. gill-slit ; Im. longitudinal muscles of 
proboscis ; n.c. nerve-cord ; p.p. proboscis pore ; sk. skeletal plate. (Modified after Spengel.) 

comparison with the notochord. The external cilia probably play a 
considerable part in locomotion; possibly they are the chief burrowing 
organs, the muscles serving mainly to perform escape movements. 

The mouth lies in a groove between the proboscis and collar (Fig. 
25). The proboscis contains many mucus-secreting cells and the food 
particles are captured on its surface and conveyed by ciliary currents 
to the mouth. In the anterior part of the trunk there is a wide pharynx, 
opening by a series of gill-slits (Figs. 24, 26). These resemble the 
gills of amphioxus in the presence of a supporting skeleton in the gill 
bars; there are also tongue bars dividing the slits from above, and 

III. 2 



Fig. 25. Feeding-currents on proboscis of Glossobalanus, shown by placing the animal 

in water containing carmine particles. The particles (gra.) are either taken directly into 

the mouth (?«.) as at w., or are caught up in strands of mucus (sec.) and passed backwards. 

(From Barrington, Quart. J. Micr. Set. 82, by permission.) 

Fig. 26. Transverse section of the pharynx of Glossobalanus. 

cil. cilia of the gill bars; dc. dorsal chamber of pharynx; es. epibranchial strip; gp. gill pore; 
VC. ventral chamber of pharynx. (From Barrington. With permission as for Fig. 25.) 

horizontal synapticulae strengthening the gill arches. The slits open 
in some species into an atrium formed by lateral folds, usually turned 
upwards to leave a long mid-dorsal opening. In some species each 
slit opens to a gill pouch. The whole branchial apparatus perhaps 



III. 2 

assists in the process of feeding, probably by serving to filter off the 
excess water from the material already collected on the proboscis, 
which often consists of large amounts of sand or mud. Relative to the 
size of the animal the pharynx is less extensive than in amphioxus, 
presumably because ciliary surfaces are provided on the outside and 
also large masses of sand are forced into the mouth during locomotion. 
There is no endostylar apparatus, but the ventral part of the pharynx 
is often partly separated from the rest (Fig. 26). Along this groove the 
matter ingested is passed to a straight oesophagus and intestine open- 
ing by a terminal anus. There is no true tail in the adult but a post- 
anal region is present in some species during development. Numerous 

v'.v. ph. 

Fig. 27. Diagram of the blood system of Balanoglossus. 

col. collar; d.v. dorsal vessel; glom. glomerulus; hp. hepatic caeca; m. mouth; not. 'notochord'; 
p. proboscis; ph. pharynx; v.v. ventral vessel. (After Bronn.) 

hepatic caeca in the anterior part of the intestine can be seen from the 
outside as folds of the body wall, often highly coloured. 

The blood system consists of a complex set of haemocoelic spaces, 
communicating with large dorsal and ventral vessels (Fig. 27). 
The former enlarges into a sinus anteriorly and this is partly sur- 
rounded by the wall of a pericardial cavity, which contains muscles 
and may be said to be the heart, though clearly lying in a very different 
position from that of other chordates. From the sinus, vessels proceed 
to the proboscis and round the pharynx to the ventral vessel. The 
blood is said to move forwards in the dorsal and backwards in the 
ventral vessels. The front of the sinus forms a series of glomeruli, 
covered by a region of the proboscis coelom specialized to form 
excretory cells, the nephrocytes, some of which drop off into the 
coelom. The blood is red in some species but usually colourless. It 
contains a few amoebocytes. 

The nervous system is one of the most interesting features of 
Enteropneusta. It resembles that of echinoderms in consisting of a 
sheet of nerve-fibres and cells lying beneath the epidermis all over the 
body (Fig. 23). This sheet is thick in the mid-dorsal and mid-ventral 



lines, and in the dorsal part of the collar region it is rolled up as a 
hollow neural tube, open at both ends (Fig. 24). These unmistakable 
resemblances not only to the uncentralized sub-epithelial plexus of 
echinoderms but also to the hollow dorsal nerve-cord of vertebrates 
are most instructive, showing the affinity of the groups and the origin 
of the general plan of the vertebrate nervous system. There are no 
organs of special sense, unless this is 
the function of a patch of special cili- 
ated cells on the collar. Receptor cells 
all over the body send their processes 
into the nerve plexus (Fig. 23), on the 
primitive plan of neurosensory cells 
found elsewhere in vertebrates only in 
the olfactory epithelium and the retina. 
The plexus is remarkable in receiving 
fibres from the outer ciliated epithelial 
cells, which thus represent the epen- 
dyma, the earliest form of neuroglia 
(Fig. 23). Nothing is known of the 
organization of pathways or of the 
connexions with the muscles. The 
collar nerve-cord contains giant nerve- 
cells whose axons proceed backwards 
to the trunk and forward to the pro- 
boscis (Fig. 28). They are probably 
responsible for rapid contractions 
(Knight-Jones, 1951). 

Bullock has investigated the beha- 
viour of the animals and found only 

one clear-cut reflex, namely, a contraction of the longitudinal muscles 
in response to tactile stimulation. Isolated pieces of the body are able 
to show reflex responses, moving away from light or tactile stimuli. 
Such local actions are an interesting sign of the uncentralized nature 
of the nervous system, and similar actions are found in echinoderms. 
A further sign of lack of special conducting pathways is that stimula- 
tion of flaps of body wall partly severed from the rest produces 
generalized contraction, proving that conduction can occur in all 
directions. The dorsal and ventral nerve-cords do, however, act as 
quick conduction pathways, and contraction of the trunk following 
stimulation of the proboscis is delayed or absent if one, and especially 
if both, cords have been cut. 

Fig. 28. Diagram of certain tracts in 
the nervous system of Balanoglossus . 

com. circular connective; col.coel. collar 
coelom; col.n.c. collar nerve-cord; 
nerve plexus in epidermis of trunk; gp. 
gill pore; tr. coel. trunk coelom; tr.n.c. 
trunk nerve-cord. (From Bullock, J. 
Comp. Neurol., vol. 80, by permission.) 


Perhaps the most interesting behaviour observed was the activity 
shown by an isolated proboscis, collar, trunk, or portion of trunk. 
These organs may move around vigorously in an exploratory manner; 
evidently the main nerve-cords are not necessary for the initiation of 
action, as is the central nervous system of higher chordates. 

There are nerve-fibres in the walls of the pharynx and oesophagus, 
where peristaltic movements have been observed. Their relationship 


Fig. 29. Young tornaria larva, seen from the side. 

an. anus; ap. apical organ; cb. longitudinal ciliated band; m. mouth; 

pb. posterior ciliated band; pp. proboscis pore. (After Stiasny.) 

to the rest of the nervous system is unknown. They may represent 
the beginnings of an autonomic nervous system. 

The sexes are separate in enteropneusts and the gonads resemble 
those of amphioxus in being a series of sacs developing from cells just 
outside the coelom. These proliferate and bulge into the coelom, 
covered by the somatopleure. They acquire a cavity and each opens 
by a narrow duct to the exterior, fertilization being external. The 
development is remarkably like that of echinoderms. Cleavage is holo- 
blastic and resembles that of amphioxus and ascidians, gastrulation is 
by invagination, and the coelom is formed as an enterocoele, later 
becoming subdivided into proboscis, collar, and trunk coeloms. Hatch- 
ing occurs to produce a pelagic tornaria larva, with a ciliated band that 
has exactly the relations found in the dipleurula larva of echinoderms. 
The band passes in front of the mouth, down the sides of the body, 
and in front of the anus (Fig. 29). It then divides into more dorsal 

III. 2 



and ventral sections, exactly as in the production of the bipinnaria 

larva of a starfish. This arrangement differs essentially from the rings 

of cilia that pass round the body in the trochophore larva found in the 

annelids and other spirally cleaving forms. In later tornaria larvae 

there is, however, in addition to the longitudinal bands always a 

posterior ring of stout cilia (telotroch), and in large oceanic forms 

(which may reach 8 mm in length) the longitudinal band itself is 

prolonged into prominent tentacle-like loops (Fig. 30). The cilia of 

the posterior ring are purely locomotive, while those of the band set 

up feeding-currents converging to the 

mouth. As the larva becomes larger the 

ciliary surface needed for locomotion 

and feeding has to increase relatively 

faster than the increasing mass of the 

body, the latter following the cube but 

the former only the square of the linear 

dimensions. Accordingly the cilia of 

the locomotive ring become broadened 

and flame-like, while the convolutions 

of the longitudinal (feeding) band reach 

fantastic proportions. In some types, 

however (Saccoglossus), the pelagic 

phase is brief and the telotroch alone 

is formed. 

Finally the larva sinks, becomes con- 
stricted into three parts, and undergoes metamorphosis into the worm- 
like adult. This development is so like that of an echinoderm that it 
would be necessary to consider the enteropneusts to be related to 
that group even if no other clues existed. Such close similarity in 
the fundamentals of development cannot be due to chance. 

These animals thus provide a very remarkable and sure demonstra- 
tion that the chordates are related to the echinoderms and similar 
groups. The general arrangement of the nervous system as a sub- 
epithelial plexus, as well as the whole course of the development, show 
the affinity with the invertebrate groups, whereas the hollow dorsal 
nerve-cord and the tongue-barred gill-slits are by themselves sufficient 
to show affinity with the chordates, this affinity being also perhaps 
suggested by other features, such as the 'notochord'. As we have seen 
already, affinities are not to be determined by single 'characters' but 
by the general pattern of organization of animals and especiallv that of 
their development. The organization of the enteropneusts is certainly 


30. Older tornaria larva seen 
from ventral surface. 

Letters as Fig. 29; coel. proboscis 
coelom. (After Stiasny.) 


highly specialized for their burrowing life, but showing through the 
special features we can clearly see a plan that has similarity with both 
the echinoderms and the chordates. The special value of study of these 
animals is that it proves decisively that an affinity between these 
groups exists. Exactly how they are all related is a more speculative 
matter, which we shall deal with later (see p. 74). 

3. Class Pterobranchia 

These are small, colonial, marine, sedentary animals, which show 
some signs of the general echinoderm-chordate plan of organization 
we have been discussing. Cephalodiscus (Fig. 31) has been found on the 
sea bottom at various depths, mainly in the southern hemisphere: 
there are several species. The colony consists of a number of zooids 
held together in a many-chambered gelatinous house. The zooids are 
formed by a process of budding, but do not maintain continuity with 
each other. Each zooid has a proboscis, collar, and trunk; there are 
coeloms in each of these parts, and proboscis and collar pores. The 
collar is prolonged into a number of ciliated arms, the lophophore, by 
means of which the animal feeds. There is a large pharynx, opening 
by a single pair of gill-slits, which serve as an outlet for the water 
drawn in by the cilia of the tentacles for the purpose of bringing food. 
The intestine is turned upon itself, so that the anus opens near the 
mouth. A thickening in the roof of the pharynx corresponds exactly in 
position with the stomochord and contains vacuolated cells. The blood 
system consists of a series of spaces arranged on a plan similar to that 
in Balanoglossus. There is a dorsal ganglion in the collar, but this is 
not hollow. The gonads are simple sacs and development takes place 
in the spaces of the gelatinous house. Gastrulation is by invagination 
at least in some species and the coelom is formed as an enterocoele. 
The larva somewhat resembles that of ectoproctous polyzoa, which 
is not closely similar to the echinoderm larvae, but could be derived 
from the same plan. 

Rhabdopleura occurs in various parts of the world, including the 
North Atlantic and northern part of the North Sea. The zooids are 
connected together and have proboscis, collar, and trunk, ciliated 
arms, coelomic spaces with pores (not 'nephridia' as is sometimes 
stated) and stomochord, but no gill-slit. The development is not 

The Pterobranchia thus show undoubted signs of the enteropneust- 
chordate plan of organization and provide also an interesting sug- 
gestion of possible affinities with Polyzoa, Brachiopoda, and Phoronis. 


Like the Pterobranchia the Polyzoa Ectoprocta are sessile, with mouth 
and anus pointing upwards. They feed by means of the cilia borne on 
a horseshoe-ring of tentacles (the lophophore); but there is no division 

Fig. 31. Longitudinal median section of Cephalodiscus. 

a. anus; b.c. 1, 2, and 3 body cavities; int. intestine; lo. lophophore; 

m. mouth; nch. 'notochord'; n.s. nervous system; oes. oesophagus; 

op. operculum (collar); ov. ovary; ph. pharynx; pp. proboscis pore; 

ps. proboscis; St. stomach; st.k. stalk. 

(Modified after Harmer, Cambridge Natural History, Macmillan.) 

into proboscis, collar, and trunk, and no tripartite coelom. The nervous 
system is in the condition of a sub-epithelial plexus, which is folded, 
around the base of the lophophore, to form a hollow tube — a remark- 
able point of similarity to the chordates. Even though it is difficult to 
compare this tube exactly with the nerve-cord of chordates, it is at 
least evidence of the organization of the nervous system on a plan that 
allows of such folding. It is probable that the modern pterobranchs 
are the surviving members of the ancient group of graptolites, but 



in. 3- 



these are known only from the skeleton. The Pogonophora may also 
be distantly related, their larva can be regarded as of tornaria type, 
the coelom develops as in enteropneusts and the larval body shows 
three parts, as does that of the adult in some species. 

Although it would be unwise to 
suggest close relationship between the 
polyzoans and the pterobranchs, the 
similarities are sufficient to suggest that 
the chordates arose from sedentary 
creatures, feeding by means of ciliated 
tentacles. The evidence is sufficiently 
strong to encourage us to look for the 
presence somewhere in the line of verte- 
brate ancestry of an animal with this 
habit. The difficulties of this view arise 
when we come to consider how the fish- 
like organization of a free-swimming 
animal first appeared, a question better 
dealt with after consideration of the 

4. Subphylum Tunicata. Sea squirts 

In the adult ascidians or sea squirts 
there is no obvious trace of the fish-like 
form at all. The majority of these 
animals are sac-like creatures living on 
the sea floor and obtaining their food 
by ciliary action. Often the separate 
individuals are grouped together to form 
large colonies, but in Ciona intestinalis, 
common in British waters, the indi- 
viduals occur separately, and this is possibly the primitive con- 
dition for the group. The whole of the outside of the body is covered 
by a tunic, in which there are only two openings, a terminal mouth and 
a more or less dorsal atriopore, both carried upon siphons (Fig. 32). 
The tunic is made mainly of a carbohydrate, tunicin, closely related to 
cellulose, with which is combined about 20 per cent, of glycoprotein. 
It is secreted by the epidermis but contains special cells that have 
arrived there by migration from the mesoderm. In some tunicates 
calcareous secretions of various shapes are found in the tunic. The 
mantle that lines the tunic is covered by a single-layered epidermis. 

Fig. 32. Diagram of structure of 

atr.p. atriopore ; e. endostyle ; gen.d. 
genital duct; h. heart; int. intestine; 
m. mouth; mu. muscle; oes. oeso- 
phagus; ph. pharynx; st. stomach. 
(After Berrill.) 

in. 4 



Ascidians are often brightly coloured, the pigment being either in the 
tunic or the underlying body, which shows through the transparent 
tunic. The colour can change, at least over a period of some days. Little 
is known about the origin of the pigment, but it is sometimes derived 
from the blood-pigment and may lie in pigment cells. 

The mantle is provided with muscle-fibres running in various 
directions but mainly longitudinally, and serving to draw the animal 
together, with the production of 
the jet of water from which the 
animals derive their common 
English name. 

The greater part of the body is 
made up of an immense pharynx, 
beginning below the mouth and 
forming a sac reaching nearly to 
the base (Fig. 32). The sac is 
attached to the mantle along one 
side (ventral) and is surrounded 
dorsally and laterally by a cavity — 
the atrium. This pharynx is, of 
course, the food-collecting appa- 
ratus ; its walls are pierced by rows 
of stigmata (gill-slits) whose cilia 
set up a food current entering at 
the mouth and leaving from the 
atriopore. The entrance to the 
pharynx is guarded by a ring of 
tentacles, which may be compared 

with the velum of amphioxus. The stigmata are very numerous 
vertical cracks, all formed by sub-division of three original gill- 
slits. Tongue bars grow down to divide each slit and then from each 
tongue bar grow horizontal synapticulae. This arrangement has clear 
resemblance to that of amphioxus and results in the production 
of a pharyngeal wall pierced by numerous holes. Immediately within 
the stigmata there is a series of papillae, provided with muscles and 
cilia. There is an endostyle, which has three rows of mucus cells 
on each side, separated by rows of ciliated cells and with a single 
median set of cells with very long cilia (Fig. 33). The mucus secreted 
in the endostyle is caught up on the papillae, whose muscles move 
them rhythmically, spreading a curtain of mucus over the inside of 
the pharynx. Food particles are caught in the mucus, which moves 

Fig. 33. Transverse section of the endo- 
style of Ciona. 

lat. cil. lateral cilia; med. cil. long median cilia; 
mu. mucous cell. (After Sokoloska.) 


upwards and is then passed back to the oesophagus by the cilia of a 
dorsal lamina or of a series of hook-like 'languets'. Autoradiographs 
made from tunicates that have been provided with isotopes of iodine 
show that iodination occurs in certain cells lying above the glandular 
tracts of the endostyle. Iodine is also abundant in the tunic, as it is in 
the exoskeletal structures of molluscs and insects. When it became 
of metabolic value its production may have become concentrated in 
the pharynx (see p. 118). 

The extensive ciliated surface of the pharyngeal wall ensures the 
passage of large volumes of water inwards at the mouth and out at the 
atriopore. Rapid change of the water is also produced by periodic 
muscular contractions (p. 65). The pressure of the exhalant current is 
sufficient to drive the water that has been used well away from the 

The oesophagus leads to a large 'stomach' with a folded wall con- 
taining gland-cells, which produce digestive enzymes. These include 
much amylase, invertase, small amounts of lipase, and a protease of 
the tryptic type. The organ is therefore not to be compared with the 
stomach of vertebrates. A branching 'pyloric gland' opens into the 
lower end of the stomach. From the stomach a rather short intestine 
leads upwards to open inside the atriopore; this is apparently the 
absorptive region of the gut. 

The heart lies below the pharynx and is a sac, surrounded by a 
pericardium (see p. 63) and communicating with a system of blood 
spaces derived from the blastocoele. The larger of these spaces have 
an endothelial lining; the biggest is a hypobranchial vessel below the 
endostyle, from which branches pass to the pharynx. From the oppo- 
site end of the heart springs a large visceral vessel and others pass to 
the dorsal side of the pharynx, tunic, body wall, &c. The heart is 
peculiar in that the beat can proceed in either direction. After passing 
blood into the hypobranchial vessel and gills for a few beats, its direc- 
tion reverses, passing the blood to the viscera. This reversal is pro- 
duced by the presence of two pacemaker centres, each capable of 
initiating rhythmical contractions, one at either end of the heart. 
Stimulation of these by warming and cooling allows control of the 
reversal of the beat. There are no capillaries and the blood system is 
a haemocoele. The blood-plasma is colourless but contains corpuscles, 
some of which are phagocytes, while others contain orange, green, or 
blue pigment (in different species). The green and other pigments are 
remarkable in that they contain vanadium. In some ascidians (Molgula) 
some individuals contain vanadium, others niobium (Carlisle, 1958). 

III. 4 



The vanadocytes contain much sulphuric acid and the metal is 
associated with a chain of pyrrol rings. This haemovanadin is able to 
reduce cytochrome but it remains uncertain what part the pigment 
plays in respiration. The blood turns blue in air but cannot take up 
more oxygen than can sea water. 

The blood is isotonic with sea water, and ascidians appear to have 
little or no power of regulating their osmotic pressure; none of them 
is found in fresh water. They are not even able to colonize brackish 
waters or those of low salinity. For example, they are rare in the 
Baltic Sea, from which only six 
species have been reported. Only 
one species, Molgula tubifera, has 
been reported from the Zuider 
Zee (salinity 8-4 per mille). 

A possible reason for this in- 
ability to regulate the internal 
composition is perhaps the need 
to expose a large surface to the 
water. There are no tubular ex- 
cretory organs such as could be 
used to maintain an osmotic 
gradient. Ninety-five per cent of 
the nitrogen is excreted as am- 
monia. Cells known as nephro- 
cytes found in the blood and 
elsewhere contain concretions 
within the cytoplasm and these 
may in some cases be stored in an excretory sac until the animal dies. 

There has been much debate as to whether the tunicates possess 
a coelomic cavity. The heart develops from a plate of cells arising 
early from the mesoderm and lying between ectoderm and endoderm. 
This becomes grooved and folded to make the heart itself and the 
pericardium. The irregular system of haemocoelomic spaces around 
the pharynx and elsewhere is usually said to consist of 'mesenchyme' 
and to be derived from the blastocoel and therefore not coelomic, but 
its walls are mesodermal. The situation is complicated by the presence 
of a pair of outpushings from the pharynx, the epicardia, or perivis- 
ceral sacs, which end blindly on either side of the heart (Fig. 34). 
Berrill and others have suggested that these epicardia may be com- 
pared with coelomic cavities. Their function in the open condition 
in which they are found in Ciona is perhaps to allow sea water to 

Fig. 34. Section through base of Ciona, 

showing heart, fit., in pericardium, p., 

and the epicardia, e.p., opening into the 

pharynx, b.s. 

at. atrium; g. gonad; int. intestine. 


circulate about the heart and hence to help excretion (and respiration ?). 
In other ascidians the epicardium loses its connexion with the pharynx. 
The closed sac functions in some cases as an excretory organ, con- 
taining concretions of uric acid, whereas in other animals it becomes 
the main source of the cells that make the asexual buds. 

The central nervous system consists of a round, solid ganglion 
(Fig. 36), lying above the front end of the pharynx. The ganglion has 
a layer of cells around the outside and a central mass of neuropil and 
is therefore quite unlike the nerve-cord of a vertebrate. From the 
ganglion nerves proceed to the siphons, other parts of the mantle, 
muscles, and viscera. Receptor cells with nerve-fibres ending around 
the base have been described, especially in the siphons. The gut is 
said to contain a plexus of cells and fibres, whose relation to the 
autonomic system of higher forms remains uncertain. 

Movement consists mainly of contraction and closure of the aper- 
tures. Light touching of either siphon causes closure proportional to 
the strength of the stimulus. Stronger stimuli cause closure of both 
siphons and if very strong there is contraction of the whole body and 
ejection of the water in the pharynx and atrium. Stimulation just 
inside either siphon produces closure of the other one and also, if 
strong enough, contraction of the body, ensuring that a jet of water 
sweeps out the aperture that received the stimulus. These crossed 
reflexes depend upon the integrity of the ganglion. 

The surface of the body is sensitive to changes in light intensity, 
and these are followed by local or total contractions, according to their 
extent. After removal of the ganglion the wider reflexes can no longer 
be obtained but local responses continue, suggesting the presence of 
nerve-cells in the body wall. Electrical stimulation also provides evi- 
dence of this. One shock may produce only a small response but if a 
second shock follows shortly afterwards there is marked facilitation 
and a large contraction occurs. These responses are also seen after 
removal of the ganglion. The various parts of the body are not all 
equally sensitive to light, the highest sensitivity being in the region 
of the ganglion. The 'ocelli' are cup-like collections of orange- 
pigmented cells around the siphons ; according to Hecht they are not 

The neuromuscular system thus appears to function mainly as a 
reflex apparatus for producing protective movements in response to 
certain stimuli. This is the role that might be expected of it in an 
animal that remains fixed in one place. The 'initiative' for food- 
gathering activities comes from the continuous action of the cilia of 


the pharynx. The nervous system shows little sign of those continuous 
activities that produce the varied and 'spontaneous' acts of behaviour 
in higher forms. Nevertheless, it would be unwise to suppose that the 
nerves are only activated by external stimuli. There are some sugges- 
tions that even in these simple animals rhythmical activities are 
initiated from within. The food-collecting operations of the pharyn- 
geal wall involve rhythmical movement of the papillae by their 
muscles. Further, in many species of ascidians there are regular 
contractions of the siphons and body musculature in rotation, with 

Fig. 35. Rhythmical 'spontaneous' contractions of Styela shown by attaching levers 

to the two siphons. Branchial siphon above, atrial siphon below. The time-marker 

shows intervals of 5 minutes. (From Yamaguchi.) 

a frequency of 8-27 per hour (Fig. 35). These contractions are 
especially marked when the animal is in filtered water and they may 
be some form of 'hunger' contraction, directed towards the obtaining 
of food. More water is moved by these contractions than by the ciliary 
current. Their presence is a striking warning of the dangers of assum- 
ing that even the simplest nervous system operates only when 
stimulated from outside. 

The neural gland is a sac lying beneath the ganglion and opening 
by a ciliated funnel on the roof of the pharynx. It arises mainly from 
the ectoderm of the larval nervous system, in part from the pharynx. 
This double embryological origin, and its position, suggest that the 
neural gland may be compared with the infundibulum and hypophysis 
of vertebrates. There is an obvious similarity with Hatschek's pit of 
amphioxus. Both seem to be receptor organs, testing the water stream 
and also producing mucus. The subneural gland has also been held 
to have a similarity to the pituitary in that it controls the release of 
gametes. When eggs or sperms of the same species are present in the 
water, signals from the neural gland apparently produce discharge 
from the gonad. The pathway of the signals is said to be partly hor- 
monal, partly nervous. Discharge is produced by injection of extract of 



in. 4-5 

neural gland or of mammalian gonadotropin, but these act through the 
ganglion, since they produce no effect if the nerves leading from this 
(and the dorsal strand) are cut. 

Further similarities with the pituitary have been claimed, such as 
the presence of vasopressor and oxytocic substances in the subneural 
gland. However, oxytocin is present elsewhere in the tunicate and in 

Fig. 36. Longitudinal section of the ganglion (g.) and subneural gland 
(s.n.g.) of an ascidian. 

cil. ciliated funnel; d.s. dorsal strand; n.a. and n.p. anterior and posterior nerves; 
ph. wall of pharynx. (After L. Bertin from Grasse.) 

any case differs from that of vertebrates. It cannot be claimed that the 
relationship with the pituitary is clear, but it seems likely that there 
is some. As in the thyroid, a pharyngeal mucus-secreting organ 
stimulated by the environment has evolved into a glycoprotein- 
secreting endocrine organ, controlled by substances reaching it in the 
blood. (Barrington, 1959, in Gorbman, Symposium on Comparative 

5. Development of ascidians 

Tunicates are hermaphrodite, the ovary and testis being sacs lying 
close to the intestine and opening by ducts near the atriopore. Fer- 
tilization is external in the solitary forms but internal in those that 
form colonies, the development in the latter taking place within the 
parent. The details of cleavage and gastrulation show a remarkable 
general similarity to those of amphioxus. Indeed, the whole develop- 
ment is so strikingly like that of chordates that it establishes the 
affinities of the tunicates far more clearly than the vague indications 



Fig. 37. Ascidian tadpole of Clavelina. 

air. atriopore; c. mantle; cer.v. cerebral vesicle; e. eye-spot; end. endostyle; ep. epicardium; 
h. heart; m. mouth; mu. muscle-cells; n.c. nerve-cord; not. notochord; ot. otocyst; St. stomach; 

sub.n. subneural gland. 

r. C. b. 

Fig. 37 A. T.S. ocellus of the free swimming tadpole stage of the sea squirt Ascidia nigra. 
(Drawing from an electron micrograph.) 

The ocellus is situated in the posterior wall of the cerebral vesicle. It consists of three parts, a lens 
cell, a pigment cell, and a retina. The lens cell usually contains three lens vesicles, which are spheres 
of cytoplasm bounded by mitochondria. The pigment cell contains granules of melanin, which 
protect the photoreceptor from stray light. The retinal cells have processes that penetrate the 
pigment cell. They are similar to vertebral rods, composed of a pile of membranes, closely applied 

to the uaner edge of the lens cell. 
a. p. attachment plaque, a membrane specialization thought to function as an anchor of the retinal 
cell process to the pigment cell membrane ; b.m. basement membrane, the outer limit of the cerebral 
vesicle; c.v. cavity of the cerebral vesicle; I.e. lens cell; l.v. lens vesicle; m. mitochondrion; p.c. 
pigment cell; p.g. pigment granule; p.m. piled menbrane of photoreceptor part of the retinal cell; 
r.c.b. retinal cell body; r.c.n. retinal cell nucleus; r.c.p. retinal cell process. 
(From a preparation by N. Dilly.) 


of a chordate plan of organization seen in the adult. The result of 
development is to produce a fish-like creature, the ascidian tadpole, 
which is immediately recognizable as a chordate (Fig. 37). The 
cleavage is total and produces a blastula with few cells, whose future 



mus. c. 

Fig. 38. The ascidian tadpole (Ascidia or Ciona type). 1. Tadpole ready to hatch. 
2. Tadpole. 3. Sensory vesicle. 4. Cross section of tail. 

atr. atrium; end. endostyle; fol. follicle cells; mus.c. muscle cells; mus.f. muscle fibrils; 

n.c. nerve-cord; n.m. nerve to tail muscles; not. notochord; oc. ocellus; ot. otolith; su. sticking 

gland; ves. sensory vesicle. (After Berrill.) 

potentialities are already determined. Gastrulation by invagination 
follows and the creature then proceeds to elongate into the fish-like 
larva. This possesses an oval 'head' and long tail, the latter supported 
by a notochord formed by cells derived from the archenteric wall. 
Forty of these cells make up the entire rod, becoming vacuolated and 
elongated by swelling. 

On either side of this notochord run three rows of muscle-cells, 
eighteen on each side, derived from mesoderm that arises from yellow- 
pigmented material already visible in the egg and later forming part 
of the wall of the archenteron. Other cells of this tissue migrate 
ventrally to make the pericardium, heart, and mesenchyme. The 


muscle-cells contain cross-striated myo-fibrils at the periphery, these 
being continuous from cell to cell. 

The nervous system is formed by folds essentially similar to those 
of vertebrates, making a hollow, dorsal tube, extending into the tail 
and enlarged in front into a cerebral vesicle, within which is an 
ocellus and also a unicellular otolith (Fig. 37 a). Nerve-fibres proceed 
only to the front end of the rows of muscles and the rest of the cord 
contains no nerve-cells or fibres (Fig. 38). 

The larva takes no food and the gut is not well developed. There is 
a pharynx with usually a single pair of gill-slits opening into an 
atrium, which develops as an ectodermal inpushing. Below or around 
the mouth various forms of sucker are formed. 

The whole process of development occupies only one or two days, 
and the larva, in the species in which it is set free, is positively photo- 
tropic and negatively geotropic and so proceeds to the sea surface. 
But its life here is also limited. Within a day or two, depending on the 
conditions, its tropisms reverse so that it passes to the bottom, turns 
to any dark place and thus finds a suitable surface. It attaches by the 
suckers, loses its tail, develops a large pharynx, and grows into an adult 
ascidian. Presumably its short life in the chordate stage is sufficient 
to ensure distribution, and the simple nervous system serves to find 
a place in which to live. 

In addition to the sexual reproduction, tunicates have great powers 
of regeneration and also often multiply by budding. The bud consists 
of an outer epicardial, mesenchymal, pharyngeal or atrial tissue. The 
epidermis develops only more tissue like itself and all the other tissues 
are formed from the inner mass. This occurs by a process of folding 
to make a central cavity; the nervous system, intestine, and peri- 
cardium are then formed by further foldings. The bud thus begins in 
a condition comparable to a gastrula but develops directly into an 
adult, without passing through the tadpole stages. The fact that a 
complete new animal is thus formed from one or two layers shows 
that the separation into three layers during development does not 
involve any fundamental loss of potentialities, as would be required 
if the 'germ layer' theory held rigorously. The germinal tissue of the 
bud is not necessarily derived from that of the parent. 

6. Various forms of tunicate 

Besides some 2,000 species of sessile tunicates, about 100 species 
have become secondarily modified for a pelagic life. These pelagic 


animals are perhaps all related, but the whole subphylum is con- 
veniently subdivided into three classes. 
Class i. Ascidiacea. 

Typical bottom-living forms such as Ciona (solitary), Botryllus 
Class 2. Thaliacea. 

Pelagic forms, simple or colonial, swimming by means of circular 
muscle bands. Salpa, Doliolum, Pyrosoma. 
Class 3. Larvacea. 

Pelagic tunicata without metamorphosis; the adult has a tail and 
resembles the tadpole of the other groups. Oikopleura. 

7. Class Ascidiacea 

The typical sessile ascidians are found in all seas. They may be 
divided into those that live as single individuals (Ascidiae simplices) 
and those forming colonies (Ascidiae compositae). Both types include 
many different forms, however, and the division is not along phylo- 
genetic lines. The colonial forms produced by budding may consist 
simply of a number of neighbouring individuals {Clavelina) or of a 
common gelatinous test in which the individuals are embedded 
{Botryllus, Amaroucium). The form of the body is related to the type 
of bottom upon which they are found; there has thus been an adap- 
tive radiation within the group; a great variety of habitats is avail- 
able for bottom living creatures, and the animals become adapted 

Most of the species live in the littoral zone, but a few deep-sea forms 
are known, such as Hypobythius calycodes, found below 5,000 metres. 

Many ascidians probably live only for a short time, becoming 
mature in their first year and dying thereafter. In some species the 
animals live over a second winter, during which they become reduced 
in size, growing and budding again in the following spring (Clavelina). 

8. Class Thaliacea 

These are pelagic tunicates living in warm water. They have 
circular bands of muscle, enabling the animal to shoot through the 
water by jet propulsion. In Doliolum and its allies the muscle-bands 
pass right round the body (Cyclomyaria), whereas in Salpa the rings 
are incomplete (Hemimyaria). The mouth and atriopore are at 
opposite ends of the body. The tunic is thin and, like the rest of the 
body, transparent. 

The life-history of these forms involves a remarkable alternation of 



Fig. 39. Doliolum, gonozooid. 

I, inhalent aperture; 2, ciliated pit; 3, ganglion and nerves; 4, pharynx; 5, mantle; 

6, sense-cells, 7, exhalant aperture; 8, ovary; 9, intestine; 10, heart; 11, endostyle; 

12, testis; 13, ciliated groove. (After Neumann.) 






Fig. 40. Cyclosalpa affinis, oozooid with chain of five wheels of blastozooids. 
an. anus; atr. atrium; at.s. atrial siphon; hi. blastozooid with egg; br.s. branchial siphon; en. endo- 
style; gn. ganglion; gr. gill ridge; ht. heart; muse, muscle ring; ph. pharynx; s. stomach. 
( X £ modified. After Ritter and Johnson and Berrill.) 

generations. In Doliolum the ascidian tadpole develops into a mother 
or nurse zooid (oozooid). This by budding gives rise to a string of 
daughter zooids, which it propels along by its muscles. The daughter 
zooids are of three types: (i) sterile, nutritive, and respiratory indi- 
viduals, the trophozooids, permanently sessile on the parent; (2) 
sterile nurse forms, which are eventually set free (phorozooids); (3) 
sexual forms (gonozooids, Fig. 39), nursed and carried by the phoro- 
zooids until sexually mature, when they also break loose. 

In Salpa the sexual form (blastozooid), produces only a single egg, 


which develops within the mother without passing through a tadpole 
stage, nourished by a diffusion placenta, whose cells also migrate into 
the developing embryo. This becomes the asexual oozoid and pro- 
duces a long chain of blastozooids, which it tows about until these 
break away by sections (Fig. 40). 

The pelagic colonial Pyrosoma of warm seas consists of a number of 
individuals associated to form an elongated barrel-shaped colony. 
The mouths open outwards and the atria inwards into a single 
cavity with a terminal outlet from which a continuous jet emerges. 

The mode of budding from the epicardium 
and other features suggest an affinity with 
Doliolum and Salpa, but Pyrosoma also 
resembles the ascidians in that its zooids 
are all sexual and capable of budding. The 
yolky eggs develop within the parent, 
without forming a larva. The outstanding 
characteristic of the creatures is the 
powerful light that they shine. This is 
Fig. 41. Photogenic cell of produced in photogenic organs on each 

Pyrosoma. (After Kukenthal.) r . r mi 1 

side or the pharynx. 1 he photogenic cells 
contain curved inclusions about 2^ in diameter (Fig. 41). These 
are considered by some to be symbiotic luminescent bacteria, but 
this is doubtful. The light is so powerful that when large masses of 
Pyrosoma occur together the whole sea is illuminated sufficiently to 
allow of reading a book. A remarkable feature of the phenomenon 
is that the light is not produced continuously but only when the animal 
is stimulated, as by the waves of a rough sea. If one individual is 
stimulated others throughout the colony may show their lights, but 
the mechanism of this effect is not known and the groups of cells that 
form the luminescent organs receive no nerves. Other types of animal 
with luminescent bacteria emit light continuously. The sudden flashes 
of light probably serve as a dymantic reaction (p. 302), giving protec- 
tion against enemies by producing a flight-reaction in the same way 
as do sudden manifestations of colour or black spots by other animals. 
It has been observed in the laboratory that colonies of Pyrosoma that 
are dying and do not light up may be eaten by fishes, whereas any 
that light up when seized may then be dropped. 

9. Class Larvacea 

The (Appendicularia) Larvacea (Figs. 42 and 43) are minute neo- 
tenous tunicates that live in the plankton. Instead of the test, each 

ill. 9 



Fig. 42. Oikopleura, one of the Larvacea, in its house, showing 

the feeding-currents. 

e. exhalant aperture; e.e. 'emergency exit'; f. p. filter pipes; filter 

window; g. gill-slit; m. mouth; r. trough; ta. tail. (After Garstang; 

this and Figs. 44 and 45 by permission of the Editors of the Quarterly 

Journal of Microscopical Science.) 

individual builds a 'house', by secretion from a special part of the skin, 
the 'oikoplastic epithelium'. The tail is a broad structure held at an 
angle to the rest of the body; its 
movement produces a current in 
which the food is carried and caught 
by a most elaborate filter arrangement 
ixi the house (Fig. 42). Water enters 
the house by a pair of posterior 
'filtering windows' and is passed 
through a system of filter pipes in the 
part of the house in front of the 
mouth. The very minute flagellates 
of the nanonplankton are stopped by 
these pipes and sucked back to the 
mouth. The pharynx has two gill-slits, 
also an endostyle and peripharyngeal 
bands. The general organization is that 
of a typical ascidian tadpole, and there 
can be no doubt that these forms have 
arisen from tunicates by the accelera- 
tion of the rate of development of the 
alimentary organs and gonads so that 
the metamorphosis and normal adult 
stage are eliminated. This may, of 
course, have happened long ago, so 
that the modern Larvacea are not FlG - «■ Appendicular* t seen from 

the side and from below. 

closely related to any living forms, (After Lehmann.) 


but the fact that they differ in many ways from known ascidian 
tadpoles does not invalidate the hypothesis; it would be expected 
that many special features would be developed during evolution 
after the paedomorphosis. Garstang, however, believed that there 
is sufficient evidence to show that the Larvacea are related to the 
Doliolidae and suggested an ingenious hypothesis by which the appendi- 
cularian home could be derived from the doliolid test, the animal 
itself remaining attached at the front end by gelatinous threads, which 
came to make the filter tubes (Fig. 44). 

Fig. 44. Sequence of stages by which the Larvacea may have 
been evolved from a doliolid type. 

A, Thaliaccan type of individual in its test (t). b, Paedomorphosis has 
occurred so that a tailed creature is found in the test; g. gill-slit, c, The 
tadpole has moved away from the inhalant aperture, leaving a series 
of threads that become the filter pipes (/./>.), the inhalant aperture 
becoming exhalant and vice versa. (After Garstang.) 

The tail is a highly developed organ, serving for locomotion, nutri- 
tion, and in the building of the house. It has a wide, continuous fin 
and is supported by a notochord of 20 cells. Bands of 10 large striped 
muscle-cells extend down each side, giving an appearance that has 
been compared with metameric segmentation. The small number of 
the cells makes any such comparison very difficult. Moreover, the 
muscles are not developed from anything resembling myotomes. The 
nerve-cord is a hollow tube with ganglionic thickenings, each con- 
taining one to four nerve-cells. From these cells fibres proceed to 
the muscles and to the skin in a series of roots that usually remain 
separate, the motor being more dorsal. 

10. The formation of the chordates 

We can now recapitulate the points that we have established about 
the origin of the chordates and attempt to piece together the evidence 
to show the sequence of events that led to the production of a free- 


swimming, fish-like animal. The chordates are related to the echino- 
derms and their allies. This is established by the similarities in early 
development (cleavage, gastrulation, mesoderm formation); by the 
presence in early members of both groups of three separate coelomic 
cavities, some with pores; by the similarity of the larva of entero- 
pneusts to the dipleurula, and by other points of general morphological 
and biochemical similarity between early chordates and echinoderms, 
especially the arrangement of the nervous system and presence of a 
mesodermal skeleton. 

The echinoderms we have to consider are not the modern star- 
fishes and sea-urchins, which are relatively active animals, but their 
sessile Palaeozoic ancestors. These were sedentary, often stalked 
animals, the cystoids, blastoids, and crinoids, feeding by ciliary 
action. Surviving animals of related phyla, such as Polyzoa Ecto- 
procta and Phoronis suggest that the ancestor for which we are looking 
may have possessed a ciliated lophophore for food-collecting. For 
purposes of dispersal its life-history presumably included a larval 
stage with a longitudinal ciliated band, similar in plan to that of the 

One might well ask how such an animal could possibly become 
converted into a motile, metameric fish, feeding with its pharynx. 
Yet the evidence of the lower chordates is sufficient to establish that 
this change has occurred, and even provides us with an outline of the 
main stages in the process of the change. Cephalodiscas, which is in 
some ways the most primitive of surviving chordates, with its lopho- 
phore also possesses gill-slits. This suggests that the pharyngeal 
mechanism was substituted for the lophophore as a means of feeding 
in the adult stage. There are other possible interpretations. It has 
been suggested that Cephalodiscus was derived from a larval entero- 
pneust (Burden-Jones). However, it is possible that ciliary mechanisms 
developed in the pharynx first to deal with food collected outside by 
tentacles or proboscis. Later the pharynx became developed into a 
self-contained feeding mechanism, making unnecessary the tentacles, 
which provide a tempting morsel for predators. The adoral band of 
cilia of the auricularia probably serves to carry food into the mouth, 
and for this purpose it is actually turned in to the floor of the pharynx. 
Garstang suggests that the endostyle has been derived from this loop 
of the adoral band. 

The pharyngeal method of food-collecting thus replaced the ten- 
tacles in the adult and the whole apparatus of an endostyle and an 
atrium to protect the gills became developed. We may notice here the 

7 6 


III. 10 

remarkable similarity of this arrangement of the pharynx in tunicates, 
amphioxus, and cyclostome larvae, and the partial similarity in 

The tunicates show us a stage in which branchial feeding has fully 
replaced tentacle feeding in a sessile adult. But they have a larva that 
is beyond all question a fish-like chordate. If the adult tunicate has 
evolved from a modified lophophore-feeding creature, how has the 

Fig. 45. To show the method by which a protochordate animal might have been 

derived from an echinoderm larva such as the auricularia. 

a. Auricularia in side view; b. protochordate in side view; c. same, dorsal view. ad.b. adoral 

band; an. anus; coel. coelom; end. endostyle; g. gill-slit; Lb. longitudinal ciliated band; 

m. mouth; n.c. nerve-cord; not. notochord. (After Garstang.) 

ascidian tadpole arisen from the auricularia larva ? Garstang's auri- 
cularia theory, first propounded in 1894, provides a possible answer. 
As a ciliated larva grows its means of locomotion becomes inadequate 
because the ciliated surface increases only as the square of the linear 
dimensions, the weight as the cube. Muscular locomotion is not sub- 
ject to this difficulty, and some of the starfish larvae actually show 
flapping of the elongated processes, movements that presumably 
assist them to remain at the surface. Garstang suggests that the fish- 
like form arose by development of muscles along the sides of the 
elongated body, the ciliated bands being pushed upwards and even- 
tually rolled up with their underlying sheets of nerve plexus to form 
the neural tube. The adoral ciliated band might then well be the 
endostyle (Fig. 45). 

This theory may seem at first sight fantastic. It is necessarily 
speculative, but it has certain strong marks of inherent probability. It 


violates no established morphological principles and certainly enables 
us to see how a ciliated auricularia-like larva could be converted by 
progressive stages into a fish-like creature with muscular locomotion, 
while the adults, at first sedentary, substituted gill-slits and endostyle 
for the original lophophore. The alternative is to suppose that the 
ascidian tadpole arose as a purely tunicate development, providing 
sufficient receptor and muscular organs to allow for the finding of 
suitable sites on the bottom (Berrill, 1955). 

We may plausibly regard the adult tunicate organization as directly 
derived from that of sessile lophophore-feeding creatures, and the 
larval organization as descended from an echinoderm-like larva. 
There is no need, on this view, to regard the sessile adult tunicate 
as a 'degenerate' chordate. The problem that remains is in fact not 
'How have sea-squirts been formed from vertebrates ?' but 'How have 
vertebrates eliminated the sea-squirt stage from their life-history?' 
It is wholly reasonable to consider that this has been accomplished by 
paedomorphosis. Advance of the time of development of the gonads 
relative to that of the soma is well known to occur in certain special 
cases such as the axolotl. The example of the Appendicularia shows 
that a similar process can happen among tunicates! Various workers 
have stressed the differences between the ascidian tadpole and the 
adult appendicularian, in attempts to show that the two are not 
comparable. But the differences, though considerable, are superficial : 
the similarity of organization is profound. Any sensible biologist with 
an understanding of the way in which the characteristic forms of 
animals arise by change in the rate and degree of development of 
features can see how the Appendicularia may represent modified 
ascidian larvae. 

The appendicularians do, indeed, carry certain characters of the 
'adult' sea-squirt, in particular they have gill-slits, though of simple 
form. Nothing is more likely, however, than that some features of the 
sessile adult would be adumbrated in its larva and capable of fuller 
development therein if advantageous. Larva and adult, it must be 
remembered, possess the same genotype; the remarkable feature in all 
animals with metamorphosis is the difference between the two stages, 
not the similarity. Any characteristic may appear at either larval or 
adult stage or be transferred by evolutionary selection from one to the 
other. There is no serious objection to the view that the early adult 
free-swimming chordates arose by paedomorphosis of some tunicate- 
like metamorphosing form. If the creatures abandoned the habit 
of fixation it would be possible for characters previously present 


separately in larva and adult to become combined in a single stage. 
This is indeed what has happened in the Appendicularia. 

Strangely enough, one of the chief difficulties of this theory is to 
find the position of the enteropneusts. Since the larva is still in the 
ciliated-band stage there should be no sign of organs characteristic of 
the muscle-swimming, fish-like pro-chordate. Yet such signs are 
present in the adult Balanoglossiis; there is a hollow nerve-cord and 
some sign of a notochord. These features almost compel us to suppose 
that the group has at one time possessed a free-swimming, fish-like 
stage. The only escape from this conclusion would be by supposing 
the hollow nerve-tube to be a case of convergence, for which a parallel 
might be cited in the hollow nervous system of Polyzoa. But there is 
no clear reason why the nerve-cord should become rolled up in the 
collar, and it is easier to suppose it a vestige. This imposes two further 
hypotheses on us. First that a fish-like stage once followed an advanced 
ciliated-band stage in ontogeny, and secondly that this fish-like stage 
later became adapted to a burrowing life, in fact that Balanoglossus is 
a 'degenerate' chordate. Neither of these propositions is impossible, 
but it must be admitted that the position of the enteropneusts is not 
clear. Showing a combination of ciliated larva and chordate characters 
they provide a valuable proof of the affinity of chordates and echino- 
derm-like creatures, but these very chordate characters become an 
embarrassment when we try to explain in detail how they have arisen! 

There is strong reason to suppose that what we may call the Bate- 
son-Garstang theory of the origin of chordates is correct. There is little 
doubt that chordates are related to the sessile lophophore-feeding 
type of creature rather than to any annulate, and we can reconstruct 
the course of events by which the lophophore-feeder may have come 
to have a pharynx with gill-slits and its larva to have muscles, a noto- 
chord, and a nerve-tube. Then by paedomorphosis the sessile stage 
disappeared and the free chordates began their course of evolution. 
There are some reasons for supposing that a type such as amphioxus 
could have been derived from a creature not distantly related to the 
simpler Appendicularia and this in turn from a neotenous doliolid or 
some similar ancestral type. 

We need not, however, follow the theory into its details, which are 
speculative. The whole treatment provides a conspicuous example 
of close morphological reasoning, allied with proper consideration of 
general biological principles, and establishes with some probability 
the main outlines of the origin of our great phylum of active creatures 
from such humble sedentary beginnings. 


Can we see in the production of the first fish-like creatures clear 
signs of an 'advance' in evolution ? In acquiring the power of active 
muscular locomotion the animals became able to live and feed in a 
variety of habitats, either at the sea surface or on the bottom. Forms 
with a sedentary adult stage are limited by the necessity for the 
presence of a sea bottom of suitable character. The larvae were evolved 
to provide the information to make sure of reaching such conditions. 
But whereas suitable situations on the bottom are not common, and 
are liable to change, the sea surface provides a generalized habitat in 
which there is always abundant food, though no doubt also strenuous 
competition for it. Paedomorphosis in this case, as in others, allows 
the race to eliminate from its life-history the stage passed in a 'special' 
environment, which is difficult to find. Although the fish-form that 
was thus produced proved to have great possibilities for further 
evolution, the change was not at first a strikingly progressive one. 
The surface of the sea is perhaps the most general of all environments ; 
possibly it was the seat of the origin of life. Races that have devised 
means of living on the sea bottom may therefore be said to have 
advanced, because they have invaded a more difficult habitat. To 
abandon the sedentary life might in this sense be regarded as a retro- 
grade step. The peculiar feature of the early fishes, however, was that 
they developed powers of active movement in a relatively large 
organism provided with efficient receptors, and by making use of the 
feeding mechanism developed at first by the bottom-living adult were 
able to live successfully at the sea surface. They acquired their 
dominance at this stage not by invading new habitats but by develop- 
ing effective means of living in the richly populated plankton. 



1. Classification 

Phylum Chordata 

Subphylum 4. Vertebrata (= Craniata) 
Superclass 1. Agnatha 
Class 1. Cyclostomata 
Order 1. Petromyzontia 

Petromyzon; Lampetra; Entosphenus; Geotria; Mordacia 
Order 2. Myxinoidea 
Myxine; Bdellostoma 

Class 2. *Osteostraci. Silurian-Devonian 
*Cephalaspis; * Tremataspis 

Class 3. *Anaspida. Silurian-Devonian 
*Birkenia; *Ja?noytius 

Class 4. *Heterostraci. Ordovician-Devonian 
*Astraspis; *Pteraspis; *Drepanaspis 

Class 5. *Coelolepida. Silurian-Devonian. 
*Thelodus; *Lanarkia 

Superclass 2. Gnathostomata 

2. General features of vertebrates 

All the remaining chordates are alike in possessing some form of 
cranium and some trace of vertebrae; they make up the great sub- 
phylum Vertebrata, also called Craniata. The organization of a verte- 
brate is similar to that of amphioxus, but with the addition of certain 
special features. A few of these novelties may now be surveyed, with 
emphasis on those that provide the basis for the capacity to live in 
difficult environments that is so characteristic of the vertebrates. 
Firstly the front end of the nervous system is differentiated into an 
elaborate brain, associated with special receptors, the nose, eye, 
and ear. Through these receptors the vertebrates are able to respond 
to more varied aspects of the environment than are any other animals. 
Some of them have the ability to discriminate between visual shapes 
and colours, and in the auditory field between patterns of tones, also 
between a host of chemical substances. The motor organization 
allows the performance of delicate movements to suit the situations 


that the receptors reveal. The swimming process, by the passage 
of waves down the body, is itself perfected by improvements in the 
shape of the fish, allowing rapid movements and turns. Besides the 
median fins there develop lateral paired ones, serving at first a 
stabilizing and steering function and then converted, when the land 
animals arose, into organs of locomotion on the ground or in the air 
and finally, in the shape of the hands, into a means of altering the 
environment to suit the individual. 

The brain itself, at first mostly devoted to the details of sensory 
and motor function, comes increasingly to preside, as it were, over 
all the bodily functions, and to give to the vertebrates the 'drive' that 
is one of their most characteristic features. The skull is developed as 
a skeletal thickening around the brain, probably at first mainly for 
protection, but later serving for the attachment of elaborate muscle 
systems. The study of vertebrates is especially identified with study 
of the skull, because in so many fossils this is the only organ preserved. 

The food of the earliest vertebrates was collected by ciliary action, 
but this habit has long been abandoned and only in rare cases today 
does the food consist of minute organisms. The pharynx of most 
vertebrates is small, there are relatively few gill-slits and these are 
respiratory. In all except the most ancient forms the more anterior of 
the arches between the gills became modified to form jaws, serving not 
only to seize and hold the food but also to 'manipulate' the environ- 

The blood system shows two of the most characteristic vertebrate 
features, namely, the presence of a heart that has at least three 
chambers and thus provides a rapid circulation, and of haemoglobin 
within corpuscles, serving to carry large amounts of oxygen to the 
tissues. The efficiency of this system must have been a major factor 
in producing the dominance of the vertebrate animals. In the air- 
breathing forms, and especially the warm-blooded birds and mam- 
mals, the respiratory and circulatory systems allow the expenditure of 
great amounts of energy per unit mass of animal, so that quite extra- 
vagant devices can be used, allowing survival under conditions that 
would otherwise not support life. 

The excretory system is based on a plan quite different from that 
of amphioxus. It consists of mesodermal funnels, leading primarily 
from the coelom to the exterior. It may be that this type of kidney 
arose in connexion with the abandoning of the sea for fresh water. 
Probably all but the earliest vertebrates have passed through a fresh- 
water stage, and it is significant that all except Myxine have less salt in 

iv. 4 AGNATHA 83 

their blood than there is in sea water. Elaborate devices for regulation 
of osmotic pressure have been developed, and the mesodermal kidneys 
play a large part in this regulation. 

This outline only gives a few suggestive features of vertebrate 
organization. The details differ bewilderingly in the different types 
and it is our business now to survey them. In the earliest forms the 
more special mechanisms are absent or at least function only crudely, 
and passing through the vertebrate series we find more and more 
devices adopted, along with more and more delicate co-ordination 
between the various parts, culminating in the extremely highly 
centralized control of almost every aspect of life that is exercised by 
the mammalian cerebral cortex. 

3. Agnatha 

The earliest vertebrates, while showing most of the characteristic 
features of the group, differ from the rest in the absence of jaws and 
are therefore grouped together in a superclass Agnatha, distinguished 
from the remaining vertebrates, which have jaws, and are therefore 
called Gnathostomata. The only living agnathous animals are the 
Cyclostomata, lampreys and hag-fishes, but the first vertebrates to 
appear in the fossil series, mostly heavily armoured and hence known 
as 'ostracoderms', found in Silurian and Devonian strata, also show 
the agnathous condition, and have some other features in common 
with the Cyclostomata. This group of agnathous vertebrates shows 
some interesting experimentation in methods of feeding, before the 
jaw-method became adopted. The modern cyclostomes are parasites 
or scavengers, in the adult state, but as larvae the lampreys still feed 
on microscopic material, using an endostyle resembling that of 
amphioxus in many ways, but making use of muscular contraction 
rather than ciliary action to produce a feeding current. The methods 
of feeding of the Devonian forms are not known for certain, but 
probably included shovelling detritus from the bottom. 

The Cyclostomata are therefore worth special study as likely to 
show us some of the characteristics possessed by the earliest vertebrate 

4. Lampreys 

The most familiar cyclostomes are the lampreys, of which there are 
various sorts found in the temperate zones of both hemispheres. All 
lampreys have a life-history that includes two distinct stages: the 
ammocoete larva lives in fresh water, buried in the mud, and is 


microphagous: the adult lamprey has a sucking mouth, and usually 
lives in the sea, where it feeds on other fishes. Lampetra the lamprey 
(Fig. 47), is a typical example, common in Great Britain. The adult 
is an eel-like animal about 30 cm long, black on the back, and white 
below. The surface is smooth, with no scales. The skin is many- 
layered (Fig. 48). The outermost cells have a striated cuticular border. 
Mixed with these epithelial cells the lamprey, like most aquatic 
vertebrates, has many gland-cells for producing slime. Below the 
epidermis lies the dermis, a layer of bundles of collagen and elastin 

Fig. 47. Brook lampreys, Lampetra planer i. 

A, ripe female, with anal fin; B, ripe male; note shape of dorsal fin and presence of 

copulatory papilla. (Curves due to fixation.) 

fibres, running mostly in a circular direction. This tissue is sharply 
marked off from a layer of subcutaneous tissue containing blood- 
vessels and fat, as well as connective tissue. There are pigment cells 
in the dermis and a thick layer of them at the boundary of dermis and 
subcutaneous tissue. The chromatophores are star-shaped cells whose 
pigment is able to migrate, making the animal dark or pale. This 
change is especially marked in the larva and is produced by variation 
in the amount of a pituitary secretion (p. 107). 

The head of the lamprey bears a pair of eyes and a conspicuous 
round sucker. On the dorsal side is a single nasal opening, and behind 
this there is a gap in the pigment layers of the skin through which the 
third or pineal eye can be seen as a yellow spot. There are seven pairs 
of round gill openings, which, with the true eyes (and some miscount- 
ing or perhaps inclusion of the nasal papilla), are responsible for the 
familiar name 'nine eyes'. There is no trace of any paired fins, but the 
tail bears a median fin, which is expanded in front as a dorsal fin. 
There are sex differences in the shape of the dorsal fins of mature 
individuals and the female has a considerable anal fin (Fig. 47). 

iv. 5 



The lamprey swims with an eel-like motion, using its myotomes in 
the serial manner that has been mentioned in amphioxus and will be 
discussed later (p. 133). The waves that pass down the body are of 
short period relative to the length, so that the swimming is mechani- 
cally inefficient; lampreys show great activity, but their progress is 
not rapid. The animal often comes to rest, attaching itself with the 
sucker to stones (hence the name, 'suck-stone') or to its prey. In this 
position water cannot of course pass in through the mouth, but both 

s. cut. 

Fig. 48. Section of skin of lamprey. 

c. club cells; der. dermis; ep. epidermis; gr. granular gland-cells; m. myotomal muscle; 
pig. pigment cells; s.cut. subcutaneous connective tissue. (After Krause.) 

enters and leaves by the gill openings. When swimming the backward 
jet of water may assist in locomotion. 

The trunk musculature consists of a series of myotomes separated 
by myocommas. Each myotome has a W-shape, instead of the simple 
V of amphioxus. The muscle-fibres run longitudinally and they are 
striped, but of a somewhat peculiar fenestrated type. 

5. Skeleton of lampreys 

The skeleton of lampreys consists of the notochord and various 
collections of cartilage. This latter is partly of the typical vertebrate 
type, that is to say, consists of large cells in groups, separated by a 
matrix of the protein chondrin, which they secrete. In other regions 
a tissue containing more cells and less matrix is found, the so-called 
fibro-cartilage, and this more nearly resembles fibrous connective 
tissue and serves to emphasize that no sharp line can be drawn 
between these tissues. There is also, in the larva, a tissue known as 


muco-cartilage, which is an elastic material serving more as an 
antagonist to the muscles than for their attachment. 

The notochord remains well developed throughout life as a rod 
below the nerve-cord. It consists of a mass of large vacuolated cells, 

Fig. 49. Transverse section through notochord of lamprey. 
c. cells; s. sheath. (After Krause.) 


Fig. 50. Lateral view of skeleton of head and branchial arches of Petromyzon. 

ac. auditory capsule; adc. antero-dorsal cartilage; anc. annular cartilage; ha. branchial 
arch; bd. basidorsal; hac. hyoid cartilage; hbc. hypo-branchial rod; lit. horizontal bar; n. 
notochord; ?ic. nasal capsule; oc. orbital cartilage; per. pericardial cartilage; pdc. postero- 
dorsal cartilage; pic. posterolateral cartilage; st. styliform cartilage; /. tendon of tongue; 
II-X, cranial nerves. (After Parker.) 

enclosed in a thick fibrous sheath (Fig. 49). The rigidity of the whole 
rod depends on the turgor of the cells and it often collapses com- 
pletely in fixed and dehydrated material (Fig. 59). No doubt in life it 
serves, like the notochord of amphioxus, to prevent shortening of the 
body when the myotomes contract. 

The notochordal sheath is continuous with a layer of connective 
tissue, which also surrounds the spinal cord and joins the myocom- 


mas and thus eventually the subcutaneous connective tissue. Within 
this connective tissue there develop certain irregular cartilaginous 
thickenings that are of special interest because they may be compared 
with vertebrae, perhaps with the basi-dorsal element (p. 132). They 
lie on either side of the spinal cord (Fig. 50), that is to say, above the 
notochord, and consist either of one nodule on each side of the seg- 
ment, through the middle of which the 
ventral nerve-root emerges, or of two 
separate nodules, with the nerve between 
them. Rods of cartilage extend dorsally 
and ventrally into the fins, but are not 
attached to the 'vertebrae'. 

The lamprey skull shows even in the 
adult the basic arrangement found only 
in the embryo of higher vertebrates. The 
floor is formed of paired parachordals on 
either side of the notochord and in front 
of this paired trabeculae. Attached to this 
base is a series of incomplete cartilagi- 
nous boxes surrounding the brain and 
organs of special sense (Fig. 51). To 
this skull is attached the skeleton that 
supports the sucker and gills. The 
arrangement of the skull differs consi- 
derably from that of later vertebrates. 
The cranium has a floor around the end 
of the notochord, and in front of this 
there is a hole containing the pituitary 
gland. The side walls are strong but the roof is composed only of 
a tough membranous fibro-cartilage. The auditory capsules are 
compact boxes surrounding the auditory organs at the sides. The 
olfactory capsule, imperfectly paired, is also almost detached from 
the cranium. Other ridges of cartilage lie below the eyes and there is 
a complex support for the sucker. 

The skeleton of the branchial region consists of a system of vertical 
plates between the gill-slits, joined by horizontal bars above and 
below them. This cartilage lies outside the muscles and nerves and is 
therefore difficult to compare with the branchial skeleton of higher 
fishes, which lies in the wall of the pharynx. The elastic action of the 
cartilages produces the movement of inspiration. A backward exten- 
sion of the branchial basket forms a box surrounding the heart. 

Fig. 51. Dorsal view of skull of 


Lettering as Fig. 50. /, olfactory 

nerve; /. hole in roof of cranium. 

(After Parker.) 


6. Alimentary canal of lampreys 

The sucker is bounded at the edges by a series of lips, which besides 
being sensory serve also to make a tight attachment when the lamprey 
sucks (Fig. 52). In the sucker are numerous teeth, whose arrangement 
varies in the different types of lamprey. These teeth are horny epi- 
dermal thickenings, supported by cartilaginous pads, and are there- 
fore not comparable with the teeth of vertebrates, which are derived 

Fig. 52. Sucker of Petromyzon show- Fig. 53. Section through tooth of lamprey 

ing outer circular lip, teeth, and tongue, 1, horny cap; 2, stellate tissue; 3, cap to replace 

with special teeth, at the centre. , ; 4> connective tissue; 5, epidermis of mouth; 

(After Parker.) 6, cartilage; 7, proliferative layers of epidermis 

that produce the horny cells. 
(After Hansen, from Kukenthal.) 

mainly from mesodermal tissues (Fig. 53). The sharper and larger 
teeth are borne on a movable tongue, which is used as a rasp (Fig. 54). 
An annular muscle runs round just above the lips of the sucker and 
presumably serves to narrow the margin and hence to release the fish. 
The remaining muscles are mostly attached to the tongue and base 
of the sucker. The largest of these muscles, the m. cardioapicalis, is 
attached posteriorly to the cartilage surrounding the heart and in front 
is prolonged into a conspicuous lingual tendon, which is attached to 
the tongue and serves to pull it backwards. Presumably the action of 
this muscle deepens the oral cavity and is thus the main agent securing 
attachment of the sucker. There is a collar of circular fibres around 
the front end of the cardio-apical muscle, serving to lock the tendon 
and maintain the suction. Dorsal and ventral to the main tendon are 

iv. 6 


groups of muscles that rock the tongue up and down to produce a 
rasping action. The muscles of the sucker are all derived from the 
lateral plate and are innervated from the trigeminal nerve; their fibres 
are striated. 

The mouth is a small opening above the tongue and leads into a 
large buccal cavity. At the hind end this divides into a dorsal passage, 
the oesophagus, for the food, and a ventral respiratory tube, which 
leads to the gill pouches but is closed behind. At the mouth of the 


m. card.ap. 


mus.2 mus.t 

Fig. 54. Longitudinal section through head of lamprey. 

ann. annular muscle of sucker; b. brain; circ.m. circular fibres of tongue-muscles; oes. oeso- 
phagus; g. gill aperture; h.s. hypophysial sac; m.card.ap. cardio-apical muscle; mus. 1 and 
2, muscles that rock the tongue; n. notochord; nas. nasal sac; nos. nostril; p. pineal; pit. 
pituitary gland; t. tooth; tend, tendon of tongue, pulled back by m.card.ap.; to. tongue. (Partly 

after Tretjakoff.) 

respiratory tube is a series of velar tentacles, corresponding exactly in 
position to those of amphioxus, and serving to separate the mouth 
and oesophagus from the respiratory tube while the lamprey is feed- 
ing. The seven branchial sacs are lined by a folded respiratory epi- 
thelium and surrounded by muscles, and these, together with the 
elastic cartilages and appropriate valves, ensure the pumping of the 
water tidally, in and out of the external openings. In front of the first 
sac is the remains of an eighth pouch, whose surface is not respiratory. 
The 'salivary' glands are curious organs of which little is known. 
They are a pair of pigmented sacs, embedded in the hypobranchial 
muscles. Each has a folded wall, from which a duct proceeds forward 
to open below the tongue. The salivary glands produce a secretion 
that prevents coagulation of the blood of the fishes on which the lam- 
prey feeds. The nature of this secretion is not known, but it rapidly 
turns black on exposure to the air and the glands for this reason 
appear to be pigmented. It has been observed that in lampreys taken 
from fishes the intestine is filled with red corpuscles, and there is 
therefore no doubt that they feed mainly on the blood of their prey. 


Little is known of the habits of lampreys in the sea, but in North 
America there are races of lampreys that are land-locked and feed on 
the fishes in the lakes, where they have recently become a most serious 
pest (Fig. 55). 

The oesophagus (fore-gut) leads directly into a straight intestine 
(mid-gut); there is no true stomach in lampreys (Fig. 56). The surface 
of the intestine is increased by a typhlosole, running a somewhat 
spiral course. There is a liver, gall-bladder, and bile-duct of typical 
vertebrate plan, but no separate pancreas. However, in the wall of the 

Fig. 55. Lake lamprey attached to a bony fish, which also shows the scars of the 
attacks of other lampreys. (After Gage.) 

anterior part of the intestine there are large patches of cells that 
resemble those of the acini of the pancreas of higher forms and con- 
tain secretory granules. Barrington has shown that extracts of this 
region have a high proteolytic power, the enzyme being of the tryptic 
type, with its optimum between pH 7-5 and 7-8. Some of this tissue is 
collected in the walls of short diverticula, reaching forwards. The 
situation is therefore essentially similar to that found in amphioxus, 
and we may regard these patches of zymogen cells, or the diverticula, 
as the forerunners of the exocrine portions of the pancreas. In the 
lampreys the endocrine portion, not yet identified in amphioxus, also 
appears. Around the junction of the fore-gut and intestine are groups 
of follicles that do not communicate with the lumen of the intestine. 
These 'follicles of Langerhans' were, appropriately enough, first seen 
by the discoverer of the islets in higher forms, and Barrington has 
now shown that following destruction of this tissue by cautery there 
is a rise in blood-sugar. Moreover, after injection of glucose, vacuola- 
tion of the cells occurs. We may safely conclude that these cells are 
involved in carbohydrate metabolism, but only one type of cell is 

iv. 7 


7. Blood system of lampreys 

The blood vascular system is arranged on the same general plan 
as in amphioxus but there is a well-developed heart. This lies behind 
the gills and can be considered as a portion of the sub-intestinal vessel, 
folded into an S-shape and divided into three chambers. The heart 
is suspended in a special portion of the coelom, the pericardium, 
whose walls are supported by cartilage. In the larva the heart first 
appears as a straight tube and owing to an abnormality of development 
it sometimes fails to develop its S-shape. Contractions can neverthe- 

Fig. 56. Mid-gut of larval lamprey. 

ai. anterior region of intestine; bd. bile-duct; ca. coeliac artery; gb. gall-bladder; hp. hepatic 

portal vein; /. liver; oes. oesophagus; p. position of 'pancreas', containing islet tissue; 

pi. posterior intestine; y. yellow area where wall of intestine contains zymogen cells. 

(From Barrington.) 

less be seen in these abnormal hearts, passing from behind forwards 
along the straight tube. Similarly in the normal heart contraction 
proceeds in the chambers from behind forwards. The most posterior 
chamber is a thin-walled sinus venosus, into which the veins pour 
blood. This leads to an auricle (atrium), also thin-walled, lying above 
the sinus. The atrium passes blood into the ventricle below it, a 
thick-walled chamber, providing the main force for sending the blood 
round the body. 

The heart receives nerve-fibres from the vagus nerve and contains 
nerve-cells, some of which give a chromaffin reaction suggesting the 
presence of adrenalin-like substances. Stimulation of the vagus nerve 
produces acceleration of the heart-beat, followed by slowing. Acetyl 
choline also accelerates the heart. In Myxine there are no nerves to 
the heart or nerve-cells in it and acetyl choline has no effect. Both 
hearts contain much adrenaline and similar substances but show little 
change when adrenaline is added to a perfusate. 

Blood leaves the ventricle by a large ventral aorta, running forwards 


between the gill pouches, to which it sends a series of eight afferent 
branchial arteries. These break up into capillaries in the gills, and 
efferent branchial arteries collect to a pair of dorsal aortae, running 
backwards, which join and form the main dorsal aorta. This passes 
down the trunk and carries blood to all the parts of the body by means 
of series of segmental arteries and special vessels to the gut, gonads, 
and excretory organs. A curious feature is that many of these arteries 
are provided with valves at the point at which they leave the main 

trunks (Fig. 57). It may be significant 
that such valves are not found where 
the efferent branchials join the dorsal 
aorta, nor at the points of exit of the 
renal arteries, so that perhaps the 
valves serve to reduce the pressure in 
the majority of the arteries, while 
leaving it high in those to the kidneys. 
The removal of large quantities of 
water is an important problem in all 
freshwater animals and is facilitated 
by a high pressure in the kidneys. 
This must be difficult to maintain in 
an animal with a branchial circulation 
and hence a double set of capillaries. 
The venous system consists of a 
network of sinuses, with contractile 
venous hearts in various places. 
There is a large caudal vein, dividing 
where it enters the abdomen into two posterior cardinals. These 
run forward in the dorsal wall of the coelom, collecting blood from 
the kidneys, gonads, &c, and opening into the heart by a single 
ductus Cuvieri on the right-hand side, this being the remains of a pair 
found in the larva. Anterior cardinals collect blood from the front 
part of the body, and there is also a conspicuous ventral jugular vein 
draining venous blood from the muscles of the sucker and gill pouches. 
Besides the veins proper there is a large system of venous sinuses, 
especially in the head. Blood from the gut passes by a hepatic portal 
vein through a contractile portal heart to the liver, from which hepatic 
veins proceed to the heart. 

The blood of lampreys, like that of all vertebrates, contains the 
respiratory pigment haemoglobin, enclosed in corpuscles, here nucle- 
ated. This arrangement immensely increases the oxygen-carrying 

Fig. 57. Valves at the origin of 
segmental arteries of a lamprey. 

1, notochord; 2, segmental artery; 3, 


(From Kukenthal, after Keibal.) 


power of the blood. Haemopoietic tissue occurs in the intestinal wall 
of the larva and this has been regarded by some as representing the 
spleen. In the adult the blood-forming tissue lies below the spinal 
cord and in the kidney. White corpuscles resembling lymphocytes 
and polymorphonuclear cells occur, produced by lymphoid tissue in 
the kidneys and elsewhere. However, there is no distinct system of 
lymphatic channels. 

8. Urinogenital system of lampreys 

The excretory and genital systems of vertebrates consist of a series 
of tubes opening from the coelom to the exterior and serving to carry 
away both excretory and genital products. This plan of organization is 

Fie. 58. Diagram to show arrangement of the pronephros in a freshly hatched 

g. gonad; pr. pronephros; prd. pronephric duct. (After Wheeler.) 

quite different from that found in amphioxus and represents a new 
acquisition by the vertebrates. It is not clear whether the excretory 
or genital component of the complex is the primary one, nor indeed 
why they are associated. The gonads develop from the walls of the 
coelom in all animals possessing that cavity; some hold that the coelom 
represents an enlargement of a sac that at first served purely as a 
gonad. Genital ducts leading from the coelom to the exterior are 
common in invertebrates, and we may guess that at their first appear- 
ance the urinogenital tubules of vertebrates served only for genital 

The conversion of these tubules to excretory purposes may have 
been a result of the adoption of the freshwater habit. The blood of 
lampreys, when in fresh water, contains a higher concentration of salts 
than the surrounding water. Little is known about the condition in 
sea lampreys, where blood is probably hypotonic to the sea. When in 
the river the animals must deal with the tendency for water to flow in. 
This water must be removed without losing salt ; accordingly in most 
freshwater animals, including vertebrates, we find some system by 
which the separation can be achieved. 


The region that gives rise to the kidney during development lies 
between the dorsal scleromyotome and the more ventral lateral plate 

card v 


on. t 


pron. F 

Fig. 59. Section through newly hatched larvae of Lampetia hehind the pharynx. 

ao. aorta; card.v. cardinal vein; glom. glomerulus; fit. heart; my. myotome; n.c. nerve-cord; 
not. notochord, which has collapsed because of lack of turbidity after fixation; oes. oeso- 
phagus; pron.f. ciliated funnel of pronephros; pron.t. twisted pronephric tubule; sp. space 

around nerve-cord. 

Fig. 60. Kidney system of a 22-millimetre larva of Lampetra. 

tnes. mesonephric tubules; mesg!. mesonephric glomeruli; pr. pronephric funnels; 
prd. pronephric duct; prgl. pronephric glomeruli. (After Wheeler.) 

mesoderm; it is known as the nephrotome. This tissue differentiates 
during development from in front backwards, making a series of 
segmental funnels, opening into a common archinephric duct (Fig. 
58). The most anterior funnels open into the pericardium; usually 
there are four of these in a freshly hatched larva, opening into a single 

iv. 8 




duct, which reaches back to an aperture near the anus. Close to each 
funnel there develops a tangle of blood-vessels, the glomerulus (Figs. 
59 and 6o). Presumably the osmotic flow of water into the body is 
relieved by the pressure of the heart-beat forcing water out from the 
glomeruli into the coelomic fluid, whence it is removed by the funnels, 
with the aid of their cilia. The tubules become longer and twisted 
after hatching and may perhaps serve for salt-reabsorption. 

These anterior funnels constitute 
the pronephros. As the animal 
grows they are replaced by a more 
posteror set, the mesonephros. 
There is, however, a gap of 
several segments in which no 
tubules appear (Fig. 6o), a strange 
and unexplained discontinuity, 
common to all vertebrates. The 
pronephric tubules gradually dis- 
appear and finally in the adult all 
that remains of the organ is a mass 
of lymphoid tissue. Meanwhile the 
mesonephros develops as a much 
larger fold, hanging into the coelom 
and containing very extensive wind- 
ing tubules. These do not open to 
the coelom (at least in the adult) but 
each to a small sac, the Malpighian 
corpuscle, which contains a portion 
of the coelom and the glomerulus. 
This is obviously a more efficient method for allowing the heart to 
pump excess water out of the blood and down the tubules. The latter 
themselves have become greatly elongated and make up the main 
bulk of the organ (Fig. 6i). The segmental arrangement is there- 
fore much obscured and as extra glomeruli are added it disappears 
completely. The mesonephros extends at its hind end as the animal 
grows, until it forms the adult kidney, a continuous ridge of tissue 
reaching back to the hind end of the coelom. Besides the excretory 
apparatus the kidney also contains much lymphoid tissue and fat, and 
it probably plays a part in the formation and destruction of red and 
white corpuscles. 

The gonads are unpaired ridges medial to the mesonephros. Pri- 
mordial germ-cells, set aside very early in development, migrate into 

Fig. 6i. Transverse section of kidney of 

gl. glomerulus; mid. middle section of 

tubule; pr. proximal region of tubule; term. 

terminal region, opening into W.d. Wolffian 


(After Krause.) 

iv. 8- 


these ridges and develop into eggs or sperms. The differentiation of 
the gonad occurs relatively late in lampreys, so that in young am- 
mocoetes the organ is 'hermaphrodite', containing developing oocytes 
and spermatocytes together. The ripe ovary consists of ova each sur- 
rounded by single-layered follicular epithelium, which finally ruptures 
and liberates the egg into the coelom, whence it escapes by pores to be 
described presently. The testis consists of a number of follicles con- 
taining sperms; it is unique among vertebrates in that the follicles 

CL U 9 . 

Fig. 62. Cloacal region of fully adult Lampetra. 

C. coelom; CI. lips of cloaca; Ct. connective tissue; D. duct leading from coelom to the 

mesonephric duct; Df. dorsal fin; M. muscle; Md. mesonephric ducts; N. notochord; 

R. rectum; Ug. urinogenital papilla. (After Knowles.) 

have no ducts; when ripe they rupture into the coelom, which becomes 
filled with spermatozoa and these escape, like the ova, by pores. 

These apertures by which the gametes escape are similar in the 
two sexes and consist of short channels, one on each side, leading from 
the coelom to the lower end of the kidney duct (Fig. 62). They nor- 
mally become open only a few weeks before spawning, but Knowles 
has shown that injections of oestrone or anterior pituitary extract will 
cause perforations of the ducts in young lampreys, indeed even in the 
ammocoete larve. 

Fertilization is external, but there are modifications of the cloaca in 
the two sexes to assist in ensuring fertilization and proper placing of 
the eggs in the 'nest' (p. 113). The lips of the cloaca of the ripe male 
are united to form a narrow penis-like tube. The cloacal lips of the 


female are enlarged and often red; in addition she has an anal fin, 
probably used, as in salmon and trout, to make a nest. These sex 
differences, which develop shortly before spawning, can also be 
initiated by injection of anterior pituitary extracts (p. 107). 

9. Nervous system of lampreys 

The nervous system of the cyclostomes is very much better 
developed than that of amphioxus and shows the characteristic plan 
that is present in all vertebrates. The essence of the vertebrate ner- 
vous organization may be said to be that it consists of large amounts 
of tissue and is highly centralized. The brains of vertebrates contain 
much larger aggregates of nervous tissue than are to be found in any 
other animals, and this tissue produces by its actions the most charac- 
teristic features of vertebrate life. Vertebrates are active, exploratory 
creatures, and their behaviour is much influenced by past experience. 

We shall return later to detailed discussion of the organization of 
the central nervous system; now we may look briefly at the plan 
found in the lamprey, as an introduction to that of other vertebrates. 
As compared with amphioxus there has been a very high degree of 
cephalization. The front end of the spinal cord is enlarged into a 
complicated brain, and the nerves connected with a number of the 
more anterior segments have become modified to form special cranial 

The spinal nerves, however, still show the plan found in amphioxus 
in that the dorsal and ventral roots do not join. In amphioxus the 
ventral roots contain motor-fibres for the myotomes and some 
proprioceptive fibres, while the dorsal roots contain sensory fibres and 
motor-fibres for the lateral plate musculature (p. 36). The details of 
the composition of the nerves of lampreys are still unknown, but there 
are hints of considerable deviations from this plan. The ventral roots 
contain many motor fibres passing to the myotomes. The dorsal roots 
consist largely of sensory fibres with bipolar cell bodies collected into 
dorsal root ganglia including proprioceptor fibres from the myotomes: 
it is not known whether the dorsal roots also contain any efferent 
fibres. In the young larva many of the afferent fibres are the processes 
of cells lying in the spinal cord (Rohon-Beard cells), which are 
typical of the early stage of many chordates. There are few types 
of cells in the cord at this time, allowing for only the simplest 
reflex arcs. 

The autonomic nervous system shows some generalized and some 
special features. The gut is mainly innervated by the vagus, which 


extends far back along the intestine. There is little contribution of 
fibres from the spinal nerves to the alimentary canal, since this has no 
mesentery, being attaached only at its cranial and caudal ends. There 
are, however, numerous fibres from the spinal nerves to the rectum, 
ureters, and cloacal region, and numerous postganglionic neurons 
are found here. Nerve-cells are also found in the intestinal plexuses. 

The sympathetic system consists of isolated fibres running in both 
dorsal and ventral roots. Many of these run directly to their endings, 
for instance in the arteries, without interpolation of neurons. A few 
postganglionic cells are present, however, but they are seldom collec- 
ted into ganglia. The system is therefore even more scattered than 
in elasmobranchs (p. 173). The 'adrenal' system is also diffuse. There 
are scattered masses of interrenal (cortical) tissue and large groups 
of suprarenal (medullary) cells, especially in the walls of the veins and 
the heart. The suprarenal tissue receives 'preganglionic' fibres from 
the spinal nerves. Its cells sometimes seem to be connected with each 
other by fibres like those of neurons and they may operate a form of 
control intermediate between nervous and hormonal (Johnels, 1956). 

The nerve-fibres in the nervous system of cyclostomes are not pro- 
vided with myelin sheaths ; in this they resemble the nerves of amphi- 
oxus. Conduction is slow in such non-medullated fibres, the only case 
actually investigated in cyclostomes being the lateral line nerve of 
Bdellostoma, found by Carlson to conduct at the low rate of 5 metres 
a second (frog about 50 m/sec, mammals up to 100 m/sec). 

The spinal cord is of a uniform transparent grey colour and is 
flattened dorso-ventrally, apparently to allow access of oxygen, and 
metabolites, no blood-vessels being present within the cord. How- 
ever, vessels are present in Myxine in which the cord is also flat. The 
nerve-cell bodies lie, as in higher vertebrates, towards the centre, but 
the synaptic contacts are not made in this 'grey' matter but at the 
periphery, in what would correspond to the white matter of higher 
forms. The outer part of the cord is thus made up of a neuropil or 
nerve feltwork, formed of the terminations of the incoming sensory 
fibres and the dendrites of the motor-cells. These cells (Fig. 63) lie 
in the ventral part of the cord, their axons running out to make the 
large fibres of the ventral roots and their dendrites passing to all parts 
of the peripheral regions of both the same and the opposite sides of the 
cord. They are thus presumably able to be stimulated directly by 
impulses in the processes of the afferent fibres that end in these 

Direct control of the spinal cord from the brain is obtained through 



Fig. 63. Cells of the spinal cord of the larva of Lampetra. 
A „nH R We motor-cells with dendrites reaching to the opposite side; C, small cells with 
^p^SSno axon; «. axon; M/. Mailer's fibres; „*«,.>. neuropil at 
P periphery of spinal cord. (After Tretjakoff.) 



IV. 9 



cerh. h. 

Mid- Hind- brain. 

opt.L med. c ^ or 

Fore. - Mid- Hind- brain. 




Hind — brain. 

Fig. 64. Brain of the lamprey. 

A, side view; B, dorsal view with choroid plexus intact; c, after removal of choroid, cereb. 
cerebellum; cer. h. cerebral hemisphere; chor. choroid plexus; hypot. hypothalamus; it. iter 
between third and fourth ventricles; lam.t. lamina terminalis (thickened anterior wall of 
third ventricle); med. medulla oblongata; opt.L optic lobe; pin. pineal eye; thai, thalamus; 
3rd v., 4th v., third and fourth ventricles. (After Sterzi.) 

a number of very large Miiller's fibres, originating from giant cells in 
the reticular formation of the brain, whose large dendrites (Fig. 65) 
receive fibres from several higher centres, providing an uncrossed final 
common pathway to the spinal cord. There is some difference of 
opinion as to whether any branches of these large fibres proceed 


directly into the ventral roots; probably they do not do so but the 
dendrites of the motor-cells branch around them and thus receive 
stimulation (Fig. 63). In the earliest larva co-ordination is by a pair of 
giant Mauthner cells, with dendrites among the entering fibres of the 
eighth nerve and an axon descending on the opposite side. Such cells 
are present in the earliest stages of nearly all fishes and amphibians. 

Other nerve-cells in the more dorsal parts of the cord have no long 
axons and apparently serve to connect the neuropil of the various 
regions. The afferent fibres reaching the cord in the dorsal roots give 
off branches that ascend for a short distance and descend for long 
distances. The pathways to the brain thus pass through multiple 

The brain itself (Fig. 64) is built on the typical vertebrate plan, as 
an enlargement of the front end of the spinal cord, with thickenings 
and evaginations corresponding to the various organs of special sense. 
Although we know little of its internal functional organization in 
lampreys, it is probably not far wrong to regard it as chiefly consisting 
of a series of hypertrophied special sensory centres; thus the forebrain 
is connected with smell, midbrain with sight, hind-brain with 
acoustico-lateral and taste-bud systems. The forebrain and olfactory 
sense are moderately well developed in adult lampreys, as is the visual 
sense, with its chief centre in the midbrain. The auditory and acoustico- 
lateral systems are not very well marked, and the cerebellum is small. 
Taste is also much less developed than in the higher fishes (p. 220). 

Parts of the brain 

Forebrain (prosencephalon) Cerebral hemispheres (telen- 

Between-brain (diencephalon) 
Midbrain (mesencephalon) Optic lobes 

Hind-brain (rhombencephalon) Cerebellum (metencephalon) 

Medulla oblongata (myelen- 

The upper surface of the brain is covered by an extensive vascular 
pad, the choroid plexus or tela choroidea (Fig. 64). This extends into 
the ventricles of the brain at three points — into the third ventricle of 
the diencephalon, into the iter (duct) leading through the midbrain 
from third to fourth ventricles, and into the fourth ventricle itself. 
The roof of the brain is thus non-nervous in these regions. In later 
vertebrates the choroid extends only into the third and fourth 


ventricles. Presumably the vascular membranes of the brain are highly 
developed in lampreys because of the absence of cerebral blood 

From the lower part of the mid- and hind-brain arise all the cranial 
nerves except the olfactory and optic. These nerves follow the same 
plan as those of gnathostomes but they are difficult to make out by 
dissection in the lamprey and will be left for consideration in con- 
nexion with the dogfish, in which they can easily be dissected. The 

beet. opt. 
chor. pL3, 4. 

otf.ep — IM-<^9 % 


Fie. 65. Sagittal section through head of lamprey. 

cereb. cerebellum; cer.h. cerebral hemisphere; 3 & 4, choroid plexuses of the 3rd and 
4th ventricle, extending also into the midbrain; h.s. naso-hypophysial tube; hab. habenular 
region; hyp. hypothalamus; interped. interpeduncular region; med. medulla oblongata; Mull. 
M Oiler's cell; not. notochord; o. glandular organ of nasal sac; olf.ep. olfactory epithelium; 
olf.n. olfactory nerve; p. ant., p. int., and p.nerv. partes anterior, intermedia, and nervosa of the 
pituitary gland; parap. parapineal; pin. pineal; ted. opt. tectum opticum. 

cranial nerves represent nerves similar to the dorsal and ventral nerve- 
roots of the trunk, much modified as a result of the special develop- 
ment of the head (p. 148). They carry afferent fibres from the skin of 
the head and gills and motor-fibres for moving the eyes, sucker, and 
branchial apparatus. 

From the relative sizes of the parts of the brain it can be seen that 
the various special sensory centres are still small. The largest part of 
the brain is the medulla oblongata, which is well developed because 


of the extensive sucking apparatus, innervated from the trigeminal 

The forebrain consists of a pair of large cerebral hemispheres and 
these open by the foramina of Munro into a median third ventricle, 
whose walls constitute the diencephalon or between-brain (Fig. 65). 
This diencephalon, besides connecting the forebrain with the mid- 
brain, includes the thalamus and serves important functions of its own. 
Its ventral part, the hypothalamus, is well developed in all vertebrates 
as a central organ controlling visceral activities and the internal life 
of the organism. Nerve-fibres from the supraoptic nucleus of the 
hypothalamus proceed to the pars nervosa of the pituitary and, as in 
other vertebrates, are filled with granules of neurosecretory material, 
which presumably controls pituitary action. A simple portal system 
of blood-vessels connects the hypothalamus with the pituitary. 

10. The pineal eyes 

The diencephalon is also the region of the brain from which the 
eyes are formed. In lampreys, besides the usual pair of eyes, there is 
also, attached to the roof of the between-brain, the so-called third, 
epiphysial, or median eye, better developed in these animals than in 
any other living vertebrate except perhaps certain reptiles. 

This organ is actually not median but consists of an unequally 
developed pair of sacs, that on the right, the pineal, being larger and 
placed dorsal to the morphologically left parapineal (Fig. 66). The 
sacs form by evagination from the brain and remain connected with 
the dorsal epithalamic or habenular region of the between-brain by 
two stalks. The two organs are similar in structure, consisting of 
irregular flattened sacs with a narrow lumen. Both upper and lower 
walls of each organ contain receptor cells, with processes that project 
into the lumen and nerve-fibres directed outwards. These fibres 
apparently mostly end within the organ, in contact with ganglion 
cells whose axons run to unequal right and left habenular ganglia. 
In addition there are supporting and pigment cells in the retinas. 
Knowles has shown that the retinal cells of the pineal make movements, 
being arranged differently under conditions of illumination and dark- 
ness. The significance of these photomechanical changes is unknown 
but they demonstrate that the pineal cells are sensitive to light. 

The structure of these pineal organs shows that they consist of 
portions of the diencephalic wall where the ciliated cells of the epen- 
dyma are specialized as photoreceptors. They show the same general 
plan as the paired eyes, but with no differentiated dioptric apparatus. 



It has been possible to find out something of the part that these 
organs play in the life of the lamprey. When a bright spot of light is 
directed upon the pineal region of a stationary ammocoete larva move- 
ment is usually initiated, but only after illumination for many seconds. 



t.s.s., o.s.s 

66. Pineal and parapineal organs of adult Lampetra fluviatilis 
A. larva, B. adult. Sagittal section. 

, inner and outer sensory cells; p. process; pin. pineal; p. pin. parapineal. 
(After Tretjakoff.) 

Moreover, these movements can be elicited even after the pineal 
organs have been removed! In the larval lamprey the paired eyes are 
deeply buried below pigmented skin, so the movement is not likely 
to be due to them; indeed it continues when they too have been taken 
out! Evidently there must be still other receptors, able to respond to 
changes of light intensity in the wall of the diencephalon. This recalls 
the fact that photoreceptors are found within the substance of the 
nervous system of amphioxus. This power of response to changes of 
illumination has been retained in the vertebrates, and persists in some 



as yet unknown cells in the brain, even after the paired and pineal 
eyes have become specialized for light reception. The whole study is 
of special interest as showing the stages by which the eyes may have 
been evolved. Higher fishes also show the power of responding to 


rm — 1 1 1 1 1 1 1 1 1 1 M 15. 

I I I i I I I I 1 ! ! I I I I II 1 I I II I I 

\t up 


Y f 

15 20 25 30 I S 

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Fig. 67. Colour-changes of larval lampreys, measured by the melanophore index (see 
p. 300). Animals kept out of doors except as shown along the line AB, where rect- 
angles above the line show illumination with electric light and below the line total 
darkness. Normal animals show a regular daily rhythm, becoming pale at night. 
Reversal of normal day and night illumination stops the change. On 19 December 
the pineal eyes were removed from five out of the ten individuals and these there- 
after remained dark (upper chart); the other five continued to show the normal 
rhythm, until placed in total darkness. (After Young.) 

changes of illumination after the paired eyes and epiphysis have been 
removed (p. 210). 

If the pineal eyes are not essential for the initiation of movement, 
what is then their function ? In the ammocoete larva there is a daily 
rhythm of change of colour, the animals becoming dark in the day- 
time and pale at night. After removal of the pineal eyes this change no 
longer occurs: the animals remain continually dark (Fig. 67). This 
effect on the colour is produced by the action of influences from the 
pineal, passing to the pituitary gland (see p. 103). It seems that 
the pineal apparatus is an organ concerned with adjustment of the 
internal activities of the animal to correspond to the changing con- 
ditions of illumination. The control may be effected by impulses 



carried in the large tract that proceeds from the habenular ganglion 
to the hypothalamus, in the floor of the diencephalon. The latter is 
known to be concerned, throughout the vertebrate series, with the 
integration of the internal activities of the animal. 

¥ d Y 


p. int. 


Fig. 68. Sagittal section of the pituitary gland of lamprey. 

dien. diencephalon; inf. infundibulum; p.ant.,, and p. tier, partes anterior, intermedia, 

and nervosa, there are two types of cell in the pars anterior; 3rd V. third ventricle. 

(After Stendell.) 

3 4 5 6 

Hours after operation 

FlG. 69. Onset of pallor in a larval lamprey after removal of the pituitary gland, 
as shown by the decline in the melanophore index. (From Young.) 

1 1 . Pituitary body and hypophysial sac 

The lower portion of the diencephalon, the hypothalamus, forms 
a prominent pair of sacs, the lobi inferiores, which contain a partly 
separated diverticulum of the third ventricle and end below in the 
infundibulum (Fig. 65). The pituitary gland (hypophysis) is pressed 
against the underside of the hypothalamus (Fig. 68). The lower wall 
of the brain in this region consists not of nerve-cells but of a single 





epithelial layer, corresponding to the pars nervosa of the pituitary of 
higher forms. The major portion of the pituitary gland is a mass of 
secreting cells in which two parts can be recognized, the partes 
anterior and intermedia. After experimental removal of the inter- 
mediate portion of the pituitary lam- 
preys become permanently pale in 
colour (Fig. 69), showing that, as in 
other vertebrates (p. 299), a melano- 
phore-expanding substance is liberated 
into the blood by this gland, the secre- 
tion being presumably under the control 
of the pineal eyes (p. 105). The lamprey 
pituitary has been shown to contain 
oxytocic and 'water balance' hormones 
as well as one producing melanophore 
expansion. Moreover injections of 
mammalian anterior pituitary extracts 
induce appearance of the secondary 
sexual characters of lampreys. Evi- 
dently the functions of the pituitary 
have remained essentially the same 
through the whole chordate series. 

The pituitary of lampreys is peculiar 
because of great development of the 
naso-hypophysial sac (Fig. 70). Charac- 
teristically in vertebrates the pituitary 
body develops by the formation of a 
pocket of buccal ectoderm, whose walls 
then become folded, so that the part 
in front of the lumen becomes the pars 
anterior, that behind the pars inter- 
media. In nearly all vertebrates the 
lumen then loses its connexion with the 
exterior. In lampreys the hypophysial 
rudiment is continuous with that of the 
olfactory epithelium. The latter then 
moves dorsally and the two remain 

connected throughout larval life by a strand of cells. At metamorphosis 
this acquires a lumen and forms a tube extending from the nostril 
below the pituitary and brain. Because of its development this is 
sometimes called the naso-hypophysial tube but others doubt that 

Fig. 70. Dissection of lamprey from 
the ventral surface after injection 
of coloured gelatine to show the 
outline of the naso-hypophysial sac 
(.1) and its duct (d), which is shown 
dotted where it runs upwards be- 
tween the nasal sacs («). g, gill 
pouches. Contraction of the bran- 
chial apparatus squeezes the sac s, 
so that water is drawn in at each 



IV. II- 

it represents the cavity of the hypophysis and prefer the name 
nasopalatine canal. 

Inside the single nostril, guarded by a valve, are openings into the 
nasal sacs, which are cavities with folded walls. Some of the cells of 
these walls are the olfactory receptors and give off the axons that make 
up the olfactory nerves, entering the olfactory bulbs on the anterior 
end of the hemisphere (Fig. 65). Behind the nasal sacs lie numerous 
glandular follicles opening into the sac in the larva, but completely 
closed in the adult (Fig. 65). They may be comparable to Jacobson's 
organ (p. 405). 

Fig. 71. Section of lateral line organ of tail of adult Lampetra. 

p. pigmented cells around the pit; s.c. receptor cells 
(not showing long hairs). (After Young.) 

The naso-hypophysial tube proceeds back behind the pituitary to 
a closed sac lying between the first pair of gill pouches (Fig. 70). 
During the movements of respiration this sac is squeezed and water 
is expelled with some force through the nostril. When the gills relax 
water flows in at the nostril, and in this way the olfactory organ is 
provided with samples. If the naso-hypophysial opening is closed with 
a plug of plasticine the lamprey no longer reacts to solutions, for 
instance of alcohol, to which it normally responds by freeing its 
sucker and swimming away. 

12. Lateral line organs of lampreys 

The lateral line receptors, peculiar to fish-like vertebrates, are little 
patches of sensory cells found along certain lines on the head and 
trunk. They are all innervated by cranial nerves, those on the body 
and tail being served by a special backward branch of the vagus nerve. 
The receptor cells carry long hairs and are thus able to detect either 
movement of the water relative to the fish or of the fish itself. Objects 
moving nearby set up disturbances that may also be detected (p. 218). 

v. i3 



In the lamprey the lateral line organs are very simple (Fig. 71), being 
open to the exterior and not sunk in a canal as in higher forms. The 
rows are somewhat irregular, especially those on the body. 

13. Vestibular organs of lampreys 

The labyrinth may be considered as a specialized portion of the 
lateral line system, concerned with recording the position of the head 


mac.laq. \ mac.ut. 
3 mac. sac. 


amp a. 

Fig. 72. Labyrinth of right side, seen in lateral view. A and B, 

Lampetrci, c, Myxitie. 

a.c. anterior canal; amp. a. and p. anterior and posterior ampullae; cil. 

ciliated chamber; cr.a. and p. cristae; end. endolymphatic duct; lag. 

lagena; mac. lag., neg., sacc, ut. maculae of the lagena, neglecta, 

saccule, and utricle; p.c. posterior canal. (After de Burlet.) 

and angular accelerations. There is no evidence to decide whether 
lampreys can respond to sound. The labyrinth develops by an in- 
pushing of the wall of the head, and this then becomes closed off from 
the exterior. Internal foldings divide up the sac into a number of 
chambers, which differ considerably from those of gnathostomes. 
There is a large central vestibule, into which open below several 
partially separate sacs, provided with patches of sensory hairs. These 
correspond, from in front backwards, to the maculae of the utricle, 
saccule, and lagena of higher forms (Fig. 72). The hairs of the maculae 
are loaded with otoliths. There are only two broad semicircular 
canals, corresponding to the anterior and posterior vertical canals 
of other vertebrates, each with an ampulla, containing a receptor 
ridge, the crista. Also opening to the vestibule are two large sacs, 


covered with cilia (Fig. 72), whose beat produces complicated 
counter currents in the dorso-ventral plane. It has been suggested 
that these function as a gyroscope, compensating for the absence of 
a horizontal canal. 

In Myxine the condition is even simpler, there being only a single 
vertical semicircular canal (Fig. 72). However, it is claimed that this 

Fig. 73. Horizontal section of the eye of a lamprey. 

er., ir., sr., external, internal, and superior rectus muscles; v.v. venous sinuses which cushion 
the eye. (From Walls, The Vertebrate Eye, Cranbrook Institute of Science.) 

has cristae at both ends. The macular system also does not show the 
characteristic subdivisions but is a single macula communis. 

14. Paired eyes of lampreys 

The structure of the paired eyes is similar to that in other verte- 
brates. They are formed, like the pineal eyes, by evaginations of the 
wall of the diencephalon; the so-called optic nerve is therefore not 
really a peripheral nerve but a portion of the brain; it should strictly 
be called the optic tract. The eyes are moved by extrinsic muscles 
arranged in a somewhat unusual manner. Accommodation is effected 
by a process found in no other vertebrates. The cornea consists of two 
distinct layers, separated by a gelatinous substance. Attached to the 
outer (or dermoid) cornea is a cornealis muscle, apparently of myo- 
tomal origin, which flattens the cornea and pushes the lens closer 
to the retina (Fig. 73). There is an iris, outlining a round pupil, which 
changes little, if at all, in diameter under different illuminations. Most 
species of lampreys are diurnal animals. They are said to move towards 

iv. is 


white objects and probably use both the eyes and the nose to find 
their prey. In the ammocoete larva the paired eyes are buried below 
the pigmented skin and the animal makes no movements when light 
is shone on to this region. 

The optic tracts of adult lampreys end in the roof of the midbrain 
(tectum opticum) which is a highly differentiated, stratified region. 
Besides the optic fibres it receives also impulses from fibres ascending 
from the spinal cord and others from the auditory and lateral line 

Fig. 74. Experiment to show behaviour of larval lampreys when illuminated. The 
tank is left in total darkness and the larvae settle in all parts. When the light is 
switched on those in the illuminated part begin to swim and continue to do so until 
by chance they arrive in the darkened part, where they settle down. (From Young.) 

centres. The midbrain is therefore undoubtedly one of the most 
important parts of the brain in lampreys, though nothing is known in 
detail of its functions. Its cells control movements of the animal, by 
means of fibres that run to make connexion with the dendrites of the 
large Midler's cells, whose axons pass down the spinal cord; other 
fibres from the tectum opticum reach to various parts of the brain, 
and it is probable that its activities are closely correlated with those of 
many other regions. 

15. Skin photoreceptors 

Like many lower vertebrates the lamprey has light-sensitive cells in 
the skin, as well as those in the eyes. These receptors are abundant in 
the tail and if a light is shone on to this region the animal rapidly 
moves away (Figs. 74 and 76). If the spinal cord is cut just behind the 
head and a light then shone on to the tail, the head will be seen to 
move. This suggests that the impulses are carried forwards by means 
of the lateral line nerves, which is confirmed by the fact that if these 
latter are sectioned, leaving the spinal cord intact, then no movements 
follow when the tail is illuminated. This sensitivity of the lateral line 


organs to light is not found in other fish-like vertebrates. Indeed the 
receptors are not strictly lateral line organs but pigmented epidermal 
cells. The sensitivity curve shows a sharp peak at 530 m/x, this being 
the region of the spectrum at which light penetrates farthest into sea 
water. The pigment is probably a porphyropsin (Steven, 1950). 

In hag-fishes (Myxine) the head and cloacal regions are more 
sensitive to light than is the rest of the body. The impulses from the 
skin are conducted through the spinal nerves in these animals, not 
the lateral line nerves. 

16. Habits and life-history of lampreys 

We have very little information about the life of lampreys during 
the time that they are in the sea. They are caught in considerable 
number attached to other fishes. It is not known how many years a 
lamprey spends in the sea, but it returns only once to the river for 
spawning and dies after this act. The up-river migration of L. fluvi- 
atilis occurs in the autumn, for instance large numbers come up the 
River Severn and are caught in traps on the way, for use as food. The 
spawning migrations of lampreys may take them for hundreds of 
miles, for example, those of the eastern Pacific ascend to the head- 
waters of the Columbia River. They are said to perform remarkable 
feats of climbing, leaping from stone to stone and hanging on by their 
suckers. During this period of migration some lampreys assume 
brilliant orange and black colour patterns. On the other hand, lam- 
preys land-locked in the lakes of New York (Petromyzon marinus 
unicolor) feed in fresh water and ascend only a few miles up streams 
to breed. 

Once in the river the lampreys do not feed again but live over the 
winter on the reserves accumulated in the form of fat, especially under 
the skin and in the muscles. During the winter the gonads ripen pro- 
gressively and the secondary sexual characters begin to become appar- 
ent only in February. The females then develop a large anal fin, while 
in the male a penis-like organ appears (Fig. 47) and the base of the 
dorsal fin becomes thickened. 

Spawning occurs in the spring and is preceded by a form of nest- 
building. Numerous lampreys collect together, usually at a place 
below a weir where the water is shallow and rather swift, and the 
bottom both stony and sandy. Stones are then dragged by the mouth 
in such a way as to make a small depression. Fertilization is secured 
by a process of copulation in which the male fixes by the sucker on to 
the fore-part of the female and the two then become intertwined and 

iv. 1 6 



undergo rapid contortions, the eggs being squeezed into the water, 
while sperms are ejected through the 'penis' (Fig. 75). Fertilization 
is therefore external, but the sperms must be placed very close to the 

Fig. 75. Spawning lampreys seen in their nest. 
(After Gage.) 

eggs, for they remain active only for about one minute after entering 
the fresh water, which provides the stimulus that activates them. The 
eggs and sperms are not all laid at once; mating is repeated several 
times until all the products have been shed, after which the animals 
are exhausted and soon die. The movements of the animals stir up 
the sand in the nest (this is probably the function of the anal fin of 
the female) ensuring that the eggs are covered up as they are carried 
away by the current. 


17. The ammocoete larva 

The eggs contain a considerable quantity of yolk, but their cleavage 
is total and proceeds in a manner not unlike that of the frog. After 
about three weeks the young hatches as the ammocoete larva, about 
7 mm long. At first this is a tiny transparent creature, but its larval 
life lasts for a long time, during which it grows into an opaque eel-like 
fish, up to 170 mm long (Fig. 76). 

Fig. 76. Ammocoete larva of Lampetra planeri, showing the effect of shining a narrow 

beam of light on to various parts of the side of the body. Illumination of 1, 2, or 8 is 

followed by movement after a few seconds, but no movement follows illumination at 

points 3-7. (From Young.) 


Fig. 77. Young ammocoete larva of lamprey fixed while feeding on green flagellates 
and detritus and then stained and cleared. 

an. auditory sac; br. brain (covered by meninges); e. eye; end. endostyle \f.c. food cord in 
pharynx; h. heart; /. liver; m. mid-gut; oes. oesophagus; v. velar fold. 

This portion of life is spent buried in the mud, the animals emerg- 
ing only occasionally to change their feeding-ground, presumably if 
the mud is not sufficiently nutritious. There is no sucker, the mouth 
being surrounded by an oral hood rather like that of amphioxus (Fig. 
77). The paired eyes are covered by muscles and skin. The head at 
this stage is little sensitive to light, but the animal quickly begins to 
swim if the tail is illuminated. We have seen already (p. 108) that in 
lampreys there are photoreceptors in the tail, connected with the 
lateral line nerves. In the larva these are the main photoreceptors, and 
they ensure that the animal lies completely buried. 

If a number of larvae are left in a vessel with a layer of mud on the 

iv. i7 

r 2 3 


Fig. 78. Development of the endostyle of the lamprey. Sagittal sections through 

the head at three stages. 

1, auditory sac; 2, medullary tube; 3, myotome; 4, conus arteriosus; 5, endostyle; 6, first 

gill-slit; 7, first arterial arch; 8, notochord; 9, inpushings which cut off the endostyle from 

the pharynx; 10, aorta; 11, stomodaeum. (After Dohrn, from Kukenthal.) 

bottom they rapidly disappear and remain hidden indefinitely, the 
heads perhaps just visible in small depressions made by the rhythmic 
respiratory movements. When disturbed they always swim with the 
head downwards and in contact when possible with the ground. This 
habit leads them to burrow rapidly. It is not known whether they 
have other receptors to guide them to mud rich in possible food 
organisms. The nasal and hypophysial sacs are poorly developed in the 
larva, and the sense of smell can hardly serve this purpose. 




Fig. 79. A, Transverse section of endostyle of ammocoete larva. 

cav. cavity of the gland; cil.g. ciliated groove in floor of pharynx; lam. lamellae of gills; 
ph. cavity of pharynx; seer, mucus-secreting cells of the gland. 

b, Transverse section of thyroid follicles of adult. (After Young and Bellerby.) 

C, Cross section of endostyle of ammocoetes larva of Petromyzon tnarinus at level 
where it is connected by a duct to the pharynx. Autoradiograph showing distribu- 
tion of protein-bound I 131 . The radioactive clumps of cellular debris in the 
glandular lumen and in the duct suggest that the material represents a holocrine 
secretion, which will probably be absorbed in the intestine. 

d. duct; hs. cellular debris; ph. pharynx; t II d. type II dorsal cells; 
t III epithelial cells, 


Feeding takes place by the intake of water through the mouth and 
the separation of small food particles from it in the pharynx (Fig. 77). 
For this purpose there is used a great quantity of mucus, which is 
secreted by the endostyle and gathered into a strand by the cilia of 
the pharynx. This endostyle is a most remarkable organ, forming early 
in development as a sac below the pharynx (Fig. 78). It consists of a 
pair of tubes, on the floor of which there are four rows of secretory 
cells (Fig. 79). There is a single opening to the pharynx, by a slit 
at about the middle of the length. As development proceeds the inner 
rows of cells at the hind part of the organ become coiled upwards, and 
at the end of larval life the endostyle therefore forms a very large mass 
below the pharynx, composed of tubes lined partly by secretory and 
partly by ciliated cells. Probably no enzymes are secreted by the 
endostyle, its function being to produce mucus in which the food 
particles become entangled. Although it resembles the endostyle of 
amphioxus in the arrangement of the secretory columns, there is a 
difference in that the organ in the ammocoete larva is not an open 
groove. There is, however, a ciliated groove in the floor of the pharynx, 
that is to say, on the roof of the endostyle (Fig. 79). 

The details of the feeding-currents of the ammocoete larva are not 
understood. An important difference from the arrangement in am- 
phioxus is that the current is produced by muscular rather than ciliary 
action. The velum, a pair of muscular flaps, provides the main current 
when the animal is at rest. The branchial basket can also be expanded 
and contracted by an elaborate system of muscles. It is not easy to 
observe how the food particles are taken up from the current, but 
apparently a strand of mucus shoots from the endostyle and occupies 
the whole of the centre of the pharynx (Fig. 77). This strand probably 
rotates and as it passes backwards into the eosophagus it catches the 

Evidently the system enables the animals to feed efficiently on the 
small unicellular algae and bacteria of the mud. In amphioxus the 
ciliated pharynx, occupying a considerable proportion of the whole 
surface, is only able to support a tiny creature, but the muscular 
feeding-system of the ammocoete allows a relatively small pharynx to 
feed a fish 170 mm long and weighing up to 10 grams. This use of 
muscles for moving the gills was evidently an important step in 
chordate evolution. It allowed the animals to escape from the limita- 
tion of size imposed by the ciliary method of feeding. After the 
development of jaws to form a still more efficient feeding mechanism 
the rhythmic movement of the branchial apparatus persisted for the 


purpose of respiration. We cannot be certain about changes which 
occurred so long ago, but it seems likely that the respiratory move- 
ments of a fish were first introduced to provide food rather than 

The endostyle therefore shows the survival of the primitive feeding- 
methods of chordates, but it also undergoes at metamorphosis an 
astonishing change into a thyroid gland. The mucus-secreting columns 
shrink and the whole organ becomes reduced to a row of closed sacs, 
lying below the pharynx (Fig. 79 b). Each of these sacs is lined by an 
epithelium, contains a structureless 'colloid' substance, and is there- 
fore closely similar to a thyroid vesicle. Moreover, experiments have 
shown that extracts of this organ contain iodine and exert an accelerat- 
ing effect on the metamorphosis of frog tadpoles. Although nothing is 
known of the part played by the secretion of this gland in the life of 
the adult lamprey, we may safely conclude that we have here the 
conversion of an externally secreting feeding-organ into a gland, of 
internal secretion. The actual mucus-secreting cells are not trans- 
formed into those of the thyroid follicles, these latter are derived from 
epithelial cells in the wall of the larval organ. One cannot avoid specu- 
lating on this extraordinary change of function. It may perhaps be 
significant that the endocrine gland that regulates basal metabolism 
(the thyroid) is derived from the part of the feeding-system that in 
the earliest chordates was responsible for providing the raw materials 
of metabolism. Experiments with radioactive iodine show that this 
element is concentrated in certain cells of the larval endostyle (Fig. 
79 c). Moreover, after addition of the anti-thyroid substance thiourea 
to the water there are changes in the endostyle. Thyroxine has been 
extracted from the gland and it probably has an endocrine function 
as well as secreting mucus, though no one has ever produced any 
changes in larval lampreys by administering thyroid hormones. 
Lampreys thus show, as larvae, a stage in which the accumulation of 
iodoproteins, previously widespread, becomes concentrated in the 
pharynx. Perhaps at this site there were already cells specialized for 
halide transport (cf. the chloride-secreting cells of teleosts, used for 
osmogulation, p. 203). In adult lampreys and all higher chordates the 
iodoprotein is secreted into the blood under the control of blood- 
borne signals (Fig. 80). The change may well be related to develop- 
ments in the regulation of metabolism, which, in the animals with a 
fully endocrine thyroid becomes more nearly independent of varia- 
tions in the external supply of iodine. 

The great change in the endostyle is only part of the complete 



metamorphosis by which the ammocoete larva changes into an adult 
lamprey. The mouth becomes rounded and its teeth, tongue, and 
complex musculature develop. The paired eyes (previously buried) 
appear; the olfactory organ becomes internally folded, and the olfac- 
tory nerve and tracts much enlarged. The naso-hypophysial sac grows 
backwards to the gills. In the pharynx the gills develop into sacs 
opening to the branchial chamber. Changes also take place in the 


Fig. 80. Diagram to show distribution of iodoproteins, at first in exoskelctal struc- 
tures, as in many invertebrates and in tunicates (a). Some of this material is 
concentrated in the pharynx. This tendency is exaggerated in amphioxus and the 
ammocoete larva, and in the adult lamprey and later animals this pharyngeal 
material forms the thyroid. A. Many invertebrates and tunicates ; n. Amphioxus ; 
c. Ammocoetes; D. Metamorphosis of ammocoetes; e. General vertebrate type. 
(After Gorbmann, A., in Comparative Endocrinology. Wiley, New York.) 

intestine. The yellow-brown colour of the larva gives place to the 
black with silver underside of the adult. The animal more and more 
frequently leaves the mud and finally migrates to the sea to begin its 
parasitic life. 

18. Races of lampreys, a problem in systematics 

Besides the river lampreys, such as L. fliwiatilis (Linn.), which 
show this characteristic migratory life-history, there are also in various 
parts of the northern hemisphere small brook lampreys ('prides'), 
such as L. planeri Bloch, which remain throughout their life in fresh 
water. These prides are very abundant in many English rivers and 
streams, but since the greater part of their life is passed in the am- 
mocoete stage they are not often seen. The larvae remain in the mud 


probably for three years and undergo metamorphosis in late summer 
and autumn. The characteristic of this type of lamprey is that the 
adults never migrate and never feed. The gonads are already well 
developed at metamorphosis and ripen during the winter. Spawning 
takes place in March or April and the animals then die. 

There has been much dispute about the status of these freshwater 
races. In structure the adult L. planeri is nearly if not quite identical 
with an adult L.fiuviatilis, except that the latter is much the larger and 
has sharper teeth. Crossing of the two sorts could presumably never 
take place in nature, on account of the size difference, but by artificial 
stripping of the adults cross-fertilization in both directions can easily 
be achieved. Unfortunately the hybrid larvae have never been reared 
to maturity; we cannot therefore say whether the small size and 
failure to migrate of the planeri forms are inherited characters or 
are produced by the influence of the environment. The effect of the 
non-migratory condition is to enable the lampreys to colonize very 
fully rivers that, because of effluents, they would be unable to occupy 
if a migration to the sea was necessary. By this process of acceleration 
of the development of the gonads a dangerous stage in the life-history 
has been avoided. 

Similar pairs of migratory and non-migratory forms of lamprey are 
found in Japan and in North America. Indeed, the condition appears 
to be developing independently in several river systems in the United 
States. Since it may be difficult for the brook lampreys to spread 
from one river system to another it is possible that many of the 
planeri forms have evolved separately, perhaps quite recently. If so, 
this is a remarkable example of a similar response produced in different 
parts of a population by a similar environmental stimulus, in this 
case the effluents. This process of alteration in the relative times of 
metamorphosis and sexual maturity (paedomorphosis) has occurred 
also in certain amphibians (the axolotl) and in tunicates (Larvacea). 
Similar changes in rates of development may have been essential 
factors in the development of the whole chordate phylum (p. 77). 

In one race, found in Italy, ammocoetes with mature gonads have 
been reported. However, in most of these lampreys the paedomor- 
phosis is only partial : metamorphosis does take place, but is immedi- 
ately followed by maturity. Since in mammals injections of anterior 
pituitary extracts accelerate development of the gonads, it was thought 
possible that complete neoteny might be produced by making such 
injections into larvae of L. planeri. No completely sexually mature 
ammocoetes have yet been produced by this method, but following 


the injections the larvae assumed the secondary sexual characters, 
which are normally shown only at maturity, namely, swelling of the 
cloaca, opening of the pore from coelom to exterior, and the changes 
in body form. No signs of metamorphosis were produced by these 
injections and we are left without information as to the cause of that 
change in the lamprey. In Amphibia even very young larvae undergo 
metamorphosis when treated with thyroid extracts, but similar treat- 
ment of ammocoete larvae has failed to produce any change. Further 
investigation of the problem should be very interesting, since it seems 
likely that the differences between the fluviatilis and planeri forms are 
the result of an endocrine factor accelerating the onset of sexual 
maturity in the latter. The fact that the change is occurring in various 
parts of the world adds further interest to this example of evolution 
in progress. 

Besides all these relatively small lampreys, there is a much larger 
form, the sea lamprey, Petromyzon marinns Linn., reaching to over a 
metre in length. This animal differs from Lampetra in body form, 
structure of sucker, and other features, as well as in size. Like most 
other groups of animals lampreys therefore present several problems 
of nomenclature. Linnaeus included the three types that occur in 
Europe in the one genus Petromyzon ; since they are all rather alike in 
shape this is in some ways a reasonable procedure. But are we then 
also to include in the same genus forms that differ more widely, such 
as those occurring in the southern hemisphere ? As so often happens, 
systematists have chosen the course of splitting up the Linnaean 
genus, even though several of the resulting genera have only one 
species. Thus Gray suggested the genus Lampetra for the brook and 
river lampreys, keeping Petromyzon for the larger species of sea 
lamprey. Other genera have been added, such as Entosphenus Gill for 
some of the North American forms and Mordacia Gray and Geotria 
Gray for the forms from the southern hemisphere (Chile, Australia, 
and New Zealand). Such distinctions, though they may seem irritating 
at first sight, are an advantage in that they call attention to the differ- 
ences which exist. For instance, it is a striking fact that lampreys are 
found in temperate waters of both hemispheres, but not in the tropics, 
and it is interesting to learn that the forms from New Zealand, 
Australia, and South America (there are none in South Africa) show 
distinct peculiarities. Thus Geotria possesses a large sac behind the 

A special problem of nomenclature arises from the fact that the 
river and brook lampreys are almost identical in structure and differ 


mainly in size, time of sexual maturity, and habits. A further com- 
plication is that the germ-cells of the two races allow cross-fertiliza- 
tion, although this probably never occurs in nature! We may take 
Dobhzansky's definition of species as 'groups of populations which 
are reproductively isolated to the extent that the exchange of genes 
between them is absent or so slow that the genetic differences are not 

Fig. 8i. Myxine, partly dissected. 

i, cloaca; 2, testis; 3 and 4, ovary with eggs; 5, liver; 6, branchial opening; 7, mouth; 
8, nostril; 9 and 11, slime glands; 10, intestine. (After Retzius, from Kukenthal.) 

diminished or swamped', and in this sense we may retain the specific 
names L. fluviatilis and L. planeri for the two populations. 

19. Hag-fishes, order Myxinoidea 

The hag-fishes, Myxine and Bdellostoma (Fig. 8 1 ), are animals highly 
modified for sucking. They live buried in mud or sand and probably eat 
polychaetes and other invertebrates, as well as scavenging dead fishes. 
The eyes are functionless rudiments, though the animals are sensitive 
to changes of illumination, through skin receptors. There are sensory 
tentacles around the mouth, and in both hag-fishes the teeth and 
sucking apparatus are well developed. They burrow into the bodies 
of dead or dying fishes. As many as 123 Myxine have been taken from 
a single fish. Since the introduction of trawling they have become less 
common in the North Sea, where they used to be a serious source of 
loss to fishermen by their attacks on fishes caught in drift nets or on 
lines. They seem to find fish when they are dying or just dead, and 
entering by the mouth of their prey eat out the whole contents of the 
body, leaving a sack of skin and bones. When they are themselves 

IV. 19 



caught on lines (for instance, with a salted herring bait) the hook is 
swallowed so deeply that it may be found near the anus! 

The gills are modified into pouches (6-14 in Bdellostoma, 6 in 


Fig. 82. Arrangement of gills in Bdellostoma and Myxine. 

1, tentacles; 2, wall of pharynx ; 3, branchial sac opened to show gill lamellae; 4, branchial 

duct; 5, branchial sac; 6, mouth; 7, common branchial aperture in Myxine. 

(From Kukenthal after Dean.) 

Myxine), opening by tubes into the pharynx, and to the exterior (Fig. 
82). In Myxine all the tubes are joined and open by a single posterior 
aperture on each side. Water enters at the nostril and is pumped back- 
wards by a muscular velum through the gill chambers and out behind. 
There is also a single posterior oesophago-cutaneous duct on the left 
side, which is probably closed during normal respiration but is 
opened to allow expulsion of large particles. If the nostril is closed 
experimentally with a plug no water enters by the mouth or posterior 
apertures but the fish survives well, presumably respiring through the 


The thyroid gland consists of a long series of sacs formed by 
evagination from the floor of the pharynx. 

Down the sides of the body are pairs of slime glands, able to secrete 
large amounts of mucus, which may be protective and is said also to 
be produced under the operculum to hasten the end of a dying fish 
that the hag has attacked. 

A curious difference from the nervous system of lampreys is that 
the dorsal and ventral roots join, though the details suggest that the 
union is not similar to that found in gnathostome vertebrates. The 
brain shows several features of reduction and simplification and no 
pineal eyes are present. There is only one semicircular canal in the ear 
(p. 109). The kidneys show a more generalized condition than in any 
other vertebrate in that the pronephros persists in the adult and is 
hardly marked off from the mesonephros, so that an almost continu- 
ous series of funnels and glomeruli can be recognized. Moreover, there 
is a regular series of mesonephric glomeruli, a pair in each segment. 

The development is known only in Bdellostoma, where the egg is 
yolky and cleavage partial, leading to the formation of an embryo 
perched on a mass of yolk. It is often stated that Myxine is a protandric 
hermaphrodite, because individuals are found in which the front end 
of the gonad contains eggs, whereas the hind part is testis-like (Fig. 
81). No ripe sperms have ever been found in this region, however, 
and, moreover, individuals with fully testicular gonads do occur. 
Since it is known that in other vertebrates (including the lampreys) 
the gonads go through a hermaphrodite stage during development it 
seems likely that Myxine is not a functional hermaphrodite but that 
the double-sexed gonad shows a rather late persistence of the indeter- 
minate stage. 

The hag-fishes all live in the sea and their blood differs from that of 
other chordates in that it is isosmotic with sea water. However, the 
individual ions are regulated; sodium and phosphate exceed their 
values in sea water, and the other ions are present in lower concentra- 
tion. It is usually assumed that fishes, with their glomerular kidneys, 
evolved in fresh water. However, the very earliest fragments of 
armoured agnathans are from Ordovician deposits that may be littoral 
or marine and it might be that the condition of the blood and kidney 
of Myxine is that of the earliest agnathans and that the glomerulus was 
not evolved as an adaptation to freshwater life, as is often supposed 
(Robertson, 1954). 

The organization of the lampreys and hag-fishes shows that they 
preserve many characteristics from a very early stage of chordate 

IV. 20 



evolution, probably that of about the Silurian period. Their special 
interest for us is in giving an insight into the organization possessed 
by the vertebrates before jaws were evolved. However, no doubt many 
changes have gone on during cyclostome evolution and we must not 
suppose that all Silurian vertebrates were like lampreys. Indeed, we 
may now complete our picture of this stage of evolution by examining 
the fossil fishes known to have existed at that period. We shall find 
them superficially so different from modern cyclostomes that only 
careful morphological comparison reveals the similarities. The inquiry 
will show us once again how a common plan of organization can be 
found in animals of very different superficial form and habits. 

Fig. 83. A ccphalaspid restored (Hemicyclaspis). 

d. dorsal fin; bf. lateral field; pec. pectoral fin; p. pineal; sclr. sclerotic ring. 
(From Stcnsio.) 

20. Fossil Agnatha, the earliest-known vertebrates 

The ostracoderms are fossil forms from freshwater Silurian and 
Devonian deposits. They are therefore the oldest fossil vertebrates 
known to us (except for a few Ordovician fragments), and this makes 
it specially interesting that they show affinity with the cyclostomes. 
These are fossils that are rarely found complete, particularly the 
pteraspids, but a quarry in Herefordshire yielded numerous whole 
specimens of Cephalaspis and Pteraspis of Old Red Sandstone age, 
probably all from a single dried-up pool. 

In the cephalaspids (Osteostraci) the head was flattened and com- 
posed largely of a shield. The rest of the body was fish-like, with an 
upturned tail (heterocercal, see p. 136) covered with heavy bony scales 
(Fig. 83). A pair of flaps behind the gills may have functioned like 
pectoral fins. 

On the dorsal surface of the shield are two median holes, one 
behind the other, which served a naso-hypophysial opening and a 
pineal eye. The whole outline of the cranial cavity is preserved and 
shows a brain remarkably like that of a lamprey, with a naso-hypo- 
physial canal below it (Fig. 84). There were paired eyes and only two 


Fig. 84. Head shield of the ccphalaspid Kiaeraspis, see from below. 5 X natural size. 

car. a. internal carotid; dorsal aorta; 4. 4th efferent branchial; efferent branchial 

of 1st arch; 1st interbranchial ridge; oes. oesophagus; orb. depression made by orbit; vest. 

depression made by vestibular apparatus. V1-X2. Cranial nerves. 

(After Stensio.) 

hup. foss 


■ C3p tat 


Fig. 85. Cast of the endocranium and system of canals in the head shield of Kiaeraspis. 
amp. ampulla of posterior semicirculr canal; can. canal leading to field; car. a. carotid artery; 
hyp.foss. hypophysial fossa; /./. lateral 'electric' fields; med. medulla oblongata; nas.c. naso- 
hypophysial canal; orb. orbit; vena capitis lateralis; vest, vestibular apparatus; III-X 

cranial nerves. (After Stensio.) 

iv. 2 o CEPHALASPIDS 127 

semicircular canals. Long tubes leading through the shield contained 
the cranial nerves, which can be reconstructed in detail (Fig. 85). 
On the under side of the shield is a series of ridges, which outline a 
set of ten pairs of branchial pouches. The first of these lies far forward 
at the sides of the mouth and the ridge in front of it is probably the 
premandibular arch; it carries the profundus nerve (p. 152), which 
was large. The ventral surface of the head was flat and covered with 
small scales. Probably the gills were pouches, as in lampreys. The 
canals of the aorta, epibranchial arteries, and some features of the veins 
and heart have been preserved. 

The mouth was a slit at the extreme front end with which the 
animals may have scooped decaying matter from the lake floor. 
On the dorsal surface there are sunken areas, covered by small scales, 
known as the median and lateral fields, and supposed by some to have 
contained electric organs. They were apparently served by a very rich 
blood-supply and a system of wide canals leads to the vestibular 
region. These canals might have contained nerves, but Watson makes 
the far more likely suggestion that they housed tubular extensions of 
the labyrinth and served to carry pressure waves to the ear, perhaps 
providing a substitute reinforcement for the defective lateral line 

We therefore know in some respects as much about these fossils as 
of many living fishes. They show in the complete segmentation of the 
head the most primitive condition known among craniates. Many of 
their features are very like those of modern lampreys and there can be 
little doubt that, as Stensio suggests, the latter represent their sur- 
viving descendants, which have lost the bony shield. 

The Anaspida (mostly Silurian) are placed by Stensio near the 
Cephalaspids but they are less well known. They were small fishes 
(up to 7 in. in length) covered with rows of bony scales (Fig. 87). The 
tail shows a lower lobe larger than the upper ('hypocercal'). This 
would presumably serve to drive the head end upwards perhaps to 
compensate for the weight of its armour. The opposite ('heterocercal') 
condition, found in cephalaspids and many modern fishes (for 
instance, the dogfish), produces a tendency to negative pitch and is 
associated with the presence of pectoral fins (p. 136). The anaspids 
possessed a curious ventral or ventro-lateral fin fold (Fig. 87) or 
perhaps a series of them. There were large paired eyes, median holes 
presumed to be nasal and pineal and a series of up to fifteen small 
round gill openings. 

We may consider here the fossil Jamoytius from the Silurian. The 


notochord was persistent and there was no calcined endoskeleton. 
There were long continuous lateral fin folds and a hypocercal tail. A 
series of transverse structures were at first interpreted as myotomes 






Figs. 86 and 87. Anaspids seen in dorsal and lateral views. 

an. anal fin; na. nasal aperture; orb. orbit; pec. pectoral spine; pi. pineal foramen; 
ros. rostrum; sc.d. dorsal scales. (After Stensio and Kiaer and Grasse.) 

but Stensio and Ritchie (i960) consider these to be scales and place 
Jamoytins with the Anaspida. In either case, the form is of the greatest 
interest, and represents as White says 'the most primitive of the 
"vertebrate" series of which we have knowledge'. It is suggested that 
it might be the ammocoete larva of an ostracoderm (Newth). 

The Heterostraci are actually the oldest known craniates, since their 
scales occur in the Ordovician. They were common in the Silurian 

IV. 20 



and lower Devonian. There were ventral as well as dorsal shields (Fig. 
88), and a long series of gill pouches, but only a single pair of exhalent 
branchial apertures, suggesting to Watson respiration by a moving 
flap (velum). The shields were of cell-less bone (isopedin) covered 
with dentine. The body was covered with scales of similar material. 
The tail was hypocercal and there were lateral horizontal keels but 
no fins. Theie were paired eyes, two semicircular canals and clearly 

Fig. 88. Three views of a restoration of Pteraspis. 
d.sp. dorsal spine; e. eye; m. mouth; r. rostrum. (From White.) 

marked lateral line canals. There was a pineal opening, closed in the 
adult, but no sign of the nostril, which may have opened into the 
mouth. The latter was surrounded by long plates, suggesting that it 
formed a protrusible apparatus, which could be pushed out to form 
'a kind of scoop or shovel (Fig. 88) whereby mud and decaying refuse 
could be taken off the bottom, for it seems likely that such were their 
food and habit' (White). 

The coelolepids or thelodonts are the least known group of agna- 
thans. The outer surface was covered with fine, placoid-like scales or 
hollow spines, which in isolation are often found in late Silurian and 
Early Devonian rocks. The anterior end was usually flattened and 
wide but the body behind was narrow, with a forked, probably 
hypocercal tail. Structures that are probably eye-spots occurred 
widely separated near the front margin. The mouth was ventral and 
traces of seven branchial arches have been found. There were flap-like 


extensions on each side of the head but no paired fins. The only 
median fin was the anal. 

The affinities of these ostracoderm fossils with each other and with 
the cyclostomes have been much disputed. Lankester claimed that 
pteraspids were related to cephalaspids 'because they are found in the 
same beds, because they have a large head shield and because there is 
nothing else with which to associate them'. At the other extreme 
Stensio holds that we have sufficient evidence to assert that the 
pteraspids have given rise to the myxinoids, and the cephalaspids to 
the lampreys. Except for the absence of jaws there is indeed little in 
common among the fossil forms. The differences in the shape of the 
tail are especially baffling. As White points out, an animal with a 
heterocercal tail and pectoral fins can hardly have lost either of these 
organs independently. He suggests that the earliest vertebrates pos- 
sessed straight ('diphycercal') tails and that from these were evolved 
on the one hand the pteraspids with hypocercal tails and on the other 
the cephalaspids with upturned heterocercal tails. The modern cyclo- 
stomes are perhaps derived from the latter, but which, if either, group 
gave rise to the earliest gnathostomes is unknown. 

The Agnatha were the first animals of the chordate type to become 
large, and they apparently all did so by feeding on the detritus at the 
bottom of rivers and lakes. They evolved into various types, mostly 
rather heavily armoured and perhaps slow-moving forms. The lam- 
preys and hag-fishes have been derived from early Agnatha by the 
evolution of a sucking mouth, perhaps with loss of the bony skeleton 
and paired limbs. However, it was the unknown forms that evolved 
a biting mouth that made the next great advance in vertebrate 



1 . The elasmobranchs : introduction 

In all parts of the sea there are to be found members of the class of 
the elasmobranchs (literally 'plate-gilled' fishes), including sharks 
ranging from monsters of 50 ft long to the common dogfish Scylio- 
rhinus caniculus of 1-2 ft. Nearly all the fishes in the group are carni- 
vorous or scavengers: the skates and rays are bottom-living relatives, 
feeding mostly on invertebrates. Although they are not quite so fully 
masters of the water as are the bony fishes, they are yet well enough 
suited to that element to survive in great numbers in all oceans. 
Perhaps the skill and cunnning of a shark is exaggerated by the 
frightened boatman or bather, who is apt to mistake a keen nose and 
the persistence of hunger for intelligence, especially when he is faced 
at intervals with a well-armed mouth; but the sharks have a large 
brain and their active, predacious habits enable many of them to 
live by eating the more elaborately organized bony fishes. 

Evidently such active creatures have changed considerably if they 
have been evolved from the heavily armoured and probably slow- 
moving agnathous vertebrates that shovelled up food from the bottom 
of Palaeozoic seas. It used to be supposed that these elasmobranch or 
cartilage fishes represent a very primitive stock, but we now realize 
that there have been great changes since the biting mouth was first 
evolved; we cannot be sure that any features we find in the elasmo- 
branchs were possessed by the earliest gnathostomes. 

The typical shark is a long-bodied fish, swimming by the passage of 
waves of contraction along tne metamerically arranged muscles. As in 
the lampreys and eels, the wave that passes down the body is of short 
period, relative to the length of the fish, and is therefore evident as it 
travels along. This is probably a less efficient system than is provided 
by the longer period waves of the most highlv developed bonv fishes; 
the sharks are good swimmers, but except for the mackerel sharks 
(Isuridae) not among the swiftest. Stability and control of direction 
are ensured by the upturned tail and the fins. The tail, with its dorsal 
lobe larger than the ventral, is called heterocercal, and tends to drive 
the head downwards. This is corrected by the flattened shape of the 
head itself and by the pectoral fins, which act as 'aerofoils', allowing 


steering in the horizontal plane (p. 140). There are two dorsal fins, 
which secure stability against rolling, and also assist in making possible 
the vertical turning movements. 

The muscles for the production of these movements are a serial 
metameric set, with longitudinal fibres, essentially like those of the 
lamprey or amphioxus. The central axis is no longer simply a rod; 
the notochord has become surrounded and partly replaced by a series 

df f s P .by Ld 



msv. pr b. 

Fig. 89. Diagram of the organization of a vertebrate. 

ac. wall of abdominal coelom ; b. body wall ; bd. basidorsal ; bv. basiventral ; bw. body wall ; dr. dorsal 

rib; i. intestine; iv. interventral; m. myocomma; ms. mesentery; msd. median dorsal septum; msv. 

ventral mesentery; nes. neural tube; ns. notochordal sheath; pr. ventral (pleural) rib; sp. neural 

spine; ts. horizontal septum. (From Goodrich.) 

of vertebrae (Fig. 89). These develop as two pairs of cartilaginous 
nodules in each segment, the basidorsals and basiventrals behind, and 
smaller elements, the interdorsals and interventrals, in the front. The 
basiventrals, lying on either side of the notochord, form the centrum 
of each vertebra, invading and almost interrupting the notochord, 
which widens again, however, between the vertebrae. The vertebrae 
are held together by ligaments, but are not articulated by complex 
facets as they are in land animals. The basidorsals form neural arches 
above the nerve-cord, and the interdorsals make intercalary arches. 
The interventrals partly separate the centra. Attached to each basi- 
ventral is a pair of transverse processes, which in the anterior region 
bear short ribs and in the tail are fused in the midline to make the 
haemal arches. 

The median and paired fins are supported by cartilaginous rods, 
the radials, and their edges are further strengthened by special horny 



rays, the ceratotrichia. The radials of the paired fins form a series 
attached to larger rods at the base. These more basal rods are attached 
to a 'girdle' of cartilage embedded in the body wall. The pectoral 

Fig. 90. Successive positions of a swimming dogfish at intervals of o-i sec. The 
lines are 3 in. apart. The passage of a wave is marked by dots. (After Gray.) 

Fig. 91. Successive positions of a swimming eel at intervals of 005 sec. Scale 3 in. 
The wave-crests are marked. (After Gray.) 

girdle is a hoop extending some way round the body, but the pelvic 
girdle is simply a transverse rod in the abdominal wall. The origin of 
these girdles and of the fins will be discussed later (p. 136). 

2. The swimming of fishes 

The propulsive forces that move a fish through the water are usually 
produced by the longitudinal muscle-fibres of the myotomes, but in 
some forms the propulsion is produced by movement of the fins, 
whose function is usually rather to give the fish its stability, enabling it 
to keep on a constant course, and also to change its course. 


The myotomes consist of blocks of longitudinal muscle-fibres, 
placed on either side of an incompressible central axis, the notochord 

or vertebral column. The effect of 
contraction of the muscle-fibres in any 
myotome is therefore to bend the body. 
In forward swimming the contraction 
of each myotome takes place after that 
in front of it. In this way waves of 
curvature are passed down the body, 
alternately on each side. This can be 
illustrated by a series of photographs 
of a fish such as the dogfish or eel in 
which the amplitude of the waves is 
large (Figs. 90 and 91). 

In other fishes the waves are not so 
immediately obvious, but serial photo- 
graphs show that even in such forms as 
the mackerel and whiting there is a 
backward movement of waves. The 
number of waves per minute in steady 
swimming varies from 54 in the dog- 
fish to 170 in the mackerel, the 
corresponding velocities of the waves 
being 55 and 77 and of the whole fish 
29 and 42-5 cm /sec. 

Gray has shown how the muscle 
contractions produce movements of 
the parts of the body, related to one 
another in such a way as to transmit 
a backward momentum to the water. 
Fig. 92 shows superposed drawings of 
an eel, made from successive photo- 
graphs. The region marked XY is 
moving from right to left and that 
X 1 Y 1 from left to right and evidently, 
as Gray puts it, 'all parts of the fish's 
body which are in transverse motion have their leading surfaces directed 
backwards and towards the direction of transverse movement, but 
the angle of inclination is most pronounced when the segment is 
crossing the axis of longitudinal motion, and at this point the segment 
of the body is travelling at its maximum speed. Each point of the body 

Fig. 92. Enlarged drawings of suc- 
cessive photographs of a young eel 
superimposed on each other so that 
the tips of the head are on the same 
transverse axis and the longitudinal 
axes of motion (ab) are made to 
coincide. As the wave passes the 
section XY it first moves to the left 
and is directed backwards and to 
the left, whereas X x Y\ moves 
in the opposite direction. The tip 
of the tail follows a figure of 8. 
(From Gray) 


is travelling along a figure 8 curve relative to a transverse line which is 
moving forward at the average forward velocity of the whole fish. 
The track of any point on the body (relative to the earth) is a sinu- 
soidal curve whose pitch or wave length is less than that of a curve 
which defines the body of the fish. There is therefore a definite angle 
between the surface of the fish and its path of motion.' 

Each portion of the side of the fish can thus be considered as moving 
like the blade of an oar used for sculling at the back of a boat. The 
principle used, that of an inclined plane, is the same as in screw pro- 
pulsion, the essential feature being that the moving surface is inclined 
at an angle to its line of motion. The effect of the movement is greatly 
increased by the fact that the amplitude of the oscillations grows 
passing backwards, as is necessary to produce additive effects in any 
coupled system of screws or turbines. The whole fish thus operates 
as a single self-propelling system. 

The magnitude of the forward thrust thus generated depends 
among other things on (a) the angle that the surface of the fish makes 
with its own path of motion, (b) the angle between the surface of 
the fish and the axis of forward movement of the whole fish, and 
(c) the velocity of transverse movement of the body (Gray). These are 
evidently factors that will vary with the shape of the body and the 
action of its muscles. The body form of the faster-moving types of 
bony fishes provides substantial advantages for swimming over that 
of the more elongated types. The essential differences are that the 
bony fishes have (1) large caudal fins, (2) a much smaller length of the 
body relative to its depth, (3) less flexibility. 

The role of the large caudal fin is to resist transverse movements; 
its effect is, again quoting Gray, 'to keep the leading surface of the 
body directed obliquely backwards during both phases of its trans- 
verse movements and thereby to exert a steady pressure on the water'. 
Since, however, the tail does execute transverse movements, and at 
the same time is being rotated towards and away from the axis of 
motion, it exerts a very large propulsive effect, probably as much as 
40 per cent, of the total thrust. 

The effect of the caudal fin, combined with the shortness of body 
and reduced flexibility, is that the front part of a bony fish makes only 
small transverse movements; the track of the head is therefore nearly 
straight and the whole front of the body presents a streamlined 
surface with little resistance. Further, the muscles just in front of the 
tail exert their tension with very little change in length. 

No doubt the shape of the body also has an important influence on 


the effect of the fish on the water and hence on the turbulence in the 
flow of water and the resistance that must be overcome. Gray has 
shown that in a dolphin the resistance cannot be that of a rigid model 
towed at the speed at which the animal moves, since this would require 
that the muscles generate energy at a rate at least seven times greater 
than is known in the muscles of other mammals. By watching the 
flow of particles past the body of fish-like models he showed that 
movements such as those produced in swimming accelerate the water 
in the direction of the posterior end, and this would greatly reduce 
the turbulence. 

Something is known of the nervous mechanism responsible for the 
production of the swimming waves. An eel can swim if its whole skin 
has been removed. If a region of the body is immobilized by a clamp, 
swimming waves can pass along. Therefore the rhythm is determined 
by some intrinsic activity of the spinal cord and not by any mechanism 
such as proprioceptor impulses arising in active muscles and causing 
others to contract. 

Experiments in which the spinal cord was cut across show that in 
the eel the rhythm is only initiated when suitable impulses reach the 
cord either from spinal afferents or from the brain. Thus the spinal 
eel can be made to swim either by fixing a clip on to its caudal fin or by 
electrical stimulation of the cut end of the spinal cord. Though the 
cord requires such afferent stimuli for its functioning, they do not 
determine the frequency of the rhythm, which bears no relationship 
to that of the applied stimuli. 

In the dogfish the isolated spinal cord is able to initiate rhythmic 
swimming. After transection behind the brain the posterior portion 
of the fish exhibits continuous swimming movements for many days. 
Light touch on the sides of the body inhibits these movements, but some 
sensory impulses are necessary for their initiation; after complete de- 
afferentation, by section of all the dorsal roots, the movements cease. 

The information available does not yet enable us to understand 
fully how the swimming rhythm is initiated and maintained, nor how 
it is influenced by the brain. It would be very interesting to have 
further knowledge on these topics, especially because the locomotor 
rhythms of land animals are probably based on the serial contractions 
of their fish ancestors. 

3. Equilibrium of fishes in water ; the functions of the fins 

Making use of the methods of investigation of aeronautical engineers, 
studies have been made of the forces that operate to keep a fish stable 


as it moves through the water, or allow it to become temporarily un- 
stable and hence to change direction. Instead of attempting to study a 
living or dead fish moving in water, Harris made models and supported 
them in a wind-tunnel in an apparatus suitable for measuring the 
forces at work in the various directions. Such a method, in which no 
compensating movements of the fins are allowed, makes it possible 
to investigate the so-called 'static stability' of the fish, that is to say, 

Fig. 93. Diagram of model of the dogfish Mustelus, showing the conventional terms 
for describing deviations of motion. The longitudinal axis X is that of the wind 
tunnel and Y (horizontal) and Z (vertical) are at right angles to it. The arrows show 
the directions known as positive rolling, pitching, and yawing, which occur about the 
X, Y, and Z axes respectively, a. is the angle of attack between the axis of the model 
and the X axis. (From Harris, J. exp. Biol. 13.) 

to see whether the body and fins are so shaped as to provide forces 
that tend to bring the fish back into its previous line of movement after 
it has deviated in any direction. Any body such as a fish or aeroplane 
is said to be in stable motion if when it veers slightly from its line of 
progress the new forces produced upon its planes tend to restore the 
original direction of motion. 

The forces acting on the fish are measured along three primary axes, 
longitudinal, horizontal, and vertical. Deviation from the line of 
motion about the longitudinal axis is known as rolling, about the 
transverse axis as pitching, and about the vertical axis as yawing 
(Fig. 93). The forces along these three axes are known as drag, lateral 
force, and lift. 

In order to discover the effect of the median fins and tail on the 
stability, these fins were removed, the heterocercal tail being replaced 
by a cone having the same taper as the actual caudal fin. The model 
was then placed in the wind-tunnel with a wind at 40 m.p.h., which 


corresponds to a motion of 3 m.p.h. in water. The lateral force was 
measured when the body was made to yaw at various angles. The 

+ 0-1 

-15 -ipl^^ f 



+5° +10° +15° 


+ 5" oX S+Yo° +iV 

+ 6 


+ 05 








+5° +10* 








Fig. 94. A. Results of yawing test on model of Mustelus without fins. The lateral force 
is plotted as a light full line, drag force as a light broken line; yawing moment about 
centre of gravity as full heavy line. Abscissae show the angle of attack in degrees, 
ordinates the lateral force and drag in pounds weight, yawing moment in in. -lb. X ^j. 
n. Yawing test similar to (a) but with the fins behind the centre of gravity in place. 

C. Yawing test with all median fins in place. 

D. Pitching test on model of Mustelus with all fins intact and pectoral fins set at an 
angle of incidence of 8°. Lift force is shown as a light full line, drag force as a light 
broken line, pitching moment about the centre of gravity as a heavy full line. 

(From Harris.) 

results showed that the equilibrium in this plane is quite unstable; a 
slight turn off the direct course would produce a turning moment 
tending to increase still further the deflection (Fig. 94). This is a 
well-known property of all airship hulls, and is known as the 'unstable 
moment' of the hull. It is corrected in the airship by the addition of 


suitable horizontal and vertical fin surfaces at the rear end, when the 
airship becomes in effect a feathered arrow. The forces operating on 
the fins tend to bring the body back into the original line of motion. 
The fins of the fish operate in a similar manner. If the experiment 
is performed with a model to which all the fins behind the centre of 
gravity have been added, namely, the caudal, anal, and second dorsal 
fins, it is found that the curve for the yawing moment now has a steep 
negative slope (Fig. 94 b), that is to say, every deviation produces 
forces that tend to give directional stability. With the first dorsal fin 
also in position the model possesses a remarkable neutral equilibrium 
(Fig. 94 c). Deviations by as much as io° produce no resultant yawing 
moment about the centre of gravity. The form of the dorsal fins is 
therefore definitely such as to maintain stable swimming and prevent 

Turning of a fish is produced either by the propagation of a wave- 
down one side only of the body or by asymmetrical braking with the 
pectoral fins (see below). The former type of turn has been investi- 
gated by Gray in the whiting, where there is a large caudal fin. This 
gives great lateral resistance, so that the first part of the turn is 
executed by bending the front part of the fish on the tail as a fulcrum. 
This enables the animal to turn through 180 within a circle of the 
diameter of its own length. After removal of the caudal fin the turns 
are much less effective. 

In both elasmobranchs and teleosts the dorsal fins are well developed 
in the active swimmers. In most elasmobranchs they are fixed, but in 
many teleosts the dorsal fin can be folded up and down, and it is 
observed that the fin is raised during turning. This would have the 
effect of increasing the yawing moment produced by asymmetrical 
action of the body muscles or by unilateral braking with the pectoral 

Since the body is so markedly flexible in the lateral plane and there 
are powerful muscles available for turning it in this direction,. the part 
played by the fins in determining the stability is important mainly 
when the body is held straight. The fish thus has the double advantage 
of great stability (by keeping the body straight) and great control- 
lability (by bending it). In a body unable to change its shape in this 
way, stability and controllability would be inversely related. This is 
the case for the stability of the fish in the vertical plane, in which the 
body is little flexible. Fig. 94 n shows the positive slope of the curve 
for the pitching moment and clearly the equilibrium in this plane is 
quite unstable. The pectoral fins contribute more than any others to 


movement in this plane, and since they lie in front of the centre of 
gravity they greatly increase the instability. The fish must be able to 
alter direction in the vertical plane, and it has apparently sacrificed 
static stability for controllability. The equilibrium in this plane is a 
dynamic one, controlled by the movable pectoral fins, and it is so 
unstable that only a small movement of these fins is necessary to 
produce a deflecting force that restores the original direction of 

The pectoral fins, lying in front of the centre of gravity, tend to 
produce a movement of positive pitch, that is to say, they force the 
head upwards. This effect is normally compensated by a component 
produced by the heterocercal tail. The upper lobe of this is rigid and 
the lower more flexible, therefore the lateral motion given by the 
swimming movements of the body produces a vertical lift force on the 
tail, giving, of course, negative pitch. After amputation of the hypo- 
caudal lobe and anal fin a dogfish swims continually along the bottom 
of the tank : in order to compensate for the absence of negative pitch 
the pectoral fins are held horizontally and hence there is no moment 
to counteract the weight of the fish. If the pectoral fins are then also 
removed the anterior end of the body is pointed upwards, often so 
much so as to cause the fish to swim with its head out of the water. 
This is the result of an over-strenuous attempt to compensate, by 
raising the head, for the negative pitch produced by the tail. The 
system is no longer suitable for making the continuous adjustments 
necessary to ensure stability. 

This analysis makes it clear why a heterocercal tail is found in 
almost all the primitive swimming chordates; it is almost a necessity 
for an animal with a specific gravity in excess of the medium and little 
flexibility in the vertical plane. The component of positive pitch 
could be provided by the flattened head or by continuous lateral fin 
folds, such as may have been present in early fishes, and adjusted 
by the limited flexibility possible in the fin. The development of 
movable pectoral fins confers much greater control. Since the useful 
portions of a fin fold for this purpose would be those well in front of 
and behind the centre of gravity, we can perhaps see the reason why 
the intervening portion has become lost. In the modern sharks the 
pelvic fins have little influence on the stability and are perhaps retained 
only for their modification as claspers. 

It is not surprising that races of fishes with stability ensured by 
systems of this sort should tend to adopt a bottom-living habit, with 
dorso-ventral flattening, such as is found in the skates and rays. 

v. 4 



Expansion of the front end is developed at first to compensate the 
effect of the tail, but the pectoral fin becomes expanded to allow ver- 
tical adjustments and then reduction of the hypocaudal lobe of the tail 
accompanies the adoption of life on the sea bottom. Eventually all 

Fig. 95. Development of denticles in the dogfish. 

A and b, first gathering of odontoblasts (sc.) below the basement membrane (brn.); ml. are the 

epidermal cells that will become modified, c, first deposition of dentine (d.). In D there is 

more dentine and a pulp cavity (p.) is seen. In E are shown stages in the formation of enamel 

(e.) and of the basal plate (bp.) while the denticle cuts the epidermis (ep.). 

(From Goodrich, Vertebrata, A. & C. Black, Ltd.) 

locomotion is produced by undulatory movements of the fins, which 
were at first used only to raise the fish off the bottom. 

4. Skin of elasmobranchs 

Being swift and predatory animals, more attackers than attacked, 
the sharks do not possess a very heavy external armament. The skin 
itself is tough, being covered by layers of epidermis. Beneath this is a 
thick dermis of connective tissue with fibres arranged at right angles 


as in a carpet, giving a tissue of great strength and flexibility, able to 
maintain the shape of the body. Scattered over the skin are the charac- 
teristic denticles or placoid scales (Fig. 95). Each of these consists of a 
pulp cavity, around the edge of which lies a layer of odontoblasts 
secreting the calcareous matter of the scale, known as dentine. This 
has a characteristic structure resulting from the fact that the odonto- 
blasts send fine processes throughout its substance. The outside of the 
dentine is covered by a layer of enamel, secreted by the overlying 
ectoderm. Usually the denticles pierce through the ectoderm, after 
which no further enamel can be added to their surface. Obviously the 
scales are similar to teeth, which are indeed to be considered as 
specialized denticles developed on the skin of the jaws. It has often 
been supposed that the denticle is the primitive type of fish scale, 
from which others have been derived, but it now seems more likely 
that the earliest covering was a continuous layer, later broken into 
large scales, from which the denticle was ultimately derived (p. 269). 
The skin also gives protection to the fish by its colour, produced 
by a layer of chromatophores beneath the epidermis. Many sharks 
have a spotted or wavy pattern, which breaks up their visible outline 
as they move in the water, especially near the surface. They are able 
to change their colour, though only slowly, becoming darker on a dark 
background (see p. 164). 

5. The skull and branchial arches 

In general organization a dogfish follows closely the fish plan, 
which we have already considered. Most of its special new features 
are in the head, and we may now turn to a consideration of the 
organization of the head and jaws of a gnathostome vertebrate. The 
jawless vertebrates of the Silurian and Devonian included fresh- 
water animals of various sorts, but the vertebrate type began to 
flourish and increase more abundantly with the appearance of creatures 
with jaws in the late Silurian. From this stage onwards we have to 
follow the parallel history of numerous orders and families, as the 
vertebrate plan of structure became adapted for various habitats. It 
seems likely that the development of a biting mouth greatly increased 
the range of possibilities of vertebrate life. The most obvious use of 
a mouth is for attacking other animals, but it may also have been used 
to collect plant food from all sorts of situations where it would not 
be available to the microphagous or shovelling Agnatha. Probably the 
mouth was also early used for defence, and in this way influenced the 
whole bodily organization, making unnecessary the heavy armature 


that is so characteristic of many early vertebrates. Modern research 
has shown that the armour has become progressively reduced along 
various lines of iish evolution. Older ideas of comparative anatomy 
regarded the 'cartilage fishes' as showing a primitive stage, preceding 
the appearance of bone. We now realize that this is the opposite of the 
truth and that the dogfish and its relatives represent a higher type, 


Fig. 96. Skull and branchial arches of the dogfish (Scyliorliimts). 
au.c. auditory capsule; b.b. basibranchial; basihyal; c. centrum; cer.b. ceratobranchials; 
cer.h. ceratohyal; d.r. foramen for dorsal root; e.b. extrabranchials; e.c.f. external carotid 
foramen; e.l. ethmoid ligament; ep.b. epibranchials; gr. groove for anterior cardinal sinus; 
g.r. gill rays; hy.a. foramen for hyoid artery; hymd. hyomandibula; i.d. interdorsal; io.c. 
interorbital canal; I.e. labial cartilages; M.c. Meckel's cartilage; na. neural arch; nas.c. nasal 
capsule; o.n.f. orbito-nasal foramen; op. foramen for ophthalmic nerve; op.g. groove for 
op.V; op.V, op. VII ophthalmic branches of V and VII; orb. orbit; ph.b. pharyngobranchials ; 
p.sp.l. prespiracular ligament; r. rib; rost. rostral cartilages; spd. supradorsals ; tr. transverse 
process; vr. foramen for ventral root; II-IX, foramina for cranial nerves. (After Borradaile.) 

able to defend themselves by mobility, by biting, and by efficient 
sensory and nervous organization. Heavy defensive armour is a 
primitive form of protection for animals, as for man. 

Besides its use in feeding and defence, the mouth can also be used as 
a means of 'handling' the environment, for instance in the nest-build- 
ing activities of many fishes. Indeed, it is difficult for us to realize the 
utility of the jaws for an animal not provided with any other means of 
seizing hold of objects. 

The development of the mouth to a point at which it could be used 
in these varied ways was, therefore, a very important stage in evolution. 
Recognition of the Gnathostomata as a separate group of animals is 
far more than a matter of classificatory convenience, it marks the 
achievement of the possibility of life in a greatly increased range of 


Morphological analysis enables us to see how this biting mouth 
was produced, by modification of one or more of the gill-slits. The 
main differences that separate the gnathostome from cyclostome ver- 
tebrates are therefore in the head and its skeleton. Although the 
modern elasmobranchs show the skull and jaws in a modified and 
reduced condition, they provide by their simplicity a good starting- 
point for discussion. The 'skull' of a dogfish consists of a series of 




Fig. 97. Diagram of skull of selachian embryo before fusion of the main cartilages; 
cranial nerves black, numbered; arteries cross-lined. 

ac. auditory capsule; bra. epibranchial; dao. dorsal aorta; eps. efferent pseudobranchial; 

ha. efferent hyoid; hv. hypophysial vein; i.e. internal carotid; nc. nasal cartilage; oc. orbital 

cartilage; oca. occipital arch; op. optic; oph. ophthalmic; or. orbital; pan. pila antotica; pf. 

profundus nerve; pch. parachordal; poc. polar cartilage; tr. trabecula. (From Goodrich.) 

cartilaginous boxes surrounding the brain and receptor organs (Fig. 
96). The nasal capsules, orbital ridges, and auditory capsules are 
largely fused with the main cranium, producing a single continuous 
structure, the chondrocranium. It is interesting to consider how this 
structure has arisen during the process of cephalization. Presumably 
parts of it represent the modified sclerotomes of trunk regions. We 
shall see presently that there is strong evidence that the head has arisen 
by modification of a segmental arrangement such as is seen in the 
trunk; the morphogenetic processes that build the skull must there- 
fore be related in some way to those of the vertebrae. The first rudi- 
ment of the skull in the embryo consists of two pairs of cartilaginous 
rods, the parachordals and trabeculae (Fig. 97). The former lie on 
either side of the notochord, the trabeculae in front of the notochord. 
These first rods fuse up to make a continuous plate; from this grow 
sides and roof, completing the cartilaginous neuro-cranium around the 
brain. Meanwhile cartilaginous capsules form around the nose, eyes, 
and ears, and become joined to the neuro-cranium. Posteriorly, behind 


the auditory capsules, the cranium is completed by the addition of a 
number of segmented elements, evidently modified vertebrae. 

The problem is, therefore, to determine the nature of the pro-otic 
part of the skull. Before we can settle this we must consider the 
visceral or branchial arches. These are pairs of rods of cartilage 
developed in the walls of the mouth and pharynx, between the gill- 
slits. In the dogfish each typical branchial arch (Fig. 96) consists of a 
series of four pieces, the pharyngo-, epi-, cerato-, and hypo-branchials. 
Ventrally some of the arches join a median basibranchial plate. These 
rods lie in the pharynx wall and on their outer sides carry a series of 
projecting rods, the branchial rays and extrabranchial cartilages, 
whose function is to support the lamellae of the gills. 

There are five such branchial arches, differing only slightly from 
each other. In front of these lie two arches, the hyoid and mandibular, 
which, though modified, are obviously of the same series. The hyoid 
the more nearly resembles a typical branchial arch. Its most dorsal 
element, the hyomandibular cartilage, is a thick rod attached dorsally 
to the skull by ligaments and at its lower end forming the support 
for the hind end of the jaw. It apparently corresponds to the epi- 
branchials. The more ventral elements, cerato- and basihyal, resemble 
the corresponding members of more posterior arches. The jaws them- 
selves (mandibular arches) depart more widely from the form of a 
typical branchial arch, but the two thick rods of which each is com- 
posed, the upper palato-pterygo-quadrate bar and the lower Meckel's 
cartilage, are recognizably members of the branchial series. Looking 
at the whole apparatus with a thought to the embryological processes 
that have produced it, with as it were a manufacturer's eye, we can 
see at once that the jaws and hyoid arch have been produced by a 
modification of the processes that make the branchial arches. 

6. The jaws 

Study of the serial relationship of the jaws and branchial arches 
gives us an understanding of the course of evolution of the mouth. 
We may suppose that the ancestors of the gnathostomes possessed a 
nearly terminal mouth, either on the front end of the body or on the 
ventral surface. The pharynx was pierced by a series of gill pouches, 
beginning shortly behind the mouth and separated by arches, each 
containing a set of cartilaginous bars (Fig. 96). There is some evidence 
that this condition persisted in the cephalaspids (p. 125), where there 
is found to be a series of ten pairs of gill-slits, beginning far forward 
on either side of the mouth. The muscles moving the more anterior 


parts of the pharynx wall and the anterior arches could be called into 
play to help in the collection of food. In this way the mouth came to 
be used for prehension, and the grasping jaws of the gnathostomes 
appeared as the more anterior arches became modified to allow more 
efficient seizing, and the skin over them was modified to form the 
teeth. The mouth probably shifted backwards during this process and 
its lateral edges joined the first gill-slit. The rods supporting the 
posterior wall of that slit thus became bent over into the characteristic 
position of the vertebrate jaws. 

There is some uncertainty as to the means of support of the jaws 
in the earlier stages of their evolution. The front end of the palato- 
pterygo-quadrate bar is attached to the cranium in the dogfish by the 
ethmo-palatine iigament'. In most elasmobranchs the hind end of the 
upper jaw is not fixed to the cranium but is slung from the latter by 
the hyomandibula and by a prespiracular ligament. This means of 
support, known as hyostylic, was for long supposed to have been the 
original one. But the earliest gnathostomes (the acanthodians) do not 
have this arrangement (p. 187), indeed, their hyoid arch is an almost 
typical branchial arch, not modified to support the jaw. In the primi- 
tive condition one would not expect the hyoid arch to have any con- 
nexion with the mandibular. In the acanthodians the jaw is supported 
by direct attachments to the cranium at its hind as well as front end, 
a condition known as autodiastylic. 

The early elasmobranchs themselves do not have a hyostylic jaw 
support, but an arrangement in which the upper jaw is both attached 
to the cranium and also supported by the hyomandibula. This 
amphistylic condition persists to-day in the primitive shark Hexan- 
chus. Apparently the jaws, which at first swung from the skull, later 
became fixed at the hind end to the hyoid, and this finally became the 
only means of support posteriorly. The advantage of this last arrange- 
ment is presumably that it allows a wide gape for swallowing, the prey 
whole. As the sharks sought to eat larger and larger fishes, those in 
which the hind end of the upper jaw was less firmly fixed to the skull 
were the more successful and so the hyostylic condition was achieved. 

If this theory of the origin of the jaws is correct we may expect to 
find some trace of a cartilaginous support for the side wall of the 
pharynx in front of the original first gill-slit, a premandibular visceral 
arch. Many sharks have two pairs of labial cartilages in this position, 
which have been held to represent arches. However, there are strong 
grounds for believing that this is represented by the trabeculae cranii, 
the rods lying on each side in front of the parachordals and contribut- 


ing to the floor of the skull (Fig. 98). Many points indicate that these 
rods are not part of the axial skeleton. The main axis of the body 
presumably ends at the front end of the notochord, that is to say, at 
the level of the front ends of the parachordals. Indeed there is much 
confirmatory evidence to show that this level represents the end of the 

^ 12.2m R £ 

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FlG. uS. Diagrams to show the condition of the visceral arches and 
jaws in early vertebrates. 
A. cephalaspid; B. acanthodian; C. elasmobranch. (i.e. auditory capsule; 
"br. a. 1" first branchial arch; c.n.c. nerve-cord; e. eye; gs. I. first gill-slit; 
//. hypophysis. /i.a. hyomandibular arch; m. a. mandibular arch; m. mouth; not. 
notochord; p.m.a. premandibular arch (trabecula); sp. spiracle; Vi, pro- 
fundus nerve; V2, 3, trigeminal nerve; VII, facial; IX, glossopharyngeal; 
X, vagus. (Modified after Westoll.) 

segmented part of the body, everything in front of this level being as 
it were pushed forward from above or below. The trabeculae have 
exactly the relations to the most anterior nerves and blood-vessels 
that would be expected of visceral arches. Confirmation of the theory 
comes from the discovery that the cartilage of the front part of the 
trabeculae, like that of the visceral arches, is formed by material 
streaming down from the neural crest, that is to say, from ectoderm. 
The branchial arches, hyoid, jaws, and trabeculae thus all constitute 
a single series, the result of the working of a repetitive or rhythmic 
process, appropriately modified at each level. 


7. Segmentation of the vertebrate head 

The rhythmicity or metamerism seen in the cartilages can be traced 
throughout the structure of the head. Although in higher vertebrates 
the head appears as a distinct structure, separated from the body by 
a neck, yet there is every reason to think that it has arrived at that 
state by gradual modification of the anterior members of an originally 
complete metameric series. The jaws, the receptor-organs, and the 
brain have become developed at the front end of the body, producing 
what zoologists conveniently if pretentiously call cephalization. 

The fundamental segmentation of the head is not very easily appar- 
ent to superficial observation; the working out of its details is an 
excellent exercise in morphological understanding. Recognition of the 
segmental value of the various structures also makes them the more 
easily remembered. For instance, the nerves found in the head have 
been named and numbered for centuries by anatomists in an arbitrary 

I. Olfactorius 
II. Opticus 

III. Oculomotorius 

IV. Trochlearis (patheticus) 
V. Trigeminus 

VI. Abducens 
VII. Facialis 
VIII. Acousticus 
IX. Glossopharyngeus 
X. Vagus 
XI. Accessorius 
XII. Hypoglossus 

Morphological study has shown that these nerves are not isolated 
structures, each developed independently, but that they represent a 
regular series of segmental dorsal and ventral roots of the head 
somites. The satisfaction and simplification given by this generaliza- 
tion is one of the clearest advantages of morphological insight. More 
important still, such understanding of the morphology of a structure 
shows us how to look for the morphogenetic processes that produce it; 
such knowledge of how organs are made is an essential step in mending 
or remaking them. 

The idea of the essential similarity of structure of the head and 
trunk was early developed by Goethe, who tried to show that the 
mammalian skull is a series of modified vertebrae. Unfortunately this 

v. 8 



view cannot be maintained in detail and the theory was brought to 
ridicule by T. H. Huxley and others. The segmental value of the skull 
floor and sides is not at all easy to determine; the parachordals arise 
as a pair of unsegmented rods on either side of the notochord. 

ma: ha 

Fig. 99. Diagram of the segmentation of the head of a dogfish. 

cr. limit of neurocranium; vr. limit of visceral arch skeleton; a. auditory nerve; aa.i, pre- 
occipital arch; aa.2, occipital arch; ab. abducens nerve; ac. auditory capsule; ah. anterior 
head cavity; c. coelom;/. facial nerve; gl. glossopharyngeal nerve; ha. hyoid arch; hm. hypo- 
glossal muscles; hy. hypoglossal nerve; la. pila antotica; m. mouth; m.2-6, myomere 2-6; 
ma. mandibular arch; tnb. muscle-bud; nc. nasal capsule; om. oculomotor nerve; prf. pro- 
fundus nerve; scl. sclerotome of segment 10; sp.1-2, ganglion of spiral nerve 1-2; t. trochlear 
nerve; tr. trigeminal nerve; v. vagus nerve; vgl. vestigial ganglion of segment 7; vc. ventral 
coelom; vr. ventral root of segment 6. (From Goodrich.) 

8. The pro-otic somites and eye-muscles 

Ideas about the segmentation of the head were first correctly for- 
mulated by F. Balfour. In his studies of the development of elasmo- 
branchs (1875) he showed that three myotomes, the pro-otic somites, 
can be recognized during development in front of the auditory capsule 
(Fig. 99). The auditory sac, pushing inwards and becoming sur- 
rounded by cartilage, then breaks the series of myotomes, so that 
several are missing in the adult, though the series is complete in the 

If this analysis is correct we should be able to recognize that the 
nerves of the head belong to a series of dorsal and ventral roots, 
similar to that in the trunk, the ventral roots being those for the 
myotomes and the dorsal roots, running between the myotomes, 
carrying sensory fibres for the segment and motor-fibres for any non- 
myotomal musculature present (p. 36). In the spinal region the 


dorsal and ventral roots join, but this is not the primitive condition 
(witness amphioxus and the lampreys), and in the head region the 
earlier state of affairs is retained, the dorsal and ventral roots remain 
separate. Presumably the arrangement we find in the head today was 
laid down in very early times, in the Silurian period or earlier, when 
the dorsal and ventral roots were still separate. The head, in spite of 
its specializations, preserves for us a relic of that ancient condition. 

The branchial nerves, such as the glossopharyngeal, show clear 
signs of this condition. Each has a small pre-trematic branch in front 
of the slit, a larger post-trematic branch behind it, and a pharyngeal 
branch to the wall of the pharynx. The pre-trematic branch usually 
contains mostly sensory fibres from the skin, the pharyngeal branch 
visceral sensory fibres, including those from taste buds. The post- 
trematic branch contains both motor and sensory fibres. In addition 
to these more ventral branches the branchial nerves also usually 
provide dorsal rami to the skin of the back. 

The three pro-otic somites become completely taken up in the 
formation of the six extrinsic muscles of the eye, arranged similarly 
in all gnathostome vertebrates. The four recti roll the eye straight 
upwards, downwards, forwards, or backwards, and the two obliques, 
lying farther forward, turn it, as their name suggests, upward or 
downward and forward (Fig. ioo). Of these muscles the superior, 
anterior, and inferior rectus and inferior oblique are all derived from 
the first myotome and are innervated by the oculomotor (third cranial) 
nerve. The superior oblique, innervated by the trochlear nerve (fourth 
cranial), is the derivative of the second and the posterior rectus 
(external rectus of man), innervated by the abducens (sixth cranial), 
of the third somite. These three nerves are evidently the ventral roots 
of the three pro-otic somites. At some early stage of vertebrate 
evolution all the myotomal musculature of the front part of the head 
became devoted to the movement of the eyes. The muscles originally 
forming part of the swimming series became attached to a cup-like 
outgrowth from the brain. 

Most of the rest of the musculature of the head, including that of 
jaws and branchial arches, is derived from the somatopleure wall of the 
coelom and is therefore lateral plate or visceral musculature. This 
lateral plate muscle is indeed better developed in the head than in 
the trunk, where all the muscles, even of the more ventral parts of the 
body, are formed by downward tongues from the myotomes. The 
lateral plate origin of the jaw-muscles at once gives us the clue to 
the nature of some more of the cranial nerves, the fifth, seventh, ninth, 




and tenth. These nerves all carry ganglia containing the cell bodies 
of sensory fibres and these are comparable to the spinal dorsal root 

' op prof 


cbl sip. 


Fig. 100. Orbit of the dogfish. 

ant. reel, anterior rectus; cereb. cerebellum; cil.a., cil.p. anterior and posterior ciliary nerves; 
epa. anterior carotid artery; ep. epiphysis; g.cil. ciliary ganglion; inf. obi. inferior oblique; 
lam. lamina terminalis of cerebrum; O.V. and VII, superficial ophthalmic branch of trigeminal 
and facial; obi. sup. superior oblique; olf.b. olfactory bulb; opt. I. optic lobe; post.rect. posterior 
rectus; r. op. prof, ramus ophthalmicus profundus of trigeminal; rs. sensory root of ciliary 
ganglion; sup.rect. superior rectus; thai, thalamus; // to A', cranial nerves. 
(After Young, Quart. J. Micr. Sci. 75.) 

ganglia. But the nerves also transmit motor-fibres to the muscles of 
the jaws and branchial arches. They are in fact mixed roots, just as 
we have seen that the primitive dorsal roots should be, carrying the 
sensory fibres for the segment and motor-fibres for the non-myotomal 
muscles (p. 36). 


9. The cranial nerves of elasmobranchs 

These nerves are more easily studied in elasmobranchs than in any 
other vertebrates, because of the relatively soft and transparent 
cartilage through which they run. We may therefore take this oppor- 
tunity to examine the whole series of cranial nerves in some detail in 
the dogfish, beginning with the oculomotor nerve, the first ventral 
root. Examination after removal of the brain will show clearly in any 
vertebrate, including man, that this nerve arises from the ventral 
surface, at the level of the hind end of the midbrain (optic lobes). 
This is not true of the trochlear or pathetic nerve, which emerges 
from the dorso-lateral surface of the brain but nevertheless is the 
ventral root of the second segment. Its cells of origin lie close behind 
those of the oculomotor nerve, in the ventral part of the brain. The 
reason for the dorsal emergence is that the muscle lies dorsally and the 
nerve has been modified so as to reach its muscle by running partly 
within the tissues of the brain. The third ventral root (abducens), 
which is very short, is clearly ventral. 

In looking for the dorsal roots that correspond to these three 
segments we have to examine the trigeminal, facial, and auditory 
nerves. The trigeminal of the dogfish, like that of man, has ophthalmic, 
maxillary, and mandibular branches (Fig. ioo), but can be shown to 
represent the dorsal roots of the two first segments. The ophthalmic 
branch is a sensory nerve carrying fibres for skin sensation from the 
snout. The maxillary branch supplies sensory fibres to the upper jaw, 
whereas the mandibular is a mixed nerve to the skin and muscles of 
the lower jaw. Besides these main branches there is also a small but 
important sensory branch from the trigeminal to the eyeball (Fig. 
ioo). This joins a motor root from the oculomotor nerve where the 
latter swells slightly to form a ciliary ganglion. Two ciliary nerves 
then carry motor and sensory fibres to the eyeball. In some specimens 
a branch of the more anterior ciliary nerve leaves the eyeball anteriorly, 
runs between the oblique muscles, and out of the orbit again to end 
in the skin of the snout (Fig. ioo). Though this branch is small and 
inconstant in the dogfish, its course corresponds exactly with that 
of a much larger nerve in the related shark Mustelus and in skates and 
rays. In these animals there are two ophthalmic branches of the 
trigeminal nerve; one, having a course similar to that of the main nerve 
in the dogfish, is the ramus ophthalmicus superficialis; the second, 
the ramus ophthalmicus profundus, runs across within the orbit, gives 
off the long ciliary nerve to the eyeball, passes between the oblique 


muscles, and leaves the orbit for the skin of the snout. In higher 
vertebrates the nasociliary nerve and the long ciliary, innervating the 
eyeball, represent the profundus, while the rest of the ophthalmic 
nerve of mammals corresponds to the superficial ophthalmic of 

The relations of these nerves to other structures shows that the 
so-called trigeminal nerve really includes the dorsal roots of two 
segments combined. The profundus can be traced back in develop- 
ment to a nerve that is obviously the dorsal root of the first somite, 
of which the oculomotor nerve is the ventral root. Indeed it may be 
noticed that the profundus and oculomotor partly join, at the ciliary 
ganglion. The ramus ophthalmicus profundus and the oculomotor 
nerve thus constitute the dorsal and ventral roots of the first or pre- 
mandibular somite, whose corresponding branchial arch is presumably 
the trabecula cranii (p. 147). The dorsal root does not show the full 
structure of a branchial nerve, presumably because there is no gill-slit. 
The profundus represents only the dorsal branch of a typical branchial 
nerve, innervating the skin. 

The ramus ophthalmicus superficialis, and the maxillary and mandi- 
bular branches together constitute the dorsal root of the second pro- 
otic somite, whose ventral root is the trochlear nerve. The correspond- 
ing gill arch is the mandibular (palato-pterygo-quadrate bar and 
Meckel's cartilage), whose gill-slit we have suggested has been in- 
corporated with the edge of the mouth. The trigeminal nerve shows 
considerable similarity to a branchial nerve, its maxillary branch repre- 
sents the pre-trematic and the mandibular the post-trematic ramus, 
while the ophthalmicus superficialis is the dorsal branch to the skin. 
There is no pharyngeal branch. An anomalous feature of the trige- 
minal is that it contains sensory fibres whose cells of origin lie within 
the brain (mesencephalic root). These fibres are probably proprio- 
ceptors from the masticatory muscles and eye-muscles. The latter run 
from the eye-muscle nerves to join the trigeminal. 

The dorsal root of the third segment, whose ventral root is the 
abducens, includes the whole of the facial and also the auditory nerve. 
The facial is a large mixed nerve in the dogfish. Its ophthalmic branch 
runs to the snout, carrying mainly fibres for the organs of the lateral 
line system that lie there. A large buccal branch supplies sensory 
fibres to the mouth and a palatine branch joins the trigeminal. A small 
prespiracular branch carries sensory fibres from the skin in front of the 
spiracle, and the main portion of the nerve continues behind the 
spiracle as the hyomandibular nerve, dividing up into motor branches 


for muscles of the hyoid arch and sensory ones for the skin of that 

This nerve is obviously the branchial nerve to the spiracle; we can 
safely say that the facial and abducens are the dorsal and ventral roots 
of the third or hyoid segment. The auditory nerve is included as part 
of the dorsal root of the third somite because the auditory sac is 
formed by sinking in of a portion of the ectoderm within the territory 
of the facial nerve. The labyrinth still communicates with the surface 
of the head in the adult dogfish by a canal, the aquaeductus vestibuli. 
The nerve that innervates the auditory sac, whatever complexities it 
may acquire, is to be regarded morphologically as a portion of the 
dorsal root of the hyoid segment. 

The segmental nature of the structures in the pro-otic region can 
therefore be made out without serious difficulty. The disturbance 
introduced by the auditory capsule makes the segmental arrangement 
of the more posterior region of the head somewhat confused. The 
series of dorsal roots is uninterrupted; the ninth (glossopharyngeal) 
nerve is the dorsal root of the fourth segment of the series and runs 
out through the cartilage of the auditory capsule. The dorsal roots of 
the succeeding segments are then fused to form that very puzzling 
nerve the vagus. The branches it sends to the gills are clearly typical 
branchial nerves, but why should they all come off together from the 
medulla oblongata, and if there is any advantage in this union, why 
is the ninth nerve not also so incorporated? Above all, why does 
the vagus send two branches far outside the segments of its origin, the 
lateral line branch carrying fibres to the organs right to the tip of the 
tail and the visceral branch fibres to the heart, stomach, and probably 
small intestine? 

Evidently these 'wanderings', from which the vagus gets its name, 
began very long ago. The nerve reaches as far back in cyclostomes as 
in any other vertebrates. It is easy to understand that if visceral 
functions are to be directed from the medulla oblongata there is an 
advantage in having sensory impulses sent direct to that region of the 
brain and motor impulses sent out direct to the viscera. It may be 
that these advantages allowed the centralization of these visceral 
functions, while the need for serial contraction of the swimming 
muscles led to the retention of the segmental arrangement of the 
spinal cord. It is an interesting thought that but for the swimming 
habits of our ancestors our nervous system might by now consist of a 
central ganglion with nerves passing from it direct to all the organs. 
Indeed we are tending in that direction, as the spinal cord shortens 

v. 9 VAGUS NERVE 155 

and becomes more and more nearly a simple pathway between the 
brain and the periphery. 

However this may be, the vagus is certainly a nerve compounded 
of the dorsal roots of several segments and it is a mixed nerve, con- 
taining both receptor and motor fibres. Some of the more posterior 
rootlets of this series are separated off in higher animals (not the dog- 
fish) to form the eleventh cranial nerve, the accessorius or spinal 
accessory, which in mammals sends motor-fibres to certain muscles 
of the neck, the sternomastoid, and part of the trapezius. Its motor 
nature has led some to suppose that this nerve is a ventral root, but 
these muscles are derived from lateral plate musculature and the 
accessorius represents the motor portion of the hinder dorsal roots 
of the vagus series. 

The ventral roots of this post-otic region have become much 
reduced. Several myotomes are always missing completely, so that 
there are no ventral roots corresponding to the glossopharyngeal and 
first three or four vagal segments. The more anterior of the surviving 
post-otic somites are to be found not in the dorsal region but ventrally, 
as the hypoglossal musculature of the tongue. The muscle-buds have 
grown round into this portion behind the gill-slits, and the nerve 
(hypoglossal) that innervates them represents the ventral roots of the 
more posterior segments of the vagus-accessorius series (Fig. 104). 
The origin of this nerve from the floor of the medulla is a clear sign 
that it is a ventral root. 

Thus the entire series of cranial nerves is : 



Dorsal root 

Ventral root 



R. op. profundus V 

Oculomotorius III 


Palato - pterygo - quad- 

Rr. op. superficialis, 

Trochlearis IV 

rate bar and Meckel's 

maxillaris, and man- 


dibularis V 



Facialis VII 
Acousticus VIII 

Abduccns VI 

1st Branchial 

1 st Branchial 

Glossopharyngeus IX 


2nd Branchial 

2nd Branchial^ 

Vagus X 

3rd Branchial 

3rd Branchial 1 


Hypoglossals XII 

4th Branchial 

4th Branchial j 

Accessorius XI 

5th Branchial 

5th Branchial J 

Two cranial nerves have not yet been considered, the first, olfactory, 
and second, optic. Our thesis is that all connexions between centre 
and periphery are made by means of a segmental series of dorsal and 
ventral roots and therefore these nerves, too, should be fitted into the 
series. No embryological or other studies have enabled this to be done 


and the reason in the case of the optic nerve is quite clear. It is not 
morphologically a peripheral nerve at all. The eye is formed as a 
vesicle attached to the brain ; the optic 'nerve' therefore develops as a 
bundle of fibres joining two portions of the central nervous system; in 
fact it is now usually called the optic tract, not the optic nerve. 

This reasoning will not apply to that very peculiar and interesting 
structure the olfactory nerve. This is unique among all craniate 
nerves in consisting of bundles of fibres whose cell bodies lie at the 
periphery. The cells of the olfactory epithelium, like the sensory cells 
in invertebrates and some of those of amphioxus, are neurosensory 
cells, that is to say, their inner ends are prolonged to make the actual 
nerve-fibres that pass into the brain. This fact does not by itself solve 
the problem of fitting the nerve into the series of dorsal and ventral 
roots, but it reminds us that the nerve is very ancient, and suggests 
that it does not fall into the rhythm of the rest of the series because it 
precedes the other cranial nerves either in time or space, or perhaps 
even both. The olfactory nerve may have existed before any seg- 
mental structure appeared, possibly as the nerve of sense-organs on 
the front end of the ciliated larva which we suppose gave rise to our 
stock (p. 76). Alternatively we can say that the olfactory nerve is as 
it is because it lies in front of the region over which the segmenting 
process operates; it is, as it were, 'prostomial'. If we wish we can hold 
both these views together. 

There are one or two other exceptions to the rhythmic arrangement 
of nerves, perhaps more difficult to account for than the first and 
second cranial nerves. If all connexions between centre and periphery 
are made by dorsal and ventral roots what is the status of the fibres 
that run down the infundibular stalk to reach the cells of the pituitary 
body? This glandular tissue, derived from the epithelium of the 
hypophysial folding of the roof of the mouth, is undoubtedly a peri- 
pheral organ. Does it receive its nerve-fibres direct from the brain ? 
If so presumably we must say that the pituitary, like' the nose, 
is prostomial, lying in front of the segmental region, and this is 
reasonable enough from its position. There is good reason to believe 
that it is an extremely ancient organ, already present in the earliest 

A still more puzzling exception is the nervus terminalis. This is 
a small bundle leaving the brain ventrally behind and below the olfac- 
tory nerves and running to the olfactory mucosa or to the accessory 
olfactory organ of Jacobson, where this is present (p. 350). In some 
vertebrates it carries a small ganglion. The fibres are probably 

v. io RESPIRATION 157 

afferents and they run backwards through the brain tissue to the 
pre-optic nucleus of the hypothalamus. A possible clue to its origin is 
that this is the region of the brain where the morphologically ventral 
region of the neuraxis ends (p. 147). The nervus terminalis may repre- 
sent the ventral olfactory nerve, the much larger main nerve being 
morphologically dorsal. 

A further puzzle of some importance which may be mentioned here 
is the course of the proprioceptor fibres for those muscles that are 
supplied purely by ventral roots. The eye-muscles contain proprio- 
ceptor organs and Sherrington and others have shown that the affer- 
ent fibres connected with these run to the brain through the third, 
fourth, and sixth nerves, that is to say, through ventral roots. Simi- 
larly, it has been shown that there are afferent fibres in the hypo- 
glossal nerves in mammals. Conversely it is now known that there are 
efferent fibres running from the brain to many receptor organs. For 
example, such fibres run in the auditory nerve. To pursue these ques 
tions farther would lead us into discussion of the factors that control 
the making of connexions within the nervous system Here we are 
concerned only with analysis of the plan that produces the main out- 
lines of the structures in the head, a plan which, with all its modifica- 
tions, is essentially segmental. 

10. Respiration 

The function of the branchial arches is not merely to support the 
gills but to allow the movements of the pharynx wall by which the 
respiratory current of water is produced. It is for this reason that 
the jointed system of rods is present. The respiratory movements con- 
sist in a lowering of the floor of the mouth by means of the hypo- 
glossal muscles, with at the same time an expansion of the walls of 
the pharynx. This causes an inrush of water through the mouth, 
which is then closed and the floor raised, forcing the water out through 
the gill-slits. The whole movement is worked by the 'visceral' (lateral 
plate) muscles of the pharynx wall, innervated by the trigeminal, 
facial, glossopharyngeal, and vagus nerves, in co-operation with the 
myotomal hypoglossal muscles, innervated by the hypoglossal nerve. 

The gill filaments bear lamellae that meet at the tips, leaving minute 
channels for the water. The blood flows through the lamellae in the 
opposite direction to the water so that just before leaving the gills 
the blood meets the highest concentration of oxygen and lowest of 
carbonic acid. 



1 1 . The gut of elasmobranchs 

The digestive system of sharks shows several changes from the plan 
found in lampreys, especially the presence of a true stomach, charac- 
teristic of all gnathostomes. Apparently little or no digestion goes on 
in the mouth and pharynx. The teeth consist of rows of backwardly 
directed denticles (Fig. ioi). They are carried on special folds of skin 
lining the jaws and are continually replaced as they are worn away on 

Fig. ioi. Sections through the jaws of a, dogfish (Scyliorhinus), and n, sand-shark 

(Odontaspis), showing the transitions between dermal denticles (d) and teeth (t). 

(From Norman, partly after Gegenbaur.) 

the edge. The replacement of milk by permanent teeth in mammals 
is a relic of such serial replacement in a fish. The 'gill rakers' arc 
rods attached to the branchial cartilages and serving to prevent 
the escape of prey. The basihyal supports a short non-protrusible 

The wall of the pharynx is lined by a stratified epithelium on to 
which open numerous mucous glands, sometimes complex. The mucus 
serves to assist the passage of the food, but probably has no strictly 
digestive function, though the salivary glands of higher vertebrates 
no doubt originate from a modification of these mucous glands. 

The pharynx narrows to an oesophagus with thick muscular walls, 
leading without sharp transition to the stomach. We have seen that in 
cyclostomes the oesophagus opens directly into the region of gut that 
receives the bile and pancreatic secretion. The stomach, which we 


now meet for the first time, has probably been formed as a special 
portion of the oesophagus. Barrington suggests that it evolved with the 
jaws, serving originally as a receptacle for the large pieces of food, or 
even whole fishes, which could now be swallowed. The mucous glands 
became modified to produce acid, since this prevents bacterial decay. 
Finally, an enzyme, pepsin, was evolved able to digest proteins in 
acid solution. In the dogfish this condition has been fully established 
and the stomach has essentially the structure and functions found in 
all higher vertebrates. However, in the gastric glands only one type 
of cell is recognizable, there are no separate pepsin-secreting and 
acid-producing cells. Nevertheless, there is a pepsin-like enzyme 
present and the contents are acid. The stomach is divided into two 
parts, a descending cardiac and ascending pyloric limb, the signifi- 
cance of the divisions being unknown. 

The region where the stomach joins the intestine is guarded by a 
powerful pyloric sphincter, immediately beyond which open the bile 
and pancreatic ducts. The liver is a large two-lobed organ, receiving 
the hepatic portal blood from the gut. It serves as a storage organ 
containing much glycogen and fat and sometimes the hydrocarbon 
squalene. It probably also plays a part in the destruction of red blood 
corpuscles. Bile is carried away to a gall-bladder, from which a bile- 
duct leads to open at the front end of the spiral intestine. 

The pancreas, hardly recognizable as a distinct organ in the lamprey, 
forms in the dogfish an elongated body between the stomach and 
intestine. It contains both exocrine and endocrine cells and its duct 
enters the intestine shortly below the pylorus. The 'small' intestine 
of elasmobranchs is of a peculiar form, being short but with its 
surface greatly increased by the presence of a spiral ridge or 'valve'. 
The intestinal contents are alkaline and contain trypsin, amylase, 
and lipase. There is no constant fauna of commensal bacteria. Ab- 
sorption presumably takes place wholly in this organ, for the remain- 
ing length of gut consists only of a short rectum, to which is attached 
an organ of unknown function, the rectal gland, containing branched 
glands and much lymphoid tissue. 

12. The circulatory system 

The heart develops as a specialization of the subintestinal vessel 
between the place where it receives the veins from the liver and the 
body wall and the gills, which are to be supplied under high pressure. 
It consists of a single series of three main chambers, sinus venosus, 



atrium, and ventricle, all of which are muscular, and there is also a 
muscular base to the ventral aorta, the conus arteriosus, provided with 
valves (Fig. 102). 

The five afferent branchial arteries carry blood to the gill lamellae, 
whence it is collected by a system of four efferents and connecting 
vessels into a median dorsal aorta, carrying blood to all parts of the 
body. Oxygenated blood is supplied to the head from three sources. 
(1) From the top of the first gill a carotid artery leaves the efferent 
branchial and runs forwards and towards the midline: it then divides 

f. eF pef 

Fig. 102. Diagram of the branchial circulation of an elasmobranch fish. 

aa. median anterior prolongation of aorta; ac. anterior carotid; afa. afferent vessel of spiracu- 
lar gill; aef. afferent vessel from last hemibranch; af. anterior efferent vessel; a/. 2-6 , five 
afferent vessels from ventral aorta; afa. afferent artery of spiracular gill; c. conus leading to 
ventral aorta; cl. coeliac artery; d. ductus Cuvieri; da. dorsal aorta; ef. epibranchial artery; 
h. a. hyoid afferent vessel; hp. hepatic veins; ht. heart; pc. posterior carotid; pef. posterior 

efferent vessel; s. spiracle; va. ventral artery; I-V, branchial slits. 

(From Goodrich, Vertebrata, A. & C. Black, Ltd., after Parker.) 

into an external carotid to the upper jaw and internal carotid to the 
brain. (2) The dorsal aorta divides at its front end into branches, 
which join the carotids before their division. (3) From the vessel 
that collects blood from the first gill arises a hyoidean artery, carry- 
ing oxygenated blood to the spiracle. From here the hyoidean artery 
runs on as the anterior carotid (Fig. 102) across the floor of the orbit 
to join the internal carotid within the brain-case. 

The heart is supplied by a cardiac artery arising from the dorsal 
aorta behind the gills. The blood-pressure in the ventral aorta is 30-40 
mm Hg and there is a drop of 10-20 mm Hg across the gills. The 
circulation is slow, with a mean circulation time as low as 2 minutes. 
The venous return of the fishes is ensured by a system of very large 
sinuses. The pericardium is almost completely enclosed in a carti- 
laginous framework by the basibranchial plate above and pectoral 
girdle below it. It may be that this produces a negative pressure in 


the veins. There is a passage of unknown function, the pericardio- 
peritoneal canal, leading from the pericardium to the abdominal 
coelom and the hinder end of this is very narrow. 

A caudal sinus from the tail opens into a renal portal system above 
the kidneys. From the latter, and from the muscles of the back, blood is 
collected into the pair of very large posterior cardinal sinuses, lying on 
the dorsal wall of the coelom. Above the heart these receive the open- 
ings of other large sinuses, such as the anterior cardinal sinus, running 
above the gills and collecting blood from the head by way of an orbital 
sinus, and the jugular, lateral cardinal, subclavian, and other sinuses from 
the body wall. Blood then passes round the oesophagus in the two 
ductus Cuvieri into the sinus venosus, where hepatic sinuses also open. 

The resistance offered by a vessel to flow within it decreases with 
approximately the fourth power of the diameter, therefore the large 
size of these vessels substantially assists in allowing return to the 
heart. The heart-muscles, like any others, require antagonists; they 
can contract in one direction only, and each chamber therefore needs 
to be actively dilated. It will be noted that the fish heart consists of 
a series of three muscular chambers, presumably because the low 
venous pressure is able to dilate only a chamber with very thin walls, 
such as the sinus venosus. Contraction of the sinus then inflates the 
auricle, and the auricle inflates the ventricle, which thus constitutes 
the third step in this serial pressure-raising system. In the land animals, 
where most of the blood only passes through a single set of capillaries, 
a two-step system (auricle and ventricle) is sufficient for each part of 
the circulation. 

Little is known of the control of the circulation but it is probably 
less effective than in higher animals. There is a cardiac branch from 
the vagus ending in an elaborate plexus in the sinus venosus (Fig. 104). 
Stimulation of this nerve slows the heart. There is no anatomical or 
physiological evidence of a sympathetic nerve to the heart, but 
abundant sympathetic fibres run to the arteries. Small doses of adren- 
aline cause prolonged rise of blood-pressure. 

There are receptors in the efferent branchial vessels and in the post- 
branchial plexus above the cardinal veins (p. 175). Nerve impulses 
from these receptors can be recorded in the vagus at each systole and 
are increased by raising the blood-pressure. Their reflex effects are 
to slow the heart and respiration and decrease the blood-pressure, 
perhaps for protection of the gill capillaries. These reflexes are pre- 
sumably the ancestors of the carotid sinus and similar reflexes of land 


13. Urinogenital system 

The blood of the elasmobranchs differs from that of all other verte- 
brates in its very high content of urea. As measured by the depression 
of the freezing-point the blood is isotonic with the surrounding sea 
water (say, 3-5 per cent. NaCl); it may even be slightly hypertonic. 
But there is far less salt in the blood than in the sea, in fact only 
about 1-7 per cent. NaCl. Although the blood is nearly isotonic with 
the sea its composition is therefore regulated (homeosmotic). This 
arrangement is apparently a legacy of the fact that the ancestors of the 
elasmobranchs were originally fresh- water animals (p. 187). The 
return passage to the sea has been accomplished by the elasmobranchs 
through the device of urea retention. The gill surfaces, in which alone 
the blood comes into close contact with sea water, are not permeable 
to urea, but this substance penetrates freely into the tissues, as it does 
in other animals. Elasmobranch tissues if placed in sea water are 
therefore in contact with a strongly hypertonic medium. They are so 
habituated to the presence of urea that they are unable to function 
unless it is present in a concentration that would be toxic to most 

This arrangement has presumably been responsible for the fact 
that few of the elasmobranchs have returned to fresh water. In the 
case of the saw-fish Pristis, which lives some hundreds of miles 
up the Mississippi and various rivers in China, Smith found that a 
considerable concentration of urea is still maintained in the blood, 
thus further increasing the work that these fishes, like any fresh-water 
animal, must do in order to maintain an osmotic concentration above 
that of the surrounding water. One shark (Carcharhinus nicaraguensis) 
and some rays, Trygon, also live in fresh water. 

In the ordinary marine elasmobranchs the high urea concentration 
is maintained by the presence of a special urea-absorbing section of 
the kidney tubules. The urinary apparatus is a mesonephros and 
these fishes show a considerable specialization in that the urinary 
functions of this organ are separated from its generative ones in the 
male. The hinder part of the kidney (sometimes called opisthone- 
phros, the term metanephros should be used only for the definitive 
kidney of amniotes, which has a different method of development) 
consists of a mass of tubules ending in very large glomeruli, and a 
section of each tubule has the function of urea absorption. All the 
tubules join to form a series of five urinary ducts and these enter a 
urinary sinus, opening to the cloaca. The sinus can be compared 


functionally with a bladder, but it is a mesodermal structure, derived 
from the main kidney duct, and not strictly comparable to the endo- 
dermal bladder of tetrapods. The urinary sinus is a small organ and 
the volume of liquid excreted is small. 

Fie. 103. A. Urinogenital system of the female, B, of the male dogfish. 
ah.p. abdominal pores; cl. cloaca; cp. claspers of the male; F. rudiment of the oviducal opening 
in the male; Md. urinary ducts; mtn. hinder (excretory) part of mesonephros; od. oviduct; 
oe. cut end of oesophagus; of. oviducal funnel; og. oviducal gland; ov. ovary; P.f. pelvic fins; 
R. rectum; s.s. sperm-sacs; T. testis; up. urinary papilla in the female; ugp. urogenital papilla 
in the male; vs. urinary sinus; vc. vasa efferentia; vs. vesicula seminalis; WD. Wolffian duct; 
Wg. Wolffian gland or mesonephros. (After Bourne, from Goodrich, Vertebrata, A. & C. 

Black, Ltd.) 

The genital system is highly specialized to allow internal fertiliza- 
tion and the production of a few very yolkv and well-protected eggs. 
There is a single large ovary, from which the eggs are carried by the 
cilia of the peritoneum to a pair of funnels lying on either side of the 
liver behind the heart (Fig. 103). These are apparently formed from 
proncphric funnels and the Mullerian duct (oviduct) separates from 
the original nephric duct. In the adult it becomes a thick-walled 
muscular tube, bearing a swelling, the nidamental gland, the upper 
part of which produces albumen, the lower the horny egg case. 


The testes are paired and sperms are collected at their front ends 
by vasa efferentia leading into the anterior or reproductive portion of 
the mesonephros. This consists of a much coiled, thick-walled, vas 
deferens, whose glands produce material that aggregates the sperms 
into spermatophores. The vas expands into a broader ampulla 
(seminal vesicle), which at its lower end gives off a forwardly directed 
blind diverticulum, the sperm sac, developmentally the lower end of 
the Miillerian duct, reduced of course in the male; small funnels are 
still visible at the upper end. 

Transmission of the sperms is produced by a large and complicated 
pair of claspers. These are modified parts of the pelvic fins of the 
male, developed into scroll-like organs and containing a pumping 
mechanism and erectile tissue; they are inserted into the female 
cloaca. The mechanism of erection is operated by nerves and may 
involve the liberation of adrenaline; experimental injection of that 
substance will produce erection, and it is perhaps significant that the 
male possesses a reserve of adrenaline-producing tissue (see p. 167). 

Development of elasmobranchs is by partial cleavage, producing a 
blastoderm, perched on the top of a large mass of yolk. The egg is 
protected by an elaborate egg-case, the 'mermaid's purse', within 
which development proceeds until the yolk has been used up. 

In several elasmobranchs development is viviparous, the oviduct 
forming a 'uterus'. In Mustelus there is a yolk-sac placenta, but in 
Trygon 'uterine milk' is secreted into the embryo by villi (trophone- 
mata) inserted through the spiracles. 

14. Endocrine glands of elasmobranchs 

Elasmobranch fishes possess the full complement of endocrine 
glands, but these show some interesting differences from those of 
higher vertebrates. The pituitary body lies in the usual place below 
the diencephalon and anterior, intermediate, tuberal, and neural 
divisions can be recognized. Little is known of the functions of the 
gland. The gonads of the dogfish retrogress after removal of the pitui- 
tary. Little or no vasopressin or oxytocin is present. The neuro- 
intermediate lobe contains a substance that produces the expansion 
of melanophores. Hogben and Waring have also produced evidence 
that the pars anterior produces a substance causing contraction of the 
melanophores, but this has not yet been isolated and the evidence for 
its existence is indirect. 

The thyroid is formed by a downgrowth from the floor of the 
pharynx, to which it often remains attached by a narrow stalk con- 

v. i 4 



sp n 

Fig. 104. Dissection of suprarenal bodies and sympathetic nervous system of the 

b.a. brachial artery; c.a. coeliac artery; d.a. dorsal aorta; g. first sympathetic ganglion; hyp. 
hypoglossal nerve; I.e. longitudinal sympathetic 'chain'; n.card. cardiac branch of vagus; 
p.b.p. post-branchial plexus; r.c. ramus communicans; s. sensory fibre; s.a. segmental artery; 
sg. sympathetic ganglion; sp.a. anterior splanchnic nerve; sp.m. middle splanchnic nerve; 
spa. spinal nerve; sup. suprarenal body; v. ventricle; v.d. vas deferens; vs. vago-sympathetic 
anastomosis; X. vagus; branchial branch of vagus; X.visc. visceral branch of vagus. 
(After Young, Quart. J. Micr. Sci. 75.) 

taining a small ciliated pit, a reminder that the organ was once a 
ciliated mucus-secreting gland. 

The adrenal tissue is especially interesting because the two parts, 
so closely associated in mammals, are here found widely separated. A 
segmental series of glands, the suprarenals, are rich in noradrenaline. 
They project into the dorsal wall of the posterior cardinal sinus and can 
be seen when it is opened (Fig. 104). The more anterior ones are 
fused to form an elongated structure on either side of the oesophagus. 

(i 66) 

n v 

Fig. 105. Diagram of transverse section through hind region of mesonephros of 


cv. cardinal vein; da. dorsal aorta; int. interrenal body; k. mesonephros; I c. longitudinal 

sympathetic connective; n c. sympathetic nerve-cells scattered in suprarenal body; nv. 

sympathetic nerves; re. ramus communicans; sg. sympathetic ganglion; sv. subcardinal vein; 

sup. suprarenal body. (From Young, Quart. J. Micr. Sci. 75.) 

Fig. 106. Diagram of arrangement in hinder mesonephric region of dogfish. 
Lettering as Fig. 105. tr. transverse sympathetic nerve. (From Young, Quart. J. Micr. Sci. 75.) 


The sympathetic ganglia are closely associated with these suprarenal 
bodies, as would be expected from their common origin from cells 
of the neural crest. The segmental series continues along the whole 
length of the abdomen, the more posterior members being embedded 
in the kidney tissue (Fig. 105). These posterior suprarenal bodies are 
larger in the male than in the female, but only the central part of the 
male glands shows the reaction with chrome salts that indicates the 
presence of adrenaline. The peripheral portion of each gland appears 
to consist of non-functioning cells, possibly a reserve used only during 
reproduction (see p. 164). 

The part of the adrenal corresponding to the cortex of mammals is 
represented in elasmobranchs by the interrenal bodies, lying medially 
in some species, paired in others, in the kidney region (Figs. 105 and 
106). The cells of these organs resemble cortical adrenal cells. Since 
they are not in contact with the suprarenals at any point, it would seem 
that the association of the two parts is not necessary for their function- 
ing, at least in these animals. Removal of the interrenal is always fatal. 
The gland is stimulated by 'stress' or by mammalian ACTH. Extracts 
of it prolong the life of adrenalectomized rats. There is evidence that 
it influences carbohydrate metabolism and activity of the gonads but 
not electrolyte balance. 

The islets of Langerhans contain two cell types as in mammals. 
The pineal body is small and without any trace of eye-like structure. 

The gonads contain endocrine organs, producing steroid hormones. 
These are formed by interstitial cells in the testes. Oestrogens probably 
come from the outer (theca) cells of the follicles that surround the 
eggs. The inner (granulosa) cells of the capsule assist in yolk produc- 
tion but may also produce progesterone and in viviparous species 
they develop into a distinct corpus luteum after ovulation. 

15. Nervous system 

The brain is large and well developed in elasmobranchs, having a 
structure characteristically different from that of both the cyclostomes 
and bony fishes (Fig. 100). The forebrain is large and has cerebral 
hemispheres thickened both in floor and roof, whereas in teleosts the 
roof is thin. The hemispheres are wide relative to their length and the 
end of the unpaired portion of the forebrain between the hemispheres, 
the lamina terminalis, is also much thickened. Attached to the ends 
of the cerebral hemispheres are large olfactory bulbs and there are 
also large nasal sacs. Evidently the olfactory sense is well developed 
in these animals and they depend greatly on it for hunting. 

1 68 


v. 15 

All parts of the cerbral hemispheres receive fibres from the olfac- 
tory bulbs and the forebrain serves mainly for analysing the olfactory 
impulses. However, it is stated that there are fibres reaching forward 
to one area at the back of the roof of the hemispheres from other 
centres. Johnston therefore called this region the 'general somatic 
area' and suggested that it represents the beginnings of that develop- 
ment so characteristic of mammals by which all the senses are centred 
on the cerebral hemispheres. Further work is needed to confirm the 

Dec interhemisph 

., Tr medianus 

Ventr o/f 

Tr olFacb. 

Tr olFacb. epistr cruc. 

Fiss Urn tel. 

Ventrical, /at. 

Fig. 107. A cross-section through the forebrain of a shark. 

Dec. interhemisph. decussatio interhemispherica; fissura limitans telencephali; 

Prim. hip. primordium hippocampi; 5. septum; Striat. striatum; Tr. medianus. tractus 

medianus; Tr.oljact. tractus olfactorius; Tr.olf act. epistr. cruc. tractus olfacto-epistriaticus 

cruciatus; ventriculus lateralis; Ventr. o.f. ventriculus olfactorius. 

(From Kappers, Huber, and Crosby.) 

existence of this pathway, and even if present its significance must 
not be exaggerated. There is of course no cortical arrangement of 
tissue in the hemispheres. The cells form thick masses around the 
ventricle (Fig. 107). The roof is quite thick and contains decussating 
fibres in the midline. The sides and floor make up the main bulk of the 
organ, the lateral wall being known as the striatum, its upper part the 
epistriatum. The medial wall is known as the septum and its upper 
portion is often referred to as the primordium hippocampi, having a 
position similar to that of the hippocampus of mammals. The main 
efferent pathways are tracts leading to the hypothalamus and to the 
optic lobes. After removal of the forebrain the sense of smell is lost 
but the fish shows no obvious disturbance of posture, locomotion, or 

The diencephalon is a narrow band of tissue, there are no extensive 
tracts leading forward through it, and the optic and other pathways 
do not end here as they do in higher animals. The lower part of the 


between-brain, the hypothalamus, is, however, as well developed 
(relatively) in these animals as in mammals. Its hind part (inferior 
lobes) receives olfactory impulses via the forebrain (the 'fornix' of 
higher vertebrates) and gustatory pathways from the medulla. Its 
efferent fibres run to reticular centres. The more anterior part of the 
hypothalamus lies above the pituitary and contains the supraoptic 
nucleus, whose axons form the hypophysial tract, ending in the inter- 
mediate lobe. The supraoptic cells of all vertebrates are large and 
contain granules of neurosecretory material that is probably passed 
down the axons and liberated in the pituitary. The anterior hypo- 
thalamus is a higher centre for visceral control, regulating, for 
example, circulation, respiration, and many metabolic activities. 
Attached to the hind end of the hypothalamus of fishes is a peculiar 
organ, the saccus vasculosus, with folded, pigmented walls. It has 
been suggested that this acts as a pressure receptor, since it is well 
developed in deep-sea fishes. It is one of the characteristic features 
that the sharks and bony fishes have in common. 

The midbrain, as in cyclostomes and teleosteans, is very large and is 
perhaps the dominant centre of the brain. The optic tracts end in its 
roof (tectum opticum) after complete decussation below the brain. 
The cells of the tectum are arranged in a complicated pattern of 
layers. Other sensory centres that send tracts to the optic lobes are 
the olfactory (cerebral hemispheres), acustico-lateral, cerebellar, 
gustatory, and probably also the general cutaneous centres of the 
spinal cord. Efferent tracts leave the midbrain roof to the base of 
the midbrain and extend backwards into the medulla, perhaps into the 
spinal cord. The efferent midbrain fibres have direct influence on 
the spinal cord, and electrical stimulation of points on the tectum 
opticum produces various movements of the fins, suggesting a system 
of control similar to that exercised over spinal centres by the cerebral 
cortex of mammals through the pyramidal tract. Various forced 
movements follow injury to the midbrain. 

The cerebellum is a very large organ in clasmobranchs, as in all 
animals that move freely in space. Its main source of sensory fibres is 
from the ear and from the organs of the lateral line system, whose 
afferent fibres enter through the seventh, ninth, and tenth cranial 
nerves. The internal structure of the cerebellum is very uniform and 
essentially similar in all vertebrates. Removal of portions of it from 
dogfishes produces aberrations of swimming. 

The medulla oblongata is the region from which most of the cranial 
nerves spring and especially those that regulate the respiration and 


visceral functions. In mammals this control is indirect, but in fishes 
the nerves that spring from the medulla directly innervate the 
respiratory muscles of the gills and floor of the mouth. It is no doubt 
for this reason that the centre for the initiation of the respiratory 
rhythm developed in the medulla. 

16. Receptor-organs of elasmobranchs 

The paired nasal sacs have much-folded walls. Water enters by a 
single opening but this may be partly divided by a fold, making a 
groove, which may open to the mouth. There are taste-buds scattered 
over the wall of the pharynx. It has been shown experimentally that, 
as in higher animals, these are receptors for sampling the food after 
it has been brought close to the animal, whereas the nose acts as a 
distance receptor. Smell and taste are therefore different senses for a 
dogfish, as for us. By training fishes to discriminate between various 
substances it can be shown that those that we should smell are 
detected by the nose in the dogfish, but its organs of taste, like ours, 
can discriminate only between a few qualities, including salt, sour, 
and bitter. 

The eyes are well developed in sharks and no doubt serve as an 
important means of finding the prey and avoiding enemies. However, 
the retina usually contains only rods, and visual discrimination is 
probably poor, but there are cones in Mustelus and Myliobatis. Unfor- 
tunately details as to the functional performance of the eyes, ability to 
discriminate shapes, &c, are scanty. Behind the retina there is often a 
reflecting layer, the tapetum lucidum. This may be provided with 
pigment cells, which expand in the light but contract in darkness, 
allowing the underlying guanophores to reflect, thus increasing 
sensitivity. The lens is spherical and very hard, as in all fishes, since 
it must perform the whole work of refraction. It is provided with a 
protractor-lentis muscle, presumed to produce active accommodation 
for near vision by swinging the lens forward. The iris is peculiar in 
those elasmobranchs that hunt by day; when it narrows it divides 
the pupil into two slits by the descent of an upper flap or operculum. 
The muscles of the iris are better developed in elasmobranchs than 
in most bony fishes and the pupil makes wide excursions. The 
sphincter iridis muscle, which narrows the pupil, works as an inde- 
pendent effector. It is stimulated to contract by light, but its move- 
ments are not controlled by any nervous mechanism. The radial 
dilatator fibres, which open the pupil, receive motor-fibres from the 
oculomotor nerve. The closure of the iris when illuminated is 


relatively slow. If the whole eye is cut out from the head, in the dark, 
the sphincter, being an independent effector, still closes when illumi- 
nated. The muscle, being without nerves, is not affected by any of the 
usual drugs that mimic action of the autonomic nervous system, 
though some of these affect the innervated dilatator muscle. We have 
therefore the curious situation that no 'autonomic' drugs applied to 
the isolated dark adapted eye cause closure of the pupil ; this can only 
be produced by illumination (Fig. 108). 

The ear of elasmobranchs contains receptors concerned (1) with 
maintenance of muscle tone, (2) with angular accelerations, (3) with 




Adrenaline j//00,000 


Fig. 108. Movements of margin of pupil of an isolated iris of the shark Mustelus, 
followed by plotting with a camera lucida and here shown magnified 53 X . Addition 
of adrenaline causes slight dilation of the already dilated pupil and illumination then 
causes closure. Acetyl choline even in concentrations of 1 in 10,000 has a similar 
dilatory effect. (From Young, Proc. Roy. Soc. B. 112.) 

gravity, (4) perhaps with hearing. There are three pairs of semi- 
circular canals, each with an ampulla containing receptor cells, whose 
hairs are embedded in a gelatinous cupula. This behaves as a highly 
damped torsion pendulum, swinging with movement of the fluid. 
These receptors discharge impulses continuously and during angular 
rotations the frequency is either increased or decreased in the appro- 
priate ampullae, initiating compensatory movements of the eyes and 

The otolith organs include three patches of receptor cells in par- 
tially distinct sacs, the utricle, saccule, and lagena. The endolym- 
phatic duct is an open canal and in some species serves to admit sand 
grains, which are attached to the maculae as gravity receptors. The 
utricle seems to be the main receptor producing appropriate postures 
in relation to gravity. The lagena shows a maximum discharge rate 
near the normal position of the head and thus serves as an 'into level' 
receptor. The areas of these maculae that carry otoliths do not 
respond to vibrational stimuli but carry only gravitational receptors. 
Vibration responses in the form of nerve impulses have been seen 
in rays but only up to 120 c/sec, although vestibular microphonics 
up to 750 c/sec occur. At high intensity there is much synchronization 


of units. These results suggest that the ear may function as a vibration 
receptor, but there are no conditioning experiments to show whether 
these fishes can hear. 

There is a well-developed system of lateral line organs, whose 
function is considered later (p. 218). The organs of this system on the 
head are highly modified in elasmobranchs to form the ampullae of 
Lorenzini, long canals filled with mucus. Sand showed that these 

Fig. 109. Drawing of a sympathetic ganglion and related structures in a dogfish. 
Lettering as in Figs. 104 and 105. s.o. sense-organs. (After Young, Quart. J. Alter. Sci. 75.) 

organs increase their discharge of nerve impulses with very slight 
falls of temperature, and he suggested that their function is to detect 
such changes. They are also sensitive to weak tactile stimulation and to 
small voltage gradients in the water. Their function therefore remains 
uncertain. It may be related to determining changes of hydrodynamic 
pressure distribution over the surface of the aerofoil-like body, 
especially in skates and rays. They may thus act as mechano-receptors 
detecting local changes of pressure near the body surface. 

No doubt elasmobranchs, like other animals, have many senses 
referred to the skin, such as we call touch, pain, and the like, but few 
studies of these exist. Sand has shown the presence of volleys of 
impulses in the nerves connected with muscles when the latter are 
stretched. Proprioceptors have been demonstrated histologically in 
the muscles of Raja. This agrees with the fact that after severance of 
the spinal cord the swimming rhythm only continues if some afferent 
nerves are intact. 

v. 17 



17. Autonomic nervous system 

The sympathetic system of elasmobranchs consists of an irregular 
series of ganglia, approximately segmental, lying dorsal to the pos- 
terior cardinal sinus and ex- 
tending back above the kidneys. 
These ganglia contain motor 
nerve-cells (post - ganglionic 
cells) whose ascons end in the 
smooth muscles either of the 
arterial walls or of the viscera. 
The cells themselves are con- 
trolled by pre-ganglionic nerve- 
fibres whose cell bodies lie in 
the spinal cord and whose pro- 
cesses run out in the ventral 
spinal roots and rami com- 
municantes (Fig. 109). In 
higher animals the sympa- 
thetic ganglia send postgangli- 
onic fibres back to the spinal 
nerves for distribution to the 
skin ('grey rami communi- 
cantes') but these are absent in 
elasmobranchs and correspon- 
dingly there is no evidence of 
sympathetic control of skin 
functions (e.g. chromato- 
phores); a very different con- 
dition is found in bony fishes 
(p. 222). Another peculiarity 
of the sympathetic system of 
elasmobranchs is that it does 
not extend into the head. This 
condition is unique among 
vertebrates, but it is not clear 
whether it is primary or the 
result of a secondary loss. 

In mammals it is usual to 
recognize a parasympathetic 
system acting in antagonism to 


Fig. i 10. Diagram of the autonomic nervous 

system of the dogfish. 
art. artery; card.n. cardiac nerve; cil.g. ciliary gang- 
lion; ft. heart; in. intestine; k. mesonephros; ov. 
oviduct; ph. pharynx; pr. profundus nerve; py. 
pylorus; st. stomach; symp. sympathetic ganglion 
(with suprarenal near it); u.s. urinogenital sinus; 
III, V, VII, IX, X, cranial nerves. (From Young, 

Quart. J. Micr. Sci. 75.) 


the sympathetic, but this is not easy to define in the elasmobranchs 
(Fig. no). The vagus, it is true, is well developed, with branches 
to the heart and gut, but little is known of autonomic fibres in the 
other cranial nerves, or of a special 'sacral' parasympathetic system. 
Stimulation of either the vagus or the sympathetic nerves causes 
contraction of the stomach. A ciliary ganglion connected with the 
oculomotor nerve is present as in other animals, but there is no 
sense in which it can be called antagonistic to the sympathetic 
system, since the latter does not extend into the head. The post- 
branchial plexus is a network of fibres and cells connected with the 
vagus but stretching back above the posterior cardinal sinus 
(Fig. 104). Receptors in this plexus and in the afferent branchials 
(Fig. 109) may be concerned with vascular reflexes (p. 161). 



1 . Characteristics of elasmobranchs 

The organization of a shark used to be considered to show the earlier 
stages of fish evolution, but we have seen evidence that this is a mis- 
take (p. 131). The sharks and skates and rays are highly developed 
creatures; in particular, the absence of bone is a secondary feature; 
they have been able to give up their defensive armour because of the 
development of other means of protection, swift swimming, good 
sense-organs and brain, and powerful jaws. We can now examine the 
history of these changes and study the varied creatures that can be 
classified as elasmobranchs. As usual in examining such histories we 
must try to discover evidence about the forces that have operated to 
produce the changes of type, and look for signs of any consistent 
trends, persisting for long periods of years. 

2. Classification 

Superclass Gnathostomata 
Class Elasmobranchii ( = Chondrichthyes) 
Subclass 1. Selachii 
*Order 1. Cladoselachii. Devonian-Permian 

*CIadoselache; *Goodrichia 
*Order 2. Pleuracanthodii. Devonian-Trias 

*Pleur acanthus 
Order 3. Protoselachii. Devonian-Recent 

*Hybodiis; Hetcrodontus 
Order 4. Euselachii. Jurassic-Recent 
Suborder 1. Pleurotremata. Jurassic-Recent 
Division 1. Notidanoidea. Jurassic-Recent 
Hexanchus ; Clilamydoselache 
Division 2. Galeoidea. Jurassic-Recent 

Scyliorhinus; Mustelus; Cetorhinus; Carcharodon 
Division 3. Squaloidea. Jurassic-Recent 
Squalus; Sqaatina; Pristiophorus ; Alopias 
Suborder 2. Hypotremata. Jurassic-Recent 
Raja; Rhinobatis; Pristis; Torpedo; Trygon 


Superclass Gnathostomata (cont.) 

Subclass 2. Bradyodonti. Devonian-Recent 
*Order 1. Eubradyodonti. Devonian-Permian 

Order 2. Holocephali. Jurassic-Recent 


The elasmobranchs form a very compact group of fishes, nearly 
always marine and of predaceous habit, having a great quantity of 
urea in the blood, with no bone in the skeleton, no operculum over 
the gills, and no air-bladder. The tail is usually heterocercal. The 
pectoral fin is anterior to the pelvic and the latter is usually provided 
with claspers, fertilization being internal. The body is more or less 
completely covered with placoid scales (denticles) and these are 
specialized in the mouth to form rows of teeth. The intestine is short 
and provided with a spiral valve. The typical cartilage-fishes with 
these characters may be placed in the subclass Selachii, to distinguish 
them from an early aberrant offshoot the Bradyodonti, represented 
today by the peculiar creature Chimaera (p. 184). 

3. Palaeozoic elasmobranchs 

The selachians are among the most numerous of the various pre- 
datory animals in the sea. There have, however, been many side- 
branches of the main shark line and we may now survey the history 
of the group from its first appearance. The characters we have used 
in our definition mark the elasmobranchs off from the earliest-known 
gnathostomes, the acanthodians and other placoderm types (Fig. 1 1 1), 
which we shall consider later (p. 186). Presumably the elasmobranchs 
were derived from some placoderm, but the earliest evidence of the 
existence of true sharks is in the form of isolated teeth and scales from 
Middle Devonian deposits, and the earliest type about which full 
information exists is *Diade?nodus from the Upper Devonian, 'an 
early and not distant offshoot from the primitive Chondrichthyan 
stock, the main line of which led through *Ctenacanthus and the 
hybodonts to the modern elasmobranchs ; *Cladoselache is a specialized 
side-line of this main stock and is not an appropriate ancestral type 
for the Chondrichthyes' (Harris). The teeth of *Diademodus are 
many-cusped and resemble the scales more closely in sculpturing 
than in other primitive sharks. The jaw suspension was amphistylic 
and the notochord unconstricted. The pectoral fin was continuous 
posteriorly with the body wall and there was no well-developed 










, t ha 

,. .„, Torpedo- 


AcMtnedu ^V^vxi L I f) 


S. * 





FlG. hi. The early evolution of vertebrates. 

i 7 8 


VI. 3 

pectoral girdle. The tail was heterocercal and there are no signs of skele- 
tal support for lateral keels. All of these Harris regards as primitive 
features; *Diademodus was specialized in having no spines in front 
of the dorsal fin and no clasper on the head. Both of these features are 
frequent in hybodonts and in *Cladoselache there is a large spine 

zd nsi 

Fig. 112. Development of the fins of the dogfish, i, Adult showing the nerve-supply 
of the fins ; 2, adult with the fins shown expanded and their nerves and muscles shown 
as if concentration had not taken place; 3, a 19-mm. embryo, showing the actual 


a. anal fin; ac. anterior collector nerve of first dorsal fin; cr. (black) cartilaginous radial 

partially hidden by the radial muscle; n. 1-57, spinal nerves and ganglia; pc. collector 

nerve of second dorsal fin; pi. pelvic fin; pt. pectoral fin; rm. radial muscle; id. and 2d. 

first and second dorsal fins. (From Goodrich, Vertebrata, A. & C. Black, Ltd.) 

in front of the first dorsal fin. These fishes were thus like modern 
sharks in their general form, but the fins were remarkable in having 
a broad base, not sharply marked off from the body- wall. It has been 
suggested by Goodrich and others that this was the earliest condition 
of the pectoral fin, perhaps showing its derivation from a continuous 
or extended fin-fold (Fig. 113). This theory has the advantage that it 
agrees with the embryological development of the fin by concentration 
of a series of segments (Fig. 112). It also seems likely that anterior 
and posterior fins expanded in the horizontal plane would be neces- 
sary for stabilization (p. 136). Moreover, this theory of the origin of 
paired fins has the great advantage that it compares them with the 
median fins, which are also continuous folds. It has been argued, 


however, that the cladoselachians are very far from the earliest known 
fishes and that in both ostracoderms (p. 125) and placoderms (p. 186) 
fins are known that have a narrowly constricted base. We cannot 
yet say for certain what has been the course of evolution of the paired 
fins, but the fin-fold theory has much plausibility, in spite of the 
difficulties raised by palaeontologists. 

Fig. 113. Pectoral fins of various fishes. 
a, *Cladoselache\ b, *Pleur acanthus; c, Ncoccratodus; d, Gadits. (From Norman.) 

The cladoselachians represent the ancestral Devonian sharks, from 
which all later forms have been derived. Animals of similar type 
were fairly common in late Devonian and Carboniferous seas. The 
ctenacanths, such as *Goodrichia, reached a length of 8 ft. Later 
radiation of the selachians took place along three different lines, 
represented by the three remaining orders shown in the classification. 
The pleuracanthodians (*Pleuracanthus) were a specialized group of 
freshwater carnivores. The tail was straight (diphycercal) and the 
paired fins had become modified accordingly (see p. 137). The axis 
was completelv freed from the body wall to give a paddle-like fin, 
with pre- and post-axial rays, a type known as archipterygial (Fig. 
113), because it was once supposed to be ancestral to all others. A 
large spine on the head gives the group its name. Claspers were pre- 
sent. These animals were common in the Carboniferous and Lower 


Permian, but in subsequent times they disappeared without leaving 

4. Mesozoic sharks 

After flourishing in Palaeozoic seas the shark line seems to have 
become nearly extinct during the Permian and Trias. During this 
period there was probably little fish life in the sea and the stock 
seems only to have survived by adopting a varied diet, including 
invertebrate food. The protoselachian or heterodont sharks of this 
period had two types of tooth, pointed ones in front and flattened 
ones, for crushing molluscs, behind. Heterodontus, the Port Jackson 
shark of the Pacific, is a surviving form having a dentition of this 

There is total cleavage of the yolk of the egg. The meroblastic form 
typical of modern elasmobranchs and teleosts was therefore a rela- 
tively late development and other survivors of the mesozoic period 
besides Heterodontus also show holoblastic cleavage (pp. 184-236). In 
later Triassic times sharks again became more abundant, and this 
agrees with the presence of numerous bony fish types, on which they 
presumably fed. Some of the Triassic sharks still possessed a hetero- 
dont dentition (*Hybodus), though otherwise much like the modern 

In Jurassic times or earlier, however, the sharks divided into the 
main lines that exist today. In the suborder Pleurotremata or true 
sharks the teeth all became sharp and the animals swift swimmers. In 
the suborder Hypotremata, on the other hand, the teeth remained 
flattened and sometimes became highly specialized for a mollusc- 
eating diet (Fig. 1 14), producing the flattened bottom-living creatures, 
the skates and rays. The stages of this transition can be followed, and 
some of the intermediate types still exist. Thus in Rhifiobatis, the 
banjo-ray (Fig. in), the pectoral fins are enlarged but still distinct 
from the body. Almost identical creatures have been found in Jurassic 
rocks. It is probable that several separate lines showed this flattening 
of the body. 

5. Modern sharks 

The Pleurotremata may be divided into three divisions all dating 
from the Jurassic. The Notidanoidea show many primitive features, 
such as an amphistylic jaw, the presence of six or seven gill-slits, and 
an unconstricted notochord. Hexanckus and Heptranchias, are long- 
bodied, slow-moving sharks from warm waters. They are viviparous 

vi. 5 



but without placentae. Chlamydoselache, the frilled shark, lives in 
deep water and feeds on cephalopods. The division Galeoidea is much 
larger and includes the sharks with two dorsal fins, not supported by 
spines. Here belong the dogfishes Scyliorhinus and Miistelus, both 
mainly bottom-living animals feeding on a mixed diet, including 

Fig. 114. Teeth of various elasmobranch fishes. 

1, Man-eater (Carcharodon); 2, tiger shark (GalaeocerJo); 3, comb-toothed shark (Hexanchus); 

4, sand-shark (Odontaspis); 5, blue shark (Carcharinus); 6, nurse shark (Ginglymostoma); 

7, guitar rish (Rhina), 8, eagle-ray {Myliobatis), (After Norman.) 

crustaceans and molluscs. In Cetorhimis, the basking shark, the pre- 
daceous habit of the group has been abandoned in favour of straining 
small food directly from the plankton by means of special combs on 
the gills (gill rakers), an arrangement recalling that of the whalebone 
whales. The great effectiveness of this method of feeding may be seen 
in the length of 35 ft or more attained by some of these sharks. Bask- 
ing sharks produce very numerous small eggs, which develop within 
an 'uterus', but without placentae. Rhineodon, the whale shark, is also 


a plankton feeder and becomes very large. It is not closely related to 
the basking sharks. It moves up and down vertically, the mouth open, 
sucking in plankton. In this group there are also many of the fiercest 
man-eating sharks, such as Carcharodon, often 30 ft long, found in 
many seas. Some fossil forms of this genus are estimated to have 
reached a much greater length, possibly of 90 ft. 

The division Squaloidea includes those sharks in which there is 
a spine in front of each dorsal fin. They are not, however, otherwise 
different in habits from the other sharks. The spiny dogfish (Squalus) 
is a well-known type and here belong also the saw-sharks (Pristio- 
phorus) and a group of bottom-living forms, the angel-fishes or monks 
[Squatina), which acquire a superficial similarity to the skates and 
rays. Alopias, the thresher, is said to differ from most sharks in that 
instead of seizing the prey as it is presented, it hunts systematically, 
several sharks working together and using their whip-like tails to 
drive smaller fishes such as mackerel into shoals, where they are then 

6. Skates and rays 

The Hypotremata, skates and rays, have become specialized for 
life on the bottom of the ocean in shallow waters, feeding mainly on 
invertebrates, and usually having blunt teeth (Fig. 114). Locomotion 
is no longer by transverse movements of the body but by waves that 
pass backwards along the fins. In the earlier stages, such as Rhino- 
bath, the banjo-ray, which has existed from the Jurassic period to the 
present, the edges of the fins are still free and the tail is well developed. 
In Pristis, another saw-fish type, outwardly similar to Pristiophorus 
and known since the Cretaceous, the head is drawn out into a long 
rostrum armed with denticles. Its use is uncertain but the head strikes 
from side to side among shoals of fishes. There are species in India, 
China, and the Gulf of Mexico that live in fresh water. In Raja, first 
found in the Cretaceous, the pectoral fins are attached to the sides of 
the body and the median fins are very small, whereas in the more 
recent Trygon and other sting-rays the tail is reduced to a defensive 
lash, the dorsal fin persisting as a poison spine. In the eagle-rays 
(Myliobatis) the teeth are flattened to form a mill able to grind mollusc 
shells (Fig. 114). The sea-devils (Mobula) have expansions of the fins 
at the front of the head, which they use to chase fishes to the mouth, 
hunting in packs. In Torpedo, the electric ray, the fins extend so far 
forward that the front of the animal presents a rounded outline. The 
animal is protected by a powerful electric organ, formed by modified 

(i8 3 ) 



FIG. 115. Various elasmobranch. fishes. 

Chimaera ^ T 


latcral plate muscle, innervated by cranial nerves. Several species of 
Raja have weak electric organs perhaps used for guidauce (p. 253). 

Life on the bottom has produced many further modifications in the 
skates and rays. In those that live in shallow and hence well-illuminated 
waters the colour of the upper surface is often elaborate, the under 
side being white. In certain species of Raja, for example, there is a 
pattern of black and white marks, which probably serves to break up 
the outline of the fish. 

The eyes of the skates and rays have moved on to the upper surface 
of the head and are protected by well-developed lids. In most forms 
the pupil is able to vary widely in diameter and often has an operculum 
by which the aperture can be reduced to two small slits. 

There is a special modification of the respiratory system so that 
water is drawn in not through the mouth but by the spiracle, which is 
provided with a special valve that shuts at expiration, as the water is 
forced out over the gills. The Hypotremata have therefore developed 
many special features for their bottom-living habits and have diverged 
among themselves into many varied lines. They have been very 
successful and are among the commonest fishes in the sea. 

7. Chimaera and the bradyodonts 

Finally we must consider an aberrant group, the bradyodonts, which 
diverged from the main stock at least as early as the Carboniferous 
and preserves for us today some features of elasmobranch life at that 
time as the strange Chimaera, the rat-fish of deep seas (Fig. 115). 
Instead of the usual large, toothed mouth these Holocephali have a 
small aperture surrounded by lips, giving the head a parrot-like 
appearance. The teeth are large plates firmly attached to jaws, and 
the upper jaw is remarkable in being fused to the skull ('holostylic'), 
the hyoid arch being free. There is no stomach or spiral intestine. 
These peculiarities are probably associated with a capacity to eat 
small pieces of animal food. The Holocephali differ further from the 
Selachii in the presence of an opercular flap attached to the hyoid 
arch. There are also extra claspers in front of the usual pelvic ones 
and an organ on the head of the male known as the cephalic clasper, 
whose function is obscure. The notochord is unconstricted and the 
vertebrae reduced to separate nodules. The cleavage is holoblastic, 
as in other fishes with features of mesozoic type (p. 180). 

Many of the internal features resemble those of selachians, for 
instance the conus arteriosus, and urinogenitals in which there are 
separate urinary and spermatic ducts. The brain has a peculiar shape 


on account of the large size of the eyes, which almost meet above the 
brain, so that the diencephalon is long and thin. 

These strange creatures appear in the Jurassic, apparently de- 
scended from the somewhat similar bradyodonts (such as *Helodus), 
which were common in the Carboniferous and Permian. They pre- 
serve some primitive features (vertebrae, jaw support, open lateral 
line canals, cleavage) but have developed many specializations in the 
teeth, operculum, fins, and brain, probably in connexion with life on 
the bottom of deep seas. 

8. Tendencies in elasmobranch evolution 

The elasmobranchs have been in existence ever since the Devonian, 
and for much of this long period of nearly 400 million years we can fol- 
low their changes with some accuracy. This type of fish was first 
formed by loss of the heavy bony armour of the earliest gnatho- 
stomes, associated with the adoption of a rapidly moving and car- 
nivorous habit. The resulting shark-like form has remained with 
relatively little change through the whole history of the group; clado- 
selachians from the Devonian are remarkably like modern sharks, and 
it would be difficult to assert that the latter show clear signs of being 
in any way of a 'higher' type. Both are in fact suited to the same mode 
of life. 

If our interpretation of the evidence is right, however, the modern 
shark type has been evolved from the Devonian type through a hetero- 
dont stage. During the late Permian and Trias there was little fish 
food for the sharks and they appear to have taken to living on inverte- 
brates. Eating this diet was presumably easier for animals possessing 
the two types of teeth described on p. 180, and the animals also 
became rather flattened with their life on the bottom. On the 
reappearance of numerous fishes in the sea, in the Jurassic, some of 
these heterodonts resumed the shark-like habit, lost the crushing 
teeth, and developed into the varied fish-eating types alive today. 
Others of the heterodonts, however, became still more specialized for 
bottom life, as the modern skates and rays. 

It is difficult to see any persistent tendency in all this, except to eat 
other animals of some sort. When fishes are available sharks will eat 
them, and the bodily organization for doing so seems to have been 
evolved at least twice. Similarly other members of the same stock ate 
molluscs and Crustacea and became modified for this. The tendency 
is for survival or continuance of the animals and this leads them 
to adopt whatever habits are possible given their surroundings. In 


meeting the circumstances certain types will be suitable at one time, 
others at another. We know that genetic variations will produce fluctua- 
tions of type — at a time when circumstances force the animals to strive 
in one direction those with a particular bodily type, say, broad, 'hetero- 
dont' teeth will be selected. When fish food again becomes available 
those animals born with quicker habits and sharper teeth will be able 
to eat the fish and the shark type returns. 

The method of ensuring stability in the pitching plane adopted by 
elasmobranchs (p. 136) necessitates a certain flattening of the front 
end of the animal. It is not therefore surprising that this tendency is 
often exaggerated and has several times produced flattened bottom- 
living creatures, such as the skates and rays. The Actinopterygii 
show the opposite tendency, to lateral flattening (p. 248). We might 
imagine that most of the modern skates and rays had become so 
modified in structure that only life on the bottom is possible for them 
and that there could be no return to a free-swimming, fish-eating 
habit, but it would not be true to say that this is certain or that the 
past history of the group shows undoubted evidence of such irrever- 
sible specialization. 

The only general conclusion from our study of elasmobranchs since 
the Devonian, then, is that they have tended to keep alive by eating 
fish or invertebrates, that some have changed little during this time 
but that, judging especially from the modern forms, the group tends 
to produce varied types at any one time, each able to find its food in a 
special manner. It is not clear that the group has advanced, in any 
sense, since the Devonian. The type has always been a successful one, 
able to produce specialized carnivores. We do not know enough to be 
sure whether the number of creatures with this organization has 
changed greatly, but it seems that, except for a reduction in numbers 
in the Triassic, they have always been moderately abundant and are 
perhaps at present on the increase. 

9. The earliest Gnathostomes, Placoderms 

*Class Placodermi (= Aphetohyoidea) 

*Order 1. Acanthodii. Silurian-Permian (*Climatius) 
*Order 2. Arthrodira. Silurian-Devonian (*Coccosteus) 
*Order 3. Macropetalichthyida. Devonian (*Lunaspis) 
*Order 4. Antiarchi (= Pterichthyomorphi). Devonian (*Bothri- 

*Order 5. Stegoselachii. Devonian-Carboniferous (*Gemundina) 
*Order 6. Palaeospondyli. Devonian {* Palaeospondylus) 

vi. 9 PLACODERMS 187 

It has already been mentioned that the earliest gnathostome verte- 
brates found in the rocks do not have the shark-like form, and present 
so many peculiarities that they are placed in a distinct class. In the 
past the fossils included here have been referred to various groups, 
usually either to the agnatha or the elasmobranchs, and there is still 
some doubt as to their position. In many respects they are highly 
specialized, but they all have one feature that may be presumed to 
have existed in the ancestral gnathostome, namely, that the hyoid arch 
played no part in the support of the jaws and the spiracle was there- 
fore a typical gill-slit. For this reason they are often given the name 
Aphetohyoidea, but we shall prefer to call them Placodermi, to em- 
phasize that they all have a heavy armour of bone-like material. The 
class contains several orders, not obviously very closely related to 
each other; all are fossil forms, none of which is known to have sur- 
vived the Permian. 

The best-known, earliest, and perhaps most interesting group is 
the acanthodians, found in freshwater deposits extending from the 
Upper Silurian to the Permian but chiefly in the Devonian. These 
were small fishes with a fusiform body (Fig. 115), with heterocercal 
tail and two, or later one, dorsal fins. The lateral fins consisted of a 
series of pairs, often as many as seven in all, down the sides of the 
body. The effect of these in stabilizing the fish would presumably be 
different from that of a continuous fold, and the problem of the form 
and function of the earliest paired fins remains obscure. The fins were 
all supported by the large spines from which the group derives its 

The whole surface of the body was covered with a layer of small 
rhomboidal scales, composed of layers of material ressembling bone, 
covered with a shiny material similar to the ganoin of early Actino- 
pterygii. On the head these scales were enlarged to make a definite 
pattern of dermal bones, numerous at first but fewer in the later forms. 
The pattern of the bones has no close similarity to that of later fishes. 
The reduced bones of the later acanthodians are related to the lateral 
line canals, which have an arrangement similar to that in other fishes, 
but run between and not through the scales and bones of the head. 
The teeth are formed as a series of modified scales. The skull is partly 
ossified — important evidence that the boneless condition of elasmo- 
branchs was not typical of all early gnathostomes. 

The jaws of acanthodians were attached by their own processes to 
the skull (autodiastyly) and are remarkable in that four separate 
ossifications take place in them (two in the upper and two in the lower 


jaw), making a series of elements similar to that found in the typical 
branchial arches. The hyoid was an unmodified branchial arch. At 
first the mandibular, hyoid, and each of the branchial arches were pro- 
vided with small flap-like opercula, but in later forms the mandibular 
operculum became especially developed and covered all the gills. 

These animals might well represent the ancestors of many if not all 
other groups of gnathostomes. They have not the peculiar features 
that we characterize as shark-like, and though they may well have 
been carnivorous they are not very highly specialized for that mode of 
life. Whether or not the known acanthodians represent the actual 
ancestors of the other gnasthostome groups, it is clear that knowledge 
of their anatomy forces us to discard two conclusions which have 
often been accepted in the past, namely, that lack of bone and an 
amphistylic jaw support are primitive gnathostome features. Here 
already in the Silurian we find animals that possessed both endo- 
chondral bone and scales composed of bony substance. Moreover, 
some of them have no trace of denticles and we must therefore regard 
with suspicion any theory that considers the placoid scale as the 
original type of all scales. It is at least as likely that scales composed of 
simple layers of bone in the dermis were the ancestral type and that 
placoid forms with a pulp cavity were a later specialization. 

Several other types of placoderm fish are known, mostly from the 
Devonian strata. The Arthrodira, Macropetalichthyida, and Anti- 
archi (Fig. in) were mostly heavily armoured fishes with dermal 
bones on the head and often a large shield over the body. There was 
usually a heterocercal tail and a covering of scales. The earlier fishes 
were mostly from fresh water, the later from the sea. Many were 
rather flattened, probably bottom-living and invertebrate-eating 
forms. The bony plates on the head were often arranged in charac- 
teristic patterns, none of which, however, shows close similarity to 
the pattern of bones on the head of bony fishes or tetrapods. Lateral 
line canals of typical arrangement were present and the 'bones' follow 
these to some extent. 

*Gemundina was a flattened animal, superficially similar to a skate, 
from marine Lower Devonian deposits. The skin was covered with 
denticles, but under these were large plates, apparently of bone. This 
fish is placed in a special order Stegoselachii and its affinities are 
unknown, but it shows again that the tendency to develop a flattened 
form has been present from the earliest appearance of fishes. *Palaeo- 
spondylus from the Devonian is another isolated form, in the past often 
classed with the cyclostomes. Moy-Thomas showed, however, that 

vi. 9 PLACODERMS 189 

jaws were present and that probably the hyomandibula was not sus- 
pensory. He therefore classed the fish with the placoderms, in spite 
of the absence of any dermal skeleton. So far as can be discovered, 
all these placoderm fishes except the acanthodians were specialized 
types and have not left any later descendants. Indeed it may well be 
that they have been preserved only because of the great extent of their 
armour; less heavily protected relatives may have existed but have 
not survived as fossils. The remains that are known are sufficient to 
establish the fact that there were, in the Devonian period, numerous 
types of fish possessing a bony skeleton. 



1 . Introduction : the success of the bony fishes 

The acanthodians and some other of the late Silurian and Devonian 
gnathostome fishes possessed bony skeletons; from these, or some 
placoderm animals like them, may have been derived not only the 
elasmobranchs but also the bony fishes and the lung-fishes, which 
gave rise to the land animals. These presumed descendants of the 
placoderms can be divided into three groups : first the elasmobranchs, 
secondly, the crossopterygians, the lobed-fin or lung-fishes, including 
the Devonian forms that led to the amphibia, and thirdly, the actino- 
pterygian or rayed-fin fishes, culminating in the modern bony fishes. 
In Devonian times the Crossopterygii and Actinopterygii were very 
alike and both, like the placoderms, contained bone. The term bony 
fishes or Osteichthyes is often applied to these two groups together, 
since they have some features in common and distinct from the 

The great group of Actinopterygii, which, for all the importance of 
the elasmobranchs, must be reckoned as the dominant fish type at the 
present time, includes most of our familiar fishes, perch, pike, trout, 
herring, and many other types of 'modern' fish. In addition there are 
placed here some surviving relics of the stages that have been passed 
before reaching this condition, such as the bichir, sturgeons, bow-fin, 
as well as related fossil forms. 

Many groups of animals have been successful in the water; Crus- 
tacea, for instance, are very numerous and so are cephalopod molluscs 
and echinoderms, but the success of the bony fishes surpasses that of 
all others. From a roach or perch in a stream, to a huge tunny or a vast 
shoal of herrings in the sea, they all have the marks of mastery of the 
water. They can stay almost still, as if suspended, dart suddenly at 
their prey or away from danger. They can avoid their enemies by 
quick and subtle changes of colour. Elaborate eyes, ears, and chemical 
receptors give news of the surrounding world and complex be- 
haviour has been evolved to meet many emergencies. Reproductive 
mechanisms may be very complex, involving elaborate nest-building 
and care of the young; social behaviour is shown in swarming move- 
ments, which may be accompanied by interchange of sounds (p. 217). 

vii. 1-2 THE TROUT 191 

Bony fishes abound not only in the sea but also in fresh water, 
which has never been effectively colonized by cephalopods or elasmo- 
branchs. They can exist under all sorts of unfavourable or foul- 
water conditions and a considerable number of them breathe air and 
live for a time on land. Perhaps the majority are carnivorous, but 
others feed on every type of food, from plankton to seaweeds. 

To whatever feature of fish life we turn we find that the bony fishes 
excel in it in several different ways in different species. It is small 
wonder that with all these advantages they are excessively numerous. 
There are some 3,000 species of living elasmobranchs, but more than 
20,000 species of bony fish have been described. 

The number of individuals of some of the species must be really 
astronomical. For instance, at least 3,000 million herrings are caught 
in the Atlantic Ocean each year, so that the whole population there 
can hardly be less than a million million. Again, it is estimated that a 
thousand million blue-fish collect every summer off the Atlantic coast 
of the United States and, being very voracious carnivores, they con- 
sume at least a thousand million million of other fishes during the 
season of four months. This gives some idea of the tremendous 
productivity of the sea, and of the way the bony fishes have made 
use of it. Needless to say, man has also made considerable use of the 
bony fishes, which indeed provide, with the elasmobranchs, a not 
inconsiderable portion of the total of human food. 

2. The trout 

Salmo trutta, the brown trout, may be taken as an example of a bony 
fish; we shall also refer at intervals to conditions in other common 
freshwater fish such as the dace, Leuciscus, and perch (Perca fluvi- 
atilis). There is considerable confusion about the various types of 
trout and their close relatives the salmon. The brown trout is abundant 
in rivers and streams throughout Europe and is commonly about 
20 cm long at maturity, though it may grow larger. It is grey above 
and yellowish below, with a number of dark spots scattered down 
the sides of the body (Fig. 116). 

The body form is typical of that of teleostean fishes in being short, 
narrow in the lateral plane but deep dorso-ventrally, in fact more ob- 
viously streamlined than the shape of elasmobranchs. The movements 
of a trout do not at first sight obviously involve the bending of the body 
into an S; nevertheless, the method of swimming is essentially by the 
propagation of waves along the body by the serial contraction of the 
longitudinally directed fibres of the myotomes (p. 133). 



VII. 2- 

The tail differs from that of elasmobranchs in being outwardly 
symmetrical, though internally there are still traces of the upturned 
tip of the vertebral column (Fig. 118). Besides the typical caudal 
'fish-tail', supported by bony rays, there are two dorsal fins and a 
ventral fin, but the hinder dorsal fin differs from the others in having 
no rays to support it and is called an adipose fin, because of its flabby 
structure. The paired fins are rather small and it is from their struc- 
ture that the whole group derives the name Actinopterygii or rayed-fin 
fishes. There is no lobe projecting from the body and containing 

Fig. i i 6. Male and female brown trout (Salmo trutta) spawning. The male is quivering — a 

short sequence of rapid shudders of whole body which excites the female. 

(After J. W. Jones, The Salmon.) 

basal fin supports, as there is in the fin of lung-fishes. All the basal 
apparatus of the fin is contained within the body wall and only the fin 
rays project outwards, as a fan. The pelvic fin of bony fishes often 
lies relatively far forward; in the trout, however, it is unusually far 
back, just in front of the anus; in other types it may be level with the 
pectoral fin, or even anterior to it (Fig. 118). The significance of the 
shape of the body and fins in swimming will be discussed later (p. 244). 
The skin consists of a thin epidermis and thicker dermis, the former 
has stratified squamous layers but contains no keratin (Burgess, 1958). 
It contains mucous glands. The mucus of some eels and other fishes 
has remarkable powers of precipitating mud from turbid water. The 
mesodermal dermis provides an elaborate web of connective tissue 
fibres. It also contains smooth muscle, nerves, chromatophores, and 
scales. The latter are thin overlapping bony plates, covered by skin, 
that is to say, they do not 'cut the gum' as do placoid denticles. The 
exposed part of each scale bears the pigment cells, which control the 
colour of the animal, in a manner presently to be described. The bone 
of the scales is absorbed at intervals by scleroclasts, making a series 
of rings, which, like the growth-rings on a tree, are due to the fact 
that growth is not constant but occurs fast in the spring and summer 

VII. 3 



and hardly at all in the winter. The age of the fish can therefore be 
determined from these rings (Fig. 117), or from the similar markings 
on the ear stones (p. 216). While an adult salmon is in fresh water no 
growth occurs, leaving a spawning mark on the scale. 

The head of the trout shows some of the most specialized and typical 
teleostean features (Fig. 119). There are two nostrils on each side, but 
no external sign of ears. The mouth is very large and its edges are 
supported by movable bones, to be described below. The maxillary 
and mandibular valves are folds 
of the buccal mucosa, serving to 
prevent the exit of water during 
respiration. The tongue, as in 
Selachians, has no muscles, but 
may carry teeth and taste-buds. 
Behind the edge of the jaw is the 
operculum, a flap covering the 
gills and also supported by bony 
plates. In connexion with these 
special developments of jaws and 
gills the skull has become much 
modified and has developed com- 
plex and characteristic features 
(Fig. 118). 

Fig. 117. Spawning mark (sp. ?nk.), the 
result of erosion or absorption of the scale 
margin due to a calcium deficiency fasting 
period. (After J. W. Jones, The Salmon.) 

1st river winter. 2. 2nd river winter. 
3. 1 st sea winter. 

3. The skull of bony fishes 

The main basis for the skull 
is a chondrocranium and set of 

branchial arches, exactly comparable to those of the elasmobranchs. 
In the early stages of development there is a set of cartilaginous boxes 
around the nasal and auditory capsules, brain and eyes, and a series 
of cartilaginous rods in the gill arches. Bones are then added in two 
ways: either (i) as cartilage bones (endochondral bones) by the re- 
placement of some parts of the original chondrocranium, or (2) as 
membrane or dermal bones, laid down as more superficial coverings 
and considered to be derived from a layer of scales in the skin. This 
outer position of the bones can be clearly seen in many cases by the 
readiness with which the membrane bones can be pulled away from 
the rest of the skull. 

The skull bones are arranged in a regular pattern, whose broad 
outlines can be seen in all fishes and in their tetrapod descendants. 
However, there are many confusing variations and the naming of 


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bones has given much controversy. No generally acceptable theory 
has yet appeared, perhaps because we know little of the factors that 
cause separate bony elements to develop. There is some evidence of 
relations between bones and teeth and bones and lateral line organs 
and the pattern of the latter may play a large part in determining the 
plan of the skull (p. 325). Provisionally we may recognize four classes 
of dermal bones (1) canal bones, (2) tooth bones, (3) 'ordinary' bones, 
whose determination is unknown, (4) extra bones, filling special areas 
(Wormian bones). 

The arrangement of the numerous bones is made less difficult to 
understand and remember if they are considered in the following 
order. First the endochondral ossifications in the original neuro- 
cranium, then the dermal bones that cover this above and below; next 
the endochondral bones formed within the original cartilaginous jaws, 
then the dermal bones that cover the edges of the jaws, and finally the 
ossifications in the branchial arches and pectoral girdle, which latter 
is in bony fishes attached to the skull. 

The endochondral ossifications may be considered by beginning at 
the hind end of the skull: here the floor ossifies as the basioccipital, 
the sides as the exoccipitals, and the roof, over the spinal cord, as the 
supra-occipital bone; these posterior bones are not well marked off 
from each other in the adult skull. In the auditory capsule are five 
separate otic bones, of these the epiotic and pterotic can be seen 
externally (Fig. 118). 

The floor in front of the basioccipital is occupied by a basisphenoid 
bone and the walls above this by alisphenoids. The eyes nearly meet in 
the midline and the orbits are here separated only by a thin orbito- 
sphenoid. The only more anterior part of the chondrocranium to 
ossify is the region between the nasal capsule and the orbit, forming 
the ectethmoid. 

The dermal bones that cover this partly ossified neurocranium may 
be identified as on top and in front a pair of frontals and a median 
supraethmoid, behind which are large paired parietals and small 
paired post-parietals. These names have been inferred from study of 
crossopterygians and early amphibians (p. 325), which showed that 
the homologies earlier accepted were wrong. Fig. 118 carries the old 
nomenclature in which the large paired bones were called frontals. 
Around the eyes is a ring of circum-orbitals, and on the floor of the 
skull two median bones, the parasphenoid and vomer. 

The jaw bones are numerous, including both endochondral and 
dermal elements, and the relation of the method of support to that 

196 BONY FISHES vn. 3- 

found in other animals is not clear. In the embryo palato-pterygo- 
quadrate bars and Meckel's cartilages are seen. The upper jaw bears 
inward projections, which extend towards the chondro-cranium and 
probably represent the traces of an autostylic means of support (see 
p. 187). But the effective support in the adult is achieved by the ossi- 
fied hyomandibular cartilage. The palato-pterygo-quadrate bar ossifies 
in several parts and palatine, pterygoid, mesopterygoid, metaptery- 
goid, and quadrate bones appear, some of them partly formed in mem- 
brane. The only part of Meckel's cartilage to ossify is the articular 
bone, at the hind end. The actual edges of the jaws are supported by 
membrane bones, the premaxilla, maxilla, and jugal, covering the 
upper jaw. The dentary covers most of the lower jaw, except for a 
small bone, the angular, that lies on the inner side at the posterior end. 

The hyomandibular bone runs from an articulation with the otic 
capsule to the upper end of the quadrate. The symplectic is a small 
separate ossification at the lower end of the hyomandibula. The rest 
of the hyoid arch is present as epi-, cerato-, and hypohyals, which 
support a large toothed tongue. Bony fishes only rarely possess an 
open spiracle and immediately behind the hyoid are attached the 
bones supporting the operculum that covers the gills. The branchial 
arches are formed of several pieces, as in elasmobranchs, each being 
ossified separately. 

The effect of this complicated set of bones is to provide an efficient 
apparatus for the protection of the brain and sense-organs, support 
of the jaws and teeth and of the respiratory apparatus. Teeth are found 
on the vomers, palatines, premaxillae, maxillae, dentary, and on the 
tongue. Covering the typical dentine (orthodentine) is a layer of 
harder vitrodentine, poor in organic matter and perhaps derived 
partly from ectodermal ameloblasts. The teeth are usually spikes 
pointing in a backwards direction, used to prevent the escape of the 
food and not usually for biting or crushing. They may, however, form 
plates or be firmly attached to the bones. Folds of the mucous mem- 
brane, supported by cartilage and carrying gill-rakers, are found in 
species that feed on small prey. 

4. Respiration 

Limitations are imposed on the respiration of fishes by the facts 
that water is 800 times more dense than air and the dissolved oxygen 
is 30 times more dilute. The cost of respiration is therefore high. There 
is a 70 per cent, increase in metabolism when a trout increases its 
ventilation volume four times in water poor in oxygen. 

vir. 4 



Respiration is produced by a current passing in a single direction, 
as in elasmobranchs, namely, in at the mouth and out over the gill 
lamellae, but the mechanism by which the current is produced is some- 
what different. The pumping action is produced by a buccal pressure 
pump and opercular suction pumps, resulting from sideways move- 

A B 

Fig. 119. Arrangement of organs of head and gills in A, a shark, and, 

B, a teleostean fish. 

gb. gill bar; GC. outer opening of gill cleft; GF. gill filament; gr. gill-rakers; cv. gill vessels; 

J, ]'. upper and lower jaw; M. mouth; N, n'. openings of nasal chamber; op. operculum; 

sp. spiracle; ST. septum between gill filaments. (From Dean, Fishes, Living & Fossil, 

The Macmillan Co.) 

ments of the operculum, enlarging the branchial cavity. The branchio- 
stegal folds, below the operculum, prevent inflow of water from 
behind. When the operculum moves inward dorsal and ventral flaps 
in the throat prevent the exit of water forwards. 

The gill lamellae differ from those of elasmobranchs in the great 
reduction of the septum between the respiratory surfaces (Fig. 119). 
This has the effect of leaving the lamellae as free flaps, increasing the 
surface available for respiration. 

The area of the gills varies greatly, being relatively larger in more 
active species. The rate of respiration is controlled by a medullary 
centre but the most active rate of respiratory exchange is only some 
four times the standard rate (as against twenty times in man). The 


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vii. 4-5 BACKBONE OF FISHES 199 

area of the respiratory surface is thus an important limiting factor in 
the movement and growth of fishes. During activity of a fish lactic 
acid accumulates in the blood and the pH falls. The fish is thus able 
to display a considerable burst of activity and then to repay the 
oxygen debt over a long subsequent period. 

5. Vertebral column and fins of bony fishes 

The vertebral column of bony fishes performs the same function as 
in other fishes, namely, to prevent shortening of the body when the 
longitudinal muscles contract. It has, however, become very compli- 
cated and with the ribs and neural and haemal arches forms an 
elaborate system serving to maintain the body form under the stresses 
of fast swimming. Like other parts of the skeleton it is extensively 
ossified, and the necessary lateral flexion is obtained by division of 
the column into a series of sections joined together. Typically there 
is one such section (vertebra) corresponding to each segment, but in 
the tail region of Amia there are twice as many vertebrae as segments. 

Each vertebra consists of a centrum, neural arch and neural spine, 
and in the tail region, in addition, haemal arch and haemal spine. 
These parts are formed partly by ossification of cartilaginous masses, 
the basidorsal and basiventral, interdorsal and interventral, such as 
we saw in elasmobranchs, and partly by extra ossification in the sclero- 
genous tissue around the notochord and nerve-cord and between the 
muscles. The vertebrae are inter-segmental, the middle of each lying 
opposite the myocomma that separates two muscle segments. 

The centra are concave both in front and behind (amphicoelous), 
and in the hollows between them are pads made of the remains of the 
notochord, an arrangement that allows the column to resist longi- 
tudinal compression and yet remain flexible; similar flat or concave 
articulations of the centra are found in other aquatic vertebrates from 
the elasmobranchs to the whales. Extra processes on the front and 
back of the vertebrae ensure the articulation and are comparable to the 
zygapophyses found in tetrapods. The ribs, which are so prominent 
in the backbone of many fishes, are of two sorts; pleural ribs between 
the muscles and the lining of the abdominal cavity, and more dorsal 
intramuscular ribs. Both sorts are attached to the centrum. The bony 
rods attached above the neural and below the haemal arches are often 
called neural and haemal spines, though it is doubtful whether they 
correspond to the neural spines of land vertebrates. They form the 
supporting rods or radials of the median fins and are usually divided 
into two or three separate bones in each segment. In addition to these 



vii. 5- 

radials the fins are also supported by a more superficial set of bony- 
rods, the dermal fin rays (dermotrichia or lepidotrichia), which may 
be considered as modified scales and accordingly lie superficial to the 
radials. These dermal fin rays are usually forked at their tips. They 
make an extra support for the fin margin and to them are attached the 
muscles that serve to throw the fin into folds. 

In the tail region the internal skeleton is not quite symmetrical and 
shows signs of origin from an animal with a heterocercal tail. The 



Fig. 121. Muscles of a teleostean fish, mainly based on Mullus. 
ad-mand. adductor mandibulae; ep. epaxonic muscles; h. horizontal myoseptum; hy. hypo- 
branchial muscles; hyp. hypaxonic muscles; lev. max. levator maxillae; my. myocomma; 
op. operculum. (From Ihle.) 

notochord turns up sharply at the tip, so that the neural spines are 
very much shorter than the haemal spines, known here as hippural 
bones. The final portion of the notochord is often surrounded by a 
single ossification, the urostyle, and the whole makes a rigid support 
for the dermotrichia of the tail. Such a tail with internal asymmetry 
but external symmetry is said to be homocercal. 

The myotomes are arranged in a complicated pattern having the 
effect that contraction of each affects a considerable section of the 
body (Fig. 121); in fast swimmers such as the tunny each myotome 
may overlap as many as nineteen vertebrae. Between the lateral and 
ventral muscle masses there is in many fishes a layer of red muscle 
and this is especially well developed in the tunnies and bonitos. 

The paired fins are similarly supported by ossified radials, covered 
by dermal fin rays. At the base the radials are connected with 'girdles' 
lying in the body wall. The pectoral girdle (Fig. 118) consists of a 
cartilaginous endo-skeletal portion in which ossify the scapula, cora- 
coid, and sometimes mesocoracoid, while dermal bones, large cleith- 
rum, and one or more small clavicles, become attached superficially. 


Above these a further series of dermal bones, the supra-clavicle and 
post-temporal, attach the pectoral girdle to the otic region of the skull. 
The pelvic girdle is very simple, consisting only of a single bone, 
the basipterygium. 

6. Alimentary canal 

The food of the trout consists mainly of small invertebrates such as 
Gammarus, Cyclops, and other crustaceans, and aquatic insects and 
their larvae, together with the fry of other fishes and perhaps some- 
times larger pieces of 'meat'. The food is mostly swallowed whole, 
being helped down the pharynx by the mucous secretions, but these, 
as in elasmobranchs, contain no enzymes. The entrance to the stomach 
is guarded by a powerful oesophageal sphincter, no doubt serving to 
prevent the entry of the water of the respiratory stream. The stomach 
is divided into cardiac and pyloric portions, though the distinction is 
less clear than in elasmobranchs. The duodenum is beset by a number 
of wide-mouthed pyloric caeca, serving to increase the intestinal 
surface (Fig. 120). The intestine and caeca are lined throughout by a 
simple columnar epithelium and there are no specialized multicellular 
glands such as the Brunners glands or crypts of Lieberkiihn of mam- 
mals. The exocrine pancreas consists of numerous diffuse glands in 
the mesentery. The endocrine portion, however, forms a compact 
mass of tissue. This is very rich in insulin and after its removal a fish 
shows hyperglycemia and glycosuria. The intestine is relatively longer 
than in elasmobranchs and often coiled; its internal surface may be 
increased by folds, but there is no true spiral valve, though this was 
present in the ancestors of the Teleostei (p. 233). There is no gland 
attached to the rectum. 

7. Air-bladder 

Dorsal to the gut is a very large sac with shiny, whitish walls, the 
air-bladder, filled with oxygen. A narrow pneumatic duct connects 
this with the pharynx in the more primitive forms. The origin and 
functions of the air-bladder will be discussed below (p. 261); it serves 
as a hydrostatic organ, enabling the animal to remain suspended in 
the water at any depth. 

8. Circulatory system 

The general plan of the circulation is similar to that of an elasmo- 
branch (Fig. 122), that is to say, there is a single circuit and all 
the blood passes through at least two sets of capillaries. The heart 

202 BONY FISHES vu. 8- 

contains a series of three chambers, sinus, auricle, and ventricle, but the 
muscular conus arteriosus is absent, there being only a thin-walled 
bulbus arteriosus at the base of the ventral aorta. The walls of the 
bulbus are elastic but not muscular, and study of its action by means 
of X-rays shows that it is dilated by the ventricular beat and then 
contracts, thus maintaining the pressure against the capillaries of the 
gills. The ventral aorta is short, but the arrangement of the afferent 
and efferent branchial vessels is essentially as in elasmobranchs. 

The blood-pressure in the ventral aorta is less than 40 mm Hg in 
most fishes at rest, and in the dorsal aorta about half this. The venous 
pressures are around zero, the pericardium being fibrous but not 
rigid as it is in elasmobranchs (p. 160). There is no communication 
between the pericardial and peritoneal chambers. There is a vagal 
cardiac depressor nerve, but no sympathetic nerve to the heart. 

There is a well-developed lymphatic system beneath the skin and 
in the muscles and viscera. Lymphoid tissue is abundant in various 
organs but there are no lymph-nodes along the vessels. There is a 
large spleen concerned with haemopoiesis, which also proceeds in the 
kidneys. The red cells are smaller in bony fishes (8-10 ix) than in 
elasmobranchs (up to 20 /z). A continuous series of white cells is 
present and acidic and basic granules may occur in the same cell. 

9. Urinogenital system and osmoregulation 

The kidneys are mesonephric in the adult and consist of an elon- 
gated brown mass above the air-bladder. The ducts of the two kidneys 
join posteriorly and are swollen to form a bladder which, being meso- 
dermal, must be distinguished from the endodermal cloacal bladder 
of tetrapods. The urinary duct opens separately behind the anus, 
there being no common cloaca. 

Nitrogenous elimination is a function mainly of the gills, which 
excrete as ammonia and urea more than six times as much nitrogen as 
the kidneys. The latter excrete creatine, uric acid, and the weak base 
trimethylamine oxide, which is present in large amounts in the blood 
of marine teleosts. 

One of the most striking features of the life of bony fishes is that 
they occur both in fresh water and the sea, and many, such as the 
trout itself, can move from one to the other. It is supposed by some 
that the earliest gnathostomes were freshwater animals (p. 187), and 
the bony fishes might be said to show evidence of this in that the 
concentration of salt in their blood is always less than in the sea, in the 
neighbourhood of 1-4 per cent. NaCl against 3-5 per cent, outside. 


In fishes in fresh water the blood is more dilute, about o-6 per cent. 
NaCl, but is, of course, more concentrated than the surrounding 
medium, which contains only traces of inorganic ions. Freshwater 
fishes are able to take up salts from the water through the gill surfaces. 
The kidney apparatus, with its filtration system of glomeruli and 
tubules for salt reabsorption, was probably developed for life in fresh 
water and still serves in this way in the freshwater forms. Various 
special devices are adopted in fresh water for minimizing the tendency 

Fig. 122. Diagram of the branchial circulation of a teleostean fish. 
ab. artery to air-bladder; a/ 3-6 , four afferent vessels from ventral aorta; ca. carotid artery; 
cc. circulus cephalicus; cl. coeliac artery; d. ductus Cuvieri; da. dorsal aorta; ef 3 . efferent 
vessel of first branchial arch; ep. epibranchial artery; ha. hyoidean artery (afferent vessel of 
pseudobranch); hp. hepatic vein; ht. heart; mis. mesenteric artery; oa. ophthalmic artery 
(efferent vessel of pseudobranch); ps. pseudobranch (hyoidean gill, possibly with spiracular 
gill); s. position of spiracle (closed); va. ventral aorta; I-V. five branchial slits. (From 
Goodrich, Vertebrata, A. & C. Black, Ltd., after Parker.) 

to gain water and lose salt. The skin is little vascularized and probably 
makes an almost waterproof layer. The production of mucus assists 
in this waterproofing, and abundant mucus is secreted when an eel is 
transferred from salt to fresh water: the full change cannot be made 
suddenly without killing the fish. 

In marine teleosts the problem is the opposite one of keeping water 
in, or keeping out salt. The usual kidney mechanism is clearly ill 
suited for this and it is found that the glomeruli are few, or often 
completely absent from the kidneys. This no doubt reduces the loss 
of water, but is not enough by itself to solve the problem, which is 
met by taking in water and salts and excreting the salts. For this 
purpose special chloride-secreting cells are present in the gills and it 
has been shown that the amount of oxygen they use, and hence the 
work they do in diluting the blood, is proportional to the difference of 
concentration between the inside and the outside. A marine fish is 
able to drink and absorb sea water in spite of the fact that this is more 



vir. 9- 

concentrated than its blood. The chloride-secreting cells dispose of 
the excess salts. It remains to explain the means by which a solution 
passes against the osmotic gradient from the cavity of the gut to the 
blood; the membranes here must have some special properties of 
which we are ignorant. Sodium and chloride enter with the water but 
magnesium is excluded and may be precipitated in the intestine. 

The genital system is nearly completely separated from the excre- 
tory in both sexes. The testes (soft roes) are a large pair of sacs opening 

into the base of the urinary 
ducts. The ovaries (hard roes) 
are also elongated in the trout 
and the eggs are shed free into 
the coelom (Fig. 123) and 
passed to the exterior by 
abdominal pores. This condi- 
tion is unusual among teleosts, 
in most the ovaries are closed 
sacs, continuous with the ovi- 

Fertilization is external and 
the eggs of the trout are shed 
in small pits or depressions in 
the sand; being sticky, they 
become attached to small 
stones. The eggs are very 
yolky and cleavage is therefore only partial, forming a cap of cells, 
the blastoderm, which eventually differentiates into the embryo. 
After hatching, the young fish may still carry the yolk sac and 
obtain food from it for some time, while beginning to eat the small 
crustaceans and other animals that are its first food. 

10. Races of trout and salmon and their breeding habits 

There is considerable confusion about the various races of trout 
and their allies the salmon. In both trout and salmon the adult 
originally spent the great part of its life in the sea but returned to the 
rivers to breed. Trout and salmon that do this are still abundant on 
the West Atlantic coasts and ascend all suitable rivers to breed, the 
process being known as the 'run'. But the trout has produced many 
races of purely fluviatile animals, living either in lakes (where they often 
become very large) or rivers, and never returning to the sea to breed. 
These freshwater races differ in small points from each other and are 

Fig. 123. Ovaries and kidneys of A, typical 

teleostean fish, B, trout and some other fishes 

where the eggs are shed into the coelom. 

(From Norman, after Rey.) 




given various common names (phinock, Severn, Loch Leven trout, 
brook trout, &c). There can be no doubt that interesting genetic 
differences between these forms exist, but they have not yet been 
fully studied. The salmon are much less prone to form purely fresh- 
water races, though such are known. 

During the breeding-season characteristic changes take place in the 
fishes and differences between the sexes appear. In the salmon the 
jaws become long, thin, and hooked, especially in the male. The 
animals make pairs and the males fight with others that approach the 
female. As the gonads ripen, the other 
parts of the fish, which were well supplied 
with fat at the beginning of the run, 
become progressively more watery. 
Finally, spawning takes place, the female 
laying the eggs in a shallow trough (redd), 
which she has 'cut' in the gravel by move- 
ments of her tail, while the male sheds 
sperms over them. She then covers the 
eggs with gravel by further cutting move- 
ments. The young male salmon (parr), 
which have not yet been to the sea, may 
become sexually mature. They accompany 
the fully grown fish, hanging around the 
cloacal region and shedding their sperms 
at the same time as the large male. It is possible that this develop- 
ment of a kind of third sex serves to increase the variability of the 
population. The spent parr eat some of the eggs and they then proceed 
to grow, migrate to the sea, and return later. 

Male trout will follow a spawning salmon and fertilize her eggs if 
her own male is not looking. Hybrids formed in this way can develop, 
but are said to be less fertile than the normal types; indeed, the males 
are wholly sterile. 

After fertilization the salmon are very exhausted (known as kelts) ; 
the males seldom return to the sea. The females, however, may recover 
and after a period in the sea return to breed again, and this process 
may be repeated several times. 

Very young trout or salmon are known as alevins or fry and remain 
mostly among the stones (Fig. 124). When they emerge they are called 
parr and have a number of characteristic parr-marks along their sides. 
After two to four years spent as parr in fresh water salmon acquire a 
silver colour and pass to the sea as smolts. Young salmon returning for 

Fig. 124. Three stages in the 

development of the salmon. 

I and II are alevins; III, parr. 

(From Norman.) 



the first time to breed are called maidens. If they have spent only one 
and a half years in the sea they are called grilse and may then return 
to the sea as kelts. Others ascend for the first time after three years 
or more at sea. 

It is well established that salmon nearly always return to breed in 
the river in which they were born, and it is certain that they may 
journey for considerable distances in the sea. The mechanisms by 
which these migrations are initiated and guided are only partly known. 

Fig. 125. Pituitary gland of the primitive teleost Elops, showing the persistent 
Rathke's pouch in the form of a hollow bucco-hypophysial canal, piercing the 

parasphenoid bone. 

ah. adenohypophysis ; b.h.c. bucco-hypophysial canal; h.v. blood-vessel; c. continuation with 

pharynx; i. infundibulum; n.h. neurohypophysis;/)^, parasphenoid. 

(After Olsson.) 

They probably involve endocrine changes, for example the thyroid 
is very active in the smolt as they begin to migrate. The return to the 
home river may be a result of olfactory conditioning (see p. 221). 

11. Endocrine glands of bony fishes 

The pituitary gland occupies the same central part in the endocrine 
signalling system that it has in mammals. Neural and glandular 
regions are present and the adenohypophysis has three parts, the 
two more posterior corresponding to the mammalian intermediate and 
anterior lobes. The most anterior glandular region may be comparable 
to the pars tuberalis. Experiments by removal and injection have 
shown that the middle portion produces hormones that stimulate 
growth, the gonads, the thyroid, adrenal, and probably the pancreas. 
The posterior lobe produces a melanophore-dispersing hormone 



(p. 260) and there may be a melanophore-concentrating one in the 
anterior lobe. Oxytocin and vasopressin are present but there is no 
evidence that excretion is controlled by the pituitary. 

The thyroid tissue is not aggregated into a compact gland but forms 
scattered masses along the ventral aorta. Its hormones appear to be 


Fig. 126. Urohypophysis of A, eel; b, loach (Misgurnus); c, the same in a loach 

after sectioning the spinal cord and injecting hypertonic saline. 

b. blood-vessels; ep. ependyma;//. filum terminate; /;/. lumps of secretion (? 'Herring bodies'); 

tie. nerve endings; ns.a. neurosecretory axon; ns.c. neurosecretory cells; s.d. storage depot of 

neurosecretion. (After F.nami, N., in Symposium on Comparative Endocrinology. Wiley, New 


identical with those of mammals, including mono- and di-iodotyrosine 
and thyroxin. Thyroid follicles are often found in the kidneys, heart, 
eye, and elsewhere in the body of fishes, especially those deprived of 

The suprarenal and interrenal tissues are partly associated in masses 
around the thickened walls of the posterior cardinal veins. Because of 
the difficulty of isolating these tissues there is little information as to 
their function. The corpuscles of Stannius are groups of gland cells 
dorsal to the kidnevs, they have been held to be related to the adrenals, 
but their nature is still uncertain. 



The ultimobranchial gland is a mass of cells developed from the 
last branchial pouch and perhaps related to the parathyroids. 

The hormone rennin, which raises the blood pressure, is said to be 
present in freshwater teleosts, with their high glomerular filtration, 
but not in marine ones. 

The gonads produce steroid hormones as in elasmobranchs (p. 
167). The secondary sex characters depend upon their presence, thus 

ns. c. 


Fig. 127. Comparison of pattern of organization of the caudal neurosecretory 
system (b) with the hypothalamo-hypophysial system (a). 

ah. adenohypophysis; b.v. blood-vessels; c.c. central canal; /.i. filum terminale; h. 'Herring 
bodies', neurosecretory products; n. neurohypophysis; n.e. nerve endings; ns.c. neurosecre- 
tory cells; o.c. optic chiasma; p. pituicytes; p.v. hypophysial portal vessels; r.f. Reissner's fibre; 
11. urohypophysis; v. vtntricle. (After Enami, N., in Symposium on Comparative Endocrinology. 

Wiley, New York.) 

the gonopodium of the male of viviparous fishes (p. 267) is developed 
if sex hormone is added to the water. 

At the hind end of the spinal cord of fishes is a small lump consisting 
of masses of secretion produced by neurosecretory cells of the spinal 
cord and hence called the urohypophysis (Figs. 126 and 127). In 
function it appears to be connected with salt regulation; injection of 
hypertonic NaCl produces hypersecretion, the products accumulating 
at the cut surface if the cord has been severed. Injection of extracts 
produces changes in the sodium content of the fish and also changes 

VII. 12 



in buoyancy, perhaps due to an influence on the carbonic anhydrase 
of the gas bladder. 

12. Brain of bony fishes 

The brain of bony fishes is built on the same general functional and 
structural plan as that of elasmobranchs, namely, the development of a 
number of separate centres, one concerned with each of the main 
receptor systems. The forebrain is often large, but it is characterized 


rec. pr. 

Fig. 127 {a). Cross-section of the forebrain of the cod. and lateral and medial tracts between olfactory region and hypothalamus; hyp. 
hypothalamus; m. membranous roof of forebrain; n.mag. nucleus magnocellularis preopticus; 
n.opt. optic tracts (that on the right has atrophied in this specimen) ; rec. pr. preoptic recess ; 
str. hind end of striatum; thai, thalamus; 3rd v. third ventricle. (From Kappers, Huber, 

and Crosby.) 

by great development of its ventral regions (the 'corpus striatum'), the 
roof being wholly membranous (Figs. 127 (a), 128). This condition is 
known as 'eversion' and is the very opposite to the inverted or thick- 
roofed forebrains that are found in the lung-fishes, close to the line 
of tetrapod descent (p. 278). The whole of this forebrain is reached by 
olfactory fibres, and there is little evidence that fibres from other 
receptor centres reach forward to it; it is mostly a smell brain. 
Extirpation of the telencephalon from various teleosts has not 
produced changes in locomotion, balance, or vision; there may be 
slight changes in general activity and social behaviour. No movements 
have been seen following electrical stimulation of it. 

The diencephalon is not large, since most of the optic fibres end 
not here, but in the midbrain. The roof is everted to form a pineal 
body, and this and other parts of the diencephalon may contain 

210 BONY FISHES vn. 12 

receptors sensitive to light. The minnow Phoxinus has a transparent 
patch on the head in this region, and it has been found possible to 
train the fish to give appropriate responses to changes of illumination 
even after removal of the paired eyes and the pineal body. Evidently 
there are light-sensitive cells in other parts of the walls of the dien- 
cephalon, besides those that become evaginated to form the eyes. 
Experiments on lampreys also showed the presence of such cells 
(p. 105). The hypothalamus is well developed and receives large tracts 
from the forebrain. Below and behind it is a large saccus vasculosus 
in some forms (p. 169). 

The midbrain is often the largest part of the brain. The cells spread 
out over its roof (tectum opticum) are not all collected round the 
ventricle but have migrated away to make an elaborately layered 
system. Into this midbrain cortex there pass not only the great optic 
tracts but also ascending tracts from the sensory regions of the spinal 
cord, lateral line system, gustatory systems, and cerebellum. Large 
motor tracts pass back towards the spinal cord; the details of their 
endings have not been traced, but they certainly exercise control over 
motor functions. Electrical stimulation of the optic lobes produces 
well-coordinated movements of local groups of muscles, for instance 
those of the eyes or fins. It can hardly be doubted that this well- 
developed midbrain apparatus thus controls much of the behaviour of 
the fish and is able to mediate quite elaborate acts of learning and 
other forms of more complex behaviour. After removal of the tectum 
of one side a minnow is blind in the opposite eye. Each part of the 
retina is mapped on to a distinct area of the tectum and if the optic 
tract is cut and allowed to regenerate this projection is exactly replaced. 
When a goldfish is trained to respond to some visual stimulus the 
learning process occurs in the midbrain and continues unaffected after 
removal of the forebrain. Conversely, olfactory learning takes place 
in the latter and is undisturbed by injury to the tectum opticum. 

The base of the midbrain (tegmentum) contains motor centres. 
Electrical stimulation here produces abrupt and massive responses of 
the locomotor apparatus, very different from the sequences of co- 
ordinated movements that appear after stimulation of the roof of the 

The cerebellum is very large in teleosts, especially in the more 
active swimmers, and a forwardly directed lobe of it, the valvula 
cerebelli, extends under the midbrain. Various disorders of movement 
have been reported after removal of the cerebellum, such as swaying 
when moving quickly. Presumably it plays an important part, as in 


Fie. 128. Transverse sections of forcbrain in various vertebrates to show the condition 

of inversion (thick roof) in A, n, and c and eversion (thin roof) in D, E, and F. 

A, lamprey; B, frog; C, chelonian; D, chimaera; E. sturgeon; F, teleostean; pall, pallium; 

sep. septum; str. striatum. (From Kappers, Huber, and Crosby.) 


Fig. 129. Sagittal section of brain of the gurnard, showing the swellings in the 

spinal cord at the point of entry of the nerves from the fin. 

C. cerebral hemisphere; ce. cerebellum; hy. hypothalamus; in. midbrain; no. swellings of 

spinal cord; v. valvula. (From Scharrer, Z. verg. Physiol. 22.) 

other vertebrates, in producing precise and correctly timed movements. 
It is enormous in the Mormyridae, where it may assist in direction- 
finding by electrical pulses (p. 253), perhaps acting as a timing device. 
The medulla oblongata is also well developed, having special lobes 
connected with the entry of the lateral line nerves and gustatory fibres 
of the cranial nerves. In the gurnard, Trigla, there are chemical 
receptors in the elongated fins. These are innervated from spinal 
nerves, and there are swellings of the dorsal part of the spinal cord at 
the points where these nerves enter (Fig. 129). 

212 BONY FISHES vn. 13- 

13. Receptors for life in the water 

The features of the environment that are relevant for life are very 
different in air and water. Man is so well used to the air that it is not 
easy to appreciate fully the conditions underwater, where changes of 
illumination, though obviously important, provide less detailed evid- 
ence of the sequence of distant events than they do in air. We can 
say that light carries less information for a fish; to put it in another 
way, fewer distinct choices between alternative behaviour pathways 
are made on the basis of visual clues by a fish than by a man. 

On the other hand, the water around the fish provides mechanical 
stimuli both at low and high frequency that are more closely related 
to distant events than is generally true in air. Both hearing and touch 
are of great importance in the water and the lateral line system pro- 
vides a system of 'distant touch' that is perhaps wholly outside our 
experience. Localization of distant objects by such a sense, perhaps 
assisted by echo-location by water movements, provides the fish with 
many relevant clues. It is interesting that these receptors are connected 
with a very large cerebellar system, perhaps concerned with measur- 
ing time differences. 

Chemical changes in the water also provide much information and 
both taste and smell are well developed. That smell is analysed by a 
distinct system in the forebrain, not directly related to the cerebellar 
system, is one of the fundamental principles of control of vertebrate 
behaviour. Distant chemical changes provide the first clue to the 
presence of food, a mate, or an enemy, whereas the detailed finding 
of these involves eyes, ears, touch, and an accurate timing system. 
There thus arises the distinction between the systems for initiation of 
action in the forebrain ('emotive') and for its fulfilment (executive) 
by centres farther back. 

14. Eyes 

An animal provided with suitable receptors can obtain much 
information about the environment from the changes in illumination. 
Control of the whole physiology to follow the rhythm of day and night 
may have been the original reason for the development of photo- 
sensitivity in the diencephalon (see p. 105). At the stage of evolution 
reached by teleosts information is gained from the fact that light 
varies in frequency (colour) and intensity (brightness) and that it is 
reflected from many substances, revealing their movement and shape. 
The greatest sensitivity of the fish eye is in the yellow-green, which 

vii. 14 EYE OF TELEOSTS 213 

is the wavelength that penetrates farthest into the water. In order to 
extract the maximum of information at high as well as low intensities 
it is necessary to adjust the sensitivity, and hence the signal/noise 
ratio. For this purpose teleosts have developed retinas with distinct 
rods, cones, and twin-cones and in some there is a fovea composed of 
numerous thin cones (e.g. in Blennius). The pupil usually varies little 
in diameter, and adjustment of sensitivity is by migration of pigment 

scleral cartilage 

epichorioKJal lymph space 


Fig. 130. Diagrammatic vertical section of a typical teleostean eye. Not all the structures 
here shown are found in all species. (From Walls, The Vertebrate Eye.) 

between the receptors and contraction of a 'myoid' segment of the 
latter. In bright light the pigment expands, the cones contract for- 
ward, towards the light and the rods contract back, beneath the pig- 
ment. These photo-mechanical changes thus serve the same end as 
changes of pupil diameter in other vertebrates. 

The photochemical change in the rods of marine fishes is the same 
as that of land vertebrates, namely the breakdown of the rose- 
coloured 'visual purple' (rhodopsin) first to the yellow retinene and 
then to colourless vitamin A v In freshwater fishes there is a different 
pigment porphyropsin, or visual violet, which breaks down to vita- 
min A 2 . Intermediates between these may be found. 

In all fishes there is a very large, dense, spherical lens, to which is 
attached a retractor muscle (campanula Halleri) inserted on to a fal- 
ciform ligament, which occupies the persistent choroidal fissure in the 
retina (Fig. 130). The eye is usually said to be myopic at rest and to be 
accommodated for distant vision by pulling the lens nearer to the 

214 BONY FISHES vn. 14 

retina. However, this has recently been disputed by Verrier, who 
denies that the campanula is muscular and believes the eye to be 
hypermetropic at rest and accommodated, if at all, by fibres of the 
ciliary body, as in other vertebrates. It may be that the fixed focus is 
already sufficiently deep and the campanula perhaps serves mainly 
to steady the lens. 

It is unwise, however, to generalize about teleostean eyes, for they 
are very varied. Whereas the trout, like most, has a round pupil, 
which varies little if at all in size, other fishes, whose eyes are more 
exposed to light from above, have a more mobile iris. In flat-fishes 
and the angler-fishes, such as Lophius, and the Mediterranean 
Uranoscopus, the star gazer, the iris has an 'operculum' and is very 
muscular; its movements are controlled by nerves and not, as in 
selachians, by the direct effect of light. The sympathetic system sends 
branches into the head in these animals (Fig. 138) and its fibres cause 
contraction of the sphincter of the iris, whereas fibres in the oculo- 
motor nerve cause contraction of the dilatator, the opposite arrange- 
ment to that in mammals. In the eel the pupil is also capable of wide 
changes of diameter, but here the control is mainly by the direct 
response of the circular sphincter iridis muscle to light incident upon 
it. The pupil of the isolated eye of an eel closes when illuminated and 
reopens again in darkness (Fig. 131). Presumably because of its lack 
of nervous control this iris is not affected by many of the usual 
'autonomic' drugs. For instance, closure will occur in the presence of 
atropine and the dark-adapted pupil remains unchanged when placed 
in a solution as strong as 1 per cent, pilocarpine, but then closes 
immediately on illumination (Fig. 132). The isolated pupil of Urano- 
scopus, however, closes when pilocarpine is applied (Fig. 133), and 
in this case the sphincter muscle is innervated by sympathetic nerve- 
fibres. Adrenaline also causes the sphincter to contract and acetyl 
choline in moderate concentrations causes dilatation 

The eyes may be small or absent in fishes living in caves, muddy 
waters, or the deep sea. In this last habitat, however, many have ex- 
ceptionally large eyes, with, apparently, high acuity as well as sensi- 
tivity. They may be elongated ('telescopic') and with large binocular 
fields and a fovea of 'rods'. In Bathylagus the rods reach a density 
of 800,000 mm 2 and are arranged in six superimposed layers, which 
presumably come into action successively as an object approaches. 
The cells of the deeper layers are less closely packed. 

The tropical fish Anableps lives with the head half out of water and 
the eyes are adapted for use in both media. The upper part of the 



White light 

Red light 









i i i 







Fig. 131. Closure of the pupil of the isolated eel's eye, followed by plotting the move- 
ment of its margin with a camera lucida. The movements are shown magnified 54 X , 

Time in minutes. 






Acetul choline . . , L ■■ 
Vmnnnnn Acetylcholine 

1/100.000 Atropine 7100,000 

Vl .000.000 

Red light 




20 11 







Time, minutes 

Fig. 132. Changes of diameter of isolated eel's iris in Ringer's solution with the 

addition of various drugs. Acetyl choline produces some closure, atropine some 

opening. Light still produces closure after application of atropine. 


Fig. 133. Movements of margin of pupil in isolated iris of Uranoscopus in isotonic 

solution. Pilocarpine produces closure and atropine opening of this pupil whose 

sphincter muscle is innervated by sympathetic nerve-fibres. 

(From Young, Proc. Roy. Soc. B. 107.) 



vii. 14- 

cornea is thickened, the iris provides two pupils, the lens is pear- 
shaped, and there are two retinas in each eye. 

15. Ear and hearing of fishes 

The ear provides receptors that ensure the maintenance of a correct 
position of the fish in relation to gravity and to angular accelerations. 
In addition, in many species it serves for hearing. The inner ear is 
completely enclosed in the otic bones. There is a perilymphatic space 
only in those species that hear well. 


Ns Sag. S. L. 

Fig. 134. Diagram of ear of the minnow Phoxinus. 

Ast. asteriscus; L. lagena; N.I., N.s. nerves of lagena and saccule; 

S. saccule; Sag. sagitta; U. utricle. (From V. Frisch, Z. vergl. 

Physiol. 25.) 

Each ear sac is subdivided into three semicircular canals and three 
other chambers, the utriculus, sacculus, and lagena (Fig. 134). In 
each chamber is carried an ear stone (otolith) and these are given 
special names, the lapillus, sagitta, and asteriscus, occupying the above 
three chambers respectively. 

The sensitive macula of the utricle lies horizontally, with the 
lapillus resting upon it, whereas the maculae of the saccule and lagena 
are vertical. These receptors with otoliths have double or triple 
functions. At rest they act as static receptors, signalling the position 
of the fish in relation to gravity and setting the fins and eyes in appro- 
priate positions. In movement, together with the semicircular canals, 
they signal angular accelerations, initiating compensatory movements. 
Thirdly, some of the otolith organs respond to sonic vibrations. 

In the fishes that hear well there is a connexion between the air 
bladder and the ear. This may be either direct, by means of a sac 
extending forwards (in Clupeidae and others) or indirectly by a chain 
of modified vertebrae, the Weberian ossicles (Fig. 135). This latter 
arrangement is found in the freshwater Ostariophysi, which hear 

vii. 15 HEARING OF FISHES 217 

particularly well. In these fishes the receptors are in the inferior part 
of the ear (saccule and lagena, Fig. 134). The sagitta carries a special 
wing projecting into the cavity and is so suspended as to serve to 
amplify vibrations. Near to it is 
a thin portion of the wall of the 
sac, which would favour the 
passage of variations of pressure 
transmitted to the endolymph by 
the ossicles. 

These Ostariophysi respond to 
sounds between about 60-6,000 
vibrations/sec. After removal of 
the pars inferior responses con- 
tinue only up to 120/sec. If the 
air bladder is punctured a min- 
now can still respond, but only 
up to 3,000/sec and with a sen- 
sitivity diminished by more than 
fifty times. 

Minnows can be trained to 
discriminate between warbled 
notes separated by I tone. Non- 
ostariophyse fishes have mostly 
a much lower upper limit of 
hearing and lower capacity for 
discrimination. The Mormyridae 
(p. 254), however, approach the 
minnows in this respect and here 
there is a special isolated portion 
of the air bladder within the otic 

In the best cases the sense of 
hearing of fishes thus approaches 
that of man, in spite of the 
absence of a coiled cochlea and 

basilar membrane with fibres of different lengths. Clearly the discrimi- 
nation of tones cannot here depend upon differential resonance as the 
theory of Helmholtz requires. In spite of the considerable powers 
of pitch discrimination there is little evidence of capacity to localize 
sounds except when they are loud and near. 


Fig. 135. Position of ear in Ostariophysi 

and its relation to the Weberian ossicles, 

which are shown in black. transverse canal between the two sacculi; 
//. brain; /. 'incus'; L. lagena; M. 'malleus'; 
S. sacculus; Sch. swim-bladder; S.i. sinus impar 
(perilymphatic space); St. 'stapes'; U. utriculus. 
(From V. Frisch.) 

218 BONY FISHES vii. 16- 

16. Sound production in fishes 

A surprisingly large number of fishes can produce sounds audible 
to ourselves, and these noises are used by the fishes either for shoaling, 
or to bring the sexes together, or to warn or startle enemies. Some fish 
may use the sounds they produce for echo-location. Among the loudest 
of the sounds is that produced by the drum-fish (Pogonias) of the 
Eastern Atlantic. The 'whistling' and other noises of the 'maigre' 
(Sciaend) are supposed to be the origin of the song of the Sirens, since 
they can easily be heard above the water. In both these fishes the 
sounds are made mostly if not wholly in the breeding season. In 
others, such as siluroids and Diodon, the noise is associated with the 
presence of spines and may be a warning. In Congiopodas the nerves 
that innervate the muscles of sound production also supply muscles 
that raise the spines (Packard). 

The mechanism for sound production is very varied, involving 
either stridulation by the vertebrae (some siluroids), operculum 
(Cottus, the bull-head), pectoral girdle (trigger-fishes), teeth (some 
mackerel and sun-fish), or phonation by the air bladder. The latter 
may be involved either by its use for 'breathing' sounds in physosto- 
matous forms (p. 261) or as a resonator. Noise production is common 
in some families (Triglidae, Sciaenidae, Siluridae) but almost absent 
from others. The advantages to be obtained from sound production 
underwater have led to parallel evolution of similar mechanisms in 
several different groups. 

17. The lateral line organs of fishes 

The lateral line organs occur partly as rows of distinct pits, partly 
in canals that communicate with the surface through pores in the 
scales. Besides the main canal running down the body and served 
by the lateral line branch of the tenth cranial nerve, there are also 
lines following a definite pattern on the head, namely, supra- and 
sub-orbital lines, a line on the lower jaw, and a temporal line across 
the back of the skull. The canals on the head are innervated mainly 
from the seventh, partly from the ninth cranial nerve. The nerve- 
fibres enter the very large acoustico-lateral centres of the medulla and 
valvula cerebelli. 

Fishes possess the capacity to react to an object moving some dis- 
tance away in the water ('distant touch sense') and this is reduced or 
absent after section of the lateral line nerve. Presumably the moving 
object sets up currents in the water, which move the fluid (or mucus) 
in the canals. It has also been suggested that the canals serve to record 

vii. 17 



displacements produced by the swimming movements of the fish 
itself, but this has not been proved. Fishes deprived of the lateral 
line show no muscular incoordination, although if blind they collide 
frequently with solid objects. It has often been suggested that these 
organs serve for hearing, perhaps at low frequencies, but this is 
probably not so. 

Fig. 136. Responses of a single end organ in a lateral canal of a ray, shown with an 
oscillograph after amplification. Time signal 10 sec. intervals. The movements of 
the continuous white line show A, the beginning of a headward flow, increasing the 
frequency of discharge; B, the end of this flow; c, return of spontaneous discharge 
after an interval of 28 sec; D, spontaneous discharge 60 sec. later; E, beginning of 
a tailward perfusion, inhibiting the discharge; F, the end of this perfusion; G, the 
spontaneous discharge 10 sec. later. (From Sand, Proc. Roy. Soc. B. 123.) 

Study of the electrical activities of these organs in rays has shown 
that many of them discharge impulses all the time, even when not 
under the influence of any external stimulation (Fig. 136). By passing 
currents of water along the tubes Sand showed that a tailward flow 
checks and a headward flow accelerates this 'spontaneous' discharge of 
impulses. Such changes in the streams of impulses arriving at the 
brain could, no doubt, form the basis for initiation of movements of 



vii. 17- 

the fish. This, however, still leaves open the question of what agency 
initiates movement of the fluid in the canals during life. It has been 
shown that when small streams of water are directed against the side 
of the tail some fish make escaping movements, but that these no 
longer appear when the lateral line nerve has been cut. The lateral 
line organs thus provide signals when agitation of the water causes 
pressure changes. In fact they provide the animal with a kind of 
water touch, though it is not certain whether this is their only func- 

/^v Lat.d. 


pelv. pect. 

Fig. 137. Dissection of whiting to show the cranial nerves, and especially the 
nerves for the taste-buds. 

an. anal fin; gust, gustatory branch of facial; lat.d. and lat.v. dorsal and ventral lateral line 

nerves of vagus; mand. and max. mandibular and maxillary divisions of trigeminal; op. 

ophthalmic; pect. pectoral fin; pelv. pelvic fin; VII, hyomandibular branch of facial; IX, 

glossopharyngeal; X.visc. visceral branch of vagus. 

tion. Why this type of receptor should need such a peculiar apparatus 
of canals, rather than a system of nerve-fibres in the skin, innervated 
by the spinal dorsal roots, is not clear, nor do we know the significance 
of the pattern of lines on the head. The lateral line system must cer- 
tainly be of great importance in aquatic life, for it is found in all types 
of fishes and also in the early Amphibia and in the aquatic larvae of 
modern members of that group. The distant touch receptors could 
obviously be used in many ways, not only to locate moving objects 
and water currents but to serve for echo-location, by computing the 
time relation of reflected waves set up by the fish itself. 

18. Chemoreceptors. Taste and smell 

As in all vertebrates, there are two separate chemical senses, taste 
and smell. The former serves mainly to produce appropriate reactions 
to food near the body, such as snapping, swallowing, or movements 
of rejection. Smell, on the other hand, is a 'distance sense', by which 
the whole animal is steered. The distinction between the two types 
of receptor is somewhat obscured in bony fishes by the fact that taste- 
buds are not restricted as they are in mammals to the tongue and 

vii. i8 TASTE AND SMELL 221 

pharynx but may occur on the whiskers and all over the body. They 
are innervated by branches of the seventh, ninth, and tenth cranial 
nerves, which may reach far backwards (Fig. 137). In some species it 
has been shown that the fish is able to turn and snap at a piece of food 
placed near the tail. This power is lost if the branches from the cranial 
nerves are cut. In mammals taste-buds serve to discriminate only four 
qualities (salt, sour, bitter, and sweet), most of our so-called 'tasting' 
being in reality the smelling of the food in the mouth. In fishes, also, 
the four taste qualities are discriminated by the taste-bud system, and 
it has been shown that the minnow (Phoxinus) continues to make such 
discriminations after the forebrain has been removed. Other chemical 
discriminations are made by the nose, however, and can only be 
performed with an intact forebrain. Thus Phoxinus tastes and smells 
the same classes of substances as man does. The taste-buds are 
exceedingly sensitive, the threshold for sweet substances being 500 
times and for salt 200 times lower than in man. On the other hand, 
some substances that are very bitter for us produce little reaction in 

In many fishes the nose is one of the chief receptors (macrosmatic). 
There are two nostrils on each side, allowing for the sampling of a 
stream of water (Fig. 119). The nose does not communicate with the 
mouth, except in a few fishes that live buried in the sand (Astroscopus). 
The sense of smell is used to find food and for recognition of the 
sex of members of the same species. Minnows can be trained to give 
distinct reactions to extracts made from the skin of other species of 
fish living in fresh water. In the presence of 'alarm substances' pro- 
duced by damaged skin of a member of the same species, minnows 
(and other fishes) show a 'fright reaction', scattering and refusing food. 
The state of development of the nose is very varied. It is large in 
macrosmatic solitary predators such as Anguilla and in many schooling 
species that also have well-developed eyes {Phoxinus, Gobio). Daylight 
predators, on the other hand, are microsmatic (Esox, Gasterosteus). 
Other evidence shows that fishes can discriminate between the smells 
of water plants and between the waters of different streams. It is 
likely that this provides part of the mechanism by which salmon 
return to the stream in which they were born, having been conditioned 
as fry to the smell of its water. It has been suggested that they might 
be decoyed to return to a stream other than that where they were 
hatched by conditioning them as fry to a substance such as morpholene 
to which they have a high sensitivity although it is neither an attract- 
ant nor repellant. 



vii. 19- 

Fig. 138. Diagram of ventral view of the 
sympathetic system of the front part of the 
body of Uranoscopus, showing the fibres 
in the sympathetic and oculomotor that are 
responsible for the light reflex. 
(From Young.) 

cil.brev. cil.long., short and long ciliary nerves;, ciliary ganglion; dors.r. dorsal root; dil. 
dilatator muscle; hypo, hypoglossal; n.splanch. 
splanchnic nerve; opt. optic nerve; p. pupil; 
pal. VII, palatine branch of facial ; prof, profun- 
dus; r.b. short root of ciliary ganglion; r.comm. 
ramus communicans; r.l. long root of ciliary 
ganglion; sph. sphincter muscle; ventr.r. ven- 
tral root; 1II-X, cranial nerves with their 
sympathetic ganglia (V.symp. &c.); VII hyo. 
hyomandibular branch of facial; r— 4 sp.symp. 
spinal sympathetic ganglia. 

19. Touch 

Touch is, of course, well 
developed in fishes, and in many 
species there are special sensory 
filaments, which presumably serve 
this sense. They are usually de- 
veloped around the mouth, as in 
the catfish; in other fishes they 
are modifications of the fins, for 
instance, the pectoral fins of 
gurnards, which also contain 

20. Autonomic nervous system 

The autonomic nervous system 
of bony fishes is organized on a 
plan rather different from that 
both of elasmobranchs and of 
land animals. There is a chain of 
sympathetic ganglia, extending 
from the level of the trigeminal 
nerve backwards, a ganglion 
being found in connexion with 
each of the cranial dorsal roots 
(Figs. 138 and 139). These gan- 
glia do not receive pre-ganglionic 
fibres from the segments in which 
they lie, but by fibres that run out 
in the ventral roots of the trunk 
region and thence forwards in the 
sympathetic chain. This emer- 
gence of the pre-ganglionic fibres 
for the head in the trunk region 
recalls the arrangement in land 

Each trunk sympathetic gan- 
glion, besides receiving a white 
ramus communicans of pre-gan- 
glionic fibres from its spinal nerve, 
also sends a grey ramus back to 

VII. 20 



that nerve, this ramus carrying post-ganglionic fibres to the skin. 
Some of these fibres control the melanophores, causing them to 
contract (p. 259). In elasmobranchs there are no grey rami communi- 
cantes and no sympathetic system in the head (p. 173); the differences 
between the two groups are therefore very striking. 

HI prof Viymp 

Fig. 139. Diagram of the autonomic nervous system of Uranoscopus seen from the side. 

bl. mesonephric bladder; ciliary ganglion; dors, dorsal root; n.sph. nerve to anal 
sphincter; n.spl. splanchnic nerve; prof, nervus ophthalmicus profundus; rad. brev. short 
root of ciliary ganglion; r.comm. ramus communicans (including both white and grey fibres); 
stan. 'corpuscle of Stannius' (adrenal cortical tissue?); ventr. ventral root; ///, oculomotor 
nerve; V— X symp. sympathetic ganglia associated with the cranial nerves. (From Young, 

Quart. J. Micr. Sci. 75.) 

Fig. 140. Tracing of the contractions of a strip of the stomach muscle of the angler- 
fish, Lophins, attached to a lever. Time in minutes. At A, faradic stimulation of the 
vagus nerve. Drugs then added to the solution to make, at B acetyl choline 1/1,000,000; 
at c acetyl choline 1/100,000; at D adrenaline 1/100,000. 
(From Young, Proc. Roy. Soc. 120.) 

Little is known about the parasympathetic system of bony fishes. 
The oculomotor nerve carries fibres to the iris, which work in the 
opposite direction to fibres from the sympathetic (p. 214). There is 
also a well-developed vagal system, but so far as is known no para- 
sympathetic fibres in other cranial nerves and probably no sacral 
parasympathetic system. Electrical stimulation of the vagus nerve 

224 BONY FISHES vn. 20- 

produces movements of the stomach but not of the intestine; the 
latter, however, shows movements when the splanchnic nerve is 
stimulated. In most of the viscera acetyl choline causes initiation of 



Fig. 141. Tracing of contractions of the muscle of the urinary bladder of Lopliius, 

attached to a lever. At A, D, and F faradic stimulation of vesicular nerve. Drugs added 

to make, at b acetyl choline 1/2,000,000; at c adrenaline 1/500,000; at E ergotoxine 

1/50,000. Time, minutes. (From Young.) 

Fig. 142. Tracing to show effect of atropine 1/50,000 added at A, on the contractions 

of the bladder of Lophius produced by faradic stimulation of the vesicular sympathetic 

nerve. Time, minutes. (From Young.) 

rhythmic contractions and these are inhibited by adrenaline (Figs. 
140 and 141). In Lophius this is true of the stomach, with motor-fibres 
from the vagus, intestine, with sympathetic motor-fibres, and of the 
muscles of the bladder, which contract on stimulation of the hinder 
sympathetic ganglia. However, in the trout adrenaline causes contrac- 
tion of the stomach (Burnstock, 1958). The effect of the nerves to the 


bladder is prevented by atropine (Fig. 142) but not by ergotoxine 
(Fig. 141), though the latter is the drug that in mammals often inhibits 
sympathetic motor-fibres. In these fishes, therefore, it is not possible 
to divide up the autonomic nervous system into sympathetic and 
parasympathetic divisions by either anatomical, physiological, or 
pharmacological criteria. Presumably the two 'antagonistic' systems 
found in mammals are a late development, allowing for a delicate 
balancing of activities for the maintenance of homeostasis. 

21. Behaviour patterns of fishes 

The well-developed receptors and brain of the teleostean fishes 
constitute perhaps the most important of all factors in giving them 

Fig. 143. The red belly of the stickleback releases attacking behaviour in other males 

and following by females. Of the above models only the two on the left acted as 

releasers. (From Tinbergen, Wilson Bulletin, 1948.) 

their great success. Varied habits and quick actions enable the fish to 
make full use of the possibilities provided by the special features of 
their structure — the air bladder, mouth, and so on. The receptors and 
brain make it possible for the fish to learn to react appropriately to 
many features of its surroundings. Thus the eyes besides orientating 
the fish to movements in the visual field allow the discrimination of 
wavelengths and distinct reactions to differing shapes (see Bull, 1957). 

The social behaviour of many species includes the development of 
special 'releasers', shapes, colours, or postures that are displayed by 
one individual and elicit specific reactions in another (Fig. 143). 

There is no doubt that fishes possess great powers of learning. 
They can form conditioned reflexes involving discrimination of tones, 
also second-order conditioned reflexes, in which after the animal has 
learnt to give a certain behaviour in response to a visual stimulus it is 
then taught to associate the latter with an olfactory stimulus. There 
are many other examples of such powers, but unfortunately we have 
as yet little information as to the way in which they are brought about 
by the brain. Nor have the naturalists provided us with very clear 
examples of the use of these powers by fishes in nature. There are 



VII. 21 

many tales of carp coming to be fed at the ringing of a bell, and similar 
powers of association must play a part in the life of fishes in more 
natural situations. Bull has shown that fishes can be trained to dis- 
criminate between very small differences of water flow, temperature, 
salinity or pH, and no doubt it is by means of such powers that they 
normally find a suitable habitat. 

Fig. 144. Migrations of the eels. The European species (A. anguilld) occurs along the 
coasts outlined with lines, the American species {A. rostrata) where there are dots. 
The curved lines show where larvae of the lengths indicated (in millimetres) are taken. 

(After Norman.) 

The migrations of fishes have attracted much attention, but are 
still imperfectly understood. They vary from the 'catadromous' down- 
ward migration of young animals to the sea and the reverse 'anadro- 
mous' movement to breed, to the astounding journeys of the eels, 
3,000 miles westwards from Europe or eastwards from America to 
their breeding-place in the Sargasso Sea (off Bermuda) and the return 
of the elvers to the homes of their parents (Fig. 144). No one has yet 
discovered the factors that direct these movements, currents may play 
a part, but can hardly be the only influence. Indeed it has been 
suggested that European eels never complete the journey but die in 

vii. 21 MIGRATION OF EELS 227 

their own continental waters. The populations of so-called European 
eels {Anguilla anguilld) would then be maintained by reinforcements 
of larvae of the American A. rostrata, the differences between the 
two being due to temperature and other factors (Tucker, 1959). 

Social behaviour is marked in many species and shoals of some 
fishes may contain many thousands of individuals. The animals are 
presumably kept together in most species by visual stimuli, though 
sounds may play a part. Shoaling gives protection to small fishes, and 
in some species the animals come together in shoals to breed (her- 
rings). There may also be some advantage for the finding of suitable 
feeding conditions, but on all these points we can do little more than 
speculate and hope for further information. 



1 . Classification 

Class Actinopterygii 
Superorder i. Chondrostei 

Order i. Palaeoniscoidei. Devonian-Recent 

*Cheirolepis; *Palaeoniscus; * Amphicentrum; *Platysomus, 
*Dorypterus ; *Cleithrolepis; *Tarrasius; Polypterus, bichir 
Order 2. Acipenseroidei. Jurassic-Recent 

*Chondrosteus; Acipenser, sturgeon; Polyodon, paddle-fish 
Order 3. Subholostei. Triassic-Jurassic 
Superorder 2. Holostei. Triassic-Recent 

*Acentrophorus; *Lepidotes; *Dapcdius; *Microdon; Amia, 
bowfin; Lepisosteus, gar-pike 
Superorder 3. Teleostei. Jurassic-Recent 
Order 1. Isospondyli 

*LeptoIepis; *Portheus; Clupea, herring; Salmo, trout 
Order 2. Ostariophysi 

Cyprinus, carp; Tinea, tench; Silurus, catfish 
Order 3. Apodes 

Angnilla, eel; Conger, conger eel 
Order 4. Mesichthyes 

Esox, pike ; Belone; Exoeoetus, flying fish ; Gasterostens, stickle- 
back; Syngnathns, pipe-fish; Hippoeampus, seahorse 
Order 5. Acanthopterygii 

*HopIopteryx; Zens, John Dory; Perca, perch; Labrus, wrasse; 
Uranoscopns, star gazer; Blennins, blenny; Gadus, whiting; 
Pleuronectes, plaice; Solea, sole; Lophius, angler-fish 

2. Order 1. Palaeoniscoidei 

The actinopterygian stock has been distinct since Devonian times. 
The early representatives lacked many of the specializations that we 
find in the successful bony fishes today and showed features of simi- 
larity to the Crossopterygii. These Devonian Actinopterygii had not 
yet acquired the striking signs of full mastery of the waters, which are 
so characteristic of the group today. They resembled their ancestors 
the placoderms and their cousins the crossopterygians in being rather 

VIII. 2 


clumsy, heavily armoured creatures. From this early type many lines 
have been derived and can be followed with some completeness to 
their extinction or modern descendants. Various classifications have 
been suggested. The one used here is simple but for that very reason 
obscures the multiplicity of parallel lines. A recent classification 
recognizes fifty-two orders of Actinopterygii (Grasse). 


Fig. 145. Scales of some early fishes. 
A, hypothetical condition with denticle-like substance (d.) attached to a basal bony plate lying 
in the connective tissue (ct:)\ B, 'cosmoid' scale of early crossopterygians, showing the cosmine 
layer (co.) ; epidermis (ep.) ; vascular canals (hv.) and underlying 'isopedin' {is.); C, palaeoniscoid 
scale with layers of 'ganoin' (ga.); d, lepidosteoid scale of the gar-fish with tubules (/.). (From 
Goodrich, Vertebrata, A. & C. Black, Ltd.) 

The Devonian and Carboniferous forms are grouped together in 
the order Palaeoniscoidei, and animals of similar type survive today 
as Polypterus, the bichir of African rivers, which though showing some 
specializations remains in its general organization near the palaeoniscid 

A typical Palaeozoic palaeoniscid such as *Cheirolepis was a long- 
bodied creature (Figs. 146 and 147) with a heterocercal tail, single 
dorsal fin, and pelvic fins placed far back on the body. The pectoral 
and pelvic fins had broad bases and the radials fanned out from a small 
muscular lobe, present in all early actinopterygians but lost in later 
forms. The body was covered with thick rhomboidal scales very 
similar to those of acanthodians. They articulated by peg and socket 
joints and have a structure known as palaeoniscoid (Fig. 145). The 
scale is deeply embedded and grows by addition both to the bony or 
isopedin portion and to the shiny surface-layer, the ganoin, which 
thus becomes very thick. There is a middle layer of 'pulp' correspond- 
ing to the cosmine layer of the cosmoid scale of Crossopterygii 

230 BONY FISHES vm. a 

(p. 269) and the two types have obvious similarities, though it is not 
clear how they are related. 

The skull was built on a distinctly different plan from that of 
Crossopterygii, in that there was no joint such as was present in those 
fishes to allow the front part to flex on the hind. The jaw support was 
amphistylic, in the sense that the palatoquadrate was attached to the 
neurocranium by a basal process, but the otic process did not reach 
the skull and the hind end of the jaw was supported by the hyomandi- 
bula. There were even more dermal bones than are found in modern 
Actinopterygii, arranged so as to form a complete covering for the 
chondrocranium and jaws. These bones were derived from the original 
scaly covering of the head and the naming and comparing them with 
the bones of other forms is a matter of some difficulty. Some of the 
main bones resemble in appearance and shape those found in tetra- 
pods, but there are others for which no such homologues can be 
found, and sometimes there is considerable difficulty in recognizing 
even the main outlines of the pattern. The problem is that we have 
no rigid criterion by which to set about giving names to the skull 
bones. No system yet discovered is wholly satisfactory, and we must 
admit to insufficient knowledge of the factors that determine that 
bone shall be laid down in certain areas and that sutures shall separate 
these from each other. However, some of the dermal bones lie in 
relation to the lateral line canals (or rows of neuromasts), which latter 
may provide the stimulus to bone formation. The lines are remarkably 
constant, perhaps because of their function in detecting water move- 
ments in relation to swimming, and this is the factor that determines 
the position of many of the bones. Others fill in the spaces between 
(anamesic bones). Yet others may be differentiated in relation to the 
teeth. However, the number of bones along any one line may vary 
greatly even in one species (e.g. in Amid). The whole pattern is more 
variable in fishes than in higher vertebrates, but it is usual to consider 
that the bones of early Actinopterygii resemble those of Crossopterygii 
and of the early amphibians (Fig. 194). 

The roof of the skull usually shows a large pair of parietals between 
the eyes, and post-parietals behind these. Between the parietals and 
the nostrils there are frontal bones and the front of the head usually 
also carries a number of rostral bones, not found in higher forms. 
Behind the post-parietals in the midline is a series of extrascapular 

The side of the skull of palaeoniscids is covered by numerous bones, 
including a series of pre- and post-frontals, post-orbitals, and jugals 


around the eyes. The outer margin of the upper jaw is covered by 
premaxillae and maxillae, which are the main tooth-bearing bones. 
Behind the orbital series of bones the cheek is very variable. Sometimes 
there is a large bone identifiable as a pre-opercular, with a series of 
opercular bones behind it. The lower portion of the throat was covered 
by a series of gular plates. The spiracle in these early forms opened 
above the opercular bones. The pectoral girdle was attached to the 
back of the skull by a supracleithrum, below which a cleithrum and 
clavicle made a series of dermal bones behind the gills, covering the 
cartilaginous girdle. The roof of the mouth contained a median para- 
sphenoid, with paired prevomers in front of it, and a series of 
pterygoid bones occupied the space between it and the edge of the 
jaws, the palatine, ectopterygoid, pterygoid, and sometimes others. 
Finally the lower jaw, besides the main dentary carrying the teeth, 
shows many small bones such as the pre-articular and coronoid on 
the inner surface; splenial, angular, and surangular on the outside. 

It will be clear that this skull of *Cheirolepis may be closely com- 
pared with the skull of a crossopterygian or a modern teleostean. 
The general plan is related to that of the lateral line organs arranged 
along occipital, supratemporal, and infra-orbital lines. The numerous 
small bones are evidently similar in the different groups, though it is 
not easy to assign a suitable name to every one of the more numerous 
bones of the earlier forms. 

These palaeoniscids from the Middle Devonian were rather rare 
freshwater fishes ; they had sharp teeth and probably lived on inverte- 
brates. We have no information about their internal anatomy, but it 
seems not unlikely that the air-bladder possessed a wide opening to 
the pharynx (as it still does in Polypterns, descended from this stock) 
and that they breathed air, as did other Devonian fishes. However, 
they did not have internal nostrils, which are found in the old crosso- 

During the Carboniferous and Permian the palaeoniscids were 
numerous, mostly as small, sharp-toothed fishes. Several distinct lines 
became laterally flattened and acquired an outwardly symmetrical tail 
and blunt crushing teeth (Fig. 147). These characteristics probably 
indicate a habit of feeding in calm waters, perhaps mainly on corals, 
and they have appeared several times in the actinopterygian stock 
(p. 241). Palaeoniscids of this type were formerly placed together in 
a family Platysomidae, but it is now considered probable that the 
type arose independently several times; thus * Amphicentrum is found 
in the Carboniferous, *PIatyso?nus and *Dorypterus in the Permian, 




Fig. 146. Various actinopterygians. 

viii. 2 PALAEONISCIDS 233 

*Cleithrulepis in the Triassic. Similar forms arose again later among 
the holosteans and teleosteans and we have therefore evidence that 
this type of animal organization tends to evolve into deep-bodied 
creatures. *Dorypterus further resembles modern teleosteans in a great 
reduction of its scales and in the forward movement of the pelvic fins. 

Towards the end of the Triassic animals of typical palaeoniscid 
type became rare; they were replaced by their more active and speedy, 
mainly marine descendants, the Holostei (p. 234). Certain of the lines 
that branched off in the Palaeozoic have, however, survived to the 
present time, and in spite of subsequent specializations they give us 
some idea of the characteristics of these early Actinopterygii. Perhaps 
the most interesting of these survivals are Polypterus, the bichir, and 
the related Calamoichthys, both inhabiting rivers in Africa. The air- 
bladder shows some similarity to a lung. It forms a pair of sacs lying 
ventrally below the intestine and opening to the pharynx by a median 
ventral 'glottis' (Fig. 157). This is the arrangement found in lung- 
fishes (except Ceratodus) and in tetrapods, and it seems reasonable to 
suppose that it has survived in Polypterus from Palaeozoic times. 
However, it is not certain to what extent the air-bladder is still used 
as a lung, for Polypterus cannot survive out of the water. 

This fish shows many other ancient characteristics. The covering 
of thick rhomboidal scales, hardly overlapping, gives the animal an 
archaic appearance; the structure of the scales is 'palaeoniscoid'. In 
the skin there is a layer of denticles outside the scales. The presence 
of a spiracle, the arrangement of the skull bones, and many other 
features suggest that Polypterus is essentially a palaeoniscid surviving 
to the present day. In the intestine there is a spiral valve, which 
appears to have been present in the early Crossopterygii and Actino- 
pterygii (as judged from fossilized 'coprolites') and occurs today not 
only in the Dipnoi but also in sturgeons and, though much reduced, in 
Lepisosteus and Amia. There is a single pyloric caecum in Polypterus 
(the caeca are well developed in sturgeons, Lepisosteus, and Amid). 
The tail of Polypterus is no longer markedly heterocercal, but shows 
distinct signs of that condition. We can even find a parallel among 
Carboniferous palaeoniscids for some of the special features of Poly- 
pterus. The long body and dorsal fin are found in the fossil *Tarrasius, 
which may have been close to the ancestry of Polypterus, though it 
lacks the covering of scales. The pectoral fin in *Tarrasius, as in 
Polypterus, has a peculiar lobed form, which has been compared with 
the 'archipterygial' pattern (p. 269) and hence held to show that 
these animals are related to the Crossoptergyii. The resemblance is, 

234 BONY FISHES vm. 2- 

however, only superficial and the plan of the fin is essentially actino- 
pterygian. In the brain there is a thin pallium, thick corpus striatum, 
and a valvula cerebelli. The pituitary is remarkable in that the hypo- 
physial sac remains open to the mouth. In this and other features 
(persistent pronephros) there are signs of neoteny. 

3. Order 2. Acipenseroidei 

The sturgeons are a rather isolated line descending from the palaeo- 
niscids and characterized by reduction of bone. This was already 
apparent in the Jurassic *Chondrosteus. Acipenser and other modern 
sturgeons live in the sea but migrate up the river to breed. They may 
reach a very large size (1,000 kg) and since a tenth of this is caviar 
they are exceedingly valuable. They feed on invertebrates, which they 
collect from mud stirred up from the bottom by a long snout. This is 
flattened into a pear-shaped structure in Polyodon, the purely fresh- 
water paddle fish of the Mississippi and in Psephurus in China. The 
mouth of all sturgeons is small and the jaws weak and without teeth. 
In Polyodon there is a filtering arrangement of gill-rakers in the 
pharynx. The jaws of sturgeons hang free from the hyomandibular 
and symplectic, and can be swung downward and forward during 
feeding. The skull and skeleton is almost wholly cartilaginous and the 
dermal skeleton much reduced. The tail is covered with rhomboidal 
scales, but on the front of the body there are five lines of bony plates 
bearing spines, with the skin in between carrying structures similar to 
denticles. There is an open spiracle. The internal anatomy of the 
sturgeons shows various features that have been held to show affinity 
with the elasmobranchs ; for instance, besides the spiral valve there is 
a conus arteriosus in the heart and a single pericardio-peritoneal canal. 
However, there can be no doubt that they are descended from an 
early offshoot from the actinopterygian line. They retain some fea- 
tures lost by most members of the line, but resemble the Teleostei in 
other characters, for instance a thin roof to the cerebral hemispheres. 

The palaeoniscids and sturgeons may be grouped together in a 
Superorder Chondrostci and placed with them is a third Order Sub- 
holostei, probably a mixed group, including forms that resemble 
palaeoniscids, but show various trends towards the holostean grade 
of organization i*Ptycholepis). 

4. Superorder 2. Holostei 

During the later Permian period the palaeoniscids gave rise to 
fishes of a different type, which replaced their ancestors almost com- 

viii. 4 HOLOSTEANS 235 

pletely during the Triassic and flourished greatly in the Jurassic. We 
may group together the fishes of this type as Holostei but the term 
is used variously by different authors and includes several lines, whose 
relationships are not clear. The earliest holostean, *Acentrophorus 
from the upper Permian, is much like a paleoniscid but with a small 
mouth, shorter, deeper body and slightly upturned tail. This 'abbrevi- 
ated heterocercal' tail was presumably made possible by the changed 
swimming habits resulting from the use of the air-bladder as a hydro- 
static organ. If the fish floats passively there is no need for a hetero- 
cercal tail to direct the head downwards (p. 140). Similarly, the head 
does not need to be flattened to produce an upward lift. The develop- 
ment of the air-bladder has thus made possible the lateral flattening 
and shortening of the body so characteristic of later Actinopterygii. 
The body of holosteans was at first covered with thick ganoid scales, 
but these became thinner in later types. The jaw suspension is 
characteristic, the maxilla being freed from the pre-opercular. As a 
result the lower jaw could now be protruded forwards in front of the 
upper and a 'sucking' action, characteristic of teleosts was evolved, 
the prey being drawn into the mouth from a distance (Gardiner, 
i960). By a change in the insertion of the adductor mandibulae 
muscle a more powerful jaw action then became possible. Some of the 
holosteans achieved crushing teeth and replaced the dipnoans in the 
early Mesozoic. There are various smaller distinctive holostean 
features, such as the loss of the clavicle. 

We do not know whether fishes of this type arose from a single 
palaeoniscid stock; it is very likely that the change occurred several 
times, and that throughout the Triassic and Jurassic there were 
several lines with these holostean characteristics, evolving separately. 
During the Cretaceous they became fewer, being replaced by their 
teleostean descendants, but two holosteans survive today, Lepisosteus 
the gar-pike (often written Lepidosteus) and Amia the bow-fin. These 
are freshwater fishes, living in the American Great Lakes and other 
parts of eastern North America, but the group is mainly a marine one, 
having taken to the sea in the Trias at a time when other groups were 
doing the same (palaeoniscids, coelacanths, elasmobranchs). The 
basic cause of this movement is not known, but perhaps there was an 
increase of planktonic and invertebrate life on which the fish depended. 

Lepisosteus shows a rather primitive structure and must have 
remained at approximately the Triassic stage. With its complete 
armour of thick scales (Fig. 146) it presents all the appearance of 
a primitive fish. The air-bladder opens to the pharynx and the 

236 BONY FISHES vm. 4- 

gar-pikes come to the surface to gulp air. On the other hand, it has 
developed certain special features, especially the long jaws, with which 
it catches other fishes, and the nearly symmetrical tail. Fossils similar 
to the modern gar-pike are found in the Eocene. 

Some of the later holosteans became deep- and short-bodied and 
developed a small mouth with flat crushing teeth or a beak, for 
instance, *Lepidotes (Trias to Cretaceous), and *Dapedius (Jurassic). 
They probably browsed on corals, like the modern parrot fishes 
(Scaridae). *Microdon and other 'pycnodonts' became laterally 
flattened, like some palaeoniscids and the modern sea butterflies 

Another line of holostean evolution, developing from the original 
stock, retained the streamlined body and from these both the modern 
teleosteans and the amioids were evolved (Fig. 147). *Caturus (Trias 
to Cretaceous) was covered with thick scales, but in *Pachycormns 
(Cretaceous) they are thinner; these were active pelagic predators. 
In Amia the scales became reduced to single bony cycloid scales, as in 
Teleostei. Meanwhile other changes took place, the tail. fin becoming 
externally completely symmetrical and the maxilla and other cheek 
bones reduced. Amia has nearly reached the teleostean stage but 
retains certain primitive features in the skeleton and the small eggs 
with holoblastic cleavage. 

5. Superorder 3. Teleostei 

The groups so far considered have been nearly completely replaced 
by the Teleostei, fishes derived from a holostean stock, which have 
carried still farther the tendencies to shortening and symmetry of the 
tail, reduction of the scales, and various changes in the skull, such as 
reduction of the maxilla. The type apparently arose in the sea in late 
Triassic times, but remained rare until the Cretaceous, by which time 
several different lines of evolution had already begun *Pholidophorus 
from the Trias still carried an armour of thick scales but may well 
have given rise to *Leptolepis from the Jurassic and Cretaceous, which 
is generally considered to be close to the ancestry of all Teleostei and 
may be placed close to the order Isospondyli, many of which are 
still alive. *Leptolepis was a long-bodied fish with the pelvic fins placed 
far back, a skull with a full complement of bones, and a large maxilla. 
The scales still show traces of the ganoin layer. 

From some fish like these leptolepids have been derived the 20,000 
or more species of bony fish found today. It is natural that in any 
group of animals that has evolved relatively recently classification will 

viii. 6 TELEOSTS 237 

be difficult, because the separate twigs of the evolutionary bush will 
show little difference from each other and there may be much parallel 
evolution. It is only when intermediate forms have become extinct 
that clear-cut major groups appear. It is therefore not easy to find 
useful subdivisions of Teleostei; we may divide them among five 
orders but most classifications require many more. 

The first, Isospondyli, fish with soft rays, show primitive features 
in the large maxilla, which forms the posterior margin of the upper 
jaw, the persistence of an open duct to the air-bladder, and the 
posterior position of the pelvic fins. Fishes of essentially similar type 
are known as far back as the Cretaceous (* Port hens). Several familiar 
fishes are of this type, including the salmon and trout (Salmo) and 
herrings (Clupea). The order Ostariophysi is a large group of fresh- 
water fishes, related to the Isospondyli. The anterior vertebrae are 
modified to form a chain of bones, the Weberian ossicles, joining the 
swim-bladder to the ear (p. 217). Here belong the carp and gold- 
fish (Cyprinus), roach (Leucisciis), and cat-fishes (Silurus). The eels 
(order Apodes) are rather isolated teleosts that diverged early from 
the main stock and retain many primitive features. The fourth order, 
the Mesichthyes, includes fishes such as the pike (Esox) and stickle- 
back (G aster osteus) of structure intermediate between that of the 
more primitive forms and the latest spiny-finned teleosts. The 
pipe-fishes {Syngnathus) and sea-horses (Hippocampus) are probably 
related to the sticklebacks. The flying-fish (Exocoetus) also belongs in 
this group. 

The members of the order Acanthopterygii are the most highly 
developed fishes, characterized by the stiff spines at the front of the 
dorsal and anal fins. The maxilla is short, the duct of the air-bladder 
is closed, the body shortened, and the pelvic fins far forward. Fishes 
of this type already existed in the Cretaceous (*Hoplopteryx) and the 
condition may have been evolved along several different lines; the 
group includes a vast array of modern types. Here belong the perches 
(Perca), mullet (Mugil), wrasse (Labrus), John Dories (Zeus), blennies 
(Blennius) as well as the gadid fishes such as the whiting (Gadus). 
Anglers (Lophius), gurnards (Trigla), and the flat-fishes, the plaice 
(Pleuronectes) and sole (Solea) and others, are further members of 
this very large order. 

6. Analysis of evolution of the Actinopterygii 

Our knowledge of the history of the Actinopterygii is sufficiently 
complete for us to be able to state more definite conclusions about the 

238 BONY FISHES vm. 6 

process of evolution than has been possible from consideration of the 
more ancient and less perfectly known groups of fishes. First of all 
we may emphasize the persistence of change. No actinopterygian 
fish living in the Devonian is to be found today. Polypterns may be 
regarded as a living palaeoniscid, showing features that were common 
in the Carboniferous, but it has undergone many changes since that 
time. Similarly the living sturgeons show the stage of organization 
present in the Jurassic Chondrostei, but they also have changed much. 
Lepisostens is in general structure similar to a Triassic holostean such 
as *Lepidotes and Amia to a Jurassic one such as *Caturus, but both 
have their own more recent specializations. It is not until we come to 
the Tertiary history of fishes that types belonging to recognizable 
modern genera can be found. 

The Actmopterygii have therefore been changing slowly, but con- 
tinuously, throughout the period of their existence. Was this change 
dictated in some way by a change in their surroundings? Unfortu- 
nately we cannot answer this question very clearly. The sea is a 
relatively constant medium, though not as 'unchanging' as is some- 
times supposed. In particular the relative extent of sea and fresh- 
water changes frequently and perhaps because of such a change the 
early freshwater actinopterygians took to the sea. Probably the life 
in the sea is not constant over long periods. Almost certainly the 
available nitrogen, phosphorus, and other essential elements change 
in amount. We have reason to suspect that there was an increase in 
the extent and productivity of the sea during the Triassic period. It 
may be that such gradual changes in the life in the water, depending 
ultimately on climate or inorganic changes, have been responsible for 
the continual change of the fish population. However, it cannot be 
said that we can detect evidence of any such relationship ; there is no 
clear proof that the changes in the fish populations follow changes in 
the environment. For the present we can only note the fact that change 
occurs, even in animals living in the relatively constant sea. 

Very striking is the fact that as evolution proceeds not merely does 
each genus change but whole types disappear and are replaced by 
others. Thus the palaeoniscid type of organization had disappeared 
almost completely by the Trias and become replaced by the holostean. 
A few members retained the old organization and still survive today 
as Polypterus and the sturgeons. Similarly the Holostei, with their 
abbreviated heterocercal tails, hardly survived into the Tertiary, but 
were replaced by the Teleostei, only Lepisosteas and Amia remaining 
to show the earlier organization. 


240 BONY FISHES vm. 6 

This replacement of one type by another appears much more 
remarkable when we reflect that by a 'type', say the palaeoniscid, we 
do not mean a homogeneous set of similar organisms all interbreeding. 
Quite the contrary; the palaeoniscids included many separate lines, 
each with its own peculiarities. When one 'type' therefore is thus 
replaced by another it must mean either that some one of these many 
stocks gives rise to a specially successful new population, which ousts 
the old ones or that all the members of the stock are changing their 
type together. It is not easy with a record such as that of the fish, 
which is far from continuous, to say which of these is true in any 
particular case, but we have sufficient evidence to be sure that either 
of them is possible. 

There is no certain example in the Actinopterygii of a single new- 
type replacing all the former ones, but the origin of the Teleostei may 
perhaps show a case of this sort. It is possible that the Teleostei is a 
monophyletic group, arising from a single type such as *Leptolepis 
and proving so successful that nearly all creatures of previous types 
soon disappeared. 

The Actinopterygii provide also examples of the other and perhaps 
even more interesting process, the parallel evolution of a number of 
different lines. There can be no doubt that from Palaeozoic times 
onwards several independent lines of fishes have shown similar 
changes. The tail has become shorter and more nearly symmetrical, 
the body has become flattened and deepened dorso-ventrally, while 
the pelvic fins have moved forward and the scaly armour has been 
reduced, all of these being signs of a more effective swimming and 
steering system (p. 244). As we come closer to modern times and the 
geological record becomes more complete we obtain more and more 
critical evidence that such changes have occurred in separate popula- 
tions. Thus in the descendants of the holosteans we can recognize at 
least three such lines, that leading to the round-shaped *Microdo?i, 
another leading through *Caturus to Amia, and a third through 
*Leptolepis to the Teleostei; probably there were many others. The 
important point is that although each line possessed peculiar speciali- 
zations of its own, they all showed some shortening, development of 
symmetry of the tail, and thinning of the scales. 

It is a considerable advance to be able to recognize such tendencies 
within a group. We begin to see the possibilities of a general state- 
ment on the matter. Instead of examining a heterogeneous mass of 
creatures called Actinopterygii we can recognize an initial palaeoniscid 
type and state that in subsequent ages this has become changed in 


certain specified ways and even at a specified rate. Imperfect though 
our knowledge still is, it enables us to approach towards the aim of our 
study, to 'have in mind' all the fishes of actinopterygian type. 

This is to make the most of our knowledge: there remains a vast 
ignorance. We cannot certainly correlate this tendency of the fishes 
to change with any other natural phenomena. Put in another way, 
we do not know why these changes have occurred. The sea certainly 
did not stay the same, but it does not seem likely that its changes have 
been responsible for those in the fishes. It would be very valuable to 
be able to make a more certain pronouncement on this point, for the 
case is one of crucial importance. On land the conditions are con- 
stantly changing, and therefore we often find reason to suspect that 
changes in the animals are following environmental changes. But 
can this be so in the water? 

The evolutionary changes in the Actinopterygii certainly involve a 
definite difference in the whole life. By development of the air- 
bladder as a hydrostatic organ the animals have become able to 
remain at rest at any level of the water, and thus, by suitable modifica- 
tion of the shape of the body and fins, to dash about with remarkable 
agility in pursuit of prey or avoidance of enemies. This has enabled 
them to dispense with the heavy armour and thus further to increase 
their mobility. But what made it necessary to adopt these changes? 
Not surely any actual change in the sea itself. We must look then for 
some factor imposed on the situation by the fishes themselves or the 
neighbouring animals that constituted their biotic environment. Is 
it the pressure of competition that has been responsible for the change 
in fish form ? It may well be that the presence of an excess of fishes 
has led them continually to search for food more and more actively, 
and in new places, with the result that those types showing the greatest 
ability have survived. Given the initial genetic make-up of the 
palaeoniscids, further agility is most easily acquired by those fishes 
in which competition tended to produce shorter tails, thinner scales, 
and the other characteristics towards which the animals of this group 

The fact that the same set of changes can be produced independently 
from several different populations of approximately similar type 
(and presumably genetic composition) is strikingly shown by the 
specialized creatures evolved for life in coral reefs. Animals with 
rounded bodies and small mouths, sometimes with grinding teeth, 
have appeared independently several times; in the Carboniferous, 
*Amphicentrnm\ Permian, *Platysomus and *I)oryptents; Triassic 

242 BONY FISHES vm. 6 

*Cleithrolepis\ Jurassic *Microdon and *Dapedius, and in some modern 
teleosteans such as parrot fishes (Scaridae) and butterfly fishes 
(Chaetodontidae). This is very valuable evidence of the way in which a 
common stimulus can work on genetical constitutions that are simi- 
lar but not identical. In this example the stimulus is a particular set of 
environmental conditions; in other cases a similar effect may be pro- 
duced by the stimulus of competition between animals, which was 
probably the 'cause' of the common changes that affected so many 
descendants of the palaeoniscids. 

The history of these fishes therefore gives plausible ground for the 
belief that the driving 'forces' that have produced evolutionary change 
are the tendencies of living things to do three things: (i) to survive 
and maintain themselves, (2) to grow and reproduce, (3) to vary from 
their ancestors, all of these operating under the further stress of any 
slow change in the environment. 

Finally we must consider whether this change in the fishes can in 
any way be considered to be an advance. Several times we have found 
ourselves implying that this is so, that the later teleosts are 'higher' 
than their Devonian ancestors. We shall be wise to suspect this judge- 
ment as a glorification of the present of which we are part. However, 
perhaps this danger is less marked when we are dealing with fishes not 
ancestral to ourselves, whose 'advance' does not therefore bring them 
nearer to man. The judgement can be put into quite specific terms: 
the later Actinopterygii are 'higher' than the earlier ones because they 
are more mobile, quicker, and can live free in the water with lesser 
expenditure of energy than their ancestors. Unfortunately we have 
no means of estimating the total amount or biomass of fish matter 
that is supported by the teleostean organization, but it seems possible 
that it is absolutely greater than that of any previous type, say the 
holostean or palaeoniscid. If this is true, the change in plan of struc- 
ture has perhaps led to an increase not only in fish biomass but in the 
total biomass of all life in the sea. 

The teleostean plan has certainly allowed for the development of a 
great range of specializations, fitting the animals to all sorts of situa- 
tions in the sea and fresh water. We must therefore not forget this 
adaptability in judging the status of the group: it seems likely that 
modern teleosts are more varied than any of their ancestors. This 
power to enter a wide range of habitats not previously occupied is 
perhaps the clearest sign of all that a group has 'advanced', and we 
have already suggested that it is in this sense of suiting animals to 
new modes of life that there has been a progress in evolution. It is 


true that the sea and fresh water have been in existence relatively 
unchanged throughout the period that we are considering: in a sense 
the fishes have not found a 'new' environment. But they have found 
endless new ways of living in the water. 



The variety of Actinopterygii is so great that it would be impossible 
to try to give a complete idea of it and the best that we can do is to 
consider various functions in more detail and specify some of the ways 
in which the animals have become specially modified. 

1 . Swimming and locomotion 

The teleosts have perfected in various ways the process of swim- 
ming by the propagation of waves of contraction along the body. 
The situation is different from that of elasmobranchs on account of 
the presence of the air-bladder, serving to maintain the fish steadily 
at any given level in the water. The stabilization of the animal during 
locomotion has therefore become a wholly different problem, and the 
fins are correspondingly changed. In the sharks the pectoral fins serve 
to correct a continual tendency to forward pitching and by adjustment 
of their position they are used to steer the animal upwards or down- 
wards in the water. 

With an air-bladder the fishes have become freed from the tendency 
to remain at the bottom, which was prevalent in the more primitive 
forms and is still so common in sharks that it has several times pro- 
duced wholly bottom-living ray-like types. A fish with an air-bladder 
needs only very little fin movement to maintain it at a constant depth 
or to change its depth. As Harris puts it, 'the elaborate mechanism 
of pectoral "aerofoils" and a lifting heterocercal tail is no longer needed 
for the maintenance of a constant horizontal cruising plane. Con- 
comitant with the loss of the heterocercal tail in evolution occurs a 
rapid and tremendous adaptive radiation of the pectoral fin in form 
and function.' A stage in this process seems to have been the use of 
the paired fins to produce oscillating movements during hovering, 
and this is still found in Amia and Lepisosteus, fishes that remain 
relatively slow and clumsy. 

Many of the lower teleosteans are relatively poor swimmers and 
some of them, like so many elasmobranchs, have become bottom- 
living. Thus in the catfishes there is a large anal fin, acting, like a 
heterocercal tail, to give lift and negative pitch. The pectoral fins are 
used to balance this tendency, very much as in sharks. 

IX. I 



In the more specialized teleosteans, however, the pectorals are 
placed high up on the body and are used as brakes (Fig. 148). The 
plane of the fins' expansion is vertical and they thus produce a large 
drag force and a small lift force. This lift, of course, tends to make the 
fish rise in the water when stopping, and there is also a pitching 

Fig. 148. Use of the paired fins for braking. A. Forces produced by the fins of 
Lepomis during deceleration. The pectoral and pelvic fin planes are represented by 
the heavy lines. P and V, the resultant forces on the pectoral and pelvic fin respectively. 
Dotted line and force P', condition during action of pectoral fins only, pelvic fins being 
held in 'neutral' position. G, position of centre of gravity. B. Sun-fish stopping by 
extending pectorals. Pelvic fins amputated. Although body remains horizontal, the fish 
rises during the stop. c. Front view of sun-fish producing a rolling moment by the action 
of one pelvic fin. // and /, horizontal and lateral forces. (From Harris,^, exp. Biol. 15.) 

moment, depending on the position of the fin in relation to the centre 
of gravity, usually positive. That the fish does not rise in the water, or 
pitch, when it stops is apparently due to the anterior position of the 
pelvic fins, so characteristic of higher Actinopterygii, which has 
puzzled many morphologists. Experiments on the sun-fish (Lepomis) 
have shown that after amputation of the pelvic fins the fish rises in the 
water when stopping and raises its head (positive pitch). In fact the 
pelvic fins are able to produce a downward moment and they tilt 
the nose downwards. By alterations in their position they can be used 
to control the rising or diving movements and turning one of them 
outwards produces rolling (Fig. 148). It has been suggested that the 



pelvic fins function as keels to prevent rolling, but their amputation 
in Lepomis does not produce excessive rolling. Stability in the trans- 
verse plane is presumably assured by the dorsal and anal fins. The 

Fig. 149. Differences in form of fishes. 

A, mackerel (Scomber); B, trunk-fish (Ostracion); C, sun-fish (.Mola); D, globe-fish 
(Chilomycterus); E, sea-horse (Hippocampus.); f, eel (Anguilla). (From Norman.) 

use of the fins for stopping was also developed in some Mesozoic 
fishes, for instance, in the Triassic coelacanth, *Laugia, which pos- 
sessed high pectorals, and pelvic fins in the anterior position. 

In the fishes with high pectoral fins, therefore, the pelvics are 
usually found far forward. In the flying-fish (Exocoetus), however 
(Fig. 151), high pectoral fins are found with posterior pelvics. In this 
position the pelvics would tend to help rather than hinder any 


tendency by the pectorals to produce a rise; the condition is exactly 
that which would be expected in a flying-fish. 

With these increased opportunities for delicate control of movement 
without the devices of flattening of the front part of the body and a 
heterocercal tail, the bony fishes have also been able to make many 
other improvements in the efficiency of their swimming. The caudal 
fin has, of course, adopted its symmetrical shape and is used to increase 
the efficiency in turning. After its amputation a fish is not able to turn 
in its own length as normally. 

With shortening of the body and its lateral flattening all sorts of 
new factors in streamlining the body are developed, but the details 
are difficult to understand. The nature of the turbulence produced 
by the movements of such a complicated structure is far from clear, 
but it seems probable that the shape of the higher fishes is such 
as to reduce the total skin-friction and to increase the efficiency of 
swimming. Other factors such as the flexibility, which has an impor- 
tant influence on the efficiency of the propulsive mechanism, have 
also been changed, again in ways not fully understood, by the special 
developments of the vertebral column and ribs. The speed that can 
be reached increases with the length of the fish. Cruising speeds, which 
are maintained for hours, are of the order of three to six times the 
body-length per second, the relationship varying with the species. 
During sudden bursts the speed may be much greater. Thus Bain- 
bridge found that 10 L/sec could be maintained only for one second, 
5 L/sec for 10 sec, and 4 L/sec for 20 sec (in dace, goldfish, and trout). 

The locomotion of each type of fish is adapted to its habits. Most 
freshwater fishes are 'sprinters' but there are varying degrees of 
staying power. Thus we may distinguish (1) typical sprinters (pike 
and perch), (2) sneakers (eel) with some staying power, (3) crawlers 
(rudd, bream), with considerable staying powers for escape, (4) 
stayers, either for migration (salmon) or for feeding (carp). In the fish 
with staying powers there is a lateral strip of narrow red muscle fibres 
in addition to the characteristic broad white fibres of fish muscles. 

Bathypelagic fishes, living in deep waters, below the thermocline 
at about 75 m, encounter special problems. Here currents and tur- 
bulence are low, but since the water is cold it is very viscous, making 
swimming difficult but sinking slow. Many deep-sea fishes have 
elaborate lures, often phosphorescent. They may be described as 
'floating fish traps'. They often have no swim-bladder and achieve 
an almost neutral buoyancy by great reductions of the skeleton and 
muscles (e.g. Ceratias). The only parts to be well ossified are the 



IX. i- 

jaws. On the other hand, deep-sea fishes that retain the swim-bladder 
have a well-developed skeleton and powerful muscles (Marshall, 

2. Various body forms and swimming habits in teleosts 

Departures from the streamlined body form typical of pelagic fishes 
have been very numerous; in nearly every case they are associated 
with a reduction in the efficiency of swimming as such and the 
development of some compensating protective mechanism (Fig. 149). 
Lateral flattening, which is already a feature of all teleostean organiza- 
tion, is carried to extremes in many types. Thus the angel-fish, 


Fig. 150. The angler-fish, Lophius. 

Pterophyllum, often seen in aquaria, is provided with long filaments 
and a brilliant coloration, which, in its natural habitat (rivers of 
South America), give it a protective resemblance to plants, among 
which it slowly moves. The flat-fishes (plaice, sole, halibut, &c.) have 
carried this flattening to extreme lengths. They feed on molluscs and 
other invertebrates on the sea bottom and lie always on one side. 
The upper side becomes darker and protectively coloured, the lower 
side white. In order to have the use of both eyes the whole head is 
twisted during the post-larval period. These forms are mostly poor 
swimmers, but their coloration gives them a remarkable protective 
resemblance to the background (p. 257). 

The John Dory (Zeus faber) has made a different use of lateral 
flattening. The fish is so thin that its swimming is very slow, but 
being inconspicuous when seen from in front it can approach close to 
its prey, which it then catches by shooting out its jaws. 

Flattening in the dorso-ventral plane is less common among teleosts 
than selachians. The flattened forms are mostly angler-fishes, of 


which there are several different sorts; Lophius piscatorins (Fig. 150) 
is common in British waters. It is much flattened, with a huge head 
and mouth and short tail. It 'angles' by means of a dorsal fin, modified 
to form a long filament with a lump at the end, which hangs over the 
mouth. Swimming, though vigorous, is slow, and protection (both for 
attack and defence) is obtained by sharp spines, protective coloration, 
and flaps of skin down the sides of the body, which break up the 
outline. There is even a special fold of pigmented skin over the lower 
jaw, serving to cover the white inside of the mouth. 

Other anglers are the star-gazers, Uranoscopiis of the Mediter- 
ranean and Astroscopes from the Western Atlantic seaboard. Their 
lure is a red process attached to the floor of the mouth and they lie in 
wait buried in the sand, with the mouth opening upwards and only 
the eyes showing. The colour is protective, there are poison spines, 
and in Astroscopus there are electrical organs located near the most 
vulnerable spot, the eyes, and formed from modified eye-muscles 

(P- 253)- 

Other fishes abandon the swift-moving habit for the protection 
afforded by the development of heavy armour, such as that of the 
trunk-fish (Ostracion) and the globe-fish (Chilomycterus) (Fig. 149). 
Special spinous dorsal rays, such as those of the sword-fish {Xiphias) 
may be developed, without loss of the swift-moving habit; indeed 
these fish are among the fastest swimmers. There are many groups in 
which an elongated body form like that of the eel has been developed. 
In Anguilla itself this is associated with the habit of moving over land. 
The Syngnathidae, sea-horses and pipe-fishes, no longer swim with 
the typical fish motion but by passing waves along the dorsal fins. 
The long and often grotesquely cut-up body form gives a strong 
protective resemblance to the weeds among which they live and on 
which they feed. The tail of the sea-horses has lost its caudal fin and 
is used as a prehensile organ, being wrapped around the stems of 
sea-weeds for attachment. 

Evidently the mastery that the Actinopterygii have acquired in the 
water has depended to a large extent on the freedom given by the use 
of the air-bladder as a hydrostatic organ. This gives special interest to 
the question of how this use first began. If we are right in supposing 
that the bladder was first a respiratory diverticulum of the pharynx, 
can we suppose that its value as a hydrostatic organ depended on any 
exertion of effort of the fishes, or was this a case in which those born 
with the organ better developed found themselves with an advantage ? 
It would seem that the latter orthodox Darwinian interpretation is the 


250 BUIM fiStltb IX. 2- 

more likely; we can hardly imagine the fishes striving to make their 
bladders bigger. But it must be remembered that only those that were 
active swimmers, continually venturing into new waters, would be 
able to make full use of the new organ. 

Fig. 151. Various fishes showing special conditions of the pectoral fins. 

A, eagle-ray (Myliobatis); B, dog-fish (Scyliorhimis); c, tunny (Thynmis) ; D, thread fin 

(Polynemus) ; e, sun-fish (Lepomis); f, mud-skipper (Periophtlialmus); c, scorpion fish 

(Pterois); n, cirrhitid fish (Paracirrhites); J, flying-fish (Exocoetus); K, catfish (Doras); 

L, gurnard (Trigla). (From Norman.) 

Many different fishes are able to jump out of the water, presumably 
to escape enemies. Salmon and tarpon can jump to 8 or 9 ft above 
the water. The flying-fishes have special structures to assist in such 
jumps. In Exocoetus (Fig. 151) the enlarged pectoral fins serve for 
gliding for distances up to 400 metres, but in the flying gurnards 
(Dactylopterus) they are actually fluttered up and down, though the 
flight is feeble. 

Several types of fish have the pectoral fin modified to allow 'walk- 
ing'. The gurnards (Trigld) move in this way over the sea bottom 
(Fig. 151), and the mud-skipper (Periophtlialmus) chases about catch- 


ing Crustacea and insects on land, using the pectoral fins as levers, 
provided with special anterior and posterior muscles. 

Fishes that live in situations from which they are likely to be carried 
away develop suckers. Thus in the gobies, found between tide-marks, 
the pelvic fins form a sucker. The cling-fishes (Lepadogaster) are another 
group with the same habit. The remoras have developed a sucking- 
plate from the first dorsal fin and by means of this they attach them- 
selves to sharks and other large fish. In order to catch their food they 
leave the transporting host, though they also feed on its ectoparasites. 

3. Structure of mouth and feeding-habits of bony fishes 

Although perhaps the majority of fishes are carnivorous, there are 
species with all sorts of other methods of feeding. The more active 
predators have strong jaws and sharp teeth, such as those of the pike 
(Esox), cod (Gadus), and very many others. The teeth on the edge of 
the jaw serve to bite and catch the prey, those on the walls of the 
pharynx to prevent its escape if, as is often the case, it is swallowed 
whole. The teeth can often be first lowered to allow entrance of the 
prey and then raised to prevent its exit (e.g. in Lophius). In connexion 
with this habit the walls of the oesophagus and even stomach are 
often composed of striped muscle, capable of quick and powerful 

Many carnivorous fishes are very fierce. For instance, the blue fish 
(Potnatomas) of the Atlantic move in shoals, cutting up every fish 
they meet, making a trail of blood in the sea. The barracuda (Sphy- 
raena) of tropical waters may attack man. They are said to chase 
shoals of fish into shallow waters and to keep them there to serve for 
food as required. 

Other fishes feed on invertebrates and are then usually bottom- 
feeders. Thus the plaice (Pleurojiectes) has developed chisel-like teeth 
on the jaws and flattened crushing teeth in the pharynx; it feeds 
largely on molluscs. The Labridae (wrasses) also have blunt teeth 
and eat molluscs and crabs. The sole {Soled) has a weaker dentition 
and eats mostly small Crustacea and worms. Fish such as the herring 
{Chipea) that live on the minute organisms of the plankton have small 
teeth and weak mouths, but are provided with a filtering system of 
branched gill-rakers, making a gauze-like net, comparable with the 
filtering system found in basking sharks (p. 181), paddle-fish (p. 234), 
and whale-bone whales (p. 669). 

Herbivorous and coral-eating fishes have crushing teeth similar to 
those of the mollusc-eaters; indeed, many forms with such dentition 

252 BONY FISHES ix. 3- 

will take either form of food. The parrot-fishes (Scaridae) have a beak 
and a grinding mill of flattened plates in the pharynx. With this they 
break up the corals, rejecting the inorganic part from the anus as a 
calcareous cloud. The Cyprinidae, including many of our commonest 
freshwater fishes (goldfish, carp, perch, and minnow), have no teeth 
on the edge of the jaw, hence the name 'leather-mouths'. There are, 
however, teeth on the pharyngeal floor, biting against a horny pad 
on the floor of the skull. These fishes are mainly vegetarians, but many 
take mouthfuls of mud and extract nourishment from the plants and 
invertebrates it contains. 

4. Protective mechanisms of bony fishes 

In general teleosts depend for protection against their enemies on 
swift swimming, powerful jaws, good receptors, and brain. The 
majority of them have thus been able to abandon the heavy armour 
of their Palaeozoic ancestors. In many cases, however, subsidiary 
protective mechanisms have been developed, and are especially pro- 
minent in fishes that have given up the fast-swimming habit and taken 
either to moving slowly among weeds or to life on the bottom. These 
developments are a striking example of the way in which, following 
adoption of a particular mode of life, appropriate subsidiary modifica- 
tions take place, presumably by selection of those varieties of struc- 
ture that are suited to the actions of the animal. 

These protective devices may be classified as follows : 

1. Protective armour of the surface of the body. 

2. Sharp spines and poison glands. 

3. Electric organs. 

4. Luminous organs. 

5. Coloration. 

5. Scales and other surface armour 

The typical cycloid teleostean scales have already been described. 
They form a covering of thin overlapping bony plates, providing some 
measure of protection, but not interfering with movement. The 
hinder edges of the scales are sometimes provided with rows of spines, 
and are then said to be ctenoid. In many fishes the scales bear 
upstanding spines and possess a pulp cavity, which recalls that of 
denticles. In the tropical globe-fishes (or puffers) and porcupine- 
fishes (Diodon) these spines are very long and sharp and the puffers 
are able to inflate themselves and cause the spines to project outwards, 
a very effective protective device. In a few fishes the scales have 


become developed to form a bony armour even more complete than 
that of the Palaeozoic fishes. Thus in the trunk- or the coffer-fishes 
(Ostracion) the scales are enlarged and thickened into a rigid box, 
from which only the pectoral fins and tail emerge as movable struc- 
tures, the former apparently assisting the respiration, the latter the 
swimming. These fishes live on the bottom of coral pools and have 
a narrow beak with which they browse on the polyps. 

6. Spines and poison glands 

Sharp protective spines are often found in teleosts, especially on the 
operculum and dorsal fins. These may be provided with modified 
dermal glands that inject poison into the wound. Thus the European 
weever (Trachinus) lives buried in the sand and has poison spines on 
the operculum and the dorsal fins. It is suggested that the dark 
colour of the fins serves as a warning. Some catfishes, scorpion fishes, 
and toad-fishes also have poison spines. Spines may be effective even 
if not poisonous; the stargazer, Uranoscopus, of the Mediterranean 
and tropical waters has powerful spines on the operculum, which 
inflict a most unpleasant wound if the animal is disturbed by hand 
or foot while lying in the sand angling for its prey (p. 249). Lophius, 
the angler, is also armed with dangerous spines. Several species of 
catfish have large spines, sometimes serrated. In the trigger-fishes 
(Balistidae and related families) of the tropics one or more of the fins 
is modified to make a spine that can be raised and locked in that posi- 
tion. These fishes have very brilliant coloration, but since some of 
them live in the highly coloured surroundings of coral reefs it cannot 
be considered certain that the colours serve as a warning. 

7. Electric organs 

The power to produce electric discharges has been developed 
independently in four distinct families of teleosts, as well as in 
torpedoes and rays. The electric organs arise bilaterally from modified 
muscle fibres, the cells of which are plate-like and arranged in rows, 
the electroplaques. Each plate is innervated on only one surface by 
motor neurons whose activity is controlled from the forebrain, in 
some fish there is a controlling nucleus located in the medulla. The 
physiological properties of transmission at the nerve endings with the 
electroplaques are similar to those of motor end plates. Unlike other 
electrogenic tissues such as muscle or nerve, electric organs can 

254 BONY FISHES ix. 7- 

develop appreciable voltages in the surrounding fluid, up to 550 volts 
in Electrophorus, the electric eel of the Amazon. These voltages are 
achieved by series summation of the electromotive forces generated 
by the individual cells. 

The columnar array of several hundreds or thousands of electro- 
plaques in series in the strongly electric fish, Electrophorus, Malapterurus 
and Torpedo are paralleled so that the electric organs of these fish can 
generate considerable current at high voltage. A maximum peak power 
of up to 600 watts has been observed in T. nobiliana. The electric 
organs form the major part of the body of the strongly electric fish. 
The discharges are used for offence and defence. The weakly 
electric fish (Gymnotidae, Mormyridae) have only a few columns 
of series arrays, and relatively few electroplaques in each column. 
However, many of the species emit pulses of low voltages more 
or less continuously and regularly (60-400/sec). These pulses prob- 
ably serve as the power components in an electrical guidance 
system. All species of the continuously emitting fish are sensitive to 
changes in the conductance of the water. Presumably the fish sense 
the altered electric field of their discharges; although the receptors 
have not yet been identified specialized lateral line organs (mormyro- 
masts) are often present. 

8. Luminous organs 

Fishes of many different families live at great depths and 95 per 
cent of individuals caught below 100 fathoms are luminescent. The 
development of luminescent organs is therefore a further example of 
parallel evolution. The organs usually show as rows of shining beads 
of various colours on the sides and ventral surface of the fish. 

In many species the light is due to organs containing luminous 
bacteria, whose appearance may be controlled by the movement of a 
fold of skin, or of the whole organ, or of chromatophores. Some 
teleosts, however, have self-luminous photophores and these are also 
found in Spinax and a few other Squalidae. They are formed from 
modified mucous glands, and may be provided with reflectors and 
even lenses. They can be flashed on and off, probably by sympathetic 

The luminous organs probably often serve for recognition of the 
sexes and often show distinctive patterns. They may serve to startle 
attackers and in a few cases to illuminate the prey. In the deep-sea 
anglers (Ceratias) the luminous tip of the fin is used as a lure. 

IX. 9 (255) 

9. Colours of fishes 

The bony fishes show perhaps the most brilliant and varied colora- 
tion of any animals, rivalling even the Lepidoptera and Cephalopoda 
in this respect. The enormous range of colour and pattern provides 
an excellent example of the detailed adjustment of the structure and 
powers of animals to enable them to survive. A great difficulty is 
introduced into the study of animal coloration by the fact that we are 
usually ignorant of the capacity for visual discrimination possessed 
by the animals likely to act as predators. Moreover, it is very difficult 
for us to obtain this information. When we examine any two objects 
we are able to say not merely that they are different but that one is 
red and the other green. A person or animal that is colour-blind may 
also be able to detect a difference, but yet remain unaware of any 
distinction of colour; the objects appear to him only as differing in 
brightness. In order to decide whether animals are able to distinguish 
between light of two wavelengths we must present them with objects 
of different colour but the same brightness. 

We are therefore faced with the possibility that some of the colours 
that appear to us so brilliant are to other animals merely differences of 
tone, and animals to us conspicuous because coloured, when seen in 
monochrome, may be protected. Some of the colours of fishes may 
be only a means of producing a pattern of protective greys, as seen 
through the eyes of an attacker. However, there is no doubt that some 
fishes are able to discriminate between illuminated bodies which 
though of different wavelength reflect light of equal brightness. In 
the subsequent description of fish coloration we shall not be able to 
consider predators further, but shall describe the colours as they 
appear to the eye of a normal man. 

The colour of fishes is produced by cells in the dermis, (a) the 
chromatophores and (b) the reflecting cells or iridocytes (Fig. 152). 
The chromatophores are branched cells containing pigment, which 
may be either black (melanin) or red, orange, or yellow (carotenoids 
or flavines). The iridocytes contain crystals of guanin, making them 
opaque and able to reflect light so as to produce, where no chroma- 
tophores are present, either a white or a silvery appearance. This 
material is used in the manufacture of artificial pearls, the scales of the 
cyprinoid Alburnus lucidus (the bleak) being used for the purpose. 
The iridocytes may be either outside the scales, when they produce 
an iridescent appearance, or inside them, giving a layer, the argenteum, 
that produces a dead white or silvery colour. By a combination of the 

256 BONY FISHES ix. 9 

chromatophores, and of these with the iridocytes to produce inter- 
ference effects, a wide range of colour is produced. Thus by mixing 
yellow and black either brown or green is produced. Blue is usually 
an interference colour. 

The use of the colour by the fish may be classified, according to the 
scheme introduced by Poulton, as cryptic or concealing, sematic or 
warning patterns, and epigamic or sex coloration. Cryptic coloration 

TpT Black chromabophore 
^pa Yellow chroma tophore 
o Iridocyte 

Fig. 152. Coloration elements in the skin of the upper side of 
a flounder (Platichthys). (After Norman.) 

may be achieved in various ways and may be subdivided into two 
main types: (1) assimilation with the background, (2) breaking up the 
outline of the fish. Assimilation is common, but is often associated 
with some degree of disruption of outline. The absence of all pig- 
mentation in pelagic fishes, for instance the Leptocephalus larvae of 
eels, is an example of assimilation. Fishes living among weeds, such 
as the sea-horses and pipe-fishes, or Lophius the angler, often resemble 
the weeds in colour, and in addition develop 'leaf-like' processes. 
The colour of many familiar fishes, such as the green of the tench, 
may be said to resemble that of the surroundings by assimilation. 
When we consider the much more numerous examples of patterns 
involving several colours the distinction between assimilation and dis- 
ruption is more difficult to draw. Many free-swimming pelagic fishes 
have the upper side dark and striped with green or blue, whereas the 
under-side is white, the beautiful pattern that is seen in the mackerel 
(Scombei). This gives them protection from above and below, the 

IX. 9 



striping probably making the animal less conspicuous in disturbed 
water than it would be if of uniform colour. The white under-side also 
serves to lessen any shadows, an important factor for animals that live 
in shallow water; similar shading is used by land animals. 

Fig. 153. Colour patterns of various tropical fishes. 

A, Muraena {Gymnothorax); b, bat-fish (Platax); c, butterfly fish (Holacanthus); n, butterfly 

fish {Cliaetodon); e, perch (Grammistes). (From Norman.) 

Devices of spots and stripes are found on fishes that live against a 
variegated background (Fig. 153). The beautiful red and brown mark- 
ings of a trout are a good example. Flat fishes, living on sandy or 
gravelly bottoms, adopt a spotted pattern, which gives them a high 
degree of protection, and we shall see later that they are able to change 
colour to suit the ground on which they rest. The brilliant colours 
of many tropical fishes probably serve mainly to break up the outline, 
though no doubt the surroundings in which they live are also brilliant. 
Great variety of colours may be found on a single fish, especially in 

258 BONY FISHES ix. 9- 

thc trunk-fishes (Ostracioti), one species of which is described as 
having a green body, yellow belly, and orange tail, while across the 
body are bands of brilliant blue, edged with chocolate-brown. More- 
over, the female has another colour scheme and was for long con- 
sidered as a different species! 

Colour differences between the sexes are frequent in fishes, the male 
being usually the brighter. Thus in the little millions fish, Lebistes, 
there are numerous 'races' of males with distinctive colours, but the 
females are all of a single drab coloration. The genetic factors that 
produce the various types of male are carried in the Y chromosome. 
Presumably the colour of the males acts as an aphrodisiac as a part 
of the mating display, but the significance of the different races is not 

Sematic or warning coloration involves the adoption of some strik- 
ing pattern that does not conceal but reveals the animal. This type 
of colouring is found in animals that have some special defence or 
unpleasant taste (such as the sting of the wasp), and its use implies that 
animals likely to attack are able to remember the pattern and the 
unpleasant effects previously associated with it. It is not easy to be 
certain when colours are used in this way, but it is possible that the 
conspicuous spots on the electric Torpedo ocellata have this function. 
Among teleosts there is the black fin of the weevers {Trachinus), pos- 
sibly a warning of their poison spines, and the spiny trigger-fishes 
and globe-fishes (p. 253) also have conspicuous colours. 

10. Colour change in teleosts 

In spite of the reputation of the chameleon the teleosts are the 
vertebrates that change their colour most quickly and completely. 
The melanophores are provided with nerve-fibres (Fig. 154), and 
these cause contraction of the pigment and hence a paling of the skin 
colour. The processes of the cells themselves are not withdrawn, the 
colour change is produced by a movement of pigment within them. 

The nerve-fibres in question are post-ganglionic sympathetic fibres, 
leaving the ganglia in the grey rami communicantes (Fig. 139) to all 
the cranial and spinal nerves. The pre-ganglionic fibres that operate 
them, however, emerge only in a few segments in the middle of the 
body (Fig. 235), so that severance of a few spinal roots will affect the 
colour of the whole body. When a nerve to any part of the skin is cut 
the chromatophores in that region at first expand, making a dark area 
(Fig. 155). After a few days, however, the skin involved gradually 
becomes lighter, the process, it is alleged, beginning at the edges and 




moving inwards. Parker, who has made a careful study of these 
phenomena, believes that they indicate the presence of melanophore- 
expanding nerve-fibres (said to be of 'parasympathetic' nature). Fol- 
lowing the cut these fibres are supposed to be stimulated to repetitive 
discharge and hence to make the dark band. Later the band pales 

Fig. 154. Nerves of the melanophores of a perch. (From Ballowitz.) 

Fig. 155. Diagrams showing, left, a cut in the tail of the fish Funduhis producing 

a band of dark melanophores; right, when the dark band has faded a second cut 

makes the melanophores again dark. (After Parker, Quart. Rev. Biol. 13.) 

because the stimulating substances ('neurohumors') produced at the 
nerve-endings of the melanophore-contracting fibres in the neigh- 
bouring areas diffuse in gradually. 

This hypothesis involves two physiological propositions which are 
so novel that they would require detailed evidence for acceptance. 
Firstly the act of cutting is presumed to set up a discharge of impulses 
lasting for several days, which is unlikely. Moreover, the discharge is 
presumed to be only in the melanophore-expanding fibres and not in 
those that produce contraction. Secondly, electrical stimulation of 
nerves in teleosts always produces paling and never darkening (except 

2 6o BONY FISHES ix. 10- 

after the use of ergotamine). We must assume, therefore, that this 
form of stimulation has the opposite effect to section and only stimu- 
lates the melanophore-contracting nerve-fibres. Since neither of these 
propositions is adequately demonstrated, we must reject the hypo- 
thesis and say that there is not sufficient evidence of melanophore- 
expanding nerve-fibres. 

There is, however, another agent that causes expansion of melano- 
phores in a wide variety of vertebrates, namely the posterior lobe of 
the pituitary(see p. 206), and there is evidence that this works also in 
teleosts. Hypophysectomized specimens of the Atlantic minnow 
Fiindulns are nearly always lighter than normal individuals, especially 
when on a dark background. Injection of posterior pituitary extracts, 
or placing of isolated scales in the extract, causes expansion of the 
chromatophores of any teleost. We may conclude that colour change 
is produced by the nerve-fibres tending to make the animals pale and 
secretion of the posterior pituitary to make them dark. Adrenaline 
induces contraction of chromatophores, and is presumably similar to 
the sympathetic transmitter. 

It is more difficult to decide how external influences are linked with 
this internal mechanism. Fishes mostly become pale in colour on a 
light background and vice versa, and the effect is produced pre- 
dominantly through the eyes. There may also be a slight direct effect 
of light on the chromatophores. The change in colour begins rapidly, 
but its completion may take many days. Analysis of the rates of 
change in normal fishes and in those with anterior and posterior 
pituitary removal has led to the suggestion that the anterior lobe 
produces a substance tending to make the fish lighter in colour, at 
least in the eel. A similar hypothesis has been fully worked out by 
Hogben and his colleagues in amphibia (p. 300). The colour is also 
influenced by the pseudobranch, a secretory tissue in the first gill 
arch. After removal of this a fish becomes dark and the choroid gland 
of the eye, which receives blood from the pseudobranch, degener- 
ates. It is suggested that the pseudobranch produces a hormone, 
whose entry into the circulation is controlled by the choroid gland. 

The value of the colour change in bringing the animals to the same 
tint as their surroundings is considerable. Fishes kept on a light back- 
ground are very conspicuous for the first few minutes when trans- 
ferred to a dark one. The fisherman acknowledges this by painting 
the inside of his minnow-can white, to ipake the bait conspicuous. In 
the flat fishes, living on the sand, the protection assured by the colour 
change is of special importance. It has been suggested that it is pos- 



sible for the fish to assume a pattern similar to that of the ground 
on which it lies, but it is probable that the degree of expansion of the 
chromatophores is adjusted to suit the amount of light reflected from 
the ground; by increasing or decreasing the areas of dark skin, effects 
approximately appropriate to various backgrounds are produced. 

Fig. 156. Special respiratory apparatus, A, in climbing perch (Anabas); b, Indian 
catfish (Saccobranchus); c, African catfish (Clarias). (From Norman.) 

11. Aerial respiration and the air-bladder 

Many fishes are able to live outside the water. The excursions on to 
the land vary from the wriggling of the eel through damp grass to the 
life of the Indian climbing perch {Anabas) spent almost entirely on 
land. In the eel there is no special apparatus for breathing air (though 
oxygen may be taken in through the skin). The climbing perch is pro- 
vided with special air chambers above the gills (Fig. 156) and even 
when in water it comes to the surface to gulp air and will 'drown' if 
prevented from doing so, even though it is placed in well-oxygenated 

Many other fishes gulp air, especially those living in shallow tropical 
waters, which readily become deoxygenated. There may be other 
special mechanisms for gaseous interchange. In the Indian catfish 



IX. 11 

Saccobranchns there are large air sacs growing a long way down the 
body from the gill chambers (Fig. 156). 

The air-bladder, which has contributed so largely to the success of 
the later teleosts, may have arisen as an accessory respiratory organ, 










Fig. 157. Air-bladder of various fishes, seen from in front and from the left side. 

A, air- or swim-bladder; ad, air-duct; D, digestive tract. (From Dean, Fishes, Living & 

Fossil, The Macmillan Co., after Wilder.) 

used in the same way as those described above. In all the more 
primitive teleosts (Isospondyli) the air-bladder preserves in the adult 
its opening to the pharynx ('physostomatous'), whereas in higher 
forms it becomes completely separated ('physoclistous'). Survivals of 
still earlier Actinopterygii have the opening especially well developed, 
though it varies from group to group (Fig. 157). Thus in the stur- 
geons there is a wide opening into the dorsal side of the pharynx. 
In Amia and Lepisostens the opening is also dorsal and the walls of 
the sac are much folded and used for respiration. In Polypterus 
the opening is ventral and the bladder has the form of a pair of lobes 
below the gut. This arrangement recalls that of the tetrapod lungs and 

ix. ii THE AIR-BLADDER 263 

is also found in the modern lung- fishes and presumably in their 
Devonian ancestors, from which we may suppose that the tetrapods 
arose (p. 276). This ventral position of the air-bladder was one of the 
features that for a long time led zoologists to suppose that Polypteriis 

A B 

Fig. 158. Diagrams illustrating the blood-supply of the air-bladder in A, Polypterus, 
b, Ceratodus, c, Aviia, and d, a teleost. The blood-vessels are seen from behind, and 

cut short in transverse section. 
a. dorsal aorta; aad. anterior dorsal artery from the coeliac; aav. ant. ventral artery; 
ab. air-bladder; aid. anterior dorsal vein to the cardinal; ba r \ 4th aortic arch (6th of the 
series); d. ductus Cuvieri; ev. coeliac artery; la. left pulmonary artery; oe. oesophagus; 
pr. portal vein receiving posterior vein from air-bladder; ra. rii^ht 'pulmonary' artery ; rpv. 
right (branch of) 'pulmonary'' vein; rv. right vein from air-bladder; v. left 'pulmonary' 
vein. (From Goodrich, Vertebrata, A. & C. Black, Ltd.) 

was a member of the crossopterygian line of fishes. It is probable, 
however, that the affinity is only that which persists between all 
primitive members of both Actinopterygii and Crossopterygii and 
is to be taken as an indication that the air-bladder was originally a 
widely open respiratory sac, or perhaps pair of sacs. Once the power 
to produce a pharyngeal diverticulum had been developed it is easy 
to imagine that the actual position of the opening might shift either 
dorsally, as in the later Actinopterygii, or ventrally, as in the tetrapods. 
The blood-supply of the air-bladder should provide some indica- 
tions both of its origin and function. In Polypterus and Dipnoi there 
are pulmonary arteries springing from the last (sixth) branchial arch 

264 BONY FISHES ix. n- 

and presumably containing venous blood (Fig. 158). Blood returns 
to the heart by pulmonary veins. Essentially the same arrangement 
is found in Amia, but in all other Actinopterygii oxygenated blood is 
supplied to the bladder from the dorsal aorta (or sometimes from the 
coeliac artery). Probably, then, the original function of the air-bladder 
was respiratory, and this may still be its main function not only in 
Amia and Lepisosteus but also in some of the physostomatous Tele- 
ostei. However, in the majority of teleosts its dorsal position, closed 
duct, and arterial blood-supply show that it has some other function 
and it has long been supposed that this is concerned in some way with 
flotation. The air-bladder is absent from bottom-living forms, such 
as flat-fishes, Lophius and Uranoscopus, though it may be present in 
their pelagic larvae. 

The bladder is provided with special glands by which it is filled 
and the gas they secrete is mostly oxygen; only in some physosto- 
matous forms is the bladder filled by gulping air. Nitrogen and carbon 
dioxide are also present and the former even constitutes the main gas 
in some freshwater fishes at great depths. In the more primitive forms 
gas is secreted all over the surface of the bladder, but later there 
develop special anterior oxygen-secreting and posterior oxygen- 
absorbing regions. The former, known as the red gland, has a special 
apparatus of blood-vessels, the rete mirabile, and the latter, or 'oval', 
which may be developed from the closed end of the pneumatic duct, 
has a special sphincter by means of which it can be closed off. 

The pressure of the gases in the swim-bladder is adjusted to make 
the fish neutrally buoyant, which is achieved when the bladder 
occupies 7-10 per cent of the total volume in fresh-water and 5 per 
cent in marine fishes. This may involve partial pressures of oxygen, 
carbon dioxide, and nitrogen many times greater than those in the 
blood. The mechanism by which the gases are secreted against a 
diffusion gradient of several atmospheres has been much discussed. 
Carbonic anhydrase is present in the gas gland and the oxyhemo- 
globin of fish blood is especially sensitive to carbon dioxide, giving up 
its oxygen even at high oxygen concentration. 

If weights or floats are attached to a fish it maintains its position 
in mid-water by swimming while gas is secreted or absorbed. The 
receptors concerned are therefore not activated by the tension in the 
bladder but perhaps by the movements that are necessary when the 
fish is not in equilibrium. The bladder is innervated by the vagus and 
sympathetic nerves and after severing the former gas secretion ceases. 

The various diverticula connecting the bladder with the ear (and 

IX. 12 



the Weberian ossicles, p. 217) may be associated with pressure recep- 
tors that assist in the control of the bladder. Loaches are famous as 
fish barometers, whose behaviour can be used to predict weather 

12. Special reproductive mechanisms in teleosts 

The teleosts show great variation in breeding habits, the eggs being 
sometimes left to develop entirely by themselves, in other cases looked 
after by one or both parents, while in a few species they develop 

Fig. 159. Deep-sea fish Photocorynus with parasite male attached. (From Norman.) 

viviparously within the mother. Hermaphrodite individuals are not 
uncommon and in some species of Sparidae and Serranidae are 
invariably monoecius and self-fertilizing. The method of association 
of the sexes is correspondingly varied and there are numerous devices 
for bringing sexes together, such as colour differences, sound produc- 
tion, and the liberation of stimulating substances into the water. In 
some deep-sea fishes the male is much smaller than the female, to 
which it remains permanently attached (Fig. 159). Breeding is often 
preceded by a migration of the fishes to suitable situations and the 
association into large shoals. 

The eggs may be classified as either pelagic, if they float, or demersal, 
if they sink to the bottom. In the former case they are sometimes pro- 
vided with an oil globule and are exceedingly numerous. Thus a 
single female turbot has been calculated to contain nearly 10 million 
eggs, a cod 7 million, and a ling 28 million, whereas the herring, 
whose eggs sink to the bottom, probably does not lay more than 

266 BONY FISHES ix. 12 

50,000 eggs. The large numbers laid by the pelagic species are pre- 
sumably an insurance against failure of fertilization and especially 
against random elimination of the eggs and young. The greater the 
care devoted to the young by the parents the smaller the number of 
eggs produced (see, however, p. 283). 

Demersal eggs, especially of freshwater animals, are usually laid 
with some special sticky covering, by means of which they are 
attached to each other and to the bottom or to stones, weeds, &c. 
Thus the eggs of many cyprinids (carp, &c.) are attached to weeds. 
The eggs of salmon and trout, however, though demersal, are not 
sticky. From depositing eggs on weeds it is only a short step to the 
building of a nest and guarding of the eggs by one or both parents. 
Thus the sand goby (Gobius minutus) lays its eggs in some protected 
spot, where they are guarded by the male, who aerates them by his 
movements. Quite elaborate nests may be built, as by the sticklebacks 
(Gasterosteus), where pairs remain together throughout the breeding- 
season. A still further development is the retention of the young 
within the body. In some catfishes they develop within the mouth of 
either parent. In pipe-fishes and sea-horses the males are provided 
with special pouches for the young. 

Although external fertilization is usual, various teleosts show 
internal fertilization and the young then develop within the ovary 
(Zoarces, Gambnsia, Lebistes). The mechanisms by which mating and 
the nutrition of the embryos are assured in these cases show some 
interesting parallels with the conditions in mammals, including the 
formation of placentae or nutritive material. In Lebistes the female 
adopts a special position of readiness for copulation, and this has been 
shown to depend partly on an internal factor in the female and partly 
on a substance secreted into the water by the male. The embryos are 
not attached to the wall of the ovary but develop free in the sac, feed- 
ing upon an 'embryotrophic' material, apparently produced by the 
discharged ovarian follicles, which become highly vascular and remain 
throughout the several months of 'pregnancy'. 

Rhodeus amarus, the bitterling (Cyprinidae), shows somewhat 
similar conditions (Fig. 160). Association of the sexes at mating is 
here made necessary by the fact that the eggs are laid within the 
siphon of a swan mussel. For this purpose the cloaca of the female 
develops into a tubular ovipositor. This development takes place 
under the influence of a hormone produced by the ovary. Addition of 
progesterone and related substances to the water containing the fish 
causes growth of the ovipositor. 



The full growth of the ovipositor and preparation of the female for 
spawning depends on the presence in the water of the male and also 
of the swan mussel. Water in which males have been kept stimulates 
growth of the ovipositor. When the female is ready to deposit the eggs 
she adopts a vertical position in the water and the spawning male, in 


Fig. 160. Male and female bitterling (Rhodeits) with swan mussel 
in which eggs are about to be deposited. (From Norman.) 

full nuptial coloration, swims around her. An egg passes into the 
oviduct and erection of the ovipositor is produced by pressure of the 
urine, produced by contraction of the walls of the urinary bladder, the 
exit being blocked by the egg. The extended ovipositor is thus able 
to place the egg within the siphon of the mussel and the male then 
immediately thereafter sheds his sperms over the opening and they 
are presumably carried in by the current. The whole process shows 
the elaborate interplay of internal devices and external stimuli neces- 
sary for the perfection of this remarkable method of caring for the 
young. Yet the various features are all developments of systems found 
in other vertebrates. 



1. Classification 

Class Crossopterygii 
Order i. Rhipidistia. Devonian-Recent. 

Suborder i. *Osteolepidoti. Devonian-Carboniferous 

*Osteolepis; *Sauripterus; *Diplopterax; *Eiisthenopteron 
Suborder 2. Coelacanthini (= Actinistia). Devonian-Recent 
*Coelacanthus; *Undina; Latimeria 
Order 2. Dipnoi. Devonian-Recent. 

*Dipterus; *Ceratodns; Neoceratodas; Protopterus; Lepidosiren 

2. Crossopterygians 

Although the lung-fishes and their allies are here considered last of 
all the groups of fishes, because they lead on to the amphibia, it is 
important to realize that in many features they stand close to the 
ancestral stock of gnathostomes. It is a mistake to consider them as 
'higher' animals than, say, the elasmobranchs or actinopterygians. 
Only four genera belonging to this group are found at the present 
time, Neoceratodus, Lepidosiren, Protopterus, the lung-fishes of Aus- 
tralia, South America, and Africa respectively, and Latimeria, recently 
discovered off the east coast of South Africa and the Comoro Islands 
off Madagascar. These are relics of a group that can be traced back 
with relatively little change to the Devonian, and there is little doubt 
that at about that period the first amphibia arose from some similar 
line. The characters of the modern crossopterygians are therefore of 
extraordinary interest, because they show an approach to the condition 
of the ancestors of all tetrapods. 

3. Osteolepids 

Osteolepis itself (Fig. 161), from the middle Devonian, was the 
earliest and most primitive member of the group. In appearance it 
shows an obvious similarity both to palaeoniscids and to early Dipnoi 
and it was probably close to the line of descent from some placoderm 
ancestor to both of these groups and to the amphibia. The body was 
long and the tail heterocercal. A feature distinguishing all early Cros- 
sopterygii from early Actinoptergyii was the presence of two dorsal 

x. 1-3 OSTEOLEPIDS 269 

fins in the former. The paired fins have a characteristic scaly lobed 
form, from which the group derives its name, and the skeleton of the 
pectoral fin contained a basal element attached to the girdle and a 
branching arrangement at the tip (Fig. 180). This plan is distinctively 
different from that of the rayed fin of the Actinopterygii, but could 
also easily have led to the evolution of a tetrapod limb (p. 307). 

The body was covered with thick, pitted rhomboidal scales, with an 
appearance very similar to that of the palaeoniscid scale. These scales 
have, however, a characteristic structure known as cosmoid. Each scale 
(Fig. 145) may be considered as composed of an upper layer of dentine 
(the cosmine), with a hard covering of shiny vitrodentine, possibly com- 
parable with enamel. Below the cosmine is a 'vascular layer' consisting 
of pulp cavities in which lay odontoblasts whose processes made the 
dentine. This layer in turn rests on a bony layer of isopedin. The struc- 
ture appears to have some relation to that of placoid scales and no 
doubt the morphogenetic processes that give rise to the isolated pulp 
cavities of placoid scales are similar to those that produce the cosmoid 
plates. It is usual to suggest that the latter are formed of 'fused den- 
ticles', but this is of course only a manner of speaking. Denticles do 
not fuse, but morphogenetic processes may occur in such a way as to 
produce flat plates of dentine. Indeed, it is possible that the evolution 
occurred in the other direction, that is to say that the placoid scale 
is a special case of the cosmoid. The condition in which a substance is 
formed nearly uniformly all over the surface of the body is a more 
general one than that in which such formation occurs only in isolated 
areas. Indeed, the discontinuous arrangement is a very remarkable 
condition, for which we have at present no explanation. The relation- 
ship of the cosmoid to the ganoid scale of early Actinopterygii is not 
quite clear, but the ganoid type seems to show a reduction of the 
pulp cavities and development of the shiny surface-layer. The early 
Dipnoi of the Devonian possessed cosmoid scales. In later osteolepids 
and Dipnoi there has been a thinning of the scales, as among the 
Actinopterygii, so that the later Dipnoi are covered with thin, over- 
lapping, 'cycloid' scales. 

The skull of osteolepids (Fig. 161) was well ossified; there was a 
series of bony plates arranged according to a pattern with a general 
similarity to that of palaeoniscids (p. 230) and which might well have 
been ancestral to that of amphibia. There was, however, a joint across 
the top of the skull between the parietal and post-parietal bones, and 
an unossified gap in the base of the skull. A movable joint at this level 
persists in the living coelacanth (p. 272). 



x. 3- 

A most important feature, common to all crossopterygians, was 
that the attachment of the jaws was autostylic, that is to say, similar 
to the arrangement in amphibia and remotely similar to the earliest 
gnathostomes (aphetohyoids) but different from that of modern elas- 

qj. pop. 

Fig. 161. Skull of Osteolepis. 

d. dentary; en. external nostril; esc. extrascapulars; gu. gular;/. jugal; la. lachrymal; 1-gu. 
lateral gular; fngu. median gular; mx. maxilla; op. opercular; pa. parietal; pm. premaxilla; 
po. postorbital; pop. preopercular; ppa. postparietal; prf. prefrontal; qj. quadratojugal; 
sop. subopercular; sq. squamosal; sut. supratemporal; ta. tabular. (After Save-Soderbergh 
and Westoll, Biol. Rev. 1943.) 

mobranchs and actinopterygians. The teeth of osteolepids were simple 
cones, not flattened plates such as are characteristic of Dipnoi, but the 
teeth on the palate show a somewhat broad folded surface and each 
tooth is replaced by another growing up near it, both of these being 
features found in the earliest amphibia. Sections of the teeth show a 
peculiar infolding of the enamel to make a labyrinthine structure, 
which is not found in other fishes but is characteristic of the teeth of 
the first amphibians (p. 327). 

There was only one pair of nostrils on the surface of the head and 
there are gaps, which are considered to be internal nostrils, at the front 


end of the palate, bordered by the premaxillae, maxillae, palatines, and 
prevomers. These fishes may have breathed air; they certainly also 
possessed gills, covered with an operculum. 

Animals of this sort seem to have been abundant in Devonian 
waters and by the end of that period had diverged into several different 
lines. It is interesting that the tendencies shown by these lines arc- 
similar to those that we discovered in the evolution of the Actino- 
pterygii. Some of the later osteolepids became shorter in body, the 
tails tended to become symmetrical (diphycercal) and the scales to 

Fig. 162. Coelacanth, Latimeria chalumnae, female. Length 142 cm. Caught 1954 
near Anjouan. (After Grasse.) 

become thinner and overlapping. *Dip!opterax and *Eiistheiiopteron 
represent separate lines from the late Devonian, both showing these 
characters. Probably the development of these features depends on 
the use of the air-bladder as a hydrostatic organ and the associated 
changes in the method of swimming. 

4. Coelacanths 

The osteolepids became rare in the Carboniferous and disappeared 
after the early Permian, but a line descended directly from them 
remained common through the Mesozoic and still survives today. 
These coelacanths (Fig. 162) show certain very characteristic features, 
which enabled the strange fish brought to the museum at East 
London, South Africa, to be recognized immediately as belonging to 
the group. They are rather deep-bodied animals, with a characteristic 
three-lobed diphycercal tail. The type first appeared in the late 
Devonian and was obviously derived from osteolepid ancestry having 
two dorsal fins, diphycercal tail, lobed fins, and a rhipidistian pattern 
of skull bones, including in most forms a fronto-parietal joint. There 
was a calcified air-bladder. *CoelacantJius and other Carboniferous 

272 LUNG-FISHES x. 4- 

forms lived in fresh water, but *Undina and other Jurassic and Creta- 
ceous types lived in the sea. 

The first living specimen of the group was fished off the east coast 
of South Africa and eleven others have since been caught around the 
Comoro Islands (Madagascar) (Fig. 162). All are referred to the genus 
Latimeria. They have been caught near the bottom at considerable 
depths (150-400 m). Unlike most of their fossil ancestors they are 
large fishes, weighing up to 80 kg; they are dull blue in colour. The 
whole body is covered with heavy cosmoid scales. 

The notochord is a massive unconstricted rod. The skull possesses 
a well-marked joint between a condyle on the hind end of the basi- 
sphenoid and a glenoid cavity on the front of the base of the oto- 
occipital region. This joint, together with fibrous unions between 
other bones allows of movement of the front part of the head on the 
hind. A large pair of muscles runs from the parasphenoid up and 
back to the pro-otic and serves to raise the front part of the head on 
the hind. Coraco-mandibular muscles attached to the palato-quadrate 
have the reverse action and the movement is presumably concerned 
with catching the prey. There are numerous small teeth on the jaws 
and palate. Latimeria lives on other fishes, apparently swallowed whole 
by the powerful oesophagus. There is a well-developed spiral intes- 

The 'air-bladder' arises by a ventral opening from the oesophagus 
and proceeds backwards and dorsally for the whole length of the 
abdominal cavity. The lumen is very small and the organ is 95 per 
cent fat. It may serve to reduce the specific gravity. Respiration is by 
the gills. The heart shows a linear 'embryonic' condition, with the 
sinus venosus and auricle behind the ventricle. There are four rows of 
valves in the conus. The red cells are large, as in elasmobranchs, 
Dipnoi, and Amphibia. Nothing is known of the development, 
except that the eggs are large. 

The brain lies far back in the cranium, of which it occupies less 
than one-hundredth part, the rest being filled with fat. Its structure 
is somewhat like that of a teleostean, with a thin fore-brain roof, and 
large striatum, but without eversion. There is no valvula to the cere- 
bellum. The pituitary cleft is large and the gland remains in continuity 
with the roof of the mouth. 

There are anterior and posterior nares but both open on the surface 
of the head and they have nothing to do with respiration. The rostral 
organ is a large median sac opening to the surface by three pairs of 
canals and richly innervated by the superficial ophthalmic nerve. 


A similar sac occurs in fossil coelacanths back to the Devonian but its 
function is quite unknown. The eye, inner-ear, and lateral line system 
are well developed. 

It is hard to see what features have enabled Latimeria to survive 
with little change since the Jurassic or earlier (see p. 771). It clearly 
cannot be by special development of the brain or receptors. Its 
habitat is isolated, but not especially protected and its population 
seems to be small since even by exceptional efforts so few specimens 
have been found. Perhaps they are more numerous in deeper waters. 
In some of its features it shows developments parallel to those of the 
Teleostei rather than to the Dipnoi, whose remote ancestry it shares. 
Several of its characteristics are paedomorphic. These can hardly be 
alone responsible for such a long survival, but some of them also 
appear in the other survivors from the Paleozoic, Polypterus, stur- 
geons, and Dipnoi. 

5. Fossil Dipnoi 

The Devonian Dipnoi were more like their osteolepid relatives than 
are the surviving modern forms (Fig. 163). The early members of this 
group, such as *Dipterns (Fig. 211), showed the typical elongated 
body, thick cosmoid scales, heterocercal tail, lobed fins, and well- 
ossified skull. The pattern of the bones was obscured by a seasonal 
deposit of cosmine, this being periodically absorbed to allow of growth. 

The individual bones have a certain similarity to those of osteolepids, 
but there are extra bones that are difficult to name. There was no 
premaxilla or maxilla, nor any teeth along the edge of the jaw; instead 
broad, ridged tooth-plates were developed on the palate and inside 
of the lower jaw, presumably as an adaptation for eating molluscs 
and other invertebrates. These crushing-plates are characteristic of 
the Dipnoi and preclude even the earliest of them from being the 
actual ancestors of the amphibia. By the end of the Devonian the 
Dipnoi were showing changes similar to those of the osteolepids and 
palaeoniscids. The body became shorter, the first dorsal fin dis- 
appeared, the tail became diphycercal, and the scales lost their shiny 
surface-layer and became thin. The teeth of *Ceratodus appear in the 
Triassic and were known to geologists long before the related living 
animal was discovered. There has been very little change in this 
animal in more than 150 million years, though the recent members are 
placed in a distinct genus Neoceratodns. 

The evolution of Dipnoi is especially interesting because the rate 
of change has actually been measured (Westoll, 1949). Twenty-six 


&£? ->'■#?£'? 

Fig. 163. The three living lung-fishes and their distribution. 
A, Protopterus; b, Lepidosiren; c, Neoceratodns. (From Norman.) 



^r • 





£ 40 







j 1 

1 1 L 

1 ' 





Age / Millions of years) 

Fig. 164. Rate of evolution in lung-fishes. Each point represents the index of a single 
genus obtained by taking twenty-six characters and rating them with grades of struc- 
ture. The lowest value was given for the most primitive condition, the highest for the 
most modern one. (After Westoll and Simpson.) 

x. 5~6 



different characteristics such as proportion of skull, nature of dermal 
bones or dentition were divided into 3-8 grades. Each fossil genus 
was thus given a score, the minimum being for characters appearing 
in the oldest lung-fish, the hypothetical ancestor being o. Actual 
scores ranged from 4 for the earliest to 100 for two of the living genera. 
Plotting against time we see that there was an early acceleration of 
evolution followed by very slow or zero change in the last 150 million 
years (Fig. 164). It has also 

been shown that a similar 
method applied to the evolu- 
tion of coelacanths gives a 
curve of similar shape (Schaef- 
fer, 1952). 

6. Modern lung-fishes 

The three surviving genera 
of lung-fishes (Fig. 163) are 
mainly inhabitants of rivers 
(though Protopterm lives in 
large lakes) and they all 
breathe air. Neoceratodas lives 
only in the Burnett and Mary 

rivers in Queensland, the pools of which become very low and stagnant 
in summer. Lepidosiren from the rivers of tropical South America, and 
Protopterus from tropical Africa, can survive when the rivers dry up 
completely. They dig into the mud, leaving a small opening for breath- 
ing, and can remain in this state for at least six months. Remains of 
cylindrical burrows found associated with dipnoan bones show that 
this habit of aestivation has been adopted by the group at least since 
Permian times. The three survivors all show similar deviations from 
the conditions found in *Dipterus, but Neoceratodus has diverged less 
than the other two. The tail fin is symmetrical (diphycercal) in all 
three, with no trace of separate dorsal fins. The paired fins are of 
'archipterygial' type in Neoceratodus, with an axis and two rows of 
radials (Fig. 165). The scapula is covered by clavicles, cleithra, and 
post-temporals, the latter articulating with the skull. The scales are 
reduced to bony plates. 

The vertebrae are cartilaginous arches, the notochord remaining 
as an unconstricted rod. In the skull there is also a great reduction of 
ossification, the dorsal bones consisting of a few bony plates, forming 
a pattern not obviously comparable with that of other forms (Fig. 

Fig. 165. Neoceratodus, showing the method of 
walking on the bottom. A, forwards; B, back- 
wards; C, resting. (From Ihle, after Dean.) 



x. 6 

166). The jaw-suspension is autostylic. The food consists of small 
invertebrates and decaying vegetable matter, which is eaten in large 
amounts. In the gut there is no stomach and the intestine is ciliated. 
There are no hepatic caeca, but a well-developed spiral valve is 

PP- qc. Pa 

Fig. 166. Skull of Neoceratodus. Above, Lateral view; below, view of medial surface 

of right half. 
a. angular; bh. basihyal; br. fifth branchial arch; ch. ceratohyal; cr. 'cranial' rib; d. dentary; 
eo. 'exoccipital'; hm. hyomandibula; hn. hyomandibular nerve; hr. hypohyal; Ip. lateral 
plate; ma. median anterior, and mp. median posterior plate; na. neural arch; nac. cartilage 
of neural arch; ns. notochordal sheath; nsp. neural spine; nt. notochord; o. opercular, and 
oc. its cartilage; pa. parasphenoid; />/. post-frontal; pp. pterygopalatine; pt. palatine tooth; 
pto. pterotic (?), and g. its downward process covering the quadrate cartilage, qc; s. sub- 
opercular; so. suborbital; sp. splenial; st. splenial tooth; vt. vomerine tooth. (From 


The external nostrils lie just at the edge of the mouth and the 
internal nostrils open into its roof. The air-bladder is developed into 
a definitely lung-like structure (there is one in Neoceratodus, a pair in 
each of the others), divided into many chambers. Neoceratodus has 
been observed to come to the surface to breathe air and is said to be 
able to survive in foul water that kills other fishes, but it cannot live 
out of the water. Lepidosiren and Protopterus have been shown to 
obtain 98 per cent of their oxygen from the air. The wall of the air- 
bladder of all forms contains muscle-fibres and the cavity is subdivided 
into a number of pouches or alveoli (Fig. 157). In Protopterus and 
Lepidosiren the edges of the slit-like glottis are controlled by muscles 
and there is an epiglottis. The lung is supplied with blood from the 
last branchial arch in Neoceratodus (Fig. 167), but in the other Dipnoi 

x. 6 



there is a more elaborate arrangement. The second and third gill- 
arches bear no lamellae and their afferent and efferent branchial vessels 
are directly continuous, so that blood flows from the ventral to the 
dorsal aorta and carotids. The pulmonary artery springs from the 
dorsal aorta. Blood returns in a special pulmonary vein to the partly 

Fig. 167. Branchial circulation of A Neoceratodus and b Protopterus. 

abr. anterior efferent vessel; ac. anterior carotid, a/ 3 " 6 , four afferent vessels (corresponding 
to the original arches 4-6) ; ah. afferent hyoidean ; c. conus ; cl. coeliac artery ; da. dorsal aorta ; 
dl. dorso-lateral aorta; eb-~*. second and fourth epibranchial arteries; eg. external gills; 
eh. efferent hyoidean; ht. heart; hyp. median hypobranchial; L. air-bladder; la. lingual 
artery; mes. mesenteric artery; pa. pulmonary artery; pc. posterior carotid; pv. pulmonary 
vein; 5. position of closed spiracle; va. ventral artery; vx. vena cava inferior; I-V five 
branchial slits. 

The gills are represented on the hyoid and next four branchial arches. (From Goodrich.) 

separated left side of the sinus venosus. The auricle is partly divided 
into two and the ventricle is almost completely divided by a ridge 
and a series of muscular trabeculae. The ventral aorta is shortened 
into a spirally twisted truncus arteriosus, provided with a system of 
valves such that the blood from the left side of the auricle is directed 
mostly into the first two branchial arches, that from the right side 
into the last two. In this way some separation of pulmonary and 
systemic circulations is achieved. Indeed, although there is every 
reason to believe that the mechanism has been in existence for nearly 
300 million years, it shows us most clearly a possible intermediate 
stage between aquatic and pulmonary respiration. It seems likely that 
the earliest amphibia employed a similar system. There is a coronary 
artery arising from the anterior efferent branchial arches (Fig. 167). 



x, 6 


A further amphibian feature of the blood-vascular system is the 

presence of an inferior vena cava, a 
vessel collecting blood from the kidneys 
and reaching to the heart by passing 
round to the right of the gut in the 
mesentery. The more dorsal cardinal 
veins, joining the ductus Cuvieri, remain 
present, however, and there is a renal 
portal system. 

The adrenals of Dipnoi are represented 
by two separate masses of tissue. The 
perirenal tissue of Protopterus is a con- 
siderable mass of material around the 
kidney, containing lipid, steroid, and 
round-cell (lymphoid) tissues, as well 
as endothelial and pigment cells. The 
steroid tissue shows histochemical pro- 
perties similar to those of mammalian 
adrenal cortex and undergoes changes 
after injection of mammalian ACTH. 
This tissue thus shows a collection of 
functions, haematopoietic, phagocytic, 
storage, endocrine, and pigmentary, 
which may show the starting point of 
the evolution of the tetrapod adrenal 
cortex. Cells that give the chrome 
reaction, the adrenal medullary tissue, lie 
in the walls of the intercostal branches 
of the dorsal aorta. This condition could 
have given rise to that of amphibia. 

The arrangement of the urinogenital 
system is similar to that of amphibia and 
is probably closer to that of the ancestral 
gnathostome than in any living elasmo- 
branch or actinopterygian. In the male 
there are vasa efFerentia by which sperms 
are passed through the excretory portion 
of the mesonephros. In the female eggs 
are shed free into the coelom and carried 
out by a Mullerian duct, whose opening lies far forward. An in- 
teresting feature is that the Mullerian duct is very well developed in 

— 1 

Fig. 168. Dorsal view of the brain 
of Protopterus. 

I, spinal cord; 2, dorsal root of first 
spinal nerve; 3, diverticula of 4, the 
saccus endolyinphaticus; 5, medulla 
oblongata; 6, fourth ventricle; 7, 
cerebellum; 8, mesencephalon (fused 
optic lobes); 9, stalk of pineal body; 
10, thalamencephalon; 11, velum 
transversum; 12, pineal body; 13, 
lobushippocampi; i4,choroidplexus ; 
15, cerebral hemisphere; 16, olfac- 
tory lobe. (After Burckhardt, from 


the male. This is one of several details (lack of ossification, un- 
constricted notochord) which raise the suspicion that the living 
Dipnoi have acquired their special characters by a process of 
paedomorphosis or partial neoteny, that is to say, becoming sexually 
mature in an early stage of morphogenesis. 

The development, again, shows similarity to that of amphibia and 
dissimilarity from the other groups of fishes in that cleavage is total 
and gastrulation takes place to form a yolk plug. There is therefore 
no blastoderm or extra-embryonic yolk sac. However, the cells of the 
vegetative pole contribute little to the shape of the embryo and indeed 
may form a partially separate yolk sac. The larvae show distinct simi- 
larity to those of amphibia, especially the larvae of Lepidosiren and 
Protopterus, in which there is a sucker and external gills. 

The nervous system shows the same affinities as the rest of the 
organization (Fig. 1 68). The forebrain is evaginated into a well-marked 
pair of cerebral hemispheres. The roof of these, though not very 
thick, is nervous and therefore is definitely of the inverted type, not 
everted as in Actinopterygii. The optic lobes are little developed, the 
mesencephalon being hardlv wider than the diencephalon. The cere- 
bellum is small. A peculiar feature is the development of the inner ear 
to form a special lobed saccus endolymphaticus, lying above the 
medulla oblongata. The significance of this is not known, but it is 
interesting that similar backward extensions of the ear are found in 

In many features, then, the Dipnoi differ from modern fishes and 
resemble the amphibia, which evolved from the same stock. The early 
crossopterygians probably competed somewhat precariously with 
other fishes, as do the Dipnoi, and indeed many urodeles, today. It 
was only after tens of millions of years of evolution during the Car- 
boniferous and Permian times that numerous land animals arose, 
in the form of the later amphibian and reptilian types (Fig. 211). 



Man's influence, which has so altered the face of the land, also reaches 
out into the water. During the last half-million years or so fishing has 
grown continually, until at the present time in fresh and shallow sea 
waters man has become the most important source of mortality of fish. 
However, he still leaves vast regions of the sea, as of the land, almost 
untouched. It may be that methods of catching the fish that swim 
above deep waters will eventually produce changes there too, pro- 
viding a substantial extension of the food-supplies of man and 
effecting great alteration in the population of the sea. 

Man has caught fish from his earliest times and he uses many parts 
of their bodies. The skin, especially of elasmobranchs, makes a useful 
leather and also a polishing material. The scales of the bleak (Alburnus) 
yield a substance that when coated on to the inside of glass beads 
makes artificial pearls. The lining of the air-bladder, especially of 
sturgeons, makes isinglass, a shiny powder used for various purposes 
as an adsorbent (i.e. in wine-making). Fish-glue is obtained from the 
connective tissue of the skin and other parts. Fish oils are used as 
food, and are also valuable in the manufacture of soap and other things. 
Besides their direct use as human food, fish products may be fed to 
animals, and the liver makes excellent manure. 

Fish therefore provide the raw material for many human activities, 
but it is, of course, principally for food that they are caught. From a 
fish diet one can obtain not only abundant calorific value, especially 
if the fish be fat, but also various proteins, often the fat-soluble 
vitamins A and D, and usually considerable amounts of combined 
phosphorus and other elements. Herring and mackerel are probably 
the cheapest source of protein available to many people in Britain. 
Fish are undoubtedly good food, and what is perhaps even more 
important they are esteemed as such; most people think that they 
taste good. 

It is not possible to give an accurate estimate of the amount of fish 
caught every year; 20 million tons, of value £200 million, is certainly 
not an overestimate for the catch of the whole world in each of the 
years between the Great Wars. An appreciable fraction of the nutri- 
ment of the human race is derived from fish. The annual catch was 
estimated at 26 million metric tons in 1951 . The greatest national 


catch was by Japan (3-8 million), followed by U.S.S.R. (2-5), U.S.A. 
(2-3), and Great Britain (i-i). 

By far the greater part of all fishing is in the sea. In Great Britain 
the total catch in fresh water annually is reckoned at only 2,000 tons 
and the entire stock at 8,000 tons. However, there are important 
fishing industries in the American Great Lakes, the African lakes, and 
in many parts of the world carp are raised on fish farms, the water 
being manured to yield a good crop of the freshwater plants and 
invertebrates on which the carp feed. The milk fish (Chanos chanos), 
which feeds directly on algae, provides high yields in many tropical 
and subtropical fish-ponds. 

Fishing in the sea is limited mainly by two considerations. First, 
the labour is only really profitable when the fish population is dense. 
Secondly, fish do not keep well unless they are treated in some special 
way and they are therefore best caught near to their market. For these 
reasons the big commercial fisheries are mostly in the relatively shal- 
low waters of the continental shelf (down to 200 fathoms) and in the 
northern hemisphere. However, by packing the fish in ice or cooling 
by other means, the vessels are now able to go longer distances than 
formerly. Japanese and American vessels now fish for tuna and salmon 
in the open ocean. 

For catching purposes fish may be divided into those that swim 
away from the bottom, the pelagic forms, such as herring or mackerel, 
and the bottom-living or demersal fishes, such as the skates and rays, 
flat-fishes and angler-fishes. For the first the gear employed is usually 
drift-net. This is of narrow mesh and is shot and left overnight, drifting 
vertically near the surface, often making a barrier two or three miles 
in length. The fish, such as herrings, swim into them, and become 
enmeshed, and are removed as the nets are hauled in. 

The success of such fishing with drift-nets depends on laying the 
nets in the path of large shoals of fish and it is therefore practised 
especially in regions where fish congregate seasonally. For instance, 
in the North Sea between East Anglia and Holland the herring con- 
gregate in the autumn; at certain times, for unknown reasons, all the 
fish in the area begin to move, making 'the swim', and they are then 
caught in great numbers. Herring are usually caught at slack water. 
At the October full moon, slack water occurs just after dusk and just 
before dawn and catches are higher then. Other drift-net fisheries 
depend on intercepting the fish when rising to feed. Evidently these 
methods demand a close knowledge of the habits and migrations of 
the fish. The fishermen have learned to know when and where to 


expect the larger and nearer aggregations, but there is still much to 
be done in tracing the migration and behaviour of pelagic fishes. 
It is not impossible that other pelagic fisheries could be developed 
that would be at least as advantageous as the herring fishery. Besides 
those eaten fresh, others are preserved as kippers by salting and smok- 
ing, or are heavily salted and smoked to make 'red herrings' for which 
there has been a large export market. 

Lining is a method that can be used for either pelagic or demersal 
fish. For instance, the cod fishery of Newfoundland uses lines with 
several thousand baited hooks. Inshore fishing may be accomplished 
by beach seining, a process of enclosure of the fish from the shore. 
There are also various forms of trap into which the fish swim and 
cannot escape. Danish seining, or purse seining, completely surrounding 
the fish and sometimes then also drawing the bottom of the net 
together, is another effective method. 

The greatest quantities of fish are caught, however, by the various 
forms of trawling. These depend essentially on dragging a bag along 
the bottom of the sea, and the different types adopt various means of 
keeping the bag open. The earlier way of doing this was by means of 
a rigid bar and these beam trawls sometimes used poles over 50 ft 
long. More recently otter-trawling has replaced the beam trawl, the 
otter boards being flat wooden structures attached at each end, so as 
to sheer away when they are dragged through the water, thus opening 
the net. Various devices are used to stir up the fish from the bottom; 
in particular the otter boards are now usually separated from the net 
by long wires and a 'tickler' chain is attached in front of the mouth. 

With such methods very large amounts of fish can be taken from 
the sea bottom. In i860 sailing-ships landed 500 tons of fish at 
Grimsby; by 190 1, 176,000 tons were landed from the steam traw lers 
50,000 tons of plaice alone are taken annually from the North Sea. 
There is evidence that the taking of such amounts of fish from rela- 
tively confined waters has a large influence on the population. For 
instance, it is estimated that 45 per cent of the stock of plaice is 
caught each year in the North Sea. Under these conditions man pro- 
vides the main source of mortality for the fishes. It is less clear 
exactly how such mortality influences the total population of the fish 
in the area. There is reliable evidence that intensive fishing reduces 
the productivity of fishing effort in some cases, but there is also 
evidence that by reducing competition fishing may produce faster 
growth of the fish. The problem is worth some further discussion 
since, besides its economic importance, it gives us an insight into the 


life of the vast populations of the sea and a glimpse of the factors that 
control the numbers of each animal species. 

It used to be held that one of the chief dangers of fishing was that 
it would destroy the breeding-stock, on the grounds that it is axio- 
matic that something is wrong if fish are destroyed before they have 
an opportunity to breed. We may detect something of anthropocentric 
sentimentality here, for reflection shows at once that it is impossible 
for every fish that is hatched to survive and, further, that the total 
annual supply of fish can be provided by relatively few adults. The 
number of fish in the sea, indeed, bears no obvious relation to the 
number of eggs. A cod may shed as many as 8 million eggs (usually 
fewer), which float at the sea surface and hatch into planktonic young. 
Yet herrings, which are much more numerous as adults, lay fewer 
eggs, usually less than 30,000 each. Presumably the risks of life are 
less for the herring, but we cannot see clearly why; the herring's eggs 
are sticky and become attached to gravel or seaweeds, which may give 
them some protection; they are known to be eaten by other fishes, 
perhaps on a smaller scale than planktonic eggs. Both herring and 
cod fry are planktonic and feed on the nauplius and other larval 
stages of Calamis and other copepods. The cod, like other bottom- 
fishes, has to undergo the risks of metamorphosis, but this hardly 
seems sufficient to explain the much greater abundance of herring, 
especially since many fishes feed on the latter, including the cod them- 
selves! As Graham puts it, 'no one really knows why the herring, 
which nearly everything eats, should be able to manage with a less 
rate of reproduction than the cod, which eats nearly everything'. 
The greater part of the mortality of pelagic fish larvae is due to pre- 
dation, including that by members of the same species. This probably 
provides a method of regulation, the number of each species eaten 
being dependent on their frequency. 

This brings us to face the difficult question of the pressure, force, 
or potential that ensures and controls the number of animals. Re- 
production is only a part of the source of this pressure, the other 
element being the feeding and growth of the animals as a result of the 
skill and persistence with which they seek and consume their food. 
It is somewhat easier to study these questions in a marine than in a 
land community, the whole population being enclosed in one vast 
bath, the additions and subtractions to which can be known. 

We must not forget, however, that conditions are far from con- 
stant, even in the 'unchanging sea'. For instance, the extent to which 
fish-fry hatch and successfully overcome the hazards of the early 

(28 4 ) 

3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 



■ ■*■ 

























II - .1 1919 

: 20 



: 60 




60 ^ 
40 £ 

60 <* 
40 ^ 

Z0 3 

-40 ^ 

: 20 



: 20 


Fig. i 

3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 
Age of fish -years 

69. Age composition of Norwegian herring catches 1907-19, showing 
the preponderance of particular year-classes. (After Hjort.) 


stages of life varies most mysteriously from year to year. By study of 
the markings on the scales, bones, and otoliths it is possible to show 
the age composition of a fish population and it is found that the 
hatches of certain years predominate. Thus the herring hatched in 
1904 dominated the population in some parts of the North Sea for 
years afterwards (Fig. 169). Subsequent good herring years occurred 
in 1913 and 1918. Similarly there were good cod years in 1904 and 
191 2. Haddock broods in the North Sea follow a rather regular 

r < 

















Vo 2 



09 s 

1920 1921 1922 1923 1924 1925 1926 1927 1928 1929 1930 1931 1932 1933 1934 

Year class 

Fig. 170. Relative strengths of haddock broods in the North Sea, showing cyclical 
fluctuations. (After Raitt, from Russell, The Overfishing Problem.) 

rhythm with a period of about three years (Fig. 170). These cyclical 
changes in hatching do not appear to produce fluctuations in the total 
population of that species, though we have inadequate data on the 
point. It seems likely that there is a limit set to the total of fish of the 
species, irrespective of age-grouping. 

In addition to such cyclical changes there are also larger ones, such 
as the increase of cod in the far north around Bear Island in recent 
years, apparently due to a northerly extension of warm water, the 
reason for which is not known. Since so many changes are going on 
in the eternal sea is it to be wondered at that the animals in it are 
changing? We might be surprised rather at the slowness of their 

All the fish-life in the sea depends ultimately on the diatoms, 
flagellates, and other green organisms of the plankton, reaching the 
fish usually after passage through one or more animals, especially 
copepods. Bottom-living fishes also depend on plankton, in this case 


after it has died and passed through a bottom-living invertebrate. 
Thus plaice feed on lamellibranchs and worms, soles on worms alone, 
haddock on star-fish, molluscs, and worms. The phytoplankton is, 
of course, built up by photosynthesis from carbon dioxide, water, 
nitrates, phosphates, and small quantities of other substances. The 
limiting factors in the plankton growth, granted adequate temperature 
and sunlight, may be nitrate, ammonia, and phosphate, the latter 
present only to the extent of less than one part in 20 million. During 
the spring and early summer nearly all the phosphate in the water may 
be taken up into the phytoplankton, which increases rapidly. The 
zooplankton (Cala?ius, Sec.) increases somewhat later and by mid- 
summer grazes down the phytoplankton to a considerable extent. It 
is at this midsummer period that the pelagic fishes feed most easily, 
and a little later it is the turn of the bottom-living invertebrates and 
fish, as some of the zooplankton dies and falls to the bottom. At the 
end of the season there may be a second increase in the phytoplankton, 
the recovery being due to breakdown of the discontinuity layer (see 
below), and then with the onset of winter the plants die off and most 
of the phosphate is returned to the inorganic condition. 

Thus to take the case of the cod, whose food chain is one of the 
longest: the activity of the plants turns carbon dioxide, nitrate, and 
phosphate into organic matter: the activity of the copepods makes 
this available to the herrings and the cod eat the herrings. There are, 
of course, many intermediate effects: Sagitta eat some of the cope- 
pods, fish-fry and large cod eat younger cod, and so on, but in general 
we shall not go wrong if we assume that the cycle depends on the 
activity of diatoms, calanoids, herrings, and codfish— all seeking, 
eating, growing, reproducing, and dying. 

The pressure of these various activities produces a complicated set 
of interrelations that may without undue extravagance of fancy be 
called a macro-organism. The activities of all the members contribute 
to the balance that is set up. Sometimes shortage of materials, such as 
phosphorus, at key-points may determine the whole cycle. 

The phosphate in the sea is increased to a small extent by drainage 
from the land and, further, in a restricted area such as the North Sea, 
by the influx of water from more open areas, in that case the Atlantic. 
Not all the phosphate in a given area of sea is available for organic 
growth, because there is usually a separation between upper and lower 
layers owing to the upper layer becoming warmer and less dense. The 
phosphate in the water below this limiting discontinuity layer, usually 
lying 20-100 metres down, is thus not available, though it may be 


made available in certain areas by particular conditions that lead to 
up-currents and mixing of the layers. 

With these facts in mind we can now make further inquiry into the 
effects on the population of the sea of removal by man of large quanti- 
ties of organic matter in the shape of fish. There are enough data to 
give us hints of the changes that follow, and the hope that with further 
study we may eventually understand the Great Sea Beast sufficiently 
well to be able, if we can control ourselves, to regulate its growth to 
our advantage. 

In a few cases it has been possible to follow the course of a fishery 
from its early beginnings, with few vessels and simple apparatus, 
through stages in which the fishing was progressively more intense. 
The statistics are seldom adequate to provide us with wholly satis- 
factory conclusions, but they suggest that (1) as fishing becomes more 
intense, the yield per unit of fishing power declines ; that is to say, the 
industry becomes relatively less profitable; (2) in spite of this, the 
total yield may remain constant, or somewhat increase, even though 
(3) the average size of the fish caught decreases. 

For example, fishing for plaice in the Barents Sea, north of Nor- 
way, was begun in 1905, and the almost 'virgin' population in 1907 
showed great preponderance of large mature fish; whereas in the 
North Sea, which had already been fished for many years, the average 
size was much smaller and few of the plaice were mature. The fish 
taken in the Barents Sea were old and had grown slowly. Transplanta- 
tion of fish of this stock to the North Sea, however, proved that they 
were able to grow as rapidly as the local fish. Some measure of the 
intensity of fishing is given by the number of days' absence of vessels 
fishing in a given area. No doubt the measure is inexact, particularly 
if the methods used are changed, but it provides the best estimate 
available. The landing of plaice taken from the Barents Sea per day's 
absence was 347 cwt in 1906, 50-4 cwt in 1909, and then fell to 46-3, 
33-7, and 20-5 cwt in the following years. The total yield showed some 
decline. The sequence of events is typical of what happens when a 
stock of mature fish is first exploited. 

Graham described a good example of a similar situation in Lake 
Victoria-Nyanza, where he found two stocks of the carp-like fish 
Tilapia, one fished heavily and the other with primitive devices only. 
The less heavily fished stock contained five times as many fish as the 
other and they were much older. Yet by the intensive fishing the 
poorer stock was being made to yield a ten times greater weight than 
the richer stock. This desirable state of affairs for man in general is 


considered unsatisfactory by the fishermen, since the yield per unit of 
effort is much greater when the richer stock is fished. 

The yield of haddock in the North Sea per day's absence averaged 
5 -8 cwt between 1906 and 191 3, rose to 15-8 cvvt in 19 19, averaged 
6-5 cvvt in 1 922-1 929, and 3-7 cwt in 1930-7. The fish are divided into 
large, medium, and small categories, and the percentage of the last 
category was 50 before the war, 70 in 1922-9, and 85 in 1930-7; 
evidently the fish were becoming smaller throughout this period, yet 
the total haddock catch changed only slightly, from 121 million kg 
( 1 910-13) to 138 million kg (1922-9) and 94 million kg (1930-6). 
Fishing seems to have made the population consist of smaller fish, 
giving a smaller yield per unit of fishing effort. This is a true index 
of stock and its decline shows the extent of reduction. 

The figures available for plaice and cod taken from the North Sea 
show much the same tendencies. Over a long period fishermen have 
been afflicted by the consequences of the decline in yield per unit 
effort indicated by such statistics. Already in the last century those 
giving evidence before Royal Commissions expressed an uneasy feel- 
ing that the profitability of the industry was declining. This situation 
has been met by continual improvement in methods of fishing and the 
exploitation of new grounds. The proportion of the total English 
catch that is obtained from the nearer waters of the North Sea is now 
much less than formerly, although the catch is no greater. We have 
already seen that steam trawling and better gear all mean increased 
labour for the crews, at greater distances from port. With all the 
improvements in technique and discovery of new grounds we succeed 
in obtaining from the sea little more fish than at the end of the last 
century; and there is no greater profit for those engaged in the 

The 'Great Law of Fishing', as Graham calls it, 'that fisheries that 
are unlimited become unprofitable' has been tested on at least three 
occasions. During the two Great Wars the intensity of fishing in the 
North Sea was reduced and thereafter both of the expected changes 
were seen : (a) fishing became more profitable, (b) there were found to 
be more old fishes in the stock. Perhaps more encouraging is a case 
where the intensity of fishing has been regulated not by war but by 
law. The halibut fishery of the Pacific coast of North America showed 
the typical history of increasing effort and decreasing yield. Fishermen 
went farther and farther afield in larger and more expensive boats, 
setting ever more and more lines, but yet brought home the same or 
a smaller amount of fish. Thus in 1907 there were 1,800,000 sets of 


lines used, in 1930, 6,400,000 sets, but instead of the 50 million 
pounds of fish caught in the first year there were only 23 million 
pounds in 1930! Then in 1932 a limitation of 23 million pounds was 
imposed on the total catch allowed. Thereafter the stocks rapidly 
increased and it was found possible to collect the standard catch in 
five months instead of nine, with greatly increased profit. 

Other attempts to regulate fisheries have been made; in particular 
by the mesh regulations, designed to avoid taking small fishes. The 
aim of regulation is nowadays not so much to save the stock from 
undue reduction or extinction but rather to crop it in such a way as 
shall make fishing profitable. Whatever we do it is unlikely that we 
shall destroy all the stocks of any species, but there is reason to think 
that the rate at which the stocks grow varies with the intensity of 
fishing. If this is so, it may be possible to find an optimum that suits 
both the fish and the fisherman. 

In order to regulate a fishery effectively it is necessary to express its 
characteristic parameters in a comprehensive equation. This has been 
done by fisheries research workers who have provided mathematical 
models such as are so often used in operational research (Beverton 
and Holt in Graham, 1956). These equations show the effects that are 
likely to follow variation in such a factor as the size of the mesh of the 
cod end of the trawl net, which is one of the means used to regulate 
a fishery. Fishing is a form of hunting, not of agriculture, and if we 
cannot improve the yield by cultivation we may be able to do so by 
working out the best way to fish. 

Four primary factors are considered in the model, recruitment (R), 
growth (W), mortality due to natural causes (M), and mortality due 
to fishing (F). The relation of these factors to the yield by weight of 
the fishery ( Yw) is considered and a theoretical equation for Yw is 
derived. If the theory is correct the equation should be able to de- 
scribe the yield of various fisheries in the past. It proves to do this 
well and forecasts that improvements in yield could be obtained by 
changing methods of fishing in the future. The data for testing the 
theory come from statistics of the fishes caught, which give catches 
per unit effort in each year class and their lengths. These are available 
for several fisheries and we may consider the plaice in the North Sea 
for the years 1929-38. Fish are said to be recruited when they first 
enter the fished area of deeper water at 2-3 years old, being much less 
than 1 per cent of the original batch of eggs. The value R for a given 
mesh size is obtained from the number of fishes in the youngest 
year class in the catch, with corrections to allow for the fact that 




g. 100 

V X 




« 1000 


o> 300 



005 100 1-50 

073 r 



50 100 150 200 250 

Cod-end mesh size (mm) 

Fig. 171A. Mortality rate of plaice. Natural logarithms of average number caught of each 
age-group of North Sea plaice per 100 hours' fishing, 1929-38. The slope of the line gives 
the estimate (F+M) = 0-83. The first three points are lowered by absence of fish from 
the exploited area (some individuals still remaining in the nursery areas) and, possibly, 

by rejection at sea. 

Fig. 171B. Growth in weight of plaice. Average weight of fish of each age-group, 1929-38, 
and the fitted von Bertalanffy equation for growth in weight. 

Fig. 171c. Annual steady yield of plaice plotted against fishing intensity. Yield of plaice 

per recruit (Y W IR) as a function of fishing mortality coefficient (F) with t p ' = 3-72 years, 

corresponding to a 70 mm gauge mesh in trawls, double twine. The vertical line at F = 0-73 

corresponds to the average pre-war fishing intensity. 

Fig. 17 id. Effect of growth rate changing with density. The yield of plaice per recruit 
(Y W IR) is shown as a function of mesh size with fishing intensity constant at F = 073, 
but in calculating curve (b) the growth-rate was assumed to be reduced progressively as 
the density of stock increases. The differences from the use of constant growth-rate, curve 
(a), are considerable. Not only is the benefit from increase of mesh estimated to be less, but 
the maximum yield is reached at a considerably smaller mesh size. 


recruitment is not simultaneous or sudden. For the plaice in the North 
Sea, with 70 mm mesh, R has been computed at 280 million fish for the 
area considered, with mean age of 3 -7 years. A check from consideration 
of numbers and mortality of eggs gave 320 million. Theoretically, we 
also require to know the length of the life of the fish. Few plaice are 
caught older than 15 years and almost none over 20 years. Since 
there are very few in these older age-classes the upper limit is un- 

The coefficients of mortality M and F are estimated from the 
numbers {N t ) of the original recruits R that survive at time t, N ( = 
R e —M (t — t p ), where e is the natural base of logarithms and t p the 
age at entry of the recruits. The total mortality (F-\-M) (due to natural 
causes (M) and to fishing (F)) is estimated from the catches (Fig. 
1 71 a). The part due to fishing alone is found by consideration of how 
the catch varies when there are known differences in the fishing effort, 
for example in the number of hours fished. In the extreme case, we 
have the war-time periods, when there was no fishing. Confirmatory 
evidence of the likelihood that a fish will be caught can be obtained from 
marking experiments, giving the time between release and recapture. 
For the plaice (F-\-M) has been estimated over the years 1929-38 as 
0-83. This is the mean for all the age-classes together, though for 
some purposes it can be calculated for each separately. That the rate 
is indeed constant is shown by the close fit of Fig. 171 a. The first 
three points do not fit because recruitment of these classes was still 
incomplete. This method of treatment, in which the contributions of 
year classes of the same age recruited in different years are considered 
together, has the effect of averaging out this variation in recruitment, 
which would be difficult to estimate. 

The value of the natural mortality of plaice cannot be obtained for 
these years from variations in fishing effort, since these were only 
slight. However, since there was almost no fishing in the southern part 
of the North Sea from 1940 to 1945, we can compare the age groups 
V and VI of samples taken before the war with their surviving fellows 
in the years after 1945. This gives a value for A/of o-i, and subtracting 
this from 0-83 as the total mortality we obtain 073 as the mortality 
due to fishing. Marking experiments give a value of 0-69, which is a 
satisfactory agreement considering that the conditions were not en- 
tirely similar. Moreover, the conclusions from marking involve other 
problems, such as damage to the fish and rate of movement away 
from the point of release. The conclusion that fishing is the most 
important source of mortality in such areas is not new, but is obviously 


of very great importance. If man is the chief predator, then change in 
his activities will greatly influence the populations. 

Knowing the number of fishes available and the rates at which they 
are removed by natural causes and fishing in a given case, we still have 
the even more difficult task of formulating the way in which the popu- 
lation grows and then deciding whether some other method of fishing 
would be more profitable. Probably there is a maximum total biomass 
of fish of any given sort that can be supported in any area, determined 
ultimately by the supply of inorganic salts. In the absence of fishing 
this biomass is carried mainly in the form of large fish, whose presence 
makes the growth of all fish in the population slow. The effect of fish- 
ing is to remove mainly these larger animals, with a resultant increased 
growth from all younger groups. The curve showing the relationship 
between the yield per recruit and the intensity of fishing effort shows 
a maximum (Fig. 171c). It should be possible to define a fishing mor- 
tality rate at which the decrease in numbers is balanced by the incre- 
ments in weight of the survivors. 

There is every reason to hope that with further study of growth, 
mortality, reproductive potential, and utilization of food by fish the 
yield could be increased and the effort of getting it reduced, making 
fishing more profitable to the fisherman and providing the maximum 
amount of food. At present the economic conditions and psychology 
of the fishing populations interact with the factors limiting the stocks 
and the growth of the fish to produce a complicated system of inter- 
relations that is unstable and unsatisfactory to all parties. 

The increase in weight of the population is perhaps the most diffi- 
cult feature of the pattern to express mathematically. Weight plotted 
against age shows an asymmetrical sigmoid shape, with an inflexion 
(Fig. 171B). The curve fitted is arbitrarily chosen, being that deduced 
from the hypothesis of Bertalanffy, that the weight is subject to 
opposing forces of anabolism and catabolism, taken as proportional to 
the absorbing surfaces, that is, to the squares of the linear dimensions. 
As before, the fit is poor for the lower points, probably because there 
are incompletely recruited classes. Elsewhere the fit is good but the 
important point for us is the inflexion, since it indicates that the 
growth-rate decreases in the later part of life. The older plaice are 
from this point of view inefficient in providing more biomass. Fur- 
ther, the longer a fish has to be kept alive in the sea before it is eaten, 
the more of the limited raw materials are devoted to this end and the 
less to providing human food. With present methods it is not possible 
to give full weight to all of these factors in deciding what is the best 


way to fish. However, the theoretical equation derived by Beverton 
and Holt gives us the yield Y w in terms of the parameters already 
discussed with in addition the maximum weight W^ and a factor K 
related to the catabolism 

d ^ = FN l W. (1) 

The number N t at the time t is given by 

N t = R^F+MXt-t,^ ( 2 ) 

and the weight W t by 

W t = W^i-e-w- 1 *?). (3) 

This last is best handled as a cubic of the form 

W t = W^2 Q -n e ' UK(l - tti) - 
n = 

Substituting (2) for N t in (1), and (3) for W t we obtain 

at ri=o 

This provides the basic equation with which forecasts of effects of 
changing the various factors are made. 

Empirical values can be obtained for the yield per recruit (Y W I R ) 
for various values of F, with a mesh of 70 mm. Such a yield/intensity 
curve of North Sea plaice is shown in Fig. 171c. The graph shows that 
with infinite effort all fish would be caught at recruitment and would 
yield their initial weight of 123 g. At the pre-war fishing mortality of 
0-73 the yield was 200 g. But the curve has a clear maximum at over 
250 g, with a fishing mortality of only 0-22. Therefore if these pre- 
dictions are correct, a lesser intensity of fishing should provide a 
greater yield. 

One possible way of reducing fishing intensity is to increase the 
size of the mesh of the cod net. If the age at recruitment were in- 
creased to ten years the yield per recruit would be as high as 400 g 
(Fig. 17 id, curve a). Beyond this maximum, the yield falls because of 
the death of fish by natural causes before entering the exploited phase. 
However, this curve assumes that the growth-rate is independent 
of density and it ignores the complex problem of the competition of 
old and young fishes for a limited supply of raw materials. Curve b 
of Fig. 17 id has assumed a reduced growth-rate with increasing 
density and it will be seen that the advantage of increasing mesh size 
is much reduced. 




^ 300 


100 • 




>T* 200- 


\ c 

\ J£- 

, ' 

/\ / 
I \ ' 

If ! -\X b) 

/ A X(cK 


Running costs 


FlG. 172A. Annual steady yield of plaice plotted against mesh at various fishing intensities. 

The yield per recruit ( Y W \R) as a function of t p ' for various values of F, to show how the 

height and location of the maximum changes with F. 

Fig. 172B. Eumetric Yield curve for plaice. If a change of mesh accompanies a change in 
fishing intensity in such a way that each value of F is matched by the mesh that would 
give the maximum steady yield at that value, the resultant curve of steady annual yield 
per recruit (Y w jR) for plaice differs widely from that of Fig. 171c, particularly in having 

no maximum. 

Fig. 172c. An exercise in bionomics. Curve (a) is a eumetric curve in which steady yield 
instead of being expressed in weight is now in money value, which is plotted against the 
economic equivalent of intensity of fishing, namely, running costs. From those are derived 
(6) the annual profit and (c) the profit expressed as a rate on running costs, which in many 
situations bear a constant relation to capital outlay. 

MP = maximum profit point; ZP = zero profit point. 


In practice it is much more economical to reduce the fishing mor- 
tality by lowering the number of hours fished than by increasing the 
mesh size. We require, therefore, to know the optimum mesh size for 
each level of fishing effort. This we can obtain by plotting, as in Fig. 
1 72 a, a series of yield/mesh curves for different sizes of mesh, that 
is, ages of recruitment t p . From the maximum of these, plotted against 
the corresponding fishing mortality, we obtain Fig. 172B, known as 
the eumetric yield curve. This shows an increasing yield towards an 
asymptote as fishing increases, but without a maximum. 

Evidently the greatest yield is obtained at the highest fishing inten- 
sity, but this could be achieved only at a prohibitive cost. In order to 
obtain the greatest possible yield, we have to consider the cost of unit 
effort of fishing and the value of the yield. This has been done, making 
certain assumptions, in Fig. 172c. Here the eumetric yield curve is 
expressed by plotting value of catch against running costs. Another 
line shows the profit (total value minus total cost) whose maximum 
might be said in one sense to be the 'best' level of fishing. This curve 
also crosses the x-axis, where there is no profit in fishing — -this being 
the condition which an uncontrolled fishery tends to approach. 

Of course the actual 'best' level of fishing for any given situation 
may be affected by many social and political factors. However, from 
studies such as these it begins to be possible to understand the vari- 
ables that are affecting a fishery and to express them precisely. The 
value of such work is shown by the fact that international regulation 
of some fisheries has been agreed. For example, since 1954 the white- 
fish populations of the North Sea have been regulated by control of 
the size of mesh used for fishing. 



1 . Classification 

Class Amphibia 

*Subclass i. *Stegocephalia. Devonian-Trias 
Order i. *Labyrinthodontia. Devonian-Trias 
Suborder i. *Ichthyostegalia. Upper Devonian 

*Ichthyostega; *Elpistostege 
Suborder 2. *Embolomeri. Carboniferous 

*Eogyrimis; *Loxomma 
Suborder 3. *Rhachitomi. Carboniferous-Triassic 

*Eryops, Lower Permian ; *Cacops, Lower Permian 
Suborder 4. # Stereospondyli. Triassic 

*Capitosaurus, Upper Triassic; *Buettneria, Upper Triassic 
Order 2. *Phyllospondyli. Carboniferous-Lower Permian 

*Bra?ichiosaurus, Lower Permian 
Order 3. *Lepospondyli. Carboniferous-Permian 

*Dohchosoma, Carboniferous ; *DipIocaulus, Permian ; *Micro- 
brachis, Permian 
Order 4. *Adelospondyli. Carboniferous-Lower Permian 
*Lysorophns, Carboniferous 
Subclass 2. Urodcla (= Caudata). Jurassic-Recent 

Molge; Salamandra; Ambystoma; Necturus 
Subclass 3. Anura (= Salientia). Carboniferous-Recent 
*Miobatrachus; *Protobatrachiis ; 
Rana; Bufo; Hyla; Pipa 
Subclass 4. Apoda (= Gymnophiona = Caecilia). Recent 
Ichthyophis; Typhlonectes 

2. Amphibia 

During the later part of the Devonian period a population of lung- 
fishes lived in the pools and there is every reason to suppose that some 
of these animals, first crawling from pool to pool and then spending 
more time on the land, gave rise to the terrestrial populations that 
we distinguish as amphibia. No doubt the early efforts at land life 
were crude. The whole locomotory and skeletal system comes under 
a completely new set of forces when the support of the water is with- 

xii. 1-2 AMPHIBIA 297 

drawn and the effects of gravity become insistent. At the same time 
the skin must be changed to resist desiccation, the respiratory system 
adapted to use gaseous oxygen, the receptors to signal the strange new 
configurations of stimuli. It is not surprising that these new conditions 
produced greater changes in vertebrate organization than had occurred 
in tens of millions of years previously. Nevertheless, so slow is the 
pace of evolution, the only known Devonian amphibia, and many of 
the Carboniferous ones too, still looked and presumably behaved very 
like fishes. Animals of this sort (e.g. *Eogyrinus) floundered about on 
land for 30 million years or more before producing definitely terrestrial 
types such as the Permian *Eryops. 

Of all the features that arose at this time in connexion with the new 
life on land the presence of pentadactyl limbs is perhaps the most 
conspicuous. It is appropriate that this should be marked in zoological 
nomenclature: the amphibia are the first of the great group of land 
vertebrates, the Tetrapoda. 

All existing amphibia have been much modified since their Devonian 
ancestry, yet they retain many features that show how the transition 
from water to land was produced. These modern forms are by 
no means a precariously existing remnant but are quite numerous 
and successful in the ecological niches that they occupy; they form 
an important element in many food chains. There are some 2,000 
species at present recognized, placed in 250 genera. However, con- 
trasting this with the numerous species of teleosts, of birds, and of 
mammals we shall see that the amphibians, though well adapted for 
certain situations, do not succeed in maintaining themselves in many 
different types of habitat. Broadly speaking they are unable to survive 
for long except in the proximity of water. There are desert toads, such 
as Chiroleptes of Australia, but these survive by burrowing and by 
special abilities, such as the power to hold large amounts of water, 
associated with loss of the glomeruli of the kidneys. 

Modern amphibia belong to three sharply separated subclasses. 
Urodela (newts and salamanders) retain the original long-bodied, 
partly fish-like form. The Anura (frogs and toads) have lost the tail 
and become specialized as jumpers. The Apoda are limbless, blind, 
burrowing animals found in the tropics. The urodeles and anurans 
are found as fossils back to the Cretaceous and Trias respectively, but 
we have only scanty information about their connexion with the 
earlier amphibians, which are grouped loosely together as the Steno- 
cephalia. These are found in rocks about 275-160 million years old, 
that is to say from the late Devonian to the Trias (Fig. 211). 

298 AMPHIBIA xii. 3- 

3. The frogs 

Perhaps the most successful of all amphibia are those belonging 
to the genus Rana, abundant in every part of the world except in 
the south of South America, on oceanic islands, and New Zealand. 
Ranid frogs are typical of the highly specialized subclass Anura, whose 
members usually inhabit damp places such as marshes or ditches, 
living for most of their life in the grass or undergrowth and feeding by 
catching flies and other insects with their tongue. They are preyed 
upon by birds, fishes, and especially snakes, and escape from these by 
their hind legs, used either for jumping or swimming. The young 
develop as tadpoles in the water, where they are omnivorous. The 
various species differ in size and small points of colour, though there 
are also some that depart widely from the usual habits, e.g. R. fossor 
which burrows. R. temporaria is the species found in Great Britain, 
R. esculenta is a slightly larger form found on the continent of Europe 
and occasionally in east England, R. pipiens is the common small 
North American frog; R. catesbiana the giant bull-frog, whose body 
is up to 9 in. long, also lives in North America. R. goliath of the 
Cameroons is over a foot long, but is mainly aquatic. 

4. Skin of Amphibia 

The earliest amphibia possessed the scales of their fish ancestors, 
but these were soon lost in most lines, though retained in some 
Apoda; perhaps they were too heavy to be worth while for creatures 
contending for the first time with gravity, unaided by water. Some 
frogs carry dermal plates on the back, however, fused to the neural 
spines (Brachycephahis of Brazil). Amphibia differ from reptiles in 
that the skin is moist and used for respiration; on the other hand, the 
skin also shows a character typical of land animals in having heavily 
cornified outer layers. The epidermis therefore consists of several 
layers in the adult frog and is renewed at intervals by a process of 
moulting. The moult is under the control of the pituitary and thyroid 
glands and does not occur if either of these be removed, the kera- 
tinized cells merely accumulating in those circumstances as a thick 
skin. Local thickenings of the epidermis often occur in amphibia, for 
instance to form the horny teeth by which the larva feeds. Such thick- 
enings are also a conspicuous feature of the warty skin of the toads 
(Bufo), which mostly have a drier skin and are more fully terrestrial 
than are the frogs. The fact that the epidermis of amphibia can pro- 
duce local thickenings is of interest in considering the origin of 
feathers and hairs. In larval amphibians the skin is ciliated. 

xii. 5 SKIN OF AMPHIBIA 299 

The glands of the skin are more highly developed than in fishes, 
and are of two types, mucous and poison glands. Both of these consist 
of little sacs of gland-cells, derived from the epidermis. The mucus 
serves to keep the skin moist, this being essential if the skin is to 
respire; the secretion may perhaps also serve for temperature regula- 
tion. The problem of regulation of temperature is important for all 
terrestial animals, since air conducts heat much less well than water 
and therefore violent changes of temperature are met. Evaporation 
produces large influences on temperature and no doubt it was the 
adjustment of these effects that led to the development of temperature- 
regulating mechanisms in birds and mammals. Frogs in dry air are 
always found to be colder than their environment, the difference 
being sometimes as much as 5 C. It is probable that in some cir- 
cumstances use is made of this cooling, since tree-frogs (Hyla) may 
be found fully exposed to tropical sunlight, which would be expected 
to raise their temperatures to a lethal level. On the other hand, the 
loss of water involved by evaporation in this way would presumably 
soon become serious. 

The poison glands or granular glands are less developed in Rana 
than in Bufo ('the envenom'd toad') where they are collected into 
masses, the parotoid glands. The effect of the poison on man is to 
produce an irritation of the eyes and nose; only rarely does it affect 
the skin of the hands. When swallowed it produces nausea and has 
a digitalis-like action on the heart. The poison of Dendrobates of 
Colombia is used on arrows; it acts on the nervous system. 

Some amphibia have characteristic smells, produced by secretions, 
and these are probably used to attract the sexes to each other. In 
some male newts (Plethodontidae) there are special collections of these 
gland-cells below the chin. 

Another use of glandular secretions is to keep the eyes and nostrils 
free from obstruction. The demands of terrestrial life require the 
production of numerous such special devices and lead to the com- 
plexity that we recognize as an attribute of these 'higher' animals. 

5. Colours of Amphibia 

The use of colour is also highly developed in amphibia. The 
animals are often greenish and the colour is produced by three layers 
of pigment cells, melanophores lying deepest, guanophores, full of 
granules, which by diffraction produce a blue-green colour, and yellow 
lipophores, overlying these and filtering out the blue. Change of colour 
is produced by expansion of the pigment in the melanophores under 



xii. 5 

the action of the secretion of the pituitary gland (Fig. 173). Move- 
ments in the other chromatophores can also affect the colour, yellow 
being produced by disarrangement of the guanophores and so on. 
Other colours may contribute to the patterns, blue (though rarely) 
by the absence of the lipophores, red by pigment in the lipophores. 
Changes in the melanophores may be of two sorts, primary or 
direct and secondary or visual. The primary response depends on the 

Fig. 173. Stages of dispersal of pigment in the melanophores in the web of 

the frog Xenopus, as used by Hogben to assess the melanophore index. 

(After Hogben and Slome, Proc. Roy. Soc. B. 108.) 

direct effect of light on the skin, causing expansion. The secondary 
effect consists in contraction of the pigment if the animal is illumin- 
ated on a light-scattering surface (light background) but expansion 
(and hence darkening of the animal) when it is illuminated from above 
on a light-absorbing (dark) background. There are, therefore, distinct 
responses from different parts of the retina. Illumination of the dorsal 
part produces contraction, of the ventral part expansion of the 

Hogben and his co-workers have shown that the control of the 
colour change of amphibians is mediated by variation in the secretion 
of the pituitary gland ; there is no direct nervous control of the melano- 
phores. There is still some doubt whether the pituitary produces its 
effects by means of one hormone or two. The most fully known in- 
fluence is that of the posterior lobe, producing a B substance, also 
known as intermedin, which makes the melanophores expand. Ex- 

xii. 5 



tracts of the pituitary of mammals (or other vertebrates) produce this 
effect when injected into frogs, and after removal of the pituitary a 
frog becomes pale in colour. There is also some evidence for secre- 
tion bv the anterior lobe of a W substance that causes paling. After 
removal of the whole pituitary the melanophores are found to be not 
in the wholly contracted stage 1 of Hogben's melanophore index (Fig. 
173) but in a state (stage 2 or 3) intermediate between this and full 
expansion (stage 5). If, however, the posterior lobe alone is removed 
the animal becomes completely pale (stage 1). This certainly suggests 

10 12 14 

Fig. 174. Effect of an extract containing the b (melanophore-expanding) substance on 

three groups of Xenopus. All were of the same weight and received the same dose. 

A, whole pituitary removed; D, intact animals; c, posterior lobe only removed. 

(From Waring, after Hogben and Slome.) 

the secretion of a W substance by the pars anterior. There are also 
differences in the response to injection of B-containing extracts after 
total and partial removal of the pituitary (Fig. 174). The position is 
complicated by the fact that extracts of mammalian pineal or adrenal 
medulla will cause contraction of amphibian melanophores, though it 
is uncertain whether these effects have any physiological significance. 

In amphibia there is no direct control of the pigment cells by 
nerve-fibres such as are present in bony fishes (p. 259). The colour 
change is therefore rather slow. After removal of the pituitary the 
melanophores still show slight changes correlated with change of in- 
cident illumination, indicating a small degree of direct response as 
independent effectors. Temperature and humidity also influence the 
colour in many amphibia. In frogs contact with water accentuates the 
black-background response and in darkness produces expansion. On 
the other hand, drying induces contraction of the melanophores, even 
upon a black background. 

The colour patterns adopted are usually cryptic or concealing in 
their effect, but the colour also has an important influence on the 
temperature and varies with it and with the humidity, as well as with 
the incident illumination. The uniform brilliant green of tree-frogs 

3 o2 AMPHIBIA xii. 5- 

makes them very difficult to see among the leaves; on the other hand, 
R. temporaria and other species living among grass show a pattern of 
dark marks, which breaks up their outline. In other amphibians, how- 
ever, the colour makes the animal 
conspicuous, for instance the 
black and yellow markings of 
Salamandra maculosa. Conspi- 
cuous colour is often associated 
with great development of the 
poisonous parotoid glands and 
is therefore presumably sematic 
or warning coloration, allowing 
recognition by possible attackers. 
This correlation is not always 
found, however; the toad Cera- 
but poisonous, whereas C. dor- 
sata has a bright pattern but is 

Many frogs make a sudden 
exposure of brightly coloured 
patches on the thighs when they 
jump. This presumably serves 
to startle the attacker and such 
colours may be called dymantic 
or startling. A similar use of 
colour is made by the cuttle- 
fish (Sepia), which may suddenly 
produce two black spots when 
alarmed, and also by some Lepi- 
doptera. It is interesting that the 
colour used in this way so often 
takes the form of black spots 
('eye-spots'), which have an es- 
pecially striking quality. In some anurans these colours are irregular 
dark marks, but in Mantipus ocellatus they take the form of definite 

It must not be forgotten that the presence of pigment serves to 
protect the organs from the effects of light, which may cause contrac- 
tion when it falls directly upon muscles. Dark colour may also assist 
in the absorption of heat, both in the adults and in the eggs. 

(a) (b) 

Fig. 175. Record of the movements of 
Ambystoma walking on a smoked drum, 
a, in rapid locomotion (with the body on 
the ground); b, in slow locomotion (raised 
up on the legs). (From Evans, Anat. Rec. 

xn. 6 


6. Vertebral column of Amphibia 

The general build of the body is essentially fish-like in stegocepha- 
lian and urodele amphibians. Such forms have two means of locomo- 
tion. When they are frightened and move fast they wriggle along with 
the belly on the ground, the effective agent being serial contraction 
of the segmentally arranged myotomal musculature, by means of which 
the animal as it were 'swims on land', with the legs hardly touching 
the ground (Fig. 175). When moving deliberately, on the other hand, 

Fig. 176. Drawings made from photographs of a newt (Triturus) 
in slow locomotion. (After Evans, Anat. Rec. 95.) 

a newt raises up its body on the legs, which then propel it along as 
movable levers, the main part of the action being produced by drawing 
back the humerus or femur, the more distal muscles of the limbs 
serving to maintain the digits pressed against the ground (Fig. 176). 
The carrying of the weight on four legs places an entirely new set 
of stresses on the vertebral column. Instead of being mainly a com- 
pression member as it is in fishes it comes to act as a girder, carrying 
the weight of the body and transmitting it to the legs. This new 
function produces a column whose parts are largely bony and articu- 
lated together, flexibility becoming less important than strength. The 
new types of strain involve new muscle attachments and the develop- 
ment of special processes and parts of the vertebrae (p. 307). These 
changes, however, have not proceeded very far in the amphibians; 
many urodeles spend much time in the water and their vertebrae often 
show a lack of ossification, parts of the notochord persist and provide 
the main compression member required for swimming. 



xii. 6 

In the anurans the entire skeletal and muscular system has become 
specialized for the peculiar swimming and jumping methods of loco- 
motion, by means of extensor thrusts of both hind limbs, acting 

Fig. 177. Reflexes associated with the transition from swimming to walking in toads. 
The shaded outlines show successive positions as the animal emerges on to solid ground. 
The first effective contact is by the left fore-limb whose retraction and extension 
elicits a crossed protraction reflex in the right fore-limb (Lj), a diagonal extensor 
response in the right hind-limb (L 2 ), and a placing response in the left hind-limb (L 3 ). 
The right fore-limb then touches the ground and produces corresponding responses 
Rx- 3 . The left fore-limb in response to stretch of its protractor muscles swings forward 
and this produces retraction of the left hind-limb (L 4 ) and protraction of the right 
hind-limb (L 5 ). Fixation of the right hind foot then produces a crossed flexor response 
(RHJ. (From Gray, J. exp. Biol. 23.) 

together. Frogs, and especially toads, also walk on land, bringing into 
play a set of myotactic (proprioceptor) reflexes that depend on the 
contraction of the muscles against an external resistance (Fig. 177). 

The actions of jumping and walking are possible because of pro- 
found changes in the arrangement of the skeleton and muscles. The 
myotomal muscles no longer perform their primitive function of pro- 
ducing metachronal waves of contraction, and accordingly the verte- 
bral column (Fig. 178) has lost its original flexibility. Instead, it is 

xii. 6 



Fig. 178. The skeleton of the frog, seen from the dorsal surface; the left 
suprascapular and scapular have been removed. 

a. astragalus; c. calcaneum; d. suprascapular; e. exoccipital ; /. femur;//), frontoparietal; 
g. metacarpals; h. humerus; i. ilium; k. metatarsals; /. carpus; m. maxilla; w. nasal; o. pro- 
otic; p. pterygoid; pm. premaxilla; q. 'quadratojugal'; r. radio-ulna; J. squamosal; se. 
sphenethmoid; s.v. sacral vertebra; t. tibio-fibula; u. urostyle. 
(After Marshall, The Frog, Macmillan.) 

attached to the pelvic girdle and acts as a support by which the 
movement of the hind limbs is transmitted to the rest of the body. 
There is no longer any sinuous motion and the number of vertebrae 
is very low (nine in the adult Ra?ia), and behind them is an unseg- 
mented rod of 'hypochordal' bone, the urostyle. Shortening of the 
body is a characteristic feature of the change from aquatic to terrestrial 


Fig. 179. Transformation of crossopterygian pectoral girdle and fin into 
pentadactyle limb. Oblique front view of left side. 

a, *Eusthenopteron\ b, *Eogyrinus; c, *Eryops; clt. cleithrum; civ. clavicle; 

h. humerus; p. pubis; sc. scapula; supracleichrum. (Modified from 

Gregory and Raven, Ann. N.Y. Acad. Sci. 42.) 

Fig. 180. Transformation of crossopterygian pelvic fin into tetrapod limb. 

a, *Eusthenopteron; B, hypothetical; c, *Trematops. f. femur; fi. fibula; il. ilium; 
is. ischium; t. tibia. (Modified from Gregory and Raven.) 

xii. 6-7 AMPHIBIAN LIMBS 307 

life, and is seen in many lines of amphibian and reptilian evolution. 
It has proceeded farther in the frogs than in any other tetrapods. 

The second to eighth vertebrae of Rana are concave in front, con- 
vex behind (procoelous), and have large transverse processes. In other 
amphibians they may be amphicoelous or opisthocoelous. They fit 
together by complex zygapophyses. The first vertebra has two con- 
cave facets for articulation with the two condyles of the skull; its 
centrum and transverse processes are much reduced. The ninth 

Fig. 181. Diagrams illustrating the probable changes in position during the 
evolution of a pelvic fin into a tetrapod limb. A as in Ceratodus; B, double 
flexure to give knee and ankle joints, leaving foot direct backwards; c and 
D, rotation of tarsus and digits turning foot forward. (From Gregory and 
Raven, after Romer and Byrne.) 

(sacral) vertebra has large transverse processes, which articulate with 
the ilia of the pelvic girdle. There are free ribs in the primitive frogs 
Ascaphus and Leiopelma. 

7. Evolution and plan of the limbs of Amphibia 

The girdles of the paired limbs have become much changed from 
their fish-like condition (Figs. 179 and 180). Their basic pattern is 
similar in the two limbs and has been retained throughout the w r hole 
tetrapod series. Whereas in fishes the girdles are rather small carti- 
lages and bones, the pelvic girdle being restricted to the ventral region 
of the body, in amphibians they become enlarged in connexion with 
the w T eight-bearing function of the limbs. 

The details of the sequence of stages by which a tetrapod limb 
arose from a fish fin are still somewhat disputed. It is probable that 
the ancestral crossopterygian possessed a lobed fin, rather like that 
seen in *Eusthenopteron (Fig. 179). As the fishes came on land the fin 

3 o8 AMPHIBIA xn. 7- 

would be used as a lever, giving greater effect to the wave-like motions 
by which the creature 'swam on land'. The muscles of the limb, con- 
tracting in a serial manner, would tend to move it backwards and 
forwards relative to the body, thus assisting in locomotion. At first 
the limb perhaps carried only little weight, but as tetrapod evolution 
proceeded the limbs became elongated and turned under the body, 
raising it off the ground. To work effectively in this way the limbs 
came to be held bent down at elbow and knee (Fig. 181) and a firm 
application to the ground was produced by bending outwards at 
wrist and ankle. Finally the limbs were brought in to the side of the 

Fig. 182. Suggested protetrapod stage, between crossopterygian and labyrinthodont. 
(From Oregon - and Raven.) 

body by rotation, such that the elbow pointed backward and the knee 

These are the changes that must have occurred at some time to 
produce the full tetrapod condition, but we cannot follow exactly the 
order in which they took place. Their effect is to convert a paddle- 
like fin, whose main movements were up and down, and were used 
for stabilization in the horizontal swimming plane, into an elongated 
jointed strut, on which the animal can balance, and which can be 
moved as a lever to produce locomotion. 

The limbs and girdles and their muscles show a remarkable con- 
stancy of pattern throughout the tetrapods. The muscles of the fins of 
fishes are concerned mainly with lowering and raising (Fig. 192), and 
they run from a girdle in the body wall to the basal radials in the fin, 
and between the radials. After the animals came on land the muscles 
served not only to raise and lower the limbs but also to draw them 
forwards and backwards; indeed, many fishes already make such 
movements, including Protopterns. The muscles therefore become 
arranged around the shoulder and hip joints into groups serving as 
adjustable braces, by which the body is balanced on its legs and by 
whose contraction the latter are moved. Those muscles that draw 
the limb towards and away from the mid-ventral line can be called 


medial and lateral braces (adductors and abductors) and the muscles 
drawing the leg backwards and forwards are posterior and anterior 
(retractor and protractor) braces. For the attachment of these muscles 
proximally the pectoral and pelvic girdles, small in fishes, become 
expanded into plates (Figs. 180 to 182), and these are divided into 
a number of characteristic pieces, though the mechanical reason for 
the division is not clear. 

8. Shoulder girdle of Amphibia 

The earliest labyrinthodonts (e.g. *Eogyrinus) inherited a shoulder 
girdle almost exactly like that of their osteolepid ancestors except that 
a new dermal element, the interclavicle, was added to the ventral 
surface. Although the presence of a sternum has never actually been 
recorded, it is generally assumed that a cartilaginous structure of this 
type was present between the hindermost margins of the epicoracoid 
cartilages. As in gnathostomes generally (except elasmobranchs) the 
shoulder girdle was a dual structure consisting of (a) a primary or 
endochondral component evolved from the basal fin elements of the 
ancestral fish form and serving to provide an articulatory surface for 
the limb as well as points of attachment for the limb musculature, and 
(b) a dermal ring of bony elements (skin scales) which had sunk 
inwards and applied themselves to the ventro-anterior surfaces of the 
endochondral girdle which, consequently, they braced and supported. 

The endochondral girdle consisted of two half rings, which over- 
lapped in the ventral midline. Each half was a single unit but, by 
topographical comparison with girdles of later tetrapods, it is often 
arbitrarily divided into two regions, a dorsal scapula and a ventral 
coracoid. Between these two regions a screw-shaped glenoid received 
the humerus. The one endochondral ossification is usually homo- 
logized with the scapula of amniotes (Watson, 191 7). Later forms 
(e.g. * Seymonria, *Diadectes) possessed a second bony element which 
is generally interpreted as a precoracoid. The endochondral girdle was 
small in the earliest amphibia (e.g. *Eogyrinus). In later genera its size 
progressively increased, presumably to withstand the greater thrust 
transmitted by the larger limbs of these forms and to provide attach- 
ment for the increased mass of brachial musculature. 

The dermal girdle consisted, typically, of paired cleithra, clavicles, 
and interclavicle. The latter, a new element, lay between and often 
beneath the clavicles and, together with the sternum, probably formed 
a locking mechanism preventing the complete separation of the epi- 
coracoid cartilages. In the earliest rhachitomes (e.g. *Eogyrinus) the 

310 AMPHIBIA xii. 8 

dermal girdle was attached to the post-temporal region of the skull, 
as in bony fish. This connexion was soon lost in later forms, pre- 
sumably to permit greater mobility of the head. This foreshadowed 
the reduction and loss that was the subsequent fate of the dermal, 
shoulder girdle elements in tetrapod evolution. 

Of the modern amphibia, the Salientia most nearly approach the 
condition of the fossil forms and they, alone, of recent tetrapods, have 
retained a cleithrum. Each half of the endochondral girdle consists 
of a dorsal, bony scapula with a cartilaginous suprascapula, and a 
ventral coracoid bone connected to an anterior precoracoid cartilage 
by a mesial epicoracoid cartilage. The precoracoids are invested by 
the clavicles and, as in all modern amphibians, the interclavicle is 

Anuran shoulder girdles may be divided into two broad categories 
according to whether the two epicoracoid cartilages are fused mesi- 
ally (a) along their entire lengths (firmisternal condition) or (b) along 
their anterior edges only (arciferal girdles). The latter occurs typically 
in 'walking', toad-like Anura (e.g. Bufonidae, Pelobatidae) and in the 
aquatic xenopids. The clavicles are the main struts for keeping the 
glenoids apart and, consequently, they are well developed and never 
lost. The coracoids, on the other hand, may only be moderately well 
developed. Immediately behind their point of fusion the epicoracoid 
cartilages diverge and overlap and their posterior margins are con- 
tinued as epicoracoid horns, which run in lateral grooves on each side 
of the sternum. The posterior tip of each horn has a muscle attach- 
ment connecting with abdominal recti. This type of sternum/epi- 
coracoid system permits a certain degree of independent movement of 
the girdle halves whilst, at the same time, preventing the epicoracoid 
cartilages from being forced too far apart. The mechanism clearly 
facilitates the independent arm movements characteristic of locomo- 
tion in the arciferal frogs. 

The firmisternal girdle is a rigid structure allowing no independent 
movement of the two halves (Fig. 183). It occurs typically in frogs 
with a jumping habit (e.g. Ranidae, Microhylidae) and provides an 
excellent landing mechanism. The glenoids are braced apart by the 
large coracoids. The clavicles and precoracoids are thus deprived of 
their strutting function and frequently become reduced or even com- 
pletely lost. No epicoracoid horns are present and the sternum, no 
longer involved in locking the girdle halves, serves principally for the 
attachment of pectoral muscles. This function is also performed, in 
some frogs, by a prezonal (omosternal) element, which is really an 




Fig. 183. Amphibian pectoral girdles. 

b. precoracoid bridge; c. coracoid; cl. clavicle; c.p. coracoid process; c.t. cleithrum; d.b. 
dorsal blade; e.l. precoracoid cartilage; e.m. epicoracoid muscle; g. glenoid; g.f. glenoid 
fossa; /;. epicoracoid horn; interclavicle; /. left epicoracoid cartilage; pc. prezonal 
cartilage; p.o. prezonal bone; po.t. posterior temporal; r. epicoracoid cartilage; s. sternum; 
sc. scapula; sk. scapulo-coracoid ; s.o. sternal bone; s.r. ventral blade; ss. suprascapular 
cartilage; st.c. sternal cartilage; su. coraco-cleithral suture; sup.ct. supra-cleithrum. 



xn. 8- 

extension of the precoracoid cartilages. This structure, although 
present in some arciferal girdles (e.g. Leptodactylidae), is more usually 
associated with the firmisternal pattern and a jumping habit. 

The shoulder girdles of modern urodeles are greatly simplified, the 
only ossification being a scapulo-coracoid encircling the glenoid. The 
two epicoracoids overlap broadly, and anteriorly are quite free of 
each other; posteriorly they are usually rather weakly locked by a 


Fig. 183(a). Leptodactylus pragnathus. Ventral view showing sternal articulation with 
girdle. The left half of the ventral sternal blade has been removed. Labelling as in Fig. 1 83 . 

cartilaginous sternum. The Apoda, of course, retain no vestiges of 
either limbs or limb girdles. 

9. Pelvic girdle of Amphibia 

The pelvic girdle is much larger in land animals than the small 
ventral cartilages found in fishes. It is formed of three main cartilage 
bones in all tetrapods (Fig. 184), but it is not clear how these origin- 
ated, nor whether the division has mechanical significance. The dorsal 
ilium becomes attached to specially modified transverse processes of 
one or more sacral vertebrae. This ilium can be regarded mechanically 
as the ossification along a line of compression stress due to the weight- 

The ventral portion of the girdle consists of an anterior pubis and 
posterior ischium, the three bones meeting at the acetabulum, where 




the femur articulates. The girdle thus provides a plate to which the 
muscles that brace the limb can be attached in such a way as to 
balance the body on the leg. 

In urodeles the pelvic, like the pectoral, girdle becomes reduced and 
mainly cartilaginous. The pelvic girdle of anurans is highly specialized 
and unlike that of any other vertebrate. The ilia are very long and 
directed forward to articulate with the transverse processes of the single 
pair of sacral vertebrae. The base of the ilium is expanded to make the 

ac. Cryptobranchus 

is. it- % 


Necturus p. 


Fig. 184. Pelvic girdles of lower tetrapods. Regions mainly cartilaginous are stippled. 
ac. acetabulum; /'/. ilium; is. ischium; of. obturator foramen; p. pubis. (After Evans.) 

dorsal portion of a disk, of which the pubis is the anterior, the ischium 
the posterior part, with the acetabulum at the centre. The girdle is 
thus developed into a long lever for transferring force from the limb 
to the vertebral column during jumping. 

Considerable movement is possible at the ilio-sacral joints, at least 
in Salientia (Whiting, 1961). In Rana the ilia may rotate through an 
angle of over 90 on the sacral ribs in the vertical plane. This move- 
ment is used during a strong leap. In Discoglossus the sacrum can be 
turned laterally on the pelvis through 20°. The movement is used both 
in turning to take food and in locomotion. In Xenopus the sacrum 
can slide backwards and forwards on the pelvis, producing a con- 
siderable shortening and lengthening of the whole animal. This 
movement is probably used in driving into the mud. 

10. The limbs of Amphibia 

The pattern of bones and muscles in fore and hind limbs of tetrapods 
is surprisingly constant in spite of the various uses to which the limbs 



XII. 10 

are put. Evidently similar morphogenetic processes are at work in 
both limbs. There are nearly always three main joints in each limb, 
at shoulder (hip), elbow (knee), and wrist (ankle). The hand and foot 
provide basically similar five-rayed levers, with several joints in the 
digits (Figs. 185 and 186). 

The bones of the limbs can be plausibly derived from those of a 
crossopterygian fin, and indeed the condition in *Eusthenopteron 
already distinctly suggests that of the limb of an early amphibian (Figs. 
179 and 180). We know less about the origin of the hind than of the 
front leg, but the two are so similar that they may be treated together 
for elementary analysis. There is a basal humerus (femur), articulating 
distally with two bones in each case, a more anterior (pre-axial) radius 
(tibia) and a posterior (post-axial) ulna (fibula). These bones articu- 
late at the wrist or ankle with a carpus or tarsus, consisting, in the fully 
developed condition, of three rows of little bones, namely 3 in the 
proximal row, about 3 centrals, and 5 distals. Each of the latter carries 
a digit, composed of numerous jointed phalanges. In naming these 
bones of the carpus and tarsus it is convenient to call the proximal 
carpals by their position radiale, intermedium, and ulnare and the 
tarsals tibiale, intermedium, and fibulare. The centrals and distal 
carpals may then be numbered beginning with 1 at the pre-axial 
border in each case. Unfortunately other less explicit systems of 
naming are in use, as shown in the following table. 

Plan of the Tetrapod Carpus and Tarsus. {The names used for the bones 
in man are shown in brackets.) 





radiale (scaphoid) 


ulnare (triquetral) 


centrale (tubercle 
of scaphoid) 


carpal i 



4 and 5 









tibiale (talus or 

intermedium (os 

fibulare (calcaneum) 


centrale (navicular) 


tarsal i 



4 and 5 

(medial cuneiform) (intermediate 

(lateral cuneiform) 



The plan of the carpals and tarsals can well be imagined to have been 
derived from that of a fin such as is seen in the fish *Eusthenopteron 
(Fig. 179), which might be said to have humerus, radius, and ulna, 


^•^ Nee tar us 

Fig. 185. Front legs of various lower tetrapods. 
H. humerus; R. radius; u. ulna. (Modified from Evans, J. Morph. 74.) 

1 m w 




Fig. 186. Hind legs of various tetrapods. 
F. femur; FI. fibula; T. tibia. (Modified from Evans.) 


Fig. 187. R. temporaria dissected from the back. 

add. adductor; anc. anconeus ('triceps'); c. calcar; c.sacr. coccygeo-sacralis; coc- 
cygeo-iliacus ; cue. cucullaris ; delt. deltoid ; dep. mand. depressor mandibulae ; dorsalis 
scapulae; ext.obl. obliquus externus abdominis; fasc. dors, dorsal fascia; flexor brevis; 
gastr. gastrocnemius; glut, gluteus; il. ilium; il.ext. iliacus externus; il.fib. ilio-fibularis; 
lat.dors. latissimus dorsi; I. dors, longissimus dorsi; n. nostril; peron. peroneus; pir. piri- 
formis; rhomb, rhomboideus; semi.m. semimembranosus; semi.t. semitendinosus; t.Ach. 
tendo Achillis; tensor fasciae latae; tib.ant. tibialis anterior; tr. transversus abdo- 
minis; tymp. tympanum. (Partly after Gaupp.) 

xii. io AMPHIBIAN LIMBS 317 

carpals, and 7 or 8 digits. In the amphibian *Eryops most of the digits 
radiate from the radius, in later forms mostly from the ulna. Moreover, 
in the hand of *Eryops there seem to have been six digits and it is 
usually stated that the first of these is a pre-pollex 'not comparable 
with the pollex of higher forms'. 

The effect of this system is to provide a lever that can be held 
firmly against the ground while it is moved by the muscles running 
from the girdles to the humerus or femur. In addition the lever is 
itself extensible by means of its own muscles. Whatever may have 
been their origin in fishes these muscles in tetrapods work in such a 
way as to bend each segment up and down. The shoulder and thigh 
joints usually allow movement in several planes, both towards and 
away from the midline (adduction and abduction), and forwards and 
backwards (protraction and retraction). As we have seen, the animal 
balances at these joints by muscles arranged round them. Movements 
of rotation are also possible at these, and sometimes at other joints, 
the distal bone turning about its own axis on the proximal one. Such 
movements may be very important for the proper placing of the limbs 
in walking. Pronation is the rotation of the radius about the ulnar 
bone, so that the manus is directed caudally, supination being the 
opposite movement. The terms flexion and extension are convenient 
at certain joints (e.g. the elbow), but have no consistent meaning with 
reference to the main axes of the body. 

The limbs of the earlier amphibians were ponderous affairs, with 
large bones and widely expanded hands and feet (Figs. 181 and 182). 
It is not certain exactly how they were used ; probably they were held 
out sideways, giving a wide base on which the somewhat precarious 
balance was maintained, the body being often slumped on to the 
ground. In modern urodeles the limbs retain the full pattern of parts, 
but with imperfect ossification, as would be expected since they carry 
little weight. 

In frogs, specialized for jumping, the radius and ulna are united and 
the carpals are reduced in number. There are only four true digits, the 
first digit (thumb or pollex) being reduced. There is, however, a small 
extra ossification, the pre-pollex, which becomes well developed as a 
copulatory organ in the male and may be compared with a similar 
digit found in some stegocephalians. It is to be expected that in a 
system of repeated parts, such as a tctrapod limb, multiplications and 
reductions will be common. It can be imagined that they can be 
produced by changes in the rhythm of morphogenetic processes, and 
it is surprising that there is such constancy in number of digits. 



The hind legs of frogs are long, giving a good leverage in jumping. 
The tibia and fibula are united and the proximal row of tarsals is 
reduced to two, greatly elongated and known as the tibiale (astragalus 
or talus) and fibulare (calcaneum). The distal tarsals are reduced to a 
total of three, bearing five 'true' digits and an extra one, the calcar or 

semL m 

Fig. 188. Deeper dissection of muscles of back 
of frog. inter-transversarii; ur. urostyle; v. vertebra; other 
letters as Fig. 187. (Partly after Gaupp.) 

1 1 . The back and belly muscles of Amphibia 

With the change in the method of locomotion the muscular system 
has become greatly modified from that found in fishes. In urodeles, 
which still use the old method and hence may be said to swim on land, 
the dorsal musculature is well developed (Fig. 189), but in anurans the 
dorsal portions of the myotomes, the epaxial musculature, no longer 
have to produce the locomotory effect by lateral flexion. They remain 
in frogs only as muscles that bend the body dorsally, serving to brace 
the vertebral column on the sacrum (Figs. 187 and 188). Short 
muscles run between the vertebrae, and dorsal to these is a continuous 
sheet of longitudinally arranged fibres, the longissimus dorsi muscle, 
running from head to sacral vertebra and urostyle. This muscle, 




though forming a continuous band, is crossed by a tendinous inter- 
section, showing its segmental origin. At the hind end the coccygeo- 
sacralis and coccygeo-iliacus muscles brace the urostyle on the pelvic 

The pectoral girdle is attached to the axial skeleton by a series of 
muscles. Rhomboid and levator scapulae muscles run from the supra- 
scapula to the vertebrae and skull. The cucullaris muscle corresponds 


Fig. 189. Muscles of larval Amby stoma. A, b, and c show successive layers. 

ep. epaxial muscles; ext.o. external oblique; h. horizontal septum; hyp. hypobranchial 

muscles; int.o. internal oblique; my. myocomma; rect. rectus abdominis; tr. transversus 

abdominis. (From Ihle, after Maurer.) 

to the mammalian sternomastoid, running from the skull to the 
suprascapula; it is derived from lateral plate musculature and in- 
nervated by the vagus. The naming of these muscles of the scapula, 
and indeed all amphibian muscles, meets the difficulty that many of 
the bundles of fibres are similar in their general course to muscles 
found in mammals and yet differ sufficiently to raise serious doubts 
about the wisdom of using the mammalian names. The similarity of 
arrangement of the limb muscles is so striking throughout the tetra- 
pods that there is probably no harm in keeping to the well-established 
system of names, but we know so little of the hereditary or mechanical 



ext. obi. 

Fig. 190. R. temporaria dissected from the ventral surface. 

add. aductor magnus; add. long, adductor longus ; anc. anconeus; br.r brachio-radialis ; 
cl. clavicle ; co. coracoid ; cr. cruralis ; delt. deltoid ; ep. episternum ; ext. obi. obliquus externus 
abdominis ; fix. rad. flexor carpi radialis ; fl.c.uln. flexor carpi ulnaris ; gastr. gastrocnemius ; 
grac. ma}, and min. gracilis major and minor; iliacus internus; o.h. omohyoid; om. 
omosternum; pect. pectoralis; r.s. rectus sheath; red. rectus abdominis; sart. sartorius; 
st.h. sterno-hyoid; submax. submaxillary; sub.hy. subhyoid; t.Ach. tendo Achillis; 
tensor fasciae latae; tars. a. and tars. p. tarsalis anterior and posterior; and long. 
tibialis anterior brevis and longus; tr. transversus abdominis; .yj. xiphisternum. 
(Partly after Gaupp.) 




factors that control the arrangement of muscle-fibres into 'muscles' 
that discussion of homologies is difficult. 

The hypaxial musculature, formed from the more ventral portions 
of the myotomes, is more developed than in fishes and differentiated 
into several parts, for the purpose of slinging the viscera, which of 
course need support in air in a way that is unnecessary in water. 

sub. max. 

dep. mand. 

d. rorrad 


Fig. 191. Dissection of muscles of frog from ventral surface. coraco-brachialis; cor.rad. coraco-radialis; dep. mand. depressor mandibulae; h. head of 

humerus; s. sternum; other letters as Fig. 190. (Partly after Gaupp.) 

These muscles are differentiated into layers whose fibres run in 
different directions. The plan found, with modifications, in all 
tetrapods is seen in amphibian larvae and includes four sets of fibres. 
The external obliques run caudally and ventrally; inside this 
layer is the internal oblique, running in the opposite direction, and 
within this again the transversus abdominis running approximately 
dorso-ventrally (Fig. 189). The rectus abdominis consists of fibres in 
the midline running antero-posteriorly. 

In the adult frog three of these sets of fibres can be recognized. In 
the mid-ventral region (Fig. 191) are the longitudinally arranged 
fibres of the rectus abdominis, making a sling between the sternum 
and the pubis. These fibres are interrupted at intervals by transverse 
fibrous tendinous inscriptions, giving an appearance of segmentation. 
In the mid-ventral line is the tendinous linea alba. The sling formed 



by the rectus abdominis is supported laterally by thin sheets of 
muscle-fibres running up to the vertebral column, the obliquus exter- 
nus and transversus abdominis (Fig. 191). 

In the anterior region the hypaxial muscles have become restricted 
to the throat, where they form the hyoid musculature, which by raising 

Fig. 192. a. Lateral surface of the fin of Neoceratodus, showing the abductor 

muscle-bundles, b. Section through the fin in the transverse plane, showing the 

arrangement of the muscle-bundles as abductors and adductors. 

ab. abductor muscles; ad, adductor muscles; g. pectoral girdle; h. horny fin rays; 

r. radials. (From Ihle, after Braus.) 

and lowering the floor of the mouth is the main agent of breathing. 
The submaxillary muscle runs transversely between the rami of 
the jaw. Deep to this lie other muscles, including the sternohyoid, 
close to the midline, which is a forward continuation of the rectus 

12. The limb muscles of Amphibia 

The muscles of the limbs were presumably derived from the radial 
muscles that moved the fins of fishes. These are formed from the 
myotomes and they are mainly arranged so as to raise and lower the 
fin (Fig. 192). In modern amphibia the limb musculature is still partly 
formed from myotomes (Griffiths, 1959). The segmental origin of the 

xii. 12 LIMB MUSCLES 323 

limbs is also shown by the fact that they are innervated by branches 
of the spinal nerves of several segments (2 for the fore-limb, 4 for the 
hind-limb in the frog). Presumably the original arrangement was such 
as to move the limbs in association with the waves of contraction 
passing down the body. In modern urodeles the limb is brought 
forward and its joints flexed as the epaxial muscles at the level of its 
front end contract, and then passes back and extends as the wave of 
contraction moves past. This may have been the primitive movement, 
making the limb more useful as a lever during the early attempts to 
'swim on land' (Fig. 176). 

The muscles of the limbs of tetrapods are presumably derived from 
those that raise and lower the fins of fishes, modified, as we have seen, 
to brace the limbs and move them, allowing standing and walking. 
The muscles that run from the girdles to the humerus and femur are 
therefore able to draw the leg forward and backward, as well as to 
raise and lower it in the transverse plane. The actions of the various 
bundles are of course not confined to a single plane: all the muscles 
running from the back to the humerus can raise (abduct) the upper 
limb, but the more anterior members also protract, the more posterior 
retract it. Similarly there is a ventral series whose anterior members 
work with the anterior dorsal muscles as protractors, although they 
antagonize the action of raising the whole limb. Moreover, many of the 
muscles have a rotating action on the humerus and femur. It is, how- 
ever, possible to consider the muscles of the arm and leg in two great 
groups; first a more anterior and ventral ('ventro-lateral') set serving 
to draw the limb mainly forward and towards the midline (protraction 
and adduction) and to flex its more distal joints, second a more 
posterior, dorsal ('dorso-medial') mass serving mainly to draw the 
limb backwards and away from the body (retraction and abduction) 
and to extend its joints. 

In the fore-limb the proximal members of the ventral group make a 
sheet of fibres running transversely to the main body axis and attached 
to the sternum and hypaxial muscles at one end and to the humerus at 
the other (Fig. 190). Within this sheet can be recognized the del- 
toideus, pectoralis, coraco-radialis, and coraco-brachialis muscles. In 
the limb itself this group is continued, there being, roughly speaking, 
a set of muscles in each segment that serves to flex it on the next. 
Thus the brachio-radialis flexes the elbow joint and in the forearm 
the flexor carpi radialis and flexor carpi ulnaris flex the wrist. The 
flexor digitorum longus muscle arises from the medial epicondyle of 
the humerus and is inserted by tendons to the carpus and terminal 

324 AMPHIBIA xn. 12- 

phalanges. Flexor digitorum brevis muscles arise from this tendon 
for insertion on the digits. 

Of the dorsal muscle mass (Fig. 187) the latissimus dorsi and 
dorsalis scapulae are the most proximal, running from the middle of 
the back to the humerus and serving to abduct and draw back the 
whole limb. The triceps (anconeus) serves to extend the elbow; in 
the forearm are extensor carpi ulnaris and radialis and extensors for 
the fingers. 

According to this plan protractor (flexor) muscles lie mainly an- 
terior to retractors (extensors), corresponding to the ancient move- 
ment by which the limb was drawn first forward then back as a swim- 
ming wave passed down the body. In all tetrapods flexor muscles are 
in general innervated by spinal roots anterior to those for the exten- 
sors. The locomotory movements of the limbs therefore still show the 
passage of an excitation wave backwards along the spinal cord, a relic 
of the swimming rhythm of fishes. However, the changes that have 
taken place in the relative positions of the parts of the limbs make it 
difficult to follow out this simple pattern in detail. It must also con- 
tinually be remembered that many muscles produce rotation as well 
as movement in the main planes of the body. 

In the hind limb, muscles of the same two general types can be 
recognized, namely anterior muscles, which draw the limb forward 
and flex and adduct its joints, and posterior ones, which draw it back 
and extend and abduct. The specialization of the main muscle masses 
has gone much farther, however, so that more individual muscles are 
found, especially round the hip joint, each serving to move the limb 
in a special way. 

In the thigh (Figs. 187 and 190) the muscles of the anterior group, 
lying on the ventral surface, are the pectineus and the adductors, 
running from the pelvic girdle to the femur and thus serving to move 
the whole limb inwards (adduction). The sartorius, biceps, semi- 
membranosus, and semitendinosus are two-joint muscles mainly pro- 
ducing flexion at the knee as well as at the hip. 

The more posterior and dorsal group of muscles includes the 
gluteus and tensor fascia lata from girdle to femur, extending the 
thigh joint, and the very large cruralis (including the rectus femoris 
and triceps femoris) running from girdle and femur to tibia. This is 
the main extensor of the knee, being helped by gracilis and semi- 
membranosus. This extension is obviously an important part of the 
jumping movement of the frog. 

In the shank the arrangement of the flexors and extensors into the 










p rose. 

xii. 13 LIMB MUSCLES 325 

anterior and posterior groups is much modified. The more con- 
spicuous muscles are the tibialis anterior and peroneus running from 
the femur to the tarsus so as to flex the ankle joint. Long and short 
flexors move the toes, as in the fore-limb. At the back of the tibio- 
fibula the gastrocnemius (plantaris longus) runs from the femur to 
be attached by the tendo Achillis to the tarsus. Its main action is to 
extend the ankle in the movements of jumping and swimming. Tibialis 
posterior runs from the tibia 
to the tarsus. Within the foot 
there is an elaborate system of n — i~~P m - 

small muscles for bending and 
stretching the toes and abduct- 
ing them away from each other, 
so as to expand the web for 

The whole system is de- 
signed to produce the charac- 
teristic sudden simultaneous 
extension movement of all the 
joints of both hind limbs, by 
which the frog moves both in 
water and on land. The hind 
limbs can also be used for 
alternate walking movements, 
especially in toads (Fig. 177). 







Fig. 193. Diagram of skull bones and other 
structures, a, an osteolepid ; B, astegocephalian. 

Letters for this and Fig. 194: ac. auditory capsule; 
ex. extrascapular; jr. frontal; hm. hyomandibula ; 
it. intertemporal; j. jugal; /. lachrimal; na. nasal; 
?nx. maxilla; p. pineal; pa. parietal; pi. pituitary; 
pm. pre-maxilla; po. post-orbital; pof. post-frontal; 
ppa. post-parietal; prf. pre-frontal; p.rost. post- 
rostrals; qj. quadratojugal; sq. squamosal; st. stapes; 
sut. supratemporal; t. tabular. 
(After Westoll.) 

The skull of Stenoce- 

The skull of the Devonian 
and Carboniferous amphibia 

was essentially like that of the osteolepid fishes in the arrangement of 
the bones, but the proportions had been altered so that the pre-optic 
region was relatively large and the more posterior 'table' of the skull 
short (Fig. 193). 

The nasals and frontals, which were small in crossopterygians, 
were quite long in stegocephalians, whereas the parietals were shorter 
and the post-parietals absent altogether in the later forms. The differ- 
ence is so marked that for a long time people were deceived in identifi- 
cation of the bones and it was said that the pineal opening lay between 
the frontal bones in fishes but between the parietal bones in tetrapods. 
The bones identified as 'frontal' in the fish types were, of course, 



xii. 13 

parietals, whereas the 'parietals' were the post parietals, which have 
gone completely from most amphibians, though still present in the 
earliest Devonian forms (Fig. 194). This is an excellent example of how 
study of changes of proportion can clear up morphological difficulties. 
The opercular apparatus covering the gills was lost early in 
amphibian evolution; perhaps the reduction of the whole posterior 
part of the head was effected by a single morphogenetic change. In 

ppa. "— — 





Palaeogurinus RomerJa Dimetrodon 

(Cotylosaur) (Pelycosaur) 

Fig. 194. Skulls of a crossopterygian and various early tetrapods to show the 
shortening of the posterior region. Lettering as Fig. 193. (After Westoll.) 

modern amphibia the skull is much flattened and its ossification 
reduced, so that large spaces are left; in the earlier forms, however, 
the skull was of the more usual domed shape and the roof and jaws 
were covered by a complete set of dermal bones. Presumably the loss 
of bone was another development producing a reduction of weight 
advantageous to a terrestrial animal. 

Lateral line organs are present in aquatic amphibians and their 
position is marked on the bones of the fossil skulls by rows of pits. 
By using these lines as reference marks it is possible to compare the 


pattern of the bones on osteolepid and early amphibian skulls and to 
confirm the remarkable similarity. The main new development found 
in the skull of early amphibians was correlated with the modification 
of the Eustachian tube in connexion with the sense of hearing, and 
the need for a sensitive resonator to pick up the air vibrations. Already 
in the earliest amphibians the opercular coverings of the gills were 
lost (there was a small pre-opercular bone in *Ichthyostega) and the 
spiracular opening thus uncovered acquired a tympanic membrane. 
The hyomandibular cartilage, no longer concerned (if it ever had 
been) with supporting the jaw, was modified to form the columella 
auris, serving to carry vibrations across to the inner ear. At first, 
however, there was no trace of the fenestra ovalis, the hole in the 
auditory capsule into which the columella fits in the frog. In modern 
urodeles the whole ear apparatus is much modified, there being no 
tympanum. Instead the columella is fused to the squamosal and the 
ear thus receives its vibrations from the ground. 

Other small changes in the skull in passing from the fish to the 
amphibian stage include the increase in size of the lachrymal bone, 
which also came to have a hole to carry the tear duct, draining the 
orbit. A series of small bones surrounds the orbit in early amphibians, 
as in fishes; large squamosals and quadrat ojugals support the quad- 
rate. At the back of the skull these stegocephalians possessed various of 
the small bones that are found in fishes but not in modern amphibians, 
the supratemporal and intertemporal, post-parietal (much smaller 
than in crossopterygians) and tabulars. In fact there are numerous 
small bones, arranged in a pattern clearly recalling that of the fish 
ancestor, but showing some reductions and less variation than in those 
very variable fish skulls. This simplification (which was later carried 
farther), together with some changes in the shape, are the chief trans- 
formations that have converted the fish skull into the amphibian 

The palate of the early amphibians also resembled that of crosso- 
pterygians, showing a complete plate made of vomer, palatines, 
pterygoids, and ecto-pterygoids. These bones, as well as the pre- 
maxillae and maxillae, often carried folded teeth (hence 'labyrin- 
thodonts'), with a pit for a replacing tooth beside each one, an 
arrangement similar to that of their fish ancestors (p. 270). The 
internal nostril opened far forward, through the palate. The lower 
jaw was covered by a number of dermal bones (Fig. 208), but the 
actual jaw articulation was made between cartilage bones, the upper 
quadrate, and the lower articular. 



xii. 14 

14. The skull of modern Amphibia 

Modern amphibia share several cranial features that distinguish 
them from typical labyrinthodonts. The number, extent, and thick- 
ness of the dermal elements are greatly reduced so that the otic 

b p. 

Fig. 195. Skull of the frog. a. Ventral view. b. Side view. 

ac. anterior cornu of hyoid ; art. articular ; as. angulosplenial ; col. columella auris ; d. dentary ; 
ex. exoccipital ; fp. fronto-parietal; m. maxilla; m.m. mento-Meckelian; n. nostril; na. nasal; 
pa. palatine; par. parasphenoid; pc. posterior cornu of hyoid; pm. premaxilla; pro. pro-otic; 
pt. pterygoid; q. quadrate; qj. quadrato-jugal; se. sphenethmoid; sq. squamosal; v. vomer; 
//, IX, and A', nerve foramina. (After Marshall, The Frog, Macmillan.) 

capsules are generally exposed. The orbits and interpterygoid vacui- 
ties are large, the mandibular ramus is short and the skull as a whole 
much flattened. The occiput is shortened so that the hypoglossal nerve 
emerges behind the skull and (with the few exceptions noted below) 
the parietal foramen has been lost. 

The skull of the frog (Fig. 1 95) shows great reduction and specializa- 
tion from the early amphibian type. It may be considered as consisting 
of a series of cartilaginous boxes or capsules, in whose walls some 
ossifications occur, partly covered by dermal bones. The cartilaginous 

xii. 14 



o.F P { ar F- 

cpt. %■, cp- ps.^v. m 

apt. c.M. 

o.c I c - c - SALAMANDER 



Fig. 196. Skulls of amphibians. 

a., articular; be, basicranial fenestra; bc.p., posterior basicranial fenestra; c.c, carotid canal; 
<-..V., Meckel's cartilage; c.p. coronoid process; cpt. pterygoid cartilage; c.r. process of 
internasal plate; d. dentary; e.o. exoccipital;/. frontal ;fen.ol. olfactory fenestra; in. internal 
naris;_/. jugal; m. maxillary; m.M. mento-Meckelian; ;;. nasal; o.c. occipital condyle; 
o.f. optic foramen; o.p. occipito-petrosal; ope. operculum; pterygoid bone; o.s. orbito- 
sphenoid; p. a. pre-articular; par. parietal; p.f. prefrontal; p. I. palatine; p.m. premaxilla; 
po.f. postfrontal (enclosing orbit); p.q. palato-quadrate; basal process; p.s. para- 
sphenoid; p.v. prevoma; q. quadrate bone; sq. squamosal; st. stapes; /. tentacular groove; 

v. vomer. 

boxes, well seen in a tadpole's skull, are the central neurocranium 
around the brain, and the olfactory and auditory capsules. Ossifications 
occur especially at the points of compression stress, namely, around 
the foramen magnum (the exoccipitals), where the auditory capsule 
joins the cranium (the pro-otic), and at the base of the nasal capsules 
(the mesethmoid). The paired occipital condyles are found only in 

33° AMPHIBIA xn. 14 

modern amphibia, and are formed by the failure of the basioccipital 
to become ossified. Paired occipital condyles have also arisen, inde- 
pendently, in the mammal-like reptiles. 

The dermal bones covering the roof of the skull are the nasals and 
frontoparietals, while on the floor is the large dagger bone, the 
parasphenoid, and a small tooth-bearing vomer. The remains of the 
cartilaginous palato-pterygo-quadrate bar can be recognized as a rod, 
covered in front by premaxillae and maxillae, and dividing behind 
into an otic process fixing it to the skull (autostylic) and a cartilaginous 
quadrate region articulating with the lower jaw. This region is covered 
by the pterygoid ventrally, the quadrato-jugal laterally, and the 
squamosal dorsally. The palatines are membrane bones forming the 
anterior wall of the orbit. The upper jaw is thus supported by struts 
formed from the nasals and palatines in front and the squamosal and 
pterygoid behind, an arrangement that gives a large mouth for res- 
piration and eating insects, combined with the advantages of strength, 
mobility of the lower jaw, and lightness in weight. 

The lower jaw consists of Meckel's cartilage, covered on its outer 
surface by a dentary and on its inner by an angulo-splenial bone. 
The anterior tips of the cartilages ossify as the mento-Meckelian bones . 

The visceral arches are well formed in the tadpole but are much 
modified in the adult frog. In the tadpole the skeleton of the hyoid 
arch consists of a large pair of ceratohyals attached to a basal hypo- 
hyal. As a result of subsequent metamorphosis the ceratohyals later 
form the long anterior cornu of the hyoid, attached to the pro-otic 
bone. The body of the hyoid is a plate lying in the floor of the mouth 
and formed from the hypohyal and from the hypobranchial plate at 
the base of the remaining arches. The posterior cornua support the 
floor of the mouth and the whole apparatus assists in respiration. The 
sixth and seventh of the series of branchial arches give rise respec- 
tively to the arytenoid and cricoid cartilages of the larynx. 

The lateral plate muscles of the branchial arches are well developed 
only as the muscles of the jaws. Certain muscles of the scapula (the 
cucullaris (p. 319) and interscapularis) are innervated from the vagus 
and recall the sternomastoid and other muscles innervated by the 
spinal accessory nerve in mammals. 

The muscles of the hyoid arch, innervated by the facial nerves, 
remain mainly as the depressor mandibulae (Fig. 197) running from 
the back to the angle of the jaw and serving to lower the floor of the 
mouth. The jaw-closing muscles, m.m. adductor mandibulae, belong 
to the mandibular segment and are innervated by the trigeminus. 


They run from the hind end of the jaw to the surface of the skull and 

The skull and jaws of the frog thus constitute a protection for the 
brain and special sense-organs, a feeding apparatus, and a means of 
respiration. The heavy protection afforded by the dermal bones of 
fishes and early amphibians has been largely dispensed with, probably 
for lightness. The front part of the skull, concerned with the nose, 
eyes, and brain, has become increased in size and the hind part, 
originally concerned with the gills and pharynx, greatly reduced. 


Fa se. dors, 
iat. dors. 

cor rad 
FL. c uin. 

Fig. 197. Muscles of head and neck of frog dissected from the side. 
add. adductor mandibulae. Other letters as in Figs. 187 and 191. (Partly after Gaupp.) 

These changes, carried to extremes in frogs, have been in progress 
throughout the evolution of amphibia. It is not difficult to imagine 
that they have been the result of rather simple genetic changes, affect- 
ing the relative growth of various parts of the skull. We are still far 
from the knowledge necessary to say exactly what developmental 
changes have occurred, but we know enough to imagine how selection 
through millions of years has changed the quantities of certain sub- 
stances so as to produce gradually less bony and shorter heads, such 
as enabled their possessors to maintain sufficient mobility to hold a 
place in a world peopled by the reptiles and other still more active 
descendants of the early amphibians. 

The preceding account, particularly with regard to the osteology, 
should not be regarded as diagnostic of all anurans. Bufonid skulls 
are completely devoid of teeth but they possess a supratemporal bone, 
which fuses with the squamosal and roofs the otic capsule. Hylids 
frequently develop secondary dermal ossifications to form expanded 
helmets; this trend also occurs in leptodactylids (e.g. Calyptocephalus), 
where the skull may be so completely roofed and sculptured as 
to simulate the condition of the extinct branchiosaurs. Pseudoteeth 

332 AMPHIBIA xn. 14- 

(serrations of the jaw elements) frequently occur on the dentary and 
pre-articular (e.g. Amphodus) but the only modern form to possess 
true teeth on the lower jaw is Amphignathodon. No recent frog retains 
the large parietal foramen so typical of the fossil amphibia but some 
leptodactylids and the aquatic xenopids have a small canal perforating 
the fronto-parietal, through which runs a fibro-nervous tract from the 
pineal organ to the habenular ganglion (Griffiths, 1954). The anuran 
skull is always easily distinguished from those of all other Amphibia 
by the fact that the frontals are fused with the parietals. 

Urodele skulls are, in some respects, less specialized than those of 
Anura. The frontals and the parietals remain discrete and in certain 
species both lacrimals and prefrontals are present. In other respects 
they are clearly more degenerate (or paedomorphic ?). No urodele has 
either a jugal or quadrato-jugal (except Tylotriton) and in perenni- 
branchs even the maxillaries and nasals are lost. Urodeles are further 
distinguished from frogs (but not from caecilians) by the great size 
of the prevomers (each consisting really of a prevomer+ palatine) and 
by the possession of a tooth-bearing coronoid, as well as a dentary 
and a prearticular. 

The apodan skull is a much more rigid structure than that of either 
of the above subclasses and, at first sight, approaches more closely to 
the ancestral pattern. The number of bones present, however, is no 
greater than in any of the other modern groups. The overall compact- 
ness is effected particularly by the expansion of the nasals and of the 
marginal elements of the upper jaw and is probably correlated with the 
burrowing habits of the group. Lower as well as upper jaws carry 
teeth and a toothed coronoid is present in the mandible. 

15. Respiration in Amphibia 

The new problems presented by life on land have led to the produc- 
tion of very varied means of respiration among amphibia. In a ter- 
restrial habitat oxygen is available in plenty; the difficulty is evidently 
to arrange for a regular interchange of air in contact with adequately 
moistened surfaces. The interchange is provided for in most cases 
by modifications of the apparatus used in fishes, but pumping air 
presents new problems and it seems that these are not easily solved, 
since in many amphibians the skin is used as an accessory respiratory 
mechanism. The retention of moisture becomes more difficult as the 
ventilation becomes efficient; probably for this reason air is often 
only transferred to the lungs after it has remained for some time in the 
mouth. We see again that the new way of life, in a medium remote 

xii. 1 6 RESPIRATION 333 

from water, makes it necessary to possess more complicated methods 
of self-maintenance. 

16. Respiration in the frog 

The lungs of the frog are paired sacs, opening to a short laryngeal 
chamber, which communicates with the pharynx by a median aper- 
ture, the glottis. The glottis and laryngeal chamber are supported by 
the arytenoid and cricoid cartilages. The arytenoids guard the open- 
ing of the glottis and are moved by special muscles. During breathing 
the mouth is kept tightly closed, the lips being so arranged as to make 
an air-tight junction. Air is sucked in through the nostrils by lowering 
the floor of the mouth by means of the hypoglossal musculature, and 
can then either be breathed out again or forced into the lungs by 
raising the floor. The external nares are closed by a special pad on the 
anterior angle of the lower jaw, supported by the mento-Meckelian 
bones. This pad is thrust upwards and pushes the premaxillaries 
apart, so altering the position of the nasal cartilage that the nostrils 
are closed. This is a special mechanism, found only among anurans. 
In urodeles the nostrils are closed by valves provided with smooth 
muscles. Such valves are present in the frog but are said to be func- 

The movements of the floor of the pharynx are not continuously of 
the same amplitude. After a period of relatively slight movements the 
nostrils are kept closed while the throat is lowered. Air is thus drawn 
from the lungs and then again returned to them once or twice before 
the nostrils are reopened. The whole procedure presumably ensures 
the maximum gaseous interchange for the minimum water-loss. 

This method of taking in air is clearly derived from the movements 
of the floor of the mouth of fishes, by which water is passed over the 
gills. In amphibian larvae water is pumped in this way and there is 
direct continuity between the mechanism of larva and adult. The 
basic rhythmic mechanism, centred on the nerve-cells of the medulla 
oblongata, is no doubt the same throughout, but the anurans have 
improved upon it by the addition of special features, requiring intri- 
cate coordination of the muscles of the larynx and the apparatus for 
closing the nostrils. 

The skin is very vascular, and especially so in the buccal cavity. It 
plays a large part in respiration, actually serving to remove more 
carbon dioxide than do the lungs. There is, however, little power to 
vary the amount of exchange through the skin, which is therefore 
constant throughout the year. There is considerable regulation of the 

334 AMPHIBIA xh. 16- 

exchange in the lungs. The rate of breathing depends, as in mammals, 
on the effect of the carbon dioxide tension of the blood on a respira- 
tory centre in the medulla. There is also a vasomotor control of the 
blood-supply to the lungs and, through the vagus nerve, of the state 
of contraction of the latter. By such means the rate of respiratory 
exchange is greatly increased during the breeding season, and made 
to vary with the activity of the animal. 

17. Respiratory adaptations in various amphibians 

The skin and the lungs show many variations according to the 
habitat of the species, special devices being adopted to enable the 
animals to live in particular environments. The lungs vary from the well 
vascularized sacs with a highly folded surface found in the frogs, 
and especially in the drier-skinned toads, to small simple sacs in some 
stream-living amphibia. The lung will serve to lift the animal in the 
water; for this reason it is reduced in the frog Ascaphus, which lives in 
mountain streams in the eastern U.S.A. In newts this hydrostatic 
function of the lungs is predominant and the inner surface is often 
quite simple. The lung is entirely lost in stream-living salamanders, 
such as the European alpine S. atra. The coldness of the water reduces 
activity and lowers the need for respiratory exchange to a level at 
which it can be fully met by the skin. The skin shows increased vascu- 
larity in these forms with reduced lungs, capillaries reaching nearly 
to the outermost layers of the epidermis. In the African frog Astylo- 
sternus, in which the lungs are vestigial, the male develops vascular 
papillae on the waist and thighs during the breeding season. 

Gills are present in amphibian larvae, and also in certain adult 
urodeles that may be considered as larvae that have failed to undergo 
metamorphosis (p. 364). The gills are extensions of the branchial 
arches, and carry branched villi, richly supplied with blood. Where 
the main trunk is long the gill projects and is 'external', whereas in 
other cases, as in the later frog tadpole, the filaments are directly 
attached to the arches and are called 'internal'. There are no profound 
differences between the two types. 

18. Vocal apparatus 

Sound is produced as a protective (fear) response and by the male 
frog as a call to attract the female. Both sexes have vocal organs, but 
those of the female are much the smaller. The noise is produced by 
the vibration of the elastic edges of a pair of folds of epithelium of the 
laryngeal chamber, the vocal cords. Air is passed backwards and 

xii. iQ 


Uroddd, larva 

FlG. 198. Diagrams illustrating development and fate of aortic arches in Amphibia, 

left-side view completed. Vessels carrying most arterial blood white, most venous 

blood black, and mixed blood stippled. 

a 1-6 , Primary arterial arches; ca. conus arteriosus; cb. carotid gland; cc. common carotid; 
da. median dorsal aorta; db. ductus Botalli; dc. left ductus Cuvieri; ec. external carotid; 
eg. blood-supply to external gill; ic. internal carotid; la. left auricle; Ida. lateral dorsal 
aorta (d. obliterated part, ductus caroticus); Ig. lung; oph. ophthalmic; or. orbital; pa. 
pulmonary artery; pea. pulmo-cutaneous arch; pv. pulmonary vein; s. closed spiracular slit; 
sa. systemic arch; sv. sinus venosus; tra. truncus arteriosus (ventral aorta); v. ventricle; 
vci, vena cava inferior. (From Goodrich.) 

forwards between the lungs and a large pair of sacs (or a single median 
sac), the vocal pouches, formed below the mouth. These also serve as 
resonators, and are developed only in the male. 

19. Circulatory system of Amphibia 

The venous and arterial systems arc less fully separated in Am- 
phibia than in lung-fishes. The auricles are completely divided by an 
inter-auricular septum, venous blood returning to the right, arterial 
to the left auricle. There is only a single ventricle, but this is provided 
with spongy projections of its wall, which may prevent the mixing of 
the blood. The ventral aorta (conus arteriosus), springs from the 

336 AMPHIBIA xn. 19 

right side of the ventricle and may thus receive first the venous blood. 
The conus arteriosus has transverse and longitudinal valves. 

The ventral aorta is very short and the arches much modified in the 
adult (Fig. 198). Of the original six that can be recognized the first 


A a . abdom 

Ailiaca comm 

A. ischiadica 

Fig. 199. Diagram to show the chief arteries and 
their anastomoses in the frog. (After Gaupp.) 

two disappear, the third on each side gives rise to the carotid artery, 
the fourth remains complete and forms the systemic arch. The fifth 
remains also in some urodeles, but disappears in anurans. The sixth 
arch becomes the pulmonary artery and loses its connexion with the 
dorsal aorta: special 'cutaneous arteries' carry de-oxygenated blood 
from this arch to the skin (Fig. 199). These pulmonary arches prob- 
ably offer a lesser resistance than do the systemic and carotid ones; 
the pressure in the latter is said to be increased by a special network, 
the 'carotid gland', though it may well be that this organ is a receptor, 

xii. iq CIRCULATION 337 

connected with regulation of the blood-pressure. However, it is 
claimed that the first blood leaving as the ventricle contracts flows to 
the lungs. In anurans this separation may be further assisted by an 
arrangement such that the pulmonary arteries join at their base and 

V pulmon dext 

Vjug int 
Vjug ext 
v subscap 
— Vsubc/avia 
V. brachlabs 
V. cutan. magna 

V cava ant 

PuLmo dext. 

V bulb cord, post 

V cava post 

V dorso-lumb. 
V. abdomen 
V oviduct- 
V dxaca communis 

V 'renal reveh 

V hepat. (revehens) 


V porta e hepat 



R.abdommaUs (VfemorJ 

V dica ext 

V ilica transversa 

V ischiadica 

V FemoraliS. 

Fig. 200. Diagram to show the chief veins of the frog. (After 

Gaupp.) The r. abdominalis is often called the pelvic and the 

v. iliaca communis the renal portal vein. 

open to the dorsal part of the truncus arteriosus (cavu'm pulmo- 
cutaneum), which is partly separated from the more ventral cavum 
aorticum, leading to the carotid and aortic arches. The classical view 
of this system is that as the pressure rises the truncus contracts and 
the spiral valve moves in such a way as to force all the blood that 
leaves the ventricle during the later part of its contraction into the 
ventral portion and hence to the systemic and carotid arches. In this 
way a separation of blood from the right and left auricles would be 
achieved. The view that the heart allows such a separation has, how- 
ever, been challenged on the basis of experiments made by injection 

338 AMPHIBIA xn. 19- 

of X-ray opaque material, allowing the course of the circulation to 
be watched. It is stated that by this method it can be shown that 
blood returning to either auricle reaches all parts of the ventricle and 
that no separation occurs. Since the blood from the skin returns to 
the right auricle (Fig. 200) it is not clear that a separation of the 
streams would be advantageous. It may be that the undivided con- 
dition of the ventricle in amphibians is a secondary development, 
perhaps not present in the earlier forms such as *Eogyrimis, which 
reached a larger size (Foxon, 1955). The spongy walls of the ventricle 
may allow metabolic exchange since the heart is provided only with 
very small coronary arteries. 

The venous system (Fig. 200) is based on the same plan as that of 
Dipnoi. The posterior cardinal veins are replaced early in life by a 
vena cava inferior. Most of the blood from the hind limbs passes 
through the renal portal system, but there is an alternative path 
through pelvic veins and a median anterior abdominal vein, which 
breaks into capillaries in the liver. 

The blood-pressure is regulated by the extrinsic nerves of the heart, 
fibres from the vagus tending to slow and from the sympathetic 
nervus accelerans tending to speed the beat. The latter nerve is a 
new development, there being no sympathetic innervation of the 
heart in fishes (the condition in Dipnoi is unknown). The diameter 
of the arteries throughout the body is also under control from sym- 
pathetic vasoconstrictor and perhaps also vasodilatator nerves. The 
arterioles in the web of the foot can be seen to constrict when the 
medulla oblongata is stimulated. Substances extracted from the 
posterior lobe of the pituitary and from the adrenal medulla also serve 
to cause constriction of the arteries and perhaps also of the capillaries. 

There is therefore a complex mechanism for ensuring that the pres- 
sure of the blood is maintained and the flow directed into the part of 
the body that requires it for the time being. 

20. Lymphatic system of Amphibia 

The transfer of substances between the cells and the blood-stream is 
effected in any vertebrate by a transudation through the walls of the 
capillaries into the tissue fluids. Under the pressure of the heart-beat 
water and solutes leave the capillaries, passing through their walls, 
while proteins remain behind. The blood passing into the venous 
ends of the capillaries therefore has a high colloid osmotic pressure 
and this serves to suck back fluid from the tissues. In this way a 
circulation from the capillaries into the spaces around the cells is 

xii. 21 BLOOD OF AMPHIBIA 339 

produced. Clearly, however, it is essential for this mechanism that 
the pressure of the ventricular heart-beat shall exceed the colloid 
osmotic pressure of the blood. This it does by about three times in the 

The lymphatic system consists of a set of spaces which, in the frog 
at least, communicate with the tissue spaces around the capillaries. 
Injection of gum into the lymphatic system, by increasing the colloid 
osmotic pressure in the tissue spaces, prevents the back suck of fluid 
into the venules and hence leads to swelling of the part injected. The 
lymph spaces in the tissues join to form larger channels and great 
sinuses, such as that below the loose skin of the back of the frog. The 
lymph is kept circulating by the action of lymph hearts. In the frog 
there are anterior and posterior pairs of these, opening into veins. The 
more posterior pair lies on either side of the coccyx and can be seen if 
the skin is removed. The lymphatic vessels also assist in the process 
of repair. If, after injury, red cells come to lie in the tissues the lym- 
phatics send out sprouts for as far as -^ mm to pick them up and 
return them to the blood-stream. 

21. The blood of Amphibia 

The red corpuscles of amphibia are much larger than those of 
mammals, reaching in the urodele Amphiuma the immense size of 
yofx; they nearly always exceed 20 fi. The red cells are formed mainly 
in the kidney, and are destroyed, after a life of about 100 days, by the 
spleen and liver. The bone-marrow is a source of red cell formation 
in Ra?ia temporaria but not, except during the breeding-season, in 
R. pipiens. A process of breaking up of the red cells occurs after they 
have entered the blood-stream, giving a number of enucleated frag- 
ments, and this, when the part remaining with the nucleus is small, 
produces a result like the extrusion of the nucleus during the develop- 
ment of the red cell of mammals. In Rana only small portions of the 
cytoplasm are broken off in this way, but in Batrachoseps a large 
proportion of enucleated corpuscles is produced. 

The haemoglobin of the frog has a lower affinity for oxygen than 
that of mammals, even when both are considered at the same tempera- 
ture, and in this respect is notably less efficient. Also, although the 
power of the blood to combine with carbon dioxide is great, there is a 
less delicate regulation of the reaction of the blood than in mammals. 

The white cells of amphibia are of three types, lymphocytes, with a 
large nucleus and small cytoplasm, monocytes, which are larger 
phagocytic macrophages, and polymorphonuclear granulocytes. 

34° AMPHIBIA xn. 21- 

These last may be neutro-, eosino, or basiphil and are migratory and 
phagocytic. Thus the white cell picture with which we are familiar in 
mammals was evidently established a very long time ago. 

There is a globular spleen near the tail of the pancreas. 

The blood of frogs also contains numerous small platelets (thrombo- 
cytes), which probably break down when in contact with foreign 
surfaces to produce the thrombin that combines with the fibrinogen 
of the blood-plasma to produce clotting. 

22. Urinogenital system of Amphibia 

The excretory organs of adult amphibia are always the tubules of 
the mesonephros. In Rana, where there is a general shortening of 
the body, these extend over only a small number of segments and the 
kidneys are compact. In urodeles and the primitive frog Ascaphus 
the kidneys are elongated and show some evidence of their segmental 
nature. The mesonephros consists essentially of a series of tubules 
leading from the nephric funnels to the Wolffian duct. In the frog the 
funnels do not open into the tubules, however, but into the veins; 
moreover, they form independently of the rest of the tubule. In the 
adult there are some 2,000 glomeruli, from each of which a short 
ciliated tube leads to the proximal convoluted tubule. There follows 
a second short ciliated region, corresponding in position to the Henle's 
loop of mammals, and leading to a distal convoluted tubule, which 
joins the Wolffian duct. 

The blood-supply of the kidney differs from that of mammals in 
that blood arrives from two distinct sources; the branches of the 
renal artery run mainly to the glomeruli, those of the renal portal 
vein to the tubules. This corresponds to the functions now well 
established for those two parts, namely that the glomerulus filters off 
water and crystalloids, some of which are then reabsorbed by the 
tubule. Many details of this process are not clear, however, for 
instance how the urea concentration in the urine is raised many times 
above that of the blood. 

The frog, having a moist skin, is presumably in constant danger of 
osmotic flooding with water when it is submerged, and of desiccation 
when on land. The flooding is prevented by the efficient functioning 
of the glomeruli; they allow the frog to excrete as much as one-third 
of its weight of water per day (man i/50th). The mechanisms for 
resistance to desiccation are less perfect. There is no long water 
reabsorbing segment, the part of the tubule corresponding to Henle's 
loop being short. There is, however, a large cloacal (allantoic) bladder 

xii. 22 REPRODUCTION 341 

(to be distinguished from the mesodermal bladder of fishes) from 
which water can be reabsorbed. Certain desert amphibia (Chiroleptes) 
conserve water by losing the glomeruli altogether. Rana cancrivora is 
euryhaline and may have 2-9% of urea in the blood (Gordon 1961). 

The Miillerian duct, by which eggs are carried to the exterior, 
develops separately from the Wolffian system in the frog, but arises 
from the latter during development in urodeles. In this, as in many 
other features, the frog shows a greater degree of specialization of its 
developmental processes. The ovaries are mere folds of the peri- 
toneum, having no solid stroma such as is found in mammals. There 
are, however, follicle cells around each egg; these presumably pro- 
duce the ovarian hormones. Sections of an ovary show eggs in various 
stages of development, but not all those that begin complete their 
maturation; many degenerating, atretic eggs are found. Ripening of 
the eggs proceeds under the influence of a hormone produced by the 
anterior lobe of the pituitary. This in turn is controlled by external 
environmental factors to ensure breeding in the spring. Suitable 
injections of mammalian anterior pituitary extracts will ensure ripen- 
ing of the ovaries and ovulation at any time of year. The 'prolans' 
excreted in the urine of pregnant women have a similar effect, and 
the production of ovulation in Xenopas is used as a test for the diagno- 
sis of human pregnancy. 

Having left the ovary the eggs find their way to the mouths of the 
oviducts mainly by ciliary action of the latter. The walls of the oviduct 
are glandular and secrete the albumen; they are dilated at the lower 
end to form uterine sacs, in which the eggs are stored until laid. 

The testes discharge directly through the mesonephros by special 
ducts, the vasa efferentia, formed by outgrowths from the mesone- 
phros into the gonad. This is presumably a secondary development 
from the original vertebrate condition in which the sperms were 
carried away by the nephrostomes. The fact that the sperms pass 
through the kidney emphasizes that the amphibia have diverged at 
a very early stage of the evolution of the vertebrate stock, and remain 
still in many respects at a lower level of evolution than the modern 
fishes, all of which have acquired separate urinary and genital ducts. 
In Alytes, in many ways primitive, the sperms do not, however, pass 
through the kidney! 

In some frogs (R. temporaria) there is a special diverticulum, the 
vesicula seminalis, leading by several small channels to the lower end 
of the Wolffian duct. It contains spermatozoa during the breeding- 
season and its appearance suggests a secretory activity. 

342 AMPHIBIA xn. 22- 

Most of the amphibia have failed to effect the complete transfer to 
land life : they return each year to the water to breed. Special modifica- 
tions of the reproductive system for land life are therefore not found. 
Secondary sexual differences are marked in many species. In frogs 
the males precede the females to the water and then attract the latter 
by their vocal apparatus. The male clings to the back of the female 
by means of a 'nuptial pad', developed as an extra digit, prepollex, 
on the hand (p. 317). Injection of male hormones or implantation 
of testis will cause this organ to develop in young female frogs. 

In newts fertilization is ensured by an elaborate courtship. Sperms 
are made into spermatophores by special pelvic and cloacal glands 
and there are also abdominal glands, which produce a secretion attrac- 
tive to the female. After a courtship ceremony the spermatophores are 
picked up by the cloaca of the female and stored in a spermathecal 

23. Digestive system of Amphibia 

Nearly all adult amphibia feed on invertebrates, mainly insects, 
partly also worms, slugs and snails, spiders and millipedes. The larval 
stages are usually omnivorous, but they may be cannibalistic, feeding 
on the tadpoles of the same or other species — an interesting form of 
provision for the next generation by excess productivity of the 
mother. There are only minor modifications of particular species in 
relation to their diet; as regards their food amphibia occupy a general- 
ized or 'easy' habitat. The fact that they are not particular in choice 
of diet has no doubt been part of the secret of their success. 

The tongue is the characteristic organ for catching the food and is 
one of the special features required for terrestrial life, being reduced 
in aquatic amphibia. In Rana it is attached to the floor of the mouth 
anteriorly and flicked outwards by its muscles. To keep it moist and 
sticky a special inter-maxillary gland is found. From the shape of the 
premaxillae it can be deduced that this gland was present in labyrin- 
thodonts. The saliva contains a weak amylase and some protease. It 
is suggested that these serve to release sufficient substances for tasting. 
Special tracts of cilia carry the secretion from the intermaxillary 
glands to the vomero-nasal organ and palatal taste-buds (Francis, 
1 961). 

Another feature made necessary by terrestrial life is the presence of 
cilia to keep the fluids moving over the oral surfaces. These cilia are 
absent in aquatic amphibia. 

The teeth on the premaxillae, maxillae, and vomers are used only 

xii. 23 FEEDING 343 

to prevent the escape of the prey; few amphibia bite. Biting teeth 
are present, however, in the adult Ceratophrys ornata, whose larvae 
also have powerful jaws and are cannibalistic. The South American 
tree-frog Amphignaihodon has teeth in the lower as well as the upper 
jaw and presumably has redeveloped them, a remarkable case of the 
reversal of evolution. Teeth are also present on the lower jaw of most 


Fig. 201. Transverse section of the spinal cord of a frog, showing cells in the grey 
matter with their axons and dendrites spreading into the 'white' matter. 

ax. axon of ventral horn cell, leaving cord in ventral root; d. dendrite of ventral horn cell; 

dhc. small cells of dorsal horn; dr. dorsal root entry; m. cell body of ventral horn cell; tieur. 

neuropil at periphery of spinal cord; vhc. small cell of ventral horn. (After Gaupp.) 

The oesophagus is not sharply marked off from either mouth or 
stomach and the latter is a simple tube. Its lining epithelium of 
mucus-secreting cells is folded and simple tubular glands open at the 
base of the folds. These glands, unlike those of mammals, are com- 
posed of only a single type of cell, which secretes both the acid and the 
pepsin found in the stomach. 

The intestine is marked off from the stomach by a pyloric sphincter. 
It is relatively short and dilates into a large intestine, there being a 
valve interposed in the frogs, though not in all amphibia. The liver 
and pancreas have the structure common to all vertebrates and pro- 
duce juices of the usual type. The intestine of the omnivorous tadpole 
is more coiled than that of the adult frog. The type of food taken 
depends on what is available, most species of amphibia are not par- 
ticular feeders. However, they can learn with only one or two trials 
to avoid distasteful insects. Frogs and toads devour large numbers of 
insects. If the common insects available are pests the amphibian's part 
in controlling their number works to the advantage of man. 


24. Nervous system of Amphibia 

The organization of the nervous system of amphibia might be said 
to be essentially similar to that of fishes. In both groups there are 
highly developed special centres in the brain, each centre related to a 

verb. 7. 




Fig. 202. Ventral branches of the spinal nerves (2-1 1) of the frog. The sympathetic chain 

is also shown. 

g.X, vagus ganglion; int. a. intestinal artery; n.spl. splanchnic nerve; n. (2-1 1), spinal nerves; 
sub. subclavier artery, sym. sympathetic chain; vert. 1, 1st vertebra. (After Gaupp.) 

special receptor system. In neither group is there a dominant part, 
integrating the activity of the whole, as does the cerebral cortex in 

The plan of the spinal cord is like that of fishes, but well-marked 
dorsal and ventral horns are present. The large motor-cells of the cord 
have dendrites that spread widely in the white matter, where their 

XII. 24 



synaptic connexions are made in a complicated 'neuropil' (Fig. 201). 
This is a simpler arrangement than is found within the grey matter of 
the mammalian curd. 




n. 9, 10,11 

Fig. 203. The brain of Rana, dorsal view. 

cer.h. cerebral hemisphere; cereb. cerebellum; epi. epiphysis; hth. hypothalamus; hyp. pitui- 
tary gland; lam.t. lamina terminalis; olf.l. olfactory lobe; n.olf. olfactory nerve; n. 3-1 1 cranial 
nerves; «. (1 and 2), spinal nerves; opt. c. optic chiasma; opt.l. optic lobe; opt.t. optic tract. 
(Modified from Gaupp.) 

The arrangement of the spinal nerves is much modified by the 
development of the limbs. Ten spinal nerves are found but since an 
embryonic first one is missing they are sometimes numbered 2-1 1 (Fig. 
202). Two spinal segments contribute to the brachial and four to the 
sciatic plexuses in the frog. From these plexuses fibres are distributed 
to the muscles and skin of the limbs (Fig. 202). 

346 AMPHIBIA xii. 24 

The brain (Figs. 203 and 204) resembles that of Dipnoi very strik- 
ingly. The prosencephalon is based on an inverted plan (p. 211); the 
large evaginated cerebral hemispheres therefore have a thick nervous 
roof as well as floor. In the frog there is only a short unpaired region 
of the forebrain (diencephalon) but this is longer in urodeles. The 
walls of each hemisphere may be divided into a dorsal pallium, medial 
ventral septum, and latero-ventral striatum (Fig. 205). The cell bodies 
lie around the ventricle in all parts of the hemisphere and there are 
several layers of them. The cells are pyramidal in shape and the con- 
nexions are made in the outer 'white' matter. 

Nearly all parts of the hemisphere are reached by olfactory tract 
fibres, the axons of the mitral cells of the olfactory bulb (Fig. 205). 
In the frog there are regions at the hind end of the hemispheres that 
receive forwardly directed fibres, some probably connected with tactile 
and others certainly with optic impulses. There is therefore some 
opportunity for the hemispheres to act as correlating centres, but we 
have little information as to the functions performed in them. Their 
backward projections are made by means of two large tracts, the 
lateral and medial forebrain bundles, but these reach only to the 
thalamus, hypothalamus, and midbrain, not back to the cord. Elec- 
trical stimulation of the forebrain does not produce movements of the 
animal; presumably such a crude method, though it may excite a 
few neurons, cannot imitate the more subtle patterns in which they 
are normally active. 

Removal of the cerebral hemispheres is said to have little influence 
on the normal feeding and other reactions of the frog. After this 
operation the animals are said to be more sluggish, to show less 
'spontaneity', and to learn less well. If the latter is true it shows a 
considerable advance in the functioning of the hemispheres over the 
stage reached in fishes, whose learning can certainly take place in 
other parts of the brain, and is apparently little affected by removal 
of the forebrain (p. 210). 

Some indication of the function of the cerebral hemispheres is given 
by the fact that by placing electrodes connected with a suitable am- 
plifier upon them, rhythmical changes of potential can be recorded 
(Fig. 206). These are most marked in the olfactory bulb and probably 
propagate backwards along the hemisphere. The rhythms continue 
even in a brain that has been removed from the head. They are there- 
fore a sign of some intrinsic activity of the brain, rather than of re- 
sponse to peripheral stimulation. 

The diencephalon is interesting chiefly for the considerable number 


Fig. 204. Two further views of the brain of Rana. 
Above: ventral view. Below: lateral view. (Modified after Gaupp.) 
Lettering as Fig. 203. 






Fig. 205. Diagrams of the structure and probable cell connexions in, A, the olfactory bulb, 
and b, the cerebral hemisphere of the frog. 

glom. glomerulus in which fibres of olfactory nerve make contact with dendrites of mitral cells ; 
gran, granule cell (cell without any axon); l.f.b. lateral forebrain bundle; m.f.b. medial forebrain 
bundle; wit. mitral cell; olf.n. fibres of olfactory nerve; olfactory tracts; p.c. periglomerular 
cell. The electrodes are shown as they would be placed for recording the potentials shown in Fig. 

206. (From Gerard and Young.) 

XII. 24-25 B R A I N 349 

of optic tract fibres that end in its walls; other sensory projections 
also reach here. In anurans, but not in urodeles, there is a partial 
division into separate thalamic sensory nuclei, such as are found in 
mammals, for touch, sight, and other receptor modalities. 

The pineal organ shows evidence of a retina in a few amphibia; 
in most it is a simple sac. 

The pituitary body is well developed and the usual partes, anterior, 
intermedia, nervosa, and tuberalis can be recognized, though they are 
not in the same relative position as in mammals. 

Fig. 206. Rhythmical changes of potential between electrodes placed on the surface 
of the olfactory bulb of the frog as in Fig. 205. (After Gerard and Young.) 

The midbrain is very well developed and shows many similarities to 
that of fishes. The cells it contains do not all lie round the ventricle, 
many have moved out to make an elaborate system of cortical layers. 
Electrical stimulation of various parts of the optic tectum produces 
movements of the limb and other muscles; there can be no doubt 
that this region plays a dominant part in behaviour. Most of the fibres 
of the optic tract end here, and there are also other pathways from 
the olfactory, auditory, medullary (gustatory?), and spinal regions. 
Efferent fibres leaving the tectum pass to the midbrain base, medulla, 
and perhaps back into the cord. This region therefore has wider con- 
nexions than any other part of the nervous system and thus nearly 
reaches the status of a dominant integrating organ. 

The cerebellum of amphibia, on the other hand, is very small; 
perhaps because these are mostly animals that do not have to adjust 
themselves freely in space during locomotion, they move mainly in a 
single plane. There is little need for control of speed or distance of 
movement, except of the head and tongue, which are controlled by 
the tectum. 

25. Skin receptors 

Lateral line organs are present in the skin of all aquatic amphibian 
larvae and in some aquatic adults, such as those of the anuran family 
Pipidae. They are of simple form, consisting of groups of cells in an 

350 AMPHIBIA xn. 25- 

open pit. In newts they are present in the larvae, which are aquatic, 
but are covered by epidermal layers during the first post-larval stage 
during which the newt lives on land. In the final aquatic adult stage 
the organs reappear. 

The skin, of course, also contains tactile organs, and in addition is 
often sensitive to chemical stimuli. This chemical sense is mediated 
by fibres running in the spinal nerves, not by special elements such as 
the taste-buds found spread out over the body in fishes. The skin is 
also sensitive to heat and cold, and there is some evidence that these 
senses are served by fibres different from those that mediate touch, 
pain, or the chemical senses. Histologically, however, there is little 
sign of the development of the special sensory corpuscles that are 
so conspicuous in the skin of birds and mammals. All the nerve- 
endings are of the type known as 'free nerve-endings', except for a few 
touch corpuscles on special regions such as the feet. In this the 
amphibia again resemble the fishes and show less differentiation than 
do the higher animals. 

The taste-buds on the tongue and palate are probably able to 
respond to the presence of only two of the four types of substance 
that are discriminated by mammals. Applications to the tongue of the 
frog and recordings of nerve-impulses in its nerves show that there 
are chemoreceptors present able to respond to salt and sour substances, 
but that no reaction is given to substances that in mammals are classed 
as sweet or bitter. 

The olfactory organ functions both on land and in the water, special 
mucous glands being present to keep it moist when in air. A continual 
circulation of water or air is maintained over the olfactory epithelium 
by cilia or the movements of respiration. The internal nostril may 
have originally developed from the double nostril of fishes, in order to 
make a circulation around the olfactory receptors possible. Jacobson's 
organ is a special diverticulum of the olfactory chamber, serving to 
test the 'smell' of food in the mouth. 

The Apoda, being blind, have a great development of the sense of 
smell, including a hollow tentacle or olfactory tube. 

26. The eyes of Amphibia 

Provided that certain requirements are met the air gives more scope 
for the use of photoreceptors than does the water. Light is trans- 
ported with less disturbance through the air and image formation is 
facilitated by the refraction of the air-corneal surface. The amphibia 
have exploited these advantages and sight has become the dominant 

xii. 26 THE EYE 351 

sense of most of the forms. For clear vision it is essential that the 
surface of the eye be protected, kept moist and free of particles, and 
for these purposes the eyelids and lachrymal glands are present. The 
upper lid is fixed, but the lower is very mobile and folded to make a 
transparent structure, the nicitating membrane, able to move rapidly 
across the surface of the eye. 


C % 

Fig. 207. The amphibian eye and its accommodation. 

a, anuran eye in vertical section, ac. area centralis; to. inferior oblique; ir. inferior rectus; 
//. lower lid; Im. lens muscles (protractors); n. optic nerve; nm. nictitating membrane; 
pn. pupillary nodules; sc. scleral cartilage; so. superior oblique; sr. superior rectus; ul. upper 
lid; z. zonula Zinnii. b, anterior segment of Bufo in relaxation. C, in accommodation; note 
forward movement of lens. (From Walls, after Franz and Ueer.) 

The eyeball is almost spherical, with a rounded cornea. The lens is 
farther from the cornea than in fishes and is flattened, more so in 
anurans than in urodeles. These modifications allow focusing of a 
more distant image. There is an iris, with a rapidly moving aperture, 
operated by powerful circular (sphincter) and radial (dilatator) 
muscles. Although these muscles are partly actuated by a nervous 
mechanism they are also directly sensitive to light, and the pupil of 
the isolated eye of the frog shows wide excursions with change of 

Accommodation is effected by protractor lentis muscles, attached 
to the fibres by which the lens is supported (Fig. 207). These muscles 

352 AMPHIBIA xil. 26- 

move the lens forward, whereas the muscles of the lens of teleostean 
fishes move it backwards. Other fibres, the musculus tensor chorioi- 
deae, run radially and around the lens. They may help the protractors, 
and are probably the ancestors of the ciliary muscles of higher 

In amphibia living in the water the eye is based much more on the 
fish plan and the lens is rounder. There are then no lids or lachrymal 
glands and the eye is enabled to make an image, in spite of the absence 
of the air-corneal interface, by a thickening of the inside of the cornea. 

Rods and cones are present in the retina, the former containing 
visual purple, which may be red or greenish. The two sets of receptor 
are apparently found throughout the retina in urodeles, but in Rana 
there is a macular region in which the cones are in excess and this is 
still further developed in Bufo. Study of the impulses in the optic 
nerves of Rana shows that six types of detector operate upon the infor- 
mation provided by the rods and cones. (1) Contrast detectors give a 
sustained response when a sharp edge moves into the visual field ; (2) 
convexity detectors respond to objects that are curved, the discharge 
being greater the more curved (smaller) they are. These two types 
together may be called 'on' fibres; (3) moving-edge detectors ('on/off' 
fibres) respond with a frequency proportional to the velocity of move- 
ment; (4) dimming detectors respond on reduction of illumination 
('off' fibres); (5) darkness detectors fire with frequency inversely pro- 
portional to illumination. These types of fibre project to different 
depths in the tectum as sheets of endings, and the arrangement of the 
retina is accurately reproduced there although the fibres are interwoven 
in the nerve (perhaps to prevent 'cross-talk'). Moreover, if the nerve 
is severed the fibres regenerate in such a way as to reconstitute the 
map. The sixth type of fibre is sensitive to blue light and is connected 
with the thalamus. 

These operations serve to provide reports of the types of change 
relevant to the animal. Thus the second type might be called 'insect 
detectors', responding when a small dark object enters the field 
and moves about intermittently. More complex visual discrimina- 
tions are also possible, for example toads can distinguish between 

The skin is probably sensitive to light in all amphibians : frogs react 
to light even after removal of the eyes and cerebral hemispheres. This 
skin sense is especially developed in certain cave-living urodeles, 
Proteus, in which the eyes are not functional. A similar degeneration 
also occurs in Apoda. 

XII. 27 (353) 

27. The ear of Amphibia 

The inner ear is divided into a utricle, from which the semicircular 
canals arise, and a saccule, from which there is a diverticulum, the 
lagena, part of whose receptor surface is covered with a tectorial 
membrane somewhat similar to that of mammals. There is, however, 
no coiled cochlea. The middle ear of the frog consists of a funnel- 
shaped tympanic cavity communicating with the pharynx and closed 
externally by a tympanum supported by a tympanic ring. Sound 
waves are transmitted across the cavity by a rod, the columella, fitting 
by an expanded foot, the otostapes, into the fenestra ovalis, a hole in 
the wall of the auditory capsule. This hole is also partly occupied by 
a second plate, the operculum, which is joined to the scapula by a 
special opercular muscle. The operculum and otostapes develop with- 
in the wall of the auditory capsule and the middle part of the colu- 
mella (mediostapes) forms as an outgrowth from the otostapes. The 
outer part of the columella (extra-columella) and the tympanic ring 
develop close to the quadrate and probably from its cartilage. 

The columella, therefore, shows no developmental relationships to 
the hyoid arch. The tympanic cavity is developed from the spiracular 
cleft, after a strange series of changes. The original cleft degenerates 
six days after hatching but about six of its lining cells persist and at 
the end of the tadpole stage form a tympanic vesicle, which becomes 
connected with the pharynx by a rod of cells. This rod then degener- 
ates again and an open air passage to the vesicle of the drum is not 
established until some thirty days after emergence from the water, 
when a pouch from the pharynx joins the tympanic cavity. These 
events show the complexities that may result from the modification 
of developmental processes, and they emphasize the difficulty in 
assigning 'homologies'. It is still debated to what extent the middle 
ear of the frog can be compared with that of amniotes. The hyo- 
mandibular nerve, which divides above the middle ear of amniotes 
(and above the spiracle of the dogfish) lies behind the tympanic cavity 
of the frog and branches below it. 

The arrangement for conveying vibrations to the ear varies con- 
siderably among amphibians. In urodeles there is no tympanum. In 
some of them the columella is attached to the squamosal, perhaps in 
connexion with a semi-aquatic or burrowing habit. A similar arrange- 
ment may have been present in the earliest amphibians, which have 
a columella but no oval window. In other urodeles (Plethodontidae) 
the columella is attached to the quadrate and there may be a second 

354 AMPHIBIA xn. 27- 

ossicle, the operculum, working in parallel, with its inner end in the 
oval window caudal to the columella and its outer end attached by a 
muscle to the scapula. In terrestrial forms the columella becomes fused 
with the window at metamorphosis and its function is taken over by 
the operculum, probably receiving vibrations from the fore-legs. The 
more aquatic forms (Cryptobranchus) retain the larval condition and 
never develop an operculum. The tympanum and columella are also 
reduced in some terrestrial anurans {Bombinator) but in the aquatic 
Xenopus and Pipa the operculum and its muscle are lost, perhaps a 
paedomorphic feature. 

The sense of hearing is certainly well developed, especially in 
Anura, which respond to vibrations from 50 to 10,000 a second. The 
hearing is used especially in the breeding-season, when the croaking 
serves to attract both sexes to the water. The prey may also be located 
by sound. Urodeles have been shown to give no response to the ring- 
ing of a bell suspended from the ceiling, which, however, produces 
reactions in Rana and Bufo. 

A peculiar feature of many Anura is an immense backward develop- 
ment of the perilymphatic space of the inner ear, forming a sac 
extending above the brain and on either side of the spinal cord as far 
back as the sacrum. Portions of this sac emerge between the vertebrae, 
showing as whitish masses on account of the granules of chalk they 
contain. The calcium salts in these sacs diminish greatly during 
metamorphosis and they then refill. The system may serve as a 
calcium reserve also for the adult. 

28. Behaviour of Amphibia 

The habits of amphibia, like their special structures, enable them 
to deal with the various emergencies that threaten the continuation of 
life on land. Frogs and toads have a strong sense of place and they 
show distinct 'homing' reactions. They are able to learn to find their 
way out of mazes and to remember the way for periods of at least 
thirty days. 

Complex migrations are made by many species; nearly all migrate 
to the water in spring. In this migration the males usually precede 
the females, then attract the latter by their calling. The receptors for 
the orientation towards the water are known in the osmoreceptors in 
the mouth of the frog. This orientation is particularly clear in uro- 
deles, in which sound plays no part in the migration. The power to 
find water is obviously of first importance for any animal living on 
land, and further study of the receptors involved would be interesting. 

xii. 28 BEHAVIOUR 355 

The search for food and the avoidance of enemies are not in prin- 
ciple more difficult on land than in the water, but they probably 
demand new mechanisms. For example, the greater range of visibility 
can be a disadvantage, especially when it is exploited by one's success- 
ful and predatory descendants. A hawk or owl makes fuller use of its 
opportunities in this respect than does the frog, who can only remain 
safe from them by behaviour that keeps it concealed. Similarly there 
are dangers in certain situations, for instance of desiccation, which 
are additional to those that are met by an animal in the water. 

In the emergence of the first land vertebrates we thus see a con- 
spicuous example of the invasion by living things of a medium far 
different from themselves. This produces a situation that calls forth 
all the powers of the race to produce new types of individual, and 
necessitates that the individuals make full use of their capacities. 
New patterns of structure and behaviour are developed as the various 
possible situations emerge. The types of organization that at first 
manage to survive gradually give place to others, still more complex 
or 'higher'. Some traces of the organization of the early venturers can 
still be seen in the amphibia, which today exploit the damper situa- 
tions on the earth. 




1 . The earliest Amphibia 

There are such close resemblances between the skulls of the earliest 
amphibians and those of the Devonian crossopterygian fishes that 
there can be no doubt of the relationship (Fig. 194). At present there 
is, however, no detailed fossil evidence of the stages of transition 
from the one type to the other. The fossils that appear to be closest 
to the possible tetrapod ancestor are the osteolepids of the Lower and 
Middle Devonian periods, about 375 million years ago. These were 
definitely fishes, though they may have breathed air. *Elpistostege is 
a single Upper Devonian skull intermediate between such fishes and 
the earliest undoubted tetrapods, *Ichthyostega and similar forms, 
found recently in freshwater beds of Greenland. These are dated as 
very late Devonian or early Carboniferous, that is to say about 350 
million years ago. They are the oldest members yet found of the 
great group of Stegocephalia, which, throughout the succeeding 100 
million years of the Carboniferous and Permian periods, flourished 
and developed many different lines, one giving rise to the reptiles and 
others to the modern amphibia. The term Stegocephalia is convenient 
to cover the whole group of palaeozoic amphibia, all probably of 
common descent. At least seven types can be recognized (p. 296), but 
attempts to group these have not been altogether successful; the 
nomenclature remains confused. The Labyrinthodontia were the central 
stock and were in the main terrestrial forms, giving off at intervals lines 
that returned to the water. A characteristic labyrinthodont feature is 
a folded pattern of the teeth, similar to that of their crossopterygian 

The earliest Stegocephalia were definitely tetrapods and already 
showed sharp changes from the fish type. *Ichthyostega is known 
chiefly from the skull (Fig. 208), which shows all the characteristic 
amphibian features, but retained traces of fish ancestry in its shape, 
with a short, wide snout and long posterior region (table), and pre- 
sence of a preopercular bone. The nostril lies on the very edge of the 
upper lip, apparently partly divided by a flange of the maxilla into 
internal and external openings. 

XIII. 1-2 


2. Terrestrial Palaeozoic Amphibia. Embolomeri and Rhachitomi 

We possess more complete information about the slightly later 
forms, the Embolomeri, such as *Eogyrinus, from the Lower Carboni- 
ferous (Fig. 21 1). These were long-bodied animals, rather newt-like, 
and their small limbs cannot have made very effective progress on 
land. They probably lived mostly in the water, eating fish. The 

Fig. 208. Skull of Ichthyostega. (From Westoll, after Save-Soderbergh.) 

d. dentary; en. external nostril; ept. ectopterygoid ; jr. frontal; in. internal nostril; ina. 
internasal; /. jugal; la. lachrymal; mx. maxilla; na. nasal; pa. parietal; pal. palatine; pm. 
premaxilla; pn. postnarial; po. postorbital; poj. postfrontal; pop. preopercular; ppa. post- 
parietal; prj. prefrontal; ps. parasphenoid ; pt. pterygoid; q. quadrate; qj. quadratojugal ; 
san. sur-angular; sq. squamosal; sut. supratemporal ; /. tabular; v. vomer. 

pectoral girdle was still joined to the skull by a process of the tabular 
bone, as in fishes. The pelvic girdle did not form a full articulation 
with the sacral vertebrae but was apparently attached only by liga- 

The structure of the vertebrae has given rise to much controversy. 
In the earliest amphibia we find three elements, a more dorsal neuro- 
pophysis and a centrum composed of two parts, pleurocentrum and 
hypocentrum, the latter associated with a ventral arch and rib. These 
elements can be identified in the vertebrae of crossopterygians but it 
is still not clear what relationship, if any, they have to the two pairs of 
vertebral 'arches' alleged to be present in elasmobranchs (see Williams, 

J 959)- 


Fig. 209. Various urodele amphibians, not all to same scale (mostly from life). 

xin. 2-3 FOSSIL AMPHIBIA 359 

The skull shows the full series of bones that we have already dis- 
cussed; there is therefore no reason to suppose that these animals 
represent a secondarily 'degenerate' branch, which had returned to 
the water. They were probably very close to the ancestors of all 
tetrapods. They were numerous in the Carboniferous swamps, but 
disappeared early in the Permian. So close were these Embolomeri 
to the ancestry of the reptiles that many workers classify them near 
the Permian * Seymour ia> which we shall consider as a cotylosaurian 
reptile (p. 386). 

Throughout the Carboniferous, Permian, and Triassic there were 
abundant amphibia of partly terrestrial habit, the Rhachitomi, in 
which both vertebral centra were present, the pleurocentrum being 
the larger. *Eryops (Fig. 211) was a typical form living in the Permian, 
about 250 million years ago. The animals were 5 ft or more in length, 
rather like crocodiles, relatively shorter in body and tail than *Eogy- 
rinus and with stronger limbs. Nevertheless they probably lived partly 
in the water and may have been fish-eaters. The skull was long and 
narrow in the front and short in the 'table' behind the eyes, continuing 
the previous tendency. A characteristic feature of later labyrinthodonts 
now began to appear, namely a dorso-ventral flattening of the skull. 
The pectoral girdle was no longer attached to the skull, but there was 
a joint between the pelvic girdle and the sacrum. Some Permian 
Rhachitomi became still more completely terrestrial than *Eryops, 
for instance *Cacops had very large limbs and protective plates along 
its back. 

3. Aquatic Amphibia of the later Palaeozoic 

Other lines of amphibia, however, show an accentuation of the 
tendency to return to the water. In the vertebrae the anterior hypo- 
centrum became large, while the pleurocentrum disappeared. At the 
same time the skull became very flattened and the limbs weak. Several 
stages are known leading from the Rhachitomi to these fully aquatic 
forms of the Trias, which are placed in the suborder Stereospondyli. 
*Capitosaurus and *Buettneria are typical of the group, which 
remained numerous until near the end of the Triassic period, about 
150 million years ago. Probably this change from rhachitomous to 
stereospondvlous condition occurred on several independent lines of 
descent. Thus amphibia, after becoming semi-terrestrial in the Car- 
boniferous and then probably giving rise to the early reptiles, later 
returned to the water. 

We also have record of various other secondarily aquatic amphi- 




Polype dates 

Ran a 

Fig. 210. Various anuran amphibians, not all to one scale. 

(Ascaphus, Nectophrynoides, and Polypedates after Noble, Breviceps after Thompson, 
Gastrotheca after B.M. Guide, others from life.) 


bians whose affinities are less certain. They have in common a reduc- 
tion of ossification in general and in particular in the centra, which 
seem not to be formed from separate cartilaginous elements as in 
labyrinthodonts but as thin continuous sheets of bone. Some of these 
animals classed as Phyllospondyli or 'Branchiosaurs' were almost 
certainly larval Rhachitomi; the external gills can be recognized and 
stages found connecting them with known adults of that group. It is 
necessary, however, to retain the order for the present. 

Other early aquatic amphibia are less easy to classify and are 
grouped for convenience as an order Lepospondyli, all having verte- 
brae composed of a single piece, and a continuous notochord. They 
show, however, at least three distinct lines, probably separate off- 
shoots from the main labyrinthodont stock. *Dolichosoma and other 
forms from the Carboniferous were like snakes and had lost the limbs. 
*Diplocaulus from the Permian possessed remarkable horned skulls. 
These creatures with broad flat heads and upward-looking eyes and 
small limbs were presumably bottom-dwellers and the development 
parallels that of the Stereospondyli. A third aberrant group placed 
here, the Microsaurs, such as *Microbrachis, were animals with long 
bodies and small limbs, presumably aquatic, but showing many 
similarities to the reptiles in the skull. 

The order Adelospondyli has been created for a further collection 
of presumably secondarily aquatic amphibia such as *Lysorophus, in 
which the neural arch and centrum are not fused but articulate by 
means of a jagged suture. The skull shows reduction and variation 
of the bones, and for this and other reasons it has been suggested that 
the urodeles may have arisen from an adelospondylous line. 

The relationship of the modern amphibia to these palaeozoic 
stegocephalians remains uncertain. The earliest anuran is *Proto- 
batrachus of the Triassic, possessing ribs and a tail, but with elongated 
ilia and an anuran type of skull. It is probably a larva in metamor- 
phosis. *Miobatrachus of the Carboniferous is a form in which the 
posterior portion of the skull is shortened and the temporal bones lost. 
In other respects the skull is like that of a rhachitome and suggests 
that the frogs diverged from the labyrinthodonts at this very early 

The urodeles can be traced back only to the Jurassic. It is often 
suggested that both they and the Apoda have arisen from aquatic 
Lepospondyli, such as the microsaurs, but there is no real evidence 
of this. 

362 AMPHIBIA xiii. 4 

4. Tendencies in the evolution of fossil Amphibia 

The changes in the form of amphibia can be followed from the 
beginning of the Carboniferous to the end of the Triassic period, and, 
indeed, in the form of their reptilian descendants far beyond. There 
are signs, however, of very many distinct lines (as we should expect), 
and it is not possible to trace details of the history or fate of par- 
tieular populations. Two distinct tendencies appear over this period: 
(i) to become fully terrestrial, (2) to return to the water. The terres- 
trial forms became very gradually shorter in body and stronger in leg. 
The skull remained fairly high and domed and the otic notch became 
deeper, as a more effective tympanum developed. In the vertebrae 
the hypocentrum became reduced as muscles developed attached to 
the pleurocentrum. 

Return to the water led to animals of two distinct types, (a) snake- 
like or (b) flattened, but in both there was a reduction of limbs and 
a secondary lengthening of the body, with return to the sinuous 
movements of fish-like locomotion. In the bottom-living forms, such 
as some Stereospondyli and *Diplocaahis among Lepospondyli, the 
skull became flattened, with the eyes looking upwards, the otic notch 
being shallow. The snake-like *Dolichosoma retained the more normal 
skull shape but became immensely elongated and lost the limbs 

These observed tendencies can be understood to result from the 
situation that developed as the vertebrates first colonized the land. 
The earlier amphibia, such as *Eogyrinus, were partly aquatic, by 
force, one might say, of inexperience. Throughout the Carboniferous 
various lines of them became more fully equipped for terrestrial life, 
moving faster, seeing and hearing better, and so on. The competition 
and predatory attacks of these more successful lines then drove others 
back into the water and so the process continued, until later the earlier 
reptilian lines, themselves driven back to the water by their own 
descendants, removed most of the amphibians from the waters as 
well as from the land, leaving only some few remaining populations, 
from which the modern orders have evolved. 

It certainly does not seem necessary to postulate any special 
directive force to explain all this. We could wish, of course, for 
much more information, but it seems reasonable to imagine that 
these changes were produced by the action of the animals with each 
other and with the environment, supposing that the animals con- 
tinually strive to feed, grow, and reproduce others rather, but not 
quite, like themselves. 



Fig. 2ii. Chart of evolution of amphibia. 

364 AMPHIBIA xiii. 4- 

It must be stated, however, that Watson, who has contributed more 
than anyone to knowledge of amphibian evolution, believes that it is 
possible to recognize a number of non-adaptive trends, which are 
independent of environmental influences. Changes suggested by 
Watson and others as non-adaptive include flattening of the skull, 
doubling of the occipital condyles, reduction of the number of roofing 
bones and loss of ossification in the neurocranium, the changes in the 
vertebrae already mentioned, and many other features. It is not 
entirely clear how the 'non-adaptive' nature of these features is estab- 
lished. SevertzofT has suggested that the flattening of the head is 
connected with the development of a large mouth for buccal respira- 
tion. Palaeontology necessarily deals with small points of structure, 
whose significance for the animal may be difficult to determine, but 
it does not follow because we are not able to discern the significance 
of a part that it therefore has none. It is not at all easy in biology to 
hold the balance between credulous acceptance of a function for 
every character and a sceptical attitude that insists on regarding the 
organic world as a jumble of unrelated substances. The only safe rule 
is to search continually for signs of regular recurrence of similarities 
of structure and action, and then to make hypotheses about function, 
which can be tested by experiment. 

5. Newts and Salamanders. Subclass Urodela 

The urodeles, also called Caudata or tailed amphibia, show less 
deviation from the general form and habitats of the amphibia as a 
whole than do the specialized anurans (Fig. 209). The adult and larval 
urodeles differ little from each other, and characters suitable for 
aquatic life are frequently found in the adult. Indeed, all stages of 
suitability for land occur, from the terrestrial salamanders, such as 
Salamandra maculosa, the European salamander, which is viviparous, 
to the fully aquatic forms, for instance Necturus, the mud-puppy of 
North America. In many of the aquatic animals there is a tendency to 
retain in the adult characters usually found in larvae. This process of 
paedomorphosis has developed to various extents, and independently 
in several groups. Thus the giant salamander Megalobatrachus, 5! ft 
in length, in China and Japan, has no eyelids, but loses its gills in 
the adult. In Cryptobranchus, the hell bender of the United States, 
the spiracle remains open and is used for the outlet of water during 

Amphiuma, also from the southern U.S.A., is a very elongate form, 
with absurdly small legs, no eyelids, and four branchial arches. In 

xiii. 6 MODERN AMPHIBIA 365 

the still more modified forms, such as Necturus, external gills are 
present and the lung is so reduced that the animals can live walking 
along the bottom. Proteus from European caves is a blind urodele 
with external gills and no pigment. Siren shows almost entirely larval 
characteristics and has no hind limbs. 

The more typical terrestrial newts are of several sorts. In North 
America the common genus Amby stoma (usually written Amblystoma) 
has eleven species, many adapted to special habits, including A. mexi- 
canum, in which some races become mature without metamorphosis, 
because of lack of iodine in the water, whereas others, the axolotls of 
Mexico, are genetically neotenous. 

The common British newt Triturus vulgaris is a typical example of 
the more definitely terrestrial urodeles, though it is not able to live in 
very dry situations. However, the limbs support much of the weight 
of the body, and their soles are applied to the ground and turned 
forwards. The tail shows various degrees of reduction to a circular 
organ, but in the breeding-season, when both sexes return to the 
water, it develops a large fin, especially in the male. The common 
newts of America form a distinct family, including Plethodon and 
many specialized forms, such as the blind Typhlomolge, inhabiting the 
waters of caves. 

6. Frogs and Toads. Subclass Anura 

Among the frogs and toads are very many suited for special modes 
of life, and it must again be emphasized that this is far from being a 
static and precariously surviving group. We have already mentioned 
the frog Ascaphns, which lives in mountain streams in the north-west 
of the United States and has reduced lungs, showing a combination 
of specialized and primitive features. Internal fertilization is assured 
by a penis-like extension of the cloaca. In this genus and the New 
Zealand Leiopelma (Fig. 210) there are several primitive features, 
including tail muscles (absent in all other anurans), amphicoelous 
vertebrae, free ribs, abdominal ribs, and persistent posterior cardinal 

In Alytes y the midwife toad of Europe, the male carries the eggs 
wrapped round the legs. Pipa is a related and still more specialized 
aquatic frog from South America; it has no tongue, and, curiously 
enough, has developed an elaborate arrangement by which the young 
are carried in pits on the back. Xenopus of Africa is related to Pipa, 
but without the habit of carrying its young (Fig. 210). 

The bufonid toads are among the most successful of all amphibian 

366 AMPHIBIA xm. 6- 

groups and are more fully adapted than most for a terrestrial life, but 
return nearly always to the water to breed. Bufo itself is found in 
almost all possible parts except in Australia and Madagascar; related 
genera, many of them with special features, are found all over the 
world. Curiously enough only one genus, Nectophrynoides from East 
Africa, is viviparous, the young being in that case provided with a 
long vascular tail, by means of which they maintain contact with the 
wall of the 'uterus', even though embedded in a mass of embryos. 

Hyla and other tree-frogs, very widely distributed, are similar to 
the bufonids but have pads on the toes by which they climb, and 
many other adaptations to arboreal life. Gastrotheca (= Nototrema), 
the marsupial frog, is a genus in which the young develop in a sac on 
the back of the female, this sac being in one species protected by 
special calcareous plates. Rana and its allies, the true frogs, are also 
cosmopolitan. A number of frogs related to Rana have taken to a tree- 
living habit, developing pads on the toes. Polypedates is a widespread 
genus and there are several others, each independently derived from 
ranids. This is therefore a striking illustration of parallel evolution — 
the hylid tree-frogs having arisen from bufonids and probably several 
sorts of polypedatids from ranids. 

Burrowing with the legs has also been evolved several times by 
anurans. In Breviceps (Fig. 210), which digs for ants, there is a large 
snout, as in other anteaters. 

7. Subclass Apoda (= Gymnophiona = Caecilia) 

These (such as Ichthyophis) are burrowing, limbless creatures living 
like earthworms, in the tropics. They show several interesting primi- 
tive features, including the retention of small scales in the skin. They 
are specialized, however, in having a very short tail and some features 
suited to their terrestrial life, such as copulatory organs. The animals 
are blind, the place of the eyes being taken by special sensory ten- 
tacles. The eggs are large and yolky and cleavage is meroblastic; they 
are laid on land and the embryos develop around the yolk sac, but 
often have long, plumed gills. Vivipary is common, including in the 
aquatic form Typhlonectes. 

8. Adaptive radiation and parallel evolution in modern Amphibia 

Even this superficial study of the 250 genera and about 2,000 species 
of modern amphibians shows that the features we have already 
recognized in fish evolution are found also in evolution on land. It is 
difficult in a short time to gain an impression of the very great variety 


that is characteristic of any group of animals when closely studied. 
Besides the main types that can be distinguished, countless lesser 
variations will be found, and one realizes that the characteristics of the 
populations are still today in process of continual and perhaps rapid 
change. Anyone trying to discover the relationships of the various 
derivatives of ranids or bufonids must be impressed by the presence 
of series of parallel lines of development, so that it is impossible to 
disentangle the relationships. Evolution viewed at close quarters by 
the student of abundant modern animals looks very different from 
the simple picture seen by the lucky collector of a few rare fossils, 
who can arrange his types in genealogical trees and is apt to forget that 
they represent only an infinitesimally small sample of abundant and 
varied populations. 

We can perhaps find certain tendencies in the modern amphibian 
populations that are similar to the tendencies of the fossil series. Many 
return to the water, especially among the urodeles. Others become 
more fully terrestrial, either by climbing trees or by burrowing into 
the earth. Both these habits have been independently adopted many 
times by recently evolved lines and, no doubt, still more often in the 
past by creatures that have died out, leaving no trace. 

9. Can Amphibia be said to be higher animals than fishes? 

It is not easy to decide whether there is a clear sense in which 
amphibians can be said to have advanced over their fish ancestors. 
They have moved from the water into environments that are in a 
sense less suitable for life. In order to maintain a watery system, such 
as a frog or toad, outside the water, various special structures and 
methods of behaviour have been evolved. The presence of such 
additional systems can be said to add complexity to the organization. 
It is difficult to make a count of the number of 'parts' involved in the 
organization of any animal. Amphibia possess many special devices, 
for instance, for respiration without loss of moisture, for control of 
water intake and water loss, for return to water to breed, and so on. 
Even without making a proper quantitative computation it seems 
reasonable to say that these add up to make an organization more 
complicated than that of a fish. The integration of the action of so 
many parts requires an elaborate nervous system, and there is evi- 
dently some connexion between the increased size and importance of 
the nervous system and the development of this more complicated 
organization that enables life to continue in a different environment. 

Considering the matter in this way it is hardly sensible to ask the 

368 AMPHIBIA xm. 9 

question 'Are the amphibians more efficient than the fishes?', the 
work that they do in maintaining life is so different that a comparison 
of 'efficiency' is fallacious. One method of assessing living efficiency 
might be to judge each animal organization by the extent to which it 
maintains its constancy — by its power of homeostasis. Data about the 
fluctuations of the internal environment are so scanty among lower 
vertebrates that we cannot proceed very far on these lines. It is 
probable that the blood of fishes shows greater fluctuations, for 
instance in osmotic pressure or lactic acid content, than does that of 
amphibians, such fluctuations being perhaps even an advantage in 
allowing life in waters of differing salinity. In fact, to say that the 
whole mechanism of homeostasis becomes more complicated in land 
animals is only to say over again that they are 'higher' because they 
have more special work to do to maintain themselves in a difficult 
environment. Almost every part of the body shows signs of this greater 
complexity; the central nervous system becomes larger, the autonomic 
nervous system develops more elaborate control of the viscera. The 
endocrine glands become more numerous and differentiated, the 
muscular system shows more distinct parts, enabling the animal to 
act in new ways. 

However difficult such comparisons may be it is hardly possible 
to deny them some validity. Amphibian organization differs from 
that of fishes and may be said to be 'higher' in the sense that it is more 
elaborate and allows life in conditions that the fish organization 
cannot tolerate. 



1 . Classification 

Class. Reptilia 
Subclass i. Anapsida 

Order i. *Cotylosauria. Carboniferous-Trias 

*Seymouria; *Captorhimis; *Diadectes 
Order 2. Chelonia. Permian-Recent 

*Eunotosaurus; *Triassochelys; Chelys; Emys; Chelone; 


Subclass 2. *Synaptosauria 

Order 1. *Protorosauria. Permian-Trias 

*Araeoscelis; * Tanystropheus 
Order 2. *Sauropterygia. Trias-Cretaceous 

*Lariosaurus; *PHosaurus; *Plesiosaurus; *Placodus 

Subclass 3. # Ichthyopterygia 

Order 1. *Ichthyosauria. Trias-Cretaceous 
*Mixosaurus; * Ichthyosaurus 

Subclass 4. Lepidosauria 

Order 1. *Eosuchia. Permian-Eocene 

* Yoimgina; *Prolacerta 
Order 2. Rhynchocephalia. Trias-Recent 

*Homoesaurus; * Rhynchosaurus ; Sphenodon (= Hatteria) 
Order 3. Squamata. Trias-Recent 

Suborder 1. Lacertilia (= Sauria). Trias-Recent 
Infraorder 1. Gekkota. Mainly Recent 

Infraorder 2. Iguania. Cretaceous-Recent 
Iguana; Anolis; Phrynosoma; Draco; Lyriocephahis ; Agama; 

Infraorder 3. Scincomorpha. Eocene-Recent 
Lacerta; Scincus; Amphisbaena 
Infraorder 4. Anguimorpha. Cretaceous-Recent 
*Dolichosaurus; * Aigialosaurus ; *Tylosaurus; Varanus; Lan- 
thanotus; Atwuis 


REPTILES xiv. i- 

1. Classification {cont.) 

Suborder 2. Ophidia (= Serpentes). Cretaceous-Recent 
*Palaeophis; Python; Natrix; Naja; Vipera 

Subclass 5. Archosauria 

Order 1. *Pseudosuchia (= *Thecodontia). Trias 

*Enparkeria; *Saltoposuchns 
Order 2. *Phytosauria. Trias 

*Phytosaurus; *Mystriosuchus 
Order 3. Crocodilia. Trias-Recent 

*Protosuchus; Crocodilus; Alligator; Caiman; Gavialis 
Order 4. *Saurischia. Trias-Cretaceous 
Suborder 1. *Theropoda 

*Compsog?iathus; *Ornitholestes; * Allosaurns ; *Tyranno- 
saurus; * Strnthiomimus 
Suborder 2. *Sauropoda 
*Apatosaurus (= *Brontosaurus); *Diplodocus; *Yaleosaurus; 
*Plateosanrus; Brachiosaurus 
Order 5. *Ornithischia. Trias-Cretaceous 
Suborder 1. *Ornithopoda 

*Camptosaurus; *Iguanodon; *Hadrosaurus 
Suborder 2. # Stegosauria 

* Stegosaurns 
Suborder 3. *Ankylosauria 

* Ankylosaurus ; *Nodosanrus 
Suborder 4. *Ceratopsia 

* Triceratops 

Order 6. *Pterosauria. Jurassic-Cretaceous 
*Rhamphorhynchns ; *Pteranodon 

Subclass 6. *Synapsida. Carboniferous-Permian 

Order 1. # Pelycosauria (= # Theromorpha) 

* Varanosaurus; *Edaphosaurus; *Dimetrodon 
Order 2. *Therapsida. Permian-Jurassic 

*Scym?iognathus; *Cyiiognathus; *Bauria; *Dromatherium; 
* Dicynodon 
Order 3. *Mesosauria (— Proganosauria). Permian 

xiv. 2 (370 

2. Reptilia 

Towards the end of the Devonian period, say 350 million years 
ago, the vertebrate organization produced a population of amphibian 
creatures and from this has been derived not only various modern 
groups classed as amphibia but also the more fully terrestrial popula- 
tions that do not need to breed in water — the Amniota. Since that 
time many divergent lines have evolved from this stock, including the 
birds and the mammals, and it is evident, therefore, that it is likely to 
be difficult to specify what is meant by a reptile, as distinct from an 
amphibian or a bird or mammal. The term does not define a single 
vertical line of development or branch of an evolutionary tree, but 
is rather a horizontal division, marking a band on the evolutionary 
bush, specifying a level of organization beyond that of an amphibian 
but before that of either bird or mammal. Attempts have been made 
to divide the reptiles vertically into sauropsidan (bird-like) and 
theropsidan (mammal-like) lines, but such a division, although it has 
some foundation, obscures the fact that their bush-like evolutionary 
radiation has produced not two but many types. 

The existing reptiles belong to four out of the dozen or more main 
lines that have existed. The most successful modern forms are placed 
in the order Squamata, the lizards and snakes, the latter being of 
relatively recent appearance in their present state. Secondly, the 
tuatara, Sphenodon, of New Zealand is a relic surviving with little 
change from the Triassic beginnings of this group. Thirdly, the 
crocodiles are an older offshoot from the stock from which the modern 
birds were derived. Finally the tortoises and turtles (Chelonia) have 
retained in some respects the organization of still earlier times, 
perhaps through the special protection of their shells. Though they 
are much modified in some ways, they still show us several character- 
istics of the earliest Permian reptiles. 

These four modern types are all that remain of the reptiles that 
flourished throughout the Mesozoic, culminating in the giant dino- 
saurs of the Jurassic and Cretaceous. Evidently a profound change 
affected the population of the world, including the sea, between the end 
of the Cretaceous and the Eocene. This change will be discussed 
further in Chapter XXI, but we must briefly discuss here the possible 
relation of the decline of the reptile populations to the rise of their 
descendants, the birds and mammals. It can hardly have been only 
the more efficient organization due to the warm blood that gave 
these their opportunity, for there were forms in the Trias so similar 

372 REPTILES xiv. z- 

to mammals in their skeletons that we may reasonably (though 
not certainly) suppose them to have been warm-blooded. There were 
birds with feathers in the Jurassic, and it is probable that they also 
already had warm blood. However, as a working hypothesis, we may 
suppose that the climate, which had been suitable for reptiles in the 
Mesozoic, became less so in the early Tertiary, and the most obvious 
suggestion is that colder conditions developed all over the earth's 
surface. The modern reptiles for the most part live in the temperate 
and tropical zones, indeed they flourish only in the latter. However, it 
must be remembered that climate fluctuates continually (p. 13); it is 
dangerous to make generalizations about conditions over such long 
periods as the Cretaceous. 

3. The organization of reptiles 

The organization we call reptilian is, generally speaking, suitable for 
life in warm countries, though two species, the common lizard 
(Lacerta vivipara) and the adder ( Vipera berus), are found as far north 
as the Arctic Circle. No doubt the distribution of reptiles is limited 
largely by the fact that they cannot maintain a temperature above that 
of the surroundings by production of heat from within. The wide- 
spread idea that reptiles have no means of regulating their body 
temperature, however, has been overemphasized. Bogert and his 
collaborators in the U.S.A. have shown that in the wild (though not 
as a rule under laboratory conditions) reptiles are often able by suitable 
behaviour to maintain their body temperatures at a remarkably high 
and constant level throughout much of the day, by varying their 
exposure to the available sources of heat. When they get cold they 
bask in the sun or rest on warm rocks; when they get too hot they 
shelter under vegetation or in holes. In some species, too, colour 
change plays a part in temperature control, the animals becoming 
darker or lighter in colour, according to whether heat absorption or 
reflection is the appropriate response. 

It has also been shown that each species of reptile has an optimum 
range of temperature, below which the animals become inactive and 
above which they quickly die. In some desert lizards the upper limit is 
above 40 C. The range tends, as one would expect, to be higher in 
diurnal than nocturnal forms, and is in general higher in lizards than 
it is in snakes or alligators. 

The reptilian method of temperature control differs essentially 
from that of mammals in that it depends on the availability of external 
sources of heat such as the sun, rather than on the ability to conserve 

xiv. 5 SKIN OF REPTILES 373 

or lose heat generated within the body. For this reason reptiles are 
sometimes termed 'ectothermic' and mammals 'endothermic'. These 
terms are perhaps preferable to 'poikilothermic' (having a variable 
temperature) and 'homoiothermic' (having a constant temperature) 
which are in more general use. 

The ectothermic method of temperature control presupposes some 
sensitive mechanism for registering slight changes in the temperature 
of the surroundings. There is evidence that the pineal complex is the 
receptor and that the hypothalamus may be involved in thermal 

It remains true to say, however, that no reptile can retain an inde- 
pendent body temperature for a long period. For this reason, reptiles 
living in temperate climes must hibernate during the winter, while in 
warm countries some, conversely, aestivate during the hottest months. 

4. Skin of reptiles 

The skin is characteristically dry; unlike the skin of amphibians and 
mammals it contains few or no glands. The Malphigian layer of the 
epidermis produces the horny scales, which are periodically shed in 
flakes, or, as in snakes, cast as a single slough. Beneath the horny 
scales many reptiles (some lizards, crocodiles, some dinosaurs) develop 
bony plates in the dermis (called osteoderms). These may be re- 
stricted to the head, where they lie superficial to the skull bones, or 
may cover most of the body. The tortoise's shell contains both horny 
(epidermal) and bony (dermal) components (p. 394). The horny 
scales are often modified to form crests, spines and other appendages. 

Many reptiles, particularly lizards and snakes, have bold and 
elaborate colour patterns. These may play a part in concealment 
(though they often seem conspicuous in captive specimens away from 
their normal terrain). In some forms, especially lizards, there are 
marked colour differences between the sexes (see p. 407). The well- 
known phenomenon of colour change, which is much more marked 
in certain lizards than in any other known reptiles, is discussed on 
p. 410. 

5. Posture, locomotion, and skeleton 

The elongated body and small laterally projecting legs of many 
reptiles recall those of a urodele, and the method of locomotion is in 
general similar in the two groups. Many retain the primitive five digits 
in both hand and foot. With the similarity of movement goes a general 
similarity in plan of the skeleton: there are, however, certain most 

374 REPTILES xiv. 5 

significant features, characteristic of the reptiles. The head is carried 
off the ground, on a well-developed neck. The two first cervical 
vertebrae are modified to form the atlas and axis. The atlas is a ring 
of bone without centrum, but with a facet in front for the occipital 
condyle and one behind for the odontoid process, a peg attached to 
the front of the axis but derived in development from the centrum of 
the atlas segment. 


Fig. 212. Shoulder girdle and sternum of a lizard (Iguana). 

el. clavicle; cor. coracoid; gl. glenoid; interclavicle; pr. procoracoid 
process; sc. scapula; st.r. sternal rib; St. sternum. (From Reynolds, after Parker.) 

The vertebrae articulate with each other by a system of interlocking 
processes much more elaborate than that found in fish-like vertebrates 
and presumably serving to allow the column to carry weight. As a 
rule, each centrum is concave in front, covering the convex hind end 
of the vertebra next to it, a condition known as procoelous. In aquatic 
vertebrates the centra articulate by flat surfaces and this condition was 
retained in the amphicoelous vertebrae of many primitive reptiles. 
Besides this articulation of the centra the vertebrae are also united by 
the zygapophyses, facets on the neural arches, so arranged that the 
upwardly facing surfaces of the anterior zygapophyses slide over the 
down-facing surfaces of the posterior zygapophyses, an arrangement 
that is found throughout the amniotes. 

Ribs are well developed in the middle or trunk region; each arti- 
culates with the body of the vertebra by a single capitular facet. 


The vertebrae can often be divided into four sets. The cervical 
vertebrae, which are very variable in number, have short ribs, not 
reaching the sternum. Sternal ribs occur in the thoraco-lumbar seg- 
ments (Fig. 212). The ribs of the two sacral vertebrae are short and 
broad and articulate with the ilia. The numerous caudal vertebrae 
show reduction of all parts, especially towards the tip of the tail. The 
chevron bones are ossicles attached to the caudal centra and represent- 
ing the reduced intercentra. 

The girdles and limbs (Figs. 183-6 and 212) show the same general 
structural and functional features as those of amphibia. The limbs 
form the main locomotor system, the metachronal contraction of the 
myotomes playing a lesser part than in urodele amphibians. The 
humerus and femur are normally held in such a position that their 
outer ends lie higher than the inner, that is to say, in a position of 
abduction. The radius and ulna and tibia and fibula proceed down- 
wards towards the ground (at right angles to the proximal bones) and 
the hand and foot are turned outwards at right angles, to rest on the 
ground. The main muscles thus draw the humerus and femur back- 
wards and forwards as well as downwards, and the ventral regions of 
the girdles are large and flattened to receive these muscles; in mam- 
mals, with a different system of progression, the more dorsal parts 
of the girdles have become developed. 

The pectoral girdle (Figs. 183, 212) consists of a dorsal scapula and 
a large ventral coracoid, which may be fenestrated. Distinct pro- and 
post-coracoid elements are probably only found in the extinct mam- 
mal-like reptiles. The dermal components are represented by the 
paired clavicles and median interclavicle. A cleithrum is found in a 
few very primitive forms. 

In the pelvic girdle (Fig. 184) the usual dorsal ilium, anterior pubis, 
and posterior ischium are found, the last two meeting their fellows in 
midline symphysis. 

The characteristic modifications of the reptilian skull are discussed 
on p. 391. The general plan is similar to that of primitive amphibians, 
but in all except the most primitive reptiles there is a development of 
holes (fossae) in the temporal region to provide space for the bulging 
temporal muscles. The skull roof is in some respects more primitive 
than that in modern amphibians (Figs. 213 and 214). It is made up of a 
large series of dermal bones, including the nasals, prefrontals, frontals, 
supra-orbitals, and parietals. The side of the skull is usually less com- 
plete, composed of the tooth-bearing premaxillaand maxilla, lacrymal, 
jugal, post-orbital, squamosal, supratemporal and quadrate. The 

376 REPTILES xiv. 5 

naming of some of the smaller bones round the orbit and above 
the quadrate is a matter of controversy. 

The margins of the palate are formed by flanges of the premaxillae 

Fig. 213. Skull and lower jaw of Lacerta. 

A, dorsal view; 13, ventral view; C, from left side; D, right half of lower jaw from inner 
side, showing the pleurodont arrangement of the teeth. E.P. ectopterygoid; Ep.P. epiptery- 
goid; F, Fr. frontal ; jug. jugal; Lac. lachrymal; Max. maxillary; N, Na. nasal; N, in B, 
inner narial opening; Pal. palatine; Par. parietal; Pmx. premaxillary ; Pr.f. prefrontal; 
Pt.f. post-orbital; Pt.f 2 . post-frontal; Ptg. pterygoid; Q. quadrate; S.ang. supra-angular; 
Sq. squamosal; '. 'o. vomer. The regions of persistent cartilage are not shown in detail. 

(After Gadow.) 

and maxillae and the small ectopterygoids. The internal nostrils 
usually lie forwards between the maxillae, vomers, and palatines. 
More posteriorly the floor of the skull is made up mainly by pterygoid 
bones and the parasphenoid, which is partly fused with the lower 
surface of the basisphenoid. Occipital bones surround the foramen 
magnum and make up the single occipital condyle, which in some 

xiv. 5 SKULL 377 

forms is indented to form three partly distinet lobes. In many reptiles 
there is an epipterygoid bone on either side of the brain-case behind 
the orbits; this is regarded as an ossification in the ascending process 
of the palato-quadrate. The lower jaw usually consists of six bones, 
the articular forming the joint with the quadrate, and the dentary 
carrying teeth. 

The anterior part of the chondrocranium, surrounding the front of 
the brain, and the nasal capsule, remain more or less unossified, and 

Fig. 214. Diagram of the skull of lizard to show temporal fossa. 

a. articular; an. angular; bo. basioccipital; bs. basisphenoid; c. coronoid; d. dentary; da. 
dermal articular; do. dermal supraoccipital; ept. ectopterygoid; eo. exoccipital ; fr. frontal; 
j. jugal; /. lachrymal; mx. maxilla; n. nostril; na. nasal; o. orbit; op. opisthotic; pa. parietal; 
pal. palatine; pv. prevomcr; pm. premaxilla; po. post-orbital; pof. post-frontal; pr. pro-otic 
pra. prearticular; pr}. prefrontal ;ps. presphenoid; pt. pterygoid; q. quadrate; qj. quadrato- 
jugal; sa. surangular; sf. upper temporal fossa (this is shown diagrammatically, as it occurs 
in many lizards; in Lacerta it is largely covered by an extension of the post-frontal — see 
Fig. 213); so. supraoccipital; sp. splenial; sq. squamosal; St. supratemporal; v. vomer. 

(From Goodrich.) 

in places may be membranous. There may, however, be small ossified 
orbitosphenoids and farther back pleuro- or laterosphenoids, which 
develop in the pila pro-otica uniting the orbital cartilage with the 
otic capsules. Between the eyes there is in most reptiles a thin sheet 
of cartilage known as the interorbital septum, which may be partly 
ossified by small presphenoid elements. The posterior part of the 
chondrocranium ossifies to form the following bones; occipital com- 
plex, basisphenoid, and the ossifications in the otic capsule (pro-otic, 
opisthotic, &c). 

In many reptiles the upper jaw and front part of the skull can move 
to some extent in relation to the occipital region and cranial base, 
such movement being termed kinesis (p. 405). This is often associated 
with mobility of the quadrate, as in lizards, snakes, and certain dino- 
saurs. Kinesis helps to widen the gape and may provide a shock- 
absorbing effect when the jaws are snapped together. 

The postmandibular visceral arches play no part in jaw support but 
are incorporated into the ear and hyoid apparatus. There is a rod-like 

378 REPTILES xiv. 5- 

columella auris with a small cartilaginous element (extra-columella) 
at its outer end. The columellar system usually conducts vibrations 
from the tympanum, lying behind the quadrate, to the fenestra ovalis 
and inner ear. In some forms, e.g. snakes, however, the tympanum is 
absent and the outer end of the columella is applied to the quadrate. 
These animals may be deaf to air-borne sounds but sensitive to 
ground vibrations, transmitted through the bones of the jaw. 

The hyoid apparatus consists of a basal plate, which projects into 
the tongue, and three pairs of ascending horns. These represent the 
remains of the hyoid and branchial arches. 

6. Feeding and digestion 

Food is seized either by the teeth or, in some specialized lizards 
such as the chameleon, with the elongated tongue. The teeth are 
situated along the edges of the jaws and often also on some of the 
bones of the palate. Typically, they are all of the same conical shape, 
but may be slightly serrated, or modified to form crushing plates, 
poison fangs, and other devices. As a rule, tooth succession is con- 
tinuous throughout life, though exceptions to this are found among 
the lizards. Salivary glands are well developed in some forms; in 
snakes and one genus of lizards (Heloderma) some of them are modified 
to form poison-glands. The tongue is very variable, being hardly 
movable in some reptiles (e.g. crocodiles) but long, forked, and highly 
mobile in others (e.g. snakes). 

Digestion proper begins in the stomach. The alimentary canal is 
built on the typical vertebrate plan, with a tubular stomach, rather 
short small intestine, and wider large intestine, leading to a short 

There is a well-marked cloacal chamber in all reptiles, subdivided 
into a coprodaeum for the faeces, and a urodaeum for the products of 
the kidneys and genital organs. These two chambers open into a final 
common proctodaeum, closed by a cloacal sphincter. This division 
of the cloaca is associated with the necessity for the retention of water, 
the cloacal chambers serving for water reabsorption from both the 
faeces and urinary excreta (p. 380). 

7. Respiration, circulation, and excretion 

The typical method of respiration is a backward movement of the 
ribs, produced by the muscles attached to them. There is no complete 
separation of the thorax from the abdomen, but a partial diaphragm 
may be present. The glottis is a slit at the back of the mouth and leads 

xiv. 7 CIRCULATION 379 

into a larynx with supporting cricoid and arytenoid cartilages. Many 
reptiles are able to produce small sounds, but the voice-box is less 
developed than in either amphibia or birds. 

The lungs are sacs whose walls are folded into ridges, separating 
a number of chambers or bronchioles. The hinder part of the lung is 

car. int. 

car. ex t. 

Fig. 215. Diagram of heart and arteries of Lacerta. 

car.ext. external carotid; car. int. internal carotid; common carotid; coel. coeliac artery; 

d.a. dorsal aorta; d.B. ductus Botalli (arteriosus); ductus caroticus; l.aur. left auricle; 

p.a. pulmonary artery; p.v. pulmonary vein; r.aur. right auricle; scl. subclavian artery; 

sept, interventricular septum; v.c. eaval veins. (From Ihle, after Goodrich.} 

nearly smooth and in some lizards, as in birds, it becomes developed 
into characteristic air sacs. The tendency is for the more anterior por- 
tion of the lung to become the effective vascular and respiratory region, 
allowing the air-stream to be drawn across it at both inspiration and 

The circulation (Fig. 215) of lizards shows a partial separation of 
venous and arterial blood; there are two auricles, but only one ven- 
tricle, this being partly divided by a septum into right and left sides. 
Three arterial trunks arise directly from the ventricle, these being the 

380 REPTILES xiv. 7- 

right and left aortae, and the pulmonary trunk. The opening of the 
latter lies opposite the right side of the ventricle and receives pre- 
dominantly venous blood. The left systemic arch opens opposite to 
the incomplete ventricular septum and receives mixed blood, whereas 
the right systemic arch opens from the left side of the ventricle and 
carries almost pure arterial blood. The carotid arteries of both sides 
arise from the right systemic arch. This 'classical' view of the cir- 
culation of the blood in the reptilian heart has recently been confirmed 
by the radiographical studies of Foxon and his colleagues on the green 
lizard. Variations may be found, however, in different species. 

The venous system is based on the same plan as that of the frog, 
with pelvic veins receiving blood from the tail and hind legs and 
returning it to the heart through either an anterior abdominal vein 
or renal portals, and the inferior vena cava. 

In the urinogenital system is seen another feature characteristic of 
amniotes, the development of a posterior region, the metanephros, 
concerned solely with excretion, leaving the mesonephric (Wolffian) 
duct to function as the vas deferens in the male. There is sometimes 
an endodermal (allantoic) bladder. 

The waste nitrogen is largely excreted as uric acid and this allows 
the reabsorption of much of the water in the urodaeum, with precipita- 
tion of the organic matter as a chalky white mass of urates. The 
advantage of this method of excretion is that it allows for a greater 
economy of water than would be possible if the end product was the 
more soluble urea. There is, however, some variation in the mode of 
excretion among certain members of the group and this may depend 
on the manner of life of the species and the necessity for water con- 
servation. Thus among Chelonia the more aquatic forms (Emys) pro- 
duce considerable amounts of ammonia and urea, but relatively little 
uric acid, whereas the last is the main excretory product of the fully 
terrestrial types, such as the Grecian tortoise (Testudo gracca), which 
can live under almost desert conditions. 

8. Reproduction of reptiles 

Fertilization has become internal, and in all modern reptiles except 
Sphenodon special organs of copulation derived from the cloacal wall 
are developed in the male. In crocodiles and tortoises there is a single 
median penis, but in lizards and snakes there are a pair of these struc- 
tures, though only one is inserted at a time. The mechanism of erec- 
tion involves both muscular action and vascular engorgement. The 
sperms pass from the vasa deferentia into the urodaeum, and after 

xiv. 8 REPRODUCTION 381 

traversing this region they are carried into a groove along each penis. 
In snakes the sperms may survive within the female for long periods, 
and instances are known of isolated individuals laying fertile eggs 
after months, sometimes even years, in captivity. 

Some of the most serious difficulties in the colonization of the land 
are concerned with reproduction, and these problems have been 
largely solved in the reptiles, allowing the animals to reproduce with- 
out returning, as many amphibia must do, to the water. 

The eggs of oviparous reptiles are always laid on land. They there- 
fore require a firm physical support and protection against desic- 
cation, as well as an adequate supply of food and special means of 
gaseous exchange and storage of waste products. These requirements 
are met by the development of a shell, secreted by the walls of the 
oviduct and often hardened by lime impregnation, by the formation 
of special embryonic membranes, the amnion and allantois, and by 
the provision of a large quantity of yolk enclosed in a bag, the yolk- 
sac. The method of embryonic cleavage is affected by the great 
amount of yolk, and as in birds is only partial. An albumen or egg- 
white layer is present in the eggs of crocodiles and tortoises and pre- 
sumably serves as a reservoir of water; in the eggs of lizards and 
snakes, however, the albuminous layer is poorly developed or absent. 

The formation of the amnion and allantois is one of the most 
remarkable features of the development of reptiles ; it is characteristic 
of all higher vertebrates, distinguishing them sharply from the lower 
types. The amnion is developed from folds, which cover the embryo 
and enclose a sac filled with fluid, where development can proceed 
in the absence of the pond that was necessary for the earlier verte- 
brates. The allantois began as an enlarged bladder, serving for the 
reception of the waste products during the life within the shell. Coming 
close to the surface and fusing with the chorion, it then becomes the 
vehicle for the transport of oxygen to the embryo. 

The evolution of eggs and embryonic membranes of the kind de- 
scribed must have been an event of critical importance in tetrapod 
history. Romer has suggested that this advance took place under 
climatic conditions of alternate drought and flooding, so that eggs 
laid above the high-water mark had the best chance of survival. Since 
many of the early reptiles are thought to have spent much of their 
time in the water, it is possible that the egg preceded the adult in the 
process of adaptation to terrestrial life. 

Most reptiles lay their eggs, but in many lizards and snakes these 
are retained within the oviduct until the young are ready or nearly 

382 REPTILES xiv. 8- 

ready to hatch (e.g. Lacerta vivipara, Anguis fragilis, Vipera berus). 
This method of reproduction is termed ovoviviparous ; in forms that 
practise it the eggshell is reduced to a thin membrane or is lost 
altogether. In some species (e.g. certain skinks and other lizards, 
sea-snakes) a placenta is developed from the chorio-allantois or the 
yolk-sac or both. The placenta may, as in Lacerta vivipara, serve only 
for the transfer of water and gases, but in the more advanced forms it 
probably provides a means of transport for food (supplementing the 
yolk) and excretory products. 

Young born alive are perhaps less susceptible to the hazards of 
weather than those left to hatch in the sun or among rotting vegeta- 
tion, and it is interesting that most, if not all, of the few reptiles that 
live in places where the climate is really severe are ovoviviparous. 

Young reptiles have special devices to assist their escape from the 
egg. In Sphenodon, Chelonia, and Crocodilia, as in birds, there is a 
horny epidermal egg-breaker on top of the snout tip, called the egg- 
caruncle. In the Squamata, a true egg-tooth, projecting from the front 
of the upper jaw, has the same function. The egg-tooth is present, 
though sometimes rudimentary, in ovoviviparous forms. 

Some reptiles make a simple nest but the group is not noted for 
maternal care, usually abandoning their new-laid eggs or newborn 
young. There are, however, some exceptions to this; female pythons 
and certain other snakes and lizards brood their eggs, and female 
alligators are said to guard their nests. 

Many reptiles exhibit well-marked courtship and display pheno- 
mena during the breeding-season, the males fighting and displaying, 
either to intimidate each other or to evoke a suitable response from 
the female. This is particularly striking in certain lizards, notably 
those of the iguanid and agamid groups, where the males are often 
brightly coloured and may be adorned with crests and distensible fans 
under the throat. In these lizards bobbing movements of the head 
and front part of the body, often accompanied by colour change, form 
an important part of the display. As in birds, courtship may be associ- 
ated with territory, a male holding an area of ground on which females, 
but not rival males, are tolerated. Breeding behaviour and sexual 
coloration are, of course, under the control of the endocrine system, 
especially the anterior pituitary and the gonads, and may be modified 
by castration. The onset of the breeding season is also influenced by 
climatic conditions; most reptiles breed only once or twice a year, 
but a few species living in warm stable climates may breed at intervals 
nearly all the year round. 

XIV. 9 (3 8 3) 

9. Nervous system and receptors of reptiles 

All the modifications of structure that fit the reptiles for life on 
land would be useless without the development of appropriate be- 
haviour. This in turn depends on suitable structure and function of 



<?** warn 


Fig. 216. Three views of the brain of a lizard. 

cereb. cerebellum; cer.h. cerebral hemispheres; hypoph. hypophysis; 

hypoth. hypothalamus; olf.b. olfactory bulb; tect.opt. tectum opticum; 

II— XII, cranial nerves. (After Frederikse.) 

the nervous system. The brain accordingly shows some interesting 
developments. The cerebral hemispheres are relatively larger in 
reptiles than in amphibians (Fig. 216). The increased bulk lies mainly 
in the basal parts of the hemisphere (the corpus striatum), as in birds 
(Fig. 217). The roof (pallium) is little developed and lacks the elabor- 
ate cortical differentiation found in mammals. The thalamus is well 
developed and receives connexions from the optic tracts, which no 
longer run mainly to the midbrain. There are also many fibres from the 
thalamus to the cerebral hemispheres. This, together with the other 
features mentioned, may be evidence for the transfer of many nervous 

384 REPTILES xiv. 9 

functions from lower levels of the nervous system to the cerebral 
hemispheres, a process that has been carried much farther in mam- 
mals. In most respects, however, the brains of modern reptiles are 
more like those of birds than of mammals. 

The behaviour of reptiles, despite the elaborate courtship of some 
forms, remains of a relatively stereotyped character. The eyes are 
usually the main exteroceptive sense-organs and are usually provided 

co it dors. 

cort. hipp. 
sutc Llm 

cert Cat 



Fig. 217. Transverse section through forebrain of Lacerta. 

archistr. archistriatum (upper part of corpus striatum); cort. dors, dorsal cortex; cort. hipp. 
medial (hippocampal) cortex; lateral (pyriform) cortex; palaeostr. paleostriatum 
(basal part of corpus striatum); sept, septum; sidclim. sulcus limitans. (After de Lange 

and Kappers.) 

with movable eyelids, including a third eyelid or nictitating membrane. 
The lacrymal and Harderian glands provide secretions that keep the 
surface of the cornea moist. The eye is supported in most reptiles by 
a scleral cartilage and a ring of bony scleral plates. Accommodation is 
produced by the striated ciliary muscles, so arranged that they cause 
the ciliary process to squeeze the lens, making its anterior surface more 
rounded (Fig. 218). In many reptiles the retina possesses both rods 
and cones, the latter predominating in diurnal types. 

The pineal complex is often well developed, and in Sphenodon and 
many lizards a 'pineal' or parietal eye is present with lens-like and 
retina-like components. In such forms there is a pineal foramen in 
the parietal bone near the fronto-parietal suture. Similar foramina 
are found in many fossil reptiles, especially the more primitive types. 
The function of the reptilian pineal is still rather obscure, but there 
is evidence that in lizards it registers solar radiations, and, perhaps 
by the secretion of hormones, influences the animal's thermoregula- 

xiv. g 



tory behaviour in exposing itself to sunlight. It is also possible that the 
pineal complex plays some part in the control of reproduction. 

In the majority of reptiles the olfactory region of the nose is quite 
well developed, but, except in crocodiles, there is only a single nasal 
concha. The organ of Jacobson (vomero-nasal organ), a specialized 
and sometimes separate region of the nose, innervated by a separate 



Fig. 218. Diagram to show the mechanism of accommodation in the eye of 


ap. annular pad of lens; bm. Brucke's muscle; bp. base plate of ciliary body; c. cornea; ch. 
chorioid; cp. ciliary process; 1. iris; lb. lens body; ot. ora terminalis; pi. pectinate ligament; 
s.s. sclera; sc. scleral cartilage; scs. sclerocorneal sulcus; so. scleral ossicle; sr. sensory retina; 
tbm. tendon of Brucke's muscle (continuous with inner layers of corneal substantia propria); 
//. tenacular ligament; z. zonule. (From Walls, The Vertebrate Eye.) 

branch of the olfactory nerve, is present in turtles, Sphenodon, and 
Squamata. In the latter it is usually very highly developed (see 
p. 405). 

The tympanum when present lies at the back of the jaws, sunk a 
little below the surface. The range of response to sound waves is not 
known in lizards, but the ears of certain tortoises are very sensitive 
to sound over a narrow range of about no cycles per second; appar- 
ently there is some resonating mechanism, perhaps the columella auris, 
which vibrates at this frequency. Generally speaking, the sense of 
hearing is best developed among reptiles in the Crocodilia and certain 



1. The earliest reptile populations, Anapsida 

The organization of a reptile is well suited to maintain life on land. 
Many features show a considerable advance in this respect over the 
amphibia, for example, the dryness of the skin, the method of repro- 
duction, and the devices for economizing in the use of water. The 
immense radiation of the reptiles into every sort of land habitat during 
the Mesozoic period shows the efficiency of these mechanisms, which 
were probably present, at least in imperfect form, in the earliest Car- 
boniferous and Permian offshoots from the ancestral Stegocephali 

(P- 356). 

We have sufficient knowledge to be able to trace the early stages of 
reptilian evolution with considerable certainty. An animal known as 
*Seymonria i found in the lower Permian of Texas (perhaps 250 million 
years old), is of critical importance in our understanding of reptile 
origins (Figs. 219, 220). It was a lizard-like creature, about 2 ft long, 
probably living on insects and perhaps some larger animals. Its charac- 
teristics are so exactly intermediate between those of amphibians and 
reptiles that it is not possible to place it definitely with either group ; 
many zoologists class it with the Amphibia. This intermediacy is 
shown in almost every structure of the body and is often a subtle 
matter of the shape or size of the parts. Although a list of anatomical 
features is apt to give an unreal picture of any living organization it is 
the only method available to us in the absence of any more ingenious 
calculus, and we may therefore give first some of the characteristically 
reptilian features of *Seymouria. (1) The neural arches of the verte- 
brae were convex dorsally so that they have a 'swollen' appearance 
which is also seen in early reptiles; (2) a canal for the lachrymal duct 
was present; (3) the occipital condyle was single; (4) the pectoral 
girdle possessed a long interclavicle; (5) the pelvic girdle was attached 
to the vertebral column by two sacral vertebrae ; (6) the blade of the 
ilium was expanded for the attachment of the large muscles used in 
walking; (7) there were five digits in the hand instead of four as in 
many labyrinthodonts and in living amphibia; (8) the phalangeal 
formula was 2:3:4:5:3 or 4, approximating to the reptilian, rather 
than the usual labyrinthodont condition, in which the phalanges are 
less numerous. 

Fig. 219. Skeleton of Seymouria. Actual length 20 in. 
(From Williston, Osteology of the Reptiles, Harvard University Press.) 

Fig. 220. Skull and pectoral girdle of Seymouria (after Williston). 

c. coracoid; cl. clavicle; id. interclaviclc; j. jugal; /. lachrymal; m. 
maxilla; po. post-orbital; qj. quadratojugal; sc. scapula; sq. squamosal. 

xv. i SEYMOURIA 389 

On the other hand, there are many considerations that would lead 
one to classify this fossil as an amphibian. (1) The skull bones were 
conspicuously pitted or 'sculptured' ; (2) the pattern of the bones was 
very like that of early amphibians ; for instance an intertemporal bone 
was present; (3) the teeth still showed a labyrinthine structure and 
the palatal teeth were distributed in pairs as in many labyrinthodonts ; 
(4) the structure of the otic notch, across which the tympanic mem- 
brane was stretched, and certain other features of the auditory appara- 
tus suggest amphibian rather than reptilian affinities; (5) other fossils 
are known which, though clearly related to *Seymouria, show trends 
such as flattening and reduced ossification of the skull that are charac- 
teristic of late labyrinthodonts rather than early reptiles; (6) perhaps 
the most significant point of all is that some adult specimens show 
signs of the presence of lateral line canals. Since the structure of the 
skeleton of *Seymouria suggests terrestrial habits, the presence of 
these canals suggests that the animal may have passed through an 
aquatic larval stage in which they were functional. Hence the case for 
classifying * Seymouria as an amphibian becomes very strong. 

It must be added that * Seymouria may show other features charac- 
teristic of both early amphibians and primitive reptiles. The neck, 
for example, was short, with the pectoral girdle lying close behind the 
skull. There was little differentiation between the vertebrae, all those 
in the cervical region bore ribs. The ribs were double-headed, a 
feature that has been retained by some more advanced reptiles. 

*Seymouria itself existed too late to have been a direct ancestor of 
the more advanced groups of reptiles, since some of the latter had 
already appeared by the early Permian. Whether it should actually 
be classified as an amphibian or a reptile is uncertain; in Romer's 
recent Osteology of the Reptiles it and its allies are placed in the latter 
group. It may be regarded as a most interesting link between the 
labyrinthodonts and the primitive stem-reptiles (Cotylosauria), from 
which soon arose a great variety of descendants, which came to 
dominate not only the land but also the sea and air throughout the 
subsequent Mesozoic period. 

The cotylosaurs must have existed throughout the later part of the 
Carboniferous, though they did not become prominent before the 
beginning of the Permian. From the Red Beds of Texas we have, 
besides ^Seymouria, forms such as *Limnoscclis, *Captorhinus y and 
*Labidosaurus, all with the rather high narrow skulls and pointed nose 
characteristic of reptiles rather than amphibians, but differing from 
the latter in the absence of the otic notch. This and other features 



suggest that these animals were related to the early mammal-like rep- 
tiles (p. 539). *Limnoscelis, however, was a particularly primitive form, 
and may have been partly aquatic in habits. 

Other rather later cotylosaurs were larger forms, such as *Diadectes 
(Fig. 222) and *Bradysaunis and other 'pareiasaurs' from the Permian 
and Triassic of Europe, Africa, and America. These were up to 10 ft 






Fig. 222. Skulls of various early reptiles. After Romer and various authors. 

long and probably carried the body well off the ground, the limbs 
being held underneath the body and showing some reduction of 
specialized digits. This, together with the large size of the animals and 
their specialized teeth, suggest that they may have been one of the 
first of the many types of large herbivore to appear on the land (see 
p. 429). In some of them the skull developed grotesque protective 
protuberances, a feature recalling similar later developments in 
reptiles (Ceratopsia, p. 426) and mammals (amblypods, p. 717). A 
characteristic structural feature was the presence of an otic notch low 
down on the side of the skull. This distinguishes the pareiasaurs from 
the more mammal-like forms and suggests affinity with some of the 
other reptilian descendants of the early cotylosaurs. These cotylo- 
saurs multiplied and became very diversified throughout the 45 million 

XV. 2 



years of the Permian period, by which time the main reptilian types 
had appeared. The individual reptilian orders nearly all became 
established during the subsequent 45 million years of the Trias and 
most of them reached their maximum development in the Jurassic 
and Cretaceous. 

2. Classification of reptiles 

Since our knowledge of reptiles depends mainly on fossil remains 
it is convenient to classify them by means of the skull into four great 



Fig. 223. Diagrams of reptilian skulls to show arrangement of the temporal openings. 

Anapsida, no opening. Synapsida, a lower opening, with post-orbital and squamosal 

meeting above it. Parapsida, an upper opening with post-orbital and squamosal 

meeting below it. Diapsida, two openings, separated by a bar. 

.jugal; pa. parietal; po. post-orbital; sq. squamosal. (From Romer, Vertebrate Paleontology, 
Chicago University Press.) 

groups (Fig. 223). Such a classification is in some ways artificial, but 
it serves to indicate in a broad way the main lines of evolution within 
the class. 

In the cotylosaurs the dermal bones of the temporal region of the 
skull presented an unbroken surface and there were no temporal 
fossae. There were therefore no arches or 'apses' of bone in the tem- 
poral region. Such forms are placed in the subclass Anapsida. The 
jaw muscles took origin from the deep surface of the temporal side 
wall, between it and the brain-case, and they passed down through 
holes in the palate to be inserted on the lower jaw. This represents the 
most primitive condition found in reptiles, and resembles that in the 
early amphibians. It is still seen today, though often in a modified 
form, in the Chelonia, which are hence placed in the anapsid sub- 

In more advanced groups of reptiles fossae bounded by bony 
arches appear in the temple region, enabling the jaw muscles to extend 

392 REPTILES xv. 2- 

through them on to the outer surface of the skull, an arrangement 
that increases their mechanical advantage. 

In many reptiles, two such fossae appeared, the condition being 
termed diapsid. This is seen in the subclasses Lepidosauria and Archo- 
sauria, perhaps the most successful groups of reptiles. In lepidosaurs 
of the order Squamata, however, the lower temporal arch is always 
incomplete, having no quadrato-jugal bone and the jugal separated 
from the squamosal. In some lizards and in snakes the upper arch 
is also lost. 

In other groups only a single fossa and arch is present. When this 
is situated high on the skull the condition is known as parapsid. 
Parapsid skulls are seen in the subclasses Ichthyopterygia (icthyo- 
saurs) and Synaptosauria (plesiosaurs, &c). Formerly, these two sub- 
classes were placed together in a group known as the Parapsida, as is 
shown in Fig. 221, but this classification is now regarded as artificial, 
since the ichthyosaurs and sauropterygians are not closely related; 
in fact a careful analysis shows that the bony relationships of their 
single temporal fossae were rather different. 

In the remaining subclass, the Synapsida, there is also a single 
fossa, but in the earlier forms at least it is placed low down, and is 
bounded below by the jugal and squamosal. The term synapsid, 
meaning 'fused arch', is actually a misnomer, due to the fact that 
early workers believed, wrongly, that the single arch was formed from 
the fusion of the two seen in diapsids. 

The synapsids comprise the mammal-like reptiles, but in the later 
members of the group, such as *Cynognathas, and in their descendants 
the mammals, the temporal fossa has greatly enlarged, and has lost 
its primitive relationships. 

3. Order 1. Chelonia 

Shut away in their boxes the tortoises and turtles have retained 
some of the features of the earliest anapsid reptiles. Even today they 
are a not unsuccessful and quite varied and widespread group, with 
more than 200 species. These include terrestrial animals, such as 
Testudo graeca, the Grecian tortoise of south Europe, which is her- 
bivorous; the freshwater tortoises, such as Chrysemys and other 
American terrapins, and Emys the European water-tortoise, all of 
which are carnivorous. The marine Chelonia, usually known as 
turtles, are often very large. Dermochelys, the leathery turtle, which 
has no horny shell, is over 6 ft long and weighs half a ton. Chelone 
my das, the green or edible turtle, is over 3 ft long. 

xv. 3 



The characteristic of chelonian organization is the shortening and 
broadening of the body, together with the development of bony 
plates, forming a box into which the head and limbs can be with- 
drawn. The total number of segments is only about 8 in the neck, io 
in the trunk, and a series of reduced caudals; the body is therefore 

Fig. 224. Skeleton of turtle (Chelone). 

carp, carpus (note hook-shaped 5th metacarpal); cen. centrum of vertebra; cor. coracoid; 
fern, femur ;fib. fibula; h. humerus; il. ilium; isch. ischium; mar. marginal plate; nuch. nucal 
plate; pr. 'proscapular' process or acromion; pub. pubis; rad. radius; rib, rib, partly fused 
with costal shell-plate; sc. scapula (foreshortened); tib. tibia; uhi. ulna. (After Shipley and 

McBride and Reynolds.) 

morphologically shorter than in any other vertebrate except the frog. 
Probably this shortening and broadening is the result of some quite 
simple change in morphogenesis. 

The shell is usually considered to include a dorsal carapace and 
ventral plastron. Each of these is made up of inner plates of bone, 
covered by separate outer plates of horny material, comparable to the 
scales of other reptiles. The carapace includes five rows of bony plates, 
namely, median neurals, and paired costals and marginals (Fig. 225). 
These plates are ossifications in the dermis, attached to the vertebrae 

394 REPTILES xv. 3 

and ribs, but not actually formed from the latter. The plastron is 
developed from the expanded dermal bones of the pectoral girdle, 
together with dermal ossifications comparable to the abdominal ribs 
found in crocodiles and other reptiles. The whole is covered in most 
chelonians by rows of special smooth epidermal plates forming the 
'tortoise shell' (Fig. 225). A new and larger layer is added to each of 
these plates each year, the old one remaining above it, thus making a 
number of 'growth rings' from which some indication of the age of the 

Neur. S. 

Neur. PL. 

Mar (j. S. 

Pect. S. 

Fig. 225. Diagram of the arrangement of the shell of the tortoise 

(Testudo). The horny shields are shown only on the left. 

cap. capitulum of rib; costal plate; cost.s. costal shield; marginal 

plate; marg.s. marginal shield; neural plate; tieur.s. neural shield; pect.s. 

pectoral shield; plast. plastron; sp.c. spinal cord. (After Gadow). 

tortoise can be calculated, though the outer members often become 
rubbed off. 

In order to support this box the limb girdles have become much 
modified and lie inside the encircling ribs. The pectoral girdle has 
three prongs, a scapula that meets the carapace dorsally and carries a 
long 'acromial process' and a backwardly directed coracoid, the two 
last being attached bv ligaments to the plastron. The ilia are attached 
to two sacral vertebrae and the ischia and pubis are broad. The limbs 
are stout, but otherwise typically reptilian, with five digits in each. 
In the marine turtles they are transformed into paddles. 

The interpretation of the skull is still somewhat doubtful, but it 
seems not unlikely that the turtle, Cheloue, shows the simplest case, 
namely, the original anapsid condition (Fig. 226). Here the roofing is 
complete, the dermal bones being widely separated from the brain- 
case, forming a tunnel for the jaw muscles and those producing 
retraction of the neck. The tympanum is stretched across a sort of otic 
notch, bounded by the squamosal, quadrato-jugal and quadrate, the 

xv. 3 SKULL 395 

columella auris articulating with the latter. In other groups of Che- 
Ionia, however, the dermal roofing has been reduced or 'emarginated', 
presumably to give still better attachment for the jaw and neck muscles 



Fig. 226. Skulls of Chelone and Trionyx. Lettering as Fig. 214, p. 377. 
(After Goodrich from Parker and Haswell, and Zittel.) 

(Fig. 226). It has been argued that the condition in Chelone is second- 
ary, but there is no evidence of true temporal fossae in any chelonian, 
and since the early form *Triassochelys also had a fully roofed skull 
there seems no reason for denying that we have here essentially an 
anapsid condition. 

A peculiarity of recent Chelonia is the entire absence of teeth, alike 



Fig. 227. Various chelonians, not all to same scale. (Emys and Chelys after Gadow, 
Dermochelys after Deraniyagala.) 


in the herbivorous and carnivorous forms. The edges of the jaws form 
sharp ridges, covered with a formidable horny beak. 

The similarity of the soft parts of Chelonia to those of other 
surviving reptiles (which are all diapsids) suggests that the 
general organization of the group has changed little since the Per- 
mian. The heart possesses a partly divided ventricle and there are two 
equal aortic arches (Fig. 244). Respiration is modified by the rigidity 
of the body wall; the lungs are spongy structures attached to the 
dorsal surface of the shell, sometimes enclosed in a separate pleural 
cavity (Testudo). Breathing is mainly brought about by the contraction 
of the modified abdominal muscles, which function in a manner 
comparable with that of the mammalian diaphragm, and by means of 
pumping movements of the pharynx. Some aquatic forms {Emys) also 
respire by taking water into special vascular sacs, diverticuli of the 
urodaeum. The metabolism of tortoises is slow and they can remain 
for long periods without breathing. In temperate climates all species 
hibernate regularly. 

The kidney is metanephric and the nitrogenous excreta are mainly 
uric acid, there being a typical subdivision of the cloaca and reabsorp- 
tion of water to form a solid whitish excretory product (see p. 380). 
There is a single copulatory organ and the eggs are whitish, with hard 
or soft shells. Like other aquatic reptiles that lay eggs, turtles all come 
ashore to breed. Thus the marine Chelone breeds in the West Indies, 
in the Straits of Malacca, and on the coast of West Africa; they are 
caught as they come ashore and made into turtle soup. On the Amazon 
chelonian eggs are (or at least were) so plentiful that large numbers 
were eaten. The eggs are usually carefully placed in holes made by 
boring with the tail and scooping with the feet (Emys). The traces of 
the nest are then covered, often with considerable success. Neverthe- 
less Bates reckoned that at least 48 million eggs were taken annually 
on the upper Amazon. The chief enemies of the young are vultures 
and alligators, and these were presumably the ultimate losers when 
collection by man began, though the numbers of turtles have also 
decreased as a result of the human depredations. 

The proverbial slowness of the tortoise is a necessary corollary of 
its heavy armour, but the nervous organization and behaviour is more 
complex than is sometimes supposed. The brain shows well-developed 
cerebral hemispheres, with not only the basal regions but also the 
pallium quite large. This was therefore probably true also of the 
earliest reptiles, as it is of amphibians. In the mammals, also derived 
from cotylosaur ancestors, there has been still further development of 

398 REPTILES xv. 3- 

the dorsal regions of the hemispheres to form the cerebral cortex, 
whereas in the remaining reptile groups, and in the birds, the ventral 
portion has become large, the dorsal thin. The eyes are probably the 
chief receptors of chelonians, but the nose is also well developed and 
the animals are very sensitive to vibration. The tympanum is often 
covered with ordinary skin and hearing is probably not acute (p. 385). 
The voice is also small. 

The various species show many special habits, some of them com- 
plicated and ingenious, especially among the aquatic forms (Fig. 227). 
For instance, the snapping turtles (Chelydra) and alligator turtles 
(Macroclemys) of North America and Emys in Europe show con- 
siderable care and skill in stalking and capturing not only fish but 
also young ducks and other birds. Similarly the smaller turtles, such 
as Chrysemys picta, the painted terrapin, with bright yellow, black, 
and red colours, feed not only on insect larvae, but also on flies, which 
they catch near the water surface. Many observers have shown that 
the common Grecian tortoise has a marked sense of locality, returning 
to a favourite spot even after hibernation. 

Our knowledge of the geological history of the Chelonia extends 
back to the Trias. *Triassochclys (Fig. 222) was an early turtle, with 
a shell like that of modern forms, but still possessing teeth on the 
palate. The skull was anapsid and the pectoral girdle contained inter- 
clavicles, clavicles, and perhaps cleithra; these dermal bones were 
already somewhat enlarged and incorporated in the plastron. The 
head, tail, and limbs could not be withdrawn into the shell and were 
protected by spines. In the later evolution of the Chelonia retraction 
of the head became possible by one of two methods. In the suborder 
Pleurodira, 'side-neck turtles', the neck is folded sideways. The group 
is known from the Cretaceous and survives today in tropical Africa 
(Chelys), South America, and Australia. The more successful group 
is the suborder Cryptodira, in which the neck is curved in a dorso- 
ventral plane. This type is also known from the Cretaceous and 
includes most of the modern types. The aquatic chelonians show 
various modifications and it is probable that several lines have inde- 
pendently returned to the water. As a result of this habit the bony 
shell is often reduced, presumably in the interests of lightness and 
because of absence of enemies. This had occurred already in *Archelon 
of the Cretaceous, which is very similar to the modern Chelone. 
Dcrmochclys, the leathery turtle, has a curious 'carapace' consisting 
only of a mosaic of small bony plates beneath its leathery skin, 
and Trionyx is a freshwater turtle with a soft shell and no horny 


plates. All of these forms are best considered as aberrant crypto- 

We can trace the history of the Chelonia back rather satisfactorily 
to the Triassic, but unfortunately there is little to show how they 
evolved to that stage from some Carboniferous cotylosaurian ances- 
tor. * Eunotosaurus from the Permian of South Africa had a small 
number of vertebrae, with very broad, expanded ribs. This perhaps 
suggests some affinity with Chelonia, though in the latter the ribs 
themselves are not expanded. There is therefore little to tell us how, 
when, or why one of the early reptilian populations shortened its 
bodies and covered them with armour for protection against the 
hazards of the land they had recently invaded. 

4. Subclass *Synaptosauria 

Order *Protorosauria 

All the Synaptosauria characteristically possessed a single temporal 
fossa in the upper or parapsid position. The earliest forms were small 
terrestrial lizard-like creatures such as *Araeoscelis from the lower 
Permian (Fig. 228). A few more specialized forms, including the 
remarkable Triassic * T any stropheus with, a long neck and short body, 
are known, but the protorosaurs seem never to have been an impor- 
tant element of the early reptilian fauna. Their relationships are not 
well understood but it is possible that they gave rise to the sauro- 
pterygians. The theory that the Squamata were derived from proto- 
rosaurs by the emargination of the lower temporal region is now held 
to be unlikely. 

Order * Saw o pterygia 

This was a very successful line of marine reptiles, extending from 
the Trias to the end of the Cretaceous. The earlier nothosaurs, such as 
*Lariosaurus (Fig. 228) from marine Triassic deposits, were small 
(3 ft long) and had a long neck, and limbs partly converted into 
paddles. The upper temporal fossa was enlarged and the nostrils lay 
rather far back, as in many water reptiles. 

All of these features were further developed in the plesiosaurs of 
the Jurassic and Cretaceous, such as *Miiraenosaurns (Fig. 228). In 
some the neck became very long, presumably for catching fish; 76 cer- 
vical vertebrae have been recorded. In others the neck was shorter 
and the skull longer. The limbs were developed into huge paddles, 
the ventral portions of the girdles being large for the attachment of 
muscle masses inserted on the flattened humerus and femur. The 



xv. 4- 

dorsal portion of the girdles, so well developed in terrestrial reptiles, 
was here small: the ilium hardly articulates with the sacral verte- 
brae. The hands and feet were enlarged by increase in number of 
joints (hyperphalangy), but there was no increase of digits (hyper- 




^^^Mmmrn^ ^ 



Ichthyosaurus \ Jf 

Fig. 228. Icthyosaurs, plesiosaurs, and their allies. (Partly after Romer.) 

dactyly) such as is seen in ichthyosaurs. The skull was as in notho- 
saurs, but with the nostril still further displaced on to the upper 

These animals were numerous in Jurassic and Cretaceous seas and 
some of them reached 50 ft in length. They were obviously fish- 
eaters, but little is known of their habits. It is not known whether they 
were viviparous or came ashore to lay eggs. *Placodus and related 


Triassic forms were related to the plesiosaurs and were specialized for 
mollusc-eating by the development of large grinding teeth on the 
jaws and palate. 

5. Order *Ichthyopterygia 

These animals, found mainly in the Triassic and Jurassic seas, 
were even more modified for aquatic life than the plesiosaurs (Fig. 
228). They occupied a position comparable to that of the dolphins 
and whales during the Tertiary period. The body possessed a stream- 
lined fish shape and swimming was by lateral undulatory movements. 
The vertebrae were amphicoelous disks and there were large dorsal 
and caudal fins, with the vertebral column apparently continued into 
the lower lobe of the latter. The paired fins were small and presumably 
used as stabilizing and steering agents. The pelvic girdle did not 
articulate with the backbone. In the limbs the number of digits was 
often greater or less than the usual five, and there was often hyper- 
phalangy. Evidently this type of skeleton gives better support for a 
fish-like paddle than does the pentadactyl tetrapod type and it is 
interesting to find it evolved again in vertebrate stocks that returned 
to the water. This seems in a sense to be a case of reversal of evolution. 

The head was much modified for aquatic life, with a very long 
snout armed with sharp teeth, and nostrils set far back. The eyes 
were large and surrounded by a ring of sclerotic bony plates. The 
temporal fossa, though in the parapsid position, had boundaries 
different from that in the synaptosaurians. 

The Triassic ichthyosaurs were already greatly modified and we 
have no trace of the origin of the group. Romer has suggested a pos- 
sible derivation from cotylosaurs related to the ancestors of mammal- 
like reptiles. The ichthyosaurs were more highly adapted to aquatic 
life than any other reptiles known. They seem to have been viviparous, 
since the skeletons of small specimens have been found within larger 
ones. Like the plesiosaurs they developed a special mollusc-eating 
type, *Omphalosanriis, in the Triassic. 

6. Subclass Lepidosauria 

Most of the animals popularly considered as characteristic of the 
period of reptilian dominance have a two-arched or diapsid skull. This 
condition, or some modification of it, is found in all the surviving 
reptiles except the Chelonia, and in the birds. Formerly all the two- 
arched reptiles were placed in a single subclass, the Diapsida, but it 
is now customary to divide them into two subclasses, the Lepidosauria, 

402 REPTILES xv. 6-7 

which includes Sphenodon, the lizards and snakes, and the Archo- 
sauria, including the crocodiles, dinosaurs, pterosaurs, and the an- 
cestors of birds. It is not known if the archosaurs were derived from 
primitive lepidosaurs such as * Yonngina, or whether the two groups 
arose independently from cotylosaurian ancestors. 

Order *Eosuchia 

The earliest lepidosaurs belong to the order Eosuchia. The best 
known of these, * Youngina (Figs. 229 and 230), was a lizard-like 
creature, found in the Upper Permian of South Africa, and retaining 
many cotylosaurian features, for instance, teeth on the palate and no 
opening between the bones of the snout (antorbital vacuity). The 
two fossae at the back of the skull immediately show the affinity with 
other diapsids. Little is known of the post-cranial skeleton. The fifth 
metatarsal does not show the hooked shape that is found in other 
diapsids and also in Chelonia. It is difficult, however, to ascribe very 
great weight to this single point, as against the general features of the 
skull, which indicate that * Youngina could have given rise to the later 
two-arched reptiles and, by loss of the lower margin of the lower 
temporal fossa, also to the lizards and snakes. *ProIacerta, from the 
Lower Trias, shows how this may have come about; it is so like 
* Youngina that it is classed as an eosuchian, but there is a gap in the 
lower temporal arch, suggesting that the animal may have been near 
the ancestry of lizards. 

7. Order Rhynchocephalia 

Sphenodon ( = Hatteria), the tuatara of New Zealand, is the oldest 
surviving lepidosaurian reptile; it still remains in essentially the 
eosuchian condition. Very similar Mesozoic fossils (e.g. *Homoeo- 
saurus from the Jurassic) show the continuity of the type (Fig. 221). 
Among the many primitive features that this race has preserved un- 
changed for 200 million years are the two complete temporal fossae 
(Fig. 231), the well-developed pineal eye (the pineal foramen is 
marked in the early diapsid fossil skulls), and the amphicoelous verte- 
brae with intercentra. Sphenodon, alone of surviving reptiles, has no 
copulatory organ. The large wedge-shaped front teeth are among the 
few specialized characters. 

The tuatara was once widespread throughout New Zealand but 
became much reduced and in danger of extinction. Recently rigid 
conservation measures seem to have allowed it to recover in numbers 
on some small northern islands. The animals are up to 2 feet long and 


Fig. 229. Diagrams of skulls of A, eosuchian, B, 
pseudosuchian, showing the plan of the diapsid skull. 
Lettering as Fig. 214. //. lower temporal fossa; pi. pre- 
orbital fossa; sf. upper temporal fossa. (From Goodrich.) 



Fig 230 Skull of Youngina. Lettering as Fig. 214. (After Romer, Vertebrate Paleontology , 

Chicago University Press.) 

4<h REPTILES xv. 7- 

are insectivorous and carnivorous. They live in burrows, often in 
association with petrels. The eggs take over a year to hatch. 

Sphenodon evidently shows us a type that has departed relatively 
little from the condition of diapsids in the late Permian. Yet its appear- 
ance, habits, and soft parts are very like those of lizards, and provide 
us with evidence that these animals remain in essentials rather close 
to the original amniote populations. A few other extinct rhyncho- 

itf. fr. 

Fig. 231. Skull of Sphenodon. Lettering as Fig. 214. (After Romer, 
Vertebrate Paleontology, Chicago University Press.) 

cephalians are known; these include the rhynchosaurs, in which the 
tip of the upper jaw had a hooked beak-like appearance. 

8. Order Squamata 

The lizards and snakes are the most successful of modern reptiles, 
numbering between them over 5,000 species. Probably the groups 
arose from eosuchians related to *Prolacerta. Such forms would also 
have been close to the Rhynchocephalia, differing from them, however, 
in a tendency to lose the lower temporal arch and to develop a movable 

It has now been shown that the lizards are a more ancient group 
than was formerly supposed, and had appeared by the end of the 
Triassic. Furthermore, some of the early forms were already con- 
siderably specialized. Our knowledge of the early lacertilian radiation 
is still incomplete, however, and none of the existing lizard families 
are known much before the Cretaceous. The earliest undoubted snake 
occurs in the upper Cretaceous and the group does not seem to have 
become abundant until the Oligocene. 


Although typical lizards preserve a number of primitive reptilian 
features, the Squamata as a group show several interesting specializa- 
tions that are absent in Sphenodon, and to which their success may 
be partly attributed. In the majority of forms, especially in the snakes, 
the skull is highly kinetic, having a freely movable quadrate, which 
imparts its motion to the bones of the upper jaw. Paired copulatory 
organs of a unique type are present in the male. There is a widespread 
tendency towards limb reduction, which has apparently occurred 

Fig. 232. Jacobson's organ. Diagram of reconstructed L.S. of snout of lizard showing nose 
and organ of Jacobson, both seen in section from the lateral side. 

ex.n. region of external nostril; in. internal nostril; j.o. (/.) Jacobson's organ lumen ;/.o. (s.e.) 
Jacobson's organ sensory epithelium; l.d. lachrymal duct, front end, cut; l.n. lining of nose; 
n.j.o. nerves to Jacobson's organ; o.b. olfactory bulb; o.n. olfactory nerves; /. tongue. 

independently in members of about half the existing families of 
lizards, and in snakes. 

The paired organs of Jacobson are highly elaborated and of great 
functional importance. In snakes and in most lizards these organs 
(Fig. 232) are hollow domed structures above the front of the palate, 
each opening into the mouth by means of a slender duct. The lachry- 
mal duct opens into or near the duct of Jacobson's organ, instead of 
into the nose, suggesting that the secretions of the eye glands may have 
some special function related to that of the organ. Odorous particles 
are carried to the ducts of Jacobson's organs, or to the immediate 
neighbourhood of them, by the tongue tip, which is forked in snakes 
and many lizards. The lumen of the organ is partly lined by sensory 
epithelium, supplied by a separate branch of the olfactory nerve. 
Experiments by Noble and others have shown that the organs assist 
in such functions as sex recognition and following trails left by prey. 



Sphenoaon /p^^f^i -^ ^- ;--<# 

^§3&> "' -"^V,- r - . , • '* ... -/ A mphisbaena 


Fig. 233. Various Squamata {Draco after B.M. Guide). 

xv. 8-9 LIZARDS 407 

In some lizards and all snakes, the eyelids are modified to form an 
immovable transparent spectacle covering the cornea, with the loss of 
the nictitating membrane. The adaptive significance of this, which is 
foreshadowed in some lizards by the development of a window in the 
lower eyelid, is not always clear, since although it is found in many 
that burrow or live in sand, it also occurs in arboreal forms. 

9. Suborder Lacertilia 

The modern lizards show extensive adaptive radiation (Fig. 233) 
and include terrestrial, arboreal, burrowing, and aquatic forms. The 
majority are carnivorous but there are some herbivores. It is difficult 
to say which of the twenty or so living families is the most primitive, 
and the grouping of these into infraorders is a matter of some difficulty. 

The Gekkota contains the geckos and a small group of Australasian 
limbless forms, the pygopodids. Geckos are mainly small nocturnal 
and arboreal insectivorous lizards of warm climates, with ridged pads 
on the toes and sharp claws that enable them to climb an almost 
smooth surface. Some species have taken to living in houses. The 
tree-gecko Ptychozoon has webs of skin on the limbs and along the 
sides of the body, which perhaps act as a parachute to break its fall. 
Many geckos live in colonies and unlike most lizards are extremely 
vocal, making clicking and cheeping sounds. Their hearing is probably 
acute. The endolymphatic ducts of the inner ear are greatly expanded 
to form sacs in the neck containing calcareous deposits, but the func- 
tional significance of this is obscure. Their eyes are, as a rule, covered 
by a spectacle. Geckos are the only Squamata that lay hard-shelled 
eggs, those of other forms being leathery in texture. 

The Iguania is a large group comprising the agamids, iguanids, and 
chameleons. The first two include terrestrial, arboreal, and amphibious 
types, sometimes of large size, and often furnished with crests, dew- 
laps, expansible throat-fans and other appendages that play a part 
in rivalry and courtship. The males are often brightly coloured and 
the whole group is characterized by a visually dominant behaviour 
pattern. In some arboreal forms, as in the chameleons, the sensory 
parts of the nose and the organ of Jacobson are reduced. 

The agamids are found in the Old World and Australasia and in- 
clude such well-known types as the oriental 'blood-sucker' (Calotes), 
so-called because of the red colour of the throat, the spiny lizards 
(Uromastix) of the north African and Indian deserts, and the Aus- 
tralian frilled lizard (Chlamydosaarns) (Fig. 240). The Indo-Malayan 
genus Draco has a large lateral web, supported by the ribs, which can 

4o8 REPTILES xv. 9 

be spread out and used for gliding, though it is not moved in true 
flight. Lyriocephalus from Ceylon is an agamid with a remarkable 
convergent similarity to the chameleons. Some agamids (and other 

Fig. 234. Chameleon catching a fly, showing its changes in colour. 

A, cream with yellow patches, the usual night colour. B, grey-green with 
darker patches. C, dark brown patches and yellow spots. D, reaction pro- 
duced by pinching tail, inflation and darkening of all spots. (After Gadow.) 

lizards) can run on their hind legs when they are in a hurry (Fig. 240). 
In agamids the teeth are set squarely on the summit of the jaw, as in 
Sphenodon; this condition is termed acrodont. In most other lizards 
the teeth are attached obliquely to the inner side of the jaw (pleuro- 

The iguanids are found mainly in the New World and parallel the 
agamids in many ways. Anolis is a small, common North American 
form. Iguana from south and central America reaches 6 ft in length. 

xv. 9 LIZARDS 409 

Amblyrhynchus, found only in the Galapagos Islands, is remarkable 
as the only existing marine lizard, though it spends much of its time 
on shore, basking and feeding on the sea-weed left at high tide. Phryno- 
soma, the horned toad, with spikes on the head and back, is found in 
the deserts of North America and burrows in the sand. This is one of 
the few ovoviviparous iguanids. 

The chameleons are highly modified arboreal lizards from Africa, 
Madagascar, and India. Some species have casques on the head, or 
one or more horns on the snout. The tail is prehensile and the digits 
are arranged in groups of two and three so as to be opposable and 
allow the grasping of branches. Chameleons live on insects, caught 
by means of the very long tongue (Fig. 234), which has an adhesive 
clubbed tip and is projected by a remarkable muscular mechanism. 
Their movements are slow and deliberate, but they show considerable 
care in stalking their prey; as they approach it their eyes, which 
normally move independently, converge so as to bring the prey into 
binocular vision, presumably serving to judge its distance. Their 
powers of colour change are described on p. 410. 

The Scincomorpha are another large assemblage, including Lacerta, 
common in Europe and North Africa, and the skinks, many of which 
are modified for burrowing, sometimes in the sand. Many skinks 
have well-developed limbs, but others show all degrees of limb reduc- 
tion, either the fore- or hind-limbs, or both, being lost. The most 
highly fossorial of all lizards, the worm-lizards or Amphisbaenidae, 
may also belong to the Scincomorpha, though they show many 
remarkable specializations. Their eyes are rudimentary, their tails are 
blunt and resemble the head, and they are able to move freely in 
either backward or forward direction. External limbs are usually 

The Anguimorpha contains the anguids, of which the European 
slow-worm Anguis is a familiar limbless example, and the monitor 
lizards (Varanus) and their allies, which are placed in the superfamily 
Platynota. The monitors of the Old World and Australia include the 
largest of existing lizards, one species, the Komodo Dragon, growing 
to at least 10 ft long. They are carnivorous, killing vertebrates as well 
as insects, and are often semi-aquatic. Three related groups, now 
extinct, occurred in the Cretaceous. The aigialosaurs and dolichosaurs 
were amphibious lizards of moderate size, but the later mosasaurs, 
such as *Tylosawus, were huge creatures, sometimes 30 ft long, and 
were highly adapted for marine life, with long jaws and paddle- 
like limbs showing some hypcrphalangy. The strikingly coloured 

410 REPTILES xv. 9- 

heloderms from North and Central America are also playtnotids and are 
of special interest as the only known poisonous lizards. Another allied 
form is the rare earless monitor, Lanthanotus, from Borneo, which 
seems to be a survivor of the primitive platynotid stock. 

Many lizards are able to change colour, the chameleons, Anolis 
(often called 'American chameleons'), and certain agamids being the 
most notable for this. The colour may change with the environment, 
serving the obvious purpose of concealment. Special colour patterns 

Fig. 235. Diagram of the nervous control of the melanophores in the chameleon 
(above) and minnow (below). 

c, spinal cord; f, pathway of pigmentomotor fibres (the synapse in the sympathetic ganglia 

is omitted); M, melanophore; n, spinal nerve; p, pigmentomotor centre; s, sympathetic. 

(From Sand, minnow after v. Frisch.) 

are displayed in courtship or threat, and colour change may also 
occur in response to temperature and other environmental changes. 
The physiological mechanism of colour control varies in different 
reptiles. In Anolis there are probably no nerves to the melanophores, 
which are controlled by hormones produced by the posterior pituitary 
and possibly other glands. In chameleons, however, the melanophores 
are controlled partly or entirely by the autonomic nervous system 
(Fig. 235). 

Many lizards are able to break off their tails when threatened or 
seized by a predator; this ability, known as autotomy, is due to the 
presence of special planes of weakness through the bodies of the caudal 
vertebrae. Such fracture planes are also found in Sphenodon, but not 
in snakes. After autotomy the tail regenerates, but the new member 
is not a replica of the normal. The vertebrae, for instance, are not 
regenerated, their place being taken by an unsegmented tube of car- 
tilage. It has been shown experimentally that in Anolis regeneration 
will not occur if the motor-nerves are prevented from growing back 

xv. io SNAKES 411 

from the stump. The new sensory innervation of the skin is derived 
entirely from the surviving dorsal roots, whose cells become greatly 

10. Suborder Ophidia 

The snakes are obviously descended from lizards of some kind, but 
their precise mode of origin is obscure. Some workers believe that 
their nearest living relatives are the platynotid lizards (monitors, &c). 
There is evidence that the snakes passed through a burrowing stage in 
their early history, although no known platynotids show marked fos- 
sorial adaptation. A burrowing ancestry is particularly suggested by 
the structure of the eye, which, as Walls has pointed out, differs 
widely from that in typical lizards (Fig. 238). Thus there are no 
scleral ossicles or cartilages in snakes, and accommodation is brought 
about in a manner unusual for reptiles, involving displacement of the 
lens. The visual cells include cones of a peculiar type, which have 
apparently been derived from rods. The yellow retinal droplets that 
serve to protect lacertilian retinae from excessive light are absent, 
and instead some diurnal snakes protect their retinas by a yellow- 
tinted lens. These features can all be interpreted on the supposition 
that the ophidian eye was once drastically reduced, but has sub- 
sequently been refurbished in response to the needs of life above 
ground. Other characters that seem to point in the same direction 
include the structure of the ears which, as in many burrowing lizards, 
have apparently degenerated. The ear drums, tympanic cavities, and 
Eustachian tubes are absent, and the columella auris articulates with 
the quadrate. It seems unlikely that snakes can hear airborne sounds 
at all well, though doubtless they are sensitive to ground vibrations 
transmitted through the bones of the jaw. 

The snakes show many other interesting peculiarities, the most 
obvious being the complete absence of limbs. Only in a few of the 
more primitive forms such as the boas and pythons can rudiments of 
the hind limbs and their girdles be found; in these snakes claws may 
be present externally on either side of the cloaca and are said to play 
a part in coitus. 

Locomotion is produced by the lateral undulation of the body, 
which exerts pressure on surrounding objects and pushes the snake 
forwards; the enlarged transverse ventral scales of most species help 
to prevent slipping. A few snakes (e.g. some boas and vipers) can also 
progress by muscular movements of the ventral scales, with their 
bodies stretched out almost in a straight line. The spine is strengthened 

4 i2 REPTILES xv. 10 

by additional intervertebral articulations known as the zygantra and 

The skull is highly modified, permitting, in all except a few bur- 
rowing forms, an enormous gape and the swallowing whole of large 
prey. The premaxilla is small and usually toothless, and the bones of 
the upper jaw are loosely attached to the rest of the skull. The two 
halves of the lower jaw are united only by ligaments. The sharp 
recurved teeth are carried on the palate bones as well as on the maxilla 

pro. / WSW5" 
sm. pi. 

Fig. 236. Diagram of skull in ophidians. 
d. dentary; ec. ectopterygoid ; jr. frontal; mx. maxilla; ». nostril; na. nasal; 0. orbit; pa. 
parietal; pf. postfrontal; pi. palatine; pm. premaxilla; prf. prefrontal; pt. pterygoid; q. quad- 
rate; s. squamosal or supratemporal; sf. upper temporal fossa (this is shown diagram- 
matically, as it occurs in many lizards; in Lacerta it is largely covered by an extension of 
the postfrontal — see Fig. 213); sm. septomaxilla. (Modified from Goodrich.) 

and dentary. The brain-case is strong and compact, the brain being 
protected from mechanical injury during swallowing by the massive 
parasphenoid and by flanges of the frontals and parietals, which lie 
between the orbits, so that there is no interorbital septum. 

In the normal ophidian kinetic mechanism the upper jaw as a whole 
is raised as the result of forward rotation of the lower end of the freely 
mobile quadrate, which is attached to the back of the pterygoid. The 
well-developed protractor muscles of the pterygoid and quadrate play 
an important part in the process. In the viperid snakes a further 
elaboration of this mechanism is seen, the maxilla being very short 
and able to rotate on the prefrontal so that the fangs can be erected 
(Fig. 237). A slip from one of the muscles is attached to the poison 
gland and helps to expel the venom as the snake bites. 

The respiratory system and viscera of snakes are also much modi- 
fled. The glottis can be protruded so as to keep the airway clear while 
prey is being swallowed, and in some forms a part of the trachea is 
specialized for respiration as a tracheal lung. The left of the two paired 




lungs is usually reduced, often to a rudiment, as in some limbless 
lizards, and the other paired viscera tend to lie at different levels on 
the two sides. The heart usually lies a quarter to a third of the way 
down the body, and the carotid arches are asymmetrical, the right 
common carotid artery tending to be suppressed. 


temp ant 

Fig. 237. Skull of rattle-snake (Crotalus) with jaws partly and fully opened. 

Lettering as Fig. 214; sph-pt. the protractor-pterygoid muscle, which pulls the pterygoid 
forward, causing it to push the ectopterygoid, which rotates the maxilla and erects the 
fang; di. the digastric muscle that assists in opening the jaw; temp. ant. the anterior temporal 
which shuts the mouth. The diagrams at the right show the actions of the levers that erect 
the fang; g is the groove characteristic of crotaline snakes. (Modified after Gadow.) 

The snakes show nearly as much adaptive radiation as the lizards, 
though there is less structural variation among them. The more pri- 
mitive forms, with pelvic rudiments, include a number of small bur- 
rowers such as Typhlops, as well as the large boas and pythons of the 
family Boidae, which tend to be arboreal and amphibious in habits 
and kill their prey by constriction. In general, the pythons lay eggs, 
whereas the boas are ovoviviparous. 

The majority of living snakes belong to the family Colubridae, which 
contains many medium-sized harmless snakes such as the grass-snake 
(Natrix) and some moderately poisonous ones with grooved fangs at 

sphincter, ci!at< 

Base pi <. 

Canal of Schlemm 
'in sclera) 
Ciliary processes 

Scleral ossicle 
■art/ muscle 

■Sclera (cartilage) 

'Retina (avascular 
cone a! droplets and with standard 
double cones) 



sphincter, dilatator 

raconjunctiysl space 

Canal cf Schlemm 
(in cornea) 

No cone oil droplets 

No epichoricidal lymph spaces 

Mesodermal Afcht^S c ' er3 (™™4 

Con us / // /y^Lhorioid 

■Retina (with 
unique double cones) 


Fig. 238. Diagrams of eyes of lizard and snake, to show the marked contrasts 

resulting from presumed loss during underground life and later acquisition by the 

snakes of features paralleling those present in their ancestors. The dotted arrows 

show the direction of application of force during accommodation. 

(From Walls, The Vertebrate Eye.) 




the back of the maxillae; these are known as back- fang snakes or 
opisthoglyphs. The South African boomslang (Dispholidus) is one of 
the few whose bite may be lethal in man. Dasypeltis, the egg-eating 
snake, is also a member of this group ; it swallows the eggs whole and 
crushes them with special tooth-like processes of the neck vertebrae. 
The family Elapidae contains the cobras, kraits, and coral snakes, 
all highly poisonous with quite small and relatively non-movable fangs 
at the front of the maxilla, and a venom predominantly neuro-toxic in 

<l'S tp 

Fig. 239. Head of crotaline snake (Lachesis) after removal of skin. 

d. duct of poison gland, bending at base of fang; dig. digastric muscle; g. sensory pit or 

groove ; n. nostril ; p.g. poison gland ; ta. and tp. anterior and posterior portions of temporalis 

muscle; tr. trachea. (From Gadow.) 

action. All the poisonous Australian snakes belong to this group. The 
hood of the cobra is expanded by the long cervical ribs and probably 
has a warning (sematic) function. The king cobra (Hamadryas) is the 
largest poisonous snake and reaches 18 feet in length. 

The very poisonous sea-snakes (Hydrophiidae) are related to the 
elapids. Their tails are vertically compressed for swimming; some 
species can hardly move on land. Like many freshwater snakes they 
are (with a few exceptions) ovoviviparous. 

The family Viperidae consists of the vipers of the Old World and 
the rattle-snakes and pit-vipers, mainly from the New World. The 
two latter groups, placed in the subfamily Crotalinae, are distinguished 
by the presence of a remarkable sensory pit on each side of the head 
between eye and nostril (Fig. 239). This is highly sensitive to tem- 
perature changes and helps the snake to detect warm-blooded prey. 
The rattle-snakes are, of course, also noted for their caudal append- 
ages, which are composed of articulated rings and modified skin. One 
ring is formed at each moult, though the older and most posterior 
ones break off periodically. The rattle is vibrated voluntarily as a 

416 REPTILES xv. 10- 

vvarning and perhaps prevents the snake from being trodden on by 
large mammals. 

Most of the Viperidae are highly poisonous, though the bite of the 
European adder {Vipera berus) is seldom fatal to man. The venom is 
predominantly haemolytic in action. The fangs are canalized, the 
canal having apparently being evolved by the progressive deepening 
of a groove until its margins have come into apposition. The fact 
that the fangs are erected when the snake strikes and can be folded 
back along the roof of the mouth when not in use, makes it possible 

Fig. 240. Drawings of three frilled lizards (Chlamydosaurus) and a Grammatophora 

(at right) to show the bipedal habit. (Drawings made by Heilmann from photographs 

of the lizards running at full speed, taken by Saville Kent.) 

for these structures to be very long, about 1 inch in the case of a large 
puff adder. 

Some of the American pit-vipers are very large, the dreaded bush- 
master (Lachesis) reaching about 10 ft. The majority of the Viperidae 
bear their young alive and the finding of late embryos within the 
bodies of female adders and rattle-snakes may have given rise to the 
tale and that these reptiles temporarily hide their young by swallowing 
them in the face of danger. 

1 1 . Superorder Archosauria 

We have seen that about 130 million years ago the diapsid stock 
produced the most successful modern reptile group, the Squamata 
(Fig. 221). Much earlier an even more successful type had developed 
from the Eosuchia, having as its outstanding feature the habit of walk- 
ing on the hind legs. Creatures of this type were the dominant land 
animals of the later Mesozoic, and they include the dinosaurs and 
pterosaurs. Crocodiles are the only living descendants of the group 

xv. i 3 ARCHOSAURS 417 

that have remained at the reptilian level. They have, of course, aban- 
doned the bipedal habit and survive as a specialized amphibious 
remnant. The birds, which are also undoubtedly descendants of this 
archosaurian group, give us in some ways a better idea of the charac- 
teristic structure than do the crocodiles. 

All the lines of archosaurs are characterized by certain common 
tendencies, mostly associated with bipedalism, which is possible also 
in some lizards (Fig. 240); features barely indicated in the earlier 
forms become developed in the later. In all archosaurs the hind legs 
were much longer than the front and the acetabulum formed a cup, 
open below, so that the legs were held vertically below the body. At 
the same time the ischium and pubis became elongated, presumably 
to allow for the attachment of muscles producing a fore-and-aft move- 
ment (see p. 375). In later forms the ilium became fused with several 
sacral vertebrae. The femur has a lateral head and the tibia becomes 
long and strong and sometimes fused with the proximal tarsals; the 
distal tarsals may fuse with the metatarsals as in birds, and the digits 
are reduced, usually to three long ones turned forward while the first 
is turned back. The skull is typically diapsid, but tends to have cer- 
tain modifications, such as the development of antorbital vacuities 
behind the nostrils and other spaces in the palate, presumably serving 
to give lightness without loss of strength. 

12. Order *Pseudosuchia 

The earliest archosaurs were the Triassic pseudosuchians, creatures 
evidently not far removed from the Permian eosuchians. These 
animals (*Saltoposuchus) can be visualized as lizards that ran on their 
hind legs (Fig. 241). They were small and carnivorous, having sharp 
teeth set in sockets along the edges of the jaws (hence 'thecodont'). 
The skeleton showed all the archosaur characters in a most interesting 
incipient form. Thus the bones of the pelvis were still plate-like, but 
arranged in the characteristic triradiate manner. The front legs were 
already much shorter than the hind. Antorbital vacuities were present 
and there was no pineal foramen. 

13. Order *Phytosauria 

Even in the Triassic at least one line, the phytosaurs, abandoned 
the bipedal habit, becoming amphibious. These creatures were not 
actually ancestral to the crocodiles, but show remarkable parallelism 
to them in the elongated jaws and general build (Fig. 241). How- 
ever the nostrils were set far back. There can be no doubt that the 

418 REPTILES xv. 13- 

phytosaurs were derived from pseudosuchians and the two groups are 
often placed together in an order Thecodontia. 


Fig. 241. The skeletons of various archosaurian diapsids. 
(Modified after various authors.) 

14. Order Crocodilia 

In the crocodiles the nostrils are at the tip of the snout and the air 
is carried back in a long tube, the maxillae, palatines, and pterygoids 
forming a bony secondary palate, as in mammals. There is a flap on 
the hind end of the tongue, which, with a fold of the palate, enables 
the mouth to be closed off from the respiratory passage and hence 
kept open under water. The nostrils can also be closed by a special 

xv. 14 



set of muscles, and the ear-drums are protected by scaly movable 
flaps. The Eustachian tubes are very complicated, and parts of the 
skull are pneumatized by extensions from the middle ear cavity, as in 

Fig. 242. Diagram of the skull of Crocodilia. 
Lettering as Fig. 214, p. 377. (From Goodrich.) 

Fig. 243. Anterior cervical vertebrae of Crocodilus. 

c. capitulum; lip. hypocentrum; wa 1-4 , neural arches; pa. pro-atlas; pi. 1-4, pleurocentra; 
prz. prezygapophysis; ptz. postzygapophysis; r. rib; t. tuberculum; tp. transverse process. 
The first neural arch and the pro-atlas of the left side have been removed to show the first 
pleuro-centrum (pi 1 ) which is the odontoid process. (From Goodrich.) 

The crocodiles use all four limbs in walking, but the front are 
shorter than the hind, indicating bipedal ancestry. The pelvis of the 
crocodiles shows signs of the typical triradiate structure, but there 
are only two sacral vertebrae. Rapid swimming is produced by lateral 
movements of the tail, but when moving slowly the partly webbed 
feet are used to push the animal along. The ribs (Fig. 243) are two- 
headed and there is a proatlas element between the skull and atlas. 
The scutes of the back and, in some forms, of the belly, are rein- 
forced by osteoderms, and there are well-developed abdominal 



xv. 14- 

The soft parts of the crocodiles are of special interest because croco- 
diles are, except the birds, the only living creatures closely related to 
the great group of dinosaurs. The heart (Fig. 245) shows a complete 
division of the ventricle, but there are still two aortic arches. The 
truncus arteriosus is divided in a spiral manner to its base, so that 
the aortae cross and the right arch opens from the thick-walled left 

car int. 

car. cxt 

car. int. 

I 1 1 1 „ car. ext 

Che Ionian 

Crocodile J 

Fig. 244. Fig. 245. 

Diagram of heart and arterial arches of a chelonian and of a crocodile, seen from below. 
Lettering as Fig. 215, p. 379. (From Ihle, after Goodrich.) 

ventricle, while the left opens with the pulmonary arteries from the 
weaker right ventricle. The left arch would therefore contain venous 
blood, but an aperture, the foramen of Panizza, connects the two 
arches near the base and presumably the higher pressure in the left 
ventricle ensures that the left arch receives at least some oxygenated 
blood. Possibly, however, the pressure in the right ventricle is in- 
creased when the crocodile dives and the blood flows through the 
foramen from right to left. 

The lungs are well developed, having a system of tubes ending in 
sacs. A transverse partition separates off a thoracic from the main 
abdominal cavity. This 'diaphragm' is not itself muscular, but is 
continued into a diaphragmatic muscle attached to the abdominal 
sternal plates. This muscle, innervated by abdominal spinal nerves, 

xv. 15 DINOSAURS 421 

presumably assists in respiration. It is a development for this purpose 
quite distinct from the mammalian diaphragm. It is not impossible 
that the dinosaurs possessed further developments of this arrangement 
of the heart and lungs, and that they owed some of their success to 
this mechanism. 

The modern crocodiles represent only the survivors of a once much 
more abundant group. Crocodilus is the most widespread genus, 
occurring in Central America, Africa and Asia, Malay and East 
Indies, and North Australia. Alligator, with each fourth lower tooth 
penetrating into a hole in the maxilla, is found in North America and 
in China. Caiman of Central and South America is related to Alligator. 
The length of the snout varies considerably in different species, and 
is extremely long and slender in the fish-eating Gavialis, Indian 
gharial, and Tomistoma of the East Indies. Crocodiles lay hard-shelled 
eggs in large clutches, depositing them in the sand or in nests com- 
posed of vegetation. The crocodiles seem to have changed little since 
they first appeared in the late Triassic, perhaps 190 million years ago. 
*Protosuchns of that time had a pelvis like that of crocodiles but was 
otherwise very like a pseudosuchian. There were numerous types of 
crocodile in the Jurassic and Cretaceous, living both in fresh water 
and in the sea. In these forms the palate was closed only as far back as 
the palatine bones; the addition of flanges of the pterygoids took 
place only in the Eocene crocodiles, which were numerous in many 
parts of the world, including northern continental regions that today 
are too cold for such animals. In spite of their specializations for 
aquatic life, the crocodiles show us many features that were present 
in the earliest archosaurs and they therefore give some idea of the 
characteristics of the ancestors of the pterodactyls, dinosaurs, 
and birds. 

15. The 'Terrible Lizards', Dinosaurs 

In the 10 million or so years at the end of the Triassic some of the 
descendants of the pseudosuchians became very successful and numer- 
ous and many of them were very large. The large size was not a 
characteristic only of one line but of two quite distinct ones, each with 
several sub-divisions. The term dinosaur is applied to all of them, but 
the two main lines have little in common beyond the characters 
common to all archosaurs. The desire to explain this extraordinary 
exuberance of reptiles has attracted much attention to these 

xv. 1 6 

Fig. 246. The skeletons of various saurischian dinosaurs. 
(Modified after various authors.) 

16. Order *Saurischia 

These include forms with a triradiate pelvis, very like that of the 
pseudosuchians. The earlier types, like their ancestors, were bipedal 
carnivores of no great size, such as *Compsognathus from the Jurassic 

xv. 16 THEROPODS 423 

of Europe and *Ornitholestes from that of North America (Fig. 241). 
The front legs were short, with 4 or 3 digits, provided with claws ; the 
pectoral girdle was reduced to scapula and small coracoid, with no 
trace of clavicles. Some members of this line, the theropods, soon 
developed into large carnivores, such as *Allosanrus (Fig. 246), over 
30 ft long (Jurassic, North America). These animals apparently 
swallowed their food whole and to help with this the quadrate was 
movable and there was a joint between the frontals and parietals, as 
in many lizards. In other respects the skull was very similar to that of 
the pseudosuchians. 

At the end of the Cretaceous this theropod line produced the largest 
carnivores that have appeared on the earth, such as *Tyrannosaurus 
rex, nearly 50 ft long and 20 ft high, from North America. All the 
previously mentioned tendencies were here accentuated, producing 
creatures with bipedal habit, very powerful head and jaws, and much- 
reduced fore-limbs. They presumably preyed upon the large herbi- 
vorous dinosaurs of the Cretaceous and became extinct with their 
prey, either from a common inability to meet the rigours of the climate 
or in competition with the mammals and birds. Throughout most 
of the Jurassic and Cretaceous the theropods were the dominant 
carnivores of the world, taking the place occupied earlier by the 
synapsid reptiles (p. 540) and later again by descendants of the synap- 
sids, the carnivorous mammals. 

In the Cretaceous the organization of this saurischian line also 
produced some exceedingly bird-like forms, *Struthiomimus and 
*Ornitho)ithnus, walking on three toes and having three also in the 
hand, one opposable and used for grasping. The skull became very 
lightly built and the teeth disappeared, possibly in connexion with an 
egg-eating habit (Fig. 246). 

All these carnivorous, bipedal saurichians may be grouped into a 
suborder Theropoda. Another line of organization, starting from 
bipedal, carnivorous Triassic theropods, adopted a herbivorous diet 
and reverted to the quadrupedal habit. These animals, the suborder 
Sauropoda, culminated in the immense Jurassic forms, * Apatosaurus 
(= *Brontosaurus) and *Diplodocus, the largest of all terrestrial 
vertebrates. Several stages of the transition from bipedal to quad- 
rupedal habit can be traced. * Yaleosaimis from the Trias was a bipedal 
creature 6 ft long but with rather long front and short hind legs. 
*Plateosaurns, also of the Trias, was 20 ft long, but still bipedal. Soon 
the front limbs became larger and more used for walking, though the 
disparity always remained. The neck was immensely elongated and 

424 REPTILES xv. 16- 

the head very small, with a lightly built skull. The nostrils lay on the 
top of the head and in *Diplodocus formed a single opening. This 
seems to indicate that the animals were aquatic or amphibious, as 
would in any case be suspected from the very large size, making it 
unlikely that the legs could bear the full weight. *Diplodocus and 
*Brachiosaurns were over 80 ft long and the weight of the latter must 
have been nearly 50 tons. However, the structure of the vertebral 
column shows that much weight was carried on the legs, for the verte- 
brae are strong, though hollowed in places. Footprints of the animals 
have been found. One or more of the digits bore claws. The skull 
became relatively short and broad, and among the many puzzling 
features of these giant animals is the weakness of the jaws and small 
size of the teeth, mostly crowded towards the front of the mouth. 
These teeth would have served well enough for cropping, but there 
are no teeth on the hind part of the jaws and no provision for grinding 
the food. Animals of large size can only have been supported by this 
feeble apparatus if some very nutritious food was readily available. 
This perhaps agrees with the small size of the brain, which was 
several times smaller than the lumbar enlargement of the cord. 

17. Order *Ornithischia 

The second main group of dinosaurs appeared later than the sauro- 
pods and possessed a 4-radiate pelvis, with the pubis directed back- 
wards and an extra pre-pubic bone pointing forwards. The teeth were 
restricted to the hind part of the jaws, the front bearing a beak. At the 
front end of the lower jaw there was an extra bone (predentary). 
These were herbivorous forms and they appeared in the Jurassic and 
achieved their maximum in the Cretaceous, by which time the sauro- 
pods had become less common. The earliest of the ornithischians 
were bipedal animals, included in a suborder Ornithopoda, from the 
Jurassic and Cretaceous. These animals, such as *Iguanodon, were 
built on the same general lines as the pseudosuchians, from which 
they were presumably derived. The skull was heavily built and adapted 
for a herbivorous diet, with powerful muscles attached to a coronoid 
process of the lower jaw. The bipedalism was less marked than in 
saurischians and the fore-limbs less reduced. Several separate lines 
then reverted to a quadrupedal habit. The trachodonts (*Hadro- 
saurus) were a very successful group of amphibious forms in the 
Cretaceous, with webbed feet. The teeth were suited for grinding, 
parallel rows being present, making as many as 2,000 teeth in one 
animal. In several types of hadrosaur the top of the head was pro- 

xv. i7 




Fig. 247. The skeletons of various ornithischian dinosaurs. 
(Modified after various authors.) 

longed in various ways, giving a structure that perhaps allowed the 
nostrils to remain above water while the animal was feeding below. 
These animals reached 30 ft in length and may have supplanted the 
sauropods as marsh-living forms, possibly when the soft foods gave 
place to harder plants. 

Other lines of ornithischians became more fully terrestrial and 
quadrupedal and were mostly heavilv armoured. Thus the stegosaurs 
of the Jurassic carried immense spines on the back and the tail bore 

426 REPTILES xv. 17- 

sharp spikes. The hind legs were much longer than the front, a relic of 
bipedal ancestry. The feet carried hoof-like structures. The skull was 
very small and the brain much smaller than the lumbar swelling of 
the cord. The teeth were in a single row and small. The ankylosaurs 
of the Cretaceous were covered all over with bony plates, somewhat 
in the manner of the mammalian glyptodonts (*Nodosaurus, Fig. 247). 
Finally, the ceratopsians, such as * Triceratops of the late Cretaceous, 
developed enormous heads, with huge horns and a large bony frill, 
formed by extension of the parietals and squamosals to cover the neck. 
These later Cretaceous animals appear to have lived on dry land and to 
have walked on all fours, although the bipedal ancestry is shown in 
the shortness of the front legs. There are several indications that the 
climate at the close of the Cretaceous was becoming drier and the 
organization of the giant reptiles became modified accordingly. They 
survived successfully for a while, but were ultimately replaced by the 
mammals, perhaps as a result of still further change in the climate 
(see p. 538). 

18. Order *Pterosauria 

The Triassic archosaurian reptiles gave rise to two independent 
stocks that took to the air, the pterodactyls and the birds. Both of 
these appear first in the Jurassic as animals already well equipped for 
flight, although obviously basically of archosaurian structure. We 
cannot therefore say anything about the steps by which their flight 
was evolved and can only speculate about the influences that drove 
them to take to the air. The early archosaurs were bipedal animals, 
and the fore-limbs were therefore free and available for use as wings. 
There has been much speculation about the intermediate stages by 
which flight was produced. Other reptiles, such as Draco, the flying 
lizard (p. 407), develop a membrane between the limbs and the body 
to assist them in making soaring jumps. The flight of pterodactyls 
and birds may have originated thus or, as suggested by Nopcsa, by 
the flapping of the fore-limbs during rapid running on the ground, 
the animals then becoming airborne for longer and longer periods. 

The stages of the evolution of flight may have been different in the 
two cases, for whereas the birds are obviously bipedal animals and the 
similarity to such reptiles as * Strnthiomimus and *Ornithomimus is 
obvious, the pterodactyls probably could not walk on their hind legs 
and may have used the wing more for soaring than for flapping flight. 
In spite of great differences there are interesting parallelisms in the 
structure of the fully evolved fliers of the two groups, for instance the 

xv. 1 8 



limb bones became light, the skull bones fused, and the jaws toothless 
and beaked. This parallelism in lines known to be distinct, although 
of remote common origin, is similar to that which we have noticed 
before in aquatic animals, and it can be interpreted as showing that 


Fig. 248. The skeleton of a pterodactyl. 

A, extra wrist bone; C, coracoid; D, elongated digit; F, femur; FF, fin; H, humerus; 
MC, metacarpal; P, pelvis; RU, radio-ulna; SC. scapula; ST, sternum; 7', tail; TF. 
tibio-fibula; lowing. (From Thompson, The Biology of Birds, Sidg\vick& Jackson, Ltd.) 

populations with similar genotypes will respond to similar environ- 
mental stimuli in the same way. 

The pterodactyls are most commonly found in the Jurassic strata, 
less often in the Cretaceous. Many specimens have been found in 
marine deposits and seem to have been fish-eaters. The characteristic 
features that have produced the pterodactyl structure from a thecodont 
ancestry may be described as a lengthening of the head and neck, 
shortening of the body and ultimately of the tail, lengthening of the 
arms and especially of the fourth digit, shortening of the legs, and 
development of the ventral parts of the limb girdles. These are the 

428 REPTILES xv. 18- 

changes that can be recognized in the bony parts available for study; 
no doubt there were many others in the soft parts also paralleling the 
evolution of birds, for instance the animals may have been warm- 
blooded. However, there is no evidence that they possessed feathers; 
the wing was a membrane (patagium). 

*Rhamphorhynchns of the Jurassic is still recognizably of archo- 
saurian structure, especially in the skull, which has two fossae and 
large forward-sloping teeth (Fig. 248). The fore-limb was elongated, 
but the carpus still short, with an extra 'pteroid' bone in front, pre- 
sumably to support the wing. The first three digits were short and 
hooked, the fourth long, supporting the wing, and the fifth absent. 
The hind-limb was slender, with five hooked digits. There was a long 
tail, ending in an expanded 'fin'. Both girdles had well-developed 
ventral regions and there was a large 'sternum', keeled in front. The 
scapula articulated directly with the vertebral column. 

*Ptera?wdon, of the Cretaceous, showed further modifications. The 
trunk became shortened to ten or fewer segments and the fore-limb 
further lengthened, the carpus being long and the fourth digit much 
longer than the other three. The hind-limb remained small and the 
tail became very short. The very large and elongated head gradually 
lost its teeth, presumably acquiring a horny beak. In the latest forms 
the skull was drawn out backwards into an extraordinary process. 
Some earlier related forms were only a few inches long, but *Pterano- 
don itself, of the late Cretaceous, had a wing-span of 25 ft. 

Zoologists have not yet succeeded in reconstructing the life of these 
animals, and it is hard to see how they could have walked on land. 
The membrane, which stretched between both legs and the body, and 
perhaps also included the head, must have been easily torn. The 
feathers of birds can be ruffled without breaking and the loss of a few 
does no great harm: the bat's wing can be torn, but at least it is 
supported by many digits, whereas that of the pterodactyl was a huge 
continuous membrane supported by a single finger. Again it is difficult 
to see how the animals can have perched ; if they hung, as the claws 
suggest, was it with the front or with the hind legs? And how can 
they have staged a take-off, which in birds is greatly helped by the 
jump of the hind legs? It is possible that they always came to rest 
hanging from cliffs, which they could leave by soaring. Even the flight 
itself presents many difficulties. Although there is a sternum and a 
strong humerus, neither suggests the presence of muscles sufficiently 
strong to carry a creature as large as *Pteranodon. We cannot solve any 
of these mysteries, but one clue is that the biggest pterodactyls were 


mostly, if not all, marine. The largest flying birds alive today are the 
albatrosses, which use their great weight to gain height with the 
increasing velocity of the wind a few feet above the sea (p. 460). It is 
possible that the pterodactyls used a similar method of soaring. They 
were presumably unable to compete with the birds, however, and died 
out at the end of the Cretaceous, along with so many other reptiles. 

19. Conclusions from study of evolution of the reptiles 

Many of the conclusions that have been drawn from study of verte- 
brate evolution in the water also apply to the forms that have come 
on land. The fossil record leaves no doubt that almost all the popula- 
tions have changed very markedly. Few forms of reptile alive today 
are closely similar to any found in the Permian or Triassic periods. 
Sphenodon has shown relatively less change than most others ; it may 
be significant that it is found in an isolated island region (but see 

P- 772). 

The data are not sufficient to show the rate of evolutionary change. 

We cannot be sure whether it has been constant or even continuous, 

but particular types are found only from a limited range of strata and 

there is little evidence that any terrestrial form remains unchanged for 

more than a few million years, at most. Each type is successful for a 

while and then the niche that it fills becomes occupied by another 

type, either descended from the first or, more usually, from some 

related stock. Thus the earliest large land herbivores were probably 

the pareiasaurs; these were replaced by other reptilian types such as 

the herbivorous mammal-like reptiles, and later the sauropods (in so 

far as these were terrestrial) and various types of ornithischians ; then 

perhaps by the hadrosaurs in the more watery habitats and the stego- 

saurs, ankylosaurs, and ceratopsia on drier ground. Finally, all these 

gave place to the earliest mammalian herbivores, which were in turn 

replaced by others (p. 776). 

Throughout early tetrapod evolution there is a tendency to return 
to the water, perhaps under some pressure of competition from 
descendants on land. This is marked among reptiles, where besides 
the chelonians and ichthyosaurs and plesiosaurs there are the phyto- 
saurs and crocodiles, and among Squamata the mosasaurs and tylo- 
saurs, not to mention the sea-snakes. 

The large size of many reptiles has been one of their most striking 
features, but it is, of course, not true to say that there is a strong 
tendency for size to increase in all reptile groups. While many 
have become enormous, others, such as the lizards, have produced 

43 o REPTILES xv. 19 

probably as great a biomass spread over a large number of small in- 
dividuals. Large size in a reptile may help to conserve heat (p. 372), 
but could also endanger the animal from overheating, since the ratio 
of surface area to volume decreases as the absolute size increases, and 
heat cannot be lost so readily through the skin. Up to a point size may 
be a protection, but it involves the dangers of those who place all the 
eggs in one basket ; incidentally, the actual eggs of these large animals 
must have provided formidable physical problems for their support. 

Parallel evolution of several lines descended from a single stock is 
as common among reptiles as among other groups of vertebrates. 
Thus the bipedal habit, with hind legs longer than the front, has been 
adopted independently by a number of diapsids; again, elongated jaws 
are found among fish-eaters, whether ichthyosaurs, plesiosaurs, phyto- 
saurs, crocodiles, or mosasaurs. 

Although it is difficult to see in all this any persistent tendency 
except to change, yet the very fact that each type is so rapidly replaced 
suggests that descendants in some way more efficient are continually 
appearing. In the case of the reptiles the more interesting of these 
are the birds and mammals, and we shall therefore leave the problem 
of serial replacement among amniotes for later discussion. Meanwhile 
we may note once again that the reptiles surviving today, although not 
of larger size nor obviously better suited for life than their mesozoic 
ancestors, yet exist in considerable numbers alongside and even in 
competition with the birds and the mammals. 



1 . Features of bird life 

The quality we define as 'life' is perhaps more fully represented in 
birds than in other vertebrates, or indeed in any animals whatsoever. 
It is difficult to find units by which accurate comparisons can be made 
of such matters, but there is a meaning in the statement that the life of 
a bird is more intense than that of, say, a reptile or a fish. Following 
out our definition of the life of a species as the total of the activities by 
which that particular type of organization is preserved, we shall find 
that the birds have many and very varied activities, by means of which 
a great deal of matter is collected into the bird type of organization. 
Moreover, this is achieved under conditions remote from those in 
which life first arose; the birds get a living by moving in the air, the 
most difficult medium of all. 

Flight is of course the characteristic that gives us most fully the 
feeling that the birds are active animals ; it impresses us as a technical 
marvel and as a means by which the animals obtain a most enviable 
and valuable freedom, enabling them to avoid their enemies and to 
seek new habitats. Almost equally important items in the active life of 
birds are the high and constant temperature and large brain. These 
features have been acquired independently by birds and mammals, 
and have led to profound changes in behaviour. A homoiothermic 
animal does not need to change its activity with the changes in environ- 
mental temperature; it can be continuously active, and, perhaps even 
more important, its steady continuity of life makes possible the accurate 
recording of past experience in the memory. Probably only with a high 
and constant temperature can full use be made of the possibilities of 
delicate balance of activities within large masses of nervous tissue. In 
homoiothermic birds and mammals we find larger brains and more 
elaborate social and family habits than in any other animals. 

2. Bird numbers and variety 

Flight necessitates a large surface-weight ratio, therefore birds do 
not become so large as some mammals; nevertheless, an immense 
biomass is produced by their very large numbers. Any attempt to 
enumerate the bird population is largely guess-work, but the density 
of breeding birds in different habitats in Britain has been estimated, 

432 THE BIRDS xvi. z- 

and varies from 200 per 10 acres in woodland to 20 on agricultural land 
and 10 or less on moorland. Calculating from such figures Fisher 
estimates that there may be 100 million land birds in Great Britain 
and 100,000 million birds in the world altogether, including sea birds. 
This is perhaps a low estimate ; it would represent a total biomass of 
the same order as that of 3,000 million human beings. With all their 
activity, therefore, the birds organize less matter into themselves than 
do the mammals. 

One of the most striking features of bird life is that although the 
basic organization remains fairly constant differing types show a great 
variety of special features, fitting them for numerous habitats. Besides 
differences in behaviour, in body form, and in powers of flight there 
are found others in the shape of the bill, and hence of food habits, and 
in the details of many other parts, such as the feet, that make fascinat- 
ing studies in adaptation to environment. 

3. The skin and feathers 

The skin of birds differs from that of mammals in being thin, loose, 
and dry; there are no sweat glands, indeed the only cutaneous gland 
present is the uropygial gland or preen gland at the base of the tail. 
The bird cleans its feathers with its beak, obtaining oil from this gland, 
which is especially well developed in aquatic birds. 

The keratin-producing powers of the skin are of course mostly 
devoted to producing feathers, but scales like those of reptiles are 
present on the legs and feet and sometimes elsewhere. The bill (p. 466) 
and claws are also specialized scale-like structures and are sometimes 

Nerve-endings are present throughout the skin, and the cere at the 
base of the bill is perhaps an organ of touch. The bill may itself have 
special endings, such as the corpuscles of Grandry found in the ducks. 

The feathers of modern birds provide a covering whose uses vary 
from heat insulation and flight to protective coloration and sexual 
display. It is likely that in evolutionary history the function of heat 
regulation came first. The two main functions of heat conservation and 
flight are indeed today performed by feathers of different types (Fig. 
249). The down-feathers or plumules, which form the covering of the 
nestling and may be present also in the adult, are simpler than the 
contour feathers or pennae, and the elaborate flattened flight feathers. 
Filoplumes are a third type, being very fine, hair-like feathers. Usually 
several generations of feathers are produced ; first the nestling feathers 
(neoptiles), then one or more generations of juvenile feathers, which 

xvi. 3 



Fig. 249. Various types of feather. 

A, filoplumes; B, nestling down-feather; C, primary wing feather of pigeon; D, permanent 

down feather; E, feather with free barbs; F, emu's feather with long aftershaft; G, contour 

feather of pheasant with aftershaft. (Partly after Thompson, The Biology of Birds, 

Sidgwick & Jackson, Ltd.) 

may be of various types, prefiloplumes, preplumules, and prepennae; 
finally, the adult feathers (teleoptiles). 

Each feather, of whatever type, is formed from a dermal papilla or 
follicle, over whose surface keratin is produced. In down-feathers the 

434 THE BIRDS xvi. 3 

surface of the papilla is ridged all round and the result is to produce a 
number of fine threads or barbs of keratin, covering the body with 
a coat of fluff, which acts as a heat insulator by preventing air circula- 

Feathers, like other epidermal structures, are moulted, either at a 
certain stage in the life-cycle or seasonally, a new generation being 

d flflb 

v. r / 

Fig. 250. The structure of a feather. 
I. Whole feather showing calamus (quill), C; rhachis (shaft), R; and vane, V. On the right 
side a small area is shown as it appears under a lens; B, barb; Bs, barbule. II. A section cut 
at right angles to two barbs in the plane of the barbules of the anterior series (Bsa). Note 
how the hamuli, H, of the anterior barbs interlock with ridges (r) on the posterior barbules 
{Bsp). III. Shows one anterior and two posterior barbules isolated. (After Pycraft, A History 
of Birds, Methuen & Co., Ltd.) 

produced from the old papillae. Most birds moult after the breeding- 
season, some a second time during the year. The down-feathers of the 
nestling are partly replaced by contour feathers; the follicle, instead 
of producing equal barbs, now forms two large ones at one side, which 
together become the central axis (rhachis), carrying a series of further 
barbs that spread at right angles to it to form the vane (vexillum). Each 
feather (Fig. 250) thus consists of a central rhachis, forming the hollow 
calamus or quill below and carrying the barbs, which make the vane. 
The calamus opens at the base by the inferior umbilicus, the entrance 
of the mesodermal papilla, and at the beginning of the vane there is a 
second hole, the superior umbilicus. At this point there is often a loose 

xvi. 3 FEATHERS 435 

tuft of barbs or an extra shaft, the aftershaft, perhaps in some way 
representing the down-feather. 

The barbs or rami that make up the vane are held together by rows 
of barbules (radii) running nearly at right angles to the barbs and 
carrying hooks (hamuli) by which the barbules of one radius become 
fixed to grooves in those of the next (Fig. 250). Anyone who has played 
with a feather knows that these connexions can be broken down so that 
the barbs become separate, but can be joined again by 'preening' the 
whole feather. 

The feathers are provided with muscles at the base and the control 
of their position is important for the regulation of heat loss, for flight, 
and in many other activities, for instance sexual display. Like the hairs 
of mammals the feathers are also used as organs for the sensation of 
touch, nerve-fibres being wound round the base of the papilla. In owls 
and other night-birds special vibrissae, analogous to those of mam- 
mals, are present. Various specialized feathers are used for eyelashes, 
ornament, and other purposes, and in some birds patches of special 
feathers without rhachis break up to make a greasy 'powder down'. 

The feathers are not spread uniformly over the body but are localized 
to certain tracts, the pterylae, separated by bare areas, apteria. Among 
the contour feathers it is usual to recognize the remiges of the wing 
and rectrices of the 'tail'. The former are divided into primaries on 
the hand and secondaries on the forearm (Fig. 256). Each large feather, 
whether in wing or tail, is usually covered above and below by several 
rows of upper and under coverts. In many birds there is a peculiar gap 
in the secondary feathers of the wing, the fifth remex feather being 
absent (diastataxis); the condition in which this feather is present is 
called eutaxis. The feathers have a remarkably flexible structure, so 
that they adopt different shapes with different positions of the wing. 
The shape of the quill and barbs varies between feathers and parts of 
a feather, for instance the barbs at the tip of the primary feathers 
provide a stream-lined cross-section, like that of certain aeroplane 
propellers (p. 453). The small covert feathers at the front of the wing 
stand up vertically, but have a right-angle bend, thus providing the 
wing camber. 

The rectrices vary greatly, being almost absent in birds that live 
near to the ground, such as the wrens, but very large in fast-moving 
birds that change direction quickly (swallows). In these latter the outer 
rectrices are enlarged for steering purposes. The rectrices may be put 
to special uses, as in the woodpeckers, where they make a rigid brace, 
or in the peacocks, whose display feathers are the tail coverts. 



xvi. 4- 

4. Colours of birds 

Birds possess colour patterns more vivid than those of any other 
vertebrates, using them not only for concealment but also as the chief 
means of recognition and sexual stimulation and hence as the basis of 
their social life. Like other animals that live far from the ground and 
move fast (primates) the birds have a poor sense of smell, often none 

at all, but they have very good 
vision, and in many species the 
turning of discriminating eyes 
by one sex upon the other has 
led to the development of a very 
gorgeous covering. The feathers 
alter the appearance of the bird 
so completely that it is not fan- 
tastic to compare their effect with 
that of clothing in man. 

As in other animal groups the 
colours are produced partly by 
pigments and partly by reflection 
and diffraction effects (structural 
coloration). The most common 
pigments are melanins, ranging 
from black through brown to 
yellow, and laid down in the 
feathers by special cells in the 
papilla. The processes of these 
amoeboid chromatophores con- 
vey pigment to the epidermal cells 
(Fig. 251). Carotenoid pigments 
(soluble in organic solvents) are also found, such as the yellow xantho- 
phyll of the duck's bill and feet and the red astaxanthin of pheasant 
wattles. White is usually given by reflection. In blue colours incident 
light is reflected from a turbid porous layer overlying a deposit of 
melanin pigment. In iridescent feathers interference of light in thin 
surface films gives colours like those of soap bubbles. The more 
specialized iridescent feathers produce Newton's rings, with colours 
of the second and even third orders. The turacos or plantain-eaters of 
Africa contain two very peculiar pigments, a copper-containing red 
porphyrin turacin, which is soluble in weakly alkaline water and dis- 
solves out in the rain, and the green, iron-containing turacoverdin. 

Fig. 251. Deposition of pigment in feather 
germ. Transverse section through a develop- 
ing arm feather. 

c.b. cell body of pigment cell; p. process of pig- 
ment cell; r. cells forming a radius; sh. sheath of 
feather germ. (After Strong, from Streseman.) 

xvi. 5 COLOURS OF BIRDS 437 

The actual colour patterns vary with the habits of the bird. Con- 
cealing (cryptic) coloration is very common; even the brighter colours 
may serve this purpose, by breaking up the outline of the bird when at 
rest or in motion. Most birds are dark above and white below. The 
feathers often show mottled or speckled patterns rather than a homo- 
geneous colour. Finches and other birds living in the sunlit upper 
branches show bright yellow, yellow-green, and blue colours, either 
singly or combined. Birds living in thickets, such as the thrush and 
blackbird, are usually duller brown or black. An example of disruptive 
coloration that is easy to observe is the white patch on the throat of a 
thrush. If the nest is approached while the bird is sitting the head is 
held rigidly still with the beak upwards ; the white mark on the neck 
breaks the outline and instead of an obvious bird's head there appear 
only the meaningless shapes of the sides of the jaws. In most species 
coloration is a compromise between concealment and conspicuous- 
ness. Sometimes selection has acted so that the female is cryptic, the 
male conspicuous (e.g. ducks). In hole-nesting shelducks both sexes 
are conspicuous. In other birds bright colours are concealed most of 
the time (e.g. the robin's red breast is underneath, many waders have 
conspicuous colours under their wings). 

Some colour patterns seem to make the bird conspicuous and may 
be a warning of a distasteful quality. The black and white pattern 
shown by the magpie may be an example of such sematic coloration; 
certainly this bird is seldom preyed upon, no doubt partly because of 
its large size. The conspicuous black of rooks and starlings may be 
connected with their social life, making it desirable that the birds 
should easily follow each other, the group being protected by the com- 
bined receptors of its many members and the quick response of all 
to escape movements by any one. 

The protective functions of the colour often give place in one or 
both sexes to garments used for communication between individuals, 
for such purposes as pair formation, aggression between males, nest 
site selection, or rearing the young. 

5. The skeleton of the bird. Sacral and sternal girders 

The arrangement of the whole locomotor apparatus is based on the 
plan of the bipedal archosaurian reptiles, modified and simplified for 
the purposes of flight and balancing and walking on two legs. The 
bones are very light and often of tubular form, but sometimes with 
internal strutting well suited to the stresses they must bear (Fig. 252). 
Many of the bones contain extensions of the air-sacs; even the wing 

438 THE BIRDS xvi. 5 

and leg bones are pneumatized in this way in very good fliers, such as 
some birds of prey and the albatross. Fusion of bones has proceeded 
so far that the skeleton consists of a few hollow girders and large 
plates of special shape (p. 441). This result is achieved by limiting 
the joints at which movement occurs and simplifying the muscular 
system. The long bones ossify from a single diaphysis, there are no 
epiphyses at the ends. 

The skeleton of the backbone and limb girdles is so modified as to 
allow the weight of the body to be carried in two quite distinct ways, 

Fig. 252. Metacarpal bone from the wing of a vulture, sectioned to show the 
arrangement of the struts similar to that known to the engineer as a Warren's truss, 
such as is often used in aeroplane wings. (After Prochnow and D'Arcy Thompson.) 

on the wings or on the legs. For this purpose there are two plate-like 
girders, the sternum and the synsacrum, curved in opposite directions. 
The muscles around the shoulder and hip joints balance the weight 
on these girders and produce propulsion. The main thrusts come from 
the pectoralis major in flying and from the leg retractors in walking. 
Perhaps no other animals are suited so perfectly for locomotion by two 
distinct means, and of course many birds can swim as well as fly and 

The whole axis of a bird is morphologically shorter than that of any 
other vertebrate except a frog or a tortoise (Fig. 253): only the neck 
remains a long and mobile structure. The number of cervical verte- 
brae varies and is greater in the birds with longer necks; there are 
fourteen in the pigeon, if we include two that bear ribs not articulating 
with the sternum. The cervical centra have saddle-shaped surfaces, 
the concavity running from side to side on the front and up and down 
behind, allowing great mobility in all directions. 

There are four or five thoracic vertebrae, all except the last united 
into a single mass. The ribs are large, double-headed, and jointed to 
the vertebrae. They bear uncinate processes on their vertebral por- 
tions, hook-like projections overlapping the rib next behind and thus 
strengthening the whole thoracic cage. There is a well-marked joint 

xvi. s SKELETON 439 

between the vertebral and sternal portions of the ribs. The latter are 
bony, not cartilaginous as in mammals, and are jointed to the sternum, 
which is a very large keeled structure in all flying birds, serving to 

(1 thoracic, 5 lumbar 
Z sacral, S caudal ) 


Fig. 253. Skeleton of the pigeon (Columba). 

at. atlas; fl.v. axis; C12, 12th cervical vertebra; car. keel of sternum; carp, carpus; cor. cora- 
coid; c.r. cervical rib; delt.r. deltoid ridge of humerus ; fern, femur ;fib. fibula ;fur. furcula; 
hyp. hypapophysis; il. ilium; isch. ischium; m. auditory meatus; mc. 2 and 3, metacarpals; 
pub. pubis; pyg. pygostyle; rad. radius; sc. scapula; St. body of sternum; tar. met. tarso- 
metatarsus; tib.tar. tibio-tarsus; uln. ulna; up. uncinate process; vac. vacuity in side of skull. 

carry the weight of the body to the wings by the attachment of the 
main wing muscles (Fig. 254). The pectoralis major, which depresses 
the wing in flight, is attached to the edge of the sternum and the great 
depth of the keel serves to increase the length and mechanical advan- 
tage of the fibres of the muscle and also, by its shape, to strengthen 
the sternum. When the bird is in the air the sternum is carrying a large 
part of the weight. By this arrangement the centre of gravity is kept 
well below the centre of pressure, giving great stability. 

44° THE BIRDS xvi. 5- 

The last thoracic (rib-bearing) veitebra is united with about five 
that can be regarded as lumbars, two sacrals and five caudals to make 
a synsacrum, which is also fused with the ilium. This produces a very 
thin plate-like structure, whose ridged shape gives it sufficient strength 
to carry the bird's weight. Finally, there is a short bony tail of about 
six free caudal vertebrae, carrying four that are fused together to form 
the upturned pygostyle, supporting the tail feathers. 

The joints of the vertebral column are therefore reduced so as to 
allow movement only in the cervical region, between the thorax and 


Fig. 254. Diagrams of the pectoral and pelvic girdles of an eagle, to show the methods of 

support in flying and walking. In each case the weight is carried on an arch, the strength 

of which is obtained by the peculiar kinked shape of the thin sheets of bone. 

synsacrum and in the tail. The axial muscles have been correspond- 
ingly reduced. Those of the neck are large and the hinder cervical and 
the thoracic vertebrae have special ventral hypapophyses for attach- 
ment of the flexor muscles of the neck. The other back muscles, except 
those of the tail, are reduced and the whole back forms a single rigid 
strut, carrying the weight of the breast and viscera through the ribs 
and the abdominal muscles either to the pelvic girdle or to the sternum. 
In flying this weight is suspended on the wings and there is therefore 
a compression stress throughout the ribs, and this no doubt accounts 
for the ossification of their ventral parts. The weight of the bird when 
resting on its wings (Fig. 254) is thus carried by the pectoralis major 
as a tension member, through the plate-like sternum; the ribs, and 
especially the coracoid, act as compression members. The last-named 
bone lies nearly in the plane of the pectoralis major and is very strongly 

6. The sacral girder and legs 

In standing, perching, and walking the weight is balanced on two 
legs. To achieve this posture the type of girder found in the vertebral 

xvi. 6 SACRAL GIRDER 441 

column of other terrestrial vertebrates has been abandoned, and with 
it the system of braces (back muscles) holding up the weight of the 
forepart of the body. Instead the whole axis is so shortened that the 
centre of gravity lies far back, low, and over the feet. This is not 

Fig. 255. Diagram of muscles of the hind leg of a bird. Tendons shown dotted. 

1, Mm. ilio-trochanterici; 2, M. ilio-femoralis; 3, M. obturator; 4, M. ischio-femoralis; 
5, M. caud-ilio-femoralis; 6, M. pub-ischio-femoralis; 7, M. ilio-tibialis posterior; "ja, 
M. ilio-tibialis anterior; 8, M. sartorius (ilio-tibialis internus); 9, M. femoro-tibialis medius ; 
ga, M. femoro-tibialis externus; 11, M. ilio-fibularis; 12, M. ischio-flexorius; 13, M. 
caud-ilio-flexorius; 14, M. gastrocnemius; 15, M. peroneus superficialis; 16, M. peroneus 
profundus; 17, M. tibialis anterior; 18, Mm. rlexores digitorum; 19, Mm. extensores 
digitorum. si. sling for M. ilio-fibularis. (After Stolpe.) 

apparent from Fig. 255, which is not in a normal perched position. 
Birds whose feet are placed far back for swimming must hold the body 
nearly upright to achieve a stable position with the centre of gravity 
over the feet (auks, penguins). The ribs and abdominal muscles trans- 
fer the weight to the greatly elongated ilia, which are fused to the 
vertebrae, making a long girder of approximately parabolic form. 
Though this is composed of bone of almost paper thinness, it is 
strengthened by longitudinal ridges (Fig. 254). Its strength, like that 
of the sternum, lies not in its arched shape in the transverse plane, but 
in the distribution of weight that is achieved by its longitudinal curve 
and peculiar kinked shape. The whole pelvic girdle is modified to allow 


Fig. 256. Dissection of pigeon from back. 

c-h. coraco-humeral; caud-il-fem. caud-ilio-femoralis; delt. deltoid; e.c.r. extensor carpi 
radialis; ex.dig. extensor digitorum; ex. poll, extensor pollicis; fl.dig. flexor digitorum; 
fl.met.uln. flexor metacarpi ulnaris; fl. poll. long, flexor pollicis longus; gastr. gastrocnemius; 
il-caud. ilio-caudalis; il-fib. ilio-fibularis (cut); il-tr. ilio-trochantericus; int. interosseus; 
isc.f. ischio-femoralis; lat.d. latissimus dorsi; lat.lig. lateral ligament of knee; m. external 
auditory meatus; n. sciatic nerve; nos. nostril; per. peroneus; pub. isc. fern, pub-ischio-femo- 
ralis; rh. rhomboid; sart. sartorius; sc. scapula; s.c.h. scapulo-humeral (cut); serr. serratus 
anterior; 5/. sling for tendon of ilio-fibularis; t. tongue; tend, tendon of pectoralis minor; 
tens. ace. tensor accessorius; tens. long, tensor longus; tri. triceps; uropygial gland; 

vin. vinculum elasticum. 

xvi. 6 LEGS 443 

this arrangement. The ischium and pubis are directed backwards and 
do not meet in a symphysis, which would prevent the underslinging 
of the viscera. 

The legs are used for balance and walking or hopping in ways that 
show interesting similarities and differences from those of man. The 
femur is turned under the body and articulates with the acetabulum 
in such a way that movement is almost restricted to the antero- 
posterior direction. The bird balances on its hips only in the sagittal 
plane; there are no movements of abduction and adduction such as are 
found in man. Abduction of the leg, or the falling medially of the 
bird's body when standing on one leg, is prevented by the fact that 
besides the ball and socket articulation of the femoral head there is 
also a second joint surface between the trochanter and an anti- 
trochanter of the ilium. The ligaments across the top of this joint are 
very strong and they limit abduction movements, while movements 
of adduction are restricted by a strong ligamentum teres attached to 
the femoral head. 

In life the femur is held nearly horizontal, bringing the legs well 
forward. The bird replaces the movements of abduction and adduc- 
tion, which we make at the hip during walking in order to prevent 
falling over while only one leg is on the ground, by movements of 
rotation at the knee. The muscles around the hip joint form a system 
of braces allowing balancing and locomotion much as in man, but they 
are well developed only anteriorly and posteriorly; the lateral and 
medial (abductor and adductor) elements are weak (Figs. 255-8). The 
anterior group (protractors) includes a sartorius (ilio-tibialis internus) 
running from the ilium to the tibia, an ilio-femoral, and a large 
anterior ilio-tibial inserted through a patella to a ridge on the front of 
the tibia. Associated with this muscle, w*hich crosses both hip and 
knee joints, there are also, as in man, femoro-tibial muscles, making 
up with the longer muscles, the extensor system of the knee. 

The lateral side of the hip joint is supported by rather small ab- 
ductor braces, the ilio-trochanteric muscles, corresponding to our 
glutei, and acting mainly as medial rotators, opposed by obturator and 
ischio-femoral muscles, which work as lateral rotators. The main loco- 
motor muscles are the posterior braces or retractors, lying behind the 
hip joint and including muscles know r n as the posterior ilio-tibial, 
ilio-fibular, caud-ilio-flexorius, pub-ischio-femoral, ischio-femoral, 
and caud-ischio-femoral. Some of these also act with the obturator 
muscle as lateral rotators, and those placed more medially function 
as adductors or medial braces, so far as such are required. 

444 THE BIRDS xvi. 6 

The femur articulates with both tibia and fibula at the knee. The 
fibula is distinct at its upper end, fused with the tibia below. The 
joints of the foot are greatly simplified by the union of the proximal 

Fig. 257. Leg of pigeon dissected from lateral side. 
amb. ambiens tendon; flexors of distal phalanges ; fib. fibula; gastr. gastrocnemius; 
il-fib. ilio-fibularis; il-tib. ilio-tibialis; isch-fl. ischio-flexorius; lig. lateral ligament of 
knee; peron.brev. peroneus brevis; peron.long. peroneus longus; flexors of proximal 
phalanges; sort, sartorius; sen. sciatic nerve; si. sling for tendon of ilio-fibularis; t.t. tibio- 
tarsus; tarso-metatarsus. 

tarsals with the tibia to make a tibio-tarsus, articulating at an inter- 
tarsal joint with the remaining three tarsal and metatarsal bones, fused 
to make a single tarso-metatarsus. There are usually four digits arti- 
culating with the tarso-metatarsus; three directed forwards and one 
backwards. In standing, the weight is usually balanced in tripod 
fashion on three of the four points provided by the front and back 
portions of the feet. 


Fig. 258. Pigeon dissected from ventral surface. 

amb. ambiens; bas. bastard wing; br-rad. brachio-radialis; b. biceps; b.t. biceps tendon; 
caud-il-flex. caud-ilio-flexorius; cl. clavicle; coraco-brachialis; cor. coracoid; d.II. 
2nd digit; e.c.r. extensor carpi radialis; ex. extensor; ext.obl. external oblique; fl.carp.uln. 
flexor carpi ulnaris; gastr. gastrocnemius; oes. oesophagus; il-tib. ilio-tibialis; int. obi. 
internal oblique; lig. lateral ligament of knee; nic. nictitating membrane; pect. pectoralis 
major; p.m. pectoralis minor (supracoracoideus); per. long, peroneus longus; pr.long. pro- 
nator longus; pub-isc-fem. pub-ischio-femoralis; sart. sartorius; tens.acc. tensor accessorius; 
tib.ant. tibialis anterior; trac. trachea; tri. triceps; uln. ulnar. 

446 THE BIRDS xvi. 6- 

The knee joint has some remarkable similarities to that of man. It is 
stabilized by lateral, medial, and cruciate ligaments and contains a pair 
of lunate cartilages or 'menisci'. The joint allows movements of flexion 
and extension and the femur as it extends on the tibia in walking 
rotates laterally because of the arrangement of the joint surfaces. The 
bird thus balances in the medio-lateral plane by rotation at the knee, 
somewhat as we do by abduction-adduction at the hip (Fig. 259). 
When it makes a step forward the weight is brought by this rotation 
at the knee over the leg that remains on the ground. 

Fig. 259. Drawings from photographs of a goose, A, standing; B, step- 
ping. The centre of gravity S is brought over the foot on the ground by 
lateral rotation of the femur on the tibia. Note the position of the tail 
in B. (After Heinroth, from Stolpe.) 

The intertarsal joint allows mainly movements of flexion and exten- 
sion. It is largely supported by ligaments and has a very strong capsule 
and lateral and cruciate ligaments rather like those of the knee; there 
is even a meniscus on the lateral side. The back of the tibia is occupied 
by the gastrocnemius and the flexor muscles of the toes and at the front 
there is a tibialis anterior acting across the inter-tarsal joint, and also 
extensors of the toes. The calf muscles are mainly concerned with pro- 
ducing flexion of the toes in the act of perching and they form an 
elaborate system of tendons attached to the phalanges. These tendons 
often act as a single unit, and there is an arrangement by which the 
flexion is passively maintained by the weight of the body, even during 
sleep. Many of the muscles are specially arranged to allow support of 
the joint whether in the flexed or extended position. The ilioflbular 
muscle passes through a conspicuous sling for this purpose (Figs. 255 
and 257). The flexor muscles of the toes are inserted largely above the 
knee and thus tend to tighten as the bird sinks. In this they may be 
assisted by the ambiens, a muscle found in reptiles and some birds, 
which takes origin from the ilium. The muscle belly lies on the medial 


side of the thigh, and its tendon runs beneath the patella on to the 
lateral surface of the lower leg, where it is attached to the upper end 
of the muscles that flex the toes. This arrangement provides a single 
string crossing hip, knee, and ankle and allows the weight of the body 
to flex the toes as the joints bend. 

The second mechanism for maintaining the bird on its perch is a 
locking device that holds the toes flexed. The under-surface of the 
flexor tendon is ridged at the metatarso-phalangeal joint, where the 
weight of the body presses it against a branch. The upper side of 
the tendon sheath is also ribbed and as the bird settles on its perch 
the two sets of ridges interlock. 

The feet show a wide variety of adaptations for special habitats (Fig. 
260). In the cursorial and walking birds there are often long digits in 
front and behind to give a long base for balance, but the number may 
be reduced — to two in running birds, such as the ostrich. Hopping is 
used by small birds on the ground and in the trees and produces quick 
movement. It is expensive because of the large displacements of the 
centre of gravity, and for long distances or large animals walking is 
more efficient. Many different groups of birds have acquired webbed 
feet for swimming. In birds exposed to cold the digits may be enclosed 
in a coat of feathers. Birds of prey develop long raptorial talons. 
Throughout the great group of perching birds one digit is directed 
backwards, allowing firm grasp of a branch. In climbing birds the 
fourth digit is often directed backwards as well as the first, so that the 
foot forms a sort of pincer, with long curved claws. 

7. Skeleton of the wings 

The wing is designed to have a minimum moment of inertia about 
an axis parallel to the sagittal plane and passing through the shoulder 
joint. Movements are produced by muscles lying either outside the 
arm or in its proximal part, with long tendons. The wing feathers are 
carried along the post-axial border of the humerus, ulna, and hand, 
and the shape of the wing depends on the position in which the feathers 
are held by their muscles, as well as on membranes, the pre- and post- 
patagia, developed where the limb joins the body. The active move- 
ments of flight are produced mainly by the pectoral muscles; the joints 
and muscles of the wing itself serve to spread the wing and to adjust its 
shape during each beat. The humerus is short and broad with a large 
head and an expanded surface for attachment of the pectoral muscles. 
Radius and ulna are both large, especially the latter. There are only 
two free proximal carpals and the remainder of the wrist is formed of 



xvi. 7- 

three metacarpals, one short and two long and fused. Only one digit, 
probably representing the second, is well developed, having two broad 
phalanges; the third and the first digits consist of single rods, the 

Fig. 260. Various types of feet in birds. 

1, shag (swimming); 2, crow (perching, lifting); 3, ptarmigan (stockinged by 

feathers); 4, jungle fowl (walking, scraping); 5, coot (lobate, swimming); 6, jacana 

(suited for walking on floating plants); 7, sea-eagle (raptorial). (From Thompson, 

Biology of Birds, Sidgwick & Jackson, Ltd.) 

latter, standing somewhat apart at the front of the base of the hand, is 
capable of independent movement ; it carries the bastard wing (alula or 
ala spuria). 

The glenoid cavity is formed at the union of a blade-like scapula and 
a stout coracoid. The former lies horizontally and is attached by 
muscles to the vertebral column and ribs. The coracoid holds the wing 

xvi. 8 WING MUSCLES 449 

away from the sternum, with which it makes a joint. The furcula, 
probably consisting of the combined clavicles and interclavicles, is 
loosely attached to the sternum and carries the origin of muscles that 
rotate the humerus about its long axis. 

8. Wing muscles 

Depression of the wing is produced mainly by a single mass of 
muscle, the huge pectoralis major, making up as much as one-fifth of 
the whole weight of the body. It runs from the sternum and furcula to 
the under side of the humerus, to which it is attached, at some distance 
from the joint, by a complicated tendon of insertion. The fibres of this 
muscle are very red in strongly flying birds and often contain numerous 
lipoid inclusions. In the fowl the fibres are white and contain glycogen, 
but little lipoid. Elevation of the wing is produced by a muscle also 
attached to the sternum, lying deep to the pectoralis major and often 
called the pectoralis minor, but more properly supracoracoideus. Its 
tendon passes through the foramen triosseum, between the furcula, 
scapula, and coracoid, to be inserted on the upper side of the humerus. 
It is assisted by latissimus dorsi and deltoid muscles. 

The chief muscles of the shoulder are thus a massive set serving to 
raise and lower the wing. There is little development of the other 
muscles such as are present in other vertebrates for the purpose of 
balance and drawing the limb backwards and forwards for standing 
and locomotion. Such a system of braces all round the joint is unneces- 
sary; the bird balances on its wings mainly by the action of the pec- 
toralis major as the chief brace, between the sternum and the humerus, 
with the coracoid as a compression member between. Stresses must of 
course arise in other directions besides those tending to produce a 
vertical fall and these are met by the muscles that produce rotation of 
the humerus and various other movements of the wing, especially a 
pronation, depressing the leading edge. The muscles used in other 
tetrapods to sling the weight of the body to the pectoral girdle and 
fore-limb are little developed. The scapula is held to the vertebral 
column by small rhomboid muscles and there is a short series of slips 
attached to the ribs, the serratus anterior. 

Other muscles running from the body to the humerus produce 
rotation of the humerus at the glenoid and adjustments of the patagia, 
movements that are very important in flight. From the outer surface 
of the scapula arises a scapulo-humeral muscle, inserted in such a way 
as to produce adduction and lateral rotation of the humerus, raising 
the hinder edge of the wing. The coraco-humeral muscle is a compact 

45© THE BIRDS xvi. 8-9 

bundle attached near to the last and producing the opposite effect of 
abduction and medial rotation, lowering the hinder aspect of the wing. 

The deltoid muscle is divided into several parts and besides its main 
abductor action on the wing also has slips inserted into the skin of the 
anterior patagium, muscles known as the long and short tensors of 
that membrane. There is also a tensor accessorius, running from the 
surface of the biceps to the skin of the leading edge of the wing. 

The muscles within the arm itself serve to extend or fold the whole 
wing and to alter the positions of the parts, especially by pronation and 
supination during flight. Large triceps and smaller biceps muscles act 
at the elbow. In the forearm there is a large extensor carpi radialis and 
an extensor carpi ulnaris, serving to keep the wing extended at the 
wrist. Flexor carpi ulnaris folds the wing. There are also two large 
pronators, brevis and longus (brachio-cradialis), rotating the radius 
medially and lifting the back of the wing. A system of digital flexors 
and extensors, inserted into the distal phalanx of the main digit, keeps 
the wing tip spread out or folds it. The position of individual feathers 
is controlled by an elaborate system of tendons and muscles along the 
back of the hand. The first digit is moved independently by abductor 
and adductor pollicis muscles, controlling the position of the bastard 
wing, which increases the angle of stall and thus allows slow flying 
speeds in take-off and landing. 

9. Principles of bird flight 

A plane surface moved through the air in a direction inclined at an 
angle to this plane is known as an aerofoil. The forces generated can 
be resolved into a lift force acting upwards and a drag force tending to 
stop the motion. On this fact depends the power of supporting weight 
in the air that is possessed by birds and human heavier-than-air 
machines. Both lift and drag forces are proportional to the square of 
the speed, and the requirement for sustained flight in still air is that 
the object shall have sufficient speed to generate a lift force equal 
to its weight. 

The flow of air over the upper surface of the wing reduces the 
pressure there and provides the main portion of the lift (Figs. 261-2). 
By tilting the wing (increasing the 'angle of attack') the pressure on the 
underside can be increased, but the air flow now tends not to follow 
the upper surface but to become turbulent, especially at the hind edge, 
destroying the lift (Figs. 261-2). When an aerofoil falls below this 
critical speed it stalls; that is to say, drops suddenly, being no longer 
supported. The smooth flow of air over the wing tends to be especially 

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452 THE BIRDS xvi. 9- 

disturbed at its hinder ('trailing') edge and by eddies round the end 
('tip vortex'). The proportion of length to breadth (aspect ratio) in the 
wing suitable for a particular type of flight depends on the need to 
provide a sufficiently large undisturbed area. 

The shape of the aerofoil is of critical importance in determining its 
aerodynamic capacities. For birds, as for aeroplanes, there are differing 
shapes, suitable for various types of flight. To understand them we 
must classify the means by which birds attain the necessary forward 
velocity. First and most obvious is flapping flight. Though the details 
of this are varied and not fully understood, it can be regarded as a 
screw-like motion of the wings, providing forward and upward com- 
ponents (p. 455). 

In still air the only alternative to flapping flight is to glide down- 
wards, which obviously cannot continue indefinitely. Yet some birds, 
such as the gulls, and especially the albatrosses and the buzzards, 
condors, and other birds of prey, can be seen to soar for many minutes, 
gaining height without flapping the wings. Lord Rayleigh showed how 
they can do this by making use of the fact that the air is seldom still. 
Theoretically the bird can use three types of air movement : (1) ascend- 
ing currents, usually thermal ; (2) variations in the wind velocity at any 
one level (gusts); (3) differences in wind velocity at different levels. 
The first method is that used by human sail-planes and is certainly 
adopted by many soaring land birds. The gustiness of the wind is 
probably turned to advantage by gulls, rooks, and many other birds, 
and the decrease in wind velocity near the sea surface is used by marine 
soaring birds, notably the albatross. 

10. Wing shape 

A wing of the shape that allows an albatross or swift to make its 
superb manoeuvres would stall immediately at the speed of flight 
adopted by a crow. In discussing wing shape the chief factors to be 
considered are (1) the wing area, (2) the aspect ratio (wing length/ 
breadth), (3) the w 7 ing outline and taper, (4) the presence of holes or 
slots, (5) the camber or curvature of the wing. 

1 1 . Wing area and loading 

A small wing area is necessary for fast flight, since the dragoc areaX 
speed 2 , at least for high speeds. For this reason fast aeroplanes and 
birds have small wings, but in the bird the fact that the wing provides 
the forward momentum as well as the lift greatly complicates matters. 
For flapping flight the wings must be moved relatively fast and for this 

xvi. i 3 ASPECT RATIO 453 

small size is an advantage. On the other hand, a large wing area allows 
slow flight (lift oc area X speed 2 ) and is found in hawks, vultures, 
storks, and other birds that fly slowly to hunt, especially if they soar 
on thermal currents, for which a large lift is necessary (p. 458). 

The loading of the wing varies considerably. Since the weight 
increases with the cube but the wing area only with the square of the 
linear dimensions, it follows that large birds must have relatively larger 
wings than small. However, the larger birds usually have a heavier 
loading of the wing, for instance, 10 kg./m. 2 in the duck (Anas), 20 in 
the swan (Cygnns) , 1 in the goldcrest (Regains), 3 in the crow (Corvus). 
A considerable 'safety margin' remains in most birds; for instance, 
pigeons were found to be able to fly until as much as 45 per cent of 
the wing surface was removed ; hawks and owls have an especially high 
safety margin and they can carry prey almost as heavy as themselves. 

12. Aspect ratio 

Although a small wing area reduces drag, many fast-flying birds 
have a large wing-span. The aerodynamic advantages of this allow a 
low rate of descent when gliding, reducing the expenditure of energy 
necessary to sustain flight. High aspect ratio is therefore found in birds 
that fly fast by flapping flight (swifts and swallows) and especially in 
those, such as the albatross, that glide fast in order to obtain sufficient 
kinetic energy to convert into altitude. However, these wings with very 
high aspect ratio stall at relatively high speeds and the birds that soar 
slowly on thermal up-currents over the land mostly have a low aspect 
ratio. Some figures for aspect ratios are: 

Albatross (Diotnedea) . . .25 

Gull (Lartis) . . . .11 

Swift (Apus) . . . .11 

Shearwater (Puffinus) . . .10 

Vulture {Neophron) . . .6 

Rook (Corvus) . . . .6 

Sparrow (Passer) . . . .5 

13. Wing tips, slots, and camber 

A pointed wing tends to stall first at its tip and is therefore only 
suitable for fast fliers. Such birds show great development of the hand 
feathers, producing a long narrow wing, whereas birds built for slower 
flight and manoeuvre have a shorter broader wing with long arm 
feathers (Fig. 263). 

The condition of the air around the wing is of first importance for 
the maintenance of lift; if there is not a smooth stream over the upper 
and under surfaces the air becomes turbulent, and the aerofoil stalls 
(Figs. 261-2). This tends to happen either if the speed falls too low or if 
the angle of the wing relative to the line of motion increases above about 

454 THE BIRDS xvi. 13- 

20 . Turbulence is mitigated, however, by the provision of openings, 
known as slots, which let through part of the air and provide the 
necessary smooth stream. The spaces that occur between the feathers, 
especially towards the wing tip, almost certainly function as slots. 
Probably the arrangement provides a series of such apertures, giving 
a very efficient high-lift device. Such slots are conspicuous in slow 


Fig. 263. Wings built for speed (falcon, Falco) and for manoeuvring 
(hawk, Accipiter). The former is long and narrow, with relatively 
large hand feathers. The latter is short and broad, the arm feathers 
being long and the primaries arranged to make slots. (After Fuertes.) 

fliers (rooks) and especially in those that soar on thermal up-currents 
(vultures). The feathers of such birds are often individually tapered 
(Fig. 263). Slots are also found in the wings of large birds that are fast 
fliers (pheasants), the wing being liable to stall in certain phases of the 
down strokes. It is possible that the bastard wing acts as a slotting 
device; indeed, consideration of it played a part in development of the 
theory of turbulence and slotting. 

The shape of the wing has a very important influence on the air 
stream. In most birds there is a stiff leading edge and a thinner trailing 
edge. Nearly all wings are cambered, that is to say, they taper from 
the leading to the trailing edge, especially in the region of the forearm 

xvi. 14 



(Figs. 261-2). This arrangement directs the air stream over the upper 
surface of the wing in such a way as to provide an extra lift by creating 
a 'suction zone' of reduced pressure. How T ever, high camber, like low 
aspect ratio, reduces the speed of the bird. 

14. Flapping flight 

Flapping flight involves a complex, 
screw-like motion of the wing, down- 
wards and forwards then upwards 
and backwards, more rapid upwards 
than downwards (Fig. 264). The 
action of the wings differs during 
take-off or landing from that in sus- 
tained flight (Brown, 1953). In the 
former conditions, when the speed 
is slow, forward velocity is provided 
by backward movement of the wings. 
During each stroke, beginning with 
the wings raised, they are first moved 
downward and then forward, pro- 
viding lift (Figs. 264, 265). This 
movement is produced mainly by 
the pectoralis major. During the 
upstroke the wing is first adducted, 
folded and flexed, and supinated at 
the wrist, by the actions of pectoralis 

minor and other muscles. A very rapid backward flick then follows, 
produced by upward and forward rotation of the humerus, extension 
of the wing, and pronation of the manus. The effect of these move- 
ments, produced largely by the triceps and other extensors, is to 
provide a forward component. 

This form of flight involves mainly the primary feathers. It is 
evidently very tiring and can only be continued for a few seconds. In 
sustained flight the downstroke is as in slow flight but the upstroke is 
much simpler, with only a slight backward flick of the primary feathers. 
The action is such that the inner part of the wing provides lift, the 
tip propulsion. The upstroke in fast flight is thus mainly passive, 
produced by the pressure of air against the under surface. The major 
part of the effort needed to provide lift and forward propulsion is thus 
provided by the pectoralis major. This muscle weighs as much as one- 
fifth of the body weight in flappers, such as the lapwing, as little as 

Fig. 264. Pathway of the wing tip and 
wrist joint relative to the body during 
free flapping flight of a gull. Equal 
time-intervals are shown. Note the 
great speed of the upward beat and 
that the forearm is raised before the 
wing tip. (After Demoll.) 


Fig. 265. Pigeon (Columba) with wings at bottom of stroke during rising. From a 

photograph taken at very short exposure. Note forward position of wings but 

upward and backward curled primary feathers. (After Aymar.) 




Fig. 266. Drawings from four photographs from film of a take-off by an eagle 
(Aquila). A. The legs are jumping and the upper arms nearly vertical before the 
wrist joint is extended. B. Wing fully extended with bastard wing spread out, 
some pronation. C. Marked pronation as the upper arm reaches its lowest point. 
D. The upper arm is proceeding upwards, although the hand has not yet reached 
its lowest point. (Drawn from photographs by Knight, from Streseman.) 

xvi. i 4 FLAPPING FLIGHT 457 

one-ninth in soarers, such as the gull. It does nearly all the work, the 
other muscles serving to give extra lift when needed. 

The feathers are held by an ela- 
borate system of tendons and in 
some birds they are allowed to 
twist only when the wing is being 
raised and the barbs of the 
feathers themselves are so ar- 
ranged that they open like the 
vanes of a blind when unaer 
pressure from above, but close 
when the pressure is from below 
(Fig. 268). In other birds, especi- 
ally those that fly fast with a slow 
wing beat, such as gulls and 
swans, the wing is probably rigid 
on the up as well as on the down 

Fig. 267. Bill-fisher leaving its hole in a 
bank, showing wings half-way through the 
upstroke. The upper arm has reached its 
highest point and the forearm is just starting 
upwards; its primary feathers have opened 
on the right wing, reducing resistance. 
(Drawn from photograph by Aymar, Bird 
Flight, published by John Lane, The Bod- 
ley Head, Ltd.) 

strokes, and is twisted so as to 

produce forward and upward components on the up stroke 




5 6 78 910 II 12 13 #. 

Fig. 268. Diagram of wing to show arrangement of the flight feathers. 
(From Pycraft, A History of Birds, Methuen & Co., Ltd.) 

The whole upward movement is usually faster than the downward 
one. Before the wing tip has reached its highest point the upper arm 
is already beginning to descend and in this way the line of flight is 



xvi. 14-16 

maintained almost straight and does not follow a wavy path as it would 
do if the parts of the wing vibrated together. In small birds the wing 
works more nearly as a whole and the flight differs in several respects 
from that of larger birds. In general the wing is a very labile system 
and regulates itself automatically with changes in the aerodynamical 
forces. This regulation is produced partly by feather plasticity and 
joint mobility, with participation of reflex muscular adjustments that 
are little understood. 

The whirring flight of some small birds, especially of humming 
birds, enables them to remain almost in one 
place in the air, or even to move backwards. 
The wings beat backwards and forwards 
(Fig. 269), often as fast as 200 times a second, 
and the 'pectoralis minor' is almost as large as 
the major. 

15. Soaring flight 

Many birds economize the energy needed 
for flapping flight by making skilful use of 
the possibilities presented by movement of the 
air. All birds glide for short distances, some 
small birds with wings folded, others with 
wings outstretched. Sustained gliding and 
soaring upwards without flapping the wings 
is found only in large birds, probably because 
considerable weight is necessary to provide 
kinetic energy sufficient to ensure continuous 
flight and efficient use of wind variations. As 
has been suggested, there are two distinct types of soaring birds: 
(1) land birds using thermal up-currents, (2) marine birds using 
variations in wind above sea level. 

Fig. 269. Spotted fly- 
catcher hovering. The 
wings are passing back- 
wards and there are spaces 
between the feathers. 
(Drawn from a photo- 
graph by E. Hosking, 
with permission.) 

16. Soaring on up-currents 

Up-currents of air arise in the neighbourhood of large objects on 
the ground (cliffs or even a ship) and particularly from variations 
in the rate of heating of the earth's surface in the sun, over rocks, 
vegetation, mountain shadows, &c. Birds using such currents usually 
proceed upwards in a series of small circles, a behaviour seen in 
buzzards and other hawks and especially characteristic of vultures, 
which may ascend in this way above 1,000 ft (Figs. 270-2). The 
characteristic features of such thermal soarers are large wing area, 



FlG. 270. Flight of an eagle (Aquila). 

a-b, flapping flight; B-C, soaring at constant height; C-D, 
soaring in ascending spirals; d-e, gliding. (After Ahlborn.) 

Fig. 271. Soaring flight of kite (Milvus). 

Losing height downwind and gaining it upwind. Time-marks one second. 
(After Hankin.) 

Fig. 272. Wings of vulture (Gyps). 

A, soaring upwind, gaining height; B, upwind on level; c, downwind, losing height; 
D-F, gliding flight. (After Ahlborn.) 



xvi. 16- 

low aspect ratio, and wings broad at the tip and usually provided 
with well-marked slots. 

17. Use of vertical wind variations 

The decreasing effect of surface friction causes the wind to blow 
faster at greater heights and this phenomenon is used by some birds 
at sea, where conditions are presumably more uniform than over the 

Fig. 273. Wings of the albatross (Diomeded), used for soaring flight. Wing very 
narrow, with long upper arm region. (Drawn from photograph by Aymar.) 

land. The albatross (Diomeded) (Fig. 273) is the classic example of this 
type of bird, proceeding in a regular series of movements, without 
flapping the wings, downwind losing height and gaining speed and 
then upwind gaining height and passing into a faster-moving layer. 
Each downwind tack is longer than the upwind one. During the upwind 
tack the wings are spread forwards, downwind backwards. The alba- 
tross remains all the time within 50 ft of the sea surface, because the 
variations in wind velocity are marked only at low levels. The 
albatross shows the characteristics suitable for this type of flight, 
namely, large size (it is the largest of all flying birds), great wing span 
(11 ft), high aspect ratio (25), and pointed wing tips, without slots. 
Other sea birds, such as the gulls, though not so highly specialized, 

xvi. 1 8 



can take advantage of variations in horizontal wind velocity, including 
gusts at any one level. The bird moves upwards as it meets an accele- 
rating gust and turns when the wind decelerates. Gulls also use up- 
currents at cliff faces and, no doubt, air movements of all sorts are 

Fig. 274. Heron (Ardea) leaving its perch. The legs have been used to make a jump 
and the wings are fully spread. (Drawn from photograph by Aymar.) 

widely used, especially by large birds. However, it is evident that the 
wing equipment only allows the bird a limited range of choice and 
probably even the slightly different wing shapes of related species 
depend on the differing conditions they are called upon to meet. A 
vulture could no more zoom backwards and forwards over the waves 
than an albatross could circle slowly on a gentle thermal up-current. 
A pigeon cannot equal a gull at steady gliding and soaring, but the 
pigeon can rise more steeply or descend more rapidly without stalling. 

18. Speed of flight 

Estimation of the speed of flight involves distinguishing between air 
and ground speed. The speed relative to the ground may be very high ; 
there are records of birds covering more than 100 land miles in an 



hour, with the help of the wind. Racing pigeons can average 40 miles 
an hour or more for considerable periods. Air speeds of 30-50 m.p.h. 
can certainly be reached by many birds: swifts are said to reach 100 
m.p.h. in still air. 

Fig. 275. Pigeons (Columba), photographed during take-off, with exposures of 
1/825 second. A, front, and b, rear view, with wings together, c, nearly, and d, 
quite at bottom of downstroke; note pronation and forward movement of wing. 
E and F, wings during the upstroke; in f the primary feathers have opened; note 
that the wing moves backwards and that the motion is faster than on the down- 
stroke. (From photographs by Aymar.) 

19. Take-off and landing 

At the take-off the bird has to acquire sufficient forward momentum 
to provide lift, and yet must leave the air sufficiently undisturbed for 
subsequent beats to be effective. In many birds, especially the smaller, 
the jump provided by the legs is adequate for the take-off (Fig. 274). 
Large birds must run or swim rapidly to obtain sufficient speed. Eagles 
are said to be unable to rise without a long run, and many large birds 
nest on a cliff or tree, which gives them an up-current for the take-off. 
Swifts usually come to rest high up and can only rise off the ground 
with difficulty. The albatross is unable to take off from the sea surface 
in a dead calm. 

The first beats are usually very large, beginning with the wings 
above the back and held at such an angle as to produce a large forward 

xvi. 19 



component. The wings may be heard actually clapping together in 
pigeons (Fig. 275). During rapid ascent, as in the larks, the body is 
nearly vertical and the wing changes its angle at the shoulder very 

Fig. 276. Jackdaw about to land. 
The wings are fully extended on 
the downbeat, and the tail is 
fanned out and bent downwards. 
(From photograph by Aymar.) 

Fig. 277. Hawk striking at a dummy owl. 
Note long legs and the method of braking. 
The wings are broad and rounded, giving a 
large safety factor. (From photograph by 

sharply between the downward and recovery strokes. The bastard 
wing is held in such a position that the beat provides extra forward 

Landing is also a delicate operation, especially since it often involves 
coming to rest suddenly on a branch (Fig. 276). This is achieved by 
lowering and fanning out the tail, which thus acts as a flap, providing 
both lift and braking. The legs are then lowered; often one further 
wing stroke is given to bring the bird forward to drop onto the perch. 
The adjustment of braking in such a way as to prevent stalling involves 
a very special system of coordination (Fig. 277). Other methods of 

464 THE BIRDS xvi. 19- 

landing are possible, for instance, rooks may make a roll and sideslip 
to the ground. 

20. The skull in birds 

The arrangement of the parts of the bird's skull is similar to that of 
archosaurian reptiles (Fig. 242). Individual bones can be recognized 
in the young, but they mostly become united in the adult to form a 
continuous thin-walled structure that encloses the brain and sense- 
organs and supports the beak (Fig. 278). Most birds are microsmatic; 
the nasal passages are simple and the turbinals reduced. There is 
seldom a complete bony secondary palate, such as there is in mammals, 
instead the internal nostril opens into the mouth relatively far forward. 
The large size of the brain and reduction of its olfactory portions are 
responsible for the rounded form of the top of the head, and there are 
very large orbits at the sides, separated by an ossified septum. The 
base of the skull is formed by a basioccipital behind, carrying a single 
occipital condyle. There is a large basisphenoid, covered ventrally by 
a pair of basitemporals, probably representing the parasphenoid, the 
front part of which makes a 'basisphenoid rostrum', as in archosaurs. 

The jaws are characteristically slender and elongated; in the more 
advanced birds they have a very special form of support. The upper 
part of the front of the skull is composed of the enlarged premaxillae, 
the nostrils lying very far back and the nasal bones being small. The 
palatines are long and fused far forward with the maxilla, while they 
articulate movably behind with the pterygoids and base of the skull. 
The pterygoid is a slender rod, itself movably articulated with the 
skull and with the quadrate, which is a triangular bone with clearly 
separate otic and basal articular processes. The upper jaw is thus a 
long thin bar composed of maxillae, quadrato-jugal, and jugal, and as 
in many reptiles it is capable of considerable movement ('kinesis'). 
It is raised when the lower end of the quadrate moves forwards. This 
mechanism is particularly well developed in parrots, where the beak 
is freely hinged on the skull. This type of palatal arrangement is known 
as neognathous. In some birds, such as the flightless ratites, the 
palatines are shorter, the vomer larger, and the pterygoids less mov- 
able, a condition called palaeognathous (p. 514). The lower jaw, also 
elongated, consists of the articular bone and four membrane bones. 

21. The jaws, beak, and feeding mechanisms 

There is a complete lower temporal bar, composed of jugal and 
quadrato-jugal bones. The temporal region is hard to interpret, but 

XVI. 21 



Fig. 278. Skull of young gosling (Anser). 
A. angular; Ar. articular; As. alisphenoid; Bo. basioccipital; Bsh. basisphenoid ; D. dentary; 
E. ethmoid; Eo. exoccipital; F. frontal; Ip. interparietal; J. jugal; L. lachrymal; Mx. 
maxillary; A r . nasal; O. supra-occipital; Op. opisthotic; P. parietal; Pa. palatine; Pm. pre- 
maxillary; Po. postorbital; Pt. pterygoid; Q. quadrate; Qj. quadrato-jugal; R. rostrum of 
basisphenoid; S. squamosal; Sa. sur-angular; V. vomer. (From Heilmann, The Origin of 
Birds, H. F. & C. Witherby, Ltd.) 

has presumably been derived from the diapsid archosaurian condition. 
Typically, there is a single large fossa, communicating with the orbit, 
but this is often partly subdivided by bony processes; occasionally, 
there is a complete post-orbital bar (parrots). There are moderately 
large temporal and pterygoid muscles, but the jaws are not usually 

4 66 


XVI. 21 

Fig. 279. Various bird beaks. 

1, Merganser; 2, Flamingo; 3, Shoveller; 4, Scissor-bill (adult); 5, Scissor-bill (young); 
6, Anastomus; 7, Hornbill; 8, Hummingbird; 9, Avocet; 10, Parrot; 11, Parrot; 12, Spoon- 
bill; 13, Crossbill; 14, Nightjar; 15, Eagle; 16, Balaeniceps. (From Pycraft, A History of 
Birds, Methuen & Co., Ltd.) 

very powerful, though, of course, formidable in carnivores. Having 
completely lost the teeth, the birds must rely largely on internal 
processes to break up the food. The beak is, however, characteristically 
modified according to the food habits (Fig. 279). There is very great 
variety in the feeding, as in so much of the life of birds, and though 
many species keep strictly to one diet others are able to adapt them- 
selves to the food available. The ingenuity and persistence with which 
birds seek and collect food must be a main factor in their success. 

Many birds with a moderately long bill, such as the song-thrush 
(Turdus), can eat either flesh (snails, earthworms, or caterpillars) or 

XVI. 21 



fruit. Incidentally we may notice the ingenious behaviour by which 
the snail's shell is cracked open to obtain the food, by beating it against 
a stone. Birds that mainly eat seeds, such as the finches, usually have 
short, thick, strong bills. Large strong bills are present in the hornbills 
and toucans ; they push through dense foliage to obtain the fruit, which 
may have a hard case. In parrots the beak is moved on the skull, 
pushed up by the upper jaw when the latter is pulled forward by the 
digastric muscle. 

Fig. 280. The Galapagos woodpecker finch (Camarhynchus pallidus) using 
its stick. (From Lack, drawn by R. Green from photograph by R. Leacock.) 

The carnivorous birds, such as most eagles and owls, have short 
and sharp beaks, whereas fish-eating, as in other vertebrates, results 
in long jaws. Another widely found arrangement is the flattened bill 
of some ducks, similar to those of some sturgeons and of the platypus, 
which also sift out food from water or mud. The long, thin beak of the 
curlew selects food from mud in a different way, mostly worms and 
other soft-bodied invertebrates. Lesser flamingos feed on blue-green 
algae and microscopic phytoplankton, collected by a filter system on 
the jaws, using a current of water produced by the sucking mouth and 
piston-like tongue. Some insectivorous birds have long beaks for 
finding their prey under bark. The woodpeckers have a strong beak 
like a pick-axe for excavating in wood, and most elaborate special 
modifications for the purpose of licking up insects; there is an enor- 
mously long protusible tongue and special hyoid. The woodpecker 
finch {Camarhynchus pallidus) on the Galapagos Islands probes insects 
from the bark by means of a cactus spine, a remarkable case of the use 
of a tool by a bird (Fig. 280). Among the most specialized feeders are 

4 68 


XVI. 21- 

the humming-birds, eating nectar, the beak being long or short accord- 
ing to the type of flower visited, and the tongue provided with a 
special tubular tip. 

i net 

22. Digestive system of 

Once the food is in the 
mouth it is manipulated by 
the long, thin tongue, mois- 
tened with saliva, which 
usually consists of mucus 
but is said to contain diasta- 
tic enzyme in some seed- 
eating finches. Food swal- 
lowed down the oesophagus 
may be stored in a large 
receptacle, the crop, found 
especially in grain-eating 
birds; its lining is of oeso- 
phageal structure (Fig. 281). 
The true stomach is divided 
into two parts, a glandular 
proventriculus and a muscu- 
lar gizzard. The structure of 
the anterior chambers of the 
gut varies greatly with the 
diet. In grain-eating birds, 
such as the pigeon, the crop 
is large and the seeds are 
first macerated by storage 
there. They are then mixed 
with peptic enzymes in the proventriculus and ground up in the mus- 
cular gizzard, which in pigeons has a horny lining and also contains 
numerous small stones. In insectivores and carnivores the crop is 
usually smaller or absent, but is very large in some fish-eating birds. 
In carnivores the gizzard has the character of a more normal stomach. 
It was stated by John Hunter that herring gulls, normally living on 
fish, readily take to eating grain, and that after a year or so of this 
diet the gizzard becomes muscular and has horny walls. 

The peptic juice has powerful digestive powers and many carni- 
vorous and fish-eating birds dissolve even the bones of their prey, 


Fig. 281. Dissection of pigeon, 
bile-ducts; cl. cloaca; coec. coeca; cr. crop; giz. 
gizzard; int. intestine; k. kidney; /. liver; oes. oeso- 
phagus; p. pancreas; p.d. pancreatic ducts; pr. pro- 
ventriculus ; sp. spleen ; test, testis. (After Schimkewitsch 
and Streseman.) 

XVI. 22 



though in owls these are regurgitated with fur or feathers, making 
characteristic pellets. The crop of pigeons is also remarkable for the 
milk it produces to nourish the young. There are special glands for 
this purpose and they become active in the breeding-season under 
the influence of a pituitary hormone, prolactin, which has been 


Fig. 282. Diagrammatic section through cloaca of pigeon. 
ap. external aperture; b.Fab. bursa Fabricii; ep. epidermis; m.sph. 
sphincter muscle; muc. mucous glands; r. rectum; ur, & vd. papillae 
for ureter and vas deferens (or oviduct). (After Clara, from Streseman.) 

crystallized and is probably protein in nature. Prolactin causes 
regression of testes and ovaries and involution of secondary sexual 
characters, but induces brooding behaviour in the female. Its action 
is comparable with that of the galactogenic hormone of the mam- 
malian pituitary. 

The duodenum and coiled intestine are of characteristic vertebrate 
tvpe, relatively rather short, though somewhat longer in grain-eating 
birds. The bile and pancreatic ducts usually open into the distal limb 
of the duodenum; in pigeons the left bile-duct enters close to the 
pylorus (Fig. 281). There is a peculiar pair of coeca at the junction of 
rectum and intestine. The food enters these coeca, but it is not clear 
what function they perform, possibly it is related to the absorption of 
water. The arrangements of the cloaca are certainly concerned with 
this end (Fig. 282). The rectum opens into a coprodaeum and this in 
turn receives a urodaeum, which is the terminal portion of the urinary 
and genital ducts. A final chamber, the proctodaeum, opens at the 
anus. The urinary products are made solid by subtraction of water in 
the urodaeum and the walls of the other chambers serve a similar 

47° THE BIRDS xvi. 22- 

purpose. The bursa Fabricii is a blind sac with much lymphoid tissue, 
opening into the proctodaeum; its function is probably to protect 
locally against infection and to produce lymphocytes for the blood- 
stream, hence it has been called a 'cloacal thymus'. Like the thymus, 
it is prominent in young animals and usually much reduced in the 

The large surface area, high temperature, and great activity of birds 
necessitate a high food intake, especially in the smaller types. This is 
made possible by rapid passage of food through the gut. Thus a shrike 
(Lanius) is said to digest a mouse in 3 hours, and hens take only 12-24 
hours over the most resistant grain. The amount of food taken per 
day may reach nearly 30 per cent of the body weight (6 g) in the very 
small goldcrest (Regains) but is about 12 per cent in a starling 
(Sturnus) weighing 75 g. 

23. Circulatory system 

Many of the features characteristic of birds depend on an efficient 
circulation, allowing of a high rate of metabolism, and hence a high 
and constant temperature. It is significant that the birds and mammals 
are the only vertebrates that have achieved complete separation of the 
respiratory and systemic circulations, making possible a high arteriolar 
pressure, which allows materials to reach the tissues rapidly. 

The heart shows its sauropsidan characteristics clearly in that the 
ventral aorta is split to its base into aortic and pulmonary trunks. The 
former arising from the left ventricle curls round the pulmonary 
trunk to form a single right aortic arch. The heart has lost the sinus 
venosus; as in mammals no such extra chamber is necessary to step 
up the venous return pressure. The ventricles are large, especially the 
left. The right auricle and ventricle are separated by a flap-like valve, 
the left side having valves with chordae tendinae, somewhat as in 
mammals. There are enormous innominate arteries to supply the 
pectoral muscles. In the venous system there are renal portal veins. 

The size of the heart and rate of heart-beat vary with the size and 
activity of the bird, larger birds having in general relatively smaller 
and less rapid hearts. In a turkey the rate of beat may be less than 100 
per minute, in a hen about 300, and in a sparrow nearly 500. 

The red corpuscles of birds differ from those of mammals in being 
oval and nucleated. They carry a large amount of a haemoglobin that 
gives up its oxygen suddenly at a relatively high oxygen tension. The 
red corpuscles are smaller in actively flying birds than in the larger 
flightless ratites. Haemopoetic tissue is widespread in the young, 

xvi. 24 R ESPI RAT ION 47 1 

restricted mainly to the marrow in the adult, although it may also be 
found in the liver and spleen. The white corpuscles are more numerous 
than in mammals. They include neutrophils laden with crystals, and 
thrombocytes, as well as the mammalian types. Lymphatic tissue is 
dispersed rather than aggregated into nodes. There is a pair of lymph 
hearts in the sacral region of the embryo and these may persist in the 
adult. There is a high basal metabolic rate and a temperature con- 
siderably higher than that of mammals, usually about 42 C, reaching 
nearly 45 ° C in some cases. The means by which this is kept constant 
in the absence of sweat glands are not known certainly. Heat loss is 
minimized by the absence of vascularized extremities, the feet being 
little more than keratin and collagen. The formation of the wing from 
large avascular surfaces has no doubt been a large part of the secret 
of the success of birds. 

The air-sacs may serve to conserve heat by providing an air cushion 
for the viscera, with perhaps the alternative possibility of losing heat 
in this way, by ventilation, when necessary. There is a system of 
direct arterio-venous connexions in the feet, and elsewhere. The anas- 
tomotic regions have powerful muscles, whose contraction closes them 
and forces the blood through the capillary system. There must be a 
whole system of nervous pathways for the control of upward and down- 
ward temperature regulation, evolved independently of that found in 
mammals. At least one species (the nightjar) is known to hibernate, 
and certain humming birds, whose small size render heat loss a 
serious problem, become temporarily poikilothermic at night. 

24. Respiration 

Special arrangements are present to provide the large supply of 
oxygen necessary for the active metabolism and these are based on the 
plan found in some reptiles. Beyond the respiratory portion of the 
lung, which is relatively small, there are membranous air-sacs, which 
are filled at inspiration and then sweep the used air out of the lungs 
at expiration, thus avoiding the 'dead space' of unrespired air, which 
is considerable in mammals. When the bird is at rest the air-sacs con- 
tain air with a high content of C0 2 , but during periods of activity the 
abdominal air-sacs fill with fresh air containing little C0 2 ; they then 
serve not only as a means of ventilating the lungs but also for regula- 
tion of the body temperature. The exact direction of the air currents 
passing through the lungs and the different air-sacs is not fully under- 

The larynx of birds is a small structure guarding the entrance to the 



XVI. 24 

trachea. The latter is often long and coiled, perhaps to warm the air. 
The tracheal rings are bony and complete. The voice is produced in 
the syrinx, a slight enlargement at the lozver end of the trachea, con- 
taining a pair of semilunar membranes with muscles that alter the 
pitch of the sound. The apparatus is simple in many birds, but the 
muscles are very complicated in the singing birds and are especially 


s clav 

s. thor 

s Lhorpost 


Fig. 283. Diagram of lungs and air-sacs of pigeon, seen from ventral side on left, 

dorsal on right. On the left side only the ventral surface of the lungs and the 

expiratory bronchi and air-sacs are shown (dotted). On the right are the inspiratory 

bronchi and air-sacs (in black). 

B. main bronchus; C. cervical ventrobronchus; M. mesobronchus; V. vestibule; s.abd. 

abdominal air-sac; s.cerv. cervical air-sac; s.clav. clavicular air-sac with diverticulum (ax.) 

in axilla; s. thor. ant. and post, thoracic air-sacs. (After Brandes and Ihle.) 

large in the males. Many varieties of sound are produced, from simple 
cries appropriate to each sex to elaborate songs. In many species the 
song is given in its full complexity by individuals that have had no 
opportunity of hearing others sing, but in some the song is largely 
learnt by the young and may show considerable local variation. The 
voice is used for communication in various ways, including, in social 
birds such as rooks, the giving of warning and the frightening away 
of intruders. The language may include as many as fifteen sounds used 
under different circumstances (chaffinch). The more elaborate song of 
male birds is used in courtship both as a sexual stimulant and as a 
threat to other birds invading the chosen territory (p. 503). 

xvi. 24 RESPIRATION 473 

The lungs are rather small spongy organs, with little elasticity. The 
air passes backwards in a large main bronchus running through the 
lungs and giving off branches to the lung substance, but continuing 
beyond to the inspiratory air-sacs (Figs. 283 and 284). These are thin- 
walled chambers, divided into two sets, the posterior inspiratory and 
anterior expiratory. The posterior, inspiratory, air-sacs are the ab- 
dominal and posterior thoracic and they 
are filled by the air rushing into them 
through the main bronchus. The anterior 
or expiratory air-sacs include an anterior 
thoracic, median interclavicular, and cer- 
vical, these often communicating with 
spaces in the bones. At expiration the 
air passes from the more posterior sacs 
through the lungs by special recurrent 
bronchi into the anterior sacs. From 
these the air may be expelled to the 
exterior, return to the lungs being pre- 
vented by closure of sphincters. In some 
conditions, however, especially in diving 
birds, the air may be passed backwards 
and forwards through the lungs several 
times, until all its oxygen has been used. 
The branches of the bronchi in the lungs 
do not end blindly in alveoli, but make an 
elaborate system of lung capillaries. Air 
sweeps through the larger channels at 
inspiration and expiration, but probably 
reaches the finer capillaries by diffusion. 

The mechanism by which the ventilation is produced is complicated 
and depends largely on the movements produced during locomotion. 
The upper surface of the lung adheres to the ribs, its lower surface is 
covered by a special membrane derived from the peritoneum and 
known as the pulmonary aponeurosis (Fig. 285). This is connected 
with the ribs by costopulmonary muscles. The floor of the thoracic 
air-sacs, which lie below the lungs, is also covered by a fibrous mem- 
brane, the oblique septum, but the walls of the remaining air-sacs are 
very thin. Quiet respiratory movements are produced by the inter- 
costal (inspiratory) and abdominal (expiratory) muscles, acting upon 
the thoracic and abdominal cavities so as to enlarge and contract the 
thorax, drawing air in and out of the air-sacs, through the lungs. During 

Fig. 284. The air-sacs of a bird. 

1.. right lung; c. cervical air-sac; ICL. 
interclavicular; A.S. outgrowth into 
humerus (h.); anterior thoracic 
air-sac; p.TH. posterior thoracic; 
AnD. abdominal air-sac; tr. trachea. 
(From Thompson, Biology of Birds, 
Sidgwick & Jackson, Ltd.) 

474 THE BIRDS xvi. 24- 

flight the movements of the pectoral muscles provide the ventilation, 
the sternum moving towards and away from the vertebral column. 

25. Excretory system 

The kidneys are, of course, metanephric and are relatively large, 
elongated, and lobulated. They are provided with venous blood by 




ms / 


Fig. 285. Diagram of transverse section through the thorax of a bird. 

ec. Excurrent passage from lung to air-sac through pulmonary aponeurosis; h. heart; 
lis. left liver-sac; Ig. lung; m. muscle; ms. mesentery below oesophagus; obi. oblique septum; 
p. pericardial coelom; pa. pulmonary aponeurosis; pic. reduced pleural coelom; r. dorsal 
rib; re. recurrent bronchus from sac to lung; rl. right lobe of liver; rpr. right pulmonary 
recess; St. sternum; thas. posterior thoracic air-sac; vr. sternal rib. (From Goodrich.) 

the renal portal veins and arterial blood from the renal arteries. The 
arrangement is essentially as in amphibia and reptiles, with the renal 
arteries supplying the glomeruli and the portal veins, which break up 
into inter-lobular branches, sending blood to the renal tubules, whence 
it is collected into a central intra-lobular vein. It is not certain, how- 
ever, exactly how the system operates, and it is possible that much of 
the blood-flow is directly from the renal portal to the renal veins, 
making little contact with the tubule walls. 

The excretory system is highly specialized for water-saving. For 
this purpose the end product of nitrogenous metabolism is the rela- 
tively insoluble uric acid, synthesized in the liver, probably from 
ammonium lactate. After excretion by the kidney the urine is con- 
centrated in the cloacal chambers and the uric acid precipitates as 

XVI. 26 



whitish granules. There is no urinary bladder in the adult bird. More 
soluble excretory end substances, such as urea, would reach toxic con- 
centrations. The glomeruli are much more numerous and smaller 
than those of mammals. The urinary tubules effect a considerable con- 
centration of the urine by means of long loops of Henle. The viscous 
fluid that enters the urodaeum then 
passes up into the coprodaeum, 
where further water is abstracted, 
and the mixed faeces and urinary 
products are then excreted as the 
characteristic semi-solid white 
guano. The water-conservation sys- 
tem is certainly very effective, and 
some desert-living birds are said to 
be able to survive for many weeks 
without water. In this respect the 
birds have freed themselves from 
the original aquatic environment to 
a remarkable degree. 



Fig. 286. Female reproductive organs 
of a hen. 

ov. ovary; K. kidneys; f.t. funnel; ovd. 
oviduct; m.ovd. muscular part of oviduct; 
OP. OVD. opening of oviduct; ur. ureters; 
op.ur. opening of right ureter; r.r.ovd. 
rudimentary right oviduct; cl. cloaca. (From 
Thompson, Biology of Birds, Sidgwick & 
Jackson, Ltd.) 

26. Reproductive system 

The testis consists of coiled 
tubules of the usual type, joining to 
form a long epididymis and vas 
deferens, opening into the urodaeum 
by an erectile papilla that is the only 
copulatory organ of most birds. 
During copulation the proctodaea 
of male and female are everted and 
pressed together, so that the sperm 
is ejaculated direct into the female urodaeum and finds its way up 
the oviduct. A definite penis (and also clitoris) is found in ratites, 
anseriformes, and a few other birds. The condition of the testis and 
its ducts varies greatly with the time of year, the weight of the gland 
being as much as 1,000 times greater in the breeding-season than it is 
in the non-breeding, when it contains only spermatogonia. 

The provision of material sufficient for the development of a warm- 
blooded creature is, of course, made possible in birds by the extremely 
yolky eggs, so large that they allow room for development of only one 
ovary, nearly always the left (Fig. 286). The right ovary remains present 
as a rudiment and if the left is destroyed by operation or disease the 



xvi. 26- 

right is able to differentiate, but then forms not an ovary but a testis. 
Complete sex reversal can thus occur, at least in some races of 
domestic fowl, and the transformed bird may acquire cock plumage 
and tread and fertilize hens (Fig. 287). Sex reversal rarely, if ever, 
takes place in the opposite direction. We must suppose that there is 
some switch over in the balance of male and female determining 

Fig. 287. Secondary sexual characters of the fowl (Gallus). 

Left cocks, right hens. 

A, normal; B, castrated; C, cock with implanted ovary and hen 

with implanted testis. (After Zawadowsky.) 

processes, taking place relatively early in the case of normal definitive 
males but later on in life also in 'females', so that all birds become 
potentially 'male' at the end of their life. 

Of the large number of oocytes only few ripen to make the enormous 
follicles. After each follicle has burst it quickly regresses; there is no 
'corpus luteum'. 

The egg is taken up by the ciliated and muscular funnel of the left 
oviduct, and passes down a tube with circular and longitudinal muscles 
and a glandular, ciliated mucosa. The albumen of the egg is produced 
by long tubular glands, opening to the lumen. The oviduct has various 

xvi. 27 BRAIN 477 

parts, the upper secreting mainly albumen, the lower producing the 
shell, and the lowest mucus, to assist the act of laying. The blue back- 
ground colour of the egg (oocyanin) is produced during shell-forma- 
tion in the upper part of the tube ; spots of red-brown ooporphyrin are 
added lower down. The pigments are derived from the bile, ultimately 
from haemoglobin. 

As much as a third of the weight of calcium in the whole skeleton 
is needed for the shells of the two eggs laid by a pigeon. A reserve is 
collected as the ovarian follicles mature. The oestrogen they produce 
increases the uptake of calcium from the food and stimulates its 
deposition in the bones. After ovulation the oestrogen level falls, the 
calcium is mobilized from the bones, and its concentration in the 
blood becomes very high, until used by the eggs. 

27. The brain of birds 

The brain is larger relative to the body in birds than in any other 
vertebrates except mammals (Fig. 288), and there is no doubt that one 
result of the high temperature has been to allow opportunity for an 
elaborate nervous organization and complicated behaviour. Unfortu- 
nately we have little information about the w^ay in which the large 
masses of tissue of the brain function ; they are certainly different from 
anything found in mammals. There are considerable differences in the 
development of the parts in various birds, for instance, the forebrain is 
especially large in the rooks and crows (Corvus) and in the parrots, the 
behaviour of which also shows signs of outstanding 'intelligence'. 

In the spinal cord the most characteristic feature is the relatively 
small size of the dorsal funiculi, and their nuclei in the medulla are 
also small. Evidently the sense of touch is less well developed over the 
body than it is in mammals, perhaps less than in reptiles. No doubt 
movement of the feathers provides impulses leading to reflex actions, 
but it is not surprising that the loose covering does not allow elaborate 
organization of the sense of touch. The finer senses of birds are 
restricted to the eyes, ears, and bill. On the other hand, there are large 
spino-cerebellar tracts, presumably proprioceptive and concerned with 
the delicate adjustments necessary for flight. The spinal cord is con- 
trolled by large efferent tracts from the brain, including cerebello- 
spinal, vestibulo-spinal, and tecto-spinal pathways. There is no direct 
tract from the forebrain to the spinal cord, but the influence of the 
large corpora striata is probably exercised through fibres running to 
the red nucleus and tegmentum of the midbrain, from which others 
pass to the cord. 



xvi. 27 


The cerebellum is also large (Fig. 288), a state of affairs perhaps 
connected with the precise timing and control of movement in all 
planes of space during flight. Besides large spino-cerebellar and 
vestibulo-cerebellar pathways there are also tecto-cerebellar and 
strio-cerebellar tracts, the latter perhaps conducting in both directions. 
The effect of the cerebellum on other parts of the brain is exercised 
through cerebellar nuclei, the cells of which give origin to the cerebello- 
spinal tract. 

The optic tracts are completely 
crossed and end mainly in the 
midbrain, as in lower verte- 
brates. However, a considerable 
portion of the optic tracts passes 
to the thalamus, and the mid- 
brain and thalamus are both 
highly developed and have inti- 
mate and reciprocal connexions 
with the striata of the cerebral 
hemispheres. The optic lobes 
also receive ascending fibres from 
the trigeminal nuclei and from 
the spinal cord. Their efferent 
pathways run to the oculomotor 
nuclei, to the underlying teg- 
mentum, and to the medulla and 
spinal cord. Evidently they play 
a large part in correlating visual with other afferent impulses. The 
thalamus is large and its dorsal part well differentiated into nuclei. 
It receives, besides optic fibres, also projections from tactile, pain, 
temperature, and perhaps auditory sources. There are large thalamo- 
striatal tracts, probably conducting in both directions. The ventral 
thalamus receives impulses from the striatum and sends them to the 
tegmentum, this being the main efferent pathway of the forebrain. 
The hypothalamus is rather small, probably because of the reduction 
in the olfactory system. 

The cerebral hemispheres are much larger than any other part of the 
brain and show an exaggeration of the condition found in the lizards 
(Fig. 289). The ventro-lateral portions are enormously developed, 
whereas the medial ventral walls are thin and the pallium is quite 
small, thin, and not folded. The olfactory regions of the brain are 
small, including the hippocampus. 

Fig. 288. Brain of a duck (Anser) 

c.h. cerebral hemisphere; cereb. cerebellum; cp. 

epiphysis;/?, flocculus; h. hypophysis; o./. optic 

lobe; olf. olfactory lobe; str. striatum; 1I-XII, 

cranial nerves. (After Butschli and Ihle.) 

XVI. 28 



The corpus striatum is a huge solid mass of tissue, receiving projec- 
tions forward from the thalamus and sending them back through the 
latter, to the midbrain roof and floor, to the cerebellum, and thence to 
the medulla and spinal cord. This very characteristic striatum can be 
divided into various regions. The part representing the 'original' or 
lower striatum is called the 'paleostriatum' ; other parts, lying above 
this, are known as the mesostriatum and hyperstriatum. 

Fig. 289. Transverse section through forebrain of sparrow. 

hip. hippocampus; hyp.str. hyperstriatum; mes.str. mesostriatum; preoptic nucleus; 
pal.str. palaeostriatum; pall, pallium. (Partly after Kappers, Huber, and Crosby.) 

28. Functioning of the brain in birds 

Loss of one complete hemisphere by a pigeon is not followed by any 
gross motor defect or asymmetry of movement. This suggests that the 
corpora striata do not control individual muscle movements, which 
agrees with the fact that there is no direct pathway from the forebrain 
to the spinal cord, corresponding to the pyramidal tract of the mam- 
mals. Electrical stimulation does not produce movements; the striata 
are 'silent areas' to stimulation. 

Complete removal of both hemispheres does not reduce a pigeon to 
a helpless state. The animal can still maintain its temperature and its 
balance and can feed itself if the food is placed near to it. However, a 
bird so treated is far from normal. It may show a lack of activity, 
remaining inert for long periods, and then become aimlessly restless 
for a while. Evidently the normal balance of excitation and inhibition 
has been upset. Deficiencies in vision can be detected in birds with 
various portions of the cerebral hemispheres removed, and the mating 
and nestine behaviour are also affected. Even small removals of the 

480 THE BIRDS xvi. 28 

cortex and top of the striatum are said to prevent incubation (though 
not copulation) and with deeper lesions the whole process of rearing 
the young becomes impossible. 

These observations on the functions of the brain of pigeons may not 
be applicable to birds in general. The forebrain is larger in many other 
birds than in the pigeon, and there is some evidence that in the parrots 
movements and even 'phonation' can be elicited by electrical stimula- 
tion of the corpora striata, which are especially large. Removal of one 
particular area is said to lead to disturbances of 'speech'. 



Fig. 290. A. Models used by Lorenz and Tinbergen. Small birds reacted with 

escape movements to the models marked + . B. The model induced escape reactions 

when towed to the right ('hawk') but not when towed to left ('goose'). 

(From Tinbergen.) 

It seems, therefore, that the large masses of nerve-cells in the striata 
are concerned in some way with the elaboration of the more complex 
acts of behaviour. This is a very vague statement, but is the best that 
we can give at present. It may be that further investigation of the 
reciprocal actions of striatum and thalamus will show whether the 
essentials of their action consist in some reverberating or scanning 
systems and whether these actions are at all similar to those in the 
forebrain of mammals. The fact that the striatum consists of solid 
masses of tissue suggests that the arrangement does not depend, as 
does the mammalian cerebral cortex, on the projection of patterns of 
excitation onto an extended surface. 

Birds are usually said to show more stereotyped pat